Surgery for intramedullary spinal cord ependymomas in the neuromonitoring era: results from a consecutive series of 100 patients

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  • 1 Section of Neurosurgery, Department of Neurosciences Biomedicine and Movement Sciences, University Hospital, Verona;
  • | 2 Institute of Neurosurgery, University Hospital, Verona; and
  • | 3 Institute of Neurosurgery, Catholic University of Rome, Rome, Italy
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OBJECTIVE

The established treatment of intramedullary spinal cord ependymomas (ISCEs) is resection. Surgical series reporting treatment results often lack homogeneity, as these are collected over long time spans and their analysis is plagued by surgical learning curves and inconsistent use of intraoperative neurophysiological monitoring (IONM). The authors report the oncological and functional long-term outcomes in a modern series of 100 consecutive ISCEs that were resected between 2000 and 2015 by a surgically experienced team that consistently utilized IONM.

METHODS

In this retrospective study, the authors tailored surgical strategy and multimodal IONM, including somatosensory evoked potentials, muscle motor evoked potentials (mMEPs), and D-waves, with the aim of gross-total resection (GTR). Preservation of the D-wave was the primary objective, and preservation of mMEPs was the second functional objective. Functional status was evaluated using the modified McCormick Scale (MMS) preoperatively, postoperatively, and at follow-up.

RESULTS

Preoperatively, 89 patients were functionally independent (MMS grade I or II). A GTR was achieved in 89 patients, 10 patients had a stable residual, and 1 patient underwent reoperation for tumor progression. At a mean follow-up of 65.4 months, 82 patients were functionally independent, and 11 lost their functional independence after surgery (MMS grades III–V). Muscle MEP loss predicted short-term postoperative worsening (p < 0.0001) only, while the strongest predictors of a good functional long-term outcome were lower preoperative MMS grades (p < 0.0001) and D-wave preservation. D-wave monitorability was 67%; it was higher with lower preoperative MMS grades and predicted a better recovery (p = 0.01).

CONCLUSIONS

In this large series of ISCEs, a high rate of GTR and long-term favorable functional outcome were achieved. Short- and long-term functional outcomes were best reflected by mMEPs and D-wave monitoring, respectively.

ABBREVIATIONS

CST = corticospinal tract; GTR = gross-total resection; IONM = intraoperative neurophysiological monitoring; ISCE = intramedullary spinal cord ependymoma; ISCT = intramedullary spinal cord tumor; mMEP = muscle motor evoked potential; MMS = modified McCormick Scale; SSEP = somatosensory evoked potential; STR = subtotal resection.

Supplementary Materials

    • Supplementary Table 1 (PDF 403 KB)

Illustration from Lee et al. (pp 822–829). Copyright Sun Joo Kim. Published with permission.

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  • 1

    Kothbauer KF, Deletis V, Epstein FJ. Motor-evoked potential monitoring for intramedullary spinal cord tumor surgery: correlation of clinical and neurophysiological data in a series of 100 consecutive procedures. Neurosurg Focus. 1998;4(5):e1.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Morota N, Deletis V, Constantini S, Kofler M, Cohen H, Epstein FJ. The role of motor evoked potentials during surgery for intramedullary spinal cord tumors. Neurosurgery. 1997;41(6):13271336.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Hadley MN, Shank CD, Rozzelle CJ, Walters BC. In reply: Guidelines for the use of electrophysiological monitoring for surgery of the human spinal column and spinal cord. Neurosurgery. 2018;83(2):E76E77.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Sweeney KJ, Reynolds M, Farrell M, Bolger C. Gross total resection rates of grade II/III intramedullary ependymomas using the surgical strategy of en-bloc resection without intra-operative neurophysiological monitoring. Br J Neurosurg. 2017;31(3):364368.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    McCormick PC, Torres R, Post KD, Stein BM. Intramedullary ependymoma of the spinal cord. J Neurosurg. 1990;72(4):523532.

  • 6

    Sala F, Palandri G, Basso E, Lanteri P, Deletis V, Faccioli F, Bricolo A. Motor evoked potential monitoring improves outcome after surgery for intramedullary spinal cord tumors: a historical control study. Neurosurgery. 2006;58(6):11291143.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Aghakhani N, David P, Parker F, Lacroix C, Benoudiba F, Tadie M. Intramedullary spinal ependymomas: analysis of a consecutive series of 82 adult cases with particular attention to patients with no preoperative neurological deficit. Neurosurgery. 2008;62(6):12791286.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Cannizzaro D, Mancarella C, Nasi D, Tropeano MP, Anania CD, Cataletti G, et al. Intramedullary spinal cord tumors: the value of intraoperative neurophysiological monitoring in a series of 57 cases from two Italian centres. J Neurosurg Sci. Published online September 23, 2019. doi:10.23736/S0390-5616.19.04758-1

