Intraoperative acceleration measurements to quantify improvement in tremor during deep brain stimulation surgery

  • Ashesh Shah
  • Jérôme Coste
  • Jean-Jacques Lemaire
  • Ethan Taub
  • W. M. Michael Schüpbach
  • Claudio Pollo
  • Erik Schkommodau
  • Raphael Guzman
  • Simone Hemm-Ode
Original Article

Abstract

Deep brain stimulation (DBS) surgery is extensively used in the treatment of movement disorders. Nevertheless, methods to evaluate the clinical response during intraoperative stimulation tests to identify the optimal position for the implantation of the chronic DBS lead remain subjective. In this paper, we describe a new, versatile method for quantitative intraoperative evaluation of improvement in tremor with an acceleration sensor that is mounted on the patient’s wrist during surgery. At each anatomical test position, the improvement in tremor compared to the initial tremor is estimated on the basis of extracted outcome measures. This method was tested on 15 tremor patients undergoing DBS surgery in two centers. Data from 359 stimulation tests were acquired. Our results suggest that accelerometric evaluation detects tremor changes more sensitively than subjective visual ratings. The effective stimulation current amplitudes identified from the quantitative data (1.1 ± 0.8 mA) are lower than those identified by visual evaluation (1.7 ± 0.8 mA) for similar improvement in tremor. Additionally, if these data had been used to choose the chronic implant position of the DBS lead, 15 of the 26 choices would have been different. These results show that our method of accelerometric evaluation can potentially improve DBS targeting.

Keywords

Deep brain stimulation Intraoperative monitoring Acceleration Tremor Parkinson’s disease Essential tremor 

