Reducing hemorrhagic complications in functional neurosurgery: a large case series and systematic literature review

Clinical article

Ludvic Zrinzo M.D., M.Sc., F.R.C.S.(Edin)1,2, Thomas Foltynie M.R.C.P., Ph.D.1, Patricia Limousin M.D., Ph.D.1, and Marwan I. Hariz M.D., Ph.D.1,3
View More View Less
  • 1 Unit of Functional Neurosurgery, Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London;
  • | 2 Victor Horsley Department of Neurosurgery, National Hospital for Neurology and Neurosurgery, London, United Kingdom; and
  • | 3 Department of Neurosurgery, University Hospital, Umeå, Sweden
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

Hemorrhagic complications carry by far the highest risk of devastating neurological outcome in functional neurosurgery. Literature published over the past 10 years suggests that hemorrhage, although relatively rare, remains a significant problem. Estimating the true incidence of and risk factors for hemorrhage in functional neurosurgery is a challenging issue.

Methods

The authors analyzed the hemorrhage rate in a consecutive series of 214 patients undergoing imageguided deep brain stimulation (DBS) lead placement without microelectrode recording (MER) and with routine postoperative MR imaging lead verification. They also conducted a systematic review of the literature on stereotactic ablative surgery and DBS over a 10-year period to determine the incidence and risk factors for hemorrhage as a complication of functional neurosurgery.

Results

The total incidence of hemorrhage in our series of image-guided DBS was 0.9%: asymptomatic in 0.5%, symptomatic in 0.5%, and causing permanent deficit in 0.0% of patients. Weighted means calculated from the literature review suggest that the overall incidence of hemorrhage in functional neurosurgery is 5.0%, with asymptomatic hemorrhage occurring in 1.9% of patients, symptomatic hemorrhage in 2.1% and hemorrhage resulting in permanent deficit or death in 1.1%. Hypertension and age were the most important patient-related factors associated with an increased risk of hemorrhage. Risk factors related to surgical technique included use of MER, number of MER penetrations, as well as sulcal or ventricular involvement by the trajectory. The incidence of hemorrhage in studies adopting an image-guided and image-verified approach without MER was significantly lower than that reported with other operative techniques (p < 0.001 for total number of hemorrhages, p < 0.001 for asymptomatic hemorrhage, p < 0.004 for symptomatic hemorrhage, and p = 0.001 for hemorrhage leading to permanent deficit; Fisher exact test).

Conclusions

Age and a history of hypertension are associated with an increased risk of hemorrhage in functional neurosurgery. Surgical factors that increase the risk of hemorrhage include the use of MER and sulcal or ventricular incursion. The meticulous use of neuroimaging—both in planning the trajectory and for target verification—can avoid all of these surgery-related risk factors and appears to carry a significantly lower risk of hemorrhage and associated permanent deficit.

Abbreviations used in this paper:

DBS = deep brain stimulation; GPi = globus pallidus internus; MER = microelectrode recording; PD = Parkinson disease; STN = subthalamic nucleus; UCL = University College London; Vim = ventralis intermedius nucleus of the thalamus.

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

USD  $505.00

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

USD  $600.00
  • 1

    Alkhani A, & Lozano AM: Pallidotomy for Parkinson disease: a review of contemporary literature. J Neurosurg 94:4349, 2001

  • 2

    Alterman RL, & Tagliati M: Deep brain stimulation for torsion dystonia in children. Childs Nerv Syst 23:10331040, 2007

  • 3

    Bejjani BP, , Dormont D, , Pidoux B, , Yelnik J, , Damier P, & Arnulf I, et al.: Bilateral subthalamic stimulation for Parkinson's disease by using three-dimensional stereotactic magnetic resonance imaging and electrophysiological guidance. J Neurosurg 92:615625, 2000

    • Search Google Scholar
    • Export Citation
  • 4

    Ben-Haim S, , Asaad WF, , Gale JT, & Eskandar EN: Risk factors for hemorrhage during microelectrode-guided deep brain stimulation and the introduction of an improved microelectrode design. Neurosurgery 64:754763, 2009

