A new screening test for idiopathic normal pressure hydrocephalus using bimanual coordination: A preliminary study

Abstract

BACKGROUND:

The clinical spectrum of idiopathic normal pressure hydrocephalus (iNPH) comprises the triad of gait disturbance, cognitive impairment, and urinary incontinence. However, motor abnormalities involving the upper extremities in iNPH patients have few quantitative studies.

OBJECTIVE:

The present study was designed to quantitatively assess bimanual tapping tasks in iNPH patients and to compare with the control groups.

METHODS:

The subjects were divided into three groups: iNPH patients, older healthy group, and younger healthy group. The tasks were three synchronization finger-to-thumb tapping tasks with the auditory stimuli specified at 1 Hz by metronome: unilateral, bimanual simultaneous, and bimanual alternate. Two-way ANOVA was used to compare the outcomes of the three errors (absolute error: AE, variable error: VE, and constant error: CE) for tapping cycles.

RESULTS:

In the iNPH group, the absolute and variable errors increased in bimanual alternate tapping task with statistical significance (AE: p < 0.05 and VE: p < 0.05). There were no significant differences in errors between the older and young healthy groups (AE: p = 0.62, CE: p = 1.00 and VE: p = 0.31).

CONCLUSIONS:

We could quantitatively evaluate the bimanual coordination on iNPH patients using the bimanual alternate tapping task, potentially useful for evaluating patients unable to walk.

Keywords

Idiopathic normal pressure hydrocephalus bimanual coordination finger-to-thumb tapping upper extremity occupational therapy

1 Introduction

Idiopathic normal pressure hydrocephalus (iNPH) occurs in the elderly due to impaired absorption of cerebrospinal fluid (CSF) and is characterized by a clinical triad of gait disturbance, cognitive impairment, and urinary incontinence (Hakim & Adams, 1965; Marmarou et al., 2005; Mori et al., 2012). Of the clinical triad, gait disturbance is found in 91% of iNPH patients (Krauss et al., 1997). Gait disturbance in iNPH patients is characterized by small-step gait, magnetic gait, and broad-based gait. It is said that the variability of step length and stride width are particularly large ( Stolze et al., 2000, 2001), and it is important in distinguishing it from other neurological diseases (Adams et al., 1965; Fisher, 1982; Morel et al., 2019).

Assessments of quantitative gait measures prior to the CSF tap test are commonly utilized as a predictor of shunt effectiveness (Ishikawa et al., 2016) However, in clinical situations, we often experience that iNPH patients have severe gait difficulty at the initial visit, unable to perform gait assessment. Therefore, the need for alternative motor function assessments is mentioned for those who have severe gait disturbance (Liouta et al., 2017).

Upper extremity dysfunction is reported in 86% of iNPH patients (Krauss et al., 1997). Though it is such a common dysfunction, there are few quantitative studies on the evaluation of upper extremity function (Lenfeldt et al., 2008; Liouta et al., 2017; Nowak & Topka, 2006), and the characteristics have not been clarified. Recently, it has been pointed out by studies using fMRI that the supplementary motor area is the lesion of upper extremities dysfunction in iNPH patients (Lenfeldt et al., 2008; Nowak & Topka, 2006). Essentially, the supplementary motor area is said to control bimanual coordination, and it is known that when impaired, the tapping cycles varies in bimanual tapping tasks (Serrien et al., 2002). Given these backgrounds, we aimed to examine a new screening test method for iNPH patients using bimanual tapping task, evaluating the bimanual coordination.

2 Methods

2.1 Participants

Ten iNPH patients (iNPH group, mean age = 78.6 years, two females) were recruited from the Department of Neurosurgery and Rehabilitation at The Jikei University Katsushika Medical Center. The iNPH patients had probable diagnoses with a positive CSF tap test result according to the iNPH diagnostic criteria (Mori et al., 2012). The inclusion criteria for probable iNPH were the following clinical features proposed in the national iNPH guidelines: (1) symptomatic onset at the age of 60 or older, (2) MRI-detected ventricular dilation (Evans Index > 0.3) accompanied by narrowing of the subarachnoid CSF space in the high convexity and interhemispheric fissure, (3) CSF pressure of 200 mmH₂O or less and normal CSF laboratory findings, (4) clinical symptoms not completely explained by other neurological or non-neurological conditions, (5) absence of other conditions associated with ventricular dilation, such as subarachnoid hemorrhage, meningitis, head injury, congenital hydrocephalus, or aqueductal stenosis, and (6) a positive clinical response to a CSF tap test.

