Reliability and Validity of Clinical Tests to Assess
the Anatomical Integrity of the Cervical Spine in
Adults with Neck Pain and its Associated Disorders:
Part 1- A Systematic Review from the Cervical Assessment
and Diagnosis Research Evaluation (CADRE) CollaborationThis section was compiled by Frank M. Painter, D.C.
Send all comments or additions to: Frankp@chiro.org
FROM: European Spine Journal 2017 (Sep); 26 (9): 2225–2241 ~ FULL TEXT
Lemeunier N, da Silva-Oolup S, Chow N, Southerst D, Carroll L, Wong JJ, Shearer H, Mastragostino P, Cox J, Côté E, Murnaghan K, Sutton D, Côté P
Institut Franco-Européen de Chiropraxie,
72 chemin de la Flambère,
31300, Toulouse, France.
nlemeunier@ifec.net
OBJECTIVE: To determine the reliability and validity of clinical tests to assess the anatomical integrity of the cervical spine in adults with neck pain and its associated disorders.
METHODS: We updated the systematic review of the 2000-2010 Bone and Joint Decade Task Force on Neck Pain and its Associated Disorders. We also searched the literature to identify studies on the reliability and validity of Doppler velocimetry for the evaluation of cervical arteries. Two independent reviewers screened and critically appraised studies. We conducted a best evidence synthesis of low risk of bias studies and ranked the phases of investigations using the classification proposed by Sackett and Haynes.
RESULTS: We screened 9022 articles and critically appraised 8 studies; all 8 studies had low risk of bias (three reliability and five validity Phase II-III studies). Preliminary evidence suggests that the extension-rotation test may be reliable and has adequate validity to rule out pain arising from facet joints. The evidence suggests variable reliability and preliminary validity for the evaluation of cervical radiculopathy including neurological examination (manual motor testing, dermatomal sensory testing, deep tendon reflexes, and pathological reflex testing), Spurling's and the upper limb neurodynamic tests. No evidence was found for doppler velocimetry.
CONCLUSIONS: Little evidence exists to support the use of clinical tests to evaluate the anatomical integrity of the cervical spine in adults with neck pain and its associated disorders. We found preliminary evidence to support the use of the extension-rotation test, neurological examination, Spurling's and the upper limb neurodynamic tests.
KEYWORDS: Neck pain, Assessment, Diagnosis, Neurological tests, Vertebrobasilar insufficiency, Stenosis, Dissection, stroke, Doppler velocimeter
From the FULL TEXT Article:
Introduction
Neck pain and its associated disorders (NAD) are common in the general population. More than 80% of individuals experience NAD during their lifetime and 30–50% of the general adult population reports neck pain annually. [1, 2] Most neck pain is benign, but patients with neck pain may present with serious underlying pathologies such as cervical spine radiculopathy, fracture, cervical artery dissections, infection, or neoplasm. Accurate diagnoses are necessary to guide patient management and inform prognosis. [3] However, ruling out pathologies can be challenging and requires an approach that is based on valid and reliable tests.
Previous systematic reviews found limited evidence to support the utility of commonly used clinical tests to assess the anatomical integrity of the cervical spine. [4, 5] Specifically, the clinical utility of provocation tests for cervical radiculopathy and doppler velocimetry for vascular lesions of the cervical arteries remains controversial. [6–14] In 2008, the Bone and Joint Decade 2000–2010 Task Force on Neck Pain and Its Associated Disorders [Neck Pain Task Force (NPTF)] conducted a systematic review of the literature on the diagnosis and assessment of neck pain. [15] The Neck Pain Task Force found three validity studies of clinical tests that assess the anatomical integrity of the cervical spine in patients with NAD. [16–18] The studies reported that sensitivity of the Spurling’s test and the upper limb neurodynamic test (ULNT)/ upper limb tension test (ULTT) ranged from 77 to 90%, and specificity ranged from 22 to 94% when compared with gold standards [MRI, nerve conduction studies (NCS), electromyography (EMG), and myelography]. [15] The NPTF found no reliability study of these tests. Furthermore, they did not report on clinical tests used to detect vascular lesions of the cervical arteries.
