Postural Adjustments and Biomechanics During Gait Initiation and Obstacle Negotiation: A Comparison Between Akinetic-Rigid and Hyperkinetic Parkinson's Disease

Marcela Zimmermann Casal, Leonardo Alexandre Peyré-Tartaruga, Ana Paula Janner Zanardi, André Ivaniski-Mello, Lucas de Liz Alves, Aline Nogueira Haas, Flávia Gomes Martinez, Marcela Zimmermann Casal, Leonardo Alexandre Peyré-Tartaruga, Ana Paula Janner Zanardi, André Ivaniski-Mello, Lucas de Liz Alves, Aline Nogueira Haas, Flávia Gomes Martinez

Abstract

Background: Individuals with Parkinson's disease (PD) exhibit different combinations of motor symptoms. The most frequent subtypes are akinetic-rigid (AK-R) and hyperkinetic (HYP). Motor symptoms, such as rigidity and bradykinesia, can directly affect postural adjustments and performance in daily tasks, like gait initiation and obstacles negotiation, increasing the risk of falls and functional dependence. Objective: To compare postural adjustments and biomechanical parameters during the gait initiation and obstacle negotiation of people with AK-R and HYP PD and correlate with functional mobility and risk of falls. Methods: Cross-sectional study. Thirty-three volunteers with PD were divided into two groups according to clinical motor manifestations: AK-R (n = 16) and HYP (n = 17). We assessed the anticipatory (APA), compensatory (CPA) postural adjustments analyzing kinematic, kinetic and, electromyographic parameters during the gait initiation and obstacle negotiation tests. We applied independent T-tests and Pearson correlation tests for comparisons and correlations, respectively (α = 0.05). Results: In the APA phase of the gait initiation test, compared to the functional HYP group, the AK-R group showed shorter time for single support (p = 0.01), longer time for double support (p = 0.01) accompanied by a smaller first step (size, p = 0.05; height, p = 0.04), and reduced muscle activation of obliquus internus (p = 0.02). Similarly, during the first step in the obstacle negotiation test, the AK-R group showed less step height (p = 0.01) and hip excursion (p = 0.02), accompanied by a reduced mediolateral displacement of the center of pressure (p = 0.02) during APA, and activation of the gluteus medius (p = 0.02) and the anterior tibialis (p = 0.04) during CPA in comparison with HYP group. Conclusion: The findings suggest that people with AK-R present impaired postural adjustments during gait initiation and obstacles negotiation compared to hyperkinetic PD. Based on defined motor symptoms, the proposition presented here revealed consistent postural adjustments during complex tasks and, therefore, may offer new insights onto PD motor evaluation and neurorehabilitation.

Keywords: Parkinsonian disorders; electromyography; kinematic; locomotion; postural adjustments; stiffness.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Casal, Peyré-Tartaruga, Zanardi, Ivaniski-Mello, Alves, Haas and Martinez.

Figures

FIGURE 1
FIGURE 1
Timeline outlining course (left to right) of the gait initiation and obstacle negotiation tests: base activity, anticipatory postural adjustment (APA), start of movement during the APA (T0), compensatory postural adjustment (CPA), and task execution periods.
FIGURE 2
FIGURE 2
Single support time (% of stride time, A), double support time (% of stride time, B), first step size (cm, C), first step height (cm, D), and electromyographic activation of ipsilateral obliquus internus during anticipatory postural adjustment phase (μV, E) for akinetic-rigid (blue circles) and hyperkinetic (orange circles) groups in the gait initiation test. The Hedges’ g between akinetic-rigid and hyperkinetic is shown in the Gardner-Altman estimation plot. Both groups are plotted on the left axes; the mean difference is plotted on floating axes on the right as a bootstrap sampling distribution. The mean difference is depicted as a black circle; 95% confidence interval is indicated by the ends of the vertical error bar.
