Hemorrhage risk, surgical management, and functional outcome of brainstem cavernous malformations

Clinical article

Da Li M.D. 1 , Yang Yang M.D. 1 , Shu-Yu Hao M.D., Ph.D. 1 , 2 , Liang Wang M.D. 1 , Jie Tang M.D., Ph.D. 1 , Xin-Ru Xiao M.D., Ph.D. 1 , Hui Zhou M.D. 3 , Gui-Jun Jia M.D., Ph.D. 1 , Zhen Wu M.D. 1 , Li-Wei Zhang M.D., Ph.D. 1 , 2 , and Jun-Ting Zhang M.D. 1
View More View Less
  • 1 Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing;
  • 2 Beijing Neurosurgical Institute, Beijing; and
  • 3 Department of Neurosurgery, Lianyungang Hospital, Xuzhou Medical College, Jiangsu, People's Republic of China
Restricted access

Purchase Now

USD  $45.00

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

USD  $505.00

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

USD  $600.00
Print or Print + Online

Object

The aim of this study was to evaluate the pre- and postoperative rehemorrhage risk, neurological function outcome, and prognostic factors of surgically treated brainstem cavernous malformations (CMs) with long-term follow-up.

Methods

The authors conducted a retrospective review of the clinical data from 242 patients with brainstem CMs that were surgically treated between 1999 and 2010. Patient charts, imaging findings, and outcomes were examined.

Results

The study included 242 patients, with a male-to-female ratio of 1.3 and mean age of 32.6 years. The mean modified Rankin Scale scores on admission, at discharge, at 3 and 6 months after surgery, and at recent evaluation were 2.2, 2.6, 2.3, 1.8, and 1.5, respectively. The preoperative calculated annual hemorrhage and rehemorrhage rates were 5.0% and 60.9%, respectively. The complete resection rate was 95%. Surgical morbidity occurred in 112 patients (46.3%). Eighty-five patients (35.1%) demonstrated worsened condition immediately after surgery; 34 (41.0%) and 51 (61.4%) of these patients recovered to their baseline level within 3 and 6 months after surgery, respectively. At a mean follow-up of 89.4 months, the patients' condition had improved in 147 cases (60.7%), was unchanged in 70 cases (28.9%), and had worsened in 25 cases (10.3%). A total of 8 hemorrhages occurred in 6 patients, and the postoperative annual hemorrhage rate was 0.4%. Permanent morbidity remained in 65 patients (26.9%). The adverse factors for preoperative rehemorrhage were age ≥ 50 years, size ≥ 2 cm, and perilesional edema. The risk factors for postoperative hemorrhage were developmental venous anomaly and incomplete resection. The independent adverse factors for long-term outcome were increased age, multiple hemorrhages, ventral-seated lesions, and poor preoperative status. Favorable, complete improvement in the postoperative deficits over time was correlated with good preoperative neurological function and continuing improvement thereafter.

Conclusions

Favorable long-term outcomes and significantly low postoperative annual hemorrhage rates were achieved via surgery. Total resection should be attempted with an aim of minimal injury to neurological function; however, postoperative deficits can improve during the postoperative course. Close follow-up with radiological examination is proposed for patients with adverse factors predictive of rehemorrhage.

Abbreviations used in this paper:CM = cavernous malformation; CN = cranial nerve; DVA = developmental venous anomaly; EMST = estimated mean survival time; mRS = modified Rankin Scale.

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

USD  $505.00

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

USD  $600.00

Contributor Notes

Address correspondence to: Jun-Ting Zhang, M.D., Tiantan Xili 6, Chongwen District, Beijing 100050, People's Republic of China. email: zhangjunting2003@yahoo.com.cn.

Please include this information when citing this paper: published online August 16, 2013; DOI: 10.3171/2013.7.JNS13462.

