- Email: [email protected]
Cervical muscles weakness in chronic whiplash patients
Clinical Biomechanics 20 (2005) 794–798 www.elsevier.com/locate/clinbiomech
Cervical muscles weakness in chronic whiplash patients Tamara Prushansky
a,*
, Reuven Gepstein b, Carlos Gordon c, Zeevi Dvir
a
a
Department of Physical Therapy, Sackler Faculty of Medicine, Tel Aviv University, 69978 Tel Aviv, Israel Spine Surgery Unit, Department of Orthopedics, Sapir Medical Center, Kfar Saba, Tel Aviv University, Israel Department of Neurology, Sapir Medical Center, Kfar Saba, Sackler Faculty of Medicine, Tel Aviv University, Israel b
c
Received 30 January 2005; accepted 6 May 2005
Abstract Background. Isometric cervical strength has been used for assessing the severity of cervical spine pathologies. However there is a conspicuous dearth of information relating to cervical strength data in patients suffering from chronic whiplash. Therefore the objective of this study was to compare absolute and ratio-based isometric cervical strength scores in chronic whiplash patients with reported corresponding scores in healthy subjects. Methods. Isometric cervical strength was measured in the directions of flexion, extension, right and left lateral flexion in 97 patients, 51 women and 46 men, using a wall-mounted dynamometer. Findings. Compared to published values of normal subjects, whiplash patients suffered sharp reductions of about 90% in both genders and in all directions. The consistency of the isometric cervical strength scores as indicated by the mean coefficient of variation was relatively low, 17% and 20% in men and women respectively. The flexion/extension strength ratio ranged 0.8–0.9, slightly higher than the reported range for normal subjects. This ratio was highly correlated (r = 0.91, P = 0.01) with the mean coefficient of variation in a subgroup of 9 patients. Interpretation. In the absence of an obvious reason such as sever atrophy or grossly dysfunctional neurological control the indicated weakness of the cervical muscles may be associated with learned pain avoidance behavior which is typical among this group of patients. 2005 Published by Elsevier Ltd. Keywords: Whiplash; Isometric strength; Cervical spine
1. Introduction The main function of the neck muscles is to maintain postural balance via the exertion of isometric tension (Ylinen et al., 1999). There is ample evidence that cervical strength is compromised in various cervical disorders and therefore the assessment of isometric cervical strength (ICS) may be an important indicator for cervical impairment (Silverman et al., 1991; Jull et al., 2004). Various instruments for measurement of ICS have been described. Most are based on the use of fixed load *
Corresponding author. E-mail address: [email protected] (T. Prushansky).
0268-0033/$ - see front matter 2005 Published by Elsevier Ltd. doi:10.1016/j.clinbiomech.2005.05.003
cells while the subject is tested in the seated position and head held in the neutral position. Reports based on a variety of devices and protocols indicate acceptable reproducibility of ICS scores (Ylinen et al., 1999; Chiu and Lo, 2002; Strimpakos et al., 2004). However a significant diversity in ICS scores has been indicated. In men strength in flexion and extension ranged 4–23 and 4–30 kgf, respectively. In women the corresponding ranges were 2–10 and 7–20 kgf (Ylinen et al., 1999; Jordan et al., 1999; Chiu and Lo, 2002; Kumar et al., 2001; Strimpakos et al., 2004; Suryanarayana and Kumar, 2005). Isometric cervical strength in lateral flexion has not been equally explored and the existing data relate to a range of 8–23 and 5–12 kgf in men and women,
T. Prushansky et al. / Clinical Biomechanics 20 (2005) 794–798
respectively (Kumar et al., 2001). Another parameter derived from sagittal ICS measurement is the flexion/ extension (F/E) strength ratio. This pooled (genders) ratio ranged typically 0.5–0.8 (Vernon et al., 1992, 1996; Jordan et al., 1999; Garce´s et al., 2002). Only a few studies of ICS in cervical pathologies have been reported. Of particular relevance is the study by Ylinen et al. (2004) which indicated that the ICS in a group of women suffering from chronic neck pain was uniformly (flexion and extension) decreased by about 30% in comparison to controls. A previous study (Ylinen and Ruuska, 1994) reported also that the F/E ratio in a similar group of women remained stable after rehabilitation ranging approximately 0.5–0.6. Among sufferers of chronic neck disorders, patients with chronic whiplash associated disorders (WAD) occupy a significant niche (Spitzer et al., 1995). Almost all WAD patients complain of varying degrees of pain while in some changes in the pattern of cervical muscle activation has been observed (Nederhand et al., 2003; Jull et al., 2004). Collectively these symptoms may result in a significant reduction in ICS. However data regarding ICS in groups of chronic or acute WAD patients is scarce, nonspecific or largely not amenable to comparative analysis due to the units in which the ICS was expressed in (Silverman et al., 1991; Vernon et al., 1992, 1996). Indeed the only study that may serve for comparison with the present findings indicated that in these patients the F/E ratio was characterized by an extremely low score: 0.24 compared to 0.52 in controls (Vernon et al., 1996). Therefore the objective of the present study was to measure and characterize ICS in WAD patients and to compare the findings with those derived from reported studies of healthy subjects.
