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April 2023; 13 (2) Research ArticleOpen Access

Isolating Neurologic Deficits in Cervical Spondylotic Myelopathy

A Case-Controlled Study, Using the NIH Toolbox Motor Battery

Fauziyya Muhammad, Alaa Baha, Grace Haynes, Hakeem Shakir, Michael Omini, Michael Martin, Kenneth A. Weber, Monica Paliwal, Michael Van Hal, Douglas Dickson, Yasin Dhaher, Yan Daniel Zhao, Zachary A. Smith
First published March 8, 2023, DOI: https://doi.org/10.1212/CPJ.0000000000200126
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Abstract

Background and Objectives Patients with cervical spondylotic myelopathy (CSM) have motor impairments, including weakness, imbalance, and loss of dexterity. The reliable assessment of these symptoms is critical for treatment decisions. This study aimed to determine, for the first time, the use of the NIH Toolbox motor battery (NIHTBm) in the objective assessment of motor deficits in patients with CSM.

Methods Patients with symptoms and MRI evidence of CSM and age-matched healthy controls (HC), with no evidence of spinal disorder or surgery were included in this case-control study based on our inclusion and exclusion criteria. We performed motor tests, dexterity, gait speed, grip strength, and balance tests, using the NIHTBm in patients with CSM and HCs. Motor impairment rates were determined in patients with CSM based on the NIHTBm scores. We determined the association between NIHTBm scores and patient-reported outcome scores; patient-reported outcome measures (the modified Japanese Orthopedic Association [mJOA] and Nurick grade) to determine the association. One-way analysis of variance was used to analyze group differences and the Spearman rank correlation to determine the relationship between assessment scores.

Results We enrolled 24 patients with CSM with a mean age (SD) of 57.96 (10.61) years and 24 age-matched HCs with a mean age (SD) of 53.17 (6.04) years in this study. Overall, we observed a significant decrease in the motor function T-scores mean (SD): dexterity 31.54 (14.82) vs 51.54 (9.72), grip strength 32.00 (17.47) vs 56.79 (8.46), balance 27.58 (16.65) vs 40.21 (6.35), and gait speed 0.64 (0.18) vs 0.99 (0.17) m/s, in patients with CSM compared with that in HCs. The lower extremity dysfunction scores on the NIHTBm, balance (ρ = −0.67) and gait speed (ρ = −0.62), were associated with higher Nurick grades. We observed a similar but weaker association with the Nurick grades and NIHTBm tests: dexterity (ρ = −0.49) and grip strength (ρ = −0.31) scores. The total motor mJOA showed a positive but weak association with NIHTBm scores, gait speed (ρ = 0.38), balance (ρ = 0.49), grip strength (ρ = 0.41), and dexterity (ρ = 0.45).

Discussion Patients with CSM had significantly lower NIHTBm scores compared with HCs. The results from the NIHTBm are consistent with the clinical presentation of CSM showing patients have motor impairments in both upper and lower extremities. As a neurologic-specific scale, NIHTBm should be used in the evaluation and clinical management of patients with CSM.

People with cervical spondylotic myelopathy (CSM) frequently present with progressive, disabling neurologic impairments. Symptoms commonly include numbness, hand clumsiness, weakness, and unsteady gait.1 These symptoms result from a progressive narrowing and compression of the cervical spinal cord.2,3 This impairs key descending and ascending white matter pathways, leading to extremity dysfunction. Of importance, patients with CSM are quite heterogeneous and frequently present with key differences in the severity of individual motor dysfunctions.

Clinical injury scores tied directly to patient-reported outcome (PRO) measures lack the ability to fully characterize ongoing injury in patients with CSM.4,5 The 2 most common grading systems, the modified Japanese Orthopedic Association (mJOA) and Nurick scales, cannot objectively measure specific deficits,6 rely heavily on patient perception, and are limited in scope. As a specific example, the Nurick scale evaluates only lower extremity dysfunction.7 This is a notable weakness for assessing a disease well known to associate with clumsiness and weakness in the hands. Therefore, a comprehensive assessment tool that incorporates all forms of dysfunction could provide information on the extent of the spinal cord injury and how specific myelopathy-related motor impairments tie to ongoing injury.