References

  1. 1.
    Abosch A, Timmermann L, Bartley S, Rietkerk HG, Whiting D, Connolly PJ et al (2013) An international survey of deep brain stimulation procedural steps. Stereotact Funct Neurosurg 91(1):1–11. doi:10.1159/000343207 CrossRefPubMedGoogle Scholar
  2. 2.
    Askari S, Zhang M, Won DS (2010) An EMG-based system for continuous monitoring of clinical efficacy of Parkinson’s disease treatments. In: Conference proceedings: Annual international conference of the IEEE engineering in medicine and biology society. IEEE engineering in medicine and biology society. Conference, 2010, pp 98–101. doi:10.1109/IEMBS.2010.5626133
  3. 3.
    Basu I, Graupe D, Tuninetti D, Shukla P, Slavin KV, Metman LV et al (2013) Pathological tremor prediction using surface electromyogram and acceleration: potential use in ‘ON–OFF’ demand driven deep brain stimulator design. J Neural Eng 10(3):36019. doi:10.1088/1741-2560/10/3/036019 CrossRefGoogle Scholar
  4. 4.
    Birdno MJ, Kuncel AM, Dorval AD, Turner DA, Grill WM (2008) Tremor varies as a function of the temporal regularity of deep brain stimulation. NeuroReport 19(5):599–602CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Chaturvedi A, Foutz TJ, McIntyre CC (2012) Current steering to activate targeted neural pathways during deep brain stimulation of the subthalamic region. Brain Stimul 5(3):369–377. doi:10.1016/j.brs.2011.05.002 CrossRefPubMedGoogle Scholar
  6. 6.
    Contarino MF, Lo Bour J, Verhagen R, Lourens MAJ, de Bie Rob M A, van den Munckhof P et al (2014) Directional steering: a novel approach to deep brain stimulation. Neurology 83(13):1163–1169. doi:10.1212/WNL.0000000000000823 CrossRefPubMedGoogle Scholar
  7. 7.
    Elble RJ, Pullman SL, Matsumoto JY, Raethjen J, Deuschl G, Tintner R (2006) Tremor amplitude is logarithmically related to 4- and 5-point tremor rating scales. Brain J Neurol 129(Pt 10):2660–2666. doi:10.1093/brain/awl190 CrossRefGoogle Scholar
  8. 8.
    Gantert C, Honerkamp J, Timmer J (1992) Analyzing the dynamics of hand tremor time series. Biol Cybern 66(6):479–484CrossRefPubMedGoogle Scholar
  9. 9.
    Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P et al (2008) Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord Off J Mov Disord Soc 23(15):2129–2170. doi:10.1002/mds.22340 CrossRefGoogle Scholar
  10. 10.
    Greenwald E, Masters MR, Thakor NV (2016) Implantable neurotechnologies: bidirectional neural interfaces-applications and VLSI circuit implementations. Med Biol Eng Comput 54(1):1–17. doi:10.1007/s11517-015-1429-x CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Griffiths RI, Kotschet K, Arfon S, Xu ZM, Johnson W, Drago J et al (2012) Automated assessment of bradykinesia and dyskinesia in Parkinson’s disease. J Parkinson’s Dis 2(1):47–55. doi:10.3233/JPD-2012-11071 Google Scholar
  12. 12.
    Hemm S, Wårdell K (2010) Stereotactic implantation of deep brain stimulation electrodes: a review of technical systems, methods and emerging tools. Med Biol Eng Comput 48(7):611–624. doi:10.1007/s11517-010-0633-y CrossRefPubMedGoogle Scholar
  13. 13.
    Jankovic J, Frost JD (1981) Quantitative assessment of parkinsonian and essential tremor: clinical application of triaxial accelerometry. Neurology 31(10):1235. doi:10.1212/WNL.31.10.1235 CrossRefPubMedGoogle Scholar
  14. 14.
    Journee HL, Postma AA, Staal MJ (2007) Intraoperative neurophysiological assessment of disabling symptoms in DBS surgery. Neurophysiol Clin Clin Neurophysiol 37(6):467–475. doi:10.1016/j.neucli.2007.10.006 CrossRefGoogle Scholar
  15. 15.
    Journée HL, Postma AA, Sun M, Staal MJ (2008) Detection of tremor bursts by a running second order moment function and analysis using interburst histograms. Med Eng Phys 30(1):75–83. doi:10.1016/j.medengphy.2006.12.005 CrossRefPubMedGoogle Scholar
  16. 16.
    Lang AE, Widner H (2002) Deep brain stimulation for Parkinson’s disease: patient selection and evaluation. Mov Disord 17(S3):S94–S101. doi:10.1002/mds.10149 CrossRefPubMedGoogle Scholar
  17. 17.
    Lauk M, Timmer J, Guschlbauer B, Hellwig B, Lücking CH (2001) Variability of frequency and phase between antagonistic muscle pairs in pathological human tremors. Muscle Nerve 24(10):1365–1370CrossRefPubMedGoogle Scholar
  18. 18.
    Mansur PHG, Cury LKP, Andrade AO, Pereira AA, Miotto GAA, Soares AB et al (2007) A review on techniques for tremor recording and quantification. Crit Rev Biomed Eng 35(5):343–362CrossRefPubMedGoogle Scholar
  19. 19.
    Martens HCF, Toader E, Decré MMJ, Anderson DJ, Vetter R, Kipke DR et al (2011) Spatial steering of deep brain stimulation volumes using a novel lead design. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 122(3):558–566. doi:10.1016/j.clinph.2010.07.026 CrossRefGoogle Scholar
  20. 20.
    Meigal AY, Rissanen SM, Tarvainen MP, Georgiadis SD, Karjalainen PA, Airaksinen O et al (2012) Linear and nonlinear tremor acceleration characteristics in patients with Parkinson’s disease. Physiol Meas 33(3):395–412. doi:10.1088/0967-3334/33/3/395 CrossRefPubMedGoogle Scholar
  21. 21.
    Meldrum SJ, Watson BW (1970) Tremor recording in Parkinson’s disease. Phys Med Biol 15(2):249–254. doi:10.1088/0031-9155/15/2/302 CrossRefPubMedGoogle Scholar
  22. 22.
    Mera T, Vitek JL, Alberts JL, Giuffrida JP (2011) Kinematic optimization of deep brain stimulation across multiple motor symptoms in Parkinson’s disease. J Neurosci Methods 198(2):280–286. doi:10.1016/j.jneumeth.2011.03.019 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Moore GP, Ding L, Bronte-Stewart HM (2000) Concurrent Parkinson tremors. J Physiol 529(Pt 1):273–281CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Morishita T, Foote KD, Wu SS, Jacobson CE, Rodriguez RL, Haq IU et al (2010) Brain penetration effects of microelectrodes and deep brain stimulation leads in ventral intermediate nucleus stimulation for essential tremor. J Neurosurg 112(3):491–496. doi:10.3171/2009.7.JNS09150 CrossRefPubMedGoogle Scholar
  25. 25.
    O’Suilleabhain PE, Matsumoto JY (1998) Time-frequency analysis of tremors. Brain J Neurol 121(Pt 11):2127–2134CrossRefGoogle Scholar
  26. 26.