2. Methods 2.1. Patients Ninety seven consecutive chronic WAD patients, 46 men and 51 women participated in this study. Their age range was 21–55 with a mean (SD) of 40.3 (10.2) years. Post injury duration ranged 6–132 months with a mean (SD) of 22.8 (22.5). However 71% were within 24 months after the accident while only 10% experienced symptoms for more than 4 years. All patients were victims of road accident and were initially treated conservatively. However due to persistent pain they were referred for further medical help at the Spinal Care Unit of the Sapir Medical Center. About 50% of the study group eventually underwent cervical radiofrequency neurotomy (CRN). The measurements in this study were performed prior to the procedure. Inclusion criteria consisted of Quebec Task Force (Spitzer et al., 1995) classification WAD II–III
795
(where grade III referred exclusively to hand paresthesias which were reported by 53/97 patients), a minimum duration of 6 months post injury, age range 18–55 years, no other spinal disorders, peripheral or central neurological conditions, inner ear pathology or dizziness prior to the whiplash injury and no direct head trauma or loss of consciousness at the time of the accident. Foe assessing the functional severity patients filled the Neck Disability Index (NDI, Vernon and Mior, 1991). The mean score was 24.5 indicating moderate to severe disability. All patients signed an informed consent approved by the Institutional Review Boards of Tel Aviv University and the Sapir Medical Center. 2.2. Instrumentation Isometric strength of the cervical muscles in the sagittal and frontal planes was measured using a locally designed and fabricated dynamometer which linear range over 0–30 kgf with an accuracy of ±0.5%. The set-up consisted of the load cell assembly and the swivel chair. The strain gauge-based load cell was located at the tip of a telescopic arm which could be moved up and down or sideways using linear slides. Analogue to digital conversion of the signal enabled display of the peak strength in kgf. In order to standardize the test a swivel chair allowing 360 rotation was fixed to the floor. A single bolt enabled locking the chair in one of the four positions corresponding to testing in flexion, extension and right and left lateral flexion. 2.3. Procedure Prior to the testing procedure each subject was given detailed explanation and was instructed to push and exert maximal force without elevating his baseline cervical pain. Testing started with the subject seated at on the chair with hands on his laps and feet supported on the floor. Trunk stabilization was provided by shoulder, thoracic and pelvis straps. A head band was used to cushion the skull at the interface area with the load cell. The position of the load cell was then adjusted to be orthogonally directed against the forehead (in flexion), occipital (in extension) and parietal (lateral flexion) regions. Following warm up of neck muscles, subject was tested in the following order: flexion (F), extension (E), right lateral flexion (RLF), and left lateral flexion (LLF). Three consecutive maximal isometric cervical force measurements were performed in each of the four direction with 30 s interval between individual exertions. All measurements were performed by the first author. 2.4. Statistical analysis Analysis was performed using the SPSS statistical software (version 9). Descriptive statistics of the four
T. Prushansky et al. / Clinical Biomechanics 20 (2005) 794–798
separated ICS directions included means, standard deviations (SD) and coefficient of variation (CV) [derived from the three consecutive measurements in each of the separated directions, CV = (SD/mean) · 100]. In addition a total strength score (TSS) was calculated from the sum of all four separated directions whereas a mean CV score (MCV) was calculated from their four corresponding CV scores. Mean and SD were calculated for the F/E ratios. Inferential statistics using mixed effect models ANOVA was performed for testing the within subject effect of the four directions on ICS and their associated CV values, accounting for gender and age (divided into four decades). Between-subject effects of gender and age on TSS and MCV values were also analyzed. PearsonÕs r was calculated for assessing association between TSS, MCV and the F/E ratio.
3. Results Table 1 presents the descriptive statistics mean and SD of the ICS in the four directions and their associated CVs as well as the TSS and MCV. Values are presented for each gender separately. The direction-based ICS values and their corresponding CVs differed significantly: F3,267 = 27.48, P < 0.0005 and F3,267 = 5.24, P < 0.002, respectively. The significant difference in individual ICS was attributed to extension strength which exceeded all other directions whereas the difference in the associated CV was due to the increase in flexion-related scores. Fig. 1 depicts the individual ICSs in both genders. Gender had a significant effect on ICS scores (F1,89 = 6.2, P < 0.015) but not on the CVs while age had no effect on either. The use of total strength score (TSS) and the mean CV (MCV) provides a more compact score while facilitating the analysis. The TSS was
15
Isometric Cervical Strength (kgf)
796
Flexion
2.1 (2.5) (kgf) 19.6c (14.0) (%)
1.0 (0.7) 26.3 (17.4)
52%
Extension
2.5 (2.6) 17.1 (11.8)
1.5 (1.1) 18.1 (14.3)
40%
RLB
1.7 (2.0) 16.0 (10.2)
0.9 (0.7) 18.1 (14.8)
47%
LLB
1.6 (2.0) 16.6 (9.9)
0.9 (0.6) 16.9 (10.5)
44%
TSS (kgf) MCV (%)
7.9 (9.1) 17.3 (8.2)
4.3 (3.0) 19.8 (8.2)
46% –
a b c
ICS scores (kgf). {1.0 (women ICS/men ICS)} · 100. Corresponding CVs (%).
