Surgical outcomes and natural history of intramedullary spinal cord cavernous malformations: a single-center series and meta-analysis of individual patient data

Clinical article

View More View Less
  • 1 Division of Neurosurgery, Department of Surgery, and
  • | 2 Department of Clinical Epidemiology and Biostatistics, McMaster University, Hamilton, Ontario, Canada
Restricted access

Purchase Now

USD  $45.00

Spine - 1 year subscription bundle (Individuals Only)

USD  $376.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $612.00
USD  $45.00
USD  $376.00
USD  $612.00
Print or Print + Online Sign in

Object

Information pertaining to the natural history of intramedullary spinal cord cavernous malformations (ISCCMs) and patient outcomes after surgery is scarce. To evaluate factors associated with favorable outcomes for patients with surgically and conservatively managed ISCCMs, the authors performed a systematic review and metaanalysis of the literature. In addition, they included their single-center series of ISCCMs.

Methods

The authors searched MEDLINE, EMBASE, CINAHL, Google Scholar, and The Cochrane Library for studies published through June 2013 that reported cases of ISCCMs. Data from all eligible studies were used to examine the epidemiology, clinical features, and neurological outcomes of patients with surgically managed and conservatively treated ISCCMs. To evaluate several variables as predictors of favorable neurological outcomes, the authors conducted a meta-analysis of individual patient data and performed univariate and multivariate logistic regression analyses. Variables included patient age, patient sex, lesion spinal level, lesion size, cerebral cavernomas, family history of cavernous malformations, clinical course, presenting symptoms, treatment strategy (operative or conservative), symptom duration, surgical approach, spinal location, and extent of resection. In addition, they performed a meta-analysis to determine a pooled estimate of the annual hemorrhage rate of ISCCMs.

Results

Eligibility criteria were met by 40 studies, totaling 632 patients, including the authors' institutional series of 24 patients. Mean patient age was 39.1 years (range 2–80 years), and the male-to-female ratio was 1.1:1. Spinal levels of cavernomas were cervical (38%), cervicothoracic (2.4%), thoracic (55.2%), thoracolumbar (0.6%), lumbar (2.1%), and conus medullaris (1.7%). Average cavernoma size was 9.2 mm. Associated cerebral cavernomas occurred in 16.5% of patients, and a family history of cavernous malformation was found for 11.9% of evaluated patients. Clinical course was acute with stepwise progression for 45.4% of patients and slowly progressive for 54.6%. Symptoms were motor (60.5%), sensory (57.8%), pain (33.8%), bladder and/or bowel (23.6%), respiratory distress (0.5%), or absent (asymptomatic; 0.9%). The calculated pooled annual rate of hemorrhage was 2.1% (95% CI 1.3%–3.3%). Most (89.9%) patients underwent resection, and 10.1% underwent conservative management (observation). Outcomes were better for those who underwent resection than for those who underwent conservative management (OR 2.79, 95% CI 1.46–5.33, p = 0.002). A positive correlation with improved neurological outcomes was found for resection within 3 months of symptom onset (OR 2.11, 95% CI 1.31–3.41, p = 0.002), hemilaminectomy approach (OR 3.20, 95% CI 1.16–8.86, p = 0.03), and gross-total resection (OR 3.61, 95% CI 1.24–10.52, p = 0.02). Better outcomes were predicted by an acute clinical course (OR 1.72, 95% CI 1.10–2.68, p = 0.02) and motor symptoms (OR 1.76, 95% CI 1.08–2.86, p = 0.02); poor neurological recovery was predicted by sensory symptoms (OR 0.58, 95% CI 0.35–0.98, p = 0.04). Rates of neurological improvement after resection were no higher for patients with superficial ISCCMs than for those with deep-seated ISCCMs (OR 1.36, 95% CI 0.71–2.60, p = 0.36).

Conclusions

Intramedullary spinal cord cavernous malformations tend to be clinically progressive. The authors' findings support an operative management plan for patients with a symptomatic ISCCM. Surgical goals include gross-total resection through a more minimally invasive hemilaminectomy approach within 3 months of presentation.

Abbreviation used in this paper:

ISCCM = intramedullary spinal cord cavernous malformation.

