Awake Resection of Adult Supratentorial Low-grade Gliomas Located within or Adjacent to Eloquent Areas

Česká verzia

Authors: A. Šteňo ¹; V. Šteňová ²; V. Belan ³; V. Hollý ⁴; J. Šurkala ¹; J. Šteňo ¹
Authors place of work: UN Bratislava Neurochirurgická klinika LF UK ¹; UN Bratislava Ambulancia klinickej logopédie ²; UN Bratislava Rádiodiagnostická klinika SZU ³; UN Bratislava Klinika anestéziológie a intenzívnej medicíny SZU ⁴
Published in the journal: Cesk Slov Neurol N 2011; 74/107(5): 539-549
Category: Original Paper

Summary

Aim:
The aim of this work was to present the advantages and limits of the use of awake resection (AR) in the surgical treatment of supratentorial low-grade gliomas (LGG) located within or adjacent to eloquent areas; to evaluate the radicality of resections and functional outcome; and to document observations of certain brain structure functions. Patients and methods: The prospectively-studied series included 20 adult patients operated upon in a period of 41 months. All the tumours were located within or adjacent to speech and language, or motor eloquent, structures. Speech and language functions were intra-operatively assessed by a speech and language therapist. Calculation of tumour residua volumes was based on a postoperative fluid attenuated inversion recovery (FLAIR) magnetic resonance sequence. Results: Gross total removal was achieved in one patient, subtotal removal (residue smaller than 10 cm3) in 12, and partial removal in seven patients. Two temporary deficits and one minor permanent neurological deficit were observed. The use of direct electrical stimulation enabled anatomical localization and function of the following cortical and subcortical structures to be identified and observed: primary and supplementary motor area, motor pathways, Broca’s and Wernicke’s areas, fasciculus arcuatus, fasciculus subcallosus and corpus callosum. Conclusions: AR is a worthwhile contribution to the surgical treatment of supratentorial LGG. In addition to avoidance of surgical sequelae, AR allows an extensive, safe resection that may not be safely achievable with general anaesthesia even with the use of current diagnostic imaging methods and electrophysiological neuromonitoring, particularly in cases involving LGG located within or adjacent to speech and language areas. The incidence of new and permanent deficits is low. However, resection in certain areas remains problematical, even with the use of AR. Some complex neurological disorders of function may not be readily assessed intra-operatively, despite surgery in a patient who is awake. The methodology of intra-operative brain function testing should improve over time.

Key words:
low-grade glioma – awake resection – eloquent area – direct electrical stimulation

Zdroje

1. Pouratian N, Schiff D. Management of low-grade glioma. Curr Neurol Neurosci Rep 2010; 10(3): 224–231.

2. Soffietti R, Baumert BG, Bello L, von Deimling A, Duffau H, Frénay M et al. Guidelines on management of low-grade gliomas: report of an EFNS-EANO Task Force. Eur J Neurol 2010; 17(9): 1124–1133.

3. Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery 2008; 62(4): 753–764.

4. Duffau H, Lopes M, Arthuis F, Bitar A, Sichez JP, Van Effenterre R et al. Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985–1996) and with (1996–2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 2005; 76(6): 845–851.

5. Claus EB, Horlacher A, Hsu L, Schwartz RB, Dello-Iacono D, Talos F et al. Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer 2005; 103(6): 1227–1233.

6. Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 2008; 26(8): 1338–1345.

7. McGirt MJ, Chaichana KL, Attenello FJ, Weingart JD, Than K, Burger PC et al. Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery 2008; 63(4): 700–707.

8. Ahmadi R, Dictus C, Hartmann C, Zürn O, Edler L, Hartmann M et al. Long-term outcome and survival of surgically treated supratentorial low-grade glioma in adult patients. Acta Neurochir (Wien) 2009; 151(11): 1359–1365.

9. Skirboll SS, Ojemann GA, Berger MS, Lettich E, Winn HR. Functional cortex and subcortical white matter located within gliomas. Neurosurgery 1996; 38(4): 678–684.

10. Schiffbauer H, Ferrari P, Rowley HA, Berger MS, Roberts TP. Functional activity within brain tumors: a magnetic source imaging study. Neurosurgery 2001; 49(6): 1313–1320.

11. Duffau H, Capelle L. Preferential brain locations of low-grade gliomas. Cancer 2004; 100(12): 2622–2626.

12. Duffau H, Denvil D, Capelle L. Long term reshaping of language, sensory, and motor maps after glioma resection: a new parameter to integrate in the surgical strategy. J Neurol Neurosurg Psychiatry 2002; 72(4): 511–516.

13. Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping for glioma resection. N Engl J Med 2008; 358(1): 18–27.

14. Lehéricy S, Duffau H, Cornu P, Capelle L, Pidoux B, Carpentier A et al. Correspondence between functional magnetic resonance imaging somatotopy and individual brain anatomy of the central region: comparison with intraoperative stimulation in patients with brain tumors. J Neurosurg 2000; 92(4): 589–598.

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; 71(3): 316–326.

16. Giussani C, Roux FE, Ojemann J, Sganzerla EP, Pirillo D, Papagno C. 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(1): 113–120.

17. Leclercq D, Duffau H, Delmaire C, Capelle L, Gatignol P, Ducros M et al. Comparison of diffusion tensor imaging tractography of language tracts and intraoperative subcortical stimulations. J Neurosurg 2010; 112(3): 503–511.

18. Otani N, Bjeljac M, Muroi C, Weniger D, Khan N, Wieser HG et al. Awake surgery for glioma resection in eloquent areas - Zurich’s experience and review. Neurol Med Chir (Tokyo) 2005; 45(10): 501–510.

19. Bertani G, Fava E, Casaceli G, Carrabba G, Casarotti A, Papagno C et al. Intraoperative mapping and monitoring of brain functions for the resection of low-grade gliomas: technical considerations. Neurosurg Focus 2009; 27(4): E4.

20. Bello L, Gallucci M, Fava M, Carrabba G, Giussani C, Acerbi F et al. Intraoperative subcortical language tract mapping guides surgical removal of gliomas involving speech areas. Neurosurgery 2007; 60(1): 67–80.

21. Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, Taillandier L. Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg 2008; 109(3): 461–471.

22. Kim SS, McCutcheon IE, Suki D, Weinberg JS, Sawaya R, Lang FF et al. Awake craniotomy for brain tumors near eloquent cortex: correlation of intraoperative cortical mapping with neurological outcomes in 309 consecutive patients. Neurosurgery 2009; 64(5): 836–845.

23. Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Taillandier L et al. Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 2003; 98(4): 764–778.

24. Keles GE, Lundin DA, Lamborn KR, Chang EF, Ojemann G, Berger MS. Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. J Neurosurg 2004; 100(3): 369–375.

25. Kamada K, Todo T, Ota T, Ino K, Masutani Y, Aoki S et al. The motor-evoked potential threshold evaluated by tractography and electrical stimulation. J Neurosurg 200; 111(4): 785–795.

26. Nimsky C, Ganslandt O, Cerny S, Hastreiter P, Greiner G, Fahlbusch R. Quantification of, visualization of, and compensation for brain shift using intraoperative magnetic resonance imaging. Neurosurgery 2000; 47(5): 1070–1079.

27. Haglund MM, Berger MS, Shamseldin M, Lettich E, Ojemann GA. Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 1994; 34(4): 567–576.

28. Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP et al. Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 2002; 125(Pt 1): 199–214.

29. Ilmberger J, Ruge M, Kreth FW, Briegel J, Reulen HJ, Tonn JC. Intraoperative mapping of language functions: a longitudinal neurolinguistic analysis. J Neurosurg 2008; 109(4): 583–592.

30. Berger MS, Hadjipanayis CG. Surgery of intrinsic cerebral tumors. Neurosurgery 2007; 61 (Suppl 1): 279–304.

31. Ojemann JG, Ojemann GA, Lettich E. Cortical stimulation mapping of language cortex by using a verb generation task: effects of learning and comparison to mapping based on object naming. J Neurosurg 2002; 97(1): 33–38.

32. Lubrano V, Roux FE, Démonet JF. Writing-specific sites in frontal areas: a cortical stimulation study. J Neurosurg 2004; 101(5): 787–798.

33. Giussani C, Roux FE, Bello L, Lauwers-Cances V, Papagno C, Gaini SM et al. Who is who: areas of the brain associated with recognizing and naming famous faces. J Neurosurg 2009; 110(2): 289–299.

34. Ellmore TM, Beauchamp MS, O’Neill TJ, Dreyer S, Tandon N. Relationships between essential cortical language sites and subcortical pathways. J Neurosurg 2009; 111(4): 755–566.

35. Mikuni N, Okada T, Enatsu R, Miki Y, Hanakawa T, Urayama S et al. Clinical impact of integrated functional neuronavigation and subcortical electrical stimulation to preserve motor function during resection of brain tumors. J Neurosurg 2007; 106(4): 593–598.

