Effect of neck pain on verticality perception: A cohort study

Effect of neck pain on verticality perception: A cohort study

412 Effect of Neck Pain on Verticality Perception: A Cohort Study Jaroslaw P. Grod, DC, FCCS(C), Peter R. Diakow, DC, FCCS(C) ABSTRACT. Grod JP, Diak...

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Effect of Neck Pain on Verticality Perception: A Cohort Study Jaroslaw P. Grod, DC, FCCS(C), Peter R. Diakow, DC, FCCS(C) ABSTRACT. Grod JP, Diakow PR. Effect of neck pain on verticality perception: a cohort study. Arch Phys Med Rehabil 2002;83:412-5. Objective: To use the Rod-and-Frame Test (RFT) as a quantification of the perception of verticality in subjects with and without neck pain. Design: Cohort study comparing perception of verticality in symptomatic subjects with neck pain versus a control group. Setting: Both groups were selected from 2 urban chiropractic offices treating typical neuromusculoskeletal conditions from the general community in Canada. Patients: Nineteen subjects (11 women, 8 men) with uncomplicated mechanical neck pain and 17 (7 women, 10 men) asymptomatic subjects. Intervention: The RFT offers a noninvasive method of measuring spatial orientation or the perception of verticality. Studies of the RFT indicate that performance is reliable. The RFT requires subjects to set a luminescent rod to the true vertical in the presence and absence of a luminescent background frame. Main Outcome Measure: The amount of rotation was measured and recorded by a dial on the back of the device. Results: Two-way analysis of variance showed statistically significant differences in judging vertical between symptomatic and asymptomatic subjects. Unpaired t tests for each test situation and the Tukey post hoc test showed statistical differences for both groups. Conclusion: There may be a direct connection between the structures that provide internal cues for the body’s ability to sense verticality and nociceptive influences affecting the afference of these structures. The overshoot of the symptomatic group could indicate the search for additional proprioceptive information. Key Words: Dizziness; Neck pain; Proprioception; Rehabilitation. © 2002 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation ECK PAIN IS a significant problem in industrialized countries. Estimates place the prevalence of neck pain in N the general population at about 35%. Chronic neck pain occurs 1

in approximately 14% of the population.1,2 Although most studies of chronic neck pain have specifically dealt with victims of whiplash type–traumatic injury, there is substantial evidence that the prevalence differs little from the general population.3,4 The costs for treatment, rehabilitation, and lost productivity from neck pain, including that related to traumatic

From the Canadian Memorial Chiropractic College, Toronto, Ont, Canada. Accepted in revised form April 16, 2001. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors(s) or upon any organization with which the author(s) is/are associated. Reprint requests to Jaroslaw P. Grod, DC, FCCS(C), Director, Continuing Education, Canadian Memorial Chiropractic College, 1900 Bayview Ave, Toronto, Ont M4G 3E6, Canada, e-mail: [email protected]. 0003-9993/02/8303-6593$35.00/0 doi:10.1053/apmr.2002.29660

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accidents, are substantial, with some estimates in excess of $2 billion yearly in the United States.5 Neck pain may also be accompanied by other symptoms related to the same pathology.6 Light-headedness, dizziness, and blurred vision affect a substantial proportion of whiplash victims.7 Dizziness is a nonspecific term that describes a sensation of altered orientation of the body in space. Vertigo, by contrast, is an illusion of movement, usually of rotation. Both sensations are symptoms of an altered spatial orientation. Spatial orientation is a key process necessary for several normal functions such as coordinating movement and maintaining posture. Achieving and maintaining vertical posture, in particular, requires normal operation of righting reflexes, which consist of labyrinthine righting reflexes, body on head reflexes, neck righting reflexes, body on body righting reflexes, and visual righting reflexes.8 Visual, vestibular, and, especially, proprioceptive signals provide the main source of information for the normal functioning of these varied reflexes. Damage to muscles, joints, or tendons in the neck that cause neck pain may affect proprioceptors in the tissues that give rise to the neckrighting reflexes.9 McPartland et al10 have shown an association among chronic neck pain, suboccipital muscle atrophy, and standing balance as measured by force platform. This article reports on the symptoms resulting from such damage. Righting reflexes involve very complex processes and many sensory structures.11 Previous histologic examination of deep neck muscles in cats, rats, and humans have shown the rich content of muscle spindles in these structures. Unfortunately, the function of muscle spindles has been studied largely only as single units with little attention to their collective operation, which makes up the sensory apparatus of the muscle as whole. Bakker and Richmond11,12 noted that it is common to find many receptors that occur not as single, isolated units but as receptor aggregations. These muscle spindles are components of a complex, information-gathering system. An analogous, complex sensory system is that of vision. The visual sensory system depends on coding differences in morphologically analogous and proximally located receptors.13 Proprioception in the neck may provide subtle clues in a complex interaction similar to the processing known to occur in the retina. Previous studies9,14 have shown that denervation or section of large neck muscles does not interfere with tonic reflexes but that the reflexes are abolished by section of the small nerves supplying tissues around intervertebral joints. Thus, powerful afferent input to the central nervous system (CNS) must originate from joint receptors or small segmental muscles around vertebral articulations.1,15 Barnsley and Bogduk7 contend there is sufficient evidence that injury to upper cervical joints or muscles can affect tonic neck reflexes and, thus, perceptions of spatial orientation. Neck pain is commonly caused by injury to cervical zygapophyseal joints.1,16 Because these same structures may affect perceptions of spatial orientation, they may also produce the symptoms of dizziness, vertigo, or related proprioceptive aberrations. Many techniques have been used to substantiate disturbed functioning of the proprioceptive array that may account for these symptoms. Caloric testing, electronystagmography, and stabilometry are used to monitor the vestibular