The purpose of this systematic review is to update the findings of the NPTF on the reliability and validity of clinical tests used to assess the anatomical integrity of the cervical spine in adults with NAD. This review is the first of a series of five systematic reviews updating the NPTF on the reliability and validity of clinical tests and tools used to assess patients with NAD. Subsequent reviews focus on screening for cervical spine injuries [19], measurement of pain and disability [20], palpation and cervical mobility [21], and functional tests of the cervical spine. [22] Together, the purpose of these reviews is to inform the development of a clinical practice guideline for the clinical assessment of the cervical spine.
Methods
Registration
This article synthesizes the evidence from three systematic reviews. The protocols for these reviews were registered with the International Prospective Register of Systematic Reviews (PROSPERO). (CRD42016039362, CRD42016042782, CRD42015025471).
Eligibility criteria
Our reviews targeted studies of adults (18 years and older) with NAD grades I–IV including whiplash-associated disorder (WAD) grades I–IV. We defined NAD according to the NPTF [23] (Online Appendix 1) and WAD according to the Quebec Task Force [24] (Online Appendix 2).
We included studies evaluating the reliability or validity of clinical tests for the assessment of anatomical lesions (musculoskeletal, neurological, or vascular). Clinical tests used to identify anatomical lesions include procedures hypothesized to stress isolated anatomical structures. [16, 17] These include:(1) the evaluation of non-pathological musculoskeletal structures such as joints, muscles, ligaments, and tendons;
(2) nerve root provocation tests used to identify cervical radiculopathy;
(3) neurological examination tests used to assess deep tendon reflexes, pathological reflexes motor strength, and sensory testing; and
(4) hand-held doppler velocimetry to identify vascular lesions.Eligible studies had to report on the validity or reliability of clinical tests.
Reliability is the extent to which repeated measurements of a stable phenomenon by different people and instruments at different times and places produce similar results.
Validity is the degree to which the data measure what they were intended to measure — that is, the results of a measurement correspond to the true state of the phenomenon being measured. [25]
Study characteristics
Studies included in our review met the following inclusion criteria:(1) English language;
(2) published in a peer-reviewed journal;
(3) report on the validity or reliability of a clinical test; and
(4) included adults (18 years of age or older) with grades I–IV NAD.Studies that included individuals less than 18 years of age were considered for inclusion if a stratified analysis was conducted and separate results were reported for adults.
We excluded:(1) practice guidelines, letters, editorials, commentaries, unpublished manuscripts, dissertations, government reports, books and book chapters, conference proceedings, meeting abstracts, lectures and addresses, consensus development statements, and guideline statements;
(2) systematic and non-systematic reviews, and case studies;
(3) cadaveric or animal studies;
(4) studies solely targeting individuals with grade IV NAD, or serious pathology (e.g., fractures, dislocations, myelopathy, neoplasms, and infection) and systemic diseases; and
(5) studies with sample size less than 20 per group.
Data sources and searches
We developed three search strategies (Online Appendices 3A, 3B, and 3C) with the assistance of a health science librarian. A second librarian peer-reviewed each search strategy. We searched MEDLINE, CINAHL, and the Cochrane Central Register of Controlled Trials (The Cochrane Library) for: (1) the evaluation of non-pathological musculoskeletal lesions from January 1, 2005 to January 1, 2016; (2) the evaluation of cervical radiculopathy (nerve root provocation and neurological tests) from January 1, 2006 to June 30, 2016; and (3) clinical tests identifying vascular lesions from January 1, 1980 to February 1, 2016. Moreover, we repeated our searches in SportsDiscus and PubMed for tests evaluating non-pathological musculoskeletal lesions, and non-neurological provocation tests and PubMed for tests that aim to identify vascular lesions. Each search strategy was developed in MEDLINE through Ovid Technologies Inc., and subsequently adapted to the other bibliographic databases. We used a broad search strategy and included terms relevant to NAD, diagnostic tests, validity, and reliability, including subject headings specific to each database (e.g., MeSH in MEDLINE) and free text words.
