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Is it all a matter of size? Impact of maximization of surgical resection in cerebral tumors

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Abstract

The oncological impact of cytoreductive surgery for malignant glioma has been analyzed in a few prospective, randomized studies; however, the impact of different cytoreductive surgical techniques of cerebral tumors remains controversial. Despite retrospective analyses revealing an oncological impact of complete surgical resection in cerebral metastases and low-grade glioma, the oncological impact of further extension of resection to a supramarginal resection remains disputable lacking high-grade evidence: supramarginal resections have yet to be analyzed in malignant glioma. Although extension of resection towards a supramarginal resection was thought to improve outcome and prevent malignant transformation in low-grade glioma, the rate of (temporary) deficits was higher than 50% in recent retrospective studies, and the oncological impact and long-term results have to be analyzed in further (prospective and controlled) studies. Cerebral metastases show a growth pattern different from glioma with less and more locally limited brain invasion. Therefore, local control may be achieved by extension of resection after complete lesionectomy of cerebral metastases. Therefore, supramarginal resection may be a promising approach but must be evaluated in further studies.

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References

  1. Acerbi F, Broggi M, Schebesch KM, Hohne J, Cavallo C, De Laurentis C, Eoli M, Anghileri E, Servida M, Boffano C, Pollo B, Schiariti M, Visintini S, Montomoli C, Bosio L, La Corte E, Broggi G, Brawanski A, Ferroli P (2018) Fluorescein-guided surgery for resection of high-grade gliomas: a multicentric prospective phase II study (FLUOGLIO). Clin Cancer Res 24:52–61

    Article  PubMed  Google Scholar 

  2. Atalar B, Choi CY, GRt H, Chang SD, Gibbs IC, Adler JR, Soltys SG (2013) Cavity volume dynamics after resection of brain metastases and timing of postresection cavity stereotactic radiosurgery. Neurosurgery 72:180–185; discussion 185

    Article  PubMed  Google Scholar 

  3. Baumert BG, Rutten I, Dehing-Oberije C, Twijnstra A, Dirx MJ, Debougnoux-Huppertz RM, Lambin P, Kubat B (2006) A pathology-based substrate for target definition in radiosurgery of brain metastases. Int J Radiat Oncol Biol Phys 66:187–194

    Article  PubMed  Google Scholar 

  4. Benveniste RJ, Ferraro N, Tsimpas A (2014) Yield and utility of routine postoperative imaging after resection of brain metastases. J Neuro-Oncol 118:363–367

    Article  Google Scholar 

  5. Berger MS, Deliganis AV, Dobbins J, Keles GE (1994) The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer 74:1784–1791

    Article  CAS  PubMed  Google Scholar 

  6. Berghoff AS, Rajky O, Winkler F, Bartsch R, Furtner J, Hainfellner JA, Goodman SL, Weller M, Schittenhelm J, Preusser M (2013) Invasion patterns in brain metastases of solid cancers. Neuro-Oncology 15:1664–1672

    Article  PubMed  PubMed Central  Google Scholar 

  7. Borgelt B, Gelber R, Kramer S, Brady LW, Chang CH, Davis LW, Perez CA, Hendrickson FR (1980) The palliation of brain metastases: final results of the first two studies by the Radiation Therapy Oncology Group. Int J Radiat Oncol Biol Phys 6:1–9

    Article  CAS  PubMed  Google Scholar 

  8. Brown PD, Ballman KV, Cerhan JH, Anderson SK, Carrero XW, Whitton AC, Greenspoon J, Parney IF, Laack NNI, Ashman JB, Bahary JP, Hadjipanayis CG, Urbanic JJ, Barker FG 2nd, Farace E, Khuntia D, Giannini C, Buckner JC, Galanis E, Roberge D (2017) Postoperative stereotactic radiosurgery compared with whole brain radiotherapy for resected metastatic brain disease (NCCTG N107C/CEC.3): a multicentre, randomised, controlled, phase 3 trial. Lancet Oncol 18:1049–1060

    Article  PubMed  PubMed Central  Google Scholar 

  9. Capelle L, Fontaine D, Mandonnet E, Taillandier L, Golmard JL, Bauchet L, Pallud J, Peruzzi P, Baron MH, Kujas M, Guyotat J, Guillevin R, Frenay M, Taillibert S, Colin P, Rigau V, Vandenbos F, Pinelli C, Duffau H, French Reseau d'Etude des G (2013) Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization Grade II gliomas: a series of 1097 cases: clinical article. J Neurosurg 118:1157–1168