In this report, we used the NIH Toolbox (NIHTB) neuroscienceblueprint.nih.gov, a functional motor battery developed as part of the NIH Blueprint for Neuroscience research,8,-,10 to assess functional neurologic outcomes in prospectively collected patients with CSM and age-matched controls. The NIHTB has been used in numerous neurologic conditions (traumatic brain injury [TBI],11,-,13 stroke,11,14 and spinal cord injury11,15); this battery is easy to use, repeatable, and can be used in an outpatient setting to objectively test motor, sensory, cognitive, and emotional dysfunction in CNS disorders.8,-,10 Given the heterogeneous presentation of clinical deficits in patients with CSM, this battery may have key advantages in assessing patients with CSM with improved granularity.

Methods

Standard Protocol Approvals, Registrations, and Patient Consents

The University of Oklahoma Health Sciences Center (OUHSC) institutional review board (IRB) approved this study, IRB number 12068. A total of 48 individuals were enrolled from March 31, 2021, to April 21, 2022, including 24 patients with CSM (13 female and 11 male) from adult Neurosurgery clinic, OUHSC, and 24 age-matched healthy participants (21 female, 3 male) from Laureate Institute for Brain Research (LIBR) volunteer pool. Three spine neurosurgeons clinically assessed patients and confirmed the diagnosis of CSM (mJOA 4–17). Table 1 summarizes the demographic data for all study participants. We recruited healthy participants from a volunteer pool at the LIBR, Tulsa, Oklahoma. All study participants were at least 22 years of age and understood written and spoken English. eTable 1, links.lww.com/CPJ/A403, details the inclusion and exclusion criteria for study participants. Our exclusionary criteria included any condition that affects motor, sensory pathway testing, and testing results. All participants signed a written informed consent before data collection. All participants completed the mJOA scale and Nurick surveys for assessing symptoms of myelopathy. In addition to the assessment surveys, we conducted NIH Toolbox motor (NIHTBm) battery testing on all participants. eTable 2, links.lww.com/CPJ/A403, includes detailed information on the clinical assessments. Participant information and data including signed consent forms are stored in OUHSC REDCap. All investigators have access to participants' data.

View this table:
Table 1

Demographic Data of Patients With CSM and Healthy Controls

Clinical Assessment Scales

The mJOA scale remains the most commonly used clinical scale for cervical myelopathy. For this study, we classified all patients with CSM into mild, moderate, or severe myelopathy based on this questionnaire. We additionally collected Nurick grades for all enrolled participants. The Nurick scale remains commonly used in the literature; description of which is provided further.

mJOA Scoring

The mJOA scoring system assesses the severity of myelopathy symptoms through a patient-focused questionnaire requiring responses on motor and sensory dysfunction of the upper and lower extremities and bladder dysfunction. Responses of participants are graded on an 18-point scale, upper extremity function is scored out of 5, lower extremity function is scored out of 7, sensory function is scored out of 3, and bladder function is scored out of 3. Participants filled their responses on this survey. We classified patients with CSM as those with mild (15–17), moderate (12–14), or severe (0–11) myelopathy based on their mJOA responses.16 Motor dysfunction was graded out of 12 based on the upper and lower extremity scores (tm-mJOA score) on the mJOA scale.

