Abstract
Study design
Prospective cross-sectional observational study.
Objective
This study aimed to develop a novel Physical Performance Test (PPT)-based scoring system by linking PPTs with the radiological severity of Degenerative Cervical Myelopathy (DCM).
Methods
The severity of spinal cord compression in DCM patients was assessed using the cross-sectional area (CSA) at the maximal stenosis, as determined by magnetic resonance imaging (MRI). Functional performance was evaluated with the modified JOA scoring system (mJOA) and PPTs: 10-second-Grip-and-Release-Test (GR), Simple-Foot-Tapping-Test (FTT), 10-second-Step-Test (SST), Nine-hole-Peg-Test (HPT), and 30-meter-Walking-Test (30MWT). Validity was determined by examining correlations between CSA and these metrics, using Pearson’s correlation. The Hong Kong Myelopathy Criteria (HKMC) were developed through Principal Component Analysis and K-means clustering to combine PPTs with the highest correlation with CSA.
Results
269 DCM patients (57% female, mean age 63 ± 9) were studied. 55% had CSA less than 70 mm2 (mean CSA 55.92 ± 7.37 mm2), symptoms for 19 ± 6 months, and mJOA of 14.4 ± 2.0. PPTs showed significant correlations with CSA (r = −0.473 to 0.837, p < 0.001), but not with mJOA. The HKMC, combining GR, FTT, and SST (loadings >0.87), with a four-tier scoring system (0-3), showed a strong correlation (r = 0.896, p < 0.001). A cutoff of 4.5 effectively indicates significant cervical stenosis, with 90% sensitivity and 94% specificity.
Conclusion
This study is the first to demonstrate a strong association between spinal cord compression and physical performance in DCM. As a novel DCM-specific assessment tool, the HKMC demonstrates bedside utility and superior validity compared to individual PPTs and mJOA to identify individuals with radiologically severe DCM.
Keywords
Introduction
Progressive spinal cord dysfunction in Degenerative Cervical Myelopathy (DCM) involves age-related changes in the cervical spine, with symptoms typically manifesting in middle age.1,2 Diagnosing DCM depends on clinical symptoms and signs, Magnetic Resonance Imaging (MRI) evidence of spinal cord compression, and standardized assessment via the Modified Japanese Orthopaedic Association Scoring System for Cervical Myelopathy (mJOA), which is recognized as the gold standard for evaluating functional deficits.3-6 However, the long waiting time for diagnostic MRI confirmation, difficulty in identifying specific clinical signs, and the inadequacy of mJOA have created a stumbling block for the timely determination of DCM.7-9
Delayed diagnosis of DCM persists due to ambiguous diagnostic criteria, insufficient awareness among primary care providers, and symptom overlap with age-related changes and other neurological disorders, such as Carpal Tunnel Syndrome (CTS).2,5,7,9,10 With the global demographic trend towards an aging population, the burden of disease will increase, and there is a growing need for innovative diagnostic techniques capable of detecting functional impairment relating to DCM at an early disease stage, thereby enhancing patient outcomes. 11
Physical performance tests have been proven effective for DCM detection and monitoring, whether using a sophisticated experimental setup or a simple bedside method.12-14 Nevertheless, no dedicated tests presently exist to determine the severity of DCM. 15 The mJOA, whilst widely adopted, relies partly on observer judgment, limiting objectivity. 16 Simple bedside assessments can result in more quantitative measures of neurological function with relation to hand clumsiness, gait disturbance, and imbalance; however, tests are interpreted in isolation, with the risk of neglecting other domains with impairment.17-19 Kobayashi et al (2023) and Muhammad et al (2023) reported that a combinatory testing format, such as the 10-second Grip and Release Test combined with grip strength and the National Institutes of Health Toolbox Motor Battery (NIHTBm), enhances sensitivity and diagnostic accuracy.20,21 Further investigations into integrated physical performance testing have the potential to substantially improve the detection and management of DCM. 22 This study aimed to develop a comprehensive combinatorial testing system for determining the severity of DCM by the evaluation of functional impairments at the bedside.
