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The impact of cerebral metastases growth pattern on neurosurgical treatment

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Abstract

The surgical resection of cerebral metastases is one key element in a multimodal therapy of brain oligometastatic patients. Standard surgery alone is often not sufficient to achieve local control. Various reasons have been discussed including microscopic and macroscopic tumor rests after surgery and different growth patterns of cerebral metastases: In this review, we assessed the surgical standard technique and then analyzed the growth pattern of cerebral metastases and discussed its oncologic impact and new strategies in the surgical management of cerebral metastases. A major percentage of cerebral metastases are not sharply delimitated but show an irregular tumor-brain interface or even an infiltrative growth pattern. Different patterns of adjacent brain invasions have been described and may correlate with the prognosis of patients with cerebral metastasis. Even metastases of the same histological subtype and the same origin show a heterogeneous brain invasion pattern. Future therapeutic strategies might have to take this heterogeneity into account. An infiltrative growth pattern of cerebral metastases might be one reason for their extraordinary high local recurrence rate and might have an influence on the individual overall survival. An intraoperative detection of residual tumor and development of more radical surgical techniques is therefore an important neurooncological challenge and might result in better tumor control. Supramarginal resection of cerebral metastases is a promising approach.

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References

  1. Andrews DW, Scott CB, Sperduto PW, Flanders AE, Gaspar LE, Schell MC, Werner-Wasik M, Demas W, Ryu J, Bahary JP, Souhami L, Rotman M, Mehta MP, Curran WJ Jr (2004) Whole brain radiation therapy with or without stereotactic radiosurgery boost for patients with one to three brain metastases: phase III results of the RTOG 9508 randomised trial. Lancet 363:1665–1672

    Article  PubMed  Google Scholar 

  2. Aoyama H, Tago M, Kato N, Toyoda T, Kenjyo M, Hirota S, Shioura H, Inomata T, Kunieda E, Hayakawa K, Nakagawa K, Kobashi G, Shirato H (2007) Neurocognitive function of patients with brain metastasis who received either whole brain radiotherapy plus stereotactic radiosurgery or radiosurgery alone. Int J Radiat Oncol Biol Phys 68:1388–1395

    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 Neurooncol 118:363–367

    Article  PubMed  Google Scholar 

  5. Berghoff AS, Bartsch R, Wohrer A, Streubel B, Birner P, Kros JM, Brastianos PK, von Deimling A, Preusser M (2014) Predictive molecular markers in metastases to the central nervous system: recent advances and future avenues. Acta Neuropathol 128:879–891

    Article  CAS  PubMed  Google Scholar 

  6. Berghoff AS, Ilhan-Mutlu A, Dinhof C, Magerle M, Hackl M, Widhalm G, Hainfellner JA, Dieckmann K, Pichler J, Hutterer M, Melchardt T, Bartsch R, Zielinski CC, Birner P, Preusser M (2015) Differential role of angiogenesis and tumour cell proliferation in brain metastases according to primary tumour type: analysis of 639 cases. Neuropathol Appl Neurobiol 41:e41–e55

    Article  CAS  PubMed  Google Scholar 

  7. Berghoff AS, Ilhan-Mutlu A, Wohrer A, Hackl M, Widhalm G, Hainfellner JA, Dieckmann K, Melchardt T, Dome B, Heinzl H, Birner P, Preusser M (2014) Prognostic significance of Ki67 proliferation index, HIF1 alpha index and microvascular density in patients with non-small cell lung cancer brain metastases. Strahlenther Onkol 190:676–685

    Article  CAS  PubMed  Google Scholar 

  8. 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 Oncol 15:1664–1672

    Article  PubMed  PubMed Central  Google Scholar 

  9. 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 

  10. Brennan C, Yang TJ, Hilden P, Zhang Z, Chan K, Yamada Y, Chan TA, Lymberis SC, Narayana A, Tabar V, Gutin PH, Ballangrud A, Lis E, Beal K (2014) A phase 2 trial of stereotactic radiosurgery boost after surgical resection for brain metastases. Int J Radiat Oncol Biol Phys 88:130–136

    Article  PubMed  PubMed Central  Google Scholar 

  11. Chacko AG, Kumar NK, Chacko G, Athyal R, Rajshekhar V (2003) Intraoperative ultrasound in determining the extent of resection of parenchymal brain tumours—a comparative study with computed tomography and histopathology. Acta Neurochir (Wien) 145:743–748