Spine - 1 year subscription bundle (Individuals Only)

USD  $376.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $612.00
USD  $376.00
USD  $612.00
  • 1

    Aoyama T, , Hida K, & Houkin K: Intramedullary cavernous angiomas of the spinal cord: clinical characteristics of 13 lesions. Neurol Med Chir (Tokyo) 51:561566, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Babu R, , Owens TR, , Karikari IO, , Moreno J, , Cummings TJ, & Gottfried ON, et al.: Spinal cavernous and capillary hemangiomas in adults. Spine (Phila Pa 1976) 38:E423E430, 2013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3

    Balak N: Unilateral partial hemilaminectomy in the removal of a large spinal ependymoma. Spine J 8:10301036, 2008

  • 4

    Begg CB, & Mazumdar M: Operating characteristics of a rank correlation test for publication bias. Biometrics 50:10881101, 1994

  • 5

    Bian LG, , Bertalanffy H, , Sun QF, & Shen JK: Intramedullary cavernous malformations: clinical features and surgical technique via hemilaminectomy. Clin Neurol Neurosurg 111:511517, 2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Bozinov O, , Burkhardt JK, , Woernle CM, , Hagel V, , Ulrich NH, & Krayenbühl N, et al.: Intra-operative high frequency ultrasound improves surgery of intramedullary cavernous malformations. Neurosurg Rev 35:269275, 2012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Canavero S, , Pagni CA, , Duca S, & Bradac GB: Spinal intramedullary cavernous angiomas: a literature meta-analysis. Surg Neurol 41:381388, 1994

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Cansever T, , Civelek E, , Sencer A, , Karasu A, , Kiriş T, & Hepgül K, et al.: Spinal cavernous malformations: a report of 5 cases. Surg Neurol 69:602607, 2008

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Cantore G, , Delfini R, , Cervoni L, , Innocenzi G, & Orlando ER: Intramedullary cavernous angiomas of the spinal cord: report of six cases. Surg Neurol 43:448452, 1995

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Cantu C, , Murillo-Bonilla L, , Arauz A, , Higuera J, , Padilla J, & Barinagarrementeria F: Predictive factors for intracerebral hemorrhage in patients with cavernous angiomas. Neurol Res 27:314318, 2005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Chabert E, , Morandi X, , Carney MP, , Riffaud L, , Louail C, & Carsin-Nicol B: Intramedullary cavernous malformations. J Neuroradiol 26:262268, 1999

    • Search Google Scholar
    • Export Citation
  • 12

    Choi GH, , Kim KN, , Lee S, , Ji GY, , Oh JK, & Kim TY, et al.: The clinical features and surgical outcomes of patients with intramedullary spinal cord cavernous malformations. Acta Neurochir (Wien) 153:16771685, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Clatterbuck RE, , Eberhart CG, , Crain BJ, & Rigamonti D: Ultrastructural and immunocytochemical evidence that an incompetent blood-brain barrier is related to the pathophysiology of cavernous malformations. J Neurol Neurosurg Psychiatry 71:188192, 2001

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Cosgrove GR, , Bertrand G, , Fontaine S, , Robitaille Y, & Melanson D: Cavernous angiomas of the spinal cord. J Neurosurg 68:3136, 1988

  • 15

    Cristante L, & Hermann HD: Radical excision of intramedullary cavernous angiomas. Neurosurgery 43:424431, 1998

  • 16

    Del Curling O Jr, , Kelly DL Jr, , Elster AD, & Craven TE: An analysis of the natural history of cavernous angiomas. J Neurosurg 75:702708, 1991

  • 17

    Deutsch H: Pain outcomes after surgery in patients with intramedullary spinal cord cavernous malformations. Neurosurg Focus 29:3 E15, 2010

  • 18

    Egger M, , Davey Smith G, , Schneider M, & Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629634, 1997

  • 19

    Eicker S, , Szelényi A, , Mathhys C, , Steiger HJ, & Hänggi D: Custom-tailored minimally invasive partial C2-corpectomy to a ventrally located intramedullary cavernous malformation. Eur Spine J 21:2385, 2012. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 20