Study selection
We used a two-stage screening process to identify eligible studies. In stage 1, pairs of reviewers (JC_NC; NC_LC; PM_JW; SdSO_DS; NL_EC; and NL_SdSO) used the inclusion and exclusion criteria to independently screen titles and abstracts, and classify articles as relevant, possibly relevant, or irrelevant. In stage 2, the same reviewers independently screened possibly relevant studies by reviewing fulltext manuscripts. In both stages, reviewers met to resolve disagreements and reach consensus on the eligibility of studies.Athird independent reviewer resolved disagreements.
Quality assessment
A pair of independent reviewers (NC_JW; NL_EC; and NL_SdSO) critically appraised the methodological quality of each eligible article. We used the modified Quality Appraisal Tool for Studies of Diagnostic Reliability (QAREL) [26] to appraise the quality of reliability studies and the modified Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2) [27] to evaluate validity studies. We modified the original QAREL and QUADAS-2 instruments for our review by: (1) adding one question to assess the clarity of the study objective; (2) adding ‘‘not applicable’’ options for questions (QAREL items # 3, 4, 5, 6, and 8, QUADAS items # 3.1, 3.2, 3.3, and 3.B); and (3) adding the Sackett and Haynes classification to the QUADAS- 2. [28] We contacted authors of eligible studies to obtain additional information if it was necessary to determine the internal validity of a study. Reviewers met to reach consensus on the internal validity of studies. A third independent reviewer was used to resolve disagreements.
Studies with a low risk of bias (adequate internal validity) were included in our best evidence synthesis. We classified each low risk of bias study into one of four categories according to the nomenclature proposed by Sackett and Haynes. [28] This classification system is useful to determine the level of scrutiny to which a clinical test/tool has been subjected to determine its clinical utility. According to this nomenclature, Phase I studies answer the following question: ‘‘Do test results in patients with the target disorder differ from those in normal people?’’ Phase II studies ask: ‘‘Are patients with certain test results more likely to have the target disorder than patients with other test results?’’ Phase III studies focus on the following question: ‘‘Does the test result distinguish patients with and without the target disorder among patients in whom it is clinically reasonable to suspect that the disease is present?’’ Finally, Phase IV studies answer the last question: ‘‘Do patients who undergo this diagnostic test fare better (in their ultimate health outcomes) than similar patients who are not tested?’’ Early studies of novel tests provide preliminary evidence of clinical utility, and Phase III or IV studies are needed to inform the validity and utility of a test in clinical practice.
Data extraction and synthesis of results
Authors (NC, NL, and SdSO) extracted data from studies with low risk of bias and built evidence tables (Tables 1, 2). A second reviewer (JW, EC, and NL) independently checked extracted data. Due to heterogeneity among accepted studies, a qualitative synthesis of findings from studies with a low risk of bias was performed to develop evidence statements according to principles of the best evidence synthesis. [29]
Statistical analyses
We computed the inter-reviewer agreement [kappa coefficient (k) with 95% confidence intervals (CI)] for article screening. [30] The percentage agreement for critical appraisal of articles was calculated. Reporting This systematic review was organized and reported based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement [31] and Statement for Reporting Studies of Diagnostic Accuracy (STARD). [32]
Results
We screened 9022 citations (Fig. 1a–c). Eight articles were critically appraised and all eight had a low risk of bias. [38–40]
The inter-rater agreement for screening of articles was kappa = 0.40 (95% CI -0.15, 0.94) for non-pathological musculoskeletal tests and kappa = 1.00 (95% CI 1.00, 1.00) for nerve root provocation tests and neurological examination. The percentage agreement for article admissibility during independent critical appraisal was 88.0% (7/8).
