Navigated transcranial magnetic stimulation for glioma removal: prognostic value in motor function recovery from postsurgical neurological deficits

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OBJECTIVE

The aim of the present study was to evaluate the usefulness of navigated transcranial magnetic stimulation (nTMS) as a prognostic predictor for upper-extremity motor functional recovery from postsurgical neurological deficits.

METHODS

Preoperative and postoperative nTMS studies were prospectively applied in 14 patients (mean age 39 ± 12 years) who had intraparenchymal brain neoplasms located within or adjacent to the motor eloquent area in the cerebral hemisphere. Mapping by nTMS was done 3 times, i.e., before surgery, and 1 week and 3 weeks after surgery. To assess the response induced by nTMS, motor evoked potential (nTMS-MEP) was recorded using a surface electromyography electrode attached to the abductor pollicis brevis (APB). The cortical locations that elicited the largest electromyography response by nTMS were defined as hotspots. Hotspots for APB were confirmed as positive responsive sites by direct electrical stimulation (DES) during awake craniotomy. The distances between hotspots and lesions (DHS-L) were measured. Postoperative neurological deficits were assessed by manual muscle test and dynamometer. To validate the prognostic value of nTMS in recovery from upper-extremity paresis, the following were investigated: 1) the correlation between DHS-L and the serial grip strength change, and 2) the correlation between positive nTMS-MEP at 1 week after surgery and the serial grip strength change.

RESULTS

From the presurgical nTMS study, MEPs from targeted muscles were identified in 13 cases from affected hemispheres. In one case, MEP was not evoked due to a huge tumor. Among 9 cases from which intraoperative DES mapping for hand motor area was available, hotspots for APB identified by nTMS were concordant with DES-positive sites. Compared with the adjacent group (DHS-L < 10 mm, n = 6), the nonadjacent group (DHS-L ≥ 10 mm, n = 7) showed significantly better recovery of grip strength at 3 months after surgery (p < 0.01). There were correlations between DHS-L and recovery of grip strength at 1 week, 3 weeks, and 3 months after surgery (r = 0.74, 0.68, and 0.65, respectively). Postsurgical nTMS was accomplished in 13 patients. In 9 of 13 cases, nTMS-MEP from APB muscle was positive at 1 week after surgery. Excluding the case in which nTMS-MEP was negative from the presurgical nTMS study, recoveries in grip strength were compared between 2 groups, in which nTMS-MEP at 1 week after surgery was positive (n = 9) or negative (n = 3). Significant differences were observed between the 2 groups at 1 week, 3 weeks, and 3 months after surgery (p < 0.01). Positive nTMS-MEP at 1 week after surgery correlated well with the motor recovery at 1 week, 3 weeks, and 3 months after surgery (r = 0.87, 0.88, and 0.77, respectively).

CONCLUSIONS

Navigated TMS is a useful tool for identifying motor eloquent areas. The results of the present study have demonstrated the predictive value of nTMS in upper-extremity motor function recovery from postsurgical neurological deficits. The longer DHS-L and positive nTMS-MEP at 1 week after surgery have prognostic values of better recovery from postsurgical neurological deficits.

ABBREVIATIONS 5-ALA = 5-aminolevulinic acid; AH = affected hemisphere; AMT = active motor threshold; AP = anterior to posterior; APB = abductor pollicis brevis; BB = biceps brachii; DES = direct electrical stimulation; DHS-L = distance between hotspot and lesion; d-MEP = direct motor evoked potential; EMCS = epidural motor cortex stimulation; FMA = Fugl-Meyer assessment; io = intraoperative; LE = lower extremity; MMT = manual muscle testing; nTMS = navigated transcranial magnetic stimulation; OO = orbicularis oris; PA = posterior to anterior; RMT = resting motor threshold; TA = tibialis anterior; Tc-MEP = transcranial MEP; UE = upper extremity; UH = unaffected hemisphere.
Article Information

Contributor Notes

Correspondence Yoshihiro Muragaki, Institute of Advanced Biomedical Engineering & Science, Graduate School of Medicine, Tokyo Women's Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo 162-8666, Japan. email: ymuragaki@twmu.ac.jp.INCLUDE WHEN CITING Published online January 6, 2017; DOI: 10.3171/2016.8.JNS16442.Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

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References
  • 1

    Amassian VEStewart MQuirk GJRosenthal JL: Physiological basis of motor effects of a transient stimulus to cerebral cortex. Neurosurgery 20:74931987

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Boroojerdi BFoltys HKrings TSpetzger UThron ATöpper R: Localization of the motor hand area using transcranial magnetic stimulation and functional magnetic resonance imaging. Clin Neurophysiol 110:6997041999

