Cervical spondylotic myelopathy (CSM) results from the degenerative narrowing of the spinal canal, which causes spinal cord compression in a slow, progressive manner. This type of compression causes a delayed onset of adapted deficits in both the spinal cord and periphery. Although the result of this compression may be tetraparesis/tetraplegia, the impairments do not present as precisely as those that result from traumatic lesions. In fact, the severity of the compression and the deficits that result are variable across individuals. CSM is the leading cause of acquired spinal cord disability in the elderly.1,2 The varying degree of impairment impacts independence and quality of life. Because CSM can have such a heterogeneous presentation, a single outcome measure cannot quantify the broad range of neurological deficits seen in this population. Therefore, in addition to a comprehensive clinical neurological examination and imaging, it is necessary to define outcome measures that characterize the deficits in this population with greater validity, reliability, and responsiveness.
The use of sensitive outcome measures is important to establish efficacy of interventions, assist in identifying the predictors of disease progression, and enable clinicians to offer treatment that is most effective and offered at the most appropriate time in the course of this disease. Understanding the deficits of this population will enable the field to establish a standard method to define a severity of disease index. Therefore, the objective of this review is to identify the most useful, quantitative, standardized outcome measures for the assessment of CSM that will establish a meaningful clinical dataset to enable clinicians to assess outcomes, monitor the natural history of CSM, and establish the prognostic value of clinical findings.
MATERIALS AND METHODS
The review process included 3 stages: (1) Initial search of PubMed to define existing measures in CSM; (2) Development of a disease framework to establish 4 criteria to select ancillary outcome measures; and (3) Second search of PubMed to determine the most useful outcome measures for assessment of CSM.
To establish the current state of outcome measurement in CSM, we evaluated the relative frequency of use of the most common outcome measures and their psychometric properties. PubMed was searched using the name of the outcome measure and the common abbreviation combined with the following terms: “CSM” or “myelopathy.” The search results were limited to human studies published in the English language with no date restriction. The titles and abstracts of the studies identified were checked to verify that the outcome of interest was reported. We also sought to identify and summarize the studies evaluating the validity, reliability, and responsiveness of these outcome measures in the CSM population. Then, we provided a description and interpretation of each measure and an indication of whether the measure had been assessed for validity, reliability, or responsiveness in CSM.
The second stage consisted of defining a disease framework that would establish the selection criteria (Figure 1). Specific criteria were established to seek the most adequate and appropriate outcome measures that would characterize the CSM population optimally. Selection of outcome measures was based on the following criteria: (1) The measure/s are specific to the identified deficits and disabilities related to CSM and capture neurological impairment related to the upper and/lower limbs (Figure 3 defines the neurological and physical deficits that can be related to CSM). (2) The measure is rigorous and has sound psychometric development (reliability, validity, and responsiveness) in CSM or related populations with normative data available. (3) Feasible to administer in an outpatient care environment. (4) Falls into the Body and Structures and Ability categories of the International Classification of Functioning of the World Health Organization.13
The third stage consisted of a second literature search, which was conducted on specified outcomes that were known to address the specified criteria 1 and 4. The literature search was used to determine if criteria 2 and 3 were met for the outcome measures selected. Six measures were selected that are known to be useful in the measurement of upper limb function, disability, balance, and gait.
Stage 1—Defining the Measures Currently Used in the Field: What Is the Current Practice in CSM With Respect to Use of Outcomes Assessment?
The list of outcome measures and their frequency of use in the CSM population can be found in Figure 2. The most commonly cited measure is the Nurick grade (N = 62 studies), followed by modified Japanese Orthopaedic Association Scale (mJOA) (N = 57), visual analogue scale (VAS) for pain (N = 27), Short-Form 36 Health Survey (SF-36) (N = 18), and Neck Disability Index (NDI) (N = 10). The Myelopathy Disability Index (MDI) (N = 6) and European Myelopathy Scale (EMS) (N = 4) were cited in less than 10 studies (Table 1; Figure 2).
The list of validity, reliability, and responsiveness study frequency in a CSM population was also established. The SF-36 was evaluated the most (N = 5) followed by MDI (N = 2), whereas mJOA scale, Nurick grade, and EMS each had one study assessing psychometric characteristics in a CSM population. No validity, reliability, or responsiveness study was found for the pain VAS or NDI in the CSM population (Table 1; Figure 3).
Modified Japanese Orthopaedic Association Scale
The mJOA3 is a modified version of the original JOA scale. It is scored on a 0 to 18 point scale with the lowest score, representing greater disability (Table 1). It is a clinician-based measure that covers items such as upper and lower extremity motor function, hand sensation, and micturition. Only one study4 was identified that tested reliability of the mJOA. This study found the mJOA to have a high degree of interobserver reliability (Table 1). Thus, this tool can be reliably used among multiple examiners.
