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J Neurol Surg A Cent Eur Neurosurg 2015; 76(02): 149-159
DOI: 10.1055/s-0034-1393925
Surgical Technique Article
Georg Thieme Verlag KG Stuttgart · New York

Surgical Management of Eloquent Supratentorial Low-Grade Gliomas with Special Emphasis on Intraoperative Imaging

Asgeir Store Jakola
1   Department of Neurosurgery, St. Olav's University Hospital, Trondheim, Norway
2   National Centre for Ultrasound and Image Guided Therapy, Trondheim, Norway
,
Christian Senft
3   Department of Neurosurgery, Johann Wolfgang Goethe-University, Frankfurt, Germany
,
Geirmund Unsgaard
1   Department of Neurosurgery, St. Olav's University Hospital, Trondheim, Norway
2   National Centre for Ultrasound and Image Guided Therapy, Trondheim, Norway
,
Ole Solheim
1   Department of Neurosurgery, St. Olav's University Hospital, Trondheim, Norway
2   National Centre for Ultrasound and Image Guided Therapy, Trondheim, Norway
› Author Affiliations
Further Information

Publication History

10 October 2013

14 July 2014

Publication Date:
24 December 2014 (online)

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Abstract

Objective Eloquent diffuse low-grade gliomas (LGGs) threaten patients' neurologic function and are also associated with inferior survival. Many neurosurgeons still refrain from early resection due to the fear of iatrogenic neurologic injury. However, the perceived safety of expectant management strategies may soon be overshadowed by the progressive deficits of tumor growth in eloquent regions. It is also known that radical and successful surgery prolongs progression-free survival, overall survival, and may reduce seizure burden and also potentially neurocognitive functions. Thus early successful surgery with preservation of function has a significant impact on patients' health. In modern neurosurgery, safe resection is often possible with detailed knowledge of anatomy and function together with the active use of various intraoperative surgical tools. We present illustrative cases of eloquent LGGs treated with different intraoperative tools.

Methods An introduction to important intraoperative tools in LGG surgery is provided by experts in the field and described in five cases viewed in the context of the recent LGG literature.

Results We present five cases with presumed eloquently located LGGs where extensive resection was offered using different intraoperative techniques. The clinical and radiologic outcomes are described.

Conclusions Correct use of intraoperative tools together with the surgeon's knowledge of anatomy and function will provide good functional and oncologic results in eloquently located LGGs. Watchful waiting or deferral of surgery due to tumor location (i.e., claiming inoperability) is very rarely good practice.