    Article  CAS  Google Scholar 

  12. Chang EL, Wefel JS, Hess KR, Allen PK, Lang FF, Kornguth DG, Arbuckle RB, Swint JM, Shiu AS, Maor MH, Meyers CA (2009) Neurocognition in patients with brain metastases treated with radiosurgery or radiosurgery plus whole-brain irradiation: a randomised controlled trial. Lancet Oncol 10:1037–1044

    Article  PubMed  Google Scholar 

  13. Choi CY, Chang SD, Gibbs IC, Adler JR, Harsh GR, Lieberson RE, Soltys SG (2012) Stereotactic radiosurgery of the postoperative resection cavity for brain metastases: prospective evaluation of target margin on tumor control. Int J Radiat Oncol Biol Phys 84:336–342

    Article  PubMed  Google Scholar 

  14. D’Andrea G, Angelini A, Romano A, Di Lauro A, Sessa G, Bozzao A, Ferrante L (2012) Intraoperative DTI and brain mapping for surgery of neoplasm of the motor cortex and the corticospinal tract: our protocol and series in BrainSUITE. Neurosurg Rev 35:401–412

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. Goeckenjan G, Sitter H, Thomas M, Branscheid D, Flentje M, Griesinger F, Niederle N, Stuschke M, Blum T, Deppermann KM, Ficker JH, Freitag L, Lubbe AS, Reinhold T, Spath-Schwalbe E, Ukena D, Wickert M, Wolf M, Andreas S, Auberger T, Baum RP, Baysal B, Beuth J, Bickeboller H, Bocking A, Bohle RM, Bruske I, Burghuber O, Dickgreber N, Diederich S, Dienemann H, Eberhardt W, Eggeling S, Fink T, Fischer B, Franke M, Friedel G, Gauler T, Gutz S, Hautmann H, Hellmann A, Hellwig D, Herth F, Heussel CP, Hilbe W, Hoffmeyer F, Horneber M, Huber RM, Hubner J, Kauczor HU, Kirchbacher K, Kirsten D, Kraus T, Lang SM, Martens U, Mohn-Staudner A, Muller KM, Muller-Nordhorn J, Nowak D, Ochmann U, Passlick B, Petersen I, Pirker R, Pokrajac B, Reck M, Riha S, Rube C, Schmittel A, Schonfeld N, Schutte W, Serke M, Stamatis G, Steingraber M, Steins M, Stoelben E, Swoboda L, Teschler H, Tessen HW, Weber M, Werner A, Wichmann HE, Irlinger Wimmer E, Witt C, Worth H, German Respiratory S, German Cancer S (2011) Prevention, diagnosis, therapy, and follow-up of lung cancer: interdisciplinary guideline of the German Respiratory Society and the German Cancer Society. Pneumologie 65:39–59

    Article  CAS  PubMed  Google Scholar 

  17. Hartford AC, Paravati AJ, Spire WJ, Li Z, Jarvis LA, Fadul CE, Rhodes CH, Erkmen K, Friedman J, Gladstone DJ, Hug EB, Roberts DW, Simmons NE (2013) Postoperative stereotactic radiosurgery without whole-brain radiation therapy for brain metastases: potential role of preoperative tumor size. Int J Radiat Oncol Biol Phys 85:650–655

    Article  PubMed  Google Scholar 

  18. Hwang SW, Abozed MM, Hale A, Eisenberg RL, Dvorak T, Yao K, Pfannl R, Mignano J, Zhu JJ, Price LL, Strauss GM, Wu JK (2010) Adjuvant Gamma knife radiosurgery following surgical resection of brain metastases: a 9-year retrospective cohort study. J Neurooncol 98:77–82

    Article  PubMed  Google Scholar 

  19. Jensen CA, Chan MD, McCoy TP, Bourland JD, deGuzman AF, Ellis TL, Ekstrand KE, McMullen KP, Munley MT, Shaw EG, Urbanic JJ, Tatter SB (2011) Cavity-directed radiosurgery as adjuvant therapy after resection of a brain metastasis. J Neurosurg 114:1585–1591

