Quantification of hand functional recovery in spinal cord injury patients

Abstract

Study design

A prospective cohort study.

Objectives

To examine the use of a circle-tracing task in quantifying hand functional recovery in cervical spinal cord injury patients.

Methods

Ten cervical spinal cord injury (SCI) patients and 10 healthy age-matched controls performed a circle-tracing task, using a computerized tablet at the beginning of the study and after 4 weeks. Data relative to performance accuracy as well as pen pressure throughout the performances were collected, and clinical assessment for all patients was performed at the beginning and at the end of the study.

Results

Significant differences were found in pen pressure profiles in the SCI patients between the initial assessment and after 4 weeks of assessment. SCI patients, when compared with controls, apply less pressure during the execution, though no significant differences were found for the other parameters. Examination of pen pressure profiles of both controls and SCI patients reveals that, in addition to the lower pressure registered, SCI patients present a more oscillating pressure profile which is direction-dependent. No significant correlations were found between clinical assessments and pen pressure, both within the initial assessment as well as after 4 weeks.

Conclusions

This study emphasizes the potential of simple computerized means for quantifying upper limb functions in SCI patients. These results of this study could be helpful for both highlighting specific functional deficits in patients as well tailoring specific interventions.

Introduction

Compromised upper limb function is considered to be the most important cause of reduced quality of life in cervical spinal cord injury (SCI) patients.^1,2 As such, the quantification of hand function during rehabilitation may be useful for number of reasons, i.e. to follow-up on patient progress, tailor-specific interventions to facilitate recovery, as well as to motivate patients during the recovery process.³ To date, there are several qualification instruments used to evaluate hand functionality, with clinical scores being the most widely used ones.^4–6 In addition, specific tests for hand function quantification, for example, the Sollerman hand Function test,⁷ the Jebsen–Taylor Hand Function Test⁸ and the 9-Hole Peg Test⁹ have also been implemented in SCI patients. However, these tests could be lengthy and require the use of specific objects not always readily found, but more importantly they provide a qualitative assessment of the movement as a whole, and do not quantify the execution movement in depth.

As an alternative to the above-mentioned methods, tracing and drawing tasks, by being rapid and requiring simple equipment for administration, have been used to evaluate upper limb functionality with some success. Specifically, the precision of performance in tracing tasks has been used to evaluate fine motor control in different types of populations from children to healthy adults.^10–12 Tracing tasks have also been used in clinical settings as part of the neurologic examination for the evaluation of fine motor control.^13–15 Moreover, as the data retrieved through computerized means can be thoroughly analyzed, interesting investigations of different patient populations have also been conducted. It was shown that the area and roundness of the circles correlated with stroke severity and were suggested to represent outcome measures for stroke rehabilitation.¹⁶ Also, pen pressure was shown to be reduced in correlation with micrographia progression in Parkinson patients.¹⁷ Moreover, pen pressure profiles were found to be different among mild cognitive impairment, Alzheimer and controls.¹⁸ In fact, the authors suggested that using a digitizing tablet and a pressure-sensitive pen could be a useful resource in the clinical setting.

When it comes to SCI rehabilitation, the information retrieved from computerized tracing/drawing tasks maybe useful not only for the quantification of progress, but also for guiding the therapeutical intervention. In the setting of occupational therapy in SCI patients, a global assessment of the upper limb function is made prior to the intervention, based on which a general rehabilitative program is constructed.¹⁹ As the sessions progress, the program is modified aiming to achieve harmonious movements which are also aimed toward the recovery of patients’ personal interests.²⁰ As these programs are dynamically changing based on the patients’ needs and ability, modification of rehabilitation programs could benefit from accurate quantification of limb function by evidencing specific muscle groups in need of more attention.

In this study, we sought to investigate the use of a circle-tracing task for evaluation of upper limb functional recovery in SCI patients. Specifically, we examine both performance accuracy as well as pen pressure throughout the performances over a period of 4 weeks. Due to the compromised upper limb function in these patients, we expect that performances would differ greatly between patients and controls, for both accuracy as well as pressure applied.

Materials and methods

Participants

Ten cervical spinal cord lesion patients (age: 53.3 ± 17.6 years) and 10 healthy age-matched controls (age: 51.4 ± 16.6 years) were recruited to the study. Inclusion criteria were as follows: documented acute cervical spinal cord injury, compromised hand function. Patient characteristics are reported in Table 1. Participants were naive to the task and the purpose of the study, and all participants reported to have a corrected-to-normal visual acuity. The study protocol was approved by the Institutional Ethics Committee (Comitato Etico Area Vasta Centro AOUCareggi, Florence, Italy). Prior to the start of the experimental procedures, all participants provided written informed consent.