    • Search Google Scholar
    • Export Citation
  • 9

    Choi I, Hyun SJ, Kang JK, Rhim SC. Combined muscle motor and somatosensory evoked potentials for intramedullary spinal cord tumour surgery. Yonsei Med J. 2014;55(4):10631071.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Ge X, Wu Z, Zhang J, Zhang L. Surgical strategies and functional outcome of intramedullary cervicomedullary ependymoma. Turk Neurosurg. 2017;27(4):563572.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Nakanishi Y, Naito K, Yamagata T, Takami T. Health-related quality of life after microscopic total removal of spinal intramedullary ependymomas in a single-institute 3-year prospective study. World Neurosurg. 2020;136:e614e624.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Abdullah KG, Lubelski D, Miller J, Steinmetz MP, Shin JH, Krishnaney A, et al. Progression free survival and functional outcome after surgical resection of intramedullary ependymomas. J Clin Neurosci. 2015;22(12):19331937.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Arima H, Naito K, Yamagata T, Kawahara S, Ohata K, Takami T. Quantitative analysis of near-infrared indocyanine green videoangiography for predicting functional outcomes after spinal intramedullary ependymoma resection. Oper Neurosurg (Hagerstown). 2019;17(5):531539.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Dauleac C, Messerer R, Obadia-Andre N, Afathi M, Barrey CY. Cysts associated with intramedullary ependymomas of the spinal cord: clinical, MRI and oncological features. J Neurooncol. 2019;144(2):385391.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Inoue T, Endo T, Nagamatsu K, Watanabe M, Tominaga T. 5-Aminolevulinic acid fluorescence-guided resection of intramedullary ependymoma: report of 9 cases. Neurosurgery. 2013;72(2)(Suppl Operative):ons159ons168.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Katsigiannis S, Carolus AE, Schmieder K, Brenke C. Posterolateral myelotomy for intramedullary spinal cord tumors: the other way to do it? Acta Neurochir (Wien). 2020;162(1):101107.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Kobayashi K, Ando K, Kato F, Kanemura T, Sato K, Kamiya M, et al. Surgical outcomes of spinal cord and cauda equina ependymoma: postoperative motor status and recurrence for each WHO grade in a multicenter study. J Orthop Sci. 2018;23(4):614621.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Lee SH, Chung CK, Kim CH, Yoon SH, Hyun SJ, Kim KJ, et al. Long-term outcomes of surgical resection with or without adjuvant radiation therapy for treatment of spinal ependymoma: a retrospective multicenter study by the Korea Spinal Oncology Research Group. Neuro Oncol. 2013;15(7):921929.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Li D, Hao SY, Wu Z, Jia GJ, Zhang LW, Zhang JT. Intramedullary medullocervical ependymoma—surgical treatment, functional recovery, and long-term outcome. Neurol Med Chir (Tokyo). 2013;53(10):663675.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Matsuyama Y, Sakai Y, Katayama Y, Imagama S, Ito Z, Wakao N, et al. Surgical results of intramedullary spinal cord tumor with spinal cord monitoring to guide extent of resection. J Neurosurg Spine. 2009;10(5):404413.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Park JH, Lee SH, Kim ES, Eoh W. Analysis of multimodal intraoperative monitoring during intramedullary spinal ependymoma surgery. World Neurosurg. 2018;120:e169e180.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Svoboda N, Bradac O, de Lacy P, Benes V. Intramedullary ependymoma: long-term outcome after surgery. Acta Neurochir (Wien). 2018;160(3):439447.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Takami T, Naito K, Yamagata T, Ohata K. Surgical management of spinal intramedullary tumors: radical and safe strategy for benign tumors. Neurol Med Chir (Tokyo). 2015;55(4):317327.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Joaquim AF, Dos Santos MJ, Tedeschi H, dos Santos MJ, Tedeschi H. Surgical management of intramedullary spinal ependymomas. Arq Neuropsiquiatr. 2009;67(2 A):284289.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Alkhani A, Blooshi M, Hassounah M. Outcome of surgery for intramedullary spinal ependymoma. Ann Saudi Med. 2008;28(2):109113.

  • 26

    Kaner T, Sasani M, Oktenoglu T, Solmaz B, Sarloglu AC, Ozer AF. Clinical analysis of 21 cases of spinal cord ependymoma: positive clinical results of gross total resection. J Korean Neurosurg Soc. 2010;47(2):102106.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Kucia EJ, Bambakidis NC, Chang SW, Spetzler RF. Surgical technique and outcomes in the treatment of spinal cord ependymomas, part 1: intramedullary ependymomas. Neurosurgery. 2011;68(1 Suppl Operative):5763.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Mohammed W, Farrell M, Bolger C. Spinal cord ependymoma—surgical management and outcome. J Neurosci Rural Pract. 2019;10(2):316320.

