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Original Article
Abstract
In this study we examined whether results from a clinical test of passive mobility of soft tissue structures in the upper cervical
spine, corresponded with signs of physical injuries, as judged by magnetic resonance imaging (MRI). Results were based on
examinations of 122 study participants, 92 with and 30 without a diagnosis of whiplash-associated disorder, type 2. The structures
considered were the alar and the transverse ligaments, and the tectorial and the posterior atlanto-occipital membranes. Ordinary and
weighted kappa coefficients were used as a measure of agreement, whereas McNemar’s test was used for evaluating differences in
rating. The clinical classification and the MRI examination both comprised four response categories (grades 0–3), with 0
representing a normal structure, and 3 indicating a structure with pronounced abnormality. In our sample, an abnormal clinical test
reflected a hyper- rather than hypo-mobility. Considering all four-response categories, the kappa coefficient indicated moderate
agreement (range 0.45–0.60) between the clinical and the MRI classification. The results for the membranes appeared somewhat
better than for the ligaments. When there was disagreement, the classifications obtained by the clinical test were significantly lower
than the MRI grading, but mainly within one grade difference. When combining grade 0–1 (normal) and 2–3 (abnormal), the
agreement improved considerably (range 0.70–0.90). Although results from the clinical test seem to be slightly more conservative
than the MRI assessment, we believe that a clinical test can serve as valuable clinical tool in the assessment of WAD patients.
However, further validity- and reliability studies are needed.
r 2007 Elsevier Ltd. All rights reserved.
Keywords: WAD; Manual therapy; MRI; Clinical assessment; Upper cervical spine
1. Introduction
1356-689X/$ - see front matter r 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.math.2007.03.007
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More detailed information on the MRI-protocol, as good agreement, and values above 0.80 indicate very
visualisations, and reliability of the classification criteria good agreement (Altman, 1994).
is given elsewhere (Krakenes et al., 2002, 2003a, b). The sensitivity, specificity and positive and negative
predictive values (PPV, NPV) for the clinical test vs. MR
2.3. The clinical classification were also calculated on the basis of the dichotomised
responses, i.e. grade/category 0–1 considered as normal,
Within manual therapy, tests of passive intervertebral and grade/category 2–3 considered as abnormal.
movements (PIMs) of the cervical spine are frequently
used for patients with neck pain (Trijffel van et al.,
2005). The clinical test used in the present study is based 3. Results
on evaluation of PIM. Such test techniques, however,
has in general not been applied in relation to WAD, or Considering all four-response categories/grades, the
for testing the neck structures considered in the present kappa coefficient showed moderate agreement (range
study. 0.45–0.60) between the clinical and the MRI classifica-
The test for each single structure considered in the tions (Table 1). Most disagreements were close, how-
present study has specific test movements, and aims at ever, and when adding weight also to cases without
clarifying the ability to withstand passive stretching. A complete agreement in the calculations, the weighted
specialist in manual therapy (BRK) performed the kappa coefficient indicated good agreement (range 0.62–
clinical examination while the patient was sitting in a 0.78). The results for the membranes were somewhat
chair. Passive stretching of the ligament and membrane better than for the ligaments (Table 1). When dichot-
was performed through the passive range of motion, or omising the classification results by combining the two
until a muscular contraction occurred due to pain in the best (0–1) and two worst (2–3) categories (Table 2),
area. The predefined clinical categories (category 0–3) agreement was good for the ligaments (values close to
were as follow: Category 0 indicated a normal ligament 0.70), and very good for the two membranes (values
or membrane function. In category 1, a minor increase above 0.90). The very high degree of agreement for the
in motion between test points was found, in category 2 a membranes is probably partly related to the low
moderately abnormal motion was found, and in prevalence of abnormal findings for these structures.
category 3 an extensive increase in motion between test In the case of disagreement, the structures were rated
points was found. Illustrations of performance of the significantly lower by the clinical test than by the MRI
PIM tests are shown in Fig. 1a–d. classification (Table 1, McNemar’s test). However, in
most cases the clinical and MRI classifications differed
2.4. Statistical analyses by only one grade. For the two membranes, the
disagreement was almost completely restricted to a
A joint analysis of persons with and without a WAD classification of grade 1 by the radiological classifica-
diagnosis was performed to ensure sufficient variation in tion, whereas the same patient was classified as grade 0
normal and abnormal findings in the study sample. The by the clinical test. When combining the two lowest and
kappa coefficient was used as a measure of agreement highest categories/grades, there was no systematic
between the classifications based on the clinical test and difference between the classifications of the membranes,
the MRI evaluations. Categories 0–3 on the clinical test but a significant difference remained for the ligaments
were compared with grade 0–3 from the MRI assess- (Table 2). For the right and the left alar ligaments, the
ment. Both ordinary and weighted kappa values were disagreement was then 13.9% and 14.7%, respectively.
