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Original Research Articles

Chronic Poststroke Deficits in Gross and Fine Motor Control of the Ipsilesional Upper Limb

Johnson, Brian P. OTR/L, PhD; Westlake, Kelly P. PT, PhD

Author Information
American Journal of Physical Medicine & Rehabilitation: April 2021 - Volume 100 - Issue 4 - p 345-348
doi: 10.1097/PHM.0000000000001569
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Abstract

What Is Known

  • Individuals with stroke often experience deficits in motor control of the ipsilesional arm.

What Is New

  • Ipsilesional deficits in hand dexterity can be measured with commonly used outcomes such as the Nine-Hole Peg Test and the Box and Blocks Test.

After unilateral stroke, sensorimotor impairment is present in both the contralesional and ipsilesional upper limbs (ULs).1–3 Although impairments of the contralesional UL can be directly attributed to the lesion location, impairments of the ipsilesional UL may be due to a multitude of factors. First, a small proportion of corticospinal tract fibers do not cross to the contralateral spinal cord.4,5 Although the extent to which this small number of corticospinal fibers contribute to ipsilateral UL control may generally be minimal, disruption of these fibers after a lesion may contribute to functional deficits. Second, there is much evidence to support bilateral reorganization of the sensorimotor cortices and corticospinal tracts.6,7 Examples include increased activity of the contralesional motor cortex during ipsilesional hand movement and increased inhibition arising from the contralesional to ipsilesional motor cortex after a stroke. Third, a growing body of research supports the dynamic dominance hypothesis, in which each hemisphere of the brain contributes to separate parameters of movement control.8,9 During reaching, this theory posits that the dominant hemisphere contributes to coding the trajectory of movement, whereas the nondominant hemisphere contributes to coding the final positions for movement. Similar findings have been reported in individuals with unilateral stroke. Left hemispheric lesions impact the movement trajectory of both ULs, whereas right hemispheric lesions affect coordination of the final position of movement in both ULs.10,11 Lastly, higher-level cognitive constructs such as praxis and visuospatial processing are important to sensorimotor control. Thus, a lesion that impacts these neural processes can also have a negative effect on UL functioning, for example, through the disruption of visuomotor transformation processing.12–15

Impairments in ipsilesional UL have been found during the acute (i.e., <3 mos), subacute (3–6 mos), and chronic (i.e., >6 mos) stages of recovery post-stroke.3,12,15–18 During the chronic post-stroke stage, these impairments can impact functional outcomes of fine dexterity, such as the Jebsen Taylor Hand Function Test2,11,15,19 and Purdue Pegboard Test.20 Fine dexterity impairments in ipsilesional UL performance of the Nine-Hole Peg Test have also been identified during the acute and subacute post-stroke phases.18,21

What remains unknown is the impact that ipsilesional UL impairments may have on gross dexterity during the chronic phase of post-stroke recovery. Impairments in ipsilesional fine dexterity at this stage have been identified, but evidence of distinct neural pathways between fine and gross dexterous function suggests that the recovery of fine and gross dexterous function may progress independent of one another.22,23 Therefore, the primary aim of this study was to investigate fine dexterity via the Nine-Hole Peg Test and gross dexterity via the Box and Blocks Test in the ipsilesional UL of individuals with chronic stroke. The findings of this study will build upon previous research demonstrating ipsilesional UL functional deficits in individuals with chronic stroke, thereby assisting clinicians in evidence-based clinical decisions, and can lead to additional lines of mechanistic research questions.

MATERIALS AND METHODS

Institutional review board approval was obtained before initiation of the current research. All individuals provided written informed consent before participating in this study. Inclusion criteria for participants with stroke were as follows: unilateral stroke more than 6 mos before study participation, with continued motor impairment; all conventional therapy completed; 50–80 yrs of age; and right hand dominance before stroke (Edinburgh Handedness Inventory of ≥75 for right hand dominance). Control participants were included if they were within 5 yrs of age and same sex of a recruited study participant with stroke and were right hand dominant (Edinburgh Handedness Inventory of ≥75 for right hand dominance). The exclusion criteria for all participants were as follows: psychologic, neurologic, cardiovascular, or other diagnosis that would impair participation; mild cognitive impairment (i.e., <27 on the Montreal Cognitive Assessment); and attentional or executive function deficits (i.e., <5 on Digit Span Forward Test). Adult normative values for both the Nine-Hole Peg Test24 and Box and Blocks Test25 were used as an additional comparison, matching for age, sex, and UL (left or right) used.

