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Insular lobe surgery and cognitive impairment in gliomas operated with intraoperative neurophysiological monitoring

  • Original Article - Tumor - Glioma
  • Published:
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Abstract

Background

For a long time, surgery of insular gliomas was considered at high risk for postoperative cognitive deficits, but recent studies highlighted the feasibility of the surgical approach. The aims of our study were to investigate the presence of language impairment before and after surgery and the relationship between language impairment and tumor volume preoperatively and extent of resection (EOR) 3 months after surgery.

Methods

Thirty-five patients with insular gliomas underwent an extensive language assessment before and few days after surgery, and after 3 months. Intraoperative neurophysiological monitoring (IOM) and brain mapping with direct electrical stimulation (DES) were used in all the cases; 8 patients underwent awake craniotomy. Statistical analysis was performed on the language tests administered.

Results

Patients with pure left insular lesion showed language impairment before and after surgery. Overall, patients with a left lesion showed a drop of performance after surgery followed by a partial recovery. Moreover, when the tumor involved the insula and adjacent networks, we observed a more severe deficit. No correlations were found between tumor volume, EOR, and language impairment.

Conclusions

Left insular lobe is an important hub in language networks; its involvement determines pre- and postsurgical deficits, together with the involvement of white matter connections. Tumor volume and EOR are not risk factors per se directly related to language functioning. Surgery of insular gliomas is possible with a pre- and intraoperative extensive study of the patient with IOM and awake surgery, and encouraged by the trend of cognitive recovery highlighted.

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Abbreviations

DES:

Direct electrical stimulation

EOR:

Extent of resection

F:

Female

FI:

Fronto-insular

FR:

Face Recognition

FTI:

Fronto-temporo-insular

HGG:

High-grade glioma

I:

Insular

IOM:

Intraoperative neurophysiological monitoring

LGG:

Low-grade glioma

LH:

Left hemisphere

M:

Male

MR:

Magnetic resonance

NWR:

Non-Word Repetition

ON:

Object Naming

PF:

Phonemic Fluency

RH:

Right hemisphere

SD:

Standard deviation

SF:

Semantic Fluency

SR:

Sentence Repetition

TI:

Temporo-insular

TT:

Token Test

VN:

Verb Naming

WHO:

World Health Organization

WR:

Word Repetition

References

  1. Ackermann H, Riecker A (2004) The contribution of the insula to motor aspects of speech production: a review and a hypothesis. Brain Lang 89(2):320–328

    PubMed  Google Scholar 

  2. Ackermann H, Riecker A (2010) The contribution(s) of the insula to speech production: a review of the clinical and functional imaging literature. Brain Struct Funct 214(5–6):419–433

    PubMed  Google Scholar 

  3. Alimohamadi M, Shirani M, Shariat Moharari R, Pour-Rashidi A, Ketabchi M, Khajavi M, Arami M, Amirjamshidi A (2016) Application of awake craniotomy and intraoperative brain mapping for surgical resection of insular gliomas of the dominant hemisphere. World Neurosurg 92:151–158

    PubMed  Google Scholar 

  4. Ardila A (1999) The role of insula in language: an unsettled question. Aphasiology 13(1):79–87

    Google Scholar 

  5. Ardila A, Bernal B, Rosselli M (2014) Participation of the insula in language revisited: a meta-analytic connectivity study. J Neurolinguistics 29(1):31–41

    Google Scholar 

  6. Ardila A, Bernal B, Rosselli M (2016) How localized are language brain areas? a review of Brodmann areas involvement in oral language. Arch Clin Neuropsychol 31(1):112–122

    PubMed  Google Scholar 

  7. Bertani G, Fava E, Casaceli G, Carrabba G, Casarotti A, Papagno C, Castellano A, Falini A, Gaini SM, Bello L (2009) Intraoperative mapping and monitoring of brain functions for the resection of low-grade gliomas: technical considerations. Neurosurg Focus 27(4):E4

    PubMed  Google Scholar 

  8. Borovsky A, Saygin AP, Bates E, Dronkers N (2007) Lesion correlates of conversational speech production deficits. Neuropsychologia 45(11):2525–2533

    PubMed  PubMed Central  Google Scholar 

  9. Calder AJ, Keane J, Manes F, Antoun N, Young AW (2000) Impaired recognition and experience of disgust following brain injury. Nat Neurosci 3(11):1077–1078

    CAS  PubMed  Google Scholar 

  10. Capitani E (1997) Normative data and neuropsychological assessment. Common problems in clinical practice and research. Neuropsychol Rehabil 7(4):295–310