E
LLF 46
46 46 men
46
51
51 51 women
51
Fig. 1. Boxplots depicting the medians (50th percentile) and the 10, 25, 75 and 90th percentiles of the individual ICSs in men and women. Outliers (circles) and extremes (asterisk) are marked above the 90th percentile. F—flexion, E—extension, RLF—right lateral flexion, LLF—left lateral flexion.
significantly affected by gender (F1,89 = 6.2, P < 0.015). The average TSS in women was 4.13 kgf less then men. Age had no affect on the TSS scores. MCV scores were not affected by age or gender. The mean F/E ratio was calculated for the whole group of patients and for men and woman separately, yielding 0.86 (0.4), 0.9 (0.4) and 0.82 (0.4) respectively. The correlation between the F/E ratio and MCV was 0.43 (Fig. 2). When correlating only those patients with F/E ratio above 1.0 (n = 25) r increased to 0.64 while the respective r for F/E > 1.38 (Vlaeyen and Linton, 2000) was 0.91 (n = 9). Noteworthy, F/E ratio did not correlate significantly with either TSS, flexion or extension scores. 60
50
Women/men% difference b
F 0
-5 N=
40 MCV%
a
Women (n = 51)
5
RLF
Table 1 Mean (SD) of ICS values (kgf) and their associated CVs (%) in the four tested directions including the total strength score (TSS) and the mean CV score (MCV) Men (n = 46)
10
30
20
10
0 0.0
.5
1.0
1.38 1.5
2.0
2.5
3.0
F/E ratio
Fig. 2. F/E ratio in relation to MCV (n = 97). Solid line is the best fit for the whole sample whereas the dashed line refers to patients for whom F/E > 1.38.
T. Prushansky et al. / Clinical Biomechanics 20 (2005) 794–798
4. Discussion The main finding of this study reveals that chronic WAD patients are characterized by very low ICS scores in comparison with the normal ICS range as reported in the majority of studies (Ylinen et al., 1999; Jordan et al., 1999; Chiu and Lo, 2002; Garce´s et al., 2002; Gabriel et al., 2004; Strimpakos et al., 2004). Of note using the same dynamometer for measuring ICS in healthy women and men, yet unpublished results which are in excellent agreement with a recent study (Gabriel et al., 2004) indicate that cervical strength in the current group of patients is reduced about 80% and 90% in women and men, respectively. Despite this dramatic difference the inter-gender and inter-directions ICS relationships remained similar to those indicated for healthy subjects (Chiu and Lo, 2002; Jordan et al., 1999). Furthermore, the present study indicates that extension strength was the highest among the four individual ICSs with the other directions being generally on a par with each other. This finding is supported by recent research relating to healthy subjects (Gabriel et al., 2004; Garce´s et al., 2002). Age, as reported for healthy subjects had no significant effect on ICS scores (Chiu et al., 2002). It should be borne in mind that the patients comprising the present sample have been suffering from pain or moderate to severe disability for at least 6 months. Moreover, as they were not responding to or satisfied with the conservative treatment they were offered surgical intervention (CRN). About 50% of the patients underwent eventually the intervention knowing that it was neither a perfect solution nor without some risk. This, in our opinion, serves as a strong indicator for the severity of their symptoms. The extent of patient collaboration in performing the test may be assessed using the patientÕs consistency of the measured scores. Consistency, as indicated by the CV, ranges for many biological parameters up to 10% and may increase with (a) the complexity of the test, (b) submaximal effort and (c) the existence of pathology (Simonsen, 1995). In the present context previous research regarding performance of cervical range of motion (Prushansky et al., in press) has indeed indicated that relative to normal subjects the mean CV (based on all individual CVs) in WAD patients increased from 3.2% to 10.4%. Regarding ICS recent findings emerging from our yet unpublished study indicate that in healthy women and men the mean CV were 13.5% and 9.7%, respectively. Therefore, the increase in CV to 17% in our patient group is very reasonable given the pathology and the tested parameter. Noteworthy, the CV was not affected by gender or age but was significantly higher in flexion, a finding which is reminiscent of the lesser consistency in performing flexion movement in normal subjects and chronic WAD patients. We suggest that
797