Nurick Grading

The Nurick grade was developed to differentiate spinal cord compressing factors (tumors or degenerative discs) and to establish the correlation of the degree of cord compression and severity of symptoms in CSM.7,17 The Nurick grading scale adequately associates the spondylosis with the degree of lower extremity weakness in CSM, and it is widely used to determine postoperative response.7 Nurick classifies myelopathy symptoms on a 6-grade scale, from 0 to 5. A score of 0 is signs and symptoms of root involvement but no evidence of spinal cord disease, and a score of 5 is the patient is chairbound or bedridden. It has practical applications and a quick way of assessing the dysfunction in CSM,18 but this scale is lower extremity focused.

The Motor Battery-NIH Toolbox

The NIHTBm consists of 5 different tests that assess dexterity (9-hole pegboard), grip strength, (handheld dynamometer), balance (accelerometer measures), gait (4 m walk speed test), and an endurance test (eTable 2, links.lww.com/CPJ/A403). In this study, we excluded endurance testing because of our patient population. The dexterity test was conducted with a 9-hole pegboard (9HT; Jamar 9 Hole Peg Test kit, Performance Health Supply, Inc., Cedarburg, WI) to assess hand coordination; grip strength was measured using a digital handheld dynamometer (Jamar plus dynamometer, Performance Health Supply, Inc., Cedarburg, WI). Study participants performed balance test to assess their ability to maintain an upright posture during 5 standing poses, 50 s each. Participants' postural sway was detected with an accelerometer (NIH Toolbox BalancePod) worn during balance test (see NIH_Toolbox_App_Administrator's_Manual_v1.23.pdf for a detailed explanation on testing). The quality and speed of gait was assessed using the 4-m walk test (locomotion). We conducted the dexterity and the grip strength on both dominant and nondominant hands.

NIH Toolbox Normative Scores

The NIH toolbox provides demographically corrected normative measures for people older than 3 years, and it is available in both English and Spanish.19 nihtoolbox.org/HowDoI/TechnicalManual/Pages/default.aspx. Table 3 summarizes the description of the motor subdomain of NIH toolbox. The motor domain tests of the NIH toolbox, dexterity, balance, and grip strength scores, were reported as a fully corrected T-score (T-score), and gait speed was recorded as raw scores in m/s.19 The T-score represents the motor performance statistics that have been demographically corrected relative to participants' age-, sex-, education-, race-, and ethnicity-matched peers. The NIH toolbox normative T-score has a mean of 50 and an SD of 10. We reported the fully corrected T-scores for grip strength, dexterity, and balance tests.

Statistical Analysis

Impairment Rates

We performed impairment rate analysis to investigate the validity of using the NIH toolbox in motor assessment of CSM dysfunction. We determined the consistency of our healthy control (HC) T-scores with the demographically corrected normative scores established by the NIH toolbox norming project. A T-score that is 2 SD or more below the mean of 50 (T-score of ≤30) is considered motor dysfunction. We calculated the percent of participants showing motor dysfunction relative to the normative mean T-score of 50 as the impairment rate.

Group Differences

We recorded T-scores were for dexterity, grip strength, and balance scores and gait speed scores in m/s. We used the Shapiro-Wilk test to determine the normality of data. If the normality is not rejected, then unpaired t test or 1-way analysis of variance (ANOVA) will be used to compare outcomes between HCs and patients with CSM; otherwise, the Wilcoxon rank sum test will be used. We performed the 1-way ANOVA followed by Tukey multiple comparison tests to examine group differences on the dexterity and grip strength measures in the dominant and nondominant hands for both HCs and patients with CSM. Unpaired t tests were conducted to determine statistical difference in balance and gait speed scores between patients with CSM and HCs. We performed Wilcoxon signed rank analysis to examine statistical differences in Nurick grade, mJOA, and tm-mJOA scores between patients with CSM and HCs. We used the Spearman rank tests to determine the strength of the relationship between all the assessment scores. A p value of <0.05 was considered as statistical significance. All statistical tests were performed with GraphPad Prism, version 9.0.2, for Windows, GraphPad Software, San Diego, CA, graphpad.com.

Data Availability

Data used to support the findings of this study are available. Anonymized data can be made available to qualified investigators on reasonable request and with permission of the University of OUHSC.