Ten age-matched older healthy adults (older group, mean age = 70.7±5.3 years, six females) and also ten young healthy adults (younger group, mean age = 30.9±6.2 years, six females) took part in the experiment as control participants. The age of older group was matched with that of iNPH group. Participants who corresponded to one or more of the following items were excluded: (1) difficult to understand and perform tasks, (2) left-handed, (3) hearing-impaired, (4) with fractures and paresis in upper extremities, or (5) with aphasia, apraxia, or agnosia.

The approval of the ethics committee of Jikei University was obtained for the implementation of this study protocol (No. 30-352 9373). All participants were given a written explanation of the purpose, method, content, voluntary participation / non-participation in this study, and protection of personal information, and then the research was conducted after obtaining their consent. In conducting the research, we strictly adhered to the Personal Information Protection Law regarding the handling of personal information of the subjects based on the Declaration of Helsinki.

2.2 Apparatus

The measurement was conducted in a soundproof room, in consideration of the experimental environment. Two sanding training single handles (SOT-1803, SAKAI Medical Co., JPN, A 20 cm×14 cm×4 cm wooden board with a φ 2.5 cm acrylic fulcrum in the center), a smartphone (iPhone X, Apple Inc., USA), and a digital video camera (HC-990M, Panasonic, Japan) were placed on a desk (SOT-810N, SAKAI Medical CO., JPN, 75 cm height with an 88 cm×57 cm top board) (Fig. 1). The two handles were placed so that their central columns were 25 cm apart, with anti-slip sheet underneath to secure them from moving. Auditory cues were created with a digital metronome (Panoramic Software Inc., Metronome^trademark) and were presented at the sampling rate of 44.1 kHz by the speaker built into the smartphone. As a marker to track finger tapping movement, we used black-dot markers (1.5-cm in diameter), printed on a 2 cm×2 cm drawing paper, and attached them at the tips of the index fingers (Fig. 1-A) as well as on the side of the metacarpophalangeal joint of the index fingers (Fig. 1-B). We used the marker on the carpometacarpal joint of the thumb (Fig. 1-B) for calibration. The recording digital camera (HC-VX990M, Panasonic, Japan) was fixed 50 cm above both hands (Fig. 1-B). Participants’ finger movements were recorded at the sampling rate of 60 Hz. The recorded images were analyzed with two-dimensional motion analysis software (Kinovea^trademark ver. 0.8.23, France). The sampled tapping movement were further analyzed with MATLAB (Math Works, Inc.) to identify the timing of taps.

Fig. 1

Apparatus and participants’ posture while performing a tapping task. A bird’s-eye view (A). The smartphone used as a metronome was placed in front of the center of the desk to consider the equality of the left and right ears. Handles (fulcrums) were gripped by the middle finger, ring finger, and little finger, and the thumb and index finger were away from the fulcrums. A horizontal view (B). By grasping the sanding handle by the participants, consideration was given so that the direction of tapping movement would be on the horizontal plane. “MP joint” refers to the side of the metacarpophalangeal joint of the index fingers, and “CM joint” the carpometacarpal joint of the thumb.