  • 29

    Prokopienko M, Kunert P, Podgórska A, Marchel A. Surgical treatment of intramedullary ependymomas. Neurol Neurochir Pol. 2017;51(6):439445.

  • 30

    Behmanesh B, Gessler F, Quick-Weller J, Spyrantis A, Imöhl L, Seifert V, Marquardt G. Regional spinal cord atrophy is associated with poor outcome after surgery on intramedullary spinal cord ependymoma: a new aspect of delayed neurological deterioration. World Neurosurg. 2017;100:250255.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Behmanesh B, Gessler F, Won SY, Dubinski D, Quick-Weller J, Imoehl L, et al. Return to work and clinical outcome after surgical treatment and conservative management of patients with intramedullary spinal cord ependymoma. Sci Rep. 2020;10(1):2335.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Huang YHH, Lin JWW. Management and outcome of primary spinal ependymomas: a single center experience from Taiwan. Clin Neurol Neurosurg. 2013;115(10):21302135.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Peker S, Ozgen S, Ozek MM, Pamir MN. Surgical treatment of intramedullary spinal cord ependymomas: can outcome be predicted by tumor parameters? J Spinal Disord Tech. 2004;17(6):516521.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Klekamp J. Spinal ependymomas. Part 1: Intramedullary ependymomas. Neurosurg Focus. 2015;39(2):E6.

  • 35

    Brotchi J, Fischer G. Spinal cord ependymomas. Neurosurg Focus. 1998;4(5):e2.

  • 36

    Klekamp J. Treatment of intramedullary tumors: analysis of surgical morbidity and long-term results. J Neurosurg Spine. 2013;19(1):1226.

  • 37

    Kobayashi K, Ando K, Ito K, Tsushima M, Morozumi M, Tanaka S, et al. Accuracy of intraoperative pathological diagnosis using frozen sections of spinal cord lesions. Clin Neurol Neurosurg. 2018;167:117121.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Lin YH, Huang CI, Wong TT, Chen MH, Shiau CY, Wang LW, et al. Treatment of spinal cord ependymomas by surgery with or without postoperative radiotherapy. J Neurooncol. 2005;71(2):205210.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39

    Chamberlain MC. Salvage chemotherapy for recurrent spinal cord ependymona. Cancer. 2002;95(5):9971002.

  • 40

    Yanni DS, Ulkatan S, Deletis V, Barrenechea IJ, Sen C, Perin NI. Utility of neurophysiological monitoring using dorsal column mapping in intramedullary spinal cord surgery. J Neurosurg Spine. 2010;12(6):623628.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Calancie B. Intraoperative Neuromonitoring and alarm criteria for judging MEP responses to transcranial electric stimulation: the threshold-level method. J Clin Neurophysiol. 2017;34(1):1221.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Quiñones-Hinojosa A, Lyon R, Zada G, Lamborn KR, Gupta N, Parsa AT, et al. Changes in transcranial motor evoked potentials during intramedullary spinal cord tumor resection correlate with postoperative motor function. Neurosurgery. 2005;56(5):982993.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Sala F, Skinner SA, Arle JE, Constantini S, Deletis V, Kothbauer KF, et al. Letter: Guidelines for the use of electrophysiological monitoring for surgery of the human spinal column and spinal cord. Neurosurgery. 2018;83(2):E82E84.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Vogel R, Balzer J, Gertsch J, Holdefer RN, Lee GR, Moreira JJ, et al. Letter: Guidelines for the use of electrophysiological monitoring for surgery of the human spinal column and spinal cord. Neurosurgery. 2018;82(6):E190E191.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Yarascavitch BA, Chuback JE, Almenawer SA, Reddy K, Bhandari M. Levels of evidence in the neurosurgical literature: more tribulations than trials. Neurosurgery. 2012;71(6):11311138.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    Rijs K, Klimek M, Scheltens-de Boer M, Biesheuvel K, Harhangi BS. Intraoperative neuromonitoring in patients with intramedullary spinal cord tumor: a systematic review, meta-analysis, and case series. World Neurosurg.2019;125:498510.e2.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47

    Daniel JW, Botelho RV, Milano JB, Dantas FR, Onishi FJ, Neto ER, et al. Intraoperative neurophysiological monitoring in spine surgery: a systematic review and meta-analysis. Spine (Phila Pa 1976).2018;43(16):11541160.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 48

    Verla T, Fridley JS, Khan AB, Mayer RR, Omeis I. Neuromonitoring for intramedullary spinal cord tumor surgery. World Neurosurg. 2016;95:108116.

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