calculated. In contrast to the ordinary kappa coefficient, The corresponding number for the transverse ligament
which consider only complete agreement between the was 13.1%.
two judgements, the weighted kappa coefficient gives The sensitivity, specificity and positive and negative
some additional weight to classifications that are close predictive values (PPV, NPV) of the clinical test vs. MRI
(original response ordinal). In the present study, a for the different ligaments and membranes were in
difference between the two classifications of 0, 1, 2 and 3 general rather good (Table 3). For the two ligaments,
was given linear weights 1, 0.67, 0.33 and 0, respectively. however, about 30–35% of the abnormal MRI results
In addition, ordinary kappa was calculated on dichot- did not have a clinically detectable correlate (sensitivity
omized response, i.e. with the two best (grade/category of 0.69, 0.72 and 0.65 for right and left alar ligaments,
0–1) and two worst (grade/category 2–3) categories and the transverse ligament, respectively). This result
combined. The absolute values of the kappa coefficient improved considerably when categories 1–3 (minor,
range from 0–1 (negative values indicate poorer agree- moderate and considerable hyper-mobility) were all
ment than expected by chance). Values less or equal to considered as abnormal on the clinical test (sensitivity
0.20 are interpreted as poor agreement, 0.21–0.40 as fair changed to 0.89, 0.85, and 0.95, respectively). The
agreement, 0.41–0.60 as moderate agreement, 0.61–0.80 NPV also improved slightly with this redefinition of
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abnormality on the clinical test, whereas the specificity abnormalities of ligaments and membranes in the upper
and PPV were somewhat worsened (results not shown), cervical spine. The high degree of agreement when
in particular for the transverse ligament (specificity classifying into normal/abnormal categories indicate that
decreased from 0.99 to 0.73, and PPV decreased from it is possible to detect lesions of these structures by a
0.97 to 0.66). clinical examination, and conversely, that MRI findings
are of clinical relevance. Results from the present study
thus indicate that the clinical assessment techniques have
4. Discussion a potential for being a useful clinical tool, and may serve
as an initial tool for location of an injury.
The present study indicated good agreement between a To our knowledge, this is the first study that has
clinical examination and MRI in the assessment of reported results from a clinical test of soft-tissue
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Table 1
Agreement in classification of lesions to ligaments and membranes in the upper cervical spine areaa, as judged by means of manual therapy techniques
(MT, 1 manual therapist) and MRI-reading (MRI, 1 radiologist)
Ligaments
Alar, right 33.6 1.6 10.7 15.6 38.5 0.45 (0.35–0.57) 0.66 (0.58–0.75) o0.001
Alar, left 33.3 2.5 11.5 13.9 38.8 0.45 (0.34–0.56) 0.62 (0.52–0.72) o0.001
Transverse 35.2 11.5 9.0 11.5 32.8 0.53 (0.41–0.64) 0.69 (0.60–0.78) o0.001
Membranes
Tectorialb 64.1 5.8 8.3 3.3 18.5 0.60 (0.45–0.74) 0.72 (0.60–0.84) o0.001
Atlanto-occ.b 62.8 0.8 8.3 9.1 19.0 0.60 (0.46–0.74) 0.78 (0.68–0.87) o0.001
a
Results based on 122 persons: 92 WAD2 patients and 30 healthy individuals.
b
One missing value.
c
McNemar’s test for systematical differences.
structures in the upper cervical spine compared to the definition of classification criteria as well as application
results of a radiological method. Our initial step in of it, are needed in order to apply these test techniques
evaluating the usefulness of these tests has been to successfully in an ordinary clinical setting.
compare with results from an MRI classification shown In the assessment of agreement, we directly compared
to correlate well with subjective symptoms in the WAD loss of collagen integrity as judged by MRI (grade 0–3),
patients (Kaale et al., 2005a). The clinical tests were with degree of increased mobility as judged by the
based on techniques within manual therapy, and were clinical examination (category 0–3). We thus explored
performed by a specialist in manual therapy (BRK) with whether signs of a physical injury of a specific neck
long experience in application of these tests on WAD structure affected the passive mobility of that structure.
