Skip to main navigation menu Skip to main content Skip to site footer
##common.pageHeaderLogo.altText##

Original article

Vol. 153 No. 5 (2023)

Combined use of intraoperative MRI and awake tailored microsurgical resection to respect functional neural networks: preliminary experience

  • Constantin Tuleasca
  • Henri-Arthur Leroy
  • Ondine Strachowski
  • Benoit Derre
  • Claude-Alain Maurage
  • Iulia Peciu-Florianu
  • Nicolas Reyns
DOI
https://doi.org/10.57187/smw.2023.40072
Cite this as:
Swiss Med Wkly. 2023;153:40072
Published
15.05.2023

Summary

INTRODUCTION: The combined use of intraoperative MRI and awake surgery is a tailored microsurgical resection to respect functional neural networks (mainly the language and motor ones). Intraoperative MRI has been classically considered to increase the extent of resection for gliomas, thereby reducing neurological deficits. Herein, we evaluated the combined technique of awake microsurgical resection and intraoperative MRI for primary brain tumours (gliomas, metastasis) and epilepsy (cortical dysplasia, non-lesional, cavernomas).

PATIENTS AND METHODS: Eighteen patients were treated with the commonly used “asleep awake asleep” (AAA) approach at Lille University Hospital, France, from November 2016 until May 2020. The exact anatomical location was insular with various extensions, frontal, temporal or fronto-temporal in 8 (44.4%), parietal in 3 (16.7%), fronto-opercular in 4 (22.2%), Rolandic in two (11.1%), and the supplementary motor area (SMA) in one (5.6%).

RESULTS: The patients had a mean age of 38.4 years (median 37.1, range 20.8−66.9). The mean surgical duration was 4.1 hours (median 4.2, range 2.6−6.4) with a mean duration of intraoperative MRI of 28.8 minutes (median 25, range 13−55). Overall, 61% (11/18) of patients underwent further resection, while 39% had no additional resection after intraoperative MRI. The mean preoperative and postoperative tumour volumes of the primary brain tumours were 34.7 cc (median 10.7, range 0.534−130.25) and 3.5 cc (median 0.5, range 0−17.4), respectively. Moreover, the proportion of the initially resected tumour volume at the time of intraoperative MRI (expressed as 100% from preoperative volume) and the final resected tumour volume were statistically significant (p= 0.01, Mann-Whitney test). The tumour remnants were commonly found posterior (5/9) or anterior (2/9) insular and in proximity with the motor strip (1/9) or language areas (e.g. Broca, 1/9). Further resection was not required in seven patients because there were no remnants (3/7), cortical stimulation approaching eloquent areas (3/7) and non-lesional epilepsy (1/7). The mean overall follow-up period was 15.8 months (median 12, range 3−36).

CONCLUSION: The intraoperative MRI and awake microsurgical resection approach is feasible with extensive planning and multidisciplinary collaboration, as these methods are complementary and synergic rather than competitive to improve patient oncological outcomes and quality of life.