  • 1

    Abdulrauf SI, , Kaynar MY, & Awad IA: A comparison of the clinical profile of cavernous malformations with and without associated venous malformations. Neurosurgery 44:4147, 1999

    • Search Google Scholar
    • Export Citation
  • 2

    Abla A, , Wait SD, , Uschold T, , Lekovic GP, & Spetzler RF: Developmental venous anomaly, cavernous malformation, and capillary telangiectasia: spectrum of a single disease. Acta Neurochir (Wien) 150:487489, 2008

    • Search Google Scholar
    • Export Citation
  • 3

    Abla AA, , Lekovic GP, , Garrett M, , Wilson DA, , Nakaji P, & Bristol R, : Cavernous malformations of the brainstem presenting in childhood: surgical experience in 40 patients. Neurosurgery 67:15891599, 2010

    • Search Google Scholar
    • Export Citation
  • 4

    Abla AA, , Lekovic GP, , Turner JD, , de Oliveira JG, , Porter R, & Spetzler RF: Advances in the treatment and outcome of brainstem cavernous malformation surgery: a single-center case series of 300 surgically treated patients. Neurosurgery 68:403415, 2011

    • Search Google Scholar
    • Export Citation
  • 5

    Abla AA, , Turner JD, , Mitha AP, , Lekovic G, & Spetzler RF: Surgical approaches to brainstem cavernous malformations. Neurosurg Focus 29:3 E8, 2010

    • Search Google Scholar
    • Export Citation
  • 6

    Aiba T, , Tanaka R, , Koike T, , Kameyama S, , Takeda N, & Komata T: Natural history of intracranial cavernous malformations. J Neurosurg 83:5659, 1995

    • Search Google Scholar
    • Export Citation
  • 7

    Al-Holou WN, , O'Lynnger TM, , Pandey AS, , Gemmete JJ, , Thompson BG, & Muraszko KM, : Natural history and imaging prevalence of cavernous malformations in children and young adults. Clinical article. J Neurosurg Pediatr 9:198205, 2012

    • Search Google Scholar
    • Export Citation
  • 8

    Al-Shahi Salman R, , Berg MJ, , Morrison L, & Awad IA: Hemorrhage from cavernous malformations of the brain: definition and reporting standards. Stroke 39:32223230, 2008

    • Search Google Scholar
    • Export Citation
  • 9

    Al-Shahi Salman R, , Hall JM, , Horne MA, , Moultrie F, , Josephson CB, & Bhattacharya JJ, : Untreated clinical course of cerebral cavernous malformations: a prospective, population-based cohort study. Lancet Neurol 11:217224, 2012

    • Search Google Scholar
    • Export Citation
  • 10

    Asaad WF, , Walcott BP, , Nahed BV, & Ogilvy CS: Operative management of brainstem cavernous malformations. Neurosurg Focus 29:3 E10, 2010

  • 11

    Awad IA, , Robinson JR Jr, , Mohanty S, & Estes ML: Mixed vascular malformations of the brain: clinical and pathogenetic considerations. Neurosurgery 33:179188, 1993

    • Search Google Scholar
    • Export Citation
  • 12

    Barker FG II, , Amin-Hanjani S, , Butler WE, , Lyons S, , Ojemann RG, & Chapman PH, : Temporal clustering of hemorrhages from untreated cavernous malformations of the central nervous system. Neurosurgery 49:1525, 2001

    • Search Google Scholar
    • Export Citation
  • 13

    Bozinov O, , Hatano T, , Sarnthein J, , Burkhardt JK, & Bertalanffy H: Current clinical management of brainstem cavernomas. Swiss Med Wkly 140:w13120, 2010

    • Search Google Scholar
    • Export Citation
  • 14

    Bruneau M, , Bijlenga P, , Reverdin A, , Rilliet B, , Regli L, & Villemure JG, : Early surgery for brainstem cavernomas. Acta Neurochir (Wien) 148:405414, 2006

    • Search Google Scholar
    • Export Citation
  • 15

    Cakirer S: De novo formation of a cavernous malformation of the brain in the presence of a developmental venous anomaly. Clin Radiol 58:251256, 2003

    • Search Google Scholar
    • Export Citation
  • 16

    Campeau NG, & Lane JI: De novo development of a lesion with the appearance of a cavernous malformation adjacent to an existing developmental venous anomaly. AJNR Am J Neuroradiol 26:156159, 2005

    • Search Google Scholar
    • Export Citation
  • 17

    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

    • Search Google Scholar
    • Export Citation
  • 18

    Cenzato M, , Stefini R, , Ambrosi C, & Giovanelli M: Post-operative remnants of brainstem cavernomas: incidence, risk factors and management. Acta Neurochir (Wien) 150:879887, 2008

    • Search Google Scholar
    • Export Citation
  • 19

    Chen L, , Zhao Y, , Zhou L, , Zhu W, , Pan Z, & Mao Y: Surgical strategies in treating brainstem cavernous malformations. Neurosurgery 68:609621, 2011