    Article  PubMed  Google Scholar 

  10. Catapano G, Sgulo FG, Seneca V, Iorio G, de Notaris M, di Nuzzo G (2018) Fluorescein-assisted stereotactic needle biopsy of brain tumors: a single-center experience and systematic review. Neurosurg Rev

  11. De Witt Hamer PC, Robles SG, Zwinderman AH, Duffau H, Berger MS (2012) Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 30:2559–2565

    Article  PubMed  Google Scholar 

  12. DeAngelis LM (2001) Brain tumors. N Engl J Med 344:114–123

    Article  CAS  PubMed  Google Scholar 

  13. Duffau H (2015) Resecting diffuse low-grade gliomas to the boundaries of brain functions: a new concept in surgical neuro-oncology. J Neurosurg Sci 59:361–371

    CAS  PubMed  Google Scholar 

  14. Duffau H, Lopes M, Arthuis F, Bitar A, Sichez JP, Van Effenterre R, Capelle L (2005) Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985–96) and with (1996–2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 76:845–851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Earnest Ft KPJ, Scheithauer BW, Kall BA, Cascino TL, Ehman RL, Forbes GS, Axley PL (1988) Cerebral astrocytomas: histopathologic correlation of MR and CT contrast enhancement with stereotactic biopsy. Radiology 166:823–827

    Article  Google Scholar 

  16. Ewelt C, Nemes A, Senner V, Wolfer J, Brokinkel B, Stummer W, Holling M (2015) Fluorescence in neurosurgery: its diagnostic and therapeutic use. Review of the literature. J Photochem Photobiol B 148:302–309

    Article  CAS  PubMed  Google Scholar 

  17. Eyupoglu IY, Hore N, Fan Z, Buslei R, Merkel A, Buchfelder M, Savaskan NE (2015) Intraoperative vascular DIVA surgery reveals angiogenic hotspots in tumor zones of malignant gliomas. Sci Rep 5:7958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Eyupoglu IY, Hore N, Merkel A, Buslei R, Buchfelder M, Savaskan N (2016) Supra-complete surgery via dual intraoperative visualization approach (DiVA) prolongs patient survival in glioblastoma. Oncotarget 7:25755–25768

    Article  PubMed  PubMed Central  Google Scholar 

  19. Gousias K, Schramm J, Simon M (2014) Extent of resection and survival in supratentorial infiltrative low-grade gliomas: analysis of and adjustment for treatment bias. Acta Neurochir 156:327–337

    Article  PubMed  Google Scholar 

  20. Ius T, Isola M, Budai R, Pauletto G, Tomasino B, Fadiga L, Skrap M (2012) Low-grade glioma surgery in eloquent areas: volumetric analysis of extent of resection and its impact on overall survival. A single-institution experience in 190 patients: clinical article. J Neurosurg 117:1039–1052

    Article  PubMed  Google Scholar 

  21. Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, Unsgard G, Solheim O (2012) Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA 308:1881–1888

    Article  CAS  PubMed  Google Scholar 

  22. Jakola AS, Unsgard G, Myrmel KS, Kloster R, Torp SH, Lindal S, Solheim O (2012) Low grade gliomas in eloquent locations—implications for surgical strategy, survival and long term quality of life. PLoS One 7:e51450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Jarvis LA, Simmons NE, Bellerive M, Erkmen K, Eskey CJ, Gladstone DJ, Hug EB, Roberts DW, Hartford AC (2012) Tumor bed dynamics after surgical resection of brain metastases: implications for postoperative radiosurgery. Int J Radiat Oncol Biol Phys 84:943–948

    Article  PubMed  Google Scholar 

  24. Kamp MA, Dibue M, Niemann L, Reichelt DC, Felsberg J, Steiger HJ, Szelenyi A, Rapp M, Sabel M (2012) Proof of principle: supramarginal resection of cerebral metastases in eloquent brain areas. Acta Neurochir 154:1981–1986

    Article  PubMed  Google Scholar 

  25. Kamp MA, Grosser P, Felsberg J, Slotty PJ, Steiger HJ, Reifenberger G, Sabel M (2012) 5-aminolevulinic acid (5-ALA)-induced fluorescence in intracerebral metastases: a retrospective study. Acta Neurochir 154:223–228 discussion 228