Materials and Methods
This study was conducted in accordance with the Declaration of Helsinki and was approved by the University of Hong Kong and the Hospital Authority Hong Kong West Cluster (UW 23-242). It was registered on ClinicalTrials.gov (NCT06528730). Written informed consent was obtained from all participants before the commencement of any assessment and procedure.
Participants
Participants in this study were recruited between September 2021 and December 2022. They were selected based on specific criteria to represent individuals with DCM and an asymptomatic control group. Controls were contacted at district recreation and sports centers, while DCM participants were recruited from 3 tertiary referral centers.
Inclusion Criteria
All participants were Chinese, aged 45 or older, independent in activities of daily living, community walkers with a Frankel Grade of D or above, possessed a Nurick’s rating of 3 or lower, and were capable of following instructions. The DCM group was diagnosed by experienced spine surgeons based on the presence of clinical symptoms and signs, which were compatible with radiological evidence of cervical canal stenosis present on MRI scans. In contrast, the controls were asymptomatic individuals without clinical signs of myelopathy or any neck-related medical history, as verified through electronic hospital records.
Exclusion Criteria
This study excluded DCM participants with myelomalacia identified on T2-weighted MRI. Both DCM and asymptomatic participants with non-myelopathic neurological issues, extra-pyramidal symptoms, vestibular deficits, neuropathies, or spinal problems like lumbar stenosis and thoracic myelopathy were excluded. To prevent bias, those with joint deformities, vision, or hearing impairments were also excluded.
Assessment Setup
All participants were evaluated by an experienced Occupational Therapist using the mJOA score as well as a series of physical performance tests which were performed at the bedside or clinic setting, including the 10-second Grip and Release Test (GR), Nine-hole Peg Test (HPT), 10-second Step Test (SST), Simple Foot Tapping Test (FTT), and 30-meter Walking Test (30MWT). MRI scans of all DCM participants were evaluated, with a confirmed diagnosis of DCM by orthopaedic surgeons. Demographic information (age, sex), clinical complaints (symptoms, onset time, evolution), and social history (smoking, drinking, exercise routines) were obtained from all participants. Measurements of height and weight were also obtained to calculate Body Mass Index (BMI).
Screening Test for Balance and Gait Coordination
Balance and coordination were screened using the Romberg and Tandem Walking Tests. In the Romberg Test, participants stand with feet together, close their eyes, and maintain a steady standing posture for 30 seconds under supervision. Losing balance indicates a positive test. 23 In the Tandem Walking Test, participants are instructed to walk 10 heel-to-toe steps without gaps, keeping their eyes closed. An eye-open practice trial helps ensure understanding. The investigator must supervise closely for safety. Failures are recorded if participants side-step, leave a gap between their feet, or open their eyes during the test. 24
The Modified Japanese Orthopaedic Association Scoring System for Cervical Myelopathy
The mJOA is a widely used tool for assessing DCM severity, covering 5 domains: Upper and Lower Limb Function, Sensory Disturbance, and Bladder Function. Muscle strength in the Deltoid or Biceps was evaluated as well (Figure 1).16,25,26 The scale peaks at 17, with severity of myelopathy classified as mild (15-17), moderate (12-<15), or severe (<12).
27
The modified Japanese Orthopaedic Association Scoring System for Cervical Myelopathy
Magnetic Resonance Imaging
Cervical MRI is the gold standard for locating and assessing for radiological evidence of cord compression in DCM.