The Nurick Scale4 was developed to assess gait impairment in patients with CSM. The Nurick Scale is a clinician-based measure containing six grades of CSM ranging from 0 to 5, with a focus on gait impairment (Table 1). As the grade increases the disability increases. One study5 was identified that tested the validity, reliability, and responsiveness of the Nurick Scale. This study compared 7 different outcome measures in a CSM population. The Nurick Scale was validated against the postoperative MDI, EMS, and Ranawat Scale (Table 1).
Myelopathy Disability Index
The MDI6 was developed to measure disability objectively in rheumatoid arthritis complicated by CSM. The MDI consists of 10 items ranging from 0 to 3 points (Table 1). It is a self-report measure that covers the items sit-to-stand, eating, walking, hygiene, and grip strength. These 10 items are summed and converted to percentage with a maximum score of 100 and minimum score of 0.5,6 Disability increases as the score increases. Two studies were identified that tested its validity, reliability, and responsiveness. In one study the MDI was validated against the 20-item Health Activity Questionnaire, Ranawat class, and Steinbrocker grade (Table 1).6 In another study, the MDI was validated against the EMS.5 The MDI was found to be reliable and responsive in both studies (Table 1).5,6 Despite the rigor of this measure's development, it is one of the least used outcomes.
Neck Disability Index
The NDI7 is a modification of the Oswestry Disability Index and developed as a self-report measure of neck pain. The NDI consists of 10 items ranging from 0 to 5 points (Table 1). Some items that the NDI measures are lifting, pain, driving, sleeping, and work activities. These 10 items are summed and normalized to 100. Maximum score is 100 and minimum score is 0. An increasing score indicates increasing disability. The NDI has not had validity or reliability testing in a CSM population but has in patients who underwent neck surgery.
European Myelopathy Scale
The EMS8 was developed to assess myelopathy. It consists of the following 5 items: gait, hand function, proprioception, bladder and bowel function, and parasthesias. Items are scored from 1 to a variable maximum of 3, 4, or 5. Items are summed with a maximum score of 18 and a minimum score of 5 points. An increasing score indicates an increase in severity of myelopathy. One study has addressed validity, reliability, and responsiveness. The EMS was validated against the MDI and, in the same study, was found to have poor sensitivity to change.5
Short-Form 36 Health Survey
The Short-Form 36 Health Survey9 is a measure of patient health status. The SF-36 consists of 8 subscales: Vitality, Physical Functioning, Bodily Pain, General Health, Physical Role, Emotional Role, Social Role, and Mental Health. Items of each subscale are averaged to yield a score of 0 to 100. A score closer to zero represents greater disability. The SF-36 has been tested for validity, reliability, and responsiveness in the CSM population. Guilfoyle et al validated the SF-36 against the MDI and Roland-Morris scale.9 King and Roberts validated the SF-36 against the Nurick Scale, Cooper Scale, and Harsh Scale10; Latimer et al compared the SF-36 with the NDI, MDI, and VAS for neck and arm pain.11 King and Roberts10 found the SF-36 to be reliable. The SF-36 was found to be responsive in 3 studies.11–13
Visual Analogue Scale (VAS) for Pain
The visual analogue scale (VAS) for pain is a single item asking respondents to rate their pain level on a continuous line between 2 end points. On a horizontal line, the further to the left the mark the greater the pain. On a vertical line, the higher the mark the greater the pain. No studies exist testing validity, reliability, or responsiveness of the VAS in the CSM population.
Stage 2—Defining a Framework and Setting Selection Criteria for the Second Search: What Are the Requirements of Outcome Measures Specific to CSM?
The initial literature search does identify measures specific to CSM, which have some psychometric development. However, none of these measures objectively quantify physical findings of the individual. Despite frequency of use, there continues to be a gap due to the insensitivity of the available outcome measures. Therefore, it is necessary to identify ancillary measures that can be used to measure this population in detail a we continue to learn about this disease from the basic and clinical perspectives. Measurement in this field has lagged and will become a concept of significant interest as we learn more about the pathophysiology of this disease, and as new discoveries are translated to humans.2 Selection criteria for outcome measures are defined in the Methods. The criteria were used to identify six outcome measures, QuickDASH, Berg Balance Scale, 30-Meter Walk Test (30MWT), a modified Graded Redefined Assessment of Strength Sensibility and Prehension (GRASSP), Grip strength (dynamometer), and GAITRite.
Stage 3—Targeted Literature Search on Specified Outcome Measures Selected on the Basis of Criteria in Stage 2: What Are the Most Reliable, Valid, Responsive, and Quantitative Outcome Measures That Can Be Used for CSM?
