Abstract
Parkinson’s disease (PD) presents several motor signs, including tremor and bradykinesia. However, these signs can also be found in other motor disorders and in neurologically healthy older adults. The incidence of bradykinesia in PD is relatively high in all stages of the disorder, even when compared to tremor. Thus, this research proposes an objective assessment of bradykinesia in patients with PD (G PD: 15 older adults with Parkinson’s disease, 65.3 ± 9.1 years) and older adults (G HV: 12 healthy older adults, 60.1 ± 6.1 years). The severity of bradykinesia in the participants of G PD was assessed using the Unified Parkinson’s Disease Rating Scale. Movement and muscular activity were detected by means of inertial (accelerometer, gyroscope, magnetometer) and electromyographic sensors while the participants performed wrist extension against gravity with the forearm on pronation. Mean and standard error of inertial and electromyographic signal parameters could discriminate PD patients from healthy older adults (p value <0.05). In discriminating patients with PD from healthy older adults, the mean sensitivity and specificity were respectively 86.67 and 83.33%. The discrimination between the groups, based on the objective evaluation of bradykinesia, may contribute to the accurate diagnosis of PD and to the monitoring of therapies to control parkinsonian bradykinesia, and opens the possibility for further comparative studies considering individuals suffering from other motor disorders.
Similar content being viewed by others
Notes
UPDRS Item 24 Hand Movements: patient opens and closes hands in rapid succession. UPDRS Item 25 Rapid Alternating Movements of Hands: pronation-supination movements of hands, vertically and horizontally, with as large an amplitude as possible, both hands simultaneously.
References
Baldissera, F., P. Cavallari, G. Marini, and G. Tassone. Differential control of in-phase and anti-phase coupling of rhythmic movements of ipsilateral hand and foot. Exp. Brain Res. 83:375–380, 1991.
Beeler, J. A., T. Shiner, B. Seymour, M. Symmonds, P. Dayan, K. P. Bhatia, and R. J. Dolan. The effect of motivation on movement: a study of bradykinesia in Parkinson’s disease. PLoS ONE 7:e47138, 2012.
Bennett, D. A., L. A. Beckett, A. M. Murray, K. M. Shannon, C. G. Goetz, D. M. Pilgrim, and D. A. Evans. Prevalence of parkinsonian signs and associated mortality in a community population of older people. N. Engl. J. Med. 334:71–76, 1996.
Biswas, D., A. Cranny, N. Gupta, K. Maharatna, J. Achner, J. Klemke, M. Jöbges, and S. Ortmann. Recognizing upper limb movements with wrist worn inertial sensors using k-means clustering classification. Hum. Mov. Sci. 40:59–76, 2015.
Bloem, B. R., D. J. Beckley, J. G. van Dijk, A. H. Zwinderman, M. P. Remler, and R. A. C. Roos. Influence of dopaminergic medication on automatic postural responses and balance impairment in Parkinson’s disease. Mov. Disord. 11:509–521, 1996.
Buchman, A. S., R. S. Wilson, J. M. Shulman, S. E. Leurgans, J. A. Schneider, and D. A. Bennett. Parkinsonism in older adults and its association with adverse health outcomes and neuropathology. J Gerontol A 71:549–556, 2016.
Cover, T., and P. Hart. Nearest neighbor pattern classification. IEEE Trans. Inf. Theory 13:21–27, 1967.
Dai H. and L. T. D’Angelo. A portable system for quantitative assessment of parkinsonian bradykinesia during deep-brain stimulation surgery. In: 2013 2nd International Conference on Advances in Biomedical Engineering (ICABME), p. 77–80, 2013.
Dai, H., H. Lin, and T. C. Lueth. Quantitative assessment of parkinsonian bradykinesia based on an inertial measurement unit. BioMed. Eng. OnLine 14:1–13, 2015.
Dai, H., B. Otten, J. H. Mehrkens, L. T. D. Angelo, and T. C. Lueth. A novel glove monitoring system used to quantify neurological symptoms during deep-brain stimulation surgery. IEEE Sens. J. 13:3193–3202, 2013.
Dai, H., P. Zhang, and T. Lueth. Quantitative assessment of parkinsonian tremor based on an inertial measurement unit. Sensors 15:25055–25071, 2015.
Davis, K. L., H. M. Edin, and J. K. Allen. Prevalence and cost of medication nonadherence in Parkinson’s disease: evidence from administrative claims data. Mov. Disord. 25:474–480, 2010.
Espay, A. J., P. Bonato, F. B. Nahab, W. Maetzler, J. M. Dean, J. Klucken, B. M. Eskofier, A. Merola, F. Horak, A. E. Lang, R. Reilmann, J. Giuffrida, A. Nieuwboer, M. Horne, M. A. Little, I. Litvan, T. Simuni, E. R. Dorsey, M. A. Burack, K. Kubota, A. Kamondi, C. Godinho, J.-F. Daneault, G. Mitsi, L. Krinke, J. M. Hausdorff, B. R. Bloem, and S. Papapetropoulos. Technology in Parkinson’s disease: challenges and opportunities. Mov. Disord. 31:1272–1282, 2016.