28
Identifying the most affected spinal cord begins with examining the mid-sagittal T2-weighted MRI images to determine the most stenotic level, while the cross-sectional area (CSA) of the most compressed cord measures the severity of compression (Figure 2).13,29 The CSA was measured on MRI by the principal investigator, and a CSA smaller than 70 mm2 was considered an independent predictor of cervical spinal cord atrophy, as described by Bednarik et al and Kadanka et al.30,31 They were named as DCM-at-risk in this study, indicating a high risk of neurological decline.31-33 Identifying the most compressed spinal cord level in the sagittal cut of the T2-weighted MRI (Left) and corresponding axial cut for measurement of CSA (Right)
Physical Performance Tests
Physical performance tests comprise simple assessment measures that can be performed in the bedside or clinic setting without specialized equipment, and which may be quantified to reflect upon deficits in power, dexterity, and proprioception. As described in detail subsequently, these included the GR, HPT, SST, FTT, and 30MWT (Figure 3).
12
All tests were repeated 3 times, and the results were averaged across the 3 trials. Both limbs were assessed separately in the GR, HPT, and FTT, and the total repetitions achieved were averaged in GR and FTT to prevent missing key data due to asymmetry details. The overall results of HPT and 30MWT were calculated as the average time taken (seconds).34-38 Validated physical performance tests for assessing individuals with degenerative cervical myelopathy
10-Second Grip and Release Test
The subject was instructed to raise the arm to chest level, extend the elbow and wrist, and quickly grip and release the fingers for 10 seconds.37,38
Nine-Hole Peg Test
This is a clinically validated hand dexterity test that involves quickly placing and removing nine pegs without a pattern using 1 hand (Figure 3). 39
10-Second Step Test
The subject was instructed to step as fast as possible continuously for 10 seconds, raising each knee until the thigh was parallel to the ground, then reciprocating on the opposite side (Figure 3). 40
Simple Foot Tapping Test
Participants sat with hips and knees at 90° and tapped their foot rapidly for 10 seconds using dorsiflexion/plantarflexion while keeping their heel on the floor, and the total taps were counted (Figure 3). 41
30-Meter Walking Test
The subject was required to walk back and forth along a 15-meter corridor, either unaided or using a walking aid, at the patient’s usual walking pace, turning once at a halfway point (Figure 3). 42
Data Analysis
Participant demographics were analyzed with a chi-squared test, Fisher’s Exact Test, an independent sample t-test, and ANOVA. The relationships among the CSA of the most compressed spinal cord in MRI, mJOA, and physical performance tests (GR, HPT, SST, FTT, 30MWT) were examined using Pearson’s correlation, while the most representative testing components were identified through multivariable linear regression.
Sample size was calculated using G-Power software (version 3.1.9.4, Heinrich Heine University Düsseldorf, Germany), based on our pilot data (n = 32), with an effect size of 0.669, considering a probability of type I error of 0.2, and a type II error of 0.05. This indicates a need for at least 148 participants with an allocation ratio between groups of 0.4, including 104 DCM subjects with CSA under 70 mm2 and 44 DCM subjects at or above 70 mm2, to ensure 80% power and 95% precision.
The inter-rater reliability between the principal investigator and an experienced spine surgeon, as well as the intra-rater reliability of the CSA measurement in the pilot study, was confirmed by intraclass correlation coefficients (ICCs) of 0.887 and 0.873, respectively. Similarly, the intra-rater reliability across these 5 tests yielded strong ICCs ranging from 0.863 to 0.924, indicating excellent internal consistency. 43 High ICCs were also observed between different assessors (experienced and junior therapists), ranging from 0.815 to 0.899.
Defining the Components and Scoring Range for a Novel Performance-Based Scoring System
Principal component analysis (PCA) was performed on all 5 physical performance tests to reduce redundancy by removing tests that measured similar functions, while retaining as much variation as possible within our cohort.
44
To compare test scores across different units in the PCA, all scores were standardized as Z-scores calculated with the following equation.
