Advertisement

Acta Neurochirurgica

, Volume 157, Issue 6, pp 947–956 | Cite as

Tractography of Meyer’s loop for temporal lobe resection—validation by prediction of postoperative visual field outcome‬‬‬‬

  • Ylva LiljaEmail author
  • Maria Ljungberg
  • Göran Starck
  • Kristina Malmgren
  • Bertil Rydenhag
  • Daniel T. Nilsson
Clinical Article - Neurosurgical Techniques

Abstract

Background

Postoperative visual field defects are common after temporal lobe resection because of injury to the most anterior part of the optic radiation, Meyer’s loop. Diffusion tensor tractography is a promising technique for visualizing the optic radiation preoperatively. The aim of this study was to assess the anatomical accuracy of Meyer’s loop, visualized by the two most common tractography methods—deterministic (DTG) and probabilistic tractography (PTG)—in patients who had undergone temporal lobe resection.

Methods

Eight patients with temporal lobe resection for temporal lobe pathology were included. Perimetry and diffusion tensor imaging were performed pre- and postoperatively. Two independent operators analyzed the distance between the temporal pole and Meyer’s loop (TP-ML) using DTG and PTG. Results were compared to each other, to data from previously published dissection studies and to postoperative perimetry results. For the latter, Spearman’s rank correlation coefficient (rs) was used.

Results

Median preoperative TP-ML distances for nonoperated sides were 42 and 35 mm, as determined by DTG and PTG, respectively. TP-ML assessed with PTG was a closer match to dissection studies. Intraclass correlation coefficients were 0.4 for DTG and 0.7 for PTG. Difference between preoperative TP-ML (by DTG and PTG, respectively) and resection length could predict the degree of postoperative visual field defects (DTG: rs = −0.86, p < 0.05; PTG: rs = −0.76, p < 0.05).

Conclusion

Both DTG and PTG could predict the degree of visual field defects. However, PTG was superior to DTG in terms of reproducibility and anatomical accuracy. PTG is thus a strong candidate for presurgical planning of temporal lobe resection that aims to minimize injury to Meyer’s loop.

Keywords

Diffusion tensor imaging Meyer’s loop Optic radiation Temporal lobe resection Tractography Visual field defect 

Notes

Acknowledgments

We thank Nils-Gunnar Pehrsson, Statistiska Konsultgruppen, for contributing with expert statistical advice and Justin Schneiderman for the language check and other much appreciated advice. We also thank the neuro-ophtalmologists, Dr. Bertil Lindblom and Dr. Lars Frisén, for their cooperation and expert clinical evaluations. We are thankful to the FMRIB Analysis Group, Oxford, UK, for providing the FSL software. Research nurse Gerd Ekstedt kept track of subjects and DTI examinations, which was invaluable.

This study was supported by research grants from the Gothenburg Medical Society, The Göteborg Foundation for Neurological Research, the “De Blindas Vänner” foundation, The Swedish Medical Society, The Swedish Epilepsy Society, GlaxoSmithKline, ALF GBG grant no. 11284 and Neuro-S Up ALF 77090 (agreement concerning research and education of doctors).

Ethical standards

The study was approved by the regional ethics board of the University of Gothenburg, Sweden. Informed written consent was obtained from all subjects prior to their inclusion in the study.

Conflicts of interest

None.