patients. Results from validity and reliability studies of In most cases of disagreement, it was an abnormal MRI
PIMs, although used in other circumstances and for result that did not have a clinical correlate, rather than
other structures that the one tested in the present study, the opposite. The sensitivity for the clinical test vs. MRI
have varied somewhat (Trijffel van et al., 2005; Piva improved when changing the definition of abnormality
et al., 2006). The performance of the clinical test will on the clinical test to include category 1 (minor hyper-
depend on the experience of the clinician. A clear mobility), rather than only categories 2–3 (moderate and
Fig. 1. (a–d) Illustrations of the clinical test techniques. The passive intervertebral movement (PIM) tests assess the occipital-atlas-axis mobility.
Each test put stress on individual soft tissue structures, and the test try to qualify the tested motion. In all test procedures, the person’s head rests
against the chest of the examiner, acting as a stabilising factor. (a) Test of the alar ligaments. The test of the alar ligaments assesses the quality of
rotation between occipital-atlas-axis. Insufficiency of the ligament gives a hypermobil function in this area. Test procedures: Both hands are placed on
the same side of the person’s cervico-occipital junction. The lower (right) hand stabilises C2 by pressing finger 2 and 3 against the lateral aspect of
C2—pulling this part backwards. The test of the ligament is performed by an upward pull into rotation with two fingers on the left hand, one finger is
placed (finger 3) under the lateral mass of atlas, and finger 2 is placed under the mastoid processus. The test is performed with different
angles of cervical rotation, to locate the exact test position that gives the maximal movement between C1 and C2. (b) Test of the transverse ligament.
The test of the transverse ligament assesses the ventral/ dorsal translation of atlas against axis. Insufficiency of this ligament gives an excessive
translation of atlas. Test procedures: C2 is stabilised by a frontal grip. This stabilisation is performed by pressing the thumb against the frontal part of
the left lateral process, while fingers 2 and 3 are pressed against the right lateral process. It is important that the finger grip must not give a feeling of
strangling. The test movement is performed by pressing the thumb against the posterior part of the left lateral mass of atlas, while holding finger 2
against the lateral mass on C1 on the opposite side. At the same time, fingers 1 and 2 are pressed firmly against the inferior part of the occiput. The
flexed fingers 3–5 support the grip from below. C1 (occiput follows the movement of atlas) is pressed forward and C2 is pressed backwards, testing
the translation of dens axis in the space from the transverse ligament to the posterior part of C1. The test is performed from neutral position between
C1 and C2, and through several steps of increasing flexion. (c) Test of the tectorial membrane. The test of the tectorial membrane assesses degree of
ventral horizontal translation between occiput-atlas-axis. The right hand, that performs the passive test movement, is placed in the suboccipital
region. Fingers 1 and 2 are formed as a semicircle, and are pressed against the lower part of occiput. Finger 1 and 2 are supported from below by
flexed fingers 3, 4 and 5. C1 is following the ventral and cranial movement of the occiput. C2 is stabilized by a frontal grip. The test movement goes
forward combined with a traction force. The test is performed with different angles of flexion and degrees of traction. A positive test result is given by
an excessive translation between occiput/ C1 and C2. (d) Test of the posterior atlanto-occipital membrane. The test of the posterior atlanto-occipital
membrane assesses the stability in the posterior part of the neck between occiput and atlas. Both hands are placed in the suboccipital region. The
lower (right) hand is stabilising the C1 by a downward pressure with thumb and fingers placed on the lateral mass of atlas. The upper (left) hand is
formed as a grip, with the fingers directed downwards. The test is performed by pulling with the left hand in the opposite direction of the downward
pressure performed by the other hand. The pulling is repeated several times through different angles of flexion.