2.3 Procedures and tapping tasks

Participants performed three finger-to-thumb tapping tasks (Enokizono et al., 2021; Suzumura et al., 2016). For all tasks, participants repetitively tapped their index finger on the thumb in synchrony with auditory cues (1 Hz) using the metronome. Task 1 is a unilateral-hand tapping task, performed with one hand by 1 Hz for fifteen seconds. They initially performed this task with their right hand, followed by the left hand. A bimanual simultaneous tapping task was performed with both hands by 1 Hz for fifteen seconds (Task 2). For the bimanual alternate tapping task (Task 3), auditory cues were presented by 1 Hz, and the performance was measured for 30 seconds. We set the time in task 3 as 30 seconds because the tapping frequency becomes 0.5 Hz (once in every two seconds) in this task, and it would take 30 seconds to have the same number of taps (15 taps) as other two tasks.

Participants were seated in front of the apparatus in a position so that they grasp the sanding training handles with shoulders in slight abduction (10–20°), elbows at 90°, and forearms supported in neutral prosupination. For their comfort, the back might be freely separated from the chair as long as extremities were in good positions. For each task, they practiced three times so that the opening of the thumb and index finger was 3 cm or more, but without auditory stimulation to eliminate possibility of learning rhythm with the practice. The recording was done once for each task with auditory cues. The measurement order of the tasks was the same for all subjects to perform all tasks accurately (Dione & Delevoye-Turrell, 2015), and the order of tasks 1 to 3 was set to the order of lowest nerve activity in the supplementary motor area (Aramaki et al., 2010).

2.4 Data analysis

The measurement to be analyzed was the inter-tap intervals (ITI; see Fig. 2) (Aoki & Fukuoka, 2010; Aramaki et al., 2010; Repp, 2005). A tap was determined as the zero crossings (from negative to positive) of the acceleration rate of the marker attached to the tip of the index finger. For each task, we dropped the first three and the last two taps and used the remaining taps to gain ITI, and defined its average as tapping cycle (Repp, 2005). For outcomes, absolute error (AE; absolute value of difference from true tapping cycle), variable error (VE; intra-participant variability), constant error (CE; direction and magnitude of the error) were used (Schmidt & Lee, 1999), not only to show the difference between the true value and the measured value, but also to analyze the systematic error due to factors other than the purpose and the error due to relative variation. The formula for AE, VE and CE were as follows (Schmidt & Lee, 1999):

Fig. 2

Temporal relationship between audio cue onsets and tap onsets. The figure shows three consecutive taps 1 to 3 when the auditory cues is 1 Hz (1000 ms interval). In the figure, tap onset 1 and 2 are tapping cycle (TC)1, and TC 2 are between tap onset 2 and 3. Since it was not a deviation from the auditory cues but a consecutive tapping interval, the effect of increasing or decreasing the number of taps were small when mistap (could not tap, or were multiple taps at a time) occurred.

AE = \frac{1}{n} \sum_{i = 1}^{n} | X_{i} - T |,

VE = \sqrt{\frac{1}{n} \sum_{i = 1}^{n} {(X_{i} - \bar{X})}^{2}},

CE = \frac{1}{n} \sum_{i = 1}^{n} (X_{i} - T),

where X_i characterizes a particular ITI. Therefore, $\bar{X}$ is average ITI and n is 20. T describes the target ITI (ms) in the task (i.e., T is 1000 for Task 1 and 2, and 2000 for Task 3).

2.5 Statistical analysis

One-way ANOVA was used for the age difference between the three groups, and the χ2 test (Chi-squared test) was used for the gender ratio test.

For data, two-way ANOVAs (three groups and three tasks) with repeated measures on task was performed as statistical analyses. Significant main and interaction effects were analyzed further using Bonferroni-corrected pairwise comparisons. The significance level was set to 0.05 %. Partial eta-squared values $(η_{ρ}^{2})$ were calculated as an unbiased estimate of the effect size in an ANOVA.

As we did not calculate the statistical sample size for the study, we examined its adequacy by performing the power analysis (1 - β err prob) on the main results based on significance level (α = 0.05), effect size $(η_{ρ}^{2})$ , and sample size (ten participants per group) by using the G^*power software (Heinrich Heine University, Duesseldorf, Germany). The acceptable power level was set to 80.0 % (Cohen, 1992).