Table 1.

Patient characteristics and ISNCSCI assessments.

Patient	Age	Lesion Level	Initial assessment							Assessment after 4 weeks
			AIS Grade	C5 Force	C6 Force	C7 Force	C8 Force	T1 Force	Force Total	AIS Grade	C5 Force	C6 Force	C7 Force	C8 Force	T1 Force	Force Total
1	49	C7	C	5	5	5	3	0	18	D	5	5	5	4	0	19
2	63	C4	D	4	4	3	2	2	15	D	5	5	5	3	3	21
3	35	C4	B	5	2	4	0	0	11	B	5	3	5	0	0	13
4	79	C6	D	5	4	2	1	0	12	D	5	5	5	5	5	25
5	72	C4	D	3	3	3	3	2	14	D	5	4	5	4	4	22
6	41	C4	D	5	4	5	3	2	19	D	5	5	5	3	3	21
7	46	C4	D	4	4	4	4	4	20	E	5	5	5	5	5	25
8	70	C5	C	5	4	4	3	2	18	D	5	4	4	4	3	20
9	54	C5	B	5	4	3	0	0	12	D	5	4	3	0	0	12
10	24	C4	D	5	3	3	2	1	14	D	5	5	5	4	4	23

Clinical assessment

The International Standards for Neurological Classification of Spinal Cord Injury (ISNCSCI) were developed in order to achieve greater precision in the definitions used to classify spinal cord injury and the latest revision of this classification has been published in 2019.²¹ The two key elements of the classification are neurological level (which refers to the most caudal segment of the cord with intact sensation and antigravity muscle function strength, provided that there is normal sensory and motor function rostrally) and the degree of impairment ranging from A (complete lesion) to E (normal function). Regarding the motor function of the upper limbs, five key muscle functions, corresponding to five paired myotomes (C5-T1) are defined and the strength of each muscle function is graded on a six-point scale, ranging from 0 (total paralysis) to 5 (normal function).

Specifically, muscular strength was determined as described in INSCSCI manual muscle testing (MMT) in the supine position. The strength of each muscle function is graded on a six-point scale: 0 = total paralysis; 1 = palpable or visible contraction; 2 = active movement, full range of motion (ROM) with gravity eliminated; 3 = active movement, full ROM against gravity; 4 = active movement, full ROM against gravity and moderate resistance in a muscle specific position; 5 = (normal) active movement, full ROM against gravity and full resistance in a muscle-specific position expected from an otherwise unimpaired person; 5* = (normal) active movement, full ROM against gravity and sufficient resistance to be considered normal if identified inhibiting factors (i.e. pain, disuse) were not present. Complete ISNCSCI evaluations were performed on each patient prior to the beginning of the study and repeated at the end of the study (i.e. after 4 weeks from the first evaluation; Table 1).

Setup and task

The setup is similar to the one used in Cohen et al. (2021), and is briefly summarized here. Participants were presented a circle template projected on a monitor mounted vertically in front of them at eye level (Figure 1). The participants were instructed to execute tracings of a circle to the best of their capabilities, using graphic pen tablet (Wacom Intuos^® CTH-690AK, Tokyo, Japan; active area: 216 mm × 135 mm). From the tablet, data relative to the cursor coordinates, execution time, and pen pressure were recorded. Our instructions further specified that participants were able to trace a circle (50 mm radius), starting from 12 o’clock as precisely as possible with no emphasis on the speed of execution. During the task execution, both the cursor position and trajectory were visible. After 4 weeks, the participants were asked again to trace the circle with the same instructions.

Figure 1.

Setup. Diagram illustrating the experimental setup. Each subject was presented a circle template projected on a monitor. The table height was adjustable so as to allow for a comfortable performance. Subjects were instructed to trace the presented circle as accurately as possible.

Pressure data

The pressure values were recorded directly from the tablet as normalized values (from 0 to 100%). As the scope of this study was that of a longitudinal comparison across subjects (i.e. improvement over time), only the normalized values were used, similar to other studies¹⁸ and considering that the same tablet and setup were used by all participants in the study.