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Table 2
Agreement in classification of lesions to ligaments and membranes in the upper cervical spine areaa, as judged by means of manual therapy techniques
(MR, 1 manual therapist) and MRI-reading (MRI, 1 radiologist)
% both normala % both abnormalb % disagree Kappa coefficient (95% C.I.) P-valuec
Alar ligament, right (n ¼ 122) 55.7 30.3 13.9 0.71 (0.58–0.83) o0.001
Alar ligament, left (n ¼ 122) 53.3 32.0 14.8 0.69 (0.57–0.82) 0.008
Transverse ligament (n ¼ 122) 63.9 23.0 13.1 0.69 (0.55–0.83) 0.001
Tectorial membrane (n ¼ 121) 86.0 12.4 1.6 0.93 (0.83–1.03) 1.00
Atlanto-occ. membrane (n ¼ 121) 81.0 18.2 0.8 0.97 (0.92–1.03) 1.00
a
For MT evaluation, normal correspond to normal or minor increase in motion, and for MRI, normal correspond to grade 0 or 1.
b
For MT evaluation, abnormal correspond to moderately or extensively increased motion, and for MRI, abnormal correspond to grade 2 or 3.
c
McNemar’s test for systematical differences.
Table 3
Number of classifications and diagnostic values for manual therapy vs. MRI classifications for ligaments and membranes in the upper cervical spine,
calculated on the basis of classifications of 122 persons; 92 WAD patients and 30 control persons
Alar ligament, right 68 37 0 17 0.69 (0.56–0.81) 1.00 (1.00–1.00) 1.00 (1.00–1.00) 0.80 (0.71–0.89)
Alar ligament, left 65 39 3 15 0.72 (0.60–0.84) 0.96 (0.91–1.00) 0.93 (0.85–1.01) 0.81 (0.73–0.90)
Transverse ligament 78 28 1 15 0.65 (0.51–0.79) 0.99 (0.96–1.01) 0.97 (0.90–1.03) 0.84 (0.76–0.91)
Tectorial membranee 104 15 1 1 0.94 (0.82–1.06) 0.99 (0.97–1.01) 0.94 (0.82–1.06) 0.99 (0.97–1.01)
Atlanto-occ. membranee 98 22 0 1 0.96 (0.87–1.04) 1.00 (1.00–1.00) 1.00 (1.00–1.00) 0.99 (0.97–1.01)
a
Sensitivity is the proportion classified as abnormal by MRI (grade 2–3) that are classified as abnormal also by MT (grade 2–3).
b
Specificity is the proportion classified as normal by MRI (grade 0–1) that are classified as normal also by MT (grade 0–1).
c
PPV (positive predictive value) is the proportion classified as abnormal by MT (grade 2–3) that are classified as abnormal also by MRI
(grade 2–3).
d
NPV (negative predictive value) is the proportion classified as normal by MT (grade 0–1) that are classified as normal also by MRI (grade 0–1).
e
1 missing value.
major hypermobility). In view of normal variation and distance to perform the test, compared with the testing
difficulties with interpretations of the MRI (Krakenes of the membranes. Pain raised from the examined area
et al., 2001, 2002, 2003a, b), false positive results based can increase the muscular tension, and thereby also
on MR cannot be ruled out. Nevertheless, MRI is so far influence the performance of the clinical test. Individual
regarded as the best tool in visualising the collagen differences in soft tissue stiffness may also be of
integrity of soft tissue structures (Erickson, 1997), and importance. Classifications into normal/ abnormal
was considered to represent the ‘gold standard’ in the categories improved agreement between clinical and
present study. radiological test results. In view of individual variations
In general, we achieved better agreement between the as well as difficulties with performing the clinical tests, a
clinical test results and the MRI classification for the two-grade system (normal, abnormal) is probably most
membranes than for the ligaments. This may be due to a efficient in an ordinary clinical setting.
considerably lower prevalence of membrane injuries in The ligaments and membranes in the upper cervical
our material, but may also be related to the higher spine participate in different combinations of functions
elasticity of the membranes, making them easier to (Williams and Warwick, 1980; Crisco et al., 1991;
assess clinically than the thicker and stiffer ligaments. Dvorak et al., 1991). Which structure and what part
For the membranes, the test techniques can be of it that is injured are probably decisive for how it will
performed through a longer range of passive motion, affect the cranio-vertebral mobility. Direction of ex-
and therefore the dysfunction can be detected more ternal and internal forces during the whiplash trauma
easily. The alar and the transverse ligaments are short has been found to be of importance for what structures
and strong, with a higher content of non-elastic collagen are injured (Kaale et al., 2005b). For a purposeful and
fibres, compared with the two membranes (Williams and efficient MRI examination, it is essential to know what
Warwick, 1980). Thus, for the ligaments, the tested specific area or structure to focus on. The present
range of motion is smaller, and we have a shorter findings of a clinically detectable hyper-mobility in
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