3 Results

3.1 Age difference and ratio of male to female

There was no age difference between iNPH and older groups (p = 0.38). Furthermore, the male-female ratio among the three groups was tested by χ2 and confirmed that there was no significant difference between the three groups (p = 0.12).

3.2 Absolute Errors (AE)

It was found that bimanual alternate task in iNPH group had decreased accuracy of tapping cycle compared to other two control groups (Fig. 3-A). For AEs, the main effects of group (F (2, 27) = 7.81, p = 0.05, $η_{ρ}^{2} = 0.37$ ) and task (F (2, 27) = 11.65, p < 0.05, $η_{ρ}^{2} = 0.30$ ) were statistically significant. The AE was significantly larger under the iNPH group than that under the other two groups. Since there was a significant difference in the interaction (F (4, 54) = 7.30, p < 0.05, $η_{ρ}^{2} = 0.35$ ), multiple comparisons were performed and showed that for the bimanual alternate task, the iNPH group had significantly larger AEs than the other two groups (Fig. 3-A). There was no significant difference of the groups and tasks between young and older healthy adults’ groups (groups: p = 0.61, tasks: p = 0.59). For the post hoc power analysis, the power (1 - β err prob) for the main effects of group, the main effects of task, and interaction were 0.94, 0.85 and 0.92, respectively.

Fig. 3

Absolute Errors (AE), Variable Errors (VE) and Constant Errors (CE). The bars represent errors for Task 1 (unilateral hand), Task 2 (bimanual simultaneous), and Task 3 (bimanual alternate) in each group, and the error bars indicate the standard deviation. Each panel represents AE (A), VE (B), and CE (C). For AE and VE of Task 3, the results of Bonferroni-corrected pairwise comparisons to the performance of two control groups are indicated for iNPH group. (A) AE of bimanual alternate tapping task in the iNPH group was significantly larger than that of the other two groups, and within iNPH group, AE was significantly larger than other two tasks. (B) Similar to the AE result, VE in Task 3 (bimanual alternate tapping task) in the iNPH group was significantly larger than that of the other two groups, and within iNHP group, it was significantly larger than other two tasks. (C) For CEs, neither the main effects of group, nor task were significant. ^**: p < 0.01, n.s.: not significant.

3.3 Variable Errors (VE)

It was found that bimanual alternate task in iNPH group had increased variability of tapping cycle compared to other two control groups (Fig. 3-B). For VEs, the main effects of group (F (2, 27) = 8.04, p < 0.05, $η_{ρ}^{2} = 0.37$ ) and task (F (2, 27) = 16.06, p < 0.05, $η_{ρ}^{2} = 0.37$ ) were statistically significant (Fig. 3-B). The VE was significantly larger under the iNPH group than that under the other two groups. Since there was a significant difference in the interaction (F(4, 54) = 5.94, p < 0.05, $η_{ρ}^{2} = 0.31$ ), multiple comparisons were performed, with that the iNPH group showed significantly larger VEs than the other two groups for the bimanual alternate task. There was no significant difference between older and young healthy adults’ groups (groups: p = 0.31, tasks: p = 0.25). For the post hoc power analysis, the power (1 - β err prob) for the main effects of group, the main effects of task, and the interaction were 0.94, 0.94 and 0.87, respectively.

3.4 Constant Errors (CE)

The consistency of the task was not significantly different in all three groups (Fig. 3-C). For CEs, neither the main effects of group (F(2, 27) =1.90, p = 0.17, $η_{ρ}^{2} = 0.12$ ), and task (F(2, 27) = 1.109, p = 0.21, $η_{ρ}^{2} = 0.06$ ) nor the interaction (F(4, 54) =1.444, p = 0.21, $η_{ρ}^{2} = 0.10$ ) were significant (Fig. 3-C). There was no significant difference between older and young healthy adults’ groups (groups: p = 0.99, tasks: p = 0.94). For the post hoc power analysis, the power (1 - β err prob) for the main effects of group, the main effects of task, and the interaction were 0.37, 0.19 and 0.65, respectively.