Giuffrida, J., and E. Rapp. Ambulatory and remote monitoring of Parkinson’s disease motor symptoms. In: Healthcare sensor networks—challenges toward practical implementation, edited by R. Lai, D. T. H. Palaniswami, and M. Begg. Boca Raton: CRC Press, 2011, pp. 247–282.
Goetz, C. G., B. C. Tilley, S. R. Shaftman, G. T. Stebbins, S. Fahn, P. Martinez-Martin, W. Poewe, C. Sampaio, M. B. Stern, R. Dodel, B. Dubois, R. Holloway, J. Jankovic, J. Kulisevsky, A. E. Lang, A. Lees, S. Leurgans, P. A. LeWitt, D. Nyenhuis, C. W. Olanow, O. Rascol, A. Schrag, J. A. Teresi, J. J. van Hilten, N. LaPelle, and U. R. T. F. Movement Disorder Society. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov. Disord. 23:2129–2170, 2008.
Heldman, D. A., J. P. Giuffrida, R. Chen, M. Payne, F. Mazzella, A. P. Duker, A. Sahay, S. J. Kim, F. J. Revilla, and A. J. Espay. The modified bradykinesia rating scale for Parkinson’s disease: reliability and comparison with kinematic measures. Mov. Disord. 26:1859–1863, 2012.
Hindle, J. V. Ageing, neurodegeneration and Parkinson’s disease. Age Ageing 39:156–161, 2010.
Johnson, M. T. V., A. N. Kipnis, M. C. Lee, R. B. Loewenson, and T. J. Ebner. Modulation of the stretch reflex during volitional sinusoidal tracking in Parkinson’s disease. Brain 114:443–460, 1991.
Jun, J.-H., J.-W. Kim, Y. Kwon, G.-M. Eom, S.-B. Koh, B. Lee, H.-S. Kim, J.-H. Yi, and G.-R. Tack. Quantification of limb Bradykinesia in patients with Parkinson’ s disease using a gyrosensor—improvement and validation. Int. J. Precis. Eng. Manuf. 12:557–563, 2011.
Kempster, P. A., B. Hurwitz, and A. J. Lees. A new look at James Parkinson’s essay on the shaking palsy. Neurology 69:482–485, 2007.
Kim, J. W., J. H. Lee, Y. Kwon, C. S. Kim, G. M. Eom, S. B. Koh, D. Y. Kwon, and K. W. Park. Quantification of bradykinesia during clinical finger taps using a gyrosensor in patients with Parkinson’s disease. Med. Biol. Eng. Comput. 49:365–371, 2011.
LeMoyne R., C. Coroian, and T. Mastroianni. Quantification of Parkinson’s disease characteristics using wireless accelerometers. In: 2009 IEEE/ICME International Conference on Complex Medical Engineering, pp. 1–5, 2009.
Machado, A. R. P., H. C. Zaidan, A. P. S. Paixão, et al. Feature visualization and classifiation for the discrimination between individuals with Parkinson’s disease under levodopa and DBS treatments. BioMed. Eng. OnLine 15:169, 2016.
Maetzler, W., R. P. Hubble, G. A. Naughton, P. A. Silburn, and M. H. Cole. Wearable sensor use for assessing standing balance and walking stability in people with Parkinson’s disease: a systematic review. PLoS ONE 10:e0123705, 2015.
Martinez-Manzanera, O., E. Roosma, M. Beudel, R. W. K. Borgemeester, T. V. Laar, and N. M. Maurits. A method for automatic and objective scoring of bradykinesia using orientation sensors and classification algorithms. IEEE Trans. Biomed. Eng. 63:1016–1024, 2016.
Martinez-Martin, P., A. Gil-Nagel, L. M. Gracia, J. Balseiro-Gomez, J. Martinez-Sarries, F. Bermejo, M. C. Jimenez-Rojas, E. Maranon, J. M. Grau Veciana, C. Roig Arnall, O. Bruna, C. Junque Plaja, S. Gimenez Roldan, and J. A. Burguera. Unified Parkinson’s disease rating scale characteristics and structure. Mov. Disord. 9:76–83, 1994.
Matsushita, N., Y. Handa, M. Ichie, and N. Hoshimiya. Electromyogram analysis and electrical stimulation control of paralysed wrist and hand. J. Electromyogr. Kinesiol. 5:117–128, 1995.
Mentzel, T. Q., C. L. Mentzel, S. V. Mentzel, R. Lieverse, H. A. M. Daanen, and P. N. V. Harten. Instrumental assessment of Bradykinesia: a comparison between motor tasks. IEEE J. Biomed. Health Inf. 20:521–526, 2016.
Moro, E., M. Scerrati, L. M. Romito, R. Roselli, P. Tonali, and A. Albanese. Chronic subthalamic nucleus stimulation reduces medication requirements in Parkinson’s disease. Neurology 53:85–90, 1999.
Niazmand K., K. Tonn, A. Kalaras, U. M. Fietzek, J. H. Mehrkens, and T. C. Lueth. Quantitative evaluation of Parkinson’s disease using sensor based smart Glove. In: 24th international symposium on computer-based medical systems. 978-971-4577-1189-4573, 2011.
Ramaker, C., J. Marinus, A. M. Stiggelbout, and B. J. V. Hilten. Systematic evaluation of rating scales for impairment and disability in Parkinson’ s disease. Mov. Disord. Soc. 17:867–876, 2002.
Rizzo, G., M. Copetti, S. Arcuti, D. Martino, A. Fontana, and G. Logroscino. Accuracy of clinical diagnosis of Parkinson disease: a systematic review and meta-analysis. Neurology 86:566–576, 2016.
Rosano, C., D. A. Bennett, A. B. Newman, V. Venkatraman, K. Yaffe, T. Harris, S. Kritchevsky, and H. J. Aizenstein. Patterns of focal gray matter atrophy are associated with bradykinesia and gait disturbances in older adults. J. Gerontol. A 67:957–962, 2012.
Salarian A., H. Russmann, F. J. G. Vingerhoets, P. R. Burkhard, Y. Blanc, C. Dehollain, and K. Aminian. An ambulatory system to quantify bradykinesia and tremor in Parkinson’s disease. In: 4th annual IEEE conference on information technology applications in biomedicine, pp. 35–38, 2003.
Salarian, A., H. Russmann, F. J. G. Vingerhoets, C. Dehollain, Y. Blanc, P. R. Burkhard, and K. Aminian. Gait assessment in Parkinson’s disease: toward an ambulatory system for long-term monitoring. IEEE Trans. Biomed. Eng. 51:1434–1443, 2004.
Salarian, A., H. Russmann, C. Wider, P. R. Burkhard, F. J. Vingerhoets, and K. Aminian. Quantification of tremor and bradykinesia in Parkinson’s disease using a novel ambulatory monitoring system. IEEE Trans. Biomed. Eng. 54:313–322, 2007.
Trojaniello, D., A. Cereatti, E. Pelosin, L. Avanzino, A. Mirelman, J. M. Hausdorff, and U. Della Croce. Estimation of step-by-step spatio-temporal parameters of normal and impaired gait using shank-mounted magneto-inertial sensors: application to elderly, hemiparetic, parkinsonian and choreic gait. J. NeuroEng. Rehab. 11:152, 2014.
Vrana, K. E., A. J. Noyce, A. Nagy, S. Acharya, S. Hadavi, J. P. Bestwick, J. Fearnley, A. J. Lees, and G. Giovannoni. Bradykinesia-Akinesia incoordination test: validating an online keyboard test of upper limb function. PLoS ONE 9:e96260, 2014.
Yang, K., W.-X. Xiong, F.-T. Liu, Y.-M. Sun, S. Luo, Z.-T. Ding, J.-J. Wu, and J. Wang. Objective and quantitative assessment of motor function in Parkinson’s disease—from the perspective of practical applications. Ann. Transl. Med. 4:90, 2016.
Yokoe, M., R. Okuno, T. Hamasaki, Y. Kurachi, K. Akazawa, and S. Sakoda. Opening velocity, a novel parameter, for finger tapping test in patients with Parkinson’s disease. Parkinsonism Relat. Disord. 15:440–444, 2009.
Acknowledgments
The present work was carried out with the support the National Council for Scientific and Technological Development (CNPq), Coordination of Improvement of Higher Level Personnel (CAPES), Foundation for Research Support of the State of Minas Gerais (FAPEMIG) and Foundation for Research Support of the State of Goiás (FAPEG). A. O. Andrade is a Fellow of CNPq, Brazil (305223/2014-3). The authors are thankful to the patients of the Parkinson’s Disease Association of Triângulo (Associação Parkinson do Triângulo, Uberlândia, Brazil) for their participation in this study.
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editor Leonidas D. Iasemidis oversaw the review of this article.
Rights and permissions
About this article
Cite this article
Rabelo, A.G., Neves, L.P., Paixão, A.P.S. et al. Objective Assessment of Bradykinesia Estimated from the Wrist Extension in Older Adults and Patients with Parkinson’s Disease. Ann Biomed Eng 45, 2614–2625 (2017). https://doi.org/10.1007/s10439-017-1908-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-017-1908-3