these observations point out to patientsÕ collaboration in performing the test. The finding relating to F/E ratio is of special interest since it is largely not outside the range reported for normal subjects. Of special significance is the observation that F/E in healthy subjects increased from 0.6 to 0.77 when subjects were asked to perform an insincere effort (Vernon et al., 1992, 1996). It was also reported by Vernon et al that WAD patients had a sharp decrease in F/ E ratio (0.24). This decrease was attributed to a relatively more severe flexion weakness compared with extension in these patients. Furthermore, it was suggested that in those WAD patients manifesting high non-organic signs a concomitant increase in the ratio to 1.07 was indicative of submaximal (insincere) ICS effort (Vernon et al., 1996). However, neither the sensitivity nor the specificity of these benchmarks were reported and without such, the analysis lacks relevance. In the current study increases in F/E scores were positively correlated with MCV but not with other measures such as NDI or cervical range of motion (not reported in this study). In particular, considering that the ratio did not correlate with the TSS, the close correlation between the F/E scores and their associated MCV in patients with very high F/E scores would in fact point to another explanation rather than insincerity. Why would flexion become stronger than extension? As amply demonstrated by previous research the neck extensors are stronger than the flexors by some 25– 100%. On the other hand, since the mechanism of whiplash injury is associated particularly with posterior structures of the cervical spine, activity in the extensors compared to flexorsÕ is more likely to provoke pain in these structures. Therefore in order to avoid exacerbation of pain we speculate that WAD patients limit the resulting applied extensor force. Thus in chronic WAD patients the severe strength insufficiency is probably related to fear of pain. This observation is well supported by research concerning pain avoidance in musculoskeletal compromise (Vlaeyen and Linton, 2000; Nederhand et al., 2004). Assuming that fear avoidance is a significant interfering factor the clinical implication of this observation is that specific behavioral treatment approach should be applied in addition to the physical rehabilitation. This indeed is in line with modern thinking but its validation requires further research. The second question relates to the clinical meaning of the MCV and particularly the potential significance of the very high correlation between extreme F/E and MCV scores. We propose that high MCV further indicates avoidance of excessive muscular exertions. When not reaching the maximal muscular potential, patients lack a neuromotor as well as a perceptual anchor and hence the degree of reproducibility of the same strength scores is compromised. Interestingly, this phenomenon
798
T. Prushansky et al. / Clinical Biomechanics 20 (2005) 794–798
has also been revealed in a recent study where severe limitations in cervical motion were shown to be associated with high MCV of the corresponding motions (Prushansky et al., in press). In view of the current findings it is suggested that future research pertaining to WAD patients should focus on: (a) reproducibility of the ICS scores, (b) correlating scales indicating fear/pain avoidance behavior with cervical muscles strength, (c) establishing effort factor parameters and (d) monitoring variations in ICS during different modes of rehabilitation.
Acknowledgement The authors extend their sincere appreciation to the Research Fund affiliated to the Consortium of Israeli Insurance Companies for supporting this research.
References Chiu, T.T.W., Lam, T.H., Hedley, A.J., 2002. Maximal isometric muscle strength of the cervical spine in healthy volunteers. Clin. Rehabil. 16, 772–779. Chiu, T.T.W., Lo, S.K., 2002. Evaluation of cervical range of motion and isometric neck muscle strength: reliability and validity. Clin. Rehabil. 16, 851–858. Gabriel, D.A., Matsumoto, J.Y., Davis, D.H., Currier, B.L., Kai-Nan, A., 2004. Multidirectional neck strength and electromyographic activity for normal controls. Clin. Biomech. 19, 653–658. Garce´s, G.L., Medina, D., Milutinovic, P., Garavote, P., Guerado, E., 2002. Normative database of isometric cervical strength in a healthy population. Med. Sci. Sports Exer. 33, 464–470. Jordan, A., Mehlsen, J., Bulow, P.M., Ostergaard, K., DanneskioldSamsoe, B., 1999. Maximal isometric strength of the cervical musculature in 100 healthy volunteers. Spine 24, 1343–1348. Jull, G., Kristajansson, E., DallÕAlba, P., 2004. Impairment in the cervical flexors: a comparison of whiplash and insidious neck pain patients. Manual Ther. 9, 89–94. Kumar, S., Narayan, Y., Amell, T., 2001. Cervical strength of young adults in sagittal, coronal and intermediate planes. Clin. Biomech. 16, 380–388.