A number of measures do exist, which are appropriate to administer in the CSM population despite their development and use in different but similar patient groups. These ancillary measures can provide information that is more sensitive and developed in a more rigorous fashion than existing tools. These measures are described in Table 2, and how to consider their use is described in Table 3.
The QuickDASH14 was developed to measure physical function and symptoms related to upper limb musculoskeletal disorders by creating a shorter version of the Disabilities of the Arm Shoulder and Hand questionnaire (DASH; see Hudak et al15) (see erratum). The QuickDASH consists of 3 modules (2 modules are optional). The disability and symptom module consists of 11 items ranging from 1 to 5 points (Table 1). It is a self-report measure that covers activities of daily living, recreation activities, social activities, work activities, arm/hand sensation and pain, and sleeping. Items are summed and then normalized from 0 to 100. The higher the score, the greater the disability. For this metric, no validity, reliability, or responsiveness studies were identified in a CSM population. Other populations in which validity, reliability, or responsiveness have been tested include: upper extremity musculoskeletal disorders,14,16–26 carpal tunnel syndrome,27 neck pain,18,19,28,29 upper limb burn,30 and Duypuytren disease.31
Berg Balance Scale
The Berg Balance Scale32 was developed to measure balance among elderly people with impairment. The Berg Balance Scale consists of 14 items scored from 0 to 4 points (Table 1). It is a performance measure that evaluates unsupported standing balance, unsupported sitting balance, and transfers. Maximum score is 56 and minimum score is 0. A lower score represents greater disability. No validity, reliability, or responsiveness studies were identified in a CSM population. Other populations in which validity, reliability, or responsiveness have been tested include: stroke,33–42 balance disorder,43,44 elderly,45–49 multiple sclerosis,41–53 and Parkinson disease,54–56 Neurological disorders including spinal cord and brain injury,57–59 cognitive disability,60,61 and knee arthroplasty.62
Walk Test—30-Meter Walk Test
Several walking tests were identified, including the 30MWT, 10-Meter Walk Test (10MWT), and 6-Minute Walk Test (6MWT). The 30MWT63 seems to be the most common and was developed to measure disability of patients with CSM. The 30MWT is a performance measure of time in seconds to walk 30 m (Table 1). The greater the time, the greater the disability. One study63 was identified that tested its validity and reliability, and no studies were identified that tested responsiveness. The 30MWT was validated against the MDI and Nurick Scale and was highly reproducible. The 30MWT has also been tested in a chronic obstructive pulmonary disease population.64
Graded Redefined Assessment of Strength Sensibility and Prehension
The GRASSP65 was developed as a clinical outcome measure specific to upper limb impairment in individuals with complete or incomplete traumatic tetraplegia. It comprises 5 subtests for each upper limb: dorsal sensation, palmar sensation, strength, and prehension. There are 5 numerical scores that provide a comprehensive profile of upper limb function. No validity, reliability, or responsiveness studies were found in a CSM population in the literature. However, the GRASSP has been validated in the chronic traumatic SCI population.65–67
Grip dynamometer is an instrument used for measuring the force of handgrip muscular contraction. Currently no validity, reliability, or responsiveness studies were found in a CSM population. It has been tested in healthy volunteer individuals.69,74–76
GAITRite Analysis71 is a computerized walkway system embedded with pressure sensors that detect a series of footfalls. The walkway is connected to a personal computer with application software that calculates temporal and spatial gait parameters. No studies were identified in a CSM population testing validity, reliability, or responsiveness. However, the GAITRite system has been tested in these populations: elderly,71–74 children with motor disabilities,73 knee replacement,74 and patients with Parkinson disease.77
As the literature and practice regarding the management of CSM evolves, a remaining challenge is the lack of validation of the outcome measures that are being used to evaluate and define the population. The literature establishes that there is a paucity of measures available, particularly specific, quantitative, sensitive, and validated measures. There are 2 main factors that limit individuals with CSM, upper limb function, and gait impairment (which is closely related to balance). Urogenital dysfunction is also a consequence of cervical cord compression. Consideration of all aspects of impairment and their impact on function are very important. Furthermore, because the variability of impairment is so large, using more than one outcome assists in characterization of the individual, which will enlighten the clinician. Ultimately the selected outcomes will establish more detail at baseline, allow for outcome assessment and assist in decision making pretreatment to determine if there is progression of disease.