    Endo T, , Aizawa-Kohama M, , Nagamatsu K, , Murakami K, , Takahashi A, & Tominaga T: Use of microscope-integrated near-infrared indocyanine green videoangiography in the surgical treatment of intramedullary cavernous malformations: report of 8 cases. Clinical article. J Neurosurg Spine 18:443449, 2013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Furuya K, , Sasaki T, , Suzuki I, , Kim P, , Saito N, & Kirino T: Intramedullary angiographically occult vascular malformations of the spinal cord. Neurosurgery 39:11231132, 1996

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Ghogawala Z, & Ogilvy CS: Intramedullary cavernous malformations of the spinal cord. Neurosurg Clin N Am 10:101111, 1999

  • 23

    Gordon CR, , Crockard HA, & Symon L: Surgical management of spinal cord cavernoma. Br J Neurosurg 9:459464, 1995

  • 24

    Gross BA, , Du R, , Popp AJ, & Day AL: Intramedullary spinal cord cavernous malformations. Neurosurg Focus 29:3 E14, 2010

  • 25

    Gross BA, , Lin N, , Du R, & Day AL: The natural history of intracranial cavernous malformations. Neurosurg Focus 30:6 E24, 2011

  • 26

    Hadlich R: Ein Fall von Tumor cavernosus des Rückenmarks mit besonderer Berücksichtigung der neueren Theorien Über die Gene des Cavernoms. Virchows Arch 172:429441, 1903

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Hegde A, , Mohan S, , Tan KK, & Lim CC: Spinal cavernous malformations: magnetic resonance imaging and associated findings. Singapore Med J 53:582586, 2012

    • Search Google Scholar
    • Export Citation
  • 28

    Jallo GI, , Freed D, , Zareck M, , Epstein F, & Kothbauer KF: Clinical presentation and optimal management for intramedullary cavernous malformations. Neurosurg Focus 21:1 E10, 2006

    • Search Google Scholar
    • Export Citation
  • 29

    Jellinger K, Pathology of spinal vascular malformations and vascular tumors. Pia H, & Djindjian R: Spinal Angiomas: Advances in Diagnosis and Therapy New York, Springer, 1978. 1320

    • Search Google Scholar
    • Export Citation
  • 30

    Kharkar S, , Shuck J, , Conway J, & Rigamonti D: The natural history of conservatively managed symptomatic intramedullary spinal cord cavernomas. Neurosurgery 60:865872, 2007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    Kim DS, , Park YG, , Choi JU, , Chung SS, & Lee KC: An analysis of the natural history of cavernous malformations. Surg Neurol 48:918, 1997

  • 32

    Kim KM, , Chung CK, , Huh W, , Lee WJ, , Park SB, & Kim CH, et al.: Clinical outcomes of conservative management of spinal cord cavernous angiomas. Acta Neurochir (Wien) 155:12091214, 2013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33

    Kivelev J, , Laakso A, , Niemelä M, & Hernesniemi J: A proposed grading system of brain and spinal cavernomas. Neurosurgery 69:807814, 2011

  • 34

    Kivelev J, , Niemelä M, & Hernesniemi J: Outcome after microsurgery in 14 patients with spinal cavernomas and review of the literature. Clinical article. J Neurosurg Spine 13:524534, 2010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35

    Labauge P, , Bouly S, , Parker F, , Gallas S, , Emery E, & Loiseau H, et al.: Outcome in 53 patients with spinal cord cavernomas. Surg Neurol 70:176181, 2008

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36

    Liang JT, , Bao YH, , Zhang HQ, , Huo LR, , Wang ZY, & Ling F: Management and prognosis of symptomatic patients with intramedullary spinal cord cavernoma. Clinical article. J Neurosurg Spine 15:447456, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37

    Lu DC, & Lawton MT: Clinical presentation and surgical management of intramedullary spinal cord cavernous malformations. Neurosurg Focus 29:3 E12, 2010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38

    Lunardi P, , Acqui M, , Ferrante L, & Fortuna A: The role of intraoperative ultrasound imaging in the surgical removal of intramedullary cavernous angiomas. Neurosurgery 34:520523, 1994