45
We applied the K-Means clustering partition method, along with the actual scoring of each test component in the principal components (PC) identified by PCA, to define distinct severity ranges for the key physical performance tests in the new scoring system. 46
Assessing Performance to Detect Critical Radiological Stenosis
To benchmark the novel performance-based score for detecting a reduced CSA of less than 70 mm2, which is associated with a high risk of neurological decline, Receiver Operating Characteristic (ROC) analysis was employed to determine the clinical thresholds.31,47-49 The assessment tool was considered adequate only when its Area Under the Curve (AUC) exceeded 80% and its sensitivity, specificity, and diagnostic accuracy were all above 50%.50,51
All statistical analyses were performed using IBM SPSS Version 29.0.1.0.0 (SPSS Inc, Chicago, USA), with a significance level set at 0.05. Participants with incomplete data were all excluded from the study.
Results
Subject Recruitment
Demographics of DCM and Control groups
Physical Performance Tests measured in DCM patients vs. Asymptomatic Controls
Clinical examination and Physical Performance Test results of the DCM and Control groups
DCM: Degenerative Cervical Myelopathy
Physical Performance Tests measure patients above and below the Critical Cross-sectional Area of the most stenotic cervical spinal cord
Comparison between DCM-at-risk and DCM-not-at-risk groups
DCM-not-at-risk: Degenerative Cervical Myelopathy individuals with a cross-sectional area of the most stenotic cervical spinal cord at or greater than 70 mm2
DCM-at-risk: Degenerative Cervical Myelopathy individuals with a cross-sectional area of the most stenotic cervical spinal cord smaller than 70 mm2mJOA: The modified Japanese Orthopaedic Association Scoring System for Cervical Myelopathy
Association Between the Severity of Spinal Cord Compression and Physical Performance Tests
Association among the Cross-sectional Area (CSA) of the most compressed cervical spinal cord, mJOA, and the performance in Physical Performance Tests
**p-value less than 0.01; *p-value less than 0.05
CSA: Cross-sectional area of the most compressed cervical spinal cord
mJOA: The modified Japanese Orthopaedic Association Scoring System for Cervical Myelopathy
GR: The 10-second Grip and Release Test; HPT: Nine-Hole Peg Test, FTT: Simple Foot Tapping Test; SST: 10-second Step Test; 30MWT: 30-meter Walking Test
The GR, FTT, and SST demonstrated a strong and significant association with radiological severity of spinal cord compression in multivariable linear regression, with covariates including age, comorbidities, exercise habits, duration of symptoms, Romberg Test, and Tandem Walking Test. The regression model yielded impressive coefficients of determination (R2) of 0.865, with regression coefficients (β) at 0.325 for GR, 0.182 for FTT, and 0.556 for SST (p < 0.001) (Figure 4). Multivariable linear regression models of CSA and physical performance tests (n = 269)
Derivation of a Novel Combinatorial Scoring System for Degenerative Cervical Myelopathy
The principal components (GR, FTT, and SST) were identified through principal component analysis (PCA), with a combined eigenvalue of 3.02, accounting for 60% of the total variance. Owing to the inadequate communalities of HPT (0.35) and 30MWT (0.34), both were excluded from the composite score to ensure optimal representation of shared variance. Based on these results, a new composite score was proposed using GR, SST, and FTT. Each component exhibited factor loadings exceeding 0.87, indicating a strong contributing underlying construct. The uniformity of these loadings suggests that components GR, FTT, and SST contributed equally to the newly developed combined scoring system, which was calculated by direct summation of their effects.