All testing procedures occurred during a single session and were performed by a single occupational therapist. The Nine-Hole Peg Test and Box and Blocks Test were administered to all participants. Briefly, the Nine-Hole Peg Test is a measure of dexterity and involves unimanually placing and removing nine pegs into and out of nine holes one at a time. The Box and Blocks Test is a measure of gross manual dexterity and involves unimanually grasping and transporting as many wooden cubes as possible (out of 150) over a partition one at a time for 60 secs. The Nine-Hole Peg Test and Box and Blocks Test were administered in random order per the standardized original procedures and instructions.24,25 The Fugl Meyer UE Scale of Motor Impairment was also assessed, with higher scores indicating less impairment (of a total of 66).26

All statistical analyses were conducted using the Statistical Package for the Social Sciences version 22 (IBM Corp, Armonk, NY). Kolmogorov-Smirnov tests, skewness, and kurtosis values were used to assess the normality of the data for each variable and to subsequently determine the applicability of parametric or nonparametric statistical analyses. The Kruskal-Wallis nonparametric analysis of variance was used to analyze between-group differences for the Nine-Hole Peg Test and Box and Blocks Test, with Dunn pairwise post hoc tests controlled for multiple comparisons performed in cases of significance. The Mann-Whitney U test was used to compare age between individuals with stroke and age-matched healthy controls. The Wilcoxon’s signed rank test and paired t-test were used to analyze within-group differences between ipsilesional and contralesional UL performance on the Nine-Hole Peg Test and Box and Blocks Test, respectively. Dominant UL scores were included in the analyses for the control group unless otherwise stated. Significance for all statistical analyses was set to an alpha of 0.05. All data are presented as mean (standard deviation) unless otherwise stated.

RESULTS

Participant Characteristics

There were 30 total participants in this study. Descriptive data for each group are provided in Table 1. There was no statistical difference in age between individuals with stroke and the control group (mean difference [95% confidence interval (CI)], −4.50 [−10.89 to 1.89] yrs; U = 133.00, P = 0.16).

TABLE 1 - Participant characteristics
Stroke Controls
n 20 10
Age, yearsa 62.3 (7.6) 66.8 (9.0)
Sex ratio (F:M) 9:11 5:5
Years since strokeb 7.8 (6.0)
Stroke hemisphere (L:R) 13:7
UL motor impairment (Fugl-Meyer)a 39.6 (4.5)
aMean (SD).
bMedian.

The Nine-Hole Peg Test

The result of the Kruskal-Wallis nonparametric analysis of variance demonstrated a significant main effect of group (X22 = 27.81, P < 0.01), indicating that at least one between-group difference was present regarding completion of the Nine-Hole Peg Test (Table 2). Subsequent pairwise comparisons (Fig. 1) indicated that individuals with stroke completed the Nine-Hole Peg Test with their ipsilesional UL significantly slower than both the normative scores (mean difference [95% CI], 6.5 [4.0–9.1] secs; P < 0.01) and the control group (mean difference [95% CI], 3.4 [−0.5 to 7.3] secs; P = 0.01), with the normative scores also significantly faster than the control group (mean difference [95% CI], −2.91 [−4.21 to −1.61] secs; P = 0.01). Of the eight individuals with stroke able to perform the Nine-Hole Peg Test with both the ipsilesional and contralesional ULs, slower times were demonstrated when using the contralesional UL compared with their ipsilesional UL (mean difference [95% CI], −9.4 [−20.2 to 1.4] secs; Z(6) = 34.00, P = 0.03) (Fig. 1).

TABLE 2 - Nine-Hole Peg Test
Ipsilesional UL Contralesional UL Normative Controls
n 20 8 20 10
Nine-Hole Peg Test, seconds 27.0 (5.6) 34.8 (15.6) 20.5 (1.0) 23.7 (3.2)
Data are presented as mean (SD).

FIGURE 1
FIGURE 1:
Plot of Nine-Hole Peg Test scores. Bars = mean; whiskers = standard deviation; circles = individual data points with connecting lines between ipsilesional and contralesional points for the same participant, when available. *P ≤ 0.05.

The Box and Blocks Test

The results of the Kruskal-Wallis nonparametric analysis of variance demonstrated a significant main effect of group (X22 = 24.56, P < 0.01), indicating that at least one between-group difference was present regarding completion of the Box and Blocks Test (Table 3). Subsequent pairwise comparisons (Fig. 2) indicated that individuals with stroke transferred significantly fewer blocks over the partition during the Box and Blocks Test using their ipsilesional UL than both the normative scores (mean difference [95% CI], −15.3 [−20.1 to −10.5] blocks; P < 0.01) and the control group (mean difference [95% CI], −12.3 [−20.3 to −4.2] blocks; P < 0.01), whereas there was no difference between the normative scores and the control group (mean difference [95% CI], 3.53 [−1.84 to 8.88] blocks; P = 1.00). Individuals with stroke transported fewer blocks over the partition during the Box and Blocks Test when using their contralesional UL compared with their ipsilesional UL (mean difference [95% CI], 33.2 [20.9–45.5] blocks; t18 = 5.30, P < 0.01) (Fig. 2).