36. Beeke S, Wilkinson R, Maxim J. Exploring aphasic grammar. 2: Do language testing and conversation tell a similar story? Clin Linguist Phon 2003; 17(2): 109–134.

37. Horton S. Critical reflection in speech and language therapy: research and practice. Int J Lang Commun Disord 2004; 39(4): 486–490.

38. Wilkinson R. Reflecting on talk in speech and language therapy: some contributions using conversation analysis. Int J Lang Commun Disord 2004; 39(4): 497–503.

39. Simmons-Mackie N. Social approach to aphasia intervention. In: Chapey R (ed). Language intervention strategies in aphasia and related neurogenic communication disorders. 5th ed. Baltimore: Lippincott Williams & Wilkins 2008: 290–318.

40. Kral T, Kurthen M, Schramm J, Urbach H, Meyer B. Stimulation mapping via implanted grid electrodes prior to surgery for gliomas in highly eloquent cortex. Neurosurgery 2006; 58 (Suppl 1): ONS36–ONS43.

41. Bartoš R, Ceé J, Zolal A, Hejčl A, Bolcha M, Prokšová J et al. Extraoperativní mapování pomocí kortikálního gridu před resekcí difuzního oligodendrogliomu v řečově dominantní hemisféře – alternativa „awake kraniotomie“ – kazuistika. Cesk Slov Neurol N 2008; 71/104(6): 718–721.

42. Bartoš R, Sameš M, Zolal A, Radovnický T, Hejčl A, Vachata P et al. Resekce inzulárních gliomů – volumetrické měření radikality. Cesk Slov Neurol N 2009; 72/105(6): 534–541.

43. Neuloh G, Pechstein U, Schramm J. Motor tract monitoring during insular glioma surgery. J Neurosurg 2007; 106(4): 582–592.

44. Ostrý S, Stejskal L. Evokované odpovědi a elektromyografie v intraoperační monitoraci v neurochirurgii. Cesk Slov Neurol N 2010; 73/106 (1): 8–19.

45. Kombos T, Suess O, Ciklatekerlio O, Brock M. Monitoring of intraoperative motor evoked potentials to increase the safety of surgery in and around the motor cortex. J Neurosurg 2001; 95(4): 608–614.

46. Hentschel SJ, Lang FF. Surgical resection of intrinsic insular tumors. Neurosurgery 2005; 57 (Suppl 1): 176–183.

47. Serletis D, Bernstein M. Prospective study of awake craniotomy used routinely and nonselectively for supratentorial tumors. J Neurosurg 2007; 107(1): 1–6.

48. Galanda M. Intraoperačné neurofyziologické monitorovanie. In: Haruštiak S (ed). Princípy chirurgie II. Bratislava: Slovak Academic Press 2010: 26–30.

49. Szelényi A, Bello L, Duffau H, Fava E, Feigl GC, Galanda M et al. Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 2010; 28(2): E7.

50. Duffau H, Moritz-Gasser S, Gatignol P. Functional outcome after language mapping for insular World Health Organization Grade II gliomas in the dominant hemisphere: experience with 24 patients. Neurosurg Focus 2009; 27(2): E7.

51. Bartoš R, Sameš M, Vachata P, Červenka M, Jech R, Vymazal J et al. Výsledky a tolerance „awake“ resekcí mozkových tumorů. Cesk Slov Neurol N 2005; 68/101(1): 39–45.

52. Fontaine D, Capelle L, Duffau H. Somatotopy of the supplementary motor area: evidence from correlation of the extent of surgical resection with the clinical patterns of deficit. Neurosurgery 2002; 50(2): 297–303.

53. Peraud A, Meschede M, Eisner W, Ilmberger J, Reulen HJ. Surgical resection of grade II astrocytomas in the superior frontal gyrus. Neurosurgery 2002; 50(5): 966–975.

54. Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Lopes M et al. Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry 2003; 74(7): 901–907.

55. Fontaine D, Capelle L, Duffau H. Somatotopy of the supplementary motor area: evidence from correlation of the extent of surgical resection with the clinical patterns of deficit. Neurosurgery 2002; 50(2): 297–303.

56. Schaltenbrand G, Spuer H, Wahren W. Electroanatomy of the corpus callosum radiation according to the facts of stereotactic stimulation in man. Z Neurol 1970; 198(1): 79–92.