    Google Scholar 

  11. Carrabba G, Bertani G, Cogiamanian F, Ardolino G, Zarino B, Di Cristofori A, Locatelli M, Caroli M, Rampini P (2016) Role of intraoperative neurophysiologic monitoring in the resection of thalamic astrocytomas. World Neurosurg 94:50–56

    PubMed  Google Scholar 

  12. Catricalà E, Della Rosa PA, Ginex V, Mussetti Z, Plebani V, Cappa SF (2013) An Italian battery for the assessment of semantic memory disorders. Neurol Sci 34(6):985–993

    PubMed  Google Scholar 

  13. Cereda C, Ghika J, Maeder P, Bogousslavsky J (2002) Strokes restricted to the insular cortex. Neurology 59(12):1950–1955

    CAS  PubMed  Google Scholar 

  14. Damasio H, Damasio AR (1980) The anatomical basis of conduction aphasia. Brain 103(2):337–350

    CAS  PubMed  Google Scholar 

  15. Dronkers NF (1996) A new brain region for coordinating speech articulation. Nature 384(6605):159–161

    CAS  PubMed  Google Scholar 

  16. Duerden EG, Arsalidou M, Lee M, Taylor MJ (2013) Lateralization of affective processing in the insula. Neuroimage 78:159–175

    PubMed  Google Scholar 

  17. Duffau H, Bauchet L, Lehéricy S, Capelle L (2001) Functional compensation of the left dominant insula for language. Neuroreport 12(10):2159–2163

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  19. Duffau H, Capelle L, Lopes M, Faillot T, Sichez JP, Fohanno D (2000) The insular lobe: physiopathological and surgical considerations. Neurosurgery 47(4):801–810 discussion 810-1

    CAS  PubMed  Google Scholar 

  20. Duffau H, Denvil D, Capelle L (2002) 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 72(4):511–516

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Duffau H, Moritz-Gasser S, Gatignol P (2009) Functional outcome after language mapping for insular World Health Organization grade II gliomas in the dominant hemisphere: experience with 24 patients. Neurosurg Focus. https://doi.org/10.3171/2009.5.FOCUS0938

  22. Eickhoff SB, Heim S, Zilles K, Amunts K (2009) A systems perspective on the effective connectivity of overt speech production. Philos Trans A Math Phys Eng Sci 367(1896):2399–2421

    PubMed  PubMed Central  Google Scholar 

  23. Eseonu CI, ReFaey K, Garcia O, Raghuraman G, Quinones-Hinojosa A (2017) Volumetric analysis of extent of resection, survival, and surgical outcomes for insular gliomas. World Neurosurg 103:265–274

    PubMed  Google Scholar 

  24. Gogolla N (2017) The insular cortex. Curr Biol 27(12):R580–R586

    CAS  PubMed  Google Scholar 

  25. Grabowski MM, Recinos PF, Nowacki AS, Schroeder JL, Angelov L, Barnett GH, Vogelbaum MA (2014) Residual tumor volume versus extent of resection: predictors of survival after surgery for glioblastoma. J Neurosurg 121(5):1115–1123

    PubMed  Google Scholar 

  26. Guldin WO, Grüsser OJ (1998) Is there a vestibular cortex? Trends Neurosci 21(6):254–259

    CAS  PubMed  Google Scholar 

  27. Ibañez A, Gleichgerrcht E, Manes F (2010) Clinical effects of insular damage in humans. Brain Struct Funct 214(5–6):397–410

    PubMed  Google Scholar 

  28. Jude Tramo M, Loftus WC, Thomas CE, Green RL, Mott LA, Gazzaniga MS (1995) Surface area of human cerebral cortex and its gross morphological subdivisions: in vivo measurements in monozygotic twins suggest differential hemisphere effects of genetic factors. J Cogn Neurosci 7(2):292–302

    Google Scholar 

  29. Kim Y-H, Kim C-Y (2012) Current surgical management of insular gliomas. Neurosurg Clin N Am 23(2):199–206

    PubMed  Google Scholar 

  30. Kreisler A, Godefroy O, Delmaire C, Debachy B, Leclercq M, Pruvo JP, Leys D (2000) The anatomy of aphasia revisited. Neurology 54(5):1117–1123

    CAS  PubMed  Google Scholar 

  31. Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214(5–6):519–534

    PubMed  PubMed Central  Google Scholar 

  32. Lacroix M, Abi-Said D, Fourney DR et al (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95(2):190–198

    CAS  PubMed  Google Scholar 

  33. Lang FF, Olansen NE, DeMonte F, Gokaslan ZL, Holland EC, Kalhorn C, Sawaya R (2001) Surgical resection of intrinsic insular tumors: complication avoidance. J Neurosurg 95(4):638–650

