Neuroscience Letters 589 (2015) 181–184
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Research article
Self-perceived and actual ability in the functional reach test in patients with Parkinson’s disease Gilles Ryckewaert a,b , Marion Luyat d , Melanie Rambour a,b , Céline Tard a,c , Myriam Noël d , Luc Defebvre a,b , Arnaud Delval a,c,∗ a
Université de Lille, U1171, F-59037 Lille cedex, France Department of Neurology, Lille University Medical Center, F-59037 Lille cedex, France c Department of Clinical Neurophysiology, Lille University Medical Center, F-59037 Lille cedex, France d Université de Lille, EA 4072, F-59650 Villeneuve d’Ascq, France b
h i g h l i g h t s • • • •
Differences between self-perceived and actual ability to reach an object could lead to falls in PD patients. Functional reach test performance was altered in PD patients. Antero-posterior CoP displacement was reduced in PD and elderly subjects. Ability to estimate self-performance was preserved in PD patients and was not linked to future falls.
a r t i c l e
i n f o
Article history: Received 19 November 2014 Received in revised form 2 January 2015 Accepted 15 January 2015 Available online 16 January 2015 Keywords: Parkinson’s disease Posture Falls Functional reach test
a b s t r a c t Falls frequently occur during daily activities such as reaching for an object in patients with Parkinson’s disease (PD). Misjudgment is also reported to be one of the circumstances that lead to falls. The functional reach test is an indicator of dynamic balance. The primary objective was to establish whether there is a difference between self-perceived and actual ability to perform the functional reach test in patients with PD who have never fallen. Three groups of participants (all with no history of falls) were studied: young adults, elderly adults and PD patients. The participants first estimated their maximum reaching distance (but without performing the action, i.e. as a motor imagery task) and then actually performed the functional reach test (i.e. as a motor task). No significant overestimation or underestimation was observed. The reaching distance was lower in PD than in the two other groups. There were no differences between PD patients and elderly adults in terms of the forward centre of pressure displacement. Seven PD patients reported a fall in the year following the experiment. The fallers had a longer history of disease. Finally, PD patients adequately estimated their ability in the functional reach test and did not adopt an “at risk” strategy and appeared to be quite conservative (as were healthy elderly adults) in their postural control behavior. Ability to estimate self-performance is preserved in PD patients with no clinical impairments of postural control although they are at risk of future falls. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Patients with Parkinson’s disease (PD) have difficulty maintaining their balance when performing tasks such as reaching for an object while standing [1]. Falls occur commonly during reaching activities in PD patients [2,3]. Moreover, misjudgment and distrac-
∗ Corresponding author at: Clinical Neurophysiology Department, Hôpital Salengro, F-59037 Lille cedex, France. Tel.: +33 320 446 362; fax: +33 320 446 355. E-mail address: [email protected] (A. Delval). http://dx.doi.org/10.1016/j.neulet.2015.01.039 0304-3940/© 2015 Elsevier Ireland Ltd. All rights reserved.
tion are involved in 12% of reported falls. Fallers frequently reported that misjudgment, lack of concentration, and loss of balance had caused them to fall [4–6]. Indeed, disrupted representation of the external space and the environment is a possible perceptual component of the motor disorders in PD [7]. The maintenance of balance in tasks such as reaching a book on a wall-mounted shelf often requires postural adjustment. The most efficient means of ensuring balance under such conditions is visual perception of the environmental properties at a distance, prospective modification of movement patterns and thus avoidance of perturbation altogether. Affordances (defined as actions that are possible within
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an environment and within the context of the individual’s capacity) are prerequisites for prospective postural adjustments [8]. Some elderly adults fail to update internal models – prompting them to make over-optimistic predictions about upcoming actions [9]. In turn, this may favor “at risk” motor decision-making, and thus, promote falls [9]. This topic has not previously been investigated in patients with PD. The functional reach test (FRT) is a valid, reliable, clinical measure of dynamic balance developed by Duncan et al. [11–13]. In the FRT, the individual is asked to elevate his or her arm to shoulder’s height and then to perform a maximum forward reach. In elderly adults, a reaching distance (RD) of below 15 cm is associated with an increased risk of falls and frailty [11,13]. The FRT is also an indicator of dynamic balance: Duncan et al. [10] reported that the RD in the FRT is highly correlated with the centre of pressure (CoP) excursion [14]. The latter parameter (recorded on a force platform) is an indicator of dynamic balance and measures the limits of stability. Both CoP excursion and RD are inversely associated with recurrent falls and physical frailty [15,16]. However, young adults perform greater CoP displacements but also achieve a higher maximum forward RD while maintaining standing posture. The simple FRT has been found to be a reliable and precise estimate of postural instability. The functional RD can be analyzed separately or as an item in Berg’s Balance score [17], which might represent an “at risk” strategy in patients with postural instability. The FRT has also been validated in a group of individuals with PD (with or without a history of falls); Behrman et al. [15] demonstrated that a cut-off RD of 254 mm accurately identifies individuals at a high risk of falls (specificity: 92%; positive predictive value: 90%). The FRT is also of particular interest in advanced PD patients who appear unstable when reaching who are at risk of further falls [18]. The primary objective of the present study was to establish whether there is a difference between self-perceived and actual ability to perform the FRT in patients with PD who have never fallen. The secondary objective was to assess the participants’ limits of stability during the FRT and identify possible “at risk” strategies induced by the task. To this end, we studied CoP excursion during the FRT. One year after the experiment, a “phone survey” (notified to the participants in advance) provided information on whether or not the participants in the three groups had fallen during that period.