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

    Brasil-Neto JPCohen LGPanizza MNilsson JRoth BJHallett M: Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J Clin Neurophysiol 9:1321361992

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

    Brogårdh CJohansson FWNygren FSjölund BH: Mode of hand training determines cortical reorganisation: a randomized controlled study in healthy adults. J Rehabil Med 42:7897942010

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

    Brown CEBoyd JDMurphy TH: Longitudinal in vivo imaging reveals balanced and branch-specific remodeling of mature cortical pyramidal dendritic arbors after stroke. J Cereb Blood Flow Metab 30:7837912010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Brown CELi PBoyd JDDelaney KRMurphy TH: Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J Neurosci 27:410141092007

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

    Coburger JKarhu JBittl MHopf NJ: First preoperative functional mapping via navigated transcranial magnetic stimulation in a 3-year-old boy. J Neurosurg Pediatr 9:6606642012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Coburger JMusahl CHenkes HHorvath-Rizea DBittl MWeissbach C: Comparison of navigated transcranial magnetic stimulation and functional magnetic resonance imaging for preoperative mapping in rolandic tumor surgery. Neurosurg Rev 36:65762013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Delvaux VAlagona GGérard PDe Pasqua VPennisi Gde Noordhout AM: Post-stroke reorganization of hand motor area: a 1-year prospective follow-up with focal transcranial magnetic stimulation. Clin Neurophysiol 114:121712252003

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

    Di Lazzaro VOliviero AMazzone PInsola APilato FSaturno E: Comparison of descending volleys evoked by monophasic and biphasic magnetic stimulation of the motor cortex in conscious humans. Exp Brain Res 141:1211272001

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Di Lazzaro VOliviero APilato FSaturno EDileone MMazzone P: The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115:2552662004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Dromerick AWEdwards DFHahn M: Does the application of constraint-induced movement therapy during acute rehabilitation reduce arm impairment after ischemic stroke?. Stroke 31:298429882000

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

    Duffau H: Does post-lesional subcortical plasticity exist in the human brain?. Neurosci Res 65:1311352009

  • 14

    Duffau HCapelle LDenvil DSichez NGatignol PLopes M: Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry 74:9019072003

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

    Escudero JVSancho JBautista DEscudero MLópez-Trigo J: Prognostic value of motor evoked potential obtained by transcranial magnetic brain stimulation in motor function recovery in patients with acute ischemic stroke. Stroke 29:185418591998

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Fontaine DCapelle LDuffau H: Somatotopy of the supplementary motor area: evidence from correlation of the extent of surgical resection with the clinical patterns of deficit. Neurosurgery 50:2973052002

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Forster MTHattingen ESenft CGasser TSeifert VSzelényi A: Navigated transcranial magnetic stimulation and functional magnetic resonance imaging: advanced adjuncts in preoperative planning for central region tumors. Neurosurgery 68:131713252011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Frey DStrack VWiener EJussen DVajkoczy PPicht T: A new approach for corticospinal tract reconstruction based on navigated transcranial stimulation and standardized fractional anisotropy values. Neuroimage 62:160016092012

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

    Fugl-Meyer ARJääskö LLeyman IOlsson SSteglind S: The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med 7:13311975

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Hartkens THill DLCastellano-Smith ADHawkes DJMaurer CR JrMartin AJ: Measurement and analysis of brain deformation during neurosurgery. IEEE Trans Med Imaging 22:82922003

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

    Hislop HJMontgomery J: Daniels and Worthingham's Muscle Testing: Techniques of Manual Examination ed 7PhiladelphiaSaunders1995

  • 22

    Hendricks HTvan Limbeek JGeurts ACZwarts MJ: Motor recovery after stroke: a systematic review of the literature. Arch Phys Med Rehabil 83:162916372002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Hendricks HTZwarts MJPlat EFvan Limbeek J: Systematic review for the early prediction of motor and functional outcome after stroke by using motor-evoked potentials. Arch Phys Med Rehabil 83:130313082002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Ius TIsola MBudai RPauletto GTomasino BFadiga L: Low-grade glioma surgery in eloquent areas: volumetric analysis of extent of resection and its impact on overall survival. A single-institution experience in 190 patients: clinical article. J Neurosurg 117:103910522012

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

    Japan Neurosurgical Society: Report of Brain Tumor Registry of Japan (1984–2000). Neurol Med Chir (Tokyo) 49:SupplPS1PS962009

  • 26

    Kammer TBeck SThielscher ALaubis-Herrmann UTopka H: Motor thresholds in humans: a transcranial magnetic stimulation study comparing different pulse waveforms, current directions and stimulator types. Clin Neurophysiol 112:2502582001