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39

    Maslehaty H, , Barth H, , Petridis AK, , Doukas A, & Mehdorn HM: Symptomatic spinal cavernous malformations: indication for microsurgical treatment and outcome. Eur Spine J 20:17651770, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40

    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. Clinical article. J Neurosurg Spine 10:404413, 2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41

    McCormick PC, , Michelsen WJ, , Post KD, , Carmel PW, & Stein BM: Cavernous malformations of the spinal cord. Neurosurgery 23:459463, 1988

  • 42

    Mitha AP, , Turner JD, , Abla AA, , Vishteh AG, & Spetzler RF: Outcomes following resection of intramedullary spinal cord cavernous malformations: a 25-year experience. Clinical article. J Neurosurg Spine 14:605611, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43

    Mitha AP, , Turner JD, & Spetzler RF: Surgical approaches to intramedullary cavernous malformations of the spinal cord. Neurosurgery 68:2 Suppl Operative 317324, 2011

    • Search Google Scholar
    • Export Citation
  • 44

    Moher D, , Liberati A, , Tetzlaff J, & Altman DG: Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 62:10061012, 2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45

    Nishikawa M, , Ohata K, , Ishibashi K, , Takami T, , Goto T, & Hara M: The anterolateral partial vertebrectomy approach for ventrally located cervical intramedullary cavernous angiomas. Neurosurgery 59:1 Suppl 1 ONS58ONS63, 2006

    • Search Google Scholar
    • Export Citation
  • 46

    Odom GL, , Woodhall B, & Margolis G: Spontaneous hematomyelia and angiomas of the spinal cord. J Neurosurg 14:192202, 1957

  • 47

    Ogilvy CS, , Louis DN, & Ojemann RG: Intramedullary cavernous angiomas of the spinal cord: clinical presentation, pathological features, and surgical management. Neurosurgery 31:219230, 1992

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 48

    Otten P, , Pizzolato GP, , Rilliet B, & Berney J: [131 cases of cavernous angioma (cavernomas) of the CNS, discovered by retrospective analysis of 24,535 autopsies.]. Neurochirurgie 35:8283, 1989. (Fr)

    • Search Google Scholar
    • Export Citation
  • 49

    Padovani R, , Acciarri N, , Giulioni M, , Pantieri R, & Foschini MP: Cavernous angiomas of the spinal district: surgical treatment of 11 patients. Eur Spine J 6:298303, 1997

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 50

    Park SB, , Jahng TA, & Chung CK: The clinical outcomes after complete surgical resection of intramedullary cavernous angiomas: changes in motor and sensory symptoms. Spinal Cord 47:128133, 2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 51

    Perrini P, , Er U, , Spetzler RF, & Lanzino G, Cavernous malformations of the spinal cord. Lanzino G, & Spetzler RF: Cavernous Malformations of the Brain and Spinal Cord New York, Thieme, 2007. 8893

    • Search Google Scholar
    • Export Citation
  • 52

    Robinson JR, , Awad IA, & Little JR: Natural history of the cavernous angioma. J Neurosurg 75:709714, 1991

  • 53

    Sandalcioglu IE, , Wiedemayer H, , Gasser T, , Asgari S, , Engelhorn T, & Stolke D: Intramedullary spinal cord cavernous malformations: clinical features and risk of hemorrhage. Neurosurg Rev 26:253256, 2003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 54

    Santoro A, , Piccirilli M, , Frati A, , Salvati M, , Innocenzi G, & Ricci G, et al.: Intramedullary spinal cord cavernous malformations: report of ten new cases. Neurosurg Rev 27:9398, 2004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 55

    Sario-glu AC, , Hanci M, , Bozkuş H, , Kaynar MY, & Kafadar A: Unilateral hemilaminectomy for the removal of the spinal space-occupying lesions. Minim Invasive Neurosurg 40:7477, 1997

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 56

    Sarwar M, & McCormick WF: Intracerebral venous angioma. Case report and review. Arch Neurol 35:323325, 1978