FIGURE 3
FIGURE 3
First step height (cm, A), range of hip motion (◯, B), anticipatory postural adjustment of mediolateral center of pressure displacement (cm, C), electromyographic activation of gluteus medius during compensatory postural adjustment phase (μV, D), electromyographic activation of tibialis anterior during compensatory postural adjustment phase (μV, E) for akinetic-rigid (blue circles) and hyperkinetic (orange circles) groups in the obstacle negotiation test. The Hedges’ g between akinetic-rigid and hyperkinetic is shown in the Gardner-Altman estimation plot. Both groups are plotted on the left axes; the mean difference is plotted on floating axes on the right as a bootstrap sampling distribution. The mean difference is depicted as a black circle. 95% confidence interval is indicated by the ends of the vertical error bar.

References

    1. Assaiante C., Woollacott M., Amblard B. (2000). Development of postural adjustment during gait initiation: kinematic and EMG analysis. J. Mot. Behav. 32 211–226. 10.1080/00222890009601373
    1. Bischoff H., Stähelin H., Monsch A., Iversen M., Weyh A., Von Dechend M. (2003). Identifying a cut-off point for normal mobility: a comparison of the timed ‘up and go’ test in community- dwelling and institutionalized elderly women. Age Ageing 32 315–320. 10.1093/ageing/32.3.315
    1. Bonora G., Mancini M., Carpinella I., Chiari L., Ferrarin M., Nutt J., et al. (2017). Investigation of anticipatory postural adjustments during one-leg stance using inertial sensors: evidence from subjects with parkinsonism. Front. Neurol. 25:361. 10.3389/fneur.2017.00361
    1. Carpinella I., Crenna P., Calabrese E., Rabuffetti M., Mazzoleni P., Nemni R., et al. (2007). Locomotor function in the early stage of Parkinson’s disease. IEEE Trans. Neural Syst. Rehabil. Eng. 15 543–551. 10.1109/TNSRE.2007.908933
    1. Chang H., Chuang T., Lee S., Shih I., Cheng H. (2004). Temporal differences in relative phasing of gait initiation and first step length in patients with cervical and lumbosacral spinal cord injuries. Spinal Cord 42 281–289. 10.1038/sj.sc.3101587
    1. Conceição N., Sousa P., Pereira M., Gobbi L., Vitorio R. (2019). Utility of center of pressure measures during obstacle crossing in prediction of fall risk in people with Parkinson’s disease. Hum. Mov. Sci. 66 1–8. 10.1016/j.humov.2019.03.010
    1. Delafontaine A., Vialleron T., Hussein T., Yiou E., Honeine J. L., Colnaghi S. (2019). Anticipatory postural adjustments during gait initiation in stroke patients. Front. Neurol. 10:352. 10.3389/fneur.2019.00352
    1. Delval A., Tard C., Defebvre L. (2014). Why we should study gait initiation in Parkinson’s disease. Clin. Neurophysiol. 44 69–76. 10.1016/j.neucli.2013.10.127
    1. Dibble L., Nicholson D., Shultz B., Macwilliams B., Marcus R., Moncur C. (2004). Sensory cueing effects on maximal speed gait initiation in persons with Parkinson’s disease and healthy elders. Gait Posture 19 215–225. 10.1016/S0966-6362(03)00065-1
    1. Dickstein R., Shefi S., Marcovitz E., Villa Y. (2004). Anticipatory postural adjustment in selected trunk muscles in poststroke hemiparetic patients. Arch. Phys. Med. Rehabil. 85 261–267. 10.1016/j.apmr.2003.05.011
    1. Di Giulio I., Maganaris C., Baltzopoulos V., Loram I. (2009). The proprioceptive and agonist roles of gastrocnemius, soleus and tibialis anterior muscles in maintaining human upright posture. J. Physiol. 587 2399–2416. 10.1113/jphysiol.2009.168690
    1. Eggers C., Kahraman D., Fink G., Schmidt M., Timmermann L. (2011). Akinetic-rigid and tremor-dominant Parkinson’s disease patients show different patterns of FP-CIT Single photon emission computed tomography. Mov. Disord. 26 416–423. 10.1002/mds.23468
    1. Esposti R., Limonta E., Esposito F., Baldissera F. G. (2013). The role of anticipatory postural adjustments in interlimb coordination of coupled arm movements in the parasagittal plane: III. Difference in the energy cost of postural actions during cyclic flexion–extension arm movements, ISO- and ANTI-directionally coupled. Exp. Brain Res. 231 293–303. 10.1007/s00221-013-3691-1
    1. Gantchev N., Viallet F., Aurenty R., Massion J. (1996). Impairment of posturo-kinetic coordination during initiation of forward oriented stepping movements in parkinsonian patients. Electroencephalogr. Clin. Neurophysiol. 101 110–120. 10.1016/0924-980x(95)00253-h
    1. Grissom R. J., Kim J. J. (2005). Effect Sizes for Research: A Broad Practical Approach. Mahwah, NJ: Lawrence Erlbaum Associates.