Nederhand, M.J., Hermens, H.J., Jzerman, M.J., Turk, D.C., Zilvold, G., 2003. Chronic neck pain disability due to an acute whiplash injury. Pain 102, 63–71. Nederhand, M.J., Jzerman, M.J., Hermens, H.J., Turk, D.C., Zilvold, G., 2004. Predictive value of fear avoidance in developing chronic neck pain disability: consequences for clinical decision making. Arch. Phys. Med. Rehabil. 85, 496–501. Prushansky, T., Pevzner, E., Gordon, C.R., Dvir, Z., in press. Performance of cervical motion in chronic whiplash patients and healthy subjects: the case of atypical patients. Spine. Silverman, J.L., Rodriquez, A.A., Agre, J.C., 1991. Quantitative cervical flexor strength in healthy subjects and in subjects with mechanical neck pain. Arch. Phys. Med. Rehabil. 72, 679–681. Simonsen, J.C., 1995. Coefficient of variation as a measure of subject effort. Arch. Phys. Med. Rehabil. 76, 516–520. Spitzer, W.O., Skovron, M.L., Salmi, L.R., 1995. Scientific monograph of the Quebec Task Force on whiplash-associated disorders: redefining ‘‘whiplash’’ and its management. Spine 20 (suppl), s1– s73. Strimpakos, N., Sakellari, V., Gipftos, G., Oldham, J., 2004. Intratester and intertester reliability of neck isometric dynamometry. Arch. Phys. Med. Rehabil., 1309–1316. Suryanarayana, L., Kumar, S., 2005. Quantification of isometric cervical strength at different ranges of flexion and extension. Clin. Biomech. 20, 138–144. Vernon, H.T., Aker, P., Aramenco, M., Battershil, D., Alpin, A., Penner, T., 1992. Evaluation of neck muscle strength with a modified sphygmomanometer: reliability and validity. J. Manip. Physiol. Ther. 15, 343–349. Vernon, H.T., McKenzie, T., Djetvai, K., Coutts, A., 1996. Muscle strength testing of the neck with a manual modified sphygmomanometer. Eur. J. Chirop. 44, 41–49. Vernon, H., Mior, S., 1991. Neck disability index: a study of reliability and validity. J. Manip. Physiol. Ther. 7, 409–415. Vlaeyen, J.W.S., Linton, S.J., 2000. Fear-avoidance and its consequences in chronic musculoskeletal pain: a state of the art. Pain 85, 317–332. Ylinen, J.J., Rezasoltani, A., Julin, M.V., Virtapohja, H.A., Malkia, E.A., 1999. Reproducibility of isometric strength: measurements of neck muscles. Clin. Biomech. 14, 217–219. Ylinen, J., Ruuska, J., 1994. Clinical use of neck isometric strength measurements in rehabilitation. Arch. Phys. Med. Rehabil. 75, 465–469. Ylinen, J., Salo, P., Nykanen, M., Kautiainen, H., Hakkinen, C., 2004. A decreased isometric neck strength in women with chronic neck pain and the reproducibility of neck strength measurements. Arch. Phys. Med. Rehabil. 85, 1303–1308.
Cervical muscles weakness in chronic whiplash patients Tamara Prushansky
a,*
, Reuven Gepstein b, Carlos Gordon c, Zeevi Dvir
a
a
Department of Physical Therapy, Sackler Faculty of Medicine, Tel Aviv University, 69978 Tel Aviv, Israel Spine Surgery Unit, Department of Orthopedics, Sapir Medical Center, Kfar Saba, Tel Aviv University, Israel Department of Neurology, Sapir Medical Center, Kfar Saba, Sackler Faculty of Medicine, Tel Aviv University, Israel b
c
Received 30 January 2005; accepted 6 May 2005
Abstract Background. Isometric cervical strength has been used for assessing the severity of cervical spine pathologies. However there is a conspicuous dearth of information relating to cervical strength data in patients suffering from chronic whiplash. Therefore the objective of this study was to compare absolute and ratio-based isometric cervical strength scores in chronic whiplash patients with reported corresponding scores in healthy subjects. Methods. Isometric cervical strength was measured in the directions of flexion, extension, right and left lateral flexion in 97 patients, 51 women and 46 men, using a wall-mounted dynamometer. Findings. Compared to published values of normal subjects, whiplash patients suffered sharp reductions of about 90% in both genders and in all directions. The consistency of the isometric cervical strength scores as indicated by the mean coefficient of variation was relatively low, 17% and 20% in men and women respectively. The flexion/extension strength ratio ranged 0.8–0.9, slightly higher than the reported range for normal subjects. This ratio was highly correlated (r = 0.91, P = 0.01) with the mean coefficient of variation in a subgroup of 9 patients. Interpretation. In the absence of an obvious reason such as sever atrophy or grossly dysfunctional neurological control the indicated weakness of the cervical muscles may be associated with learned pain avoidance behavior which is typical among this group of patients. 2005 Published by Elsevier Ltd. Keywords: Whiplash; Isometric strength; Cervical spine
1. Introduction The main function of the neck muscles is to maintain postural balance via the exertion of isometric tension (Ylinen et al., 1999). There is ample evidence that cervical strength is compromised in various cervical disorders and therefore the assessment of isometric cervical strength (ICS) may be an important indicator for cervical impairment (Silverman et al., 1991; Jull et al., 2004). Various instruments for measurement of ICS have been described. Most are based on the use of fixed load *
Corresponding author. E-mail address: [email protected] (T. Prushansky).