We contacted the authors of five studies to obtain additional information [35, 36, 41–43] and two responded. [35, 36]
Study characteristics
Three of the eight low risk of bias studies evaluated reliability [33, 37, 38] (Table 1). All three studies reporting on reliability assessed inter-examiner reliability [33, 37, 38] and one assessed intra-examiner reliability. [33] Five studies reported on validity [34–36, 39, 40] (Table 2): three were classified as Phase II studies [34, 36, 39] and two were classified as Phase III studies. [35, 40]
The available evidence focussed on the reliability and validity of the cervical extension–rotation test (two studies) [33, 34], the Spurling’s test (four studies) [36–39], and neurological examination (two studies). [35, 38] The reliability of upper limb tension tests was assessed in two studies. [37, 38] One study assessed the validity of upper limb neurodynamic tests. [40] Although they have different names (upper limb tension test and upper limb neurodynamic test), both are similar nerve root provocation tests.
No article studying doppler velocimetry for the assessment of cervical artery vascular lesions in patients with NAD was found.
Risk of bias
The methodological quality of eligible studies is presented in Tables 3 and 4. All reliability studies with low risk of bias used a clearly focused and appropriate research question and chose samples of subjects and raters that were representative of the intended population. Furthermore, the time interval between assessments was stable and all studies used appropriate statistical measures.
However, we noted the following potential methodological limitations:(1) o blinding of raters to the results of other examiners (n = 2/3) [33, 37] or unclear (1/3) [38];
(2) the order of the examinations was not varied (n = 1/3) [37]; and
(3) methods of performing and interpreting the test were unclear (n = 1/3). [37]All validity studies with low risk of bias avoided inappropriate exclusion criteria in the patient selection, described the use of an appropriate reference standard, and ensured that all patients received the same reference standard.
However, the following limitations were noted:(1) a consecutive sampling method was not used [39] or the sampling method was unclear (n = 2/5) [36];
(2) or blinding of the examiners to the reference standard (n = 1/5) [36] or unclear (n = 1/5) [39];
(3) no pre-specified threshold for interpretation of the reference standard (n = 1/5) [35];
(4) time interval between the index test and reference standard was not clearly described (n = 1/5) [36]; and
(5) unclear if all patients were included in the analysis (n = 2/5). [36, 39]
Summary of evidenceReliability
Cervical extension–rotation test Evidence from one study suggests that the extension–rotation test has adequate reliability for the detection of pain originating from the cervical facet joints in patients with NAD. [33] The inter-examiner reliability was kappa = 0.92 (95% CI 0.43, 0.98) for the right side and kappa = 0.93 (95% CI 0.45, 0.98) for the left side of the neck. The intraexaminer reliability was kappa = 0.73 (95% CI 0.18, 0.86) for the right side and kappa = 0.75 (95% CI 0.23, 0.88) for the left side. [33]
Nerve root provocation tests Evidence from two studies suggests that for the assessment of patients with persistent NAD grades I–III, the reliability of the upper limb neurodynamic test or upper limb tension test, and Spurling’s test is inadequate and associated with important misclassification of patients. [37, 38] One study reported that the interrater reliability of Spurling’s test was kappa = 0.13 (95% CI -0.19, 0.45) [37], whereas two studies [37, 38] found that the inter-examiner reliability of the upper limb neurodynamic test/upper limb tension test was kappa = 0.36 (95% CI 0.04, 0.68) and kappa = 0.45 (95% CI 0.27, 0.63), respectively. The inter-rater reliability for the median nerve upper limb tension test was kappa = 0.54 (SE 0.18). [38]
Neurological examination Evidence from one study suggests that the inter-examiner reliability of manual motor testing and dermatomal sensory testing for the assessment of adults with persistent NAD grades I–III is likely associated with misclassification of patients. [38] Schmid et al. found that the inter-examiner reliability was kappa = 0.68 (95% CI 0.53, 0.83) for manual motor testing and kappa = 0.53 (SE 0.13) for dermatomal sensory testing.