2. Material Two force platforms (OR6 from AMTI, Watertown, MA, USA, each measuring 46.5 cm × 51 cm) were used to assess the participant’s kinetic parameters (e.g. the CoP trajectory) during the FRT. The force platform signal was sampled at 250 Hz. Kinematic measurements were recorded by means of a video motion system (VICON Video System, Oxford Metrics, Oxford, UK) with eight infrared cameras and a sampling frequency of 50 Hz. Thirty spherical, retroreflective markers were placed on different body segments (Plug-In-Gait, Full-body model). The system’s measurement precision for movement was 2 mm.
3. Methods Three groups were studied: young adults (between 18 and 30 years of age), elderly adults (over 65 years of age) and PD patients with no history of falls. Patients with PD were only included if their Hoehn and Yahr scale score was below 2.5 [19]. This criterion means that the included PD patients had mild bilateral disease but no clinical impairments of postural control. The PD patients performed the experiment while on their usual antiparkinsonian medication. Participants were excluded if they had any neurological conditions (other than PD for the patient group), signs of dementia (according to the DSM IV criteria), musculoskeletal disorders, vestibular disorders, recurrent dizziness, or known hip- or ankle-related disease or injury or if they were taking medications that could have affected posture. All the subjects gave their informed consent and the study was approved by the local ethics committee. In the experiment, the participant stood barefoot with one foot on each force plate and with the feet parallel and set a comfortable distance apart. The participant first had to estimate his/her maximum RD (but without performing the action, i.e. as a motor imagery task) and then actually perform the FRT (i.e. as a motor task). In the motor imagery task, the investigator placed a vertical bar (height: 1600 mm) at the participant’s index finger (arm extended) and asked the participant not to move. The bar was then sequentially moved away from and towards the participant by random amounts (in multiples of 50 mm steps, for example: 500, 350, 1000, 50, 550, 800, 150, 450, 950, 650, 200, 750, 100, 900, 700, 300, 600, 850, 400, 250 mm). After each placement of the bar,
Fig. 1. The CoP trajectory in a PD patient (A) and in a young adult (B) during the FRT. Note the differences in the anteroposterior axis. Foot placement was determined by heel, ankle and toe markers on each foot.
G. Ryckewaert et al. / Neuroscience Letters 589 (2015) 181–184
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Fig. 2. Dispersion of the values of the RD (Y axis) and the CoP displacement during the FRT (x axis) for each of the three groups (PD patients, elderly adults and young adults). PD patients displayed lower RD than elderly and young subjects and smaller CoP displacement than young adults.
the participant was asked to state whether he/she would be able to reach the bar without taking a step forward. The predicted RD was tested twice and was defined as mean of the furthest two bar positions within the participant’s estimated reach. In the motor task (the FRT itself), the participant raised his/her dominant hand to shoulder height, with the elbow fully extended and the arm held horizontally. The participant was given the following verbal instructions (with no demonstration): “Reach as far forward as you can, doing whatever you wish except taking a step. Begin reaching when I say “go””. Data collection began when the tester said “Ready” and continued for 5 s. The actual RD was defined as the horizontal translational displacement of the right index finger’s marker between the beginning and end of the test. The beginning of the FRT motor task was defined as the position just after the investigator had said “ready”. The maximum RD in 3 FRTs was used in our subsequent analysis except for correlations between RD and CoP displacement. The peak velocity of the index finger marker in the FRT was also noted. The forward CoP displacement during the FRT was recorded (Fig.1). 3.1. Statistics An analysis of variance (ANOVA) with one between-subjects factor (group) was performed on the study variables. Overestimation or underestimation were defined by the difference between actual (motor task) RD and estimated RD. If the value was positive, no overestimation was observed. Accuracy of the estimation was evaluated by the absolute value of the difference between actual RD and estimated RD. If an effect of group was observed, Bonferroni post hoc tests were performed. When the data were not normally distributed, the Conover procedure (ANOVA on ranks) was applied. Spearman’s test was performed to assess correlations between RD and CoP displacement. Additionally, an interview of patients was done one year after the experiments and comparisons between ‘a posteriori’ fallers and non-fallers was done using U Mann and Whitney test.