Keywords

glioma - magnetic resonance imaging - ultrasound - technology
 

  • References

  • 1 Seiz M, Freyschlag CF, Schenkel S , et al. Management of patients with low-grade gliomas—a survey among German neurosurgical departments. Cent Eur Neurosurg 2011; 72 (4) 186-191
    Article in Thieme ConnectPubMedGoogle Scholar
  • 2 Jakola AS, Myrmel KS, Kloster R , et al. Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA 2012; 308 (18) 1881-1888
    CrossrefPubMedGoogle Scholar
  • 3 Aaronson NK, Taphoorn MJB, Heimans JJ , et al. Compromised health-related quality of life in patients with low-grade glioma. J Clin Oncol 2011; 29 (33) 4430-4435
    CrossrefPubMedGoogle Scholar
  • 4 Pallud J, Fontaine D, Duffau H , et al. Natural history of incidental World Health Organization grade II gliomas. Ann Neurol 2010; 68 (5) 727-733
    CrossrefPubMedGoogle Scholar
  • 5 Potts MB, Smith JS, Molinaro AM, Berger MS. Natural history and surgical management of incidentally discovered low-grade gliomas. J Neurosurg 2011; 116 (2) 365-372
    PubMedGoogle Scholar
  • 6 Mandonnet E, Delattre J-Y, Tanguy M-L , et al. Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 2003; 53 (4) 524-528
    CrossrefPubMedGoogle Scholar
  • 7 Pallud J, Varlet P, Devaux B , et al. Diffuse low-grade oligodendrogliomas extend beyond MRI-defined abnormalities. Neurology 2010; 74 (21) 1724-1731
    CrossrefPubMedGoogle Scholar
  • 8 Chang EF, Clark A, Smith JS , et al. Functional mapping-guided resection of low-grade gliomas in eloquent areas of the brain: improvement of long-term survival. Clinical article. J Neurosurg 2011; 114 (3) 566-573
    CrossrefPubMedGoogle Scholar
  • 9 Jakola AS, Unsgård G, Myrmel KS , et al. Low grade gliomas in eloquent locations—implications for surgical strategy, survival and long term quality of life. PLoS ONE 2012; 7 (12) e51450
    CrossrefPubMedGoogle Scholar
  • 10 Kuhnt D, Ganslandt O, Schlaffer SM, Buchfelder M, Nimsky C. Quantification of glioma removal by intraoperative high-field magnetic resonance imaging: an update. Neurosurgery 2011; 69 (4) 852-862 ; discussion 862–863
    CrossrefPubMedGoogle Scholar
  • 11 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
    CrossrefPubMedGoogle Scholar
  • 12 Smith JS, Chang EF, Lamborn KR , 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
    CrossrefPubMedGoogle Scholar
  • 13 Capelle L, Fontaine D, Mandonnet E , et al; French Réseau d'Étude des Gliomes. Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization grade II gliomas: a series of 1097 cases: clinical article. J Neurosurg 2013; 118 (6) 1157-1168
    CrossrefPubMedGoogle Scholar
  • 14 Gil-Robles S, Duffau H. Surgical management of World Health Organization grade II gliomas in eloquent areas: the necessity of preserving a margin around functional structures. Neurosurg Focus 2010; 28 (2) E8
    PubMedGoogle Scholar
  • 15 Szelényi A, Bello L, Duffau H , et al; Workgroup for Intraoperative Management in Low-Grade Glioma Surgery within the European Low-Grade Glioma Network. Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 2010; 28 (2) E7
    PubMedGoogle Scholar
  • 16 Yordanova YN, Moritz-Gasser S, Duffau H. Awake surgery for WHO Grade II gliomas within “noneloquent” areas in the left dominant hemisphere: toward a “supratotal” resection. Clinical article. J Neurosurg 2011; 115 (2) 232-239
    CrossrefPubMedGoogle Scholar
  • 17 Borchers S, Himmelbach M, Logothetis N, Karnath HO. Direct electrical stimulation of human cortex—the gold standard for mapping brain functions?. Nat Rev Neurosci 2012; 13 (1) 63-70
    PubMedGoogle Scholar
  • 18 Mandonnet E, Winkler PA, Duffau H. Direct electrical stimulation as an input gate into brain functional networks: principles, advantages and limitations. Acta Neurochir (Wien) 2010; 152 (2) 185-193
    CrossrefPubMedGoogle Scholar
  • 19 Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping for glioma resection. N Engl J Med 2008; 358 (1) 18-27
    CrossrefPubMedGoogle Scholar
  • 20 De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS. Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 2012; 30 (20) 2559-2565