    • Search Google Scholar
    • Export Citation
  • 5

    Beric A, , Kelly PJ, , Rezai A, , Sterio D, , Mogilner A, & Zonenshayn M, et al.: Complications of deep brain stimulation surgery. Stereotact Funct Neurosurg 77:7378, 2001

    • Search Google Scholar
    • Export Citation
  • 6

    Bhatia S, , Oh M, , Whiting T, , Quigley M, & Whiting D: Surgical complications of deep brain stimulation. A longitudinal single surgeon, single institution study. Stereotact Funct Neurosurg 86:367372, 2008

    • Search Google Scholar
    • Export Citation
  • 7

    Binder DK, , Rau GM, & Starr PA: Risk factors for hemorrhage during microelectrode-guided deep brain stimulator implantation for movement disorders. Neurosurgery 56:722732, 2005

    • Search Google Scholar
    • Export Citation
  • 8

    Blomstedt P, , Hariz GM, & Hariz MI: Pallidotomy versus pallidal stimulation. Parkinsonism Relat Disord 12:296301, 2006

  • 9

    Blomstedt P, & Hariz MI: Are complications less common in deep brain stimulation than in ablative procedures for movement disorders?. Stereotact Funct Neurosurg 84:7281, 2006

    • Search Google Scholar
    • Export Citation
  • 10

    Chan DT, , Zhu XL, , Yeung JH, , Mok VC, , Wong E, & Lau C, et al.: Complications of deep brain stimulation: a collective review. Asian J Surg 32:258263, 2009

    • Search Google Scholar
    • Export Citation
  • 11

    Chen CC, , Pogosyan A, , Zrinzo LU, , Tisch S, , Limousin P, & Ashkan K, et al.: Intra-operative recordings of local field potentials can help localize the subthalamic nucleus in Parkinson's disease surgery. Exp Neurol 198:214221, 2006

    • Search Google Scholar
    • Export Citation
  • 12

    Chhabra V, , Sung E, , Mewes K, , Bakay RA, , Abosch A, & Gross RE: Safety of magnetic resonance imaging of deep brain stimulator systems: a serial imaging and clinical retrospective study. Clinical article. J Neurosurg 112:497502, 2010

    • Search Google Scholar
    • Export Citation
  • 13

    Coubes P, , Cif L, , El Fertit H, , Hemm S, , Vayssiere N, & Serrat S, et al.: Electrical stimulation of the globus pallidus internus in patients with primary generalized dystonia: long-term results. J Neurosurg 101:189194, 2004

    • Search Google Scholar
    • Export Citation
  • 14

    de Bie RM, , de Haan RJ, , Schuurman PR, , Esselink RA, , Bosch DA, & Speelman JD: Morbidity and mortality following pallidotomy in Parkinson's disease: a systematic review. Neurology 58:10081012, 2002

    • Search Google Scholar
    • Export Citation
  • 15

    Deep-Brain Stimulation for Parkinson's Disease Study Group: Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. N Engl J Med 345:956963, 2001

    • Search Google Scholar
    • Export Citation
  • 16

    Deuschl G, , Schade-Brittinger C, , Krack P, , Volkmann J, , Schäfer H, & Bötzel K, et al.: A randomized trial of deep-brain stimulation for Parkinson's disease. N Engl J Med 355:896908, 2006

    • Search Google Scholar
    • Export Citation
  • 17

    Elias WJ, , Sansur CA, & Frysinger RC: Sulcal and ventricular trajectories in stereotactic surgery. Clinical article. J Neurosurg 110:201207, 2009

    • Search Google Scholar
    • Export Citation
  • 18

    Eskandar EN, , Shinobu LA, , Penney JB Jr, , Cosgrove GR, & Counihan TJ: Stereotactic pallidotomy performed without using microelectrode guidance in patients with Parkinson's disease: surgical technique and 2-year results. J Neurosurg 92:375383, 2000