    Article  PubMed  Google Scholar 

  26. Kamp MA, Rapp M, Buhner J, Slotty PJ, Reichelt D, Sadat H, Dibue-Adjei M, Steiger HJ, Turowski B, Sabel M (2015) Early postoperative magnet resonance tomography after resection of cerebral metastases. Acta Neurochir 157:1573–1580

    Article  PubMed  Google Scholar 

  27. Kamp MA, Rapp M, Slotty PJ, Turowski B, Sadat H, Smuga M, Dibue-Adjei M, Steiger HJ, Szelenyi A, Sabel M (2015) Incidence of local in-brain progression after supramarginal resection of cerebral metastases. Acta Neurochir 157:905–910 discussion 910-901

    Article  PubMed  Google Scholar 

  28. Kamp MA, Slotty PJ, Cornelius JF, Steiger HJ, Rapp M, Sabel M (2016) The impact of cerebral metastases growth pattern on neurosurgical treatment. Neurosurg Rev

  29. Kelly PJ, Daumas-Duport C, Scheithauer BW, Kall BA, Kispert DB (1987) Stereotactic histologic correlations of computed tomography- and magnetic resonance imaging-defined abnormalities in patients with glial neoplasms. Mayo Clin Proc 62:450–459

    Article  CAS  PubMed  Google Scholar 

  30. Kocher M, Soffietti R, Abacioglu U, Villa S, Fauchon F, Baumert BG, Fariselli L, Tzuk-Shina T, Kortmann RD, Carrie C, Ben Hassel M, Kouri M, Valeinis E, van den Berge D, Collette S, Collette L, Mueller RP (2011) Adjuvant whole-brain radiotherapy versus observation after radiosurgery or surgical resection of one to three cerebral metastases: results of the EORTC 22952-26001 study. J Clin Oncol 29:134–141

    Article  PubMed  Google Scholar 

  31. Kocher M, Wittig A, Piroth MD, Treuer H, Seegenschmiedt H, Ruge M, Grosu AL, Guckenberger M (2014) Stereotactic radiosurgery for treatment of brain metastases. A report of the DEGRO Working Group on Stereotactic Radiotherapy. Strahlenther Onkol 190:521–532

    Article  PubMed  Google Scholar 

  32. Laws ER, Parney IF, Huang W, Anderson F, Morris AM, Asher A, Lillehei KO, Bernstein M, Brem H, Sloan A, Berger MS, Chang S, Glioma Outcomes I (2003) Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project. J Neurosurg 99:467–473

    Article  PubMed  Google Scholar 

  33. Li YM, Suki D, Hess K, Sawaya R (2016) The influence of maximum safe resection of glioblastoma on survival in 1229 patients: can we do better than gross-total resection? J Neurosurg 124:977–988

    Article  PubMed  Google Scholar 

  34. Lima GL, Zanello M, Mandonnet E, Taillandier L, Pallud J, Duffau H (2016) Incidental diffuse low-grade gliomas: from early detection to preventive neuro-oncological surgery. Neurosurg Rev 39:377–384

    Article  PubMed  Google Scholar 

  35. McGirt MJ, Chaichana KL, Attenello FJ, Weingart JD, Than K, Burger PC, Olivi A, Brem H, Quinones-Hinojosa A (2008) Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery 63:700–707; author reply 707-708

    Article  PubMed  Google Scholar 

  36. Network TEL-GG (2017) Evidenced-based medicine in glioma: molecular biology is only part of the story. Lancet Oncol 18:e429

    Article  Google Scholar 

  37. Osswald M, Jung E, Sahm F, Solecki G, Venkataramani V, Blaes J, Weil S, Horstmann H, Wiestler B, Syed M, Huang L, Ratliff M, Karimian Jazi K, Kurz FT, Schmenger T, Lemke D, Gommel M, Pauli M, Liao Y, Haring P, Pusch S, Herl V, Steinhauser C, Krunic D, Jarahian M, Miletic H, Berghoff AS, Griesbeck O, Kalamakis G, Garaschuk O, Preusser M, Weiss S, Liu H, Heiland S, Platten M, Huber PE, Kuner T, von Deimling A, Wick W, Winkler F (2015) Brain tumour cells interconnect to a functional and resistant network. Nature 528:93–98

    Article  CAS  PubMed  Google Scholar 

  38. Pallud J, Audureau E, Blonski M, Sanai N, Bauchet L, Fontaine D, Mandonnet E, Dezamis E, Psimaras D, Guyotat J, Peruzzi P, Page P, Gal B, Parraga E, Baron MH, Vlaicu M, Guillevin R, Devaux B, Duffau H, Taillandier L, Capelle L, Huberfeld G (2014) Epileptic seizures in diffuse low-grade gliomas in adults. Brain 137:449–462