    CAS  PubMed  Google Scholar 

  34. Loit MP, Rheault F, Gayat E, Poisson I, Froelich S, Zhi N, Velut S, Mandonnet E (2019) Hotspots of small strokes in glioma surgery: an overlooked risk? Acta Neurochir 161(1):91–98

    PubMed  Google Scholar 

  35. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131(6):803–820

    PubMed  Google Scholar 

  36. Mandonnet E (2019) Transopercular resection of IDH–mutated insular glioma: a critical appraisal of an initial experience. World Neurosurg 132:e563–e576

    PubMed  Google Scholar 

  37. Mandonnet E, Martino J, Sarubbo S, Corrivetti F, Bouazza S, Bresson D, Duffau H, Froelich S (2017) Neuronavigated fiber dissection with pial preservation: laboratory model to simulate opercular approaches to insular tumors. World Neurosurg 98:239–242

    PubMed  Google Scholar 

  38. Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214(5–6):655–667

    PubMed  PubMed Central  Google Scholar 

  39. Miceli G, Laudanna C, Burani C, Capasso R (1994) Batteria per l’analisi dei deficit afasici (BADA). Università Cattolica del Sacro Cuore Policlinico Gemelli/Cepsag, Rome

  40. Nestor PJ, Graham NL, Fryer TD, Williams GB, Patterson K, Hodges JR (2003) Progressive non-fluent aphasia is associated with hypometabolism centred on the left anterior insula. Brain 126(11):2406–2418

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  42. Novelli G, Papagno C, Capitani E, Laiacona M, Vallar G, Cappa SF (1986) Tre test clinici di ricerca e produzione lessicale. Taratura su soggetti normali. Arch Psicol Neurol Psichiatr

  43. Oh A, Duerden EG, Pang EW (2014) The role of the insula in speech and language processing. Brain Lang 135:96–103

    PubMed  PubMed Central  Google Scholar 

  44. Papagno C, Casarotti A, Comi A, Gallucci M, Riva M, Bello L (2012) Measuring clinical outcomes in neuro-oncology. A battery to evaluate low-grade gliomas (LGG). J Neuro-Oncol 108(2):269–275

    Google Scholar 

  45. Papagno C, Casarotti A, Zarino B, Crepaldi D (2020) A new test of action verb naming: normative data from 290 Italian adults. Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology, 41(10), 2811–2817

  46. Penfield W, Faulk ME (1955) The insula: further observations on its function. Brain 78(4):445–470

    CAS  PubMed  Google Scholar 

  47. Ribas EC, Yagmurlu K, De Oliveira E, Ribas GC, Rhoton A (2018) Microsurgical anatomy of the central core of the brain. J Neurosurg 129(3):752–769

    PubMed  Google Scholar 

  48. Rizzo S, Venneri A, Papagno C (2002) Famous face recognition and naming test: a normative study. Neurol Sci 23(4):153–159

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  50. Sanai N, Polley M-Y, Berger MS (2010) Insular glioma resection: assessment of patient morbidity, survival, and tumor progression. J Neurosurg 112(1):1–9

    PubMed  Google Scholar 

  51. Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS (2011) An extent of resection threshold for newly diagnosed glioblastomas: clinical article. J Neurosurg 115(1):3–8

    PubMed  Google Scholar 

  52. Santini B, Talacchi A, Squintani G, Casagrande F, Capasso R, Miceli G (2012) Cognitive outcome after awake surgery for tumors in language areas. J Neuro-Oncol 108(2):319–326

    CAS  Google Scholar 

  53. Satoer D, Visch-Brink E, Smits M, Kloet A, Looman C, Dirven C, Vincent A (2014) Long-term evaluation of cognition after glioma surgery in eloquent areas. J Neuro-Oncol 116(1):153–160

    Google Scholar 

  54. Saygin AP, Wilson SM, Dronkers NF, Bates E (2004) Action comprehension in aphasia: linguistic and non-linguistic deficits and their lesion correlates. Neuropsychologia 42(13):1788–1804

    PubMed  Google Scholar 

  55. Shuren J (1993) Insula and aphasia. J Neurol 240(4):216–218

    CAS  PubMed  Google Scholar 

  56. Simon M, Neuloh G, Von Lehe M, Meyer B, Schramm J (2009) Insular gliomas: the case for surgical management - clinical article. J Neurosurg 110(4):685–695