TABLE 3 - Box and Blocks Test
Ipsilesional UL Contralesional UL Normative Controls
n 20 8 20 10
Box and Blocks Test (blocks) 56.8 (10.1) 24.8 (28.2) 72.0 (3.3) 69.0 (10.1)
Data are presented as mean (SD).

FIGURE 2
FIGURE 2:
Plot of Box and Blocks Test scores. Bars = mean; whiskers = standard deviation; circles = individual data points with connecting lines between ipsilesional and contralesional points. *P ≤ 0.05.

DISCUSSION

A common clinical focus while treating individuals with a history of stroke involves focusing on restoring function in the contralateral and not ipsilesional UL. This study sought to identify deficits in ipsilesional UL dexterity in individuals with chronic stroke. The Nine-Hole Peg Test was administered to corroborate past findings of ipsilesional UL fine dexterity deficits, whereas the Box and Blocks Test was administered to investigate gross dexterity. The primary result was that even in the chronic stage after the completion of all formal rehabilitation, individuals continued to demonstrate reduced ipsilesional UL fine and gross motor dexterity.

The presence of ipsilesional UL deficits may be due to the extent of impairment of the contralesional UL.27 Participants in the current study demonstrated moderate to mild level of contralesional impairment as defined by previously established cutoff scores for the Fugl Meyer UE.28 That is, participants demonstrated a limited ability to move the contralesional UL out of synergistic motor patterns. Individuals with a similar level of impairment have been found to demonstrate a tendency to recruit contralesional brain regions more so than those with milder impairment.29 This bihemispheric activation may therefore interfere with ipsilesional UL motor output and possibly account for the ipsilesional UL deficits reported here. Future research should therefore aim to include a range of impairments, from mild to severe, to determine the existence of a relationship between contralesional and ipsilesional UL deficits.

Reduced dexterity of the ipsilesional ULs was found despite the variability in lesion locations (13 dominant hemisphere, 7 nondominant hemisphere). As stated earlier, the dynamic dominance model of motor control posits that dominant and nondominant brain hemispheres contribute differentially to UL motor control.8,9 The dominant hemisphere codes precise movement trajectories under predictable conditions, whereas the nondominant hemisphere codes impedance control mechanisms to enable stabilization against unanticipated internal and external forces.30 In the current study, differences in lesion location may have led to different motor control deficits, although the end result of impaired functional dexterity was same. For example, participants with dominant hemisphere lesions may have experienced a reduced ability to modulate acceleration and movement amplitude along the reaching path, whereas those with nondominant hemisphere damage may have experienced reduced ability to achieve stability when faced with target errors at the end point of either grasping or placing the peg or block. Future investigations of the kinematic and kinetic differences in individuals with dominant vs. nondominant hemispheric stroke while performing measures of dexterity may provide further insights into the possible mechanistic differences.

The results of this study provide clinicians evidence and insights as to which tools to use to quantitatively assess ipsilesional UL deficits. The Nine-Hole Peg Test and Box and Blocks Test are of high clinical utility because of the speed of assessment, sound psychometric properties, low cost, and widespread clinical use and availability.24,25 Moreover, the standard administration of these tests already requires measurement of both contralesional and ipsilesional UEs. Taking into consideration the score of each UL and comparing these scores with normative values can thus provide clinicians with valuable information as to the presence and extent of ipsilesional UL deficits without additional clinical testing. These clinical findings can then be used to assist in planning treatment regimens and potentially lead to improved UL function of both limbs.

There are several limitations to this study worth mentioning. First, the sample size of this study was not large enough to allow for an examination of the effect of laterality of stroke lesion on ipsilesional UL performance. Second, potential participants were not tested for perceptual dysfunction beyond the information provided by the Montreal Cognitive Assessment. Therefore, that perceptual dysfunctions may have influenced the results of this study cannot be ruled out.

Overall, this study found that ipsilesional UL motor function deficits are measurable years after the occurrence of a stroke. Furthermore, these ipsilesional UL deficits can be measured with commonly used clinical outcome measures. These results are of particular clinical interest given that physical rehabilitation treatment is often solely focused on the contralesional UL, which may be at the expense of ipsilesional UL function. The current results, in conjunction with those of previous studies regarding ipsilesional motor deficits, suggest that an approach of motor remediation of the ipsilesional UL is also appropriate and may even be necessary. At the very least, inclusion of an assessment of ipsilesional UL deficits is recommended to appropriately guide intervention approaches.

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Keywords:

Stroke; Ipsilesional; Physical Rehabilitation; Motor Control

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