There was no difference in BMI between the elderly adults and the PD patients. The mean duration of PD was 6 ± 4 years. The patients’ mean Motor Unified Parkinson’s Disease Rating Scale (UPDRS) score (out of 108) was 17.8 ± 7.0. The mean Mini Mental State Examination score (out of 30) was 28 ± 2 for the PD patients and 28 ± 2 for the elderly adults. The RD was lower in PD patients (306 ± 79 mm) than in elderly adults (371 ± 70 mm; p = 0.01 vs. patients) and young adults (468 ± 127 mm; p < 0.001 vs. patients). The speed of the right index finger marker was lower in PD patients (53 ± 21 mm/s) than in elderly adults (86 ± 37 mm/s, p < 0.001 vs. patients) and young adults (116 ± 40 mm/s; p < 0.001 vs. patients). CoP displacement was 96 mm ± 33 mm in PD patients, 105 ± 31 mm in elderly adults and 139 ± 22 mm in young adults. There was no significant difference between PD patients and elderly adults in terms of forward CoP displacement. However, both these groups differed from young adults (p < 0.001) (Fig. 2). The estimated RD was 270 ± 116 mm in PD patients, 351 ± 151 mm in elderly adults and 434 ± 108 in young adults. The mean difference between estimated RD and actual RD was 37 ± 120 mm in PD patients, 22 ± 129 mm in elderly subjects, 34 ± 170 in young adults, the absolute error was 98 ± 76 mm in PD patients, 94 ± 90 mm in elderly subjects and 121 ± 121 mm in young adults. The three groups did not differ in terms of the difference between the actual RD and the estimated RD or accuracy of the estimation. No significant overestimation (i.e. an estimated RD greater than the actual RD) was observed. However, we should note a high interindividual variability with subjects either underestimating or overestimating their performance. The actual RD and the CoP displacement were highly correlated (R = 0.626, p < 0.001) (Fig. 2). Seven PD patients (and no elderly or young adults) reported a fall in the year following the experiment. The fallers and non-fallers were compared a posteriori and were found to differ significantly in terms of disease duration (8 ± 1 years for fallers and 5 ± 4 years for non-fallers) but not in terms of RD or CoP displacement (respectively, p = 0.91 and 0.26).
4. Results
5. Discussion
Twenty-three participants were included in each group. The mean ± SD age was 66 ± 8 years for the PD patients, 70 ± 8 for the elderly adults and 23 ± 2 for the young adults. There was no difference in mean age between the elderly adults and the PD patients. The mean body mass index (BMI) was respectively 29 ± 3 in PD patients, 27 ± 4 in the elderly adults and 23 ± 3 in the young adults.