    • Search Google Scholar
    • Export Citation
  • 20

    Clatterbuck RE, , Elmací I, & Rigamonti D: The juxtaposition of a capillary telangiectasia, cavernous malformation, and developmental venous anomaly in the brainstem of a single patient: case report. Neurosurgery 49:12461250, 2001

    • Search Google Scholar
    • Export Citation
  • 21

    de Aguiar PH, , Zicarelli CA, , Isolan G, , Antunes A, , Aires R, & Georgeto SM, : Brainstem cavernomas: a surgical challenge. Einstein (Sao Paulo) 10:6773, 2012

    • Search Google Scholar
    • Export Citation
  • 22

    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

    • Search Google Scholar
    • Export Citation
  • 23

    Detwiler PW, , Porter RW, , Zabramski JM, & Spetzler RF: De novo formation of a central nervous system cavernous malformation: implications for predicting risk of hemorrhage. Case report and review of the literature. J Neurosurg 87:629632, 1997

    • Search Google Scholar
    • Export Citation
  • 24

    Dukatz T, , Sarnthein J, , Sitter H, , Bozinov O, , Benes L, & Sure U, : Quality of life after brainstem cavernoma surgery in 71 patients. Neurosurgery 69:689695, 2011

    • Search Google Scholar
    • Export Citation
  • 25

    Ferroli P, , Sinisi M, , Franzini A, , Giombini S, , Solero CL, & Broggi G: Brainstem cavernomas: long-term results of microsurgical resection in 52 patients. Neurosurgery 56:12031214, 2005

    • Search Google Scholar
    • Export Citation
  • 26

    Flemming KD, , Bovis GK, & Meyer FB: Aggressive course of multiple de novo cavernous malformations. Case report. J Neurosurg 115:11751178, 2011

    • Search Google Scholar
    • Export Citation
  • 27

    François P, , Ben Ismail M, , Hamel O, , Bataille B, , Jan M, & Velut S: Anterior transpetrosal and subtemporal transtentorial approaches for pontine cavernomas. Acta Neurochir (Wien) 152:13211329, 2010

    • Search Google Scholar
    • Export Citation
  • 28

    Fritschi JA, , Reulen HJ, , Spetzler RF, & Zabramski JM: Cavernous malformations of the brain stem. A review of 139 cases. Acta Neurochir (Wien) 130:3546, 1994

    • Search Google Scholar
    • Export Citation
  • 29

    Garrett M, & Spetzler RF: Surgical treatment of brainstem cavernous malformations. Surg Neurol 72:Suppl 2 S3S10, 2009

  • 30

    Giliberto G, , Lanzino DJ, , Diehn FE, , Factor D, , Flemming KD, & Lanzino G: Brainstem cavernous malformations: anatomical, clinical, and surgical considerations. Neurosurg Focus 29:3 E9, 2010

    • Search Google Scholar
    • Export Citation
  • 31

    Gross BA, , Batjer HH, , Awad IA, & Bendok BR: Brainstem cavernous malformations. Neurosurgery 64:E805E818, 2009

  • 32

    Gross BA, , Batjer HH, , Awad IA, , Bendok BR, & Du R: Brainstem cavernous malformations: 1390 surgical cases from the literature. World Neurosurg [epub ahead of print], 2013

    • Search Google Scholar
    • Export Citation
  • 33

    Gross BA, , Dunn IF, , Du R, & Al-Mefty O: Petrosal approaches to brainstem cavernous malformations. Neurosurg Focus 33:2 E10, 2012

  • 34

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

  • 35

    Hauck EF, , Barnett SL, , White JA, & Samson D: The presigmoid approach to anterolateral pontine cavernomas. Clinical article. J Neurosurg 113:701708, 2010

    • Search Google Scholar
    • Export Citation
  • 36

    Hauck EF, , Barnett SL, , White JA, & Samson D: Symptomatic brainstem cavernomas. Neurosurgery 64:6171, 2009

  • 37

    Huang AP, , Chen JS, , Yang CC, , Wang KC, , Yang SH, & Lai DM, : Brain stem cavernous malformations. J Clin Neurosci 17:7479, 2010

  • 38

    Ichinose T, , Goto T, , Morisako H, , Takami T, & Ohata K: Microroll retractor for surgical resection of brainstem cavernomas. World Neurosurg 73:520522, 2010

    • Search Google Scholar
    • Export Citation
  • 39

    Juan G, , Ramón M, , Ciscar MA, , García B, , Lloret T, & Cervelló MA, : [Acute respiratory insufficiency as initial manifestation of brain stem lesions.]. Arch Bronconeumol 35:560563, 1999. (Span)