    1. Guimarães M., Severino V., Pinheiro H. (2013). Correlation between functionality and severity of Parkinson’s disease in the elderly. Geriatr. Gerontol. Aging 7 203–207.
    1. Halliday S., Winter D., Frank J. (1998). The initiation of gait in young, elderly, and Parkinson’s disease subjects. Gait Posture 8 8–14. 10.1016/s0966-6362(98)00020-4
    1. Hass C., Waddell D., Fleming R., Juncos J., Gregor R. (2005). Gait initiation and dynamic balance control in Parkinson’s disease. Arch. Phys. Med. Rehabil. 86 2172–2176. 10.1016/j.apmr.2005.05.013
    1. Hass C., Waddell D., Wolf S., Juncos J., Gregor R. (2008). Gait initiation in older adults with postural instability. Clin. Biomech. 23 743–753. 10.1016/j.clinbiomech.2008.02.012
    1. Hausdorff J., Schaafsma J., Balash Y., Bartels A., Gurevich T., Giladi N. (2003). Impaired regulation of stride variability in Parkinson’s disease subjects with freezing of gait. Exp. Brain Res. 149 187–194. 10.1007/s00221-002-1354-8
    1. Hodges P., Richardson C. (1997). Contraction of the abdominal muscles associated with movement of the lower limb. Phys. Ther. 77 132–142. 10.1093/ptj/77.2.132
    1. Hoehn M., Yahr M. (1967). Parkinsonism: onset, progression and mortality. Neurology 17 427–442. 10.1212/wnl.17.5.427
    1. Iansek R., Huxham F., Mcginley J. (2006). The sequence effect and gait festination in Parkinson disease: Contributors to freezing of gait? Mov. Disord. 21 1419–1424. 10.1002/mds.20998
    1. Jacobs J., Henry S., Nagle K. (2008). People with chronic low back pain exhibit decreased variability in the timing of their anticipatory postural adjustments. Behav. Neurosci. 132 455–458. 10.1037/a0014479
    1. Jacobs J., Lou J., Kraakevik J., Horak F. (2009). The supplementary motor area contributes to the timing of the anticipatory postural adjustment during step initiation in participants with and without Parkinson’s disease. Neuroscience 164 877–885. 10.1016/j.neuroscience.2009.08.002
    1. Jankovic J., Mcdermott M., Carter J., Gauthier S., Goetz C., Golbe L., et al. (1990). Variable expression of Parkinson’s disease: a base-line analysis of the DATATOP cohort: the parkinson study group. Neurology 40 1529–1534. 10.1212/wnl.40.10.1529
    1. Jankovic J., Kapadia A. (2001). Functional decline in parkinson disease. JAMA Neurol. 58 1611–1615. 10.1001/archneur.58.10.1611
    1. Jellinger K. (1999). Post mortem studies in Parkinson’s disease - is it possible to detect brain areas for specific symptoms? J. Neural Transm. Suppl. 56 1–29. 10.1007/978-3-7091-6360-3_1
    1. Kim H. D., Jae H. D., Jeong J. H. (2014). Tai Chi Exercise can improve the obstacle negotiating ability of people with Parkinson’s disease: a preliminary study. J. Phys. Ther. Sci. 26 1025–1030. 10.1589/jpts.26.1025
    1. Kirker S., Simpson D., Jenner J., Wing A. (2000). Stepping before standing: hip muscle function in stepping and standing balance after stroke. J. Neurol. Neurosurg. Psychiatry 68 458–464. 10.1136/jnnp.68.4.458
    1. Krishnan V., Latash M., Aruin A. (2012). Early and late components of feed-forward postural adjustments to predictable perturbations. Clin. Neurophysiol. 123 1016–1026. 10.1016/j.clinph.2011.09.014