The RD was dramatically lower (reflecting hypokinesia) in PD patients than in healthy elderly adults and young adults. Moreover, the PD patients performed the task more slowly (decreased speed of index marker, reflecting bradykinesia). Importantly, the PD patients adequately estimated their impaired ability to perform the FRT (‘imagery task’). When analyzing the limits of stability, PD
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patients did not adopt the “at risk” strategy that would have consisted of moving their CoP forward towards the boundary of their base of support (deviation of the CoP was dramatically lower in PD patients than in young adults). Differences in RD between elderly adults and young adults have been attributed to several factors, including (i) more ample rotation of the thoracic spine during the FRT (15) and (ii) differences in the strategies used (ankle flexion, which is less performant than hip flexion, or the use of “combined” strategies) [16,20]. Our PD group’s performance of the FRT is similar to that reported in the literature. According to Brusse et al. [21], the mean FRT was 184 mm in patients with a Hoehn and Yahr score ranging from 1 to 4. Brusse et al.’s study including fallers, which might explain why the mean UPDRS score for PD patients in their study (28) was higher than in our group (17.8). Behrman et al. [15] observed similar values in elderly adults (mean: 364 mm) and PD patients (mean: 334 mm) and determined a threshold (254 mm) to differentiate between fallers and non-fallers with good sensitivity (92%) but very poor specificity (30%). Hence, the FRT was not effective for determining the risk of falls. It should be borne in mind that none of our PD patients reported any falls before the study. Our PD patients and elderly adults did not differ significantly in terms of forward CoP displacement but both groups differed with respect to younger participants. This effect of age on the strategy used to perform the FRT was also observed by Cavanaugh et al. [17] (with a 30 mm difference in forward displacement between young and elderly adults, vs. 26 mm in our study). Projecting the CoP forward increases postural instability by reaching the limits of stability. Younger subjects use a ‘reach maximization strategy’ by projecting their CoP forward. However, neither elderly adults nor PD patients used this “at risk” postural control strategy to improve their FRT performance. In the present study, PD patients adequately estimated their ability to perform the task. In fact, they slightly underestimated their performance. The same was true of elderly and young adults. Nevertheless, despite overestimation of performance was not observed in average, it must be noted a between-subjects variability in the tested groups with participants who tended to underestimate their performance while others tended to overestimate their performance. Seven PD patients subsequently reported a fall in the year following the experiment (according to a “phone survey” performed by the investigators). Retrospectively, none of the fallers had overestimated his/her RD during the experiment. Patients with PD were able to predict their performance before performing of the task but appeared to be more conservative (as were healthy elderly adults) in their postural control behavior. It would be interesting to evaluate the ability to estimate self-performance in patients at more advanced stages of PD (when worsened postural instability is accompanied by cognitive disorders). Relevant conflicts of interest/financial disclosures Gilles Ryckewaert, Marion Luyat, Myriam Noël, Mélanie Rambour, Céline Tard, Luc Defebvre and Arnaud Delval have no actual or potential conflicts of interest. This project received a funding source
from French ministry of research (Appel d’offre PIR “Longévité et Viellissement”, CNRS, 2009). Acknowledgment We thank Dr. David Fraser (Biotech Communication, Damery, France) for helpful comments on the manuscript’s English. References [1] M.E. Morris, Movement disorders in people with Parkinson disease: a model for physical therapy, Phys. Ther. 80 (2000) 578–597. [2] A. Ashburn, E. Stack, C. Ballinger, L. Fazakarley, C. Fitton, The circumstances of falls among people with Parkinson’s disease and the use of falls diaries to facilitate reporting, Disabil. Rehabil. 30 (2008) 1205–1212, http://dx.doi.org/10.1080/09638280701828930. [3] M.E. Jenkins, A.M. Johnson, J.D. Holmes, F.F. Stephenson, S.J. Spaulding, Predictive validity of the UPDRS postural stability score and the Functional Reach Test, when compared with ecologically valid reaching tasks, Parkinsonism Relat. Disord. 16 (2010) 409–411, http://dx.doi.org/10.1016/j.parkreldis.2010.04.002. [4] M.J.H. Heijnen, B.C. Muir, S. Rietdyk, Factors leading to obstacle contact during adaptive locomotion, Exp. Brain Res. 223 (2012) 219–231, http://dx.doi.org/10.1007/s00221-012-3253-y. [5] D. Hyndman, A. Ashburn, E. Stack, Fall events among people with stroke living in the community: circumstances of falls and characteristics of fallers, Arch. Phys. Med. Rehabil. 83 (2002) 165–170, http://dx.doi.org/10.1053/apmr.2002.28030. [6] M. Woollacott, A. Shumway-Cook, Attention and the control of posture and gait: a review of an emerging area of research, Gait Posture 16 (2002) 1–14. [7] A.C. Lee, J.P. Harris, E.A. Atkinson, M.S. Fowler, Disruption of estimation of body-scaled aperture width in Hemiparkinson’s disease, Neuropsychologia 39 (2001) 1097–1104. [8] J. Gibson, The theory of affordances, in: R. Shaw, J. Bransford (Eds.), Perceiving, Acting, and Knowing: Toward an ecological psychology, 1977, pp. 67–82. [9] G. Lafargue, M. Noël, M. Luyat, In the elderly, failure to update internal models leads to over-optimistic predictions about upcoming actions, PloS One 8 (2013) e51218, http://dx.doi.org/10.1371/journal.pone.0051218. [10] P.W. Duncan, D.K. Weiner, J. Chandler, S. Studenski, Functional reach: a new clinical measure of balance, J. Gerontol. 