    Article  PubMed  Google Scholar 

  20. Kalkanis SN, Kondziolka D, Gaspar LE, Burri SH, Asher AL, Cobbs CS, Ammirati M, Robinson PD, Andrews DW, Loeffler JS, McDermott M, Mehta MP, Mikkelsen T, Olson JJ, Paleologos NA, Patchell RA, Ryken TC, Linskey ME (2010) The role of surgical resection in the management of newly diagnosed brain metastases: a systematic review and evidence-based clinical practice guideline. J Neurooncol 96:33–43

    Article  PubMed  Google Scholar 

  21. 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 (Wien) 154:1981–1986

    Article  Google Scholar 

  22. Kamp MA, Felsberg J, Sadat H, Kuzibaev J, Steiger HJ, Rapp M, Reifenberger G, Dibue M, Sabel M (2015) 5-ALA-induced fluorescence behavior of reactive tissue changes following glioblastoma treatment with radiation and chemotherapy. Acta Neurochir (Wien) 157:207–213

    Article  Google Scholar 

  23. 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 (Wien) 154:223–228

    Article  Google Scholar 

  24. 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 (Wien) 157:1573–1580

    Article  Google Scholar 

  25. 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 (Wien) 157:905–910, discussion 910-901

    Article  Google Scholar 

  26. Kellogg RG, Straus DC, Choi M, Chaudhry TA, Diaz AZ, Munoz LF (2013) Stereotactic radiosurgery boost to the resection cavity for cerebral metastases: report of overall survival, complications, and corticosteroid protocol. Surg Neurol Int 4:S436–S442

    Article  PubMed  PubMed Central  Google Scholar 

  27. 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 

  28. 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 

  29. Kondziolka D, Lunsford LD (1996) Intraoperative navigation during resection of brain metastases. Neurosurg Clin N Am 7:267–277

    CAS  PubMed  Google Scholar 

  30. Kondziolka D, Patel A, Lunsford LD, Kassam A, Flickinger JC (1999) Stereotactic radiosurgery plus whole brain radiotherapy versus radiotherapy alone for patients with multiple brain metastases. Int J Radiat Oncol Biol Phys 45:427–434

    Article  CAS  PubMed  Google Scholar 

  31. Krieg SM, Schaffner M, Shiban E, Droese D, Obermuller T, Gempt J, Meyer B, Ringel F (2013) Reliability of intraoperative neurophysiological monitoring using motor evoked potentials during resection of metastases in motor-eloquent brain regions: clinical article. J Neurosurg 118:1269–1278

    Article  PubMed  Google Scholar 

  32. Livne O, Harel R, Hadani M, Spiegelmann R, Feldman Z, Cohen ZR (2014) Intraoperative magnetic resonance imaging for resection of intra-axial brain lesions: a decade of experience using low-field magnetic resonance imaging, Polestar N-10, 20, 30 systems. World Neurosurg 82:770–776

    Article  PubMed  Google Scholar 

  33. Mathieu D, Kondziolka D, Flickinger JC, Fortin D, Kenny B, Michaud K, Mongia S, Niranjan A, Lunsford LD (2008) Tumor bed radiosurgery after resection of cerebral metastases. Neurosurgery 62:817–82334

    Article  PubMed  Google Scholar 

  34. Mintz AH, Kestle J, Rathbone MP, Gaspar L, Hugenholtz H, Fisher B, Duncan G, Skingley P, Foster G, Levine M (1996) A randomized trial to assess the efficacy of surgery in addition to radiotherapy in patients with a single cerebral metastasis. Cancer 78:1470–1476

    Article  CAS  PubMed  Google Scholar 

  35. Moghaddasi L, Bezak E, Marcu LG (2012) Current challenges in clinical target volume definition: tumour margins and microscopic extensions. Acta Oncol 51:984–995

    Article  PubMed  Google Scholar 

  36. Nataf F, Schlienger M, Liu Z, Foulquier JN, Gres B, Orthuon A, Vannetzel JM, Escudier B, Meder JF, Roux FX, Touboul E (2008) Radiosurgery with or without a 2-mm margin for 93 single brain metastases. Int J Radiat Oncol Biol Phys 70:766–772