Validity
Cervical extension–rotation test Evidence from one Phase II study suggests that the cervical extension–rotation test has a sensitivity = 82.7% (95% CI 70.3, 90.6) and a specificity = 58.9% (95% CI 47.5, 69.5) compared to comparative medial branch blocks as a reference standard [34] for the evaluation of cervical facet jointmediated pain. When the extension–rotation test was used in combination with other examination techniques (e.g., manual spinal examination and/or palpation for segmental tenderness), the specificity improved [from 58.9% (95% CI 47.5, 69.5) with extension–rotation test alone to 83.4% (95% CI 73.4, 90.3) with the three examination techniques combined]; the same applies for the positive likelihood ratios [from LR+ 2.01 (95% CI 1.49, 2.72) LR–: 0.29 (95% CI 0.16, 0.55) with extension– rotation test alone to LR+: 4.71 (95% CI 2.75, 8.05); LR–: 0.27 (95% CI 0.16, 0.45) for the three techniques combined]; however, sensitivity decreased [from 82.7% (95% CI 70.3, 90.6) to 77.4% (95% CI 64.5, 86.6)] with the three techniques combined (extension– rotation test, manual spinal examination, and palpation for segmental tenderness).
Nerve root provocation tests Two Phase II low risk of bias studies assessed the validity of Spurling’s test for the assessment of cervical nerve root compression. [36, 39] Evidence from one study suggests that the sensitivity and specificity of Spurling’s test were 0.95 and 0.94, respectively, when compared to CT findings. [36] The positive and negative likelihood ratios were 15.8 and 0.05, respectively. In the other Phase II study, Anekstein et al. assessed the validity of six variations of the Spurling’s test [39] and found that the manoeuvre consisting of extension, lateral bending, and axial compression of the neck elicited more arm pain (mean VAS 7/10) and more distally elicited pain (mean pain = 2.5/3 with 0 = no pain; 1 = neck pain only; 2 = pain provoked only proximal to the elbow, and 3 = pain provoked distal to the elbow) compared to control groups.
In one Phase III study of patients with grades II–III NAD, the sensitivity and specificity of the upper limb neurodynamic test used to assess cervical nerve root compression were 0.97 (95% CI 0.85, 0.99) and 0.69 (95% CI 0.44, 0.86) when compared to MRI findings, patient history, and clinical examination. [40] The positive and negative predictive values were 0.87 (95% CI 0.73, 0.96) and 0.92 (95% CI 0.61, 1.00), respectively. The positive and negative likelihood ratios were 3.13 and 0.04, respectively.
Neurological examination Evidence from one Phase III study suggests that the sensitivity and specificity of a neurological examination (i.e., manual muscle testing, dermatomal sensory testing, deep tendon reflexes, and pathological reflex testing) were 0.83 (95% CI 0.55, 0.95) and 0.28 (95% CI 0.15, 0.46), respectively, when compared to needle EMG. [35] The positive and negative predictive values were 0.32 and 0.80, respectively. The positive and negative likelihood ratios were 1.15 (95% CI 0.82, 1.61) and 0.60 (95% CI 0.15, 2.44), respectively.
Discussion
We reviewed the evidence on the reliability and validity of clinical tests for the assessment of the anatomical integrity of the cervical spine in adults with NAD grades I–IV. Very little evidence is available to justify the use of these clinical tests. We found preliminary evidence suggesting that the extension–rotation test may be valid to rule out pain originating from the cervical facet joints in adults with persistent NAD. However, this is based on Phase II evidence and these results need to be tested in a Phase III study. Similarly, we found preliminary evidence suggesting that the Spurling’s test may be valid to rule out radiculopathy in patients with persistent NAD III. Again, this evidence is from a Phase II study; therefore, diagnostic accuracy of the Spurling’s test needs to be tested in a Phase III study.
Our review suggests that the upper limb neurodynamic test/upper limb tension may be valid to rule out cervical radiculopathy. Finally, the execution of manual motor muscle testing and dermatomal sensory testing is associated with important misclassification and the neurological examination (including manual muscle testing, sensory dermatomal testing, deep tendon reflexes, and pathological reflex testing) may be sensitive, but has poor specificity.