    Palmer JL, Coats MA, Roe CM, Hanko SM, Xiong C, Morris JC (2010) Unified Parkinson’s disease rating scale-motor exam: inter-rater reliability of advanced practice nurse and neurologist assessments. J Adv Nurs 66(6):1382–1387. doi:10.1111/j.1365-2648.2010.05313.x CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Papapetropoulos S, Jagid JR, Sengun C, Singer C, Gallo BV (2008) Objective monitoring of tremor and bradykinesia during DBS surgery for Parkinson disease. Neurology 70(15):1244–1249. doi:10.1212/01.wnl.0000308936.27780.94 CrossRefPubMedGoogle Scholar
  28. 28.
    Papapetropoulos S, Katzen HL, Scanlon BK, Guevara A, Singer C, Levin BE (2010) Objective quantification of neuromotor symptoms in Parkinson’s disease: implementation of a portable, computerized measurement tool. Parkinson’s Dis 2010:760196. doi:10.4061/2010/760196 Google Scholar
  29. 29.
    Patel S, Lorincz K, Hughes R, Huggins N, Growdon J, Standaert D et al (2009) Monitoring motor fluctuations in patients with Parkinson’s disease using wearable sensors. IEEE Trans Inf Technol Biomed Publ IEEE Eng Med Biol Soc 13(6):864–873. doi:10.1109/TITB.2009.2033471 CrossRefGoogle Scholar
  30. 30.
    Perera T, Yohanandan SAC, McDermott HJ (2015) A simple and inexpensive test-rig for evaluating the performance of motion sensors used in movement disorders research. Med Biol Eng Comput 54(2–3):333–339. doi:10.1007/s11517-015-1314-7 PubMedGoogle Scholar
  31. 31.
    Pollo C, Kaelin-Lang A, Oertel MF, Stieglitz L, Taub E, Fuhr P et al (2014) Directional deep brain stimulation: an intraoperative double-blind pilot study. Brain J Neurol 137(Pt 7):2015–2026. doi:10.1093/brain/awu102 CrossRefGoogle Scholar
  32. 32.
    Popović Maneski L, Jorgovanović N, Ilić V, Došen S, Keller T, Popović MB et al (2011) Electrical stimulation for the suppression of pathological tremor. Med Biol Eng Comput 49(10):1187–1193. doi:10.1007/s11517-011-0803-6 CrossRefPubMedGoogle Scholar
  33. 33.
    Post B, Merkus MP, de Bie Rob M A, de Haan Rob J, Speelman JD (2005) Unified Parkinson’s disease rating scale motor examination: are ratings of nurses, residents in neurology, and movement disorders specialists interchangeable? Mov Disord Off J Mov Disord Soc 20(12):1577–1584. doi:10.1002/mds.20640 CrossRefGoogle Scholar
  34. 34.
    Pulliam CL, Heldman DA, Orcutt TH, Mera TO, Giuffrida JP, Vitek JL (2015) Motion sensor strategies for automated optimization of deep brain stimulation in Parkinson’s disease. Parkinsonism Rel Disord 21(4):378–382. doi:10.1016/j.parkreldis.2015.01.018 CrossRefGoogle Scholar
  35. 35.
    Rissanen SM, Kankaanpää M, Meigal A, Tarvainen MP, Nuutinen J, Tarkka IM et al (2008) Surface EMG and acceleration signals in Parkinson’s disease: feature extraction and cluster analysis. Med Biol Eng Comput 46(9):849–858. doi:10.1007/s11517-008-0369-0 CrossRefPubMedGoogle Scholar
  36. 36.
    Rissanen SM, Kankaanpaä M, Tarvainen MP, Novak V, Novak P, Hu K et al (2011) Analysis of EMG and acceleration signals for quantifying the effects of deep brain stimulation in Parkinson’s disease. IEEE Trans Biomed Eng 58(9):2545–2553. doi:10.1109/TBME.2011.2159380 CrossRefPubMedGoogle Scholar
  37. 37.
    Riviere CN, Reich SG, Thakor NV (1997) Adaptive Fourier modeling for quantification of tremor. J Neurosci Methods 74(1):77–87CrossRefPubMedGoogle Scholar
  38. 38.
    Rocon E, Pons JL, Andrade AO, Nasuto SJ (2006) Application of EMD as a novel technique for the study of tremor time series. In: Conference proceedings: annual international conference of the IEEE engineering in medicine and biology society. IEEE engineering in medicine and biology society. Annual conference, Supplementary, pp 6533–6536. doi:10.1109/IEMBS.2006.260871
  39. 39.
    Sarem-Aslani A, Mullett K (2011) Industrial perspective on deep brain stimulation: history, current state, and future developments. Front Integr Neurosci. doi:10.3389/fnint.2011.00046 PubMedPubMedCentralGoogle Scholar
  40. 40.
    Senova S, Querlioz D, Thiriez C, Jedynak P, Jarraya B, Palfi S (2015) Using the accelerometers integrated in smartphones to evaluate essential tremor. Stereotact Funct Neurosurg 93(2):94–101. doi:10.1159/000369354 CrossRefPubMedGoogle Scholar
  41. 41.
    Shah A, Coste J, Lemaire J-J, Schkommodau E, Hemm-Ode S (2013) A method to quantitatively evaluate changes in tremor during deep brain stimulation surgery. In: 6th international IEEE/EMBS conference on neural engineering, pp 1202–1205. doi:10.1109/NER.2013.6696155
  42. 42.
    Shah AA, Coste J, Lemaire J-J, Ulla M, Schkommodau E, Hemm-Ode S (2014) Using acceleration sensors to quantify symptoms during deep brain stimulation surgery: poster presentations. Mov Disord 29(S1):30. doi:10.1002/mds.25914 Google Scholar
  43. 43.
    Shamir RR, Eitan R, Sheffer S, Marmor-Levin O, Valsky D, Moshel S et al (2013). Intra-operative identification of the subthalamic nucleus motor zone using goniometers. In Hutchison D, Kanade T, Kittler J, Kleinberg JM, Mattern F, Mitchell JC et al (eds) Information processing in computer-assisted interventions, vol 7915. Lecture notes in computer science). Springer, Berlin, pp 21–29Google Scholar
  44. 44.
    Sowman PF, Türker KS (2005) Methods of time and frequency domain examination of physiological tremor in the human jaw. Hum Mov Sci 24(5–6):657–666. doi:10.1016/j.humov.2005.09.003 CrossRefPubMedGoogle Scholar
  45. 45.
    Spearman C (1904) The Proof and measurement of association between two things. Am J Psychol 15(1):72. doi:10.2307/1412159 CrossRefGoogle Scholar
  46. 46.
    Stacy M (2009) Medical treatment of Parkinson disease. Neurol Clin 27(3):605–631. doi:10.1016/j.ncl.2009.04.009 CrossRefPubMedGoogle Scholar
  47. 47.
    Sturman MM, Vaillancourt DE, Metman LV, Bakay RAE, Corcos DM (2004) Effects of subthalamic nucleus stimulation and medication on resting and postural tremor in Parkinson’s disease. Brain J Neurol 127(Pt 9):2131–2143. doi:10.1093/brain/awh237 CrossRefGoogle Scholar
  48. 48.
    Tarvainen M, Ranta-aho P, Karjalainen P (2002) An advanced detrending method with application to HRV analysis. IEEE Trans Biomed Eng 49(2):172–175. doi:10.1109/10.979357 CrossRefPubMedGoogle Scholar
  49. 49.
    Veluvolu KC, Ang WT (2011) Estimation of physiological tremor from accelerometers for real-time applications. Sensors 11(12):3020–3036. doi:10.3390/s110303020 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Wilcoxon F (1945) Individual comparisons by ranking methods. Biom Bull 1(6):80–83CrossRefGoogle Scholar