Results

Participant Demographic Information

Our sample included 48 participants: 24 patients with a history and MRI evidence of CSM3,20 (13 female and 11 male) and 24 HCs (21 female and 3 male). The mean age (SD) of patients with CSM was 57.96 (10.61) years (range 34–76 years) and that of HCs was 53.17 (6.04) years (range 42–66 years). Participant ages were not significantly different between patients with CSM and HCs (95% CI: HCs = 50.62–55.72; CSM = 53.48–62.44; p = 0.06). The mean (SD) BMI of patients with CSM was 29.74 kg/m2 (6.02), (95% CI 27.14–32.34) and that of HCs was 27.85 kg/m2 (6.03), (95% CI 25.40–30.29); p = 0.28. See Table 1 for detailed demographic information and group differences by age, sex, BMI, race, and ethnicity.

Assessment Scores

The severity of dysfunction in patients with myelopathy was graded based on the mJOA scores16 and Nurick grade5,7 (Figure 1A). Detailed of the scoring system are summarized in eTable 3, links.lww.com/CPJ/A403. Based on the mJOA score, 33.3% of patients with CSM had mild (15–17), 29.2% moderate (12–14), and 37.5% severe (0–11) myelopathy (eFigure 1A, links.lww.com/CPJ/A402). Patients with CSM had significantly lower mJOA scores, mean (SD) scores 12.29 (3.65), 95% CI 10.75–13.83, compared with HCs, 18.0 (0), 95% CI 18.00–18.00; p < 0.0001 (Table 2). Using the Nurick grade to classify myelopathy severity, patients with CSM had a Nurick grade of 0–1 (20.83%), 2 (16.7%), 3 (41.67%), 4 (16.67%), or 5 (4.17%). Patients with CSM had significantly higher Nurick grade mean (SD) 2.5 (1.41); 95% CI: 1.90–3.10, compared with HCs, 0 (0), 95% CI: 0.0–0.0; p ≤ 0.0001. Assessment scores are provided in Figure 1 and listed in Table 2.

Figure 1
Figure 1 Clinical Assessment Scores of Participants

(A) Bar graphs displaying mJOA scores, the total motor-mJOA (tm-mJOA), and Nurick scores for HCs and patients with CSM. (B) Bar graphs displaying the difference in dexterity and grip strength scores (dominant and nondominant hand scores). (C) Balance scores. (D) Gait speed scores between patients with CSM and HCs. **p < 0.01, ***p < 0.001, ****p < 0.0001. CSM = cervical spondylotic myelopathy; HCs = healthy controls; mJOA = modified Japanese Orthopedic Association.

View this table:
Table 2

Summary of NIHTMB, Nurick, and mJOA Performance for Patients With CSM and HCs

Motor Assessment With NIHTBm

We observed group differences in all 4 domains of the NIHTBm testing listed in Table 2 and presented in Figure 1, B–D. Findings from Tukey post hoc analyses examining differences in motor function using the NIHTBm was consistent with our hypotheses, and it showed patients with CSM with significantly lower dexterity and grip strength in both dominant and nondominant hand scores. In addition, balance and gait speed scores were significantly lower in patients with CSM (Table 2). For dexterity test, compared with HCs, patients with CSM had a mean (SD) T-score of 31.54 (14.82), 95% CI 25.28, 37.80 vs 51.54 (9.72), 95% CI: 47.44–55.65; p < 0.0001 in the dominant hand and 34.83 (13.25) 95% CI: 29.24–40.43 vs 49.00 (7.69), 95% CI: 45.75–52.25; p = 0.0004 in the nondominant hand. Similarly, compared with HCs, patients with CSM demonstrated lower grip strength, with a mean (SD) T-score of 32.00 (17.47) 95% CI: 24.62–39.38 vs 56.79 (8.46), 95% CI: 53.22–60.36; p < 0.0001 in the dominant hand and 29.75 (16.16), 95% CI: 22.93–36.57 vs 53.75 (7.46), 95% CI: 50.60–56.90; p < 0.0001 in the nondominant hand. Furthermore, compared with HCs, patients with CSM had lower mean (SD) T-scores in the standing balance test, 27.58 (16.65), 95% CI: 20.55–34.61 vs 40.21 (6.35), 95% CI: 37.53–42.89; p = 0.0011, and gait speed tests, mean (SD) m/s 0.64 (0.22), 95% CI: 0.54–0.73 vs 0.99 (0.17), 95% CI: 0.92–1.07; (p < 0.0001).