References

  1. 1.
    Basser PJ (1995) Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed 8:333–344CrossRefPubMedGoogle Scholar
  2. 2.
    Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? NeuroImage 34:144–155CrossRefPubMedGoogle Scholar
  3. 3.
    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 Off J Soc Magn Reson Med Soc Magn Reson Med 50:1077–1088CrossRefGoogle Scholar
  4. 4.
    Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. NeuroImage 17:77–94CrossRefPubMedGoogle Scholar
  5. 5.
    Catani M, Jones DK, Donato R, Ffytche DH (2003) Occipito-temporal connections in the human brain. Brain J Neurol 126:2093–2107CrossRefGoogle Scholar
  6. 6.
    Chen X, Weigel D, Ganslandt O, Buchfelder M, Nimsky C (2009) Prediction of visual field deficits by diffusion tensor imaging in temporal lobe epilepsy surgery. NeuroImage 45:286–297CrossRefPubMedGoogle Scholar
  7. 7.
    Chen X, Weigel D, Ganslandt O, Fahlbusch R, Buchfelder M, Nimsky C (2007) Diffusion tensor-based fiber tracking and intraoperative neuronavigation for the resection of a brainstem cavernous angioma. Surg Neurol 68:285–291, discussion 291CrossRefPubMedGoogle Scholar
  8. 8.
    Chowdhury FH, Khan AH (2010) Anterior & lateral extension of optic radiation & safety of amygdalohippocampectomy through middle temporal gyrus: a cadaveric study of 11 cerebral hemispheres. Asian J Neurosurg 5:78–82PubMedCentralPubMedGoogle Scholar
  9. 9.
    Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, Shimony JS, McKinstry RC, Burton H, Raichle ME (1999) Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci U S A 96:10422–10427CrossRefPubMedCentralPubMedGoogle Scholar
  10. 10.
    Ebeling U, Reulen HJ (1988) Neurosurgical topography of the optic radiation in the temporal lobe. Acta Neurochir (Wien) 92:29–36CrossRefGoogle Scholar
  11. 11.
    Egan RA, Shults WT, So N, Burchiel K, Kellogg JX, Salinsky M (2000) Visual field deficits in conventional anterior temporal lobectomy versus amygdalohippocampectomy. Neurology 55:1818–1822CrossRefPubMedGoogle Scholar
  12. 12.
    Fleiss JL (1986) Design and analysis of clinical experiments. John Wiley & Sons, New YorkGoogle Scholar
  13. 13.
    Good P (2000) Permutation tests. A practical guide to resampling methods for testing hypotheses. Springer, Inc, New York, pp 51–52Google Scholar
  14. 14.
    Gross DW, Concha L, Beaulieu C (2006) Extratemporal white matter abnormalities in mesial temporal lobe epilepsy demonstrated with diffusion tensor imaging. Epilepsia 47:1360–1363CrossRefPubMedGoogle Scholar
  15. 15.
    Guenot M, Krolak-Salmon P, Mertens P, Isnard J, Ryvlin P, Fischer C, Vighetto A, Mauguiere F, Sindou M (1999) MRI assessment of the anatomy of optic radiations after temporal lobe epilepsy surgery. Stereotact Funct Neurosurg 73:84–87CrossRefPubMedGoogle Scholar
  16. 16.
    Hughes TS, Abou-Khalil B, Lavin PJ, Fakhoury T, Blumenkopf B, Donahue SP (1999) Visual field defects after temporal lobe resection: a prospective quantitative analysis. Neurology 53:167–172CrossRefPubMedGoogle Scholar
  17. 17.
    Jensen I, Seedorf H (1976) Temporal lobe epilepsy and neuro-ophthalmology. Ophthalmological findings in 74 temporal lobe resected patients. Acta Ophthalmol 54:827–840CrossRefGoogle Scholar
  18. 18.
    Jones DK (2008) Studying connections in the living human brain with diffusion MRI. Cortex 44:936–952CrossRefPubMedGoogle Scholar
  19. 19.
    Lee SK, Kim DI, Mori S, Kim J, Kim HD, Heo K, Lee BI (2004) Diffusion tensor MRI visualizes decreased subcortical fiber connectivity in focal cortical dysplasia. NeuroImage 22:1826–1829CrossRefPubMedGoogle Scholar
  20. 20.
    Lilja Y, Ljungberg M, Starck G, Malmgren K, Rydenhag B, Nilsson DT (2014) Visualizing Meyer’s loop: a comparison of deterministic and probabilistic tractography. Epilepsy Res 108:481–490CrossRefPubMedGoogle Scholar