    • Search Google Scholar
    • Export Citation
  • 19

    Favre J, , Taha JM, & Burchiel KJ: An analysis of the respective risks of hematoma formation in 361 consecutive morphological and functional stereotactic procedures. Neurosurgery 50:4857, 2002

    • Search Google Scholar
    • Export Citation
  • 20

    Fisher R, , Salanova V, , Witt T, , Worth R, , Henry T, & Gross R, et al.: Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia 51:899908, 2010

    • Search Google Scholar
    • Export Citation
  • 21

    Follett KA, , Weaver FM, , Stern M, , Hur K, , Harris CL, & Luo P, et al.: Pallidal versus subthalamic deep-brain stimulation for Parkinson's disease. N Engl J Med 362:20772091, 2010

    • Search Google Scholar
    • Export Citation
  • 22

    Foltynie T, , Zrinzo L, , Martinez-Torres I, , Tripoliti E, , Petersen E, & Holl E, et al.: MRI-guided STN DBS in Parkinson's disease without microelectrode recording: efficacy and safety. J Neurol Neurosurg Psychiatry 82:358363, 2011

    • Search Google Scholar
    • Export Citation
  • 23

    Gill CE, , Konrad PE, , Davis TL, & Charles D: Deep brain stimulation for Parkinson's disease: the Vanderbilt University Medical Center experience, 1998–2004. Tenn Med 100:4547, 2007

    • Search Google Scholar
    • Export Citation
  • 24

    Goodman RR, , Kim B, , McClelland S III, , Senatus PB, , Winfield LM, & Pullman SL, et al.: Operative techniques and morbidity with subthalamic nucleus deep brain stimulation in 100 consecutive patients with advanced Parkinson's disease. J Neurol Neurosurg Psychiatry 77:1217, 2006

    • Search Google Scholar
    • Export Citation
  • 25

    Gorgulho A, , De Salles AA, , Frighetto L, & Behnke E: Incidence of hemorrhage associated with electrophysiological studies performed using macroelectrodes and microelectrodes in functional neurosurgery. J Neurosurg 102:888896, 2005

    • Search Google Scholar
    • Export Citation
  • 26

    Halpern C, , Hurtig H, , Jaggi J, , Grossman M, , Won M, & Baltuch G: Deep brain stimulation in neurologic disorders. Parkinsonism Relat Disord 13:116, 2007

    • Search Google Scholar
    • Export Citation
  • 27

    Halpern CH, , Samadani U, , Litt B, , Jaggi JL, & Baltuch GH: Deep brain stimulation for epilepsy. Neurotherapeutics 5:5967, 2008

  • 28

    Hamani C, , Richter E, , Schwalb JM, & Lozano AM: Bilateral subthalamic nucleus stimulation for Parkinson's disease: a systematic review of the clinical literature. Neurosurgery 56:13131324, 2005

    • Search Google Scholar
    • Export Citation
  • 29

    Hariz MI: From functional neurosurgery to “interventional” neurology: survey of publications on thalamotomy, pallidotomy, and deep brain stimulation for Parkinson's disease from 1966 to 2001. Mov Disord 18:845853, 2003

    • Search Google Scholar
    • Export Citation
  • 30

    Hariz MI: Safety and risk of microelectrode recording in surgery for movement disorders. Stereotact Funct Neurosurg 78:146157, 2002

  • 31

    Hariz MI, , Krack P, , Melvill R, , Jorgensen JV, , Hamel W, & Hirabayashi H, et al.: A quick and universal method for stereotactic visualization of the subthalamic nucleus before and after implantation of deep brain stimulation electrodes. Stereotact Funct Neurosurg 80:96101, 2003

    • Search Google Scholar
    • Export Citation
  • 32

    Hertel F, , Züchner M, , Weimar I, , Gemmar P, , Noll B, & Bettag M, et al.: Implantation of electrodes for deep brain stimulation of the subthalamic nucleus in advanced Parkinson's disease with the aid of intraoperative microrecording under general anesthesia. Neurosurgery 59:E1138, 2006