Motor Impairment Rates

Impairment rates were elevated in patients with CSM for all NIHTBm measures. Impairment rate is set at the percentage of participants with greater than 2 SD worse than the normative mean score of 50.19 In the CSM patient group, 45.8% and 37.5% of patients with CSM had impairment in the dexterity measure of the dominant and non-dominant hands, respectively. In addition, 33.3% and 41.7% of patients with CSM had impairment in grip strength in the dominant and nondominant hands, respectively. Half (50%) of the patients with CSM had balance impairment. By contrast, only 1 of the HCs showed a balance impairment (Table 2). We did not observe motor impairments in dexterity or grip strength across the HCs.

Association Between Nurick Grading, tm-mJOA, and NIHTBm

Table 3 and eTable 3, links.lww.com/CPJ/A403 summarize the associations between the NIHTBm, the tm-mJOA scores, and the Nurick grade in patients with CSM. As Nurick grades increase, the total motor mJOA scores decrease in DCM patients: total motor mJOA (tm mJOA, eFigure 2A, links.lww.com/CPJ/A402), mJOA (eFigure 2B, links.lww.com/CPJ/A402), balance (Figure 2C), and gait speed (Figure 2D). Patients with CSM with increasing Nurick grades showed decreasing motor assessment scores with the tm-mJOA scale and the NIHTBm. Specifically, the Nurick grade significantly correlated with the tm-mJOA (r = −0.67, p = 0.0003, eFigure 2A, links.lww.com/CPJ/A402), and mJOA (r = −0.69, p = 0.0002, eFigure 2B, links.lww.com/CPJ/A402). In addition, the Nurick grade correlated with NIHTBm scores, better with balance (r = −0.65, p = 0.0005, Figure 2C), gait speed (r = −0.49, p = 0.03, Figure 2D), dexterity (r = −0.44, p = 0.03, Figure 2A) than with grip strength (r = −0.35, p = 0.09, Figure 2B). Regarding the mJOA and NIHTBm scores, there was significant relationship between tm-mJOA and dexterity (r = 0.60, p = 0.002, Figure 3A), grip strength (r = 0.57, p = 0.004, Figure 3B), and balance (r = 0.52, p = 0.01, Figure 3C), but not gait speed (r = 0.23, p = 0.30, Figure 3D).

View this table:
Table 3

Correlation Between tm-mJOA, Nurick Grade, and the NIH Toolbox Motor Battery

Figure 2
Figure 2 Relationships Between Nurick Grade and NIHTBm Scores in Patients With CSM

Scatterplots showing the correlation between the Nurick grades and (A) dexterity (dominant hand) scores. (B) Grip strength (dominant hand) scores. (C) Balance scores. (D) Gait speed scores. CSM = cervical spondylotic myelopathy; NIHTBm = NIH Toolbox motor.

Figure 3
Figure 3 Correlation Between tm-mJOA and NIHTBm Scores

(A) Scatterplot showing the correlation between the dexterity (dominant hand) and tm-mJOA scores. (B) The correlation between grip strength (dominant hand) and tm-mJOA. (C) The correlation between the balance score and tm-mJOA score. (D) The correlation between gait speed and tm-mJOA score. NIHTBm = NIH Toolbox motor; Tm mJOA = total motor modified Orthopedic Association score.