  21. 21.
    Lo CY, Chao YP, Chou KH, Guo WY, Su JL, Lin CP (2007) DTI-based virtual reality system for neurosurgery. Conf Proc IEEE Eng Med Biol Soc 2007:1326–1329PubMedGoogle Scholar
  22. 22.
    Ludwig EKJ (1956) Atlas Cerebri Humani. Karger, BaselGoogle Scholar
  23. 23.
    Marino R Jr, Rasmussen T (1968) Visual field changes after temporal lobectomy in man. Neurology 18:825–835CrossRefPubMedGoogle Scholar
  24. 24.
    Melhem ER, Mori S, Mukundan G, Kraut MA, Pomper MG, van Zijl PC (2002) Diffusion tensor MR imaging of the brain and white matter tractography. AJR Am J Roentgenol 178:3–16CrossRefPubMedGoogle Scholar
  25. 25.
    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 Reson Med Off J Soc Magn Reson Med Soc Magn Reson Med 47:215–223CrossRefGoogle Scholar
  26. 26.
    Mori S, van Zijl PC (2002) Fiber tracking: principles and strategies—a technical review. NMR Biomed 15:468–480CrossRefPubMedGoogle Scholar
  27. 27.
    Mori S, Zhang J (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527–539CrossRefPubMedGoogle Scholar
  28. 28.
    Nguyen TH, Yoshida M, Stievenart JL, Iba-Zizen MT, Bellinger L, Abanou A, Kitahara K, Cabanis EA (2005) MR tractography with diffusion tensor imaging in clinical routine. Neuroradiology 47:334–343CrossRefPubMedGoogle Scholar
  29. 29.
    Nilsson C, Markenroth Bloch K, Brockstedt S, Latt J, Widner H, Larsson EM (2007) Tracking the neurodegeneration of parkinsonian disorders—a pilot study. NeuroradiologyGoogle Scholar
  30. 30.
    Nilsson D, Malmgren K, Rydenhag B, Frisen L (2004) Visual field defects after temporal lobectomy—comparing methods and analysing resection size. Acta Neurol Scand 110:301–307CrossRefPubMedGoogle Scholar
  31. 31.
    Nilsson D, Starck G, Ljungberg M, Ribbelin S, Jonsson L, Malmgren K, Rydenhag B (2007) Intersubject variability in the anterior extent of the optic radiation assessed by tractography. Epilepsy Res 77:11–16CrossRefPubMedGoogle Scholar
  32. 32.
    Nimsky C, Ganslandt O, Fahlbusch R (2006) Implementation of fiber tract navigation. Neurosurgery 58:ONS-292-303, discussion ONS-303-294CrossRefGoogle Scholar
  33. 33.
    Nimsky C, Ganslandt O, Hastreiter P, Wang R, Benner T, Sorensen AG, Fahlbusch R (2005) Preoperative and intraoperative diffusion tensor imaging-based fiber tracking in glioma surgery. Neurosurgery 56:130–137, discussion 138PubMedGoogle Scholar
  34. 34.
    Okada T, Mikuni N, Miki Y, Kikuta K, Urayama S, Hanakawa T, Fushimi Y, Yamamoto A, Kanagaki M, Fukuyama H, Hashimoto N, Togashi K (2006) Corticospinal tract localization: integration of diffusion-tensor tractography at 3-T MR imaging with intraoperative white matter stimulation mapping–preliminary results. Radiology 240:849–857CrossRefPubMedGoogle Scholar
  35. 35.
    Peuskens D, van Loon J, Van Calenbergh F, van den Bergh R, Goffin J, Plets C (2004) Anatomy of the anterior temporal lobe and the frontotemporal region demonstrated by fiber dissection. Neurosurgery 55:1174–1184CrossRefPubMedGoogle Scholar
  36. 36.
    Powell HW, Parker GJ, Alexander DC, Symms MR, Boulby PA, Wheeler-Kingshott CA, Barker GJ, Koepp MJ, Duncan JS (2005) MR tractography predicts visual field defects following temporal lobe resection. Neurology 65:596–599CrossRefPubMedGoogle Scholar
  37. 37.
    Rubino PA, Rhoton AL Jr, Tong X, Oliveira E (2005) Three-dimensional relationships of the optic radiation. Neurosurgery 57:219–227, discussion 219–227CrossRefPubMedGoogle Scholar
  38. 38.
    Rydenhag B, Silander HC (2001) Complications of epilepsy surgery after 654 procedures in Sweden, September 1990–1995: a multicenter study based on the Swedish National Epilepsy Surgery Register. Neurosurgery 49:51–56, discussion 56–57PubMedGoogle Scholar
  39. 39.