    PubMed  Google Scholar 

  57. Singer T, Klimecki OM (2014) Empathy and compassion. Curr Biol 24(18):R875–R878

    CAS  PubMed  Google Scholar 

  58. Skrap M, Mondani M, Tomasino B, Weis L, Budai R, Pauletto G, Eleopra R, Fadiga L, Ius T (2012) Surgery of insular nonenhancing gliomas: volumetric analysis of tumoral resection, clinical outcome, and survival in a consecutive series of 66 cases. Neurosurgery 70(5):1081–1093 discussion 1093-4

    PubMed  Google Scholar 

  59. Small DM, Prescott J (2005) Odor/taste integration and the perception of flavor. Experimental brain research 166(3–4):345–357

  60. Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, Tihan T, Vandenberg S, McDermott MW, Berger MS (2008) Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26(8):1338–1345

    PubMed  Google Scholar 

  61. Spinnler H, Tognoni G (1987) Standardizzazione e taratura italiana di test neuropsicologici. Gruppo Italiano per lo Studio Neuropsicologico dell'Invecchiamento [Italian standardization and classification of Neuropsychological tests. The Italian Group on the Neuropsychological Study of Aging]. Ital J Neurol Sci Suppl 8, 1–120

  62. Sul B, Lee KB, Hong BY, Kim JS, Kim J, Hwang WS, Lim SH (2019) Association of Lesion Location With Long-Term Recovery in Post-stroke Aphasia and Language Deficits. Front Neurol 10:776. https://doi.org/10.3389/fneur.2019.00776

  63. Swisher LP, Sarno MT (1969) Token test scores of three matched patient groups: left brain-damaged with aphasia; right brain-damaged without aphasia; non-brain-damaged. Cortex 5(3):264–273

    CAS  PubMed  Google Scholar 

  64. Uddin LQ, Nomi JS, Hébert-Seropian B, Ghaziri J, Boucher O (2017) Structure and function of the human insula. J Clin Neurophysiol 34(4):300–306

    PubMed  PubMed Central  Google Scholar 

  65. Wu AS, Witgert ME, Lang FF, Xiao L, Bekele BN, Meyers CA, Ferson D, Wefel JS (2011) Neurocognitive function before and after surgery for insular gliomas. J Neurosurg 115(6):1115–1125

    PubMed  Google Scholar 

  66. Yaşargil MG, von Ammon K, Cavazos E, Doczi T, Reeves JD, Roth P (1992) Tumours of the limbic and paralimbic systems. Acta Neurochir 118(1–2):40–52

    PubMed  Google Scholar 

  67. Zarino B, Crespi M, Launi M, Casarotti A (2014) A new standardization of semantic verbal fluency test. Neurol Sci 35(9):1405–1411

    PubMed  Google Scholar 

  68. Zarino B, Di Cristofori A, Fornara GA, Bertani GA, Locatelli M, Caroli M, Rampini P, Cogiamanian F, Crepaldi D, Carrabba G (2020) Long-term follow-up of neuropsychological functions in patients with high grade gliomas: can cognitive status predict patient’s outcome after surgery? Acta Neurochir 162(4):803–812

    PubMed  Google Scholar 

  69. Zentner J, Meyer B, Stangl A, Schramm J (1996) Intrinsic tumors of the insula: a prospective surgical study of 30 patients. J Neurosurg 85(2):263–271

    CAS  PubMed  Google Scholar 

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Author information

Author notes

  1. Barbara Zarino and Martina Andrea Sirtori contributed equally to the study and should therefore be considered as first co-authors.

Authors and Affiliations

  1. Neurosurgery Unit, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Via Francesco Sforza 35, Padiglione Monteggia, 20122, Milan, Italy

    Barbara Zarino, Martina Andrea Sirtori, Giulio Andrea Bertani, Manuela Caroli, Marco Locatelli & Giorgio Carrabba

  2. Department of Psychology, University of Milano-Bicocca, Milan, Italy

    Martina Andrea Sirtori & Marco Locatelli

  3. Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy

    Tommaso Meschini & Marco Locatelli

  4. Neuropathophysilogy Unit, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Milan, Italy

    Cristina Bana & Linda Borellini

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  1. Barbara Zarino
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Correspondence to Barbara Zarino.

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Zarino, B., Sirtori, M.A., Meschini, T. et al. Insular lobe surgery and cognitive impairment in gliomas operated with intraoperative neurophysiological monitoring. Acta Neurochir 163, 1279–1289 (2021). https://doi.org/10.1007/s00701-020-04643-9

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