    CrossrefPubMedGoogle Scholar
  • 21 Senft C, Bink A, Franz K, Vatter H, Gasser T, Seifert V. Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 2011; 12 (11) 997-1003
    CrossrefPubMedGoogle Scholar
  • 22 Nimsky C, von Keller B, Schlaffer S , et al. Updating navigation with intraoperative image data. Top Magn Reson Imaging 2009; 19 (4) 197-204
    PubMedGoogle Scholar
  • 23 Prabhu SS, Gasco J, Tummala S, Weinberg JS, Rao G. Intraoperative magnetic resonance imaging-guided tractography with integrated monopolar subcortical functional mapping for resection of brain tumors. Clinical article. J Neurosurg 2011; 114 (3) 719-726
    CrossrefPubMedGoogle Scholar
  • 24 Claus EB, Horlacher A, Hsu L , et al. Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer 2005; 103 (6) 1227-1233
    CrossrefPubMedGoogle Scholar
  • 25 Pamir MN, Ozduman K, Dinçer A, Yildiz E, Peker S, Ozek MM. First intraoperative, shared-resource, ultrahigh-field 3-Tesla magnetic resonance imaging system and its application in low-grade glioma resection. J Neurosurg 2010; 112 (1) 57-69
    CrossrefPubMedGoogle Scholar
  • 26 Levy R, Cox RG, Hader WJ, Myles T, Sutherland GR, Hamilton MG. Application of intraoperative high-field magnetic resonance imaging in pediatric neurosurgery. J Neurosurg Pediatr 2009; 4 (5) 467-474
    CrossrefPubMedGoogle Scholar
  • 27 Nimsky C, Fujita A, Ganslandt O, Von Keller B, Fahlbusch R. Volumetric assessment of glioma removal by intraoperative high-field magnetic resonance imaging. Neurosurgery 2004; 55 (2) 358-370 ; discussion 370–371
    CrossrefPubMedGoogle Scholar
  • 28 Senft C, Franz K, Ulrich CT , et al. Low field intraoperative MRI-guided surgery of gliomas: a single center experience. Clin Neurol Neurosurg 2010; 112 (3) 237-243
    CrossrefPubMedGoogle Scholar
  • 29 Schulder M, Salas S, Brimacombe M , et al. Cranial surgery with an expanded compact intraoperative magnetic resonance imager. Technical note. J Neurosurg 2006; 104 (4) 611-617
    CrossrefPubMedGoogle Scholar
  • 30 Senft C, Forster M-T, Bink A , et al. Optimizing the extent of resection in eloquently located gliomas by combining intraoperative MRI guidance with intraoperative neurophysiological monitoring. J Neurooncol 2012; 109 (1) 81-90
    CrossrefPubMedGoogle Scholar
  • 31 Leuthardt EC, Lim CC, Shah MN , 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 205–206
    CrossrefPubMedGoogle Scholar
  • 32 Senft C, Schoenes B, Gasser T , et al. Feasibility of intraoperative MRI guidance for craniotomy and tumor resection in the semisitting position. J Neurosurg Anesthesiol 2011; 23 (3) 241-246
    CrossrefPubMedGoogle Scholar
  • 33 Hirschl RA, Wilson J, Miller B, Bergese S, Chiocca E. The predictive value of low-field strength magnetic resonance imaging for intraoperative residual tumor detection. Clinical article. J Neurosurg 2009; 111 (2) 252-257
    CrossrefPubMedGoogle Scholar
  • 34 Belhawi SM, Hoefnagels FW, Baaijen JC , et al. Early postoperative MRI overestimates residual tumour after resection of gliomas with no or minimal enhancement. Eur Radiol 2011; 21 (7) 1526-1534
    CrossrefPubMedGoogle Scholar
  • 35 Sæther CA, Torsteinsen M, Torp SH, Sundstrøm S, Unsgård G, Solheim O. Did survival improve after the implementation of intraoperative neuronavigation and 3D ultrasound in glioblastoma surgery? A retrospective analysis of 192 primary operations. J Neurol Surg A Cent Eur Neurosurg 2012; 73 (2) 73-78
    Article in Thieme ConnectPubMedGoogle Scholar
  • 36 Unsgaard G, Selbekk T, Brostrup Müller T , et al. Ability of navigated 3D ultrasound to delineate gliomas and metastases—comparison of image interpretations with histopathology. Acta Neurochir (Wien) 2005; 147 (12) 1259-1269 ; discussion 1269
    CrossrefPubMedGoogle Scholar
  • 37 Unsgaard G, Rygh OM, Selbekk T , et al. Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir (Wien) 2006; 148 (3) 235-253 ; discussion 253
    CrossrefPubMedGoogle Scholar