Analysis

Circle-tracing analysis consisted of calculation of traced circle radii, measured as point distances from the template’s center (i.e. radius). To avoid overestimations, the tracing of the circle was first reduced to 360 points (1 point per angle). Following that, for each point drawn, the distance from said point to the template center was calculated and was considered as a measure for the radius for said point. For each measured radius, deviations from the template’s radius were also calculated (i.e. radius error). Since we are interested in overall error, the radius error values were considered as absolute values. Furthermore, as a measure of accuracy we considered the coefficient of variation (CV) of the radii, bearing in mind that for a perfect circle the variability would be zero.

Statistics

Considering the small sample size in this study, data were analyzed using nonparametric methods. For comparison between groups, we used the Mann–Whitney U test, a commonly used nonparametric approach for comparison of independent variables (i.e. different subjects) on the CVs, radius error, execution time and pen pressure for both the initial assessment and 4-week assessment. For comparison between sessions, we used the Wilcoxon Signed-Rank test, a commonly used nonparametric approach, repeated measures (i.e. same subject at different times) on the CVs, radius error, execution time, pen pressure, and ISNCSCI scores. The Spearman correlation coefficient was used on the ISNCSCI scores and pen pressure values for both the initial assessment and 4-week assessment.

Results

Radius CV

Mean CVs for the patient group were 0.10 ± 0.06 for the initial assessment and 0.08 ± 0.05 after 4 weeks (Table 2). For the control group, CVs for the initial assessment were 0.12 ± 0.07 and 0.13 ± 0.10 after 4 weeks (Table 3). CV between patients and control did not reveal any significant differences for the initial assessment (Mann–Whitney U = 36, n1 = n2 = 10, P = .315) nor for after 4 weeks (Mann–Whitney U = 41, n1 = n2 = 10, P = .529). For the control group, Wilcoxon Signed-rank test did not reveal any significant differences between the CVs of the initial assessment and after 4 weeks (W = 24, Z = –.356, P = .721). No significant differences were found also for the patient group between the initial assessment and after 4 weeks (W = 23, Z = –.459, P = .646).

Table 2.

Patient results.

Patient	Initial assessment				Assessment after 4 weeks
	CV	Error (mm)	Time (sec)	Pressure (%)	CV	Error (mm)	Time (sec)	Pressure (%)
1	0.052	2.2 ± 1.4	43.6	22.8 ± 7.4	0.050	2.2 ± 1.2	55.3	41.3 ± 7.8
2	0.096	4.2 ± 2.3	48.2	19.4 ± 6.9	0.038	2.0 ± 1.3	33.6	71.6 ± 6.2
3	0.050	3.8 ± 2.5	14.1	19.6 ± 4.4	0.127	5.8 ± 2.8	26.6	34.1 ± 5.9
4	0.137	6.1 ± 3.5	61.1	24.1 ± 4.3	0.134	6.1 ± 3.3	43.3	45.9 ± 10.8
5	0.108	12.7 ± 6.7	2.3	35.6 ± 10.1	0.219	16.0 ± 13.3	5.8	43.1 ± 4.0
6	0.043	2.0 ± 1.9	36.5	21.6 ± 6.3	0.019	0.8 ± 0.4	48.2	23.3 ± 7.2
7	0.049	2.2 ± 1.1	58.4	80.6 ± 16.0	0.084	3.7 ± 1.8	81.2	82.3 ± 8.0
8	0.090	3.8 ± 2.3	13.2	55.2 ± 6.9	0.090	3.9 ± 2.1	56.3	39.7 ± 11.5
9	0.263	25.6 ± 18.0	6.2	24.8 ± 9.7	0.059	13.5 ± 3.7	7.4	52.2 ± 13.1
10	0.120	5.3 ± 2.7	53.2	13.7 ± 6.0	0.049	2.1 ± 1.4	61.8	68.3 ± 8.7

Table 3.

Control results.