    Article  PubMed  Google Scholar 

  37. Neves S, Mazal PR, Wanschitz J, Rudnay AC, Drlicek M, Czech T, Wustinger C, Budka H (2001) Pseudogliomatous growth pattern of anaplastic small cell carcinomas metastatic to the brain. Clin Neuropathol 20:38–42

    CAS  PubMed  Google Scholar 

  38. Noel G, Simon JM, Valery CA, Cornu P, Boisserie G, Hasboun D, Ledu D, Tep B, Delattre JY, Marsault C, Baillet F, Mazeron JJ (2003) Radiosurgery for brain metastasis: impact of CTV on local control. Radiother Oncol 68:15–21

    Article  PubMed  Google Scholar 

  39. Noordijk EM, Vecht CJ, Haaxma-Reiche H, Padberg GW, Voormolen JH, Hoekstra FH, Tans JT, Lambooij N, Metsaars JA, Wattendorff AR et al (1994) The choice of treatment of single brain metastasis should be based on extracranial tumor activity and age. Int J Radiat Oncol Biol Phys 29:711–717

    Article  CAS  PubMed  Google Scholar 

  40. Obermueller T, Schaeffner M, Shiban E, Droese D, Negwer C, Meyer B, Ringel F, Krieg SM (2015) Intraoperative neuromonitoring for function-guided resection differs for supratentorial motor eloquent gliomas and metastases. BMC Neurol 15:211

    Article  PubMed  PubMed Central  Google Scholar 

  41. 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 

  42. Patchell RA, Tibbs PA, Walsh JW, Dempsey RJ, Maruyama Y, Kryscio RJ, Markesbery WR, Macdonald JS, Young B (1990) A randomized trial of surgery in the treatment of single metastases to the brain. N Engl J Med 322:494–500

    Article  CAS  PubMed  Google Scholar 

  43. Patel AJ, Suki D, Hatiboglu MA, Abouassi H, Shi W, Wildrick DM, Lang FF, Sawaya R (2010) Factors influencing the risk of local recurrence after resection of a single brain metastasis. J Neurosurg 113:181–189

    Article  PubMed  Google Scholar 

  44. Patel AJ, Suki D, Hatiboglu MA, Rao VY, Fox BD, Sawaya R (2015) Impact of surgical methodology on the complication rate and functional outcome of patients with a single brain metastasis. J Neurosurg 122:1132–1143

    Article  PubMed  Google Scholar 

  45. Patil CG, Pricola K, Sarmiento JM, Garg SK, Bryant A, Black KL (2012) Whole brain radiation therapy (WBRT) alone versus WBRT and radiosurgery for the treatment of brain metastases. Cochrane Database Syst Rev 9:CD006121

    Google Scholar 

  46. Raore B, Schniederjan M, Prabhu R, Brat DJ, Shu HK, Olson JJ (2011) Metastasis infiltration: an investigation of the postoperative brain-tumor interface. Int J Radiat Oncol Biol Phys 81:1075–1080

    Article  PubMed  Google Scholar 

  47. Renner C, Lindner D, Schneider JP, Meixensberger J (2005) Evaluation of intra-operative ultrasound imaging in brain tumor resection: a prospective study. Neurol Res 27:351–357

    Article  CAS  PubMed  Google Scholar 

  48. Roberge D, Parney I, Brown PD (2012) Radiosurgery to the postoperative surgical cavity: who needs evidence? Int J Radiat Oncol Biol Phys 83:486–493

    Article  PubMed  Google Scholar 

  49. Sahgal A, Aoyama H, Kocher M, Neupane B, Collette S, Tago M, Shaw P, Beyene J, Chang EL (2015) Phase 3 trials of stereotactic radiosurgery with or without whole-brain radiation therapy for 1 to 4 brain metastases: individual patient data meta-analysis. Int J Radiat Oncol Biol Phys 91:710–717

    Article  PubMed  Google Scholar 

  50. 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 

  51. Shojania KG, Burton EC, McDonald KM, Goldman L (2003) Changes in rates of autopsy-detected diagnostic errors over time: a systematic review. JAMA 289:2849–2856