    1. Latash M., Aruin A., Neyman I., Nicholas J. (1995). Anticipatory postural adjustments during self-inflicted and predictable perturbations in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 53 326–334. 10.1136/jnnp.58.3.326
    1. Lees A., Hardy J., Revesz T. (2009). Parkinson’s disease. Lancet 373 2055–2066. 10.1016/S0140-6736(09)60492-X
    1. León-Jiménez C. (2019). Síndrome rígido acinético. Rev. Med. Clin. 3 104–108.
    1. Lewis M., Du G., Sen S., Kawaguchi A., Truong Y., Lee S., et al. (2011). Differential involvement of striato and cerebello-thalamocortical pathways in tremor and akinetic/rigid-predominant Parkinson’s disease. Neuroscience 177 230–239. 10.1016/j.neuroscience.2010.12.060
    1. Lyon I., Day B. (1997). Control of frontal plane body motion in human stepping. Exp. Brain Res. 115 345–356. 10.1007/pl00005703
    1. Mancini M., Zampieri C., Carlson-Kuhta P., Chiari L., Horak F. (2009). Anticipatory postural adjustments prior to step initiation are hypometric in untreated Parkinson’s disease: an accelerometer-based approach. Eur. J. Neurol. 16 1028–1034. 10.1111/j.1468-1331.2009.02641.x
    1. Marras C., Rochon P., Lang A. E. (2002). Predicting motor decline and disability in Parkinson disease: a systematic review. Arch. Neurol. 59 1724–1728. 10.1001/archneur.59.11.1724
    1. Mellroy W., Maki B. (1999). The control of lateral stability during rapid stepping reactions evoked by antero-posterior perturbation: does anticipatory control play a role? Gait Posture 9 190–198. 10.1016/s0966-6362(99)00013-2
    1. Merletti R., Rainoldi A., Farina D. (2001). Surface electromyography for non-invasive characterization of muscle. Exerc. Sport Sci. Rev. 29 20–25. 10.1097/00003677-200101000-00005
    1. Mickelborough J., Van Der Linden M., Tallis R. C., Ennos A. (2004). Muscle activity during gait initiation in normal elderly people. Gait Posture 19 50–57. 10.1016/s0966-6362(03)00016-x
    1. Monteiro E. P., Franzoni L. T., Cubillos D. M., de Oliveira Fagundes A., Carvalho A. R., Oliveira H. B., et al. (2017). Effects of Nordic walking training on functional parameters in Parkinson’s disease: a randomized controlled clinical trial. Scand. J. Med. Sci. Sports. 27 351–358. 10.1111/sms.12652
    1. Morris M., Iansek R., Matyas T., Summers J. (1996). Stride length regulation in Parkinson’s disease: normalization strategies and underlying mechanisms. Brain 119 551–568. 10.1093/brain/119.2.551
    1. Morris M., Iansek R., McGinley J., Matyas T., Huxham F. (2005). Three-dimensional gait biomechanics in Parkinson’s disease: evidence for a centrally mediated amplitude regulation disorder. Mov. Disord. 20 40–50. 10.1002/mds.20278
    1. Morris S., Morris M., Iansek R. (2001). Reliability of measurements obtained with the timed “Up & Go” test in people with Parkinson disease. Phys. Ther. 81 810–818. 10.1093/ptj/81.2.810
    1. Morris S., Alisson G. (2006). Effects of abdominal muscle fatigue on anticipatory postural adjustments associated with arm raising. Gait Posture 24 342–348. 10.1016/j.gaitpost.2005.10.011