    • Search Google Scholar
    • Export Citation
  • 40

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

  • 41

    Kondziolka D, , Lunsford LD, & Kestle JR: The natural history of cerebral cavernous malformations. J Neurosurg 83:820824, 1995

  • 42

    Kondziolka D, , Monaco EA III, & Lunsford LD: Cavernous malformations and hemorrhage risk. Prog Neurol Surg 27:141146, 2013

  • 43

    Kupersmith MJ, , Kalish H, , Epstein F, , Yu G, , Berenstein A, & Woo H, : Natural history of brainstem cavernous malformations. Neurosurgery 48:4754, 2001

    • Search Google Scholar
    • Export Citation
  • 44

    Labauge P, , Brunereau L, , Laberge S, & Houtteville JP: Prospective follow-up of 33 asymptomatic patients with familial cerebral cavernous malformations. Neurology 57:18251828, 2001

    • Search Google Scholar
    • Export Citation
  • 45

    Li H, , Ju Y, , Cai BW, , Chen J, , You C, & Hui XH: Experience of microsurgical treatment of brainstem cavernomas: report of 37 cases. Neurol India 57:269273, 2009

    • Search Google Scholar
    • Export Citation
  • 46

    Mai JC, , Ramanathan D, , Kim LJ, & Sekhar LN: Surgical resection of cavernous malformations of the brainstem: evolution of a minimally invasive technique. World Neurosurg 79:691703, 2013

    • Search Google Scholar
    • Export Citation
  • 47

    Maraire JN, & Awad IA: Intracranial cavernous malformations: lesion behavior and management strategies. Neurosurgery 37:591605, 1995

  • 48

    Mathiesen T, , Edner G, & Kihlström L: Deep and brainstem cavernomas: a consecutive 8-year series. J Neurosurg 99:3137, 2003

  • 49

    Menon G, , Gopalakrishnan CV, , Rao BR, , Nair S, , Sudhir J, & Sharma M: A single institution series of cavernomas of the brainstem. J Clin Neurosci 18:12101214, 2011

    • Search Google Scholar
    • Export Citation
  • 50

    Moriarity JL, , Clatterbuck RE, & Rigamonti D: The natural history of cavernous malformations. Neurosurg Clin N Am 10:411417, 1999

  • 51

    Moriarity JL, , Wetzel M, , Clatterbuck RE, , Javedan S, , Sheppard JM, & Hoenig-Rigamonti K, : The natural history of cavernous malformations: a prospective study of 68 patients. Neurosurgery 44:11661173, 1999

    • Search Google Scholar
    • Export Citation
  • 52

    Ohue S, , Fukushima T, , Friedman AH, , Kumon Y, & Ohnishi T: Retrosigmoid suprafloccular transhorizontal fissure approach for resection of brainstem cavernous malformation. Neurosurgery 66:6 Suppl Operative 306313, 2010

    • Search Google Scholar
    • Export Citation
  • 53

    Ohue S, , Fukushima T, , Kumon Y, , Ohnishi T, & Friedman AH: Surgical management of brainstem cavernomas: selection of approaches and microsurgical techniques. Neurosurg Rev 33:315324, 2010

    • Search Google Scholar
    • Export Citation
  • 54

    Pandey P, , Westbroek EM, , Gooderham PA, & Steinberg GK: Cavernous malformation of brainstem, thalamus and basal ganglia—a series of 176 patients. Clinical studies. Neurosurgery 72:573589, 2013

    • Search Google Scholar
    • Export Citation
  • 55

    Perrini P, & Lanzino G: The association of venous developmental anomalies and cavernous malformations: pathophysiological, diagnostic, and surgical considerations. Neurosurg Focus 21:1 e5, 2006

    • Search Google Scholar
    • Export Citation
  • 56

    Porter PJ, , Willinsky RA, , Harper W, & Wallace MC: Cerebral cavernous malformations: natural history and prognosis after clinical deterioration with or without hemorrhage. J Neurosurg 87:190197, 1997

    • Search Google Scholar
    • Export Citation
  • 57

    Porter RW, , Detwiler PW, , Spetzler RF, , Lawton MT, , Baskin JJ, & Derksen PT, : Cavernous malformations of the brainstem: experience with 100 patients. J Neurosurg 90:5058, 1999