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

    Kantelhardt SRFadini TFinke MKallenberg KSiemerkus JBockermann V: Robot-assisted image-guided transcranial magnetic stimulation for somatotopic mapping of the motor cortex: a clinical pilot study. Acta Neurochir (Wien) 152:3333432010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Kawashima AKrieg SMFaust KSchneider HVajkoczy PPicht T: Plastic reshaping of cortical language areas evaluated by navigated transcranial magnetic stimulation in a surgical case of glioblastoma multiforme. Clin Neurol Neurosurg 115:222622292013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Kayama T: The guidelines for awake craniotomy guidelines committee of the Japan Awake Surgery Conference. Neurol Med Chir (Tokyo) 52:1191412012

  • 30

    Krainik ADuffau HCapelle LCornu PBoch ALMangin JF: Role of the healthy hemisphere in recovery after resection of the supplementary motor area. Neurology 62:132313322004

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

    Krieg SMShiban EBuchmann NGempt JFoerschler AMeyer B: Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas. J Neurosurg 116:99410012012

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

    Krieg SMShiban EBuchmann NMeyer BRingel F: Presurgical navigated transcranial magnetic brain stimulation for recurrent gliomas in motor eloquent areas. Clin Neurophysiol 124:5225272013

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

    Krieg SMSollmann NHauck TIlle SMeyer BRingel F: Repeated mapping of cortical language sites by preoperative navigated transcranial magnetic stimulation compared to repeated intraoperative DCS mapping in awake craniotomy. BMC Neurosci 15:202014

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

    Kuhnt DBecker AGanslandt OBauer MBuchfelder MNimsky C: Correlation of the extent of tumor volume resection and patient survival in surgery of glioblastoma multiforme with high-field intraoperative MRI guidance. Neuro Oncol 13:133913482011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35

    Laakso IHirata AUgawa Y: Effects of coil orientation on the electric field induced by TMS over the hand motor area. Phys Med Biol 59:2032182014

  • 36

    Lacroix MAbi-Said DFourney DRGokaslan ZLShi WDeMonte F: A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:1901982001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Laplane DTalairach JMeininger VBancaud JOrgogozo JM: Clinical consequences of corticectomies involving the supplementary motor area in man. J Neurol Sci 34:3013141977

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

    Lefaucheur JPHolsheimer JGoujon CKeravel YNguyen JP: Descending volleys generated by efficacious epidural motor cortex stimulation in patients with chronic neuropathic pain. Exp Neurol 223:6096142010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Li YMSuki DHess KSawaya R: The influence of maximum safe resection of glioblastoma on survival in 1229 patients: Can we do better than gross-total resection?. J Neurosurg 124:9779882016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Muragaki YIseki HMaruyama TKawamata TYamane FNakamura R: Usefulness of intraoperative magnetic resonance imaging for glioma surgery. Acta Neurochir Suppl 98:67752006

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

    Muragaki YIseki HMaruyama TTanaka MShinohara CSuzuki T: Information-guided surgical management of gliomas using low-field-strength intraoperative MRI. Acta Neurochir Suppl 109:67722011

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

    Ngomo SLeonard GMoffet HMercier C: Comparison of transcranial magnetic stimulation measures obtained at rest and under active conditions and their reliability. J Neurosci Methods 205:65712012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Nitta MMuragaki YMaruyama TIseki HIkuta SKonishi Y: Updated therapeutic strategy for adult low-grade glioma stratified by resection and tumor subtype. Neurol Med Chir (Tokyo) 53:4474542013

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

    Nudo RJMilliken GWJenkins WMMerzenich MM: Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16:7858071996

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

    Opitz AZafar NBockermann VRohde VPaulus W: Validating computationally predicted TMS stimulation areas using direct electrical stimulation in patients with brain tumors near precentral regions. Neuroimage Clin 4:5005072014

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

    Paiva WSFonoff ETMarcolin MACabrera HNTeixeira MJ: Cortical mapping with navigated transcranial magnetic stimulation in low-grade glioma surgery. Neuropsychiatr Dis Treat 8:1972012012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47

    Patton HDAmassian VE: Single and multiple-unit analysis of cortical stage of pyramidal tract activation. J Neurophysiol 17:3453631954

  • 48

    Pennisi GRapisarda GBella RCalabrese VMaertens De Noordhout ADelwaide PJ: Absence of response to early transcranial magnetic stimulation in ischemic stroke patients: prognostic value for hand motor recovery. Stroke 30:266626701999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49

    Picht TKrieg SMSollmann NRösler JNiraula BNeuvonen T: A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. Neurosurgery 72:8088192013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50