Based on the principal components, a four-cluster severity range was defined for each representative test using the elbow method, which evaluated the within-cluster sum of squares against the number of clusters. The clustering structure was supported by ANOVA, showing significant differences in centroid-point distances among cluster members (p < 0.001). Additionally, cluster membership was strongly associated with the severity of spinal cord compression (χ2 = 99.8, p < 0.001), confirming clinical relevance. The severity scores were labeled according to functional deficiency levels: “0” (Profound), “1” (Severe), “2” (Moderate), and “3” (Mild) (Figure 5). Principal components clustering of the Hong Kong Myelopathy Criteria (HKMC)
The Hong Kong Myelopathy Criteria
The Hong Kong Myelopathy Criteria (HKMC), a novel integrative scoring system based on combinatorial methods, has been developed as an objective performance-based tool for assessing the severity of DCM in the context of diagnosis and intervention decision-making. It includes 3 key components that assess overall body balance and coordination of both upper and lower limbs, as illustrated in Figure 6. A strong correlation was found between the severity of spinal cord compression and the HKMC, with a correlation coefficient r of 0.896 (p < 0.001). This correlation was notably more robust than any single unimodal physical performance test (GR: r = 0.820; FTT: r = 0.812; SST: r = 0.837; p < 0.001). The novel scoring system for Degenerative Cervical Myelopathy –The Hong Kong Myelopathy Criteria (HKMC)
Clinical Threshold Indication for Significant Spinal Cord Compression
The clinical threshold of 4.5 in the HKMC indicating the individuals having a chance of having significant cervical spinal cord compression with a cross-sectional area less than 70 mm2 was derived from the ROC analysis, demonstrating an excellent AUC of 0.959 (95% CI: 0.931, 0.986), with 90% sensitivity, 94% specificity, and a diagnostic accuracy of 90%, highlighting its ability and reliability in assessing individuals affected by DCM (Figure 7). Receiver Operating Characteristic curve illustrating the evolution of the threshold in HKMC for DCM-at-risk individuals
Discussion
To the best of our knowledge, this study is the first to comprehensively quantify and establish the relationship between the severity of spinal cord compression and physical performance tests in DCM. After individual evaluation, physical performance tests were integrated to create a new, multimodal bedside assessment tool for assessing DCM, namely, the HKMC.
The HKMC showed a notably stronger correlation with the severity of spinal cord compression on MRI (r = 0.896, p < 0.001), exceeding the mJOA gold standard (r = −0.001, p > 0.05). In addition, the HKMC exhibits high sensitivity, specificity, and diagnostic accuracy (90-94%) in identifying DCM patients at risk of severe neurological decline when CSA was below the critical clinical threshold. Conversely, Treanor et al reported that mJOA has a limited sensitivity of 60% and a marginal diagnostic accuracy of 57%, despite a high specificity of 90%. 52
Physical performance tests have been used at the bedside and clinic since GR was first introduced by Ono et al in 1987, followed by the measures of 30MWT, HPT, SST, and FTT from 1999 to 2012.38,40,41,53,54 Beyond their use as a screening tool for the presence or absence of DCM, physical performance tests have not been used to assess the severity of radiological compression. When MRI imaging may be delayed or repeated assessment is hindered by facility or economic constraints, our results indicate that physical performance tests are an accurate, non-invasive measure correlating with radiological compression severity—a significant advancement in their clinical utility that has remained stagnant since the 1980s with the inception of JOA scoring.55-57 The HKMC score is intended to support, not replace, clinical judgment. In cases where a patient presents with significant radiculopathy or motor weakness despite a higher HKMC score, clinical discretion should prevail, and MRI should not be delayed. 58 The tool is designed to assist in triaging ambiguous or borderline cases, particularly in resource-limited settings, rather than to dictate imaging decisions in clear-cut presentations. 20 PPTs are advantageous as compared to patient-reported outcome measures (PROMs) utilized to assess DCM, such as the Neck Disability Index (NDI), the Health-related Quality of Life Short Form 36 Questionnaire (SF-36), and mJOA, which lack correlation with the extent of cord compression.59-62 Furthermore, these physical performance tests may be easily adopted in other cultures and socioeconomic backgrounds, as no specialized tools are required, and maneuvers are universal across ethnicities, unlike the use of chopsticks, which restricts the relevance of the original JOA scoring system. 63
Validity and Reliability of the Physical Performance Tests for DCM