    • Search Google Scholar
    • Export Citation
  • 58

    Pozzati E, , Acciarri N, , Tognetti F, , Marliani F, & Giangaspero F: Growth, subsequent bleeding, and de novo appearance of cerebral cavernous angiomas. Neurosurgery 38:662670, 1996

    • Search Google Scholar
    • Export Citation
  • 59

    Ramina R, , Mattei TA, , de Aguiar PH, , Meneses MS, , Ferraz VR, & Aires R, : Surgical management of brainstem cavernous malformations. Neurol Sci 32:10131028, 2011

    • Search Google Scholar
    • Export Citation
  • 60

    Rao GS, , Ramesh VJ, & Lalla RK: Ventilatory management and weaning in a patient with central hypoventilation caused by a brainstem cavernoma. Acta Anaesthesiol Scand 49:12141217, 2005

    • Search Google Scholar
    • Export Citation
  • 61

    Recalde RJ, , Figueiredo EG, & de Oliveira E: Microsurgical anatomy of the safe entry zones on the anterolateral brainstem related to surgical approaches to cavernous malformations. Neurosurgery 62:3 Suppl 1 917, 2008

    • Search Google Scholar
    • Export Citation
  • 62

    Rigamonti D, & Spetzler RF: The association of venous and cavernous malformations. Report of four cases and discussion of the pathophysiological, diagnostic, and therapeutic implications. Acta Neurochir (Wien) 92:100105, 1988

    • Search Google Scholar
    • Export Citation
  • 63

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

  • 64

    Samii M, , Eghbal R, , Carvalho GA, & Matthies C: Surgical management of brainstem cavernomas. J Neurosurg 95:825832, 2001

  • 65

    Sola RG, , Pulido P, , Pastor J, , Ochoa M, & Castedo J: Surgical treatment of symptomatic cavernous malformations of the brainstem. Acta Neurochir (Wien) 149:463470, 2007

    • Search Google Scholar
    • Export Citation
  • 66

    Steinberg GK, , Chang SD, , Gewirtz RJ, & Lopez JR: Microsurgical resection of brainstem, thalamic, and basal ganglia angiographically occult vascular malformations. Neurosurgery 46:260271, 2000

    • Search Google Scholar
    • Export Citation
  • 67

    Steňo J, , Bízik I, , Steňová J, & Timárová G: Subtemporal transtentorial resection of cavernous malformations involving the pyramidal tract in the upper pons and mesencephalon. Acta Neurochir (Wien) 153:19551962, 2011

    • Search Google Scholar
    • Export Citation
  • 68

    Tarnaris A, , Fernandes RP, & Kitchen ND: Does conservative management for brain stem cavernomas have better long-term outcome?. Br J Neurosurg 22:748757, 2008

    • Search Google Scholar
    • Export Citation
  • 69

    Wang CC, , Liu A, , Zhang JT, , Sun B, & Zhao YL: Surgical management of brain-stem cavernous malformations: report of 137 cases. Surg Neurol 59:444454, 2003

    • Search Google Scholar
    • Export Citation
  • 70

    Washington CW, , McCoy KE, & Zipfel GJ: Update on the natural history of cavernous malformations and factors predicting aggressive clinical presentation. Neurosurg Focus 29:3 E7, 2010

    • Search Google Scholar
    • Export Citation
  • 71

    Wurm G, , Schnizer M, & Fellner FA: Cerebral cavernous malformations associated with venous anomalies: surgical considerations. Neurosurgery 61:1 Suppl 390406, 2007

    • Search Google Scholar
    • Export Citation
  • 72

    Yamada S, , Liwnicz BH, , Thompson JR, , Colohan AR, , Iacono RP, & Tran JT: Pericapillary arteriovenous malformations angiographically manifested as cerebral venous malformations. Neurol Res 23:513521, 2001

    • Search Google Scholar
    • Export Citation
  • 73

    Zabramski JM, , Wascher TM, , Spetzler RF, , Johnson B, , Golfinos J, & Drayer BP, : The natural history of familial cavernous malformations: results of an ongoing study. J Neurosurg 80:422432, 1994

    • Search Google Scholar
    • Export Citation
  • 74

    Zimmerman RS, , Spetzler RF, , Lee KS, , Zabramski JM, & Hargraves RW: Cavernous malformations of the brain stem. J Neurosurg 75:3239, 1991

Metrics

All Time Past Year Past 30 Days
Abstract Views 1233 263 14
Full Text Views 285 38 1
PDF Downloads 185 24 0
EPUB Downloads 0 0 0