    1. Okada Y., Fukumoto T., Takatori K., Nagino K., Hiraoka K. (2011). Variable initial swing side and prolonged double limb support represent abnormalities of the first three steps of gait initiation in patients with Parkinson’s disease with freezing of gait. Front. Neurol. 2:85. 10.3389/fneur.2011.00085
    1. Plate A., Klein K., Pelykh O., Singh A., Botzel K. (2016). Anticipatory postural adjustments are unaffected by age and are not absent in patients with the freezing of gait phenomenon. Exp. Brain Res. 234 2609–2618. 10.1007/s00221-016-4665-x
    1. Peterson D., Horak F. (2016). Neural control of walking in people with parkinsonism. Physiology 126 95–107. 10.1152/physiol.00034.2015
    1. Rajput A., Voll A., Rajput M., Robinson C., Rajput A. (2009). Course in Parkinson disease subtypes a 39-year clinicopathologic study. Neurology 73 206–212. 10.1212/WNL.0b013e3181ae7af1
    1. Reichel G., Kirchhöfer U., Stenner A. (2001). Camptocormia–segmental dystonia. Proposal of a new definition for an old disease. Nervenarzt 72 281–285. 10.1007/s001150050751
    1. Rocchi L., Carlson-Kuhta P., Chiari L., Burchiel K., Hogarth P., Horak F. (2012). Effects of deep brain stimulation in the subthalamic nucleus or globus pallidus internus on step initiation in Parkinson disease. J. Neurosurg. 117 1141–1149. 10.3171/2012.8.JNS112006
    1. Roemmich R., Nocera J., Vallabhajosula S., Amano S., Naugle K., Stegemöller E., et al. (2012). Spatiotemporal variability during gait initiation in Parkinson’s disease. Gait Posture 36 340–343. 10.1016/j.gaitpost.2012.01.018
    1. Rosenthal J. (1996). Qualitative descriptors of strength of association and effect size. J. Soc. Serv. Res. 21 37–59. 10.1300/J079v21n04_02
    1. Rosin R., Topka H., Dichgans J. (1997). Gait initiation in parkinson’s disease. Mov. Disord. 12 682–690. 10.1002/mds.870120509
    1. Saghazadeh M., Tsunoda K., Okura T. (2014). Foot arch height and rigidity index associated with balance and postural sway in elderly women using a 3D foot scanner. Foot Ankle Online J. 7:1. 10.3827/faoj.2014.0704.0001
    1. Santos M., Kanekar N., Aruin A. (2010). The role of anticipatory postural adjustments in compensatory control of posture: 1. electromyography analysis. J. Electromyogr. Kinesiol. 20 388–397. 10.1016/j.jelekin.2009.06.006
    1. Scalzo P., Nova I., Perracini M., Sacramento D., Cardoso F., Ferraz H., et al. (2009). Validation of the Brazilian version of the Berg balance scale for patients with Parkinson’s disease. Arq. Neuropsiquiatr. 67 831–835. 10.1590/S0004-282X2009000500010
    1. Schaafsma J., Giladi N., Balash Y., Bartels A., Gurevich T., Hausdorff J. (2003). Gait dynamics in Parkinson’s disease: relationship to Parkinsonian features, falls and response to levodopa. J. Neurol. Sci. 12 47–53. 10.1016/s0022-510x(03)00104-7
    1. Schlenstedt C., Mancini M., Nutt J., Hiller A., Maetzler W., Deuschl G., et al. (2018). Are hypometric anticipatory postural adjustments contributing to freezing of gait in parkinson’s disease? Front. Aging Neurosci. 10:36. 10.3389/fnagi.2018.00036