0268-0033/$ - see front matter 2005 Published by Elsevier Ltd. doi:10.1016/j.clinbiomech.2005.05.003
cells while the subject is tested in the seated position and head held in the neutral position. Reports based on a variety of devices and protocols indicate acceptable reproducibility of ICS scores (Ylinen et al., 1999; Chiu and Lo, 2002; Strimpakos et al., 2004). However a significant diversity in ICS scores has been indicated. In men strength in flexion and extension ranged 4–23 and 4–30 kgf, respectively. In women the corresponding ranges were 2–10 and 7–20 kgf (Ylinen et al., 1999; Jordan et al., 1999; Chiu and Lo, 2002; Kumar et al., 2001; Strimpakos et al., 2004; Suryanarayana and Kumar, 2005). Isometric cervical strength in lateral flexion has not been equally explored and the existing data relate to a range of 8–23 and 5–12 kgf in men and women,
T. Prushansky et al. / Clinical Biomechanics 20 (2005) 794–798
respectively (Kumar et al., 2001). Another parameter derived from sagittal ICS measurement is the flexion/ extension (F/E) strength ratio. This pooled (genders) ratio ranged typically 0.5–0.8 (Vernon et al., 1992, 1996; Jordan et al., 1999; Garce´s et al., 2002). Only a few studies of ICS in cervical pathologies have been reported. Of particular relevance is the study by Ylinen et al. (2004) which indicated that the ICS in a group of women suffering from chronic neck pain was uniformly (flexion and extension) decreased by about 30% in comparison to controls. A previous study (Ylinen and Ruuska, 1994) reported also that the F/E ratio in a similar group of women remained stable after rehabilitation ranging approximately 0.5–0.6. Among sufferers of chronic neck disorders, patients with chronic whiplash associated disorders (WAD) occupy a significant niche (Spitzer et al., 1995). Almost all WAD patients complain of varying degrees of pain while in some changes in the pattern of cervical muscle activation has been observed (Nederhand et al., 2003; Jull et al., 2004). Collectively these symptoms may result in a significant reduction in ICS. However data regarding ICS in groups of chronic or acute WAD patients is scarce, nonspecific or largely not amenable to comparative analysis due to the units in which the ICS was expressed in (Silverman et al., 1991; Vernon et al., 1992, 1996). Indeed the only study that may serve for comparison with the present findings indicated that in these patients the F/E ratio was characterized by an extremely low score: 0.24 compared to 0.52 in controls (Vernon et al., 1996). Therefore the objective of the present study was to measure and characterize ICS in WAD patients and to compare the findings with those derived from reported studies of healthy subjects.
2. Methods 2.1. Patients Ninety seven consecutive chronic WAD patients, 46 men and 51 women participated in this study. Their age range was 21–55 with a mean (SD) of 40.3 (10.2) years. Post injury duration ranged 6–132 months with a mean (SD) of 22.8 (22.5). However 71% were within 24 months after the accident while only 10% experienced symptoms for more than 4 years. All patients were victims of road accident and were initially treated conservatively. However due to persistent pain they were referred for further medical help at the Spinal Care Unit of the Sapir Medical Center. About 50% of the study group eventually underwent cervical radiofrequency neurotomy (CRN). The measurements in this study were performed prior to the procedure. Inclusion criteria consisted of Quebec Task Force (Spitzer et al., 1995) classification WAD II–III
795
(where grade III referred exclusively to hand paresthesias which were reported by 53/97 patients), a minimum duration of 6 months post injury, age range 18–55 years, no other spinal disorders, peripheral or central neurological conditions, inner ear pathology or dizziness prior to the whiplash injury and no direct head trauma or loss of consciousness at the time of the accident. Foe assessing the functional severity patients filled the Neck Disability Index (NDI, Vernon and Mior, 1991). The mean score was 24.5 indicating moderate to severe disability. All patients signed an informed consent approved by the Institutional Review Boards of Tel Aviv University and the Sapir Medical Center. 2.2. Instrumentation Isometric strength of the cervical muscles in the sagittal and frontal planes was measured using a locally designed and fabricated dynamometer which linear range over 0–30 kgf with an accuracy of ±0.5%. The set-up consisted of the load cell assembly and the swivel chair. The strain gauge-based load cell was located at the tip of a telescopic arm which could be moved up and down or sideways using linear slides. Analogue to digital conversion of the signal enabled display of the peak strength in kgf. In order to standardize the test a swivel chair allowing 360 rotation was fixed to the floor. A single bolt enabled locking the chair in one of the four positions corresponding to testing in flexion, extension and right and left lateral flexion. 2.3. Procedure Prior to the testing procedure each subject was given detailed explanation and was instructed to push and exert maximal force without elevating his baseline cervical pain. Testing started with the subject seated at on the chair with hands on his laps and feet supported on the floor. Trunk stabilization was provided by shoulder, thoracic and pelvis straps. A head band was used to cushion the skull at the interface area with the load cell. The position of the load cell was then adjusted to be orthogonally directed against the forehead (in flexion), occipital (in extension) and parietal (lateral flexion) regions. Following warm up of neck muscles, subject was tested in the following order: flexion (F), extension (E), right lateral flexion (RLF), and left lateral flexion (LLF). Three consecutive maximal isometric cervical force measurements were performed in each of the four direction with 30 s interval between individual exertions. All measurements were performed by the first author. 2.4. Statistical analysis Analysis was performed using the SPSS statistical software (version 9). Descriptive statistics of the four
T. Prushansky et al. / Clinical Biomechanics 20 (2005) 794–798
separated ICS directions included means, standard deviations (SD) and coefficient of variation (CV) [derived from the three consecutive measurements in each of the separated directions, CV = (SD/mean) · 100]. In addition a total strength score (TSS) was calculated from the sum of all four separated directions whereas a mean CV score (MCV) was calculated from their four corresponding CV scores. Mean and SD were calculated for the F/E ratios. Inferential statistics using mixed effect models ANOVA was performed for testing the within subject effect of the four directions on ICS and their associated CV values, accounting for gender and age (divided into four decades). Between-subject effects of gender and age on TSS and MCV values were also analyzed. PearsonÕs r was calculated for assessing association between TSS, MCV and the F/E ratio.