Discussion

This study was designed to establish the use of the NIHTBm testing in patients with CSM. Although the PRO measures, Nurick scale, and mJOA grading scale are typically used for the evaluation of motor and sensory deficits in CSM,18 the NIHTB provides reliable, repeatable, and quantitative measures across a variety of neurologic deficits.10 The NIHTB was designed by the NIH Blueprint for Neuroscience Research Initiative for research purposes and has been used to assess motor, sensory, cognitive, and emotional impairments across neurologic disorders including stroke, TBI, and SCI.9,11,-,13 The data presented in this study provide for the first time the use of NIHTBm battery in the assessment of CSM dysfunction. We also show how the NIHTB can be an appropriate tool for the evaluation of patients with CSM in the clinic. Specifically, the NIHTB can help clinicians quantitatively measure motor deficits and as such enhance their understanding of a patient's ongoing injury.12 Our results indicate that patients with CSM have significantly lower functional scores across all motor domains of the NIHTB similar to assessments reported with the Nurick grade or mJOA score. However, these data with the NIHTB showed patients with CSM are heterogeneous with a broad spectrum of motor dysfunctions (Figure 3).21 Unlike the mJOA scale that focuses on assessing weakness and incoordination5,22 or the Nurick grade that assesses only lower extremity weakness,7 the NIHTBm evaluates several domains (proprioception, muscle tone, strength, and reflexes) of the motor system in both upper and lower extremities.8 Therefore, the NIHTBm can help clinicians to more broadly evaluate each and overall motor deficits in CSM and highlights the extent and severity of spinal cord injuries that occur in CSM.

We observed significant motor deficits in patients with CSM across all the motor domains including grip strength, dexterity, balance, and gait speed. Patients with CSM performed poorly with T-scores greater than 2 SD below the normative mean score of 50 in all motor tests. In addition, the impairment rates were significantly high, and more than 50% of patients had at least 2 or more motor deficits. These results support the validity of NIHTBm as a sensitive scale that can isolate specific motor dysfunction in CSM. Unlike other assessment scales, normative scores for all ages and domains are available with the NIHTB instruments and are important for clinicians to attempt to interpret the motor measures in clinical practice.8,19 Our HC measures were within the normal limits provided on the NIH Toolbox normative scores.8 These consistent findings across healthy individuals indicate that the NIHTBm is a reliable clinical assessment tool for CSM. Expansion of this work is needed to establish the clinical use of these measures; the data in this study provide an important first step in establishing the validity and use of the NIHTBm in CSM.

The precise identification of motor deficits is critical for treating patients with neurologic and musculoskeletal diseases. Many disorders such as CSM, stroke, TBI, multiple sclerosis, and SCI present with motor, sensory, cognitive, and/or emotional impairments.23,-,25 However, the clinical assessment of these deficits is measured with different, disease-specific, subjective, and patient-reported measures that have little consistency in the assessment of these neurologic symptoms.26,27 Therefore, this makes a comparison of motor dysfunction across these neurologic diseases difficult. The NIHTB provides a normalized assessment scale that precisely allows measures of impairments in the specific domain across multiple diseases. The motor impairment rates observed in CSM with the NIHTBm were consistent with motor impairment measures in patients with stroke, TBI, or SCI.11 The average T-scores of motor deficits of patients with CSM were better compared with the motor T-scores of patients with SCI (≤2 SD from the mean T-score).11 But the average T-scores for each motor domain were generally lower in patients with CSM compared with the T-scores of patients with TBI or stroke (mean T-scores were within 1 SD below the mean).11 These findings were expected, given that patients with spinal cord damage especially in the cervical region (SCI and CSM) have more generalized upper and lower extremity motor impairments.28 Individuals with stroke and TBI have localized neurologic deficits indicative of the distinct subregion of the brain involved. The assessment of individual subdomain measures with the NIHTBm will assist in identifying specific motor deficits in CSM and allow for exclusion of differential diagnoses that might not be otherwise identified with the other clinical assessment scales.