References

  1. Lapointe S , Perry A , Butowski NA . Primary brain tumours in adults. Lancet. 2018 Aug;392(10145):432–46. https://doi.org/10.1016/S0140-6736(18)30990-5 DOI: https://doi.org/10.1016/S0140-6736(18)30990-5
  2. Berger MS , Rostomily RC . Low grade gliomas: functional mapping resection strategies, extent of resection, and outcome. J Neurooncol. 1997 Aug;34(1):85–101. https://doi.org/10.1023/A:1005715405413 DOI: https://doi.org/10.1023/A:1005715405413
  3. Laws ER , Parney IF , Huang W , Anderson F , Morris AM , Asher A , et al.; Glioma Outcomes Investigators . Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project. J Neurosurg. 2003 Sep;99(3):467–73. https://doi.org/10.3171/jns.2003.99.3.0467 DOI: https://doi.org/10.3171/jns.2003.99.3.0467
  4. Sanai N , Berger MS . Glioma extent of resection and its impact on patient outcome. Neurosurgery. 2008 Apr;62(4):753–64. https://doi.org/10.1227/01.neu.0000318159.21731.cf DOI: https://doi.org/10.1227/01.neu.0000318159.21731.cf
  5. Berger MS , Deliganis AV , Dobbins J , Keles GE . The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer. 1994 Sep;74(6):1784–91. https://doi.org/10.1002/1097-0142(19940915)74:6<1784::AID-CNCR2820740622>3.0.CO;2-D DOI: https://doi.org/10.1002/1097-0142(19940915)74:6<1784::AID-CNCR2820740622>3.0.CO;2-D
  6. Martin C , Alexander E 3rd , Wong T , Schwartz R , Jolesz F , Black PM . Surgical treatment of low-grade gliomas in the intraoperative magnetic resonance imager. Neurosurg Focus. 1998 Apr;4(4):e8. https://doi.org/10.3171/foc.1998.4.4.11 DOI: https://doi.org/10.3171/foc.1998.4.4.11
  7. Stummer W , Novotny A , Stepp H , Goetz C , Bise K , Reulen HJ . Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg. 2000 Dec;93(6):1003–13. https://doi.org/10.3171/jns.2000.93.6.1003 DOI: https://doi.org/10.3171/jns.2000.93.6.1003
  8. Stummer W , Pichlmeier U , Meinel T , Wiestler OD , Zanella F , Reulen HJ ; ALA-Glioma Study Group . Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 2006 May;7(5):392–401. https://doi.org/10.1016/S1470-2045(06)70665-9 DOI: https://doi.org/10.1016/S1470-2045(06)70665-9
  9. Oh DS , Black PM . A low-field intraoperative MRI system for glioma surgery: is it worthwhile? Neurosurg Clin N Am. 2005 Jan;16(1):135–41. https://doi.org/10.1016/j.nec.2004.07.010 DOI: https://doi.org/10.1016/j.nec.2004.07.010
  10. Schulder M , Carmel PW . Intraoperative magnetic resonance imaging: impact on brain tumor surgery. Cancer Contr. 2003;10(2):115–24. https://doi.org/10.1177/107327480301000203 DOI: https://doi.org/10.1177/107327480301000203
  11. Coburger J , Merkel A , Scherer M , Schwartz F , Gessler F , Roder C , et al. Low-grade Glioma Surgery in Intraoperative Magnetic Resonance Imaging: Results of a Multicenter Retrospective Assessment of the German Study Group for Intraoperative Magnetic Resonance Imaging. Neurosurgery. 2016 Jun;78(6):775–86. https://doi.org/10.1227/NEU.0000000000001081 DOI: https://doi.org/10.1227/NEU.0000000000001081
  12. Coburger J , Wirtz CR . Fluorescence guided surgery by 5-ALA and intraoperative MRI in high grade glioma: a systematic review. J Neurooncol. 2019 Feb;141(3):533–46. https://doi.org/10.1007/s11060-018-03052-4 DOI: https://doi.org/10.1007/s11060-018-03052-4
  13. Berger MS , Kincaid J , Ojemann GA , Lettich E . Brain mapping techniques to maximize resection, safety, and seizure control in children with brain tumors. Neurosurgery. 1989 Nov;25(5):786–92. https://doi.org/10.1227/00006123-198911000-00015 DOI: https://doi.org/10.1227/00006123-198911000-00015