Update of findings from the NPTF
Our review expands on the findings of the NPTF. In their 2008 systematic review, the NPTF did not identify studies on the validity of tests for the assessment of nonpathological musculoskeletal lesions. Despite their call for further research, our review found only two highquality studies on this topic. Our update of the NTPF found limited evidence suggesting that the cervical extension–rotation test may be useful for the identification of pain originating from the cervical facet joint in adults with persistent NAD grades I–II. Our review supports the findings of the NPTF concerning the validity of nerve root provocation tests. Specifically, we found evidence consistent with the conclusions of the NPTF that the Spurling’s test and the upper limb neurodynamic test/upper limb tension test may be valid for the evaluation of nerve root compression in adults with persistent NAD grades I–III. [15] However, it is important to note that the reliability of the Spurling’s and upper limb neurodynamic test/upper limb tension tests is not adequate. Therefore, its clinical utility could be improved. We found no evidence on the assessment of cervical artery patency using doppler velocimetry in patients with NAD.
Strengths and limitations
Our review has strengths. First, our search strategy was reviewed by a second librarian. Second, we defined a specific set of inclusion and exclusion criteria to identify all possibly relevant citations from the searched literature. Third, two independent reviewers screened and critically appraised all articles. Fourth, we used a wellaccepted and valid set of criteria to critically appraise studies. [26, 27] Finally, our best evidence synthesis minimizes bias by synthesizing evidence from low risk of bias studies. [29]
Our review also has limitations. First, we restricted our search to studies published in the English language; therefore, we may have omitted relevant studies. However, previous systematic reviews have found that this restriction does not lead to a bias. [44–48] Second, critical appraisal requires scientific judgment that may vary among reviewers. This potential bias was minimized by training reviewers to use a standardized critical appraisal tool and using a consensus process among reviewers to reach decisions. Finally, like all systematic reviews, our search may not have included all relevant studies. The inter-rater agreement for screening of titles and abstracts could have been higher. However, disagreements were resolved by a consensus discussion between two reviewers before a final decision on its eligibility was made.
Clinical implication
Most of the evidence on the assessment of the anatomical integrity of the cervical spine is preliminary. Therefore, few clinical tests can be used to assess adults with NAD. Based on preliminary evidence, clinicians may consider using the extension–rotation test, neurological examination (manual motor testing, dermatomal sensory testing, deep tendon reflexes, and pathological reflex testing), Spurling’s test, and upper limb neurodynamic tests. However, clinicians should be aware that the validity of these tests is not firmly established and could lead to misdiagnosis. The clinical utility of these tests could be increased with a proper training, leading to reduced misclassification error and improved reliability.
The current evidence suggests that clinicians must conduct a thorough clinical history and investigate red flags to rule out serious pathology. This is a clinician’s most important responsibility. Clinical tests that do not have evidence of reliability and validity can lead to misdiagnosis and should not be used in clinical practice; therefore, they should not be used until their validity has been demonstrated.
Conclusions
We found limited evidence to support the use of clinical tests used to evaluate the anatomical integrity of the cervical spine. The evidence is at best preliminary for a few tests. Clinicians have very few valid and reliable clinical tests to evaluate patients and arrive at a meaningful diagnosis. This emphasizes the importance of a thorough clinical history to exclude red flags and avoid misdiagnosis of patients with neck pain. Future research needs to address this important gap.
Acknowledgements
The authors acknowledge and thank Mrs. Sophie Despeyroux, librarian at the Haute Autorite´ de Sante´, for her suggestions and review of the search strategy. This research was undertaken, in part, thanks to funding and supervision from the Canada Research Chairs program to Dr. Pierre Cote, Canada Research Chair in Disability Prevention and Rehabilitation at the University of Ontario Institute of Technology.
Funding
This study was funded by the Institut Franco-Europe´en de Chiropraxie, the Association Franc¸aise de Chiropraxie, and the Fondation de recherche en chiropraxie in France. None of these associations were involved in the collection of data, data analysis, interpretation of data, or drafting of the manuscript.
Conflict of interest
The authors declare that they have no conflict of interest.
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