3. Results Table 1 presents the descriptive statistics mean and SD of the ICS in the four directions and their associated CVs as well as the TSS and MCV. Values are presented for each gender separately. The direction-based ICS values and their corresponding CVs differed significantly: F3,267 = 27.48, P < 0.0005 and F3,267 = 5.24, P < 0.002, respectively. The significant difference in individual ICS was attributed to extension strength which exceeded all other directions whereas the difference in the associated CV was due to the increase in flexion-related scores. Fig. 1 depicts the individual ICSs in both genders. Gender had a significant effect on ICS scores (F1,89 = 6.2, P < 0.015) but not on the CVs while age had no effect on either. The use of total strength score (TSS) and the mean CV (MCV) provides a more compact score while facilitating the analysis. The TSS was
15
Isometric Cervical Strength (kgf)
796
Flexion
2.1 (2.5) (kgf) 19.6c (14.0) (%)
1.0 (0.7) 26.3 (17.4)
52%
Extension
2.5 (2.6) 17.1 (11.8)
1.5 (1.1) 18.1 (14.3)
40%
RLB
1.7 (2.0) 16.0 (10.2)
0.9 (0.7) 18.1 (14.8)
47%
LLB
1.6 (2.0) 16.6 (9.9)
0.9 (0.6) 16.9 (10.5)
44%
TSS (kgf) MCV (%)
7.9 (9.1) 17.3 (8.2)
4.3 (3.0) 19.8 (8.2)
46% –
a b c
ICS scores (kgf). {1.0 (women ICS/men ICS)} · 100. Corresponding CVs (%).
E
LLF 46
46 46 men
46
51
51 51 women
51
Fig. 1. Boxplots depicting the medians (50th percentile) and the 10, 25, 75 and 90th percentiles of the individual ICSs in men and women. Outliers (circles) and extremes (asterisk) are marked above the 90th percentile. F—flexion, E—extension, RLF—right lateral flexion, LLF—left lateral flexion.
significantly affected by gender (F1,89 = 6.2, P < 0.015). The average TSS in women was 4.13 kgf less then men. Age had no affect on the TSS scores. MCV scores were not affected by age or gender. The mean F/E ratio was calculated for the whole group of patients and for men and woman separately, yielding 0.86 (0.4), 0.9 (0.4) and 0.82 (0.4) respectively. The correlation between the F/E ratio and MCV was 0.43 (Fig. 2). When correlating only those patients with F/E ratio above 1.0 (n = 25) r increased to 0.64 while the respective r for F/E > 1.38 (Vlaeyen and Linton, 2000) was 0.91 (n = 9). Noteworthy, F/E ratio did not correlate significantly with either TSS, flexion or extension scores. 60
50
Women/men% difference b
F 0
-5 N=
40 MCV%
a
Women (n = 51)
5
RLF
Table 1 Mean (SD) of ICS values (kgf) and their associated CVs (%) in the four tested directions including the total strength score (TSS) and the mean CV score (MCV) Men (n = 46)
10
30
20
10
0 0.0
.5
1.0
1.38 1.5
2.0
2.5
3.0
F/E ratio
Fig. 2. F/E ratio in relation to MCV (n = 97). Solid line is the best fit for the whole sample whereas the dashed line refers to patients for whom F/E > 1.38.