    Picht TMularski SKuehn BVajkoczy PKombos TSuess O: Navigated transcranial magnetic stimulation for preoperative functional diagnostics in brain tumor surgery. Neurosurgery 65:6 Suppl93992009

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51

    Picht TSchmidt SBrandt SFrey DHannula HNeuvonen T: Preoperative functional mapping for rolandic brain tumor surgery: comparison of navigated transcranial magnetic stimulation to direct cortical stimulation. Neurosurgery 69:5815882011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52

    Picht TSchulz JHanna MSchmidt SSuess OVajkoczy P: Assessment of the influence of navigated transcranial magnetic stimulation on surgical planning for tumors in or near the motor cortex. Neurosurgery 70:124812572012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53

    Picht TStrack VSchulz JZdunczyk AFrey DSchmidt S: Assessing the functional status of the motor system in brain tumor patients using transcranial magnetic stimulation. Acta Neurochir (Wien) 154:207520812012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54

    Platz TPinkowski Cvan Wijck FKim IHdi Bella PJohnson G: Reliability and validity of arm function assessment with standardized guidelines for the Fugl-Meyer Test, Action Research Arm Test and Box and Block Test: a multicentre study. Clin Rehabil 19:4044112005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 55

    Rösler JNiraula BStrack VZdunczyk ASchilt SSavolainen P: Language mapping in healthy volunteers and brain tumor patients with a novel navigated TMS system: evidence of tumor-induced plasticity. Clin Neurophysiol 125:5265362014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56

    Rossini PMBarker ATBerardelli ACaramia MDCaruso GCracco RQ: Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79921994

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 57

    Rossini PMCalautti CPauri FBaron JC: Post-stroke plastic reorganisation in the adult brain. Lancet Neurol 2:4935022003

  • 58

    Rossini PMDal Forno G: Neuronal post-stroke plasticity in the adult. Restor Neurol Neurosci 22:1932062004

  • 59

    Roth YPell GSChistyakov AVSinai AZangen AZaaroor M: Motor cortex activation by H-coil and figure-8 coil at different depths. Combined motor threshold and electric field distribution study. Clin Neurophysiol 125:3363432014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 60

    Ruohonen JIlmoniemi RJ: Modeling of the stimulating field generation in TMS. Electroencephalogr Clin Neurophysiol Suppl 51:30401999

  • 61

    Saito TMuragaki YMaruyama TTamura MNitta MOkada Y: Intraoperative functional mapping and monitoring during glioma surgery. Neurol Med Chir (Tokyo) 55:1132015

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 62

    Sanai NBerger MS: Glioma extent of resection and its impact on patient outcome. Neurosurgery 62:7537642008

  • 63

    Schieber MHHibbard LS: How somatotopic is the motor cortex hand area?. Science 261:4894921993

  • 64

    Szelényi ABello LDuffau HFava EFeigl GCGalanda M: Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 28:2E72010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 65

    Takahashi SVajkoczy PPicht T: Navigated transcranial magnetic stimulation for mapping the motor cortex in patients with rolandic brain tumors. Neurosurg Focus 34:4E32013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 66

    Talelli PGreenwood RJRothwell JC: Arm function after stroke: neurophysiological correlates and recovery mechanisms assessed by transcranial magnetic stimulation. Clin Neurophysiol 117:164116592006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 67

    Tarapore PEFindlay AMHonma SMMizuiri DHoude JFBerger MS: Language mapping with navigated repetitive TMS: proof of technique and validation. Neuroimage 82:2602722013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 68

    Tarapore PETate MCFindlay AMHonma SMMizuiri DBerger MS: Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. J Neurosurg 117:3543622012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 69

    Terao YUgawa Y: Basic mechanisms of TMS. J Clin Neurophysiol 19:3223432002

  • 70

    Turton AWroe STrepte NFraser CLemon RN: Contralateral and ipsilateral EMG responses to transcranial magnetic stimulation during recovery of arm and hand function after stroke. Electroencephalogr Clin Neurophysiol 101:3163281996

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 71

    Vargo M: Brain tumor rehabilitation. Am J Phys Med Rehabil 90:5 Suppl 1S50S622011

  • 72

    Zdunczyk AFleischmann RSchulz JVajkoczy PPicht T: The reliability of topographic measurements from navigated transcranial magnetic stimulation in healthy volunteers and tumor patients. Acta Neurochir (Wien) 155:130913172013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 73

    Zentner JHufnagel APechstein UWolf HKSchramm J: Functional results after resective procedures involving the supplementary motor area. J Neurosurg 85:5425491996

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
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