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EFFECT OF NECK PAIN ON VERTICALITY PERCEPTION, Grod

Fig 1. (A) The rod and frame are in a vertical position. (B) The rod is displaced 30° from the vertical.

system. The perception of verticality, which depends on proprioceptive internal cues, has not been used until now. The Rod-and-Frame Test (RFT) offers a convenient, noninvasive method of measuring this aspect of spatial orientation. It requires subjects to set a rod to the true vertical either with or without the presence of a background frame. Studies have proven the RFT’s reliability.17-19 This study used the RFT to test whether subjects with neck pain have a significantly different performance on the RFT than do subjects without neck pain. METHODS Participants Nineteen subjects (11 women, 8 men), aged 15 to 72 years (mean, 38.5y), with uncomplicated mechanical neck pain (acute or recurrent neck pain without pain referral to the upper limbs and no neurologic deficits) and 17 asymptomatic subjects (7 women, 10 men), aged 12 to 66 years (mean, 38.6y), participated. Both groups were typical patients selected from 2 chiropractic offices. The asymptomatic group included patients

with low back pain (LBP) or peripheral joint complaints but no current neck pain. The symptomatic group may have had concurrent LBP or other nonrelated peripheral joint pain as well as neck pain. Exclusion criteria were any bone pathology (ie, neoplasm, infection, serious congenital anomalies); recent history of cervical spine surgery, blindness, or serious visual impairment; and vestibulocochlear disease affecting balance. Materials The RFT requires subjects to set a rod to the true vertical with or without a background frame. In the test environment, subjects were seated 2.5m from the rod-and-frame device. The frame is 107cm2, and the rod is 102cm long (fig 1). The rod was positioned within the square so they shared a common midpoint. The rod was rotated independently of the frame. The amount of rotation for each can be measured in degrees and recorded by a dial on the back of the rod-and-frame device. The rod and frame were covered with luminescent strips so that they were the only visual objects in a darkened room. The rod and frame were hidden from view before each test. Subjects were told that the lights would be extinguished and that 3 tests

Table 1: Repeat ANOVA and ICCs for Averages of the 3 Trials Test

Trial 1 (mean ⫾ SD)

Trial 2 (mean ⫾ SD)

Trial 3 (mean ⫾ SD)

Repeated ANOVA F Statistic

P

ICC†

A1 A2 A3 S1 S2 S3

1.12 ⫾ 1.26 5.82 ⫾ 3.41 .59 ⫾ .87 3.26 ⫾ 3.97 7.37 ⫾ 4.50 2.63 ⫾ 3.18

1.41 ⫾ 1.66 4.53 ⫾ 3.43 .65 ⫾ .79 2.95 ⫾ 3.88 6.74 ⫾ 3.89 2.37 ⫾ 2.85

1.06 ⫾ 1.56 4.71 ⫾ 3.42 .41 ⫾ .79 2.63 ⫾ 3.42 7.37 ⫾ 3.56 2.90 ⫾ 3.53

.73 1.93 .61 1.09 .63 .76

.49* .16* .55* .35* .54* .48*

.63 .60 .40 .90 .74 .83

Abbreviation: ICC, intraclass correlation coefficient; SD, standard deviation. * Not statistically significant at either ␣ ⫽ .05 or ␣