    Article  PubMed  Google Scholar 

  39. Patchell RA, Tibbs PA, Regine WF, Dempsey RJ, Mohiuddin M, Kryscio RJ, Markesbery WR, Foon KA, Young B (1998) Postoperative radiotherapy in the treatment of single metastases to the brain: a randomized trial. JAMA 280:1485–1489

    Article  CAS  PubMed  Google Scholar 

  40. Pessina F, Navarria P, Cozzi L, Ascolese AM, Maggi G, Rossi M, Riva M, Scorsetti M, Bello L (2016) Role of surgical resection in patients with single large brain metastases: feasibility, morbidity, and local control evaluation. World Neurosurg 94:6–12

    Article  PubMed  Google Scholar 

  41. Rapp M, Baernreuther J, Turowski B, Steiger HJ, Sabel M, Kamp MA (2017) Recurrence pattern analysis of primary glioblastoma. World Neurosurg 103:733–740

    Article  PubMed  Google Scholar 

  42. Roelz R, Strohmaier D, Jabbarli R, Kraeutle R, Egger K, Coenen VA, Weyerbrock A, Reinacher PC (2016) Residual tumor volume as best outcome predictor in low grade glioma—a nine-years near-randomized survey of surgery vs. biopsy. Sci Rep 6:32286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Sahm F, Capper D, Jeibmann A, Habel A, Paulus W, Troost D, von Deimling A (2012) Addressing diffuse glioma as a systemic brain disease with single-cell analysis. Arch Neurol 69:523–526

    Article  PubMed  Google Scholar 

  44. Schebesch KM, Brawanski A, Hohenberger C, Hohne J (2016) Fluorescein sodium-guided surgery of malignant brain tumors: history, current concepts, and future project. Turk Neurosurg 26:185–194

    PubMed  Google Scholar 

  45. Schebesch KM, Proescholdt M, Hohne J, Hohenberger C, Hansen E, Riemenschneider MJ, Ullrich W, Doenitz C, Schlaier J, Lange M, Brawanski A (2013) Sodium fluorescein-guided resection under the YELLOW 560 nm surgical microscope filter in malignant brain tumor surgery--a feasibility study. Acta Neurochir 155:693–699

    Article  PubMed  Google Scholar 

  46. Schomas DA, Laack NN, Brown PD (2009) Low-grade gliomas in older patients: long-term follow-up from Mayo Clinic. Cancer 115:3969–3978

    Article  PubMed  Google Scholar 

  47. Schomas DA, Laack NN, Rao RD, Meyer FB, Shaw EG, O'Neill BP, Giannini C, Brown PD (2009) Intracranial low-grade gliomas in adults: 30-year experience with long-term follow-up at Mayo Clinic. Neuro-Oncology 11:437–445

    Article  PubMed  PubMed Central  Google Scholar 

  48. Senft C, Bink A, Franz K, Vatter H, Gasser T, Seifert V (2011) Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 12:997–1003

    Article  PubMed  Google Scholar 

  49. Siam L, Bleckmann A, Chaung HN, Mohr A, Klemm F, Barrantes-Freer A, Blazquez R, Wolff HA, Luke F, Rohde V, Stadelmann C, Pukrop T (2015) The metastatic infiltration at the metastasis/brain parenchyma-interface is very heterogeneous and has a significant impact on survival in a prospective study. Oncotarget 6:29254–29267

    Article  PubMed  PubMed Central  Google Scholar 

  50. 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 26:1338–1345

    Article  PubMed  Google Scholar 

  51. Stummer W, Kamp MA (2009) The importance of surgical resection in malignant glioma. Curr Opin Neurol 22:645–649

    Article  PubMed  Google Scholar 

  52. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ, Group AL-GS (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392–401

    Article  CAS  PubMed  Google Scholar 

  53. Stummer W, Reulen HJ, Meinel T, Pichlmeier U, Schumacher W, Tonn JC, Rohde V, Oppel F, Turowski B, Woiciechowsky C, Franz K, Pietsch T, Group AL-GS (2008) Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 62:564–576 discussion 564-576

    Article  PubMed  Google Scholar 

  54. Thien A, Han JX, Kumar K, Ng YP, Rao JP, Ng WH, King NKK (2018) Investigation of the usefulness of fluorescein sodium fluorescence in stereotactic brain biopsy. Acta Neurochir 160:317–324