Copyright information

© International Federation for Medical and Biological Engineering 2016

Authors and Affiliations

  • Ashesh Shah
    • 1
  • Jérôme Coste
    • 2
    • 3
  • Jean-Jacques Lemaire
    • 2
    • 3
  • Ethan Taub
    • 4
  • W. M. Michael Schüpbach
    • 5
    • 6
  • Claudio Pollo
    • 7
  • Erik Schkommodau
    • 1
  • Raphael Guzman
    • 4
  • Simone Hemm-Ode
    • 1
  1. 1.Institute for Medical and Analytical TechnologiesUniversity of Applied Sciences and Arts Northwestern SwitzerlandMuttenzSwitzerland
  2. 2.Image-Guided Clinical Neuroscience and Connectomics (EA 7282)Université Clermont AuvergneClermont-FerrandFrance
  3. 3.Service de NeurochirurgieCHU Clermont-FerrandClermont-FerrandFrance
  4. 4.Departments of Neurosurgery and BiomedicineUniversity of BaselBaselSwitzerland
  5. 5.Department of NeurologyUniversity Hospital Bern and University of BernBernSwitzerland
  6. 6.Assistance Publique Hôpitaux de Paris, Institut National de Santé et en Recherche Médicale, Institut du Cerveau et de la Moelle Epinière, Centre d’Investigation Clinique 1422, Département de NeurologieHôpital Pitié-SalpêtrièreParisFrance
  7. 7.Department of NeurosurgeryUniversity Hospital BernBernSwitzerland

Personalised recommendations