45 (1990) M192–M197. [11] P.W. Duncan, S. Studenski, J. Chandler, B. Prescott, Functional reach: predictive validity in a sample of elderly male veterans, J. Gerontol. 47 (1992) M93–98. [12] D.K. Weiner, P.W. Duncan, J. Chandler, S.A. Studenski, Functional reach: a marker of physical frailty, J. Am. Geriatr. Soc. 40 (1992) 203–207. [13] D.K. Weiner, D.R. Bongiorni, S.A. Studenski, P.W. Duncan, G.G. Kochersberger, Does functional reach improve with rehabilitation? Arch. Phys. Med. Rehabil. 74 (1993) 796–800. [14] L. de Waroquier-Leroy, S. Bleuse, R. Serafi, E. Watelain, V. Pardessus, A.-V. Tiffreau, et al., The functional reach test: strategies, performance and the influence of age, Ann. Phys. Rehabil. Med. (2014), http://dx.doi.org/10.1016/j.rehab.2014.03.003. [15] A.L. Behrman, K.E. Light, S.M. Flynn, M.T. Thigpen, Is the functional reach test useful for identifying falls risk among individuals with Parkinson’s disease? Arch. Phys. Med. Rehabil. 83 (2002) 538–542. [16] M. Wernick-Robinson, D.E. Krebs, M.M. Giorgetti, Functional reach: does it really measure dynamic balance? Arch. Phys. Med. Rehabil. 80 (1999) 262–269. [17] J.T. Cavanaugh, M. Shinberg, L. Ray, K.M. Shipp, M. Kuchibhatla, M. Schenkman, Kinematic characterization of standing reach: comparison of younger vs. older subjects, Clin. Biomech. Bristol Avon 14 (1999) 271–279. [18] E. Stack, A. Ashburn, K. Jupp, Postural instability during reaching tasks in Parkinson’s disease, Physiother. Res. Int. J. Res. Clin. Phys. Ther. 10 (2005) 146–153. [19] M.M. Hoehn, M.D. Yahr, Parkinsonism: onset, progression and mortality, Neurology 17 (1967) 427–442. [20] C.-F. Liao, S.-I. Lin, Effects of different movement strategies on forward reach distance, Gait Posture 28 (2008) 16–23, http://dx.doi.org/10.1016/j.gaitpost.2007.09.009. [21] K.J. Brusse, S. Zimdars, K.R. Zalewski, T.M. Steffen, Testing functional performance in people with Parkinson disease, Phys. Ther. 85 (2005) 134–141.
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Research article
Self-perceived and actual ability in the functional reach test in patients with Parkinson’s disease Gilles Ryckewaert a,b , Marion Luyat d , Melanie Rambour a,b , Céline Tard a,c , Myriam Noël d , Luc Defebvre a,b , Arnaud Delval a,c,∗ a
Université de Lille, U1171, F-59037 Lille cedex, France Department of Neurology, Lille University Medical Center, F-59037 Lille cedex, France c Department of Clinical Neurophysiology, Lille University Medical Center, F-59037 Lille cedex, France d Université de Lille, EA 4072, F-59650 Villeneuve d’Ascq, France b
h i g h l i g h t s • • • •
Differences between self-perceived and actual ability to reach an object could lead to falls in PD patients. Functional reach test performance was altered in PD patients. Antero-posterior CoP displacement was reduced in PD and elderly subjects. Ability to estimate self-performance was preserved in PD patients and was not linked to future falls.
a r t i c l e
i n f o
Article history: Received 19 November 2014 Received in revised form 2 January 2015 Accepted 15 January 2015 Available online 16 January 2015 Keywords: Parkinson’s disease Posture Falls Functional reach test
a b s t r a c t Falls frequently occur during daily activities such as reaching for an object in patients with Parkinson’s disease (PD). Misjudgment is also reported to be one of the circumstances that lead to falls. The functional reach test is an indicator of dynamic balance. The primary objective was to establish whether there is a difference between self-perceived and actual ability to perform the functional reach test in patients with PD who have never fallen. Three groups of participants (all with no history of falls) were studied: young adults, elderly adults and PD patients. The participants first estimated their maximum reaching distance (but without performing the action, i.e. as a motor imagery task) and then actually performed the functional reach test (i.e. as a motor task). No significant overestimation or underestimation was observed. The reaching distance was lower in PD than in the two other groups. There were no differences between PD patients and elderly adults in terms of the forward centre of pressure displacement. Seven PD patients reported a fall in the year following the experiment. The fallers had a longer history of disease. Finally, PD patients adequately estimated their ability in the functional reach test and did not adopt an “at risk” strategy and appeared to be quite conservative (as were healthy elderly adults) in their postural control behavior. Ability to estimate self-performance is preserved in PD patients with no clinical impairments of postural control although they are at risk of future falls. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Patients with Parkinson’s disease (PD) have difficulty maintaining their balance when performing tasks such as reaching for an object while standing [1]. Falls occur commonly during reaching activities in PD patients [2,3]. Moreover, misjudgment and distrac-
∗ Corresponding author at: Clinical Neurophysiology Department, Hôpital Salengro, F-59037 Lille cedex, France. Tel.: +33 320 446 362; fax: +33 320 446 355. E-mail address: [email protected] (A. Delval). http://dx.doi.org/10.1016/j.neulet.2015.01.039 0304-3940/© 2015 Elsevier Ireland Ltd. All rights reserved.