The 2 most commonly used measures to quantify CSM are the JOA scale78 and the Nurick grade.4 Both are measures of signs and symptoms, which evaluate gait, lower extremity function, hand function, and bladder control. Despite the widespread use of these outcome measures, they lack the sensitivity to assess the full range of CSM, especially patients with a mild presentation. However, the mJOA is the only measure that addresses the bladder dysfunction in this disease. Commonly used self-perceived measures of improvement in CSM are the NDI79 and the general outcome, SF-36.80 These measures have both been validated for use in patients with cervical spine disorders and provide adequate information regarding self-perceived function.79,80 Neither the JOA nor Nurick assess in a quantitative manner gait, balance, or hand function as it may relate to one's ability to function on a daily basis. Thus, a method using ancillary measures to define severity is required to define clinical presentation in a standardized manner. Measures with greater responsiveness are necessary to define the milder subpopulation and define the predictors of progression, particularly for those individuals who are not offered surgery early in the course of CSM. Use of ancillary measures will also provide the pertinent information required to establish predictors of recovery and outcome after intervention.
To date, the most common methods for treating CSM are by conservative management or performing decompressive surgery. Surgery is more commonly offered to those with a moderate to severe presentation of CSM; however, there is an increase in the number of individuals with mild CSM having surgery. Surgical techniques and approaches have evolved during the past 2 decades, as a result, outcomes are much improved.81,82 Despite the advances in surgical management, the void that remains in the clinical field is the lack of outcome measures which can characterize the population with greater precision. More sensitive outcomes will be useful in establishing efficacy of interventions; assist in identifying the predictors of disease progression and enable clinicians to offer treatment that is most effective and offered at the most appropriate time in the course of this disease. Essentially this will lead to the treatment of CSM before the irreversible sequelae are manifested. Understanding the deficits of this population will enable the establishment of a standard method to define a severity of disease index. Therefore, the objective of this review was to identify the most clinically relevant, quantitative, reliable, valid, and responsive outcome measures for the assessment of CSM that will establish a meaningful clinical dataset, which will allow clinicians to assess outcomes, monitor the natural history of CSM, and establish the predictive value of clinical findings.
Clinicians should consider use of the ancillary measures: QuickDASH, Berg Balance Scale, GRASSP Version 1.0, Grip Strength, GAITRite Analysis, and the 30MWT.
These measures should be implemented into clinical practice either for screening, longitudinal clinical assessment, or longitudinal research assessment. A clinician should consider the use of the outcome measure prior to selection and whether the role of the measure is for screening, longitudinal follow-up, or research follow-up. Use of measures will vary depending on the practice one conducts. However, the NDI and mJOA should always be administered when a patient presents with CSM. These should be standard measures used across centers (see Supplemental Digital Content Appendix 1, available at http://links.lww.com/BRS/A822).
The goal of this review was to identify the most reliable, valid, responsive, and quantitative, outcome measures for the assessment of CSM that will establish a meaningful clinical dataset to allow clinicians to assess outcomes, monitor the natural history of CSM, and establish the prognostic value of clinical findings. The CSM population is a heterogeneous population that cannot be defined thoroughly with a single score on a single outcome measure. Because the clinical presentation and manifestation of CSM is not unidimensional, it is not feasible to use a single unidimensional outcome without missing a large aspect of meaningful clinical information. On the basis of the measures that are available specifically for CSM and related populations, we have established a framework for the use of outcome measures. In summary, we recommend that the mJOA, Nurick grade, MDI, NDI, and 30MWT are most appropriate for the assessment of CSM. However, 6 additional outcome measures (QuickDASH, Berg Balance Scale, GRASSP, Grip Dynamometer, GAITRite Anlaysis) were identified, which provide complementary assessments for CSM.
Summary Statements. There does not exist a single or composite of outcomes instruments that measures myelopathy impairment, function/disability, and participation that has also demonstrated reliability, validity, and responsiveness in a CSM population. More work in the development and psychometric evaluation of new or existing measures is necessary to identify the ideal composite of measures to be used in the clinical and research settings.
- The mJOA, Nurick grade, NDI, MDI, and 30MWT should be adopted in any clinical practice that treats CSM both for screening and clinical follow-up.
- We propose that clinicians and researchers consider using the ancillary measures identified, such as the QuickDASH, Berg Balance Scale, GRASSP version 1.0, Grip Strength, and GAITRite Analysis.
- It is highly recommended that baseline and follow-up measurements should be performed in patients with CSM.
- Although a single outcome measure cannot define the broad range of deficits seen in the CSM population, we recommend the use of the mJOA, NDI, Nurick Scale, and the 30MWT.
- Use of reliable, valid, and responsive outcome measures in CSM is necessary to establish improved management of the population.
- Measures that specifically and sensitively quantify gait, balance, hand strength, hand function, and self-perceived function related to tetraparesis provide more refined information regarding this population.
- Use of such measures will improve clinical management, monitoring, and prognosis for patients with CSM.
Supplemental digital content is available for this article. Direct URL citation appearing in the printed text is provided in the HTML and PDF version of this article on the journal's web site (www.spinejournal.com).
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