  14. Duffau H . Intraoperative cortico-subcortical stimulations in surgery of low-grade gliomas. Expert Rev Neurother. 2005 Jul;5(4):473–85. https://doi.org/10.1586/14737175.5.4.473 DOI: https://doi.org/10.1586/14737175.5.4.473
  15. Ojemann G , Ojemann J , Lettich E , Berger M . Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg. 1989 Sep;71(3):316–26. https://doi.org/10.3171/jns.1989.71.3.0316 DOI: https://doi.org/10.3171/jns.1989.71.3.0316
  16. Zanello M , Meyer B , Still M , Goodden JR , Colle H , Schichor C , et al. Surgical resection of cavernous angioma located within eloquent brain areas: international survey of the practical management among 19 specialized centers. Seizure. 2019 Jul;69:31–40. https://doi.org/10.1016/j.seizure.2019.03.022 DOI: https://doi.org/10.1016/j.seizure.2019.03.022
  17. Motomura K , Natsume A , Iijima K , Kuramitsu S , Fujii M , Yamamoto T , et al. Surgical benefits of combined awake craniotomy and intraoperative magnetic resonance imaging for gliomas associated with eloquent areas. J Neurosurg. 2017 Oct;127(4):790–7. https://doi.org/10.3171/2016.9.JNS16152 DOI: https://doi.org/10.3171/2016.9.JNS16152
  18. Tuleasca C , Leroy HA , Peciu-Florianu I , Strachowski O , Derre B , Levivier M , et al. Impact of combined use of intraoperative MRI and awake microsurgical resection on patients with gliomas: a systematic review and meta-analysis. Neurosurg Rev. 2021 Dec;44(6):2977–90. https://doi.org/10.1007/s10143-021-01488-3 DOI: https://doi.org/10.1007/s10143-021-01488-3
  19. Ghinda D , Zhang N , Lu J , Yao CJ , Yuan S , Wu JS . Contribution of combined intraoperative electrophysiological investigation with 3-T intraoperative MRI for awake cerebral glioma surgery: comprehensive review of the clinical implications and radiological outcomes. Neurosurg Focus. 2016 Mar;40(3):E14. https://doi.org/10.3171/2015.12.FOCUS15572 DOI: https://doi.org/10.3171/2015.12.FOCUS15572
  20. Leuthardt EC , Lim CC , Shah MN , Evans JA , Rich KM , Dacey RG , et al. Use of movable high-field-strength intraoperative magnetic resonance imaging with awake craniotomies for resection of gliomas: preliminary experience. Neurosurgery. 2011;69(1):194-205; discussion -6. https://doi.org/10.1227/NEU.0b013e31821d0e4c DOI: https://doi.org/10.1227/NEU.0b013e31821d0e4c
  21. Lu J , Wu J , Yao C , Zhuang D , Qiu T , Hu X , et al. Awake language mapping and 3-Tesla intraoperative MRI-guided volumetric resection for gliomas in language areas. J Clin Neurosci. 2013 Sep;20(9):1280–7. https://doi.org/10.1016/j.jocn.2012.10.042 DOI: https://doi.org/10.1016/j.jocn.2012.10.042
  22. Maldaun MV , Khawja SN , Levine NB , Rao G , Lang FF , Weinberg JS , et al. Awake craniotomy for gliomas in a high-field intraoperative magnetic resonance imaging suite: analysis of 42 cases. J Neurosurg. 2014 Oct;121(4):810–7. https://doi.org/10.3171/2014.6.JNS132285 DOI: https://doi.org/10.3171/2014.6.JNS132285
  23. Mehdorn HM , Schwartz F , Becker J . Awake Craniotomy for Tumor Resection: Further Optimizing Therapy of Brain Tumors. Acta Neurochir Suppl (Wien). 2017;124:309–13. https://doi.org/10.1007/978-3-319-39546-3_45 DOI: https://doi.org/10.1007/978-3-319-39546-3_45