tion are involved in 12% of reported falls. Fallers frequently reported that misjudgment, lack of concentration, and loss of balance had caused them to fall [4–6]. Indeed, disrupted representation of the external space and the environment is a possible perceptual component of the motor disorders in PD [7]. The maintenance of balance in tasks such as reaching a book on a wall-mounted shelf often requires postural adjustment. The most efficient means of ensuring balance under such conditions is visual perception of the environmental properties at a distance, prospective modification of movement patterns and thus avoidance of perturbation altogether. Affordances (defined as actions that are possible within
182
G. Ryckewaert et al. / Neuroscience Letters 589 (2015) 181–184
an environment and within the context of the individual’s capacity) are prerequisites for prospective postural adjustments [8]. Some elderly adults fail to update internal models – prompting them to make over-optimistic predictions about upcoming actions [9]. In turn, this may favor “at risk” motor decision-making, and thus, promote falls [9]. This topic has not previously been investigated in patients with PD. The functional reach test (FRT) is a valid, reliable, clinical measure of dynamic balance developed by Duncan et al. [11–13]. In the FRT, the individual is asked to elevate his or her arm to shoulder’s height and then to perform a maximum forward reach. In elderly adults, a reaching distance (RD) of below 15 cm is associated with an increased risk of falls and frailty [11,13]. The FRT is also an indicator of dynamic balance: Duncan et al. [10] reported that the RD in the FRT is highly correlated with the centre of pressure (CoP) excursion [14]. The latter parameter (recorded on a force platform) is an indicator of dynamic balance and measures the limits of stability. Both CoP excursion and RD are inversely associated with recurrent falls and physical frailty [15,16]. However, young adults perform greater CoP displacements but also achieve a higher maximum forward RD while maintaining standing posture. The simple FRT has been found to be a reliable and precise estimate of postural instability. The functional RD can be analyzed separately or as an item in Berg’s Balance score [17], which might represent an “at risk” strategy in patients with postural instability. The FRT has also been validated in a group of individuals with PD (with or without a history of falls); Behrman et al. [15] demonstrated that a cut-off RD of 254 mm accurately identifies individuals at a high risk of falls (specificity: 92%; positive predictive value: 90%). The FRT is also of particular interest in advanced PD patients who appear unstable when reaching who are at risk of further falls [18]. The primary objective of the present study was to establish whether there is a difference between self-perceived and actual ability to perform the FRT in patients with PD who have never fallen. The secondary objective was to assess the participants’ limits of stability during the FRT and identify possible “at risk” strategies induced by the task. To this end, we studied CoP excursion during the FRT. One year after the experiment, a “phone survey” (notified to the participants in advance) provided information on whether or not the participants in the three groups had fallen during that period.
2. Material Two force platforms (OR6 from AMTI, Watertown, MA, USA, each measuring 46.5 cm × 51 cm) were used to assess the participant’s kinetic parameters (e.g. the CoP trajectory) during the FRT. The force platform signal was sampled at 250 Hz. Kinematic measurements were recorded by means of a video motion system (VICON Video System, Oxford Metrics, Oxford, UK) with eight infrared cameras and a sampling frequency of 50 Hz. Thirty spherical, retroreflective markers were placed on different body segments (Plug-In-Gait, Full-body model). The system’s measurement precision for movement was 2 mm.