    Schulz G, Crooijmans HJ, Germann M, Scheffler K, Muller-Gerbl M, Muller B (2011) Three-dimensional strain fields in human brain resulting from formalin fixation. J Neurosci Methods 202:17–27CrossRefPubMedGoogle Scholar
  40. 40.
    Sherbondy AJ, Dougherty RF, Napel S, Wandell BA (2008) Identifying the human optic radiation using diffusion imaging and fiber tractography. J Vis 8(12):11CrossRefGoogle Scholar
  41. 41.
    Shrout PE, Fleiss JL (1979) Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86:420–428CrossRefPubMedGoogle Scholar
  42. 42.
    Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23(Suppl 1):S208–S219CrossRefPubMedGoogle Scholar
  43. 43.
    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 14:723–735CrossRefPubMedGoogle Scholar
  44. 44.
    Taoka T, Sakamoto M, Nakagawa H, Nakase H, Iwasaki S, Takayama K, Taoka K, Hoshida T, Sakaki T, Kichikawa K (2008) Diffusion tensor tractography of the meyer loop in cases of temporal lobe resection for temporal lobe epilepsy: correlation between postsurgical visual field defect and anterior limit of meyer loop on tractography. AJNR Am J NeuroradiolGoogle Scholar
  45. 45.
    Thudium MO, Campos AR, Urbach H, Clusmann H (2010) The basal temporal approach for mesial temporal surgery: sparing the Meyer loop with navigated diffusion tensor tractography. Neurosurgery 67:385–390Google Scholar
  46. 46.
    Wang YX, Zhu XL, Deng M, Siu DY, Leung JC, Chan Q, Chan DT, Mak CH, Poon WS (2010) The use of diffusion tensor tractography to measure the distance between the anterior tip of the Meyer loop and the temporal pole in a cohort from Southern China. J NeurosurgGoogle Scholar
  47. 47.
    Wiebe S, Blume WT, Girvin JP, Eliasziw M (2001) A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 345:311–318CrossRefPubMedGoogle Scholar
  48. 48.
    Winston GP, Daga P, Stretton J, Modat M, Symms MR, McEvoy AW, Ourselin S, Duncan JS (2012) Optic radiation tractography and vision in anterior temporal lobe resection. Ann Neurol 71:334–341CrossRefPubMedCentralPubMedGoogle Scholar
  49. 49.
    Winston GP, Mancini L, Stretton J, Ashmore J, Symms MR, Duncan JS, Yousry TA (2011) Diffusion tensor imaging tractography of the optic radiation for epilepsy surgical planning: a comparison of two methods. Epilepsy Res 97:124–132CrossRefPubMedCentralPubMedGoogle Scholar
  50. 50.
    Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM (2009) Bayesian analysis of neuroimaging data in FSL. NeuroImage 45:S173–S186CrossRefPubMedGoogle Scholar
  51. 51.
    Yamamoto T, Yamada K, Nishimura T, Kinoshita S (2005) Tractography to depict three layers of visual field trajectories to the calcarine gyri. Am J Ophthalmol 140:781–785CrossRefPubMedGoogle Scholar
  52. 52.
    Yogarajah M, Focke NK, Bonelli S, Cercignani M, Acheson J, Parker GJ, Alexander DC, McEvoy AW, Symms MR, Koepp MJ, Duncan JS (2009) Defining Meyer’s loop-temporal lobe resections, visual field deficits and diffusion tensor tractography. Brain J Neurol 132:1656–1668CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Ylva Lilja
    • 1
    • 5
    Email author
  • Maria Ljungberg
    • 2
    • 3
  • Göran Starck
    • 2
    • 3
  • Kristina Malmgren
    • 1
  • Bertil Rydenhag
    • 1
    • 4
  • Daniel T. Nilsson
    • 1
    • 4
  1. 1.Institute of Neuroscience and Physiology, Department of Clinical Neuroscience and RehabilitationThe Sahlgrenska Academy at the University of GothenburgGothenburgSweden
  2. 2.Department of Radiation Physics, Institute of Clinical SciencesThe Sahlgrenska Academy at the University of GothenburgGothenburgSweden
  3. 3.Medical Physics and Biomedical EngineeringSahlgrenska University HospitalGothenburgSweden
  4. 4.Department of NeurosurgerySahlgrenska University HospitalGothenburgSweden
  5. 5.Ear, Nose and Throat ClinicSahlgrenska University HospitalGöteborgSweden

Personalised recommendations