    Article  PubMed  Google Scholar 

  55. Toennis W, Walter W. Glioblastoma multiforme (report on 2611 cases). Acta Neurochir Suppl (Wien) 1959;6:40–62.

    CAS  Google Scholar 

  56. Vuorinen V, Hinkka S, Farkkila M, Jaaskelainen J (2003) Debulking or biopsy of malignant glioma in elderly people—a randomised study. Acta Neurochir 145:5–10

    Article  CAS  PubMed  Google Scholar 

  57. Weller M, Butowski N, Tran DD, Recht LD, Lim M, Hirte H, Ashby L, Mechtler L, Goldlust SA, Iwamoto F, Drappatz J, O'Rourke DM, Wong M, Hamilton MG, Finocchiaro G, Perry J, Wick W, Green J, He Y, Turner CD, Yellin MJ, Keler T, Davis TA, Stupp R, Sampson JH, AIt i (2017) Rindopepimut with temozolomide for patients with newly diagnosed, EGFRvIII-expressing glioblastoma (ACT IV): a randomised, double-blind, international phase 3 trial. Lancet Oncol 18:1373–1385

    Article  CAS  PubMed  Google Scholar 

  58. Weller M, van den Bent M, Tonn JC, Stupp R, Preusser M, Cohen-Jonathan-Moyal E, Henriksson R, Le Rhun E, Balana C, Chinot O, Bendszus M, Reijneveld JC, Dhermain F, French P, Marosi C, Watts C, Oberg I, Pilkington G, Baumert BG, MJB T, Hegi M, Westphal M, Reifenberger G, Soffietti R, Wick W, European Association for Neuro-Oncology Task Force on G (2017) European Association for Neuro-Oncology (EANO) guideline on the diagnosis and treatment of adult astrocytic and oligodendroglial gliomas. Lancet Oncol 18:e315–e329

    Article  PubMed  Google Scholar 

  59. Yan JL, van der Hoorn A, Larkin TJ, Boonzaier NR, Matys T, Price SJ (2017) Extent of resection of peritumoral diffusion tensor imaging-detected abnormality as a predictor of survival in adult glioblastoma patients. J Neurosurg 126:234–241

    Article  PubMed  Google Scholar 

  60. Yeh SA, Ho JT, Lui CC, Huang YJ, Hsiung CY, Huang EY (2005) Treatment outcomes and prognostic factors in patients with supratentorial low-grade gliomas. Br J Radiol 78:230–235

    Article  PubMed  Google Scholar 

  61. Yoo H, Kim YZ, Nam BH, Shin SH, Yang HS, Lee JS, Zo JI, Lee SH (2009) Reduced local recurrence of a single brain metastasis through microscopic total resection. J Neurosurg 110:730–736

    Article  PubMed  Google Scholar 

  62. Yordanova YN, Moritz-Gasser S, Duffau H (2011) Awake surgery for WHO grade II gliomas within “noneloquent” areas in the left dominant hemisphere: toward a “supratotal” resection. Clinical article J Neurosurg 115:232–239

    Article  PubMed  Google Scholar 

  63. Youland RS, Khwaja SS, Schomas DA, Keating GF, Wetjen NM, Laack NN (2013) Prognostic factors and survival patterns in pediatric low-grade gliomas over 4 decades. J Pediatr Hematol Oncol 35:197–205

    Article  PubMed  Google Scholar 

  64. Youland RS, Schomas DA, Brown PD, Nwachukwu C, Buckner JC, Giannini C, Parney IF, Laack NN (2013) Changes in presentation, treatment, and outcomes of adult low-grade gliomas over the past fifty years. Neuro-Oncology 15:1102–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Marcel A. Kamp.

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Prof. Sabel is a consultant for Johnson & Johnson Company and Integra Company. Dr. Dibué-Adjei is an employee of LivaNova PLC, manufacturer of vagus nerve stimulators. All other authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interests; and expert testimony or patent-licensing arrangements) or non-financial interest (such as personal or professional relationships, affiliations, knowledge, or beliefs) in the subject matter or materials discussed in this manuscript.

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Kamp, M.A., Dibué-Adjei, M., Cornelius, J. et al. Is it all a matter of size? Impact of maximization of surgical resection in cerebral tumors. Neurosurg Rev 42, 835–842 (2019). https://doi.org/10.1007/s10143-018-0963-z

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