3. Methods Three groups were studied: young adults (between 18 and 30 years of age), elderly adults (over 65 years of age) and PD patients with no history of falls. Patients with PD were only included if their Hoehn and Yahr scale score was below 2.5 [19]. This criterion means that the included PD patients had mild bilateral disease but no clinical impairments of postural control. The PD patients performed the experiment while on their usual antiparkinsonian medication. Participants were excluded if they had any neurological conditions (other than PD for the patient group), signs of dementia (according to the DSM IV criteria), musculoskeletal disorders, vestibular disorders, recurrent dizziness, or known hip- or ankle-related disease or injury or if they were taking medications that could have affected posture. All the subjects gave their informed consent and the study was approved by the local ethics committee. In the experiment, the participant stood barefoot with one foot on each force plate and with the feet parallel and set a comfortable distance apart. The participant first had to estimate his/her maximum RD (but without performing the action, i.e. as a motor imagery task) and then actually perform the FRT (i.e. as a motor task). In the motor imagery task, the investigator placed a vertical bar (height: 1600 mm) at the participant’s index finger (arm extended) and asked the participant not to move. The bar was then sequentially moved away from and towards the participant by random amounts (in multiples of 50 mm steps, for example: 500, 350, 1000, 50, 550, 800, 150, 450, 950, 650, 200, 750, 100, 900, 700, 300, 600, 850, 400, 250 mm). After each placement of the bar,
Fig. 1. The CoP trajectory in a PD patient (A) and in a young adult (B) during the FRT. Note the differences in the anteroposterior axis. Foot placement was determined by heel, ankle and toe markers on each foot.
G. Ryckewaert et al. / Neuroscience Letters 589 (2015) 181–184
183
Fig. 2. Dispersion of the values of the RD (Y axis) and the CoP displacement during the FRT (x axis) for each of the three groups (PD patients, elderly adults and young adults). PD patients displayed lower RD than elderly and young subjects and smaller CoP displacement than young adults.
the participant was asked to state whether he/she would be able to reach the bar without taking a step forward. The predicted RD was tested twice and was defined as mean of the furthest two bar positions within the participant’s estimated reach. In the motor task (the FRT itself), the participant raised his/her dominant hand to shoulder height, with the elbow fully extended and the arm held horizontally. The participant was given the following verbal instructions (with no demonstration): “Reach as far forward as you can, doing whatever you wish except taking a step. Begin reaching when I say “go””. Data collection began when the tester said “Ready” and continued for 5 s. The actual RD was defined as the horizontal translational displacement of the right index finger’s marker between the beginning and end of the test. The beginning of the FRT motor task was defined as the position just after the investigator had said “ready”. The maximum RD in 3 FRTs was used in our subsequent analysis except for correlations between RD and CoP displacement. The peak velocity of the index finger marker in the FRT was also noted. The forward CoP displacement during the FRT was recorded (Fig.1). 3.1. Statistics An analysis of variance (ANOVA) with one between-subjects factor (group) was performed on the study variables. Overestimation or underestimation were defined by the difference between actual (motor task) RD and estimated RD. If the value was positive, no overestimation was observed. Accuracy of the estimation was evaluated by the absolute value of the difference between actual RD and estimated RD. If an effect of group was observed, Bonferroni post hoc tests were performed. When the data were not normally distributed, the Conover procedure (ANOVA on ranks) was applied. Spearman’s test was performed to assess correlations between RD and CoP displacement. Additionally, an interview of patients was done one year after the experiments and comparisons between ‘a posteriori’ fallers and non-fallers was done using U Mann and Whitney test.
There was no difference in BMI between the elderly adults and the PD patients. The mean duration of PD was 6 ± 4 years. The patients’ mean Motor Unified Parkinson’s Disease Rating Scale (UPDRS) score (out of 108) was 17.8 ± 7.0. The mean Mini Mental State Examination score (out of 30) was 28 ± 2 for the PD patients and 28 ± 2 for the elderly adults. The RD was lower in PD patients (306 ± 79 mm) than in elderly adults (371 ± 70 mm; p = 0.01 vs. patients) and young adults (468 ± 127 mm; p < 0.001 vs. patients). The speed of the right index finger marker was lower in PD patients (53 ± 21 mm/s) than in elderly adults (86 ± 37 mm/s, p < 0.001 vs. patients) and young adults (116 ± 40 mm/s; p < 0.001 vs. patients). CoP displacement was 96 mm ± 33 mm in PD patients, 105 ± 31 mm in elderly adults and 139 ± 22 mm in young adults. There was no significant difference between PD patients and elderly adults in terms of forward CoP displacement. However, both these groups differed from young adults (p < 0.001) (Fig. 2). The estimated RD was 270 ± 116 mm in PD patients, 351 ± 151 mm in elderly adults and 434 ± 108 in young adults. The mean difference between estimated RD and actual RD was 37 ± 120 mm in PD patients, 22 ± 129 mm in elderly subjects, 34 ± 170 in young adults, the absolute error was 98 ± 76 mm in PD patients, 94 ± 90 mm in elderly subjects and 121 ± 121 mm in young adults. The three groups did not differ in terms of the difference between the actual RD and the estimated RD or accuracy of the estimation. No significant overestimation (i.e. an estimated RD greater than the actual RD) was observed. However, we should note a high interindividual variability with subjects either underestimating or overestimating their performance. The actual RD and the CoP displacement were highly correlated (R = 0.626, p < 0.001) (Fig. 2). Seven PD patients (and no elderly or young adults) reported a fall in the year following the experiment. The fallers and non-fallers were compared a posteriori and were found to differ significantly in terms of disease duration (8 ± 1 years for fallers and 5 ± 4 years for non-fallers) but not in terms of RD or CoP displacement (respectively, p = 0.91 and 0.26).