  • 38 Renovanz M, Hickmann AK, Henkel C, Nadji-Ohl M, Hopf NJ. Navigated versus non-navigated intraoperative ultrasound: is there any impact on the extent of resection of high-grade gliomas? A retrospective clinical analysis. J Neurol Surg A Cent Eur Neurosurg 2014; 75 (3) 224-230
    Article in Thieme ConnectPubMedGoogle Scholar
  • 39 Šteňo A, Karlík M, Mendel P, Čík M, Šteňo J. Navigated three-dimensional intraoperative ultrasound-guided awake resection of low-grade glioma partially infiltrating optic radiation. Acta Neurochir (Wien) 2012; 154 (7) 1255-1262
    CrossrefPubMedGoogle Scholar
  • 40 Selbekk T, Jakola AS, Solheim O , et al. Ultrasound imaging in neurosurgery: approaches to minimize surgically induced image artefacts for improved resection control. Acta Neurochir (Wien) 2013; 155 (6) 973-980
    CrossrefPubMedGoogle Scholar
  • 41 Picht T, Krieg SM, Sollmann N , et al. A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. Neurosurgery 2013; 72 (5) 808-819
    CrossrefPubMedGoogle Scholar
  • 42 Berntsen EM, Gulati S, Solheim O , et al. Functional magnetic resonance imaging and diffusion tensor tractography incorporated into an intraoperative 3-dimensional ultrasound-based neuronavigation system: impact on therapeutic strategies, extent of resection, and clinical outcome. Neurosurgery 2010; 67 (2) 251-264
    CrossrefPubMedGoogle Scholar
  • 43 Wilden JA, Voorhies J, Mosier KM, O'Neill DP, Cohen-Gadol AA. Strategies to maximize resection of complex, or high surgical risk, low-grade gliomas. Neurosurg Focus 2013; 34 (2) E5
    PubMedGoogle Scholar
  • 44 Shaw EG, Berkey B, Coons SW , et al. Recurrence following neurosurgeon-determined gross-total resection of adult supratentorial low-grade glioma: results of a prospective clinical trial. J Neurosurg 2008; 109 (5) 835-841
    CrossrefPubMedGoogle Scholar
  • 45 Duffau H. Awake surgery for incidental WHO grade II gliomas involving eloquent areas. Acta Neurochir (Wien) 2012; 154 (4) 575-584; discussion 584
    CrossrefPubMedGoogle Scholar
  • 46 Dropcho EJ, Soong SJ. The prognostic impact of prior low grade histology in patients with anaplastic gliomas: a case-control study. Neurology 1996; 47 (3) 684-690
    CrossrefPubMedGoogle Scholar
  • 47 Rees J, Watt H, Jäger HR , et al. Volumes and growth rates of untreated adult low-grade gliomas indicate risk of early malignant transformation. Eur J Radiol 2009; 72 (1) 54-64
    CrossrefPubMedGoogle Scholar
  • 48 Rapp M, Floeth FW, Felsberg J , et al. Clinical value of O-(2-[(18)F]-fluoroethyl)-L-tyrosine positron emission tomography in patients with low-grade glioma. Neurosurg Focus 2013; 34 (2) E3
    PubMedGoogle Scholar
  • 49 Jakola AS, Unsgård G, Solheim O. Quality of life in patients with intracranial gliomas: the impact of modern image-guided surgery. J Neurosurg 2011; 114 (6) 1622-1630
    CrossrefPubMedGoogle Scholar
  • 50 Kumabe T, Higano S, Takahashi S, Tominaga T. Ischemic complications associated with resection of opercular glioma. J Neurosurg 2007; 106 (2) 263-269
    CrossrefPubMedGoogle Scholar
  • 51 Khan RB, Gutin PH, Rai SN, Zhang L, Krol G, DeAngelis LM. Use of diffusion weighted magnetic resonance imaging in predicting early postoperative outcome of new neurological deficits after brain tumor resection. Neurosurgery 2006; 59 (1) 60-66 ; discussion 60–66
    CrossrefPubMedGoogle Scholar
  • 52 Dützmann S, Geßler F, Bink A , et al. Risk of ischemia in glioma surgery: comparison of first and repeat procedures. J Neurooncol 2012; 107 (3) 599-607
    CrossrefPubMedGoogle Scholar
  • 53 Neuloh G, Simon M, Schramm J. Stroke prevention during surgery for deep-seated gliomas. Neurophysiol Clin 2007; 37 (6) 383-389
    CrossrefPubMedGoogle Scholar
  • 54 Sanai N, Polley MY, Berger MS. Insular glioma resection: assessment of patient morbidity, survival, and tumor progression. J Neurosurg 2010; 112 (1) 1-9
    CrossrefPubMedGoogle Scholar
  • 55 Duffau H. The conceptual limitation to rely on intraoperative MRI in glioma surgery. World Neurosurg 2014; March 17 (Epub ahead of print)
    PubMedGoogle Scholar
  • 56 Albert FK, Forsting M, Sartor K, Adams HP, Kunze S. Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 1994; 34 (1) 45-60 ; discussion 60–61
    Google Scholar