    • Search Google Scholar
    • Export Citation
  • 33

    Herzog J, , Volkmann J, , Krack P, , Kopper F, , Pötter M, & Lorenz D, et al.: Two-year follow-up of subthalamic deep brain stimulation in Parkinson's disease. Mov Disord 18:13321337, 2003

    • Search Google Scholar
    • Export Citation
  • 34

    Higuchi Y, & Iacono RP: Surgical complications in patients with Parkinson's disease after posteroventral pallidotomy. Neurosurgery 52:558571, 2003

    • Search Google Scholar
    • Export Citation
  • 35

    Hirabayashi H, , Tengvar M, & Hariz MI: Stereotactic imaging of the pallidal target. Mov Disord 17:Suppl 3 S130S134, 2002

  • 36

    Holl EM, , Petersen EA, , Foltynie T, , Martinez-Torres I, , Limousin P, & Hariz MI, et al.: Improving targeting in image-guided frame-based deep brain stimulation. Neurosurgery 67:2 Suppl Operative 437447, 2010

    • Search Google Scholar
    • Export Citation
  • 37

    Kenney C, , Simpson R, , Hunter C, , Ondo W, , Almaguer M, & Davidson A, et al.: Short-term and long-term safety of deep brain stimulation in the treatment of movement disorders. J Neurosurg 106:621625, 2007

    • Search Google Scholar
    • Export Citation
  • 38

    Khatib R, , Ebrahim Z, , Rezai A, , Cata JP, , Boulis NM, & John Doyle D, et al.: Perioperative events during deep brain stimulation: the experience at Cleveland Clinic. J Neurosurg Anesthesiol 20:3640, 2008

    • Search Google Scholar
    • Export Citation
  • 39

    Kleiner-Fisman G, , Herzog J, , Fisman DN, , Tamma F, , Lyons KE, & Pahwa R, et al.: Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov Disord 21:Suppl 14 S290S304, 2006

    • Search Google Scholar
    • Export Citation
  • 40

    Koller WC, , Lyons KE, , Wilkinson SB, , Troster AI, & Pahwa R: Long-term safety and efficacy of unilateral deep brain stimulation of the thalamus in essential tremor. Mov Disord 16:464468, 2001

    • Search Google Scholar
    • Export Citation
  • 41

    Kondziolka D, , Bonaroti E, , Baser S, , Brandt F, , Kim YS, & Lunsford LD: Outcomes after stereotactically guided pallidotomy for advanced Parkinson's disease. J Neurosurg 90:197202, 1999

    • Search Google Scholar
    • Export Citation
  • 42

    Krack P, , Batir A, , Van Blercom N, , Chabardes S, , Fraix V, & Ardouin C, et al.: Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 349:19251934, 2003

    • Search Google Scholar
    • Export Citation
  • 43

    Larson PS, , Richardson RM, , Starr PA, & Martin AJ: Magnetic resonance imaging of implanted deep brain stimulators: experience in a large series. Stereotact Funct Neurosurg 86:92100, 2008

    • Search Google Scholar
    • Export Citation
  • 44

    Lee JY, , Deogaonkar M, & Rezai A: Deep brain stimulation of globus pallidus internus for dystonia. Parkinsonism Relat Disord 13:261265, 2007

    • Search Google Scholar
    • Export Citation
  • 45

    López-Flores G, , Miguel-Morales J, , Teijeiro-Amador J, , Vitek J, , Perez-Parra S, & Fernández-Melo R, et al.: Anatomic and neurophysiological methods for the targeting and lesioning of the subthalamic nucleus: Cuban experience and review. Neurosurgery 52:817831, 2003

    • Search Google Scholar
    • Export Citation
  • 46

    Machado A, , Rezai AR, , Kopell BH, , Gross RE, , Sharan AD, & Benabid AL: Deep brain stimulation for Parkinson's disease: surgical technique and perioperative management. Mov Disord 21:Suppl 14 S247S258, 2006