**p-value less than 0.01; *p-value less than 0.05
Currently, MRI is considered the gold standard for diagnosing DCM. 71 Advanced MRI techniques, such as digitized tensor imaging (DTI) and functional MRI (fMRI), have been studied for disease detection and prognostication. However, their limited global availability and cost precludes their use as screening tools.72-74 Researchers have proposed other standardized, comprehensive assessment tools to define disease severity in DCM, such as the Graded Redefined Assessment of Strength Sensibility and Prehension Version Myelopathy (GRASSP-M) and the National Institutes of Health Toolbox Motor Battery (NIHTBm).13,75 Previous studies demonstrated strong inter-rater reliability for both GRASSP-M and NIHTBm, with ICCs of 0.87. However, their validity was lower than that of HKMC (r = 0.896, p < 0.001), despite validation using the NDI and mJOA, respectively.13,75 Kalsi-Ryan et al found that GRASSP-M had moderate validity, with correlation coefficients ranging from 0.51 to 0.53 (p < 0.05). Similarly, NIHTBm also demonstrated moderate validity (r = 0.35-0.53, p < 0.05).13,75 Furthermore, these tests required a standardized kit purchased directly from the National Institutes of Health (USA) and University Health Network (Canada), with the GRASSP-M also requiring further clinical licensing.14,21 Each assessment tool requires at least 35 minutes to administer, which limits its practicality in busy clinical environments.76,77 Recently, Kobayashi et al proposed a convenient assessment protocol that combines grip strength and GR for diagnosing DCM, reportedly an increase in testing accuracy by up to 76%. 20 This work inspired the idea of combining different tests, although it primarily focuses on the upper limbs and currently lacks integration and appropriate weighting of individual components.
Ultimately, our results promise to shorten the time to diagnosis of DCM, especially in patients with significant radiological compression. Delayed diagnosis has been a longstanding concern, with previous studies indicating that delays of 1 to 2 years are common due to factors including the non-specificity of symptoms and knowledge gaps among primary care physicians.10,78-80 Delayed diagnosis has a significant impact on outcomes, as those diagnosed and who received appropriate management within 4 months are more likely to have improved mJOA scores. 60 Additionally, Guo et al found that a prolonged duration of symptoms of more than 6.5 months increases the likelihood of poor prognosis and worsens with further delay. 81 Our innovative HKMC establishes a reliable and effective clinical threshold for identifying DCM-at-risk individuals, achieving 90% sensitivity, 94% specificity, and 90% overall accuracy. This helps efficiently allocate resources, so imaging and/or specialist referral targets those with radiologically severe cord compression. 4
Limitations of the Study
Whilst the sample size was considerable, patients were restricted to a single ethnicity, and it was insufficient to capture overall disease severity fully. Future studies should be conducted in different locales to confirm our findings, release the recruitment criteria to broaden the capture of DCM across various disease severities, and facilitate prospective external validation of the clinical threshold for DCM individuals at risk of severe neurological deficits.
Conclusion
The HKMC combined 3 major physical performance tests — GR, FTT, and SST — and a four-tiered scoring system. Scoring results showed a strong correlation with spinal cord compression severity, with a critical cutoff score of 4.5 for identifying the risk of neurological decline in DCM with a subcritical CSA of less than 70 mm2. This cutoff achieved 90% sensitivity, 94% specificity, and 90% overall accuracy. This comprehensive metric creates a new, integrated objective tool to enhance early diagnosis of DCM, enabling the identification of patients at risk of irreversible neurological damage.
Footnotes
Acknowledgement
The authors would like to thank Professor Jason Cheung, Professor Kenny Kwan, Dr Paul Koljonen, Dr Chris Tang, Professor Janus Wong, and Professor Chor Yin Lam for their assistance with subject recruitment.
Ethical Considerations
Funding
The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The authors disclosed receipt of the following financial support for the research of this article. KKP LAW has received the AO Spine Asia Pacific Research National Grant [AOSRG2023031], and KMC Cheung received the Shenzhen Key Medical Discipline Construction Fund [SZXK2020084] and the Sanming Project of Medicine in Shenzhen, China [SZSM202211004].
Declaration of Conflicting Interests
Each author certifies that he or she has no commercial association (eg, consultancies, stock ownership, equity interest, patent/licensing arrangements, etc.) that might pose a conflict of interest in connection with the submitted article.