T. Prushansky et al. / Clinical Biomechanics 20 (2005) 794–798
4. Discussion The main finding of this study reveals that chronic WAD patients are characterized by very low ICS scores in comparison with the normal ICS range as reported in the majority of studies (Ylinen et al., 1999; Jordan et al., 1999; Chiu and Lo, 2002; Garce´s et al., 2002; Gabriel et al., 2004; Strimpakos et al., 2004). Of note using the same dynamometer for measuring ICS in healthy women and men, yet unpublished results which are in excellent agreement with a recent study (Gabriel et al., 2004) indicate that cervical strength in the current group of patients is reduced about 80% and 90% in women and men, respectively. Despite this dramatic difference the inter-gender and inter-directions ICS relationships remained similar to those indicated for healthy subjects (Chiu and Lo, 2002; Jordan et al., 1999). Furthermore, the present study indicates that extension strength was the highest among the four individual ICSs with the other directions being generally on a par with each other. This finding is supported by recent research relating to healthy subjects (Gabriel et al., 2004; Garce´s et al., 2002). Age, as reported for healthy subjects had no significant effect on ICS scores (Chiu et al., 2002). It should be borne in mind that the patients comprising the present sample have been suffering from pain or moderate to severe disability for at least 6 months. Moreover, as they were not responding to or satisfied with the conservative treatment they were offered surgical intervention (CRN). About 50% of the patients underwent eventually the intervention knowing that it was neither a perfect solution nor without some risk. This, in our opinion, serves as a strong indicator for the severity of their symptoms. The extent of patient collaboration in performing the test may be assessed using the patientÕs consistency of the measured scores. Consistency, as indicated by the CV, ranges for many biological parameters up to 10% and may increase with (a) the complexity of the test, (b) submaximal effort and (c) the existence of pathology (Simonsen, 1995). In the present context previous research regarding performance of cervical range of motion (Prushansky et al., in press) has indeed indicated that relative to normal subjects the mean CV (based on all individual CVs) in WAD patients increased from 3.2% to 10.4%. Regarding ICS recent findings emerging from our yet unpublished study indicate that in healthy women and men the mean CV were 13.5% and 9.7%, respectively. Therefore, the increase in CV to 17% in our patient group is very reasonable given the pathology and the tested parameter. Noteworthy, the CV was not affected by gender or age but was significantly higher in flexion, a finding which is reminiscent of the lesser consistency in performing flexion movement in normal subjects and chronic WAD patients. We suggest that
797
these observations point out to patientsÕ collaboration in performing the test. The finding relating to F/E ratio is of special interest since it is largely not outside the range reported for normal subjects. Of special significance is the observation that F/E in healthy subjects increased from 0.6 to 0.77 when subjects were asked to perform an insincere effort (Vernon et al., 1992, 1996). It was also reported by Vernon et al that WAD patients had a sharp decrease in F/ E ratio (0.24). This decrease was attributed to a relatively more severe flexion weakness compared with extension in these patients. Furthermore, it was suggested that in those WAD patients manifesting high non-organic signs a concomitant increase in the ratio to 1.07 was indicative of submaximal (insincere) ICS effort (Vernon et al., 1996). However, neither the sensitivity nor the specificity of these benchmarks were reported and without such, the analysis lacks relevance. In the current study increases in F/E scores were positively correlated with MCV but not with other measures such as NDI or cervical range of motion (not reported in this study). In particular, considering that the ratio did not correlate with the TSS, the close correlation between the F/E scores and their associated MCV in patients with very high F/E scores would in fact point to another explanation rather than insincerity. Why would flexion become stronger than extension? As amply demonstrated by previous research the neck extensors are stronger than the flexors by some 25– 100%. On the other hand, since the mechanism of whiplash injury is associated particularly with posterior structures of the cervical spine, activity in the extensors compared to flexorsÕ is more likely to provoke pain in these structures. Therefore in order to avoid exacerbation of pain we speculate that WAD patients limit the resulting applied extensor force. Thus in chronic WAD patients the severe strength insufficiency is probably related to fear of pain. This observation is well supported by research concerning pain avoidance in musculoskeletal compromise (Vlaeyen and Linton, 2000; Nederhand et al., 2004). Assuming that fear avoidance is a significant interfering factor the clinical implication of this observation is that specific behavioral treatment approach should be applied in addition to the physical rehabilitation. This indeed is in line with modern thinking but its validation requires further research. The second question relates to the clinical meaning of the MCV and particularly the potential significance of the very high correlation between extreme F/E and MCV scores. We propose that high MCV further indicates avoidance of excessive muscular exertions. When not reaching the maximal muscular potential, patients lack a neuromotor as well as a perceptual anchor and hence the degree of reproducibility of the same strength scores is compromised. Interestingly, this phenomenon
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T. Prushansky et al. / Clinical Biomechanics 20 (2005) 794–798
has also been revealed in a recent study where severe limitations in cervical motion were shown to be associated with high MCV of the corresponding motions (Prushansky et al., in press). In view of the current findings it is suggested that future research pertaining to WAD patients should focus on: (a) reproducibility of the ICS scores, (b) correlating scales indicating fear/pain avoidance behavior with cervical muscles strength, (c) establishing effort factor parameters and (d) monitoring variations in ICS during different modes of rehabilitation.
Acknowledgement The authors extend their sincere appreciation to the Research Fund affiliated to the Consortium of Israeli Insurance Companies for supporting this research.
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