Controls	Initial assessment				Assessment after 4 weeks
	CV	Error (mm)	Time (sec)	Pressure (%)	CV	Error (mm)	Time (sec)	Pressure (%)
1	0.061	2.5 ± 1.7	34.8	61.8 ± 6.1	0.027	1.1 ± 0.7	35.4	73.8 ± 4.3
2	0.019	5.5 ± 2.7	31.0	69.8 ± 6.5	0.030	3.2 ± 1.5	33.4	74.9 ± 9.0
3	0.234	0.8 ± 0.5	30.8	84.8 ± 6.9	0.196	1.3 ± 0.7	33.3	91.6 ± 7.5
4	0.156	1.1 ± 0.6	34.0	83.8 ± 8.0	0.257	2.0 ± 0.8	34.1	86.4 ± 8.6
5	0.122	10.4 ± 4.6	15.3	76.0 ± 6.6	0.072	8.7 ± 4.0	17.9	85.5 ± 10.5
6	0.026	7.3 ± 3.3	23.0	73.3 ± 8.8	0.043	5.8 ± 2.4	17.5	81.4 ± 8.4
7	0.163	6.9 ± 3.3	15.2	97.6 ± 8.5	0.127	11.7 ± 4.3	13.4	87.0 ± 8.4
8	0.110	4.9 ± 2.4	29.6	69.3 ± 2.9	0.076	3.4 ± 1.6	21.1	81.0 ± 7.0
9	0.236	10.5 ± 4.7	11.7	95.5 ± 5.5	0.353	15.7 ± 6.1	9.4	84.8 ± 9.3
10	0.144	6.5 ± 2.8	17.6	86.1 ± 7.4	0.135	6.1 ± 2.6	12.6	73.8 ± 8.1

Radius error

Mean radius error for the patient group in the initial assessment was 6.8 ± 7.3 mm and 5.6 ± 5.1 mm after 4 weeks (Table 2). Though there was a slight improvement between the performances, there were no statistically significant differences (W = 24, Z = –.357, P = .720). The same was true also for the control group, which measured 5.6 ± 3.4 mm in the initial assessment and 5.9 ± 4.8 mm after 4 weeks (Table 3). Again, no significant differences were found between the performances (W = 24, Z = –.357, P = .721). Radius error between patients and control did not reveal any significant differences for the initial assessment (Mann–Whitney U = 56, n1 = n2 = 10, P  = .684) nor for after 4 weeks (Mann–Whitney U = 50, n1 = n2 = 10, P  = .0.99).

Execution time

Mean execution time for the patient group in the initial assessment was 33.7 ± 22.6 sec and 42.0 ± 23.9 sec after 4 weeks (Table 2). There were no statistically significant differences between assessments (W =  40, Z = 1.27, P  = .230). The same was true also for the control group which measured 24.3 ± 8.7 sec in the initial assessment and 22.8 ± 10.2 sec after 4 weeks (Table 3). Again, no significant differences were found between the performances (W = 21, Z = –.663, P = .508). Mean execution time between patients and control did not reveal any significant differences for the initial assessment (Mann–Whitney U = 38, n1 = n2 = 10, P = .393) nor for after 4 weeks (Mann–Whitney U = 26, n1 = n2 = 10, P = 0.07).

Pen pressure

Mean pen pressure for the patient group was 31.7 ± 20.7 for the initial assessment, increasing to 50.2 ± 18.4 after 4 weeks (Table 2). For the control group, pen pressure values for the initial assessment were 79.8 ± 11.7 and 82.0 ± 6.1 after 4 weeks (Table 3). Significant differences were found between patients and control for the initial assessment (Mann–Whitney U = 5, n1 = n2 = 10, P < .001) as well as after 4 weeks (Mann–Whitney U = 95, n1 = n2 = 10, P < .001). For the control group, Wilcoxon Signed-rank test did not reveal any significant differences between the pen pressure of the initial assessment and after 4 weeks (W = 32, Z = .459, P = .646). For the patient group, significant differences were found between the initial assessment and after 4 weeks (W = 50, Z  = 2.293, P < .05 (P = .022); Figure 2).

Figure 2.

Pen pressure results. The bar plots represent the mean and standard deviations of the pressure values obtained for each of the experimental groups in the initial assessment (on the left side), and after 4 weeks (on the right side). It is possible to note that while no significant differences were found for the controls groups (blue), significant differences were found for the patients’ groups (red) both between assessments, and between the controls for both assessments.

Clinical assessment

Patient force scores for upper limb force (Table 1) measured 15.3 ± 3.2 for the initial assessment, increasing to 20.1 ± 4.4 after 4 weeks, which proved to be significantly different (W = 45, Z  = 2.267, P < .05 (P = .007)). A moderate correlation was found between pressure values for the initial assessment in patients and force scores (r = .324, P = .360). A higher, yet still moderate, correlation was found between force score and pressure after 4 weeks (r = .469, P = .171).

Discussion

This study investigated the use of a circle-tracing task for evaluating upper limb functional recovery in cervical SCI patients. As expected, a general improvement was found in all SCI patients after 4 weeks for both ISNCSCI scores as well as general force (Table 1). When compared with controls, significant differences were found for pen pressure at both the initial assessment as well as after 4 weeks (Figure 2). Moreover, significant differences were found for pen pressure in the SCI patients between the initial assessment and after 4 weeks of assessment (Figure 2). Surprisingly, no significant correlations were found between force measurements and pen pressure, both within the initial assessment as well as after 4 weeks. Also, no significant differences were found in performance accuracy (CVs and radius error) between SCI patients and controls, both for the initial assessment and after 4 weeks (Tables 2 and 3).