4 Discussion

The gait assessment has been the main motor function assessment tool to see the clinical change before and after CFS tap test in iNPH patients (Ishikawa et al, 2016). However, oftentimes we encounter patients with gait disturbance so severe that their activities of daily living are wheelchair based, and it is impossible to perform gait assessment. For such cases, bimanual tapping task, which is performed in the sitting position, can be useful as an alternative motor function assessment (Liouta et al., 2017). In iNHP patients, the error was significant with bimanual alternate tasks but not with bimanual simultaneous tasks (Fig. 3-A, 3-B). The possible explanation for this result is the decreased control of internal timing mechanism with auditory stimuli (Repp, 2005). The cycle of 1 Hz (1000 ms) is said to be a cycle easy to recognize (Ito et al., 2013), and when it falls below 0.55 Hz (1800 ms), it required attention to predict the next stimulus point, making it difficult to recognize (Miyake et al., 2004). In bimanual alternate tapping task, the tapping cycle of one hand is halved into 0.5 Hz, compared to the auditory stimulation cycle of 1 Hz. As a result, bimanual alternate tapping task is performed in less than 0.55 Hz, leading to erroneous tapping. Also, there was no significant difference in older healthy adults group compared with young healthy adults group, consistent with the report by Vanneste J. H. Wearden, S (2001). Thus, it can be said that the recognition of the intervals is a function that is not affected by age and is rather retained.

In our study, the iNPH group showed no significant difference in consistency, despite the fact that the iNPH group showed large variability specifically in bimanual alternate tapping tasks (Fig. 3-B, 3-C). This result could be due to our study setting. Since our study did not exclude iNPH patients without upper extremity dysfunction, we had both of those with and without upper extremity dysfunctions. Therefore, there was a large variability between patients who were able to perform bimanual alternate tapping task and those who were not. This large variability is the result of timing inconsistencies and is not biased toward either positive or negative (early or late timing). Of course, the result could suggest that this large variability was the characteristics of iNPH patients’ upper extremity dysfunction, but our study is insufficient to lead to such conclusion. Since we used only one auditory stimulus at 1 Hz in our study, the tapping cycle was not unified in all tasks. Consequently, it became not possible to clarify whether it was the auditory stimulation cycle or the bimanual alternate tapping task itself that affected the results. Further studies with bimanual alternate tapping task at 2 Hz (i.e., the tapping cycle of one hand is 1 Hz) added are needed.

Two limitations are identifiable in our study. First, the analysis of iNHP patient characteristics is lacking. The number of iNPH patients is small and the relationship with neuroimaging has not been examined. To utilize bimanual tapping task as a screening test for iNPH patients, it is necessary to show that the bimanual coordination characteristics of iNPH patients are related to supplementary motor area. Although our analysis had enough power as preliminary study, it is desirable to perform a study with larger numbers of cases to confirm the robustness of our findings. Furthermore, future research of the relationship between bimanual tapping task and the supplementary motor area detected by neuroimaging such as fMRI and SPECT should be added. Second, the influence of the order effects is disregarded in our study. Since the present study was preliminary and the upper extremity characteristics of iNPH patients were not clear from prior researches, we ordered the tasks in the same order for all participants based on the report by Aramaki et al. (2010). In the future, it will be necessary to randomize task orders to reduce the influence of the order effect.

5 Conclusions

In this study, we quantitatively evaluated bimanual coordination of iNPH patients using the bimanual alternate tapping task. The results showed that the accuracy of tapping cycle decrease and the variability increased in bimanual alternate tapping task. This finding suggested that bimanual alternate tapping task may be useful for evaluating iNPH patients unable to walk.

Conflict of interest

The authors have no conflicts of interest.

Footnotes

Acknowledgments

The authors would like to thank all the participants in this study, the staff of the Department of Rehabilitation Medicine, the Jikei University Katsushika Medical Center, and the members of the Higuchi Laboratory, Department of Health Promotion Science, Tokyo Metropolitan University. We also thank Takahiro Higuchi, Ryo Watanabe, Takuya Goto, and Ryuji Kobayashi for their suggestions and advice in conducting this study.

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