4. Results
5. Discussion
Twenty-three participants were included in each group. The mean ± SD age was 66 ± 8 years for the PD patients, 70 ± 8 for the elderly adults and 23 ± 2 for the young adults. There was no difference in mean age between the elderly adults and the PD patients. The mean body mass index (BMI) was respectively 29 ± 3 in PD patients, 27 ± 4 in the elderly adults and 23 ± 3 in the young adults.
The RD was dramatically lower (reflecting hypokinesia) in PD patients than in healthy elderly adults and young adults. Moreover, the PD patients performed the task more slowly (decreased speed of index marker, reflecting bradykinesia). Importantly, the PD patients adequately estimated their impaired ability to perform the FRT (‘imagery task’). When analyzing the limits of stability, PD
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patients did not adopt the “at risk” strategy that would have consisted of moving their CoP forward towards the boundary of their base of support (deviation of the CoP was dramatically lower in PD patients than in young adults). Differences in RD between elderly adults and young adults have been attributed to several factors, including (i) more ample rotation of the thoracic spine during the FRT (15) and (ii) differences in the strategies used (ankle flexion, which is less performant than hip flexion, or the use of “combined” strategies) [16,20]. Our PD group’s performance of the FRT is similar to that reported in the literature. According to Brusse et al. [21], the mean FRT was 184 mm in patients with a Hoehn and Yahr score ranging from 1 to 4. Brusse et al.’s study including fallers, which might explain why the mean UPDRS score for PD patients in their study (28) was higher than in our group (17.8). Behrman et al. [15] observed similar values in elderly adults (mean: 364 mm) and PD patients (mean: 334 mm) and determined a threshold (254 mm) to differentiate between fallers and non-fallers with good sensitivity (92%) but very poor specificity (30%). Hence, the FRT was not effective for determining the risk of falls. It should be borne in mind that none of our PD patients reported any falls before the study. Our PD patients and elderly adults did not differ significantly in terms of forward CoP displacement but both groups differed with respect to younger participants. This effect of age on the strategy used to perform the FRT was also observed by Cavanaugh et al. [17] (with a 30 mm difference in forward displacement between young and elderly adults, vs. 26 mm in our study). Projecting the CoP forward increases postural instability by reaching the limits of stability. Younger subjects use a ‘reach maximization strategy’ by projecting their CoP forward. However, neither elderly adults nor PD patients used this “at risk” postural control strategy to improve their FRT performance. In the present study, PD patients adequately estimated their ability to perform the task. In fact, they slightly underestimated their performance. The same was true of elderly and young adults. Nevertheless, despite overestimation of performance was not observed in average, it must be noted a between-subjects variability in the tested groups with participants who tended to underestimate their performance while others tended to overestimate their performance. Seven PD patients subsequently reported a fall in the year following the experiment (according to a “phone survey” performed by the investigators). Retrospectively, none of the fallers had overestimated his/her RD during the experiment. Patients with PD were able to predict their performance before performing of the task but appeared to be more conservative (as were healthy elderly adults) in their postural control behavior. It would be interesting to evaluate the ability to estimate self-performance in patients at more advanced stages of PD (when worsened postural instability is accompanied by cognitive disorders). Relevant conflicts of interest/financial disclosures Gilles Ryckewaert, Marion Luyat, Myriam Noël, Mélanie Rambour, Céline Tard, Luc Defebvre and Arnaud Delval have no actual or potential conflicts of interest. This project received a funding source
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