    1. Tassorelli C., Furnari A., Buscone S., Alfonsi E., Pacchetti C., Zangaglia R., et al. (2012). Pisa syndrome in Parkinson’s disease: clinical, electromyographic, and radiological characterization. Mov. Disord. 27 227–235. 10.1002/mds.23930
    1. Tateuchi H., Ichihashi N., Shinya M., Oda S. (2011). Anticipatory adjustments during lateral step motion in patients with hip osteoarthritis. J. Appl. Biomech. 27 32–39. 10.1123/jab.27.1.32
    1. Tumas V., Borges V., Ballalai-Ferraz H., Zabetian C., Mata I., Brito M., et al. (2016). Some aspects of the validity of the montreal cognitive assessment (MoCA)for evaluating cognitive impairment in Brazilian patients with Parkinson’s disease. Dement. Neuropsychol. 10 333–338. 10.1590/S1980-5764-2016DN1004013
    1. Van Rooden S., Colas F., Martinez-Martin P., Visser M., Verbaan D., Marinus J., et al. (2011). Clinical subtypes of Parkinson’s disease. Mov. Disord. 26 51–58. 10.1002/mds.23346
    1. Vitório R., Pieruccini-Faria F., Stella F., Gobbi S., Gobbi L. (2010). Effects of obstacle height on obstacle crossing in mild Parkinson’s disease. Gait Posture 31 143–146. 10.1016/j.gaitpost.2009.09.011
    1. Watson M. (2002). Refining the ten-metre walking test for use with neurologically impaired people. Physiotherapy 88 386–397. 10.1016/S0031-9406(05)61264-3
    1. Winogrodzka A., Wagenaar R., Booij J., Wolters E. (2005). Rigidity and bradykinesia reduce interlimb coordination in Parkinsonian gait. Arch. Phys. Med. Rehabil. 86 183–189. 10.1016/j.apmr.2004.09.010
    1. Winter D., Mackinnon C., Ruder G., Wieman C. (1993). An integrated EMG/biomechanical model of upper body balance and posture during human gait. Prog. Brain Res. 97 359–367. 10.1016/s0079-6123(08)62295-5
    1. Winter D., Prince F., Frank J., Powell C., Zabjek K. (1996). Unified theory regarding A/P and M/L balance in quiet stance. J. Neurophysiol. 75 2334–2343. 10.1152/jn.1996.75.6.2334
    1. Winter D., Patla A., Ishac M., Gage W. (2003). Motor mechanisms of balance during quiet standing. J. Electromyogr. Kinesiol. 13 49–56. 10.1016/s1050-6411(02)00085-8
    1. Winter D. (2005). Biomechanics and Motor Control of Human Movement. New Jersey, NJ: John Wiley & Sons.
    1. Yardley L., Beyer N., Hauer K., Kempen G., Piot-ziegler C., Todd C. (2005). Development and initial validation of the falls efficacy scale-international (FES-I). Age Ageing 34 614–619. 10.1093/ageing/afi196
    1. Yelshyna D., Gago M., Bicho E., Fernandes V., Gago N., Costa L., et al. (2016). Compensatory postural adjustments in Parkinson’s disease assessed via a virtual reality environment. Behav. Brain Res. 1 384–392. 10.1016/j.bbr.2015.08.017
    1. Zanardi A. P. J., Martinez F. G., da Silva E. S., Casal M. Z., Martins V. F., Passos-Monteiro E., et al. (2019). Effects of nordic walking on gait symmetry in mild Parkinson’s disease. Symmetry 11:1481. 10.3390/sym11121481
    1. Zhang J., Wei L., Hu X., Xie B., Zhang Y., Wu G., et al. (2015). Akinetic-rigid and tremor-dominant Parkinson’s disease patients show different patterns of intrinsic brain activity. Parkinsonism Relat. Disord. 21 23–30. 10.1016/j.parkreldis.2014.10.017

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere