New Insights from Clinical Assessment of Upper Extremities in Cervical Traumatic Spinal Cord Injury

Abstract

Upper extremity function has a strong impact on the quality of life in cervical spinal cord–injured patients. Upper extremity function depends on many factors, such as muscle strength, level of lesion, and extension of the cord damage in its axial axis produced by the injury. These variables can be obtained by the International Standards for Neurological Classification of Spinal Cord Injury, which is the standard for the functional evaluation of traumatic spinal cord injury (SCI) patients. The aim of this study was to describe the relationship between upper limb muscle strength, level of injury, and axial damage with the functionality of upper limb measured using the Jebsen-Taylor Hand Function Test (JTHFT) and the 9 Hole Peg Test (9HPT) in cervical SCI. Twenty-nine patients were included in this study. Our results suggest that both the JTHFT and 9HPT can be similarly used to quantify functional impairment after cervical SCI. Moreover, our data suggest that the upper extremity motor score, JTHFT, and 9HPT strongly correlate with the American Spinal Injury Association (ASIA) impairment scale (graded from A to E), but not with the lesion level. Our findings can be of great importance for the clinician or researchers whose therapeutic interventions have as a main objective to improve upper limb functionality in patients with cervical SCI. We suggest that ASIA impairment scale, ASIA motor score, and functional tests (including JTHFT and/or 9HPT) could be used as outcome measures in cervical SCI clinical trials.

Introduction

Spinal cord injury (SCI) has a great impact on the quality of life of affected people.¹ The functionality of the upper limb has a considerable impact on the quality of life of the patient with cervical SCI. In fact, 75–80% of these patients indicated that an important to very important improvement in the quality of their lives was related to an improvement in hand function.² Therefore, attending to the incidence of the cervical SCI and the impact of the functionality of the upper limb function in their quality of life, it seems relevant to wonder about the evaluation, rehabilitation treatments, and future restorative approaches of the functionality of the upper limb in tetraplegic patients.

The American Spinal Injury Association (ASIA) scale is the standard evaluation of the SCI patients; it includes muscle function grading, sensory grading, lesion level, and ASIA impairment scale (AIS). AIS is used to classify the patients in five main groups (A–E).³ It would be conceivable that upper limb functions should be related to the cervical lesion level and to the AIS. However, some authors suggest that the International Standards for Neurological Classification of Spinal Cord Injury (ISNCSCI), the level of lesion, and the ASIA impairment scale are not linked with the functionality of the upper limb.⁴ It also has been suggested that other factors, such as strength, sensibility, or even the motivation of the patient, is more related to this functionality in the upper limb.⁵

The aim of this study was to examine the relationship between lesion level, AIS, and muscle strength on the hand function in subjects with cervical SCI. We estimated the severity of SCI using the AIS (A-E). We evaluated the lesion level and the AIS following the ASIA scale guidelines and we quantified the upper limb motor score by using the upper limb motor score of the ASIA scale.

Moreover, we evaluated hand function using the Jebsen-Taylor Hand Function Test (JTHFT) and the Nine Hole Peg Test (9HPT). The JTHFT is a standardized measure for assessment of hand function that is reliable and valid for use with SCI subjects.^6,7 The 9-HPT is a brief standardized and quantitative test of upper extremity function.⁷

It is important to note that general function in SCI patients is frequently measured using the Functional Independence Measure (FIM) and/or the Spinal Cord Independence Measure (SCIM). However, these tests refer to the general situation of the patient and his/her relationship with the environment. Often, FIM and SCIM are considered to provide an indirect measure of upper limb functions (self-care and mobility sub-sections). On the other hand, these tests do not specifically evaluate hand function. Therefore, we decided to test JTHFT and 9HPT, which have been extensively validated in other neurological disorders, as more reliable tests for upper limb function.

Twenty-nine SCI subjects participated in this study: 21 men, eight women (mean age, 40.3 ± 15.3 years). The inclusion criteria were cervical SCI rostral to T1 and age of 18 to 70 years. Cervical SCI classified as central cord syndrome were excluded (n = 2). Patients provided informed consent and the study was approved by the local ethical committee. We used the ISNCSCI to classify subjects.³

Hand function assessment tests

Upper extremity motor score

The ASIA Motor Index Score uses standard manual muscle testing on a 6-grade scale: absent = 0; trace = 1, visible or palpable contraction; poor = 2, active movement through range of motion with gravity eliminated; fair = 3, active movement through range of motion against gravity; good = 4, active movement through range of motion against resistance; normal = 5; and NT = not testable. The key muscles/functions included in the ASIA Motor Index Score are elbow flexors, wrist extensors, elbow extensors, finger flexors, hand intrinsic, hip flexors, knee extensors, ankle dorsi flexors, long toe extensors, and ankle plantar flexors, with a possible total motor score of 100. The motor score was obtained from the clinical reports of the patients. For analysis purpose, we used only the upper limb subscore (score from 0 to 50). We will refer to this variable as the upper extremity motor score (UEMS).

JTHFT

The JTHFT is a standardized measure that consists of seven functional tasks that require finger and hand movement. The JTHFT is a widely used for the assessment of functional hand motor skills.^7
–9 It has good validity and reliability, and normative data are available for different ages and both genders.^8,9 The seven JTHFT tasks to be addressed are: turning over cards; picking up small objects and placing them in a can; picking up small objects with a teaspoon and placing them in a can mimicking a feeding function; stacking checkers; moving large light cans; moving heavy cans; and a writing task. Patients were instructed to perform the tasks as rapidly and accurately as possible according to written standardized instructions in the testing set.^8
–10 Total JTHFT time and partial subtest JTHFT times were recorded for analysis. Feedback on task performance was not provided. Dropping of an object (cards, small objects, and cans) was counted as an accuracy error and analyzed off-line. In our case, the writing task was not included in the JTHFT total score. When a subtest was not possible to be performed, it was scored with 60 seconds, as maximal score.

9HPT

The 9HPT is a brief, standardized, quantitative test of upper extremity function. The dominant and non-dominant hands are tested three times. The 9HPT was developed by Kellor and colleagues¹¹ with the purpose of measure the dexterity; it has a good inter-rater reliability.⁷ The 9HPT requires a small shallow container holding nine pegs and a plastic block containing nine empty holes. On a start command when a stopwatch is started, the patient picks up the nine pegs one at a time as quickly as possible, puts them in the nine holes, and, once they are in the holes, removes them again as quickly as possible one at a time, replacing them into the shallow container.¹² The total time to complete the task is recorded. A trial with the dominant hand is immediately followed by a trial with the non-dominant hand. The complete procedure was repeated three times and the three times obtained were averaged to obtain the final 9HPT score. When the test was not possible to be performed, it was scored with 120 sec as maximal score.

For the JTHFT and 9HPT, subjects were seated in front of a table in a well-illuminated room and constant temperature. They were instructed to concentrate during the entire performance, to do it as quickly and accurately as possible, and not to talk unless required to.

Statistical analysis

Descriptive statistics were used to summarize the scores. Mean and standard deviation were reported (mean ± standard deviation). The relationships between the UEMS and the JTHFT and 9HPT were analyzed using the Pearson correlation test. The relationships between the clinical variables neurological level of lesion (a value from 1 = C1 to 9 = T1 was used for non-parametrical correlation) and the AIS (categorized from A to E) and the UEMS, and the functional variables (JTHFT and 9HPT) were analyzed using the Spearman's correlation test (Fig. 1).

FIG. 1.

(A) Correlation between American Spinal Injury Association (AISA) motor score as a measure of the muscle strength and ASIA impairment scale (AIS) as measure of the axial section damage. (B) Correlation between the Jebsen-Taylor Hand Function Test (JTHFT) as a measure of upper limb functionality and AIS. (C) Correlation between a functionality measure (JTHFH) and a muscle strength measure (ASIA Motor Score).

Results

Mean UEMS was 25.3 ± 12.1, mean JTHFT was 161.3 ± 120.4 sec and mean 9HPT was 80.96 ± 33.54 sec. As expected, 9HPT was significantly correlated to the JTHFT (r = 0.808; p = 0.000), and UEMS was significantly negatively correlated to both the JTHFT (r = −0.658; p = 0.000) and the 9HPT (r = −0.550; p = 0.001). AIS was significantly correlated to the JTHFT (Rho = 0.577; p = 0.001) and to the 9HPT (Rho = 0.396; p = 0.034). Moreover, AIS was significantly correlated to the UEMS (Rho = 0.601; p = 0.001). Lesion level was not correlated to the JTHFT (Rho = −0.193; p = 0.316), and UEMS (Rho = 0.305; p = 0.108) and it showed a weak correlation with the 9HPT (Rho = −0.369; p = 0.049).

Discussion

Our results suggest that both JTHFT and 9HPT can be similarly used to quantify the functional impairment after cervical SCI. Moreover, both functional tests reflect the global strengths of upper limbs; the higher the motor score, the faster the tests execution. Moreover, our data suggest that UEMS, JTHFT, and 9HPT strongly correlate with the AIS but not with the lesion level (Fig. 1).

Our data are partially in agreement with those from Thorsen and colleagues⁴ that reported that the lesion levels are not correlated with the functionality of the upper limb, and therefore suggest that the upper limb functionality has to be specifically addressed. On the other hand, our data differ from those of Thorsen and colleagues⁴ as we found a correlation between AIS and upper limb functionality. This difference could be due to the different hand function tests used in the two studies.

Theoretically, the cervical SCI may affect the hand functions in different ways, depending on the lesion level and the axial section damage.^6,13
–15 There is a direct relationship between the lesion level and the amount of affected myotomes. Moreover, hand function may depend on how much strength is preserved independently of the lesion level and on the damage on the axial section.^6,13
–15 The AIS provides a gross measure of the spinal cord damage in its axial section: The more extended is the axial section damage, the more severe is the clinical lesion. For example, a complete transection of the spinal cord produces (at least theoretically) a complete SCI lesion (AIS-A). It also presents a direct relationship between the axial section damage and the amount of affected corticospinal connections.^6,13
–15 We confirmed the relationship between the axial damage and the global strength with upper limb functions, whereas we failed to find a correlation between the lesion level and the upper limb function. Our findings can be of great importance for clinicians or researchers whose therapeutic interventions have as main objective to improve upper limb functionality in patients with cervical SCI. We suggest that AIS, ASIA motor score, and functional tests (including JTHFT and/or 9HPT) could be used as outcome measures. Moreover, AIS and functional tests can provide valuable indirect information about the corticospinal function.^13
–15

JTHFT and 9HPT repeatedly have been shown to be valid indicators of upper limb function in neurological and traumatic pathologies.^7
–9,12,16 Some other tests are appropriate for the measurement of hand function in SCI patients, for example the Graded Redefined Assessment of Strength, Sensibility and Prehension or the Capabilities of Upper Extremity Test, among others.^5,17 However, we chose JTHFT and 9HPT because they can be completed in a short period of time. This aspect is important because in clinical trials, patients typically undergo a huge number of clinical, neurophysiological and radiological evaluations. Sparing time will improve the quality of data collecting. Moreover, JTHFT and 9HPT measure one hand at a time, reducing possible bimanual interactions and compensations.

We would like to underline some limitations of our study: a) sensibility and proprioception were not measured; b) spasticity and pain were not taken into account; c) different drugs normally taken by the SCI patients can affect hand motor evaluation; and d) at least two mechanisms can cause the hand dysfunction (descending and ascending pathway damage and direct damage of spinal motorneurons and cervical roots). Even with these limitations, we consider our data to provide a picture of hand motor function of real SCI patients.

Moreover, these tests can provide accurate and reproducible information not only about the initial assessment of damage severity, but also about hand function evolution afterwards. Finally, because of the easy and fast application of these tests for both clinicians and patients, we would like to recommend their use in a more extended way in clinical practice, even in SCI patients. In order to evaluate the real benefit of these tests, more studies are required.

Footnotes

Author Disclosure Statement

No existing financial interests exist.

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