The improvements in pressure measurement between the sessions for the SCI, corresponding to the improvement in ISNCSCI scores for force, were somewhat expected. These improvements may be due to the fact that the patients in this study were all acute lesion patients and, as such, may be subject to spontaneous functional recovery over time.²² It should also be considered that during the 4-week interval, all patients participated in occupational therapy sessions, which consisted in daily sessions lasting 60 min plus 90 min of physical therapy for each patient. During the occupational therapy sessions, patients tried out and trained their upper limb abilities through preparatory exercises and activities, in addition to activities of daily living (ADLs) training. They performed grasp\release exercises, full grip, power grip, finger scissor, finger spread, thumb touch and writing activities, and fine motor activity according to their motor capabilities and their injury level. The ADLs training focused on self-care activities; moreover, patients performed therapeutic activities in leisure and productivity areas. Therefore, we cannot exclude the fact that the improvements in performances are due to intervention, though in order to conclude the specific contribution a specific study should be formulated. Still, given the complexity of occupational therapy intervention, there is a strong need for reliable and accurate assessment measures, in order to monitor the progression of functional recovery and deliver a tailored and effective treatment. The evaluation instrument presented in this paper grants an objective assessment for therapists and increase patients’ awareness of their motor skills and performance.

Interestingly, the pen pressure result did not correlate with the clinical scores. This may be due to the fact that clinical scores, though standardized, are more subjective in nature and as such are subject to error and bias in human judgement,²³ whereas the pen pressure data are an objective measurements. Though in clinical settings, often times the need for precise measurements is not needed, still precise objective measurements can benefit practitioners when tailoring interventions to meet specific patient needs. Another element of discrepancy could be related to the higher resolution of the pen pressure results (1024 pressure levels for the tablet used in this study, meaning that between the 0 and 100% of recorded pressure the tablet can discriminate between increments of 0.0977%) compared to the clinical scores (measured from 0 to 5) which may evidence subclinical details.²⁴ Consequently, the discrepancy between measurements may be due to the fact that the pen pressure results, by having a higher resolution compared to the clinical scores, are more sensitive to improvement. As such, the magnitude of improvement does not correlate between measurements.

It should be mentioned that pen pressure profiles obtained during the trials, other than the mere quantification of hand function, may provide some additional useful information. Considering that the shape used during the task (i.e. a circle) covers a wide and continuous range of motion, involving the use of different muscles in different phases of the execution, examination of the pressure profile may provide direction specific functional deficits. When performances between controls and patients are confronted it is possible to notice that controls, a part from registering higher pressure values, have a more constant and sustained pressure compared to an oscillating one in patients. Moreover, examination of specific pressure profiles in patients demonstrates that certain directions of the execution are more difficulty controlled than other. This knowledge can be useful to guide intervention, targeting specific muscle groups (Figure 3).

Figure 3.

Pressure profile comparison. Within the figure the pressure profiles of a control subject (blue) and a SCI patient (red) are compared for each direction of movement during the execution of the circle tracing. The pressure profiles for each corresponding segment of execution are highlighted sequentially (from left to right). It is possible to not that the control subject, a part from registering higher pressure values, has a more constant and sustained pressure compared to an oscillating one registered in the patient. Specifically, lower and more oscillating values for the patient were registered for the downward motion, specifically the first quarter of the circle.

The lack of improvement for accuracy between assessments is partially expected, as it was previously shown that the learning effect is discrete for tracing tasks, even for performances that are relatively close to each other.¹⁰ To support this, the control group enrolled in the study also did not show any significant improvement in precision. However, a relatively surprising result from this study is the fact that no differences were found in terms of performance accuracy between SCI patients and controls. However, as it was previously shown, it is possible that subjects may have their own inherit accuracy for fine motor control tasks.¹¹ Therefore, as long as the task may be executed, that same accuracy is maintained. Furthermore, as there were no task constraints, such as timing, the execution at a comfortable speed may be a determining factor for maintaining accuracy during performances.²⁵ In fact, although there were no significant differences between execution time, the time for the patient group was slower compared to the controls.

Disclaimer statements

Contributions None.

Funding None.

Conflict of interest Authors have no conflict of interests to declare.