  24. Tuominen J , Yrjänä S , Ukkonen A , Koivukangas J . Awake craniotomy may further improve neurological outcome of intraoperative MRI-guided brain tumor surgery. Acta Neurochir (Wien). 2013 Oct;155(10):1805–12. https://doi.org/10.1007/s00701-013-1837-3 DOI: https://doi.org/10.1007/s00701-013-1837-3
  25. Whiting BB , Lee BS , Mahadev V , Borghei-Razavi H , Ahuja S , Jia X , et al. Combined use of minimal access craniotomy, intraoperative magnetic resonance imaging, and awake functional mapping for the resection of gliomas in 61 patients. J Neurosurg. 2019:1–9. DOI: https://doi.org/10.3171/2018.9.JNS181802
  26. Reyns N , Leroy HA , Delmaire C , Derre B , Le-Rhun E , Lejeune JP . Intraoperative MRI for the management of brain lesions adjacent to eloquent areas. Neurochirurgie. 2017 Jun;63(3):181–8. https://doi.org/10.1016/j.neuchi.2016.12.006 DOI: https://doi.org/10.1016/j.neuchi.2016.12.006
  27. Nabavi A , Goebel S , Doerner L , Warneke N , Ulmer S , Mehdorn M . Awake craniotomy and intraoperative magnetic resonance imaging: patient selection, preparation, and technique. Top Magn Reson Imaging. 2009 Jan;19(4):191–6. https://doi.org/10.1097/RMR.0b013e3181963b46 DOI: https://doi.org/10.1097/RMR.0b013e3181963b46
  28. Leroy HA , Delmaire C , Le Rhun E , Drumez E , Lejeune JP , Reyns N . High-field intraoperative MRI and glioma surgery: results after the first 100 consecutive patients. Acta Neurochir (Wien). 2019 Jul;161(7):1467–74. https://doi.org/10.1007/s00701-019-03920-6 DOI: https://doi.org/10.1007/s00701-019-03920-6
  29. Weingarten DM , Asthagiri AR , Butman JA , Sato S , Wiggs EA , Damaska B , et al. Cortical mapping and frameless stereotactic navigation in the high-field intraoperative magnetic resonance imaging suite. J Neurosurg. 2009 Dec;111(6):1185–90. https://doi.org/10.3171/2009.5.JNS09164 DOI: https://doi.org/10.3171/2009.5.JNS09164
  30. White T , Zavarella S , Jarchin L , Nardi D , Schaffer S , Schulder M . Combined Brain Mapping and Compact Intraoperative MRI for Brain Tumor Resection. Stereotact Funct Neurosurg. 2018;96(3):172–81. https://doi.org/10.1159/000488991 DOI: https://doi.org/10.1159/000488991
  31. Zhuang DX , Wu JS , Yao CJ , Qiu TM , Lu JF , Zhu FP , et al. Intraoperative Multi-Information-Guided Resection of Dominant-Sided Insular Gliomas in a 3-T Intraoperative Magnetic Resonance Imaging Integrated Neurosurgical Suite. World Neurosurg. 2016 May;89:84–92. https://doi.org/10.1016/j.wneu.2016.01.067 DOI: https://doi.org/10.1016/j.wneu.2016.01.067
  32. Hervey-Jumper SL , Li J , Lau D , Molinaro AM , Perry DW , Meng L , et al. Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period. J Neurosurg. 2015 Aug;123(2):325–39. https://doi.org/10.3171/2014.10.JNS141520 DOI: https://doi.org/10.3171/2014.10.JNS141520
  33. Huncke K , Van de Wiele B , Fried I , Rubinstein EH . The asleep-awake-asleep anesthetic technique for intraoperative language mapping. Neurosurgery. 1998 Jun;42(6):1312–6. https://doi.org/10.1097/00006123-199806000-00069 DOI: https://doi.org/10.1097/00006123-199806000-00069
  34. Piccioni F , Fanzio M . Management of anesthesia in awake craniotomy. Minerva Anestesiol. 2008;74(7-8):393–408.
  35. Meng L , Berger MS , Gelb AW . The Potential Benefits of Awake Craniotomy for Brain Tumor Resection: An Anesthesiologist’s Perspective. J Neurosurg Anesthesiol. 2015 Oct;27(4):310–7. https://doi.org/10.1097/ANA.0000000000000179 DOI: https://doi.org/10.1097/ANA.0000000000000179
  36. Komatsu R , Turan AM , Orhan-Sungur M , McGuire J , Radke OC , Apfel CC . Remifentanil for general anaesthesia: a systematic review. Anaesthesia. 2007 Dec;62(12):1266–80. https://doi.org/10.1111/j.1365-2044.2007.05221.x DOI: https://doi.org/10.1111/j.1365-2044.2007.05221.x
  37. Potters JW , Klimek M . Local anesthetics for brain tumor resection: current perspectives. Local Reg Anesth. 2018 Feb;11:1–8. https://doi.org/10.2147/LRA.S135413 DOI: https://doi.org/10.2147/LRA.S135413
  38. Danks RA , Rogers M , Aglio LS , Gugino LD , Black PM . Patient tolerance of craniotomy performed with the patient under local anesthesia and monitored conscious sedation. Neurosurgery. 1998;42(1):28-34; discussion -6. https://doi.org/10.1097/00006123-199801000-00006 DOI: https://doi.org/10.1097/00006123-199801000-00006
  39. Danks RA , Aglio LS , Gugino LD , Black PM . Craniotomy under local anesthesia and monitored conscious sedation for the resection of tumors involving eloquent cortex. J Neurooncol. 2000 Sep;49(2):131–9. https://doi.org/10.1023/A:1026577518902 DOI: https://doi.org/10.1023/A:1026577518902
  40. Chowdhury T , Singh GP , Zeiler FA , Hailu A , Loewen H , Schaller B , et al. Anesthesia for Awake Craniotomy for Brain Tumors in an Intraoperative MRI Suite: challenges and Evidence. Front Oncol. 2018 Nov;8:519. https://doi.org/10.3389/fonc.2018.00519 DOI: https://doi.org/10.3389/fonc.2018.00519
  41. Duffau H . Awake surgery for nonlanguage mapping. Neurosurgery. 2010 Mar;66(3):523–8. https://doi.org/10.1227/01.NEU.0000364996.97762.73 DOI: https://doi.org/10.1227/01.NEU.0000364996.97762.73
  42. Fontaine D , Almairac F , Santucci S , Fernandez C , Dallel R , Pallud J , et al. Dural and pial pain-sensitive structures in humans: new inputs from awake craniotomies. Brain. 2018 Apr;141(4):1040–8. https://doi.org/10.1093/brain/awy005 DOI: https://doi.org/10.1093/brain/awy005
  43. Sartorius CJ , Wright G . Intraoperative brain mapping in a community setting—technical considerations. Surg Neurol. 1997 Apr;47(4):380–8. https://doi.org/10.1016/S0090-3019(96)00340-0 DOI: https://doi.org/10.1016/S0090-3019(96)00340-0
  44. Sartorius CJ , Berger MS . Rapid termination of intraoperative stimulation-evoked seizures with application of cold Ringer's lactate to the cortex. Technical note. J Neurosurg. 1998 Feb;88(2):349–51. https://doi.org/10.3171/jns.1998.88.2.0349 DOI: https://doi.org/10.3171/jns.1998.88.2.0349
  45. Rosenow F , Lüders H . Presurgical evaluation of epilepsy. Brain. 2001 Sep;124(Pt 9):1683–700. https://doi.org/10.1093/brain/124.9.1683 DOI: https://doi.org/10.1093/brain/124.9.1683
  46. Thorsteinsdottir J , Vollmar C , Tonn JC , Kreth FW , Noachtar S , Peraud A . Outcome after individualized stereoelectroencephalography (sEEG) implantation and navigated resection in patients with lesional and non-lesional focal epilepsy. J Neurol. 2019 Apr;266(4):910–20. https://doi.org/10.1007/s00415-019-09213-3 DOI: https://doi.org/10.1007/s00415-019-09213-3
  47. Luders HO , Najm I , Nair D , Widdess-Walsh P , Bingman W . The epileptogenic zone: general principles. Epileptic disorders : international epilepsy journal with videotape. 2006;8 Suppl 2:S1-9.
  48. Abel TJ , Woodroffe RW , Nourski KV , Moritani T , Capizzano AA , Kirby P , et al. Role of the temporal pole in temporal lobe epilepsy seizure networks: an intracranial electrode investigation. J Neurosurg. 2018 Jul;129(1):165–73. https://doi.org/10.3171/2017.3.JNS162821 DOI: https://doi.org/10.3171/2017.3.JNS162821