  • 57

    Schultze F: Weiterer Beitrag zur Diagnose und operativen Behandlung von Geschwulsten der Ruckenmarkshaute und des Ruckenmarks: Erfolgreiche Operation eines intramedullaren Tumors. Dtsch Med Wochenschr 38:16761679, 1912

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 58

    Spetzger U, , Gilsbach JM, & Bertalanffy H: Cavernous angiomas of the spinal cord clinical presentation, surgical strategy, and postoperative results. Acta Neurochir (Wien) 134:200206, 1995

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 59

    Steiger HJ, , Turowski B, & Hänggi D: Prognostic factors for the outcome of surgical and conservative treatment of symptomatic spinal cord cavernous malformations: a review of a series of 20 patients. Neurosurg Focus 29:3 E13, 2010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 60

    Stroup DF, , Berlin JA, , Morton SC, , Olkin I, , Williamson GD, & Rennie D, et al.: Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 283:20082012, 2000

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 61

    Sun CX, , Meng XL, , Xie SN, , Yu Y, , Yang HJ, & Wu B: Unilateral hemilaminectomy for patients with intradural extramedullary tumors. J Zhejiang Univ Sci B 12:575581, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 62

    Tong X, , Deng X, , Li H, , Fu Z, & Xu Y: Clinical presentation and surgical outcome of intramedullary spinal cord cavernous malformations. Clinical article. J Neurosurg Spine 16:308314, 2012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 63

    Tu YK, , Liu HM, , Chen SJ, & Lin SM: Intramedullary cavernous haemangiomas: clinical features, imaging diagnosis, surgical resection and outcome. J Clin Neurosci 6:212216, 1999

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 64

    Turjman F, , Joly D, , Monnet O, , Faure C, , Doyon D, & Froment JC: MRI of intramedullary cavernous haemangiomas. Neuroradiology 37:297302, 1995

  • 65

    Vishteh AG, , Sankhla S, , Anson JA, , Zabramski JM, & Spetzler RF: Surgical resection of intramedullary spinal cord cavernous malformations: delayed complications, long-term outcomes, and association with cryptic venous malformations. Neurosurgery 41:10941101, 1997

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 66

    Voigt K, & Yaşargil MG: Cerebral cavernous haemangiomas or cavernomas. Incidence, pathology, localization, diagnosis, clinical features and treatment. Review of the literature and report of an unusual case. Neurochirurgia (Stuttg) 19:5968, 1976

    • Search Google Scholar
    • Export Citation
  • 67

    Wachter D, , Psychogios M, , Gilsbach JM, & Rohde V: Spinal cord cavernoma–operative strategy and results in 30 patients. J Neurol Surg A Cent Eur Neurosurg 73:125131, 2012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 68

    Weinzierl MR, , Krings T, , Korinth MC, , Reinges MH, & Gilsbach JM: MRI and intraoperative findings in cavernous haemangiomas of the spinal cord. Neuroradiology 46:6571, 2004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 69

    Wells GA, , Shea B, , O'Connell D, , Peterson J, , Welch V, & Losos M, et al.: The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa Hospital Research Institute (http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp)[Accessed June 12, 2014]

    • Search Google Scholar
    • Export Citation
  • 70

    Wong JH, , Awad IA, & Kim JH: Ultrastructural pathological features of cerebrovascular malformations: a preliminary report. Neurosurgery 46:14541459, 2000

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 71

    Wood MW, , White RJ, & Kernohan JW: Cavernous hemangiomatosis involving the brain, spinal cord, heart, skin and kidney: report of case. Proc Staff Meet Mayo Clin 32:249254, 1957

    • Search Google Scholar
    • Export Citation
  • 72

    Yu Y, , Zhang X, , Hu F, , Xie T, & Gu Y: Minimally invasive microsurgical treatment of cervical intraspinal extramedullary tumors. J Clin Neurosci 18:11681173, 2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 73

    Zevgaridis D, , Medele RJ, , Hamburger C, , Steiger HJ, & Reulen HJ: Cavernous haemangiomas of the spinal cord. A review of 117 cases. Acta Neurochir (Wien) 141:237245, 1999

    • Crossref
    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 1341 441 49
Full Text Views 773 90 24
PDF Downloads 629 104 21
EPUB Downloads 0 0 0