The Nurick grading scale was developed to identify neurologic deficits specific to CSM. This grading scale classifies patients with CSM on a 6-point scale that addresses lower extremity function.7,17 A higher score is indicative of severe dysfunction. The mJOA was designed to assess motor and sensory function in the upper and lower extremities and bladder dysfunction. These assessment scales are widely accepted and have been used in determining the severity of CSM and track response to intervention. We observed consistency in the lower extremity dysfunction scores (balance and gait speed) of the NIHTBm and the Nurick or mJOA. However, the Nurick grades were less associated with dexterity and grip strength scores as were the mJOA scores. These association results were not surprising because the Nurick grade assesses only lower extremity functions and the mJOA provides generalized patient-reported measures. The association of the NIHTB measures with that of the PRO measures provides opportunities to validate the toolbox as an assessment tool for CSM, and the discrepancies in the outcome scores could inform the use of the NIHTB to complement the subjective assessment scales in isolating specific deficits in CSM.

The clinical sequel of spinal cord compression in CSM presents a broad spectrum of symptoms. Patients with CSM can present with mild symptoms that include hand clumsiness or imbalance to severe symptoms of complete paralysis.20,21 An assessment tool that captures the mechanism of CSM symptoms is much better at driving interventions that target specific deficits and enhance recovery. These insights cannot be deduced using the Nurick grade or mJOA assessment. Semiquantitative measures of specific dysfunction have been the focus of many reports and could indicate the region(s) of spinal cord damage in CSM. The 9-hole pegboard dexterity test (9HPT) is known to be an objective measure of hand dysfunction, a common devastating symptom in CSM.29 The dexterity test represents the assessment of motor strength, joint position sense, and proprioception in the hands.4 The proprioceptive function is carried through the dorsal column of the spinal cord, and lesions of these tracts lead to ataxia that manifests as a loss of hand coordination.30 Using a 9HPT battery of the NIHTBm domain, we quantify hand incoordination to assess the dorsal column function. We observed patients with CSM have diminished hand coordination similar to other published reports.31 Furthermore, the 9HPT also allowed for patient-to-patient comparison, including detecting hand-to-hand differences, which were observed in our study participants. Impaired proprioception, in addition to muscle weakness and spasticity, leads to poor balance and gait dysfunction.32,-,34 Damage to the corticospinal tracts and posterior columns are attributed to these lower extremity dysfunctions.35 Quantitative measures using the gait and balance tests measure the extent of damage to these tracts.36 Fifty percent of our patient group had balance impairment (Table 2) and in fact, studies have shown that the lateral corticospinal tracts are the most vulnerable during CSM and imbalance is the earliest presenting symptom of myelopathy.37,38 Therefore, an accurate measurement of these dysfunctions could inform the identification of specific lesions and improve our understanding of the mechanism and extent of spinal cord injury in CSM. Despite the importance of the objective assessment of these motor dysfunctions highlighted in numerous studies due to their high sensitivity and reliability, individual measures of these dysfunctions are not sufficient to provide a complete understanding of the mechanism and severity of CSM. Accordingly, most of the patient population in this study presented with 2 or more neurologic impairments. Therefore, utilization of the NIHTBm for motor assessment will evaluate the motor deficits in their totality in CSM.