    • Search Google Scholar
    • Export Citation
  • 47

    Maldonado IL, , Roujeau T, , Cif L, , Gonzalez V, , El-Fertit H, & Vasques X, et al.: Magnetic resonance-based deep brain stimulation technique: a series of 478 consecutive implanted electrodes with no perioperative intracerebral hemorrhage. Neurosurgery 65:6 Suppl 196202, 2009

    • Search Google Scholar
    • Export Citation
  • 48

    Mallet L, , Polosan M, , Jaafari N, , Baup N, , Welter ML, & Fontaine D, et al.: Subthalamic nucleus stimulation in severe obsessive-compulsive disorder. N Engl J Med 359:21212134, 2008

    • Search Google Scholar
    • Export Citation
  • 49

    Mikos A, , Pavon J, , Bowers D, , Foote KD, , Resnick AS, & Fernandez HH, et al.: Factors related to extended hospital stays following deep brain stimulation for Parkinson's disease. Parkinsonism Relat Disord 16:324328, 2010

    • Search Google Scholar
    • Export Citation
  • 50

    Ory-Magne F, , Brefel-Courbon C, , Simonetta-Moreau M, , Fabre N, , Lotterie JA, & Chaynes P, et al.: Does ageing influence deep brain stimulation outcomes in Parkinson's disease?. Mov Disord 22:14571463, 2007

    • Search Google Scholar
    • Export Citation
  • 51

    Palur RS, , Berk C, , Schulzer M, & Honey CR: A metaanalysis comparing the results of pallidotomy performed using microelectrode recording or macroelectrode stimulation. J Neurosurg 96:10581062, 2002

    • Search Google Scholar
    • Export Citation
  • 52

    Patel NK, , Plaha P, & Gill SS: Magnetic resonance imaging-directed method for functional neurosurgery using implantable guide tubes. Neurosurgery 61:5 Suppl 2 358366, 2007

    • Search Google Scholar
    • Export Citation
  • 53

    Patel NK, , Plaha P, , O'Sullivan K, , McCarter R, , Heywood P, & Gill SS: MRI directed bilateral stimulation of the subthalamic nucleus in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 74:16311637, 2003

    • Search Google Scholar
    • Export Citation
  • 54

    Rezai AR, , Kopell BH, , Gross RE, , Vitek JL, , Sharan AD, & Limousin P, et al.: Deep brain stimulation for Parkinson's disease: surgical issues. Mov Disord 21:Suppl 14 S197S218, 2006

    • Search Google Scholar
    • Export Citation
  • 55

    Richardson RM, , Ostrem JL, & Starr PA: Surgical repositioning of misplaced subthalamic electrodes in Parkinson's disease: location of effective and ineffective leads. Stereotact Funct Neurosurg 87:297303, 2009

    • Search Google Scholar
    • Export Citation
  • 56

    Sansur CA, , Frysinger RC, , Pouratian N, , Fu KM, , Bittl M, & Oskouian RJ, et al.: Incidence of symptomatic hemorrhage after stereotactic electrode placement. J Neurosurg 107:9981003, 2007

    • Search Google Scholar
    • Export Citation
  • 57

    Schoenen J, , Di Clemente L, , Vandenheede M, , Fumal A, , De Pasqua V, & Mouchamps M, et al.: Hypothalamic stimulation in chronic cluster headache: a pilot study of efficacy and mode of action. Brain 128:940947, 2005

    • Search Google Scholar
    • Export Citation
  • 58

    Schrader B, , Hamel W, , Weinert D, & Mehdorn HM: Documentation of electrode localization. Mov Disord 17:Suppl 3 S167S174, 2002

  • 59

    Seijo FJ, , Alvarez-Vega MA, , Gutierrez JC, , Fdez-Glez F, & Lozano B: Complications in subthalamic nucleus stimulation surgery for treatment of Parkinson's disease. Review of 272 procedures. Acta Neurochir (Wien) 149:867876, 2007