    Article  PubMed  Google Scholar 

  52. 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 

  53. Soffietti R, Ducati A, Ruda R (2012) Brain metastases. Handb Clin Neurol 105:747–755

    Article  CAS  PubMed  Google Scholar 

  54. Soffietti R, Kocher M, Abacioglu UM, 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, Mueller RP, Tridello G, Collette L, Bottomley A (2013) A European Organisation for Research and Treatment of Cancer phase III trial of adjuvant whole-brain radiotherapy versus observation in patients with one to three brain metastases from solid tumors after surgical resection or radiosurgery: quality-of-life results. J Clin Oncol 31:65–72

    Article  PubMed  Google Scholar 

  55. Soffietti R, Trevisan E, Ruda R (2012) Targeted therapy in brain metastasis. Curr Opin Oncol 24:679–686

    Article  CAS  PubMed  Google Scholar 

  56. Spena G, Garbossa D, Panciani PP, Griva F, Fontanella MM (2013) Purely subcortical tumors in eloquent areas: awake surgery and cortical and subcortical electrical stimulation (CSES) ensure safe and effective surgery. Clin Neurol Neurosurg 115:1595–1601

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  58. Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ (2000) Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg 93:1003–1013

    Article  CAS  PubMed  Google Scholar 

  59. 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  Google Scholar 

  60. 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

    Article  Google Scholar 

  61. Stummer W, Stocker S, Novotny A, Heimann A, Sauer O, Kempski O, Plesnila N, Wietzorrek J, Reulen HJ (1998) In vitro and in vivo porphyrin accumulation by C6 glioma cells after exposure to 5-aminolevulinic acid. J Photochem Photobiol B 45:160–169

    Article  CAS  PubMed  Google Scholar 

  62. Suki D, Abouassi H, Patel AJ, Sawaya R, Weinberg JS, Groves MD (2008) Comparative risk of leptomeningeal disease after resection or stereotactic radiosurgery for solid tumor metastasis to the posterior fossa. J Neurosurg 108:248–257

    Article  PubMed  Google Scholar 

  63. Tabaka J, Nowacki P, Pankowski J (2006) The interaction between lung cancer metastases to the brain and their surroundings. Folia Neuropathol 44:42–49

    PubMed  Google Scholar 

  64. Tan TC, Black PM (2007) Image-guided craniotomy for cerebral metastases: techniques and outcomes. Neurosurgery 61:349–356

    Article  PubMed  Google Scholar 

  65. Tsao MN, Rades D, Wirth A, Lo SS, Danielson BL, Vichare A, Hahn C, Chang EL (2012) International practice survey on the management of brain metastases: Third International Consensus Workshop on Palliative Radiotherapy and Symptom Control. Clin Oncol (R Coll Radiol) 24:e81–e92

    Article  CAS  Google Scholar 

  66. Unsgaard G, Rygh OM, Selbekk T, Muller TB, Kolstad F, Lindseth F, Hernes TA (2006) Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir (Wien) 148:235–253

    Article  CAS  Google Scholar 

  67. Unsgaard G, Selbekk T, Brostrup Muller T, Ommedal S, Torp SH, Myhr G, Bang J, Nagelhus Hernes TA (2005) Ability of navigated 3D ultrasound to delineate gliomas and metastases—comparison of image interpretations with histopathology. Acta Neurochir (Wien) 147:1259–1269

    Article  CAS  Google Scholar 

  68. Utsuki S, Miyoshi N, Oka H, Miyajima Y, Shimizu S, Suzuki S, Fujii K (2007) Fluorescence-guided resection of metastatic brain tumors using a 5-aminolevulinic acid-induced protoporphyrin IX: pathological study. Brain Tumor Pathol 24:53–55

    Article  CAS  PubMed  Google Scholar 

  69. Vecht CJ, Haaxma-Reiche H, Noordijk EM, Padberg GW, Voormolen JH, Hoekstra FH, Tans JT, Lambooij N, Metsaars JA, Wattendorff AR et al (1993) Treatment of single brain metastasis: radiotherapy alone or combined with neurosurgery? Ann Neurol 33:583–590

    Article  CAS  PubMed  Google Scholar 

  70. 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 

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Prof. Sabel is a consultant for Johnson& Johnson and Integra Company. 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 interest; 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., Slotty, P.J., Cornelius, J.F. et al. The impact of cerebral metastases growth pattern on neurosurgical treatment. Neurosurg Rev 41, 77–86 (2018). https://doi.org/10.1007/s10143-016-0760-5

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