This study provides an important description of NIHTBm use in the CSM. However, it is important to acknowledge the following limitations. First, the number of patients used in the study is moderate in size. A large series of study participants is needed to discern the use of the NIHTBm in monitoring the progression of dysfunction. Only preoperative measures were assessed and presented in the study; posttreatment measures are especially important to describe the use of the NIH toolbox in monitoring response to treatment. We are currently collecting longitudinal data at 6 months interval in all patients with CSM. The sex distribution of the healthy group was unequal; most of them were White non-Hispanic women. However, the NIHTB scores including the normative scores correct for age, sex, race, and ethnicity. One of the healthy participants had a lower balance score of less than 2 SD of the mean T-score, and additional screening could help exclude individuals with other comorbid conditions with imbalance that influence the performance of the NIHTBm. Conducting the NIHTB testing is time-consuming, but the toolbox provides better diagnostics and long-term assessment compared with the mJOA and Nurick surveys. Therefore, conducting the assessment tests with the NIHTB is worth the time, especially for this cohort of patients. Healthcare providers need to be trained to administer the NIHTB testing. In addition, the NIH toolbox is a performance-based test and requires the participant to maintain an upright posture for balance and gait tests. This requirement automatically excludes patients with severe myelopathy or wheelchair-bound patients from performing the lower extremity tests. However, objective measures of upper extremity such as grip strength and dexterity could provide meaningful assessment of neurologic deficits in these patients, and the ability to perform the lower balance and gait tests in this patient subset after surgery points to improvements in dysfunction.

Regardless of the study limitations, the NIHTBm is a reliable, repeatable, inexpensive tool for clinical assessments.8,19 The toolbox incorporates advances in technology into the clinical evaluation of patients. The data presented in this study provides evidence for the use of the NIHTBm in CSM because the toolbox provides a quantitative real-time measure of dysfunction and access to accurate range of normal functions. Future work should examine the relationship of the NIHTB measures with the newly developed quantitative spinal cord image outcomes that better characterize the region of injury in the cord. The NIHTB may be used to monitor disease progression in patients with CSM that exhibit mild symptoms and do not have surgery through repeated measures. In addition, future work needs to include postoperative patients to evaluate symptom recovery and prognosis. The NIHTBm should be integrated during clinical examination and PRO measures for a more comprehensive evaluation of patients with myelopathy.

In conclusion, the NIHTBm provides a sensitive and quantitative measure of motor deficits in CSM. The NIHTB demonstrates validity for use in the clinical assessment of patients with CSM consistent with its use in other neurologic disorders.

Acknowledgment

The authors thank the Laureate Institute for Brain Research (LIBR) for providing them with healthy participants for this study and the NIH Blueprint for Neuroscience Research Initiative for developing the NIH Toolbox tests. The authors also thank the study participants and their families who gave their time to participants in this study.

Study Funding

Zachary Smith received funding from the National Institute on Neurologic Disorders and Stroke (grant K23NS091430), Presbyterian Health Foundation Team Science Research, and Oklahoma Shared Clinical and Translational Research (OSCTR) NIH-IDeA grant.

Disclosure

F. Muhammad, A. Baha, G. Haynes, H. Shakir, M. Omini, and M. Martin report no disclosures relevant to the manuscript. K.A. Weber II received funding from the National Institute on Neurologic Disorders and Stroke (grant K23NS104211 and L30NS108301). M. Paliwal, M. Van Hal, and D. Dickson report no disclosures relevant to the manuscript. Y. Dhaher received funding from the National Institute of Arthritis and Musculoskeletal and Skin Diseases (grant R01 AR06976-03). Y.D. Zhao reports no disclosures relevant to the manuscript. Z.A. Smith is funded by NIH-NINDS K23 grant K23NS091430, Presbyterian Health Foundation Team Science Research, and Oklahoma Shared Clinical and Translational Research (OSCTR) NIH-IDeA grant. Full disclosure form information provided by the authors is available with the full text of this article at Neurology.org/cp.

Appendix Authors

Table

Footnotes

  • Funding information and disclosures are provided at the end of the article. Full disclosure form information provided by the authors is available with the full text of this article at Neurology.org/cp.

  • Submitted and externally peer reviewed. The handling editor was Deputy Editor Kathryn Kvam, MD.

  • Received August 9, 2022.
  • Accepted November 8, 2022.

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

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