    • Search Google Scholar
    • Export Citation
  • 60

    Tagliati M, , Jankovic J, , Pagan F, , Susatia F, , Isaias IU, & Okun MS: Safety of MRI in patients with implanted deep brain stimulation devices. Neuroimage 47:Suppl 2 T53T57, 2009

    • Search Google Scholar
    • Export Citation
  • 61

    Terao T, , Takahashi H, , Yokochi F, , Taniguchi M, , Okiyama R, & Hamada I: Hemorrhagic complication of stereotactic surgery in patients with movement disorders. J Neurosurg 98:12411246, 2003

    • Search Google Scholar
    • Export Citation
  • 62

    Tisch S, , Zrinzo L, , Limousin P, , Bhatia KP, , Quinn N, & Ashkan K, et al.: Effect of electrode contact location on clinical efficacy of pallidal deep brain stimulation in primary generalised dystonia. J Neurol Neurosurg Psychiatry 78:13141319, 2007

    • Search Google Scholar
    • Export Citation
  • 63

    Umemura A, , Jaggi JL, , Hurtig HI, , Siderowf AD, , Colcher A, & Stern MB, et al.: Deep brain stimulation for movement disorders: morbidity and mortality in 109 patients. J Neurosurg 98:779784, 2003

    • Search Google Scholar
    • Export Citation
  • 64

    Velasco AL, , Velasco F, , Jiménez F, , Velasco M, , Castro G, & Carrillo-Ruiz JD, et al.: Neuromodulation of the centromedian thalamic nuclei in the treatment of generalized seizures and the improvement of the quality of life in patients with Lennox-Gastaut syndrome. Epilepsia 47:12031212, 2006

    • Search Google Scholar
    • Export Citation
  • 65

    Voges J, , Hilker R, , Bötzel K, , Kiening KL, , Kloss M, & Kupsch A, et al.: Thirty days complication rate following surgery performed for deep-brain-stimulation. Mov Disord 22:14861489, 2007

    • Search Google Scholar
    • Export Citation
  • 66

    Voges J, , Volkmann J, , Allert N, , Lehrke R, , Koulousakis A, & Freund HJ, et al.: Bilateral high-frequency stimulation in the subthalamic nucleus for the treatment of Parkinson disease: correlation of therapeutic effect with anatomical electrode position. J Neurosurg 96:269279, 2002

    • Search Google Scholar
    • Export Citation
  • 67

    Xiaowu H, , Xiufeng J, , Xiaoping Z, , Bin H, , Laixing W, & Yiqun C, et al.: Risks of intracranial hemorrhage in patients with Parkinson's disease receiving deep brain stimulation and ablation. Parkinsonism Relat Disord 16:96100, 2010

    • Search Google Scholar
    • Export Citation
  • 68

    Zrinzo L, , van Hulzen AL, , Gorgulho AA, , Limousin P, , Staal MJ, & De Salles AA, et al.: Avoiding the ventricle: a simple step to improve accuracy of anatomical targeting during deep brain stimulation. Clinical article. J Neurosurg 110:12831290, 2009

    • Search Google Scholar
    • Export Citation
  • 70

    Zrinzo L, , Zrinzo LV, , Tisch S, , Limousin PD, , Yousry TA, & Afshar F, et al.: Stereotactic localization of the human pedunculopontine nucleus: atlas-based coordinates and validation of a magnetic resonance imaging protocol for direct localization. Brain 131:15881598, 2008

    • Search Google Scholar
    • Export Citation
  • 71

    Zrinzo LU, & Hariz MI, Impedance recording in functional neurosurgery. Lozano AM, , Gildenberg PL, & Tasker RR: Textbook of Stereotactic and Functional Neurosurgery ed 2 Berlin, Springer, 2009. 13251330

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 1173 376 28
Full Text Views 452 61 5
PDF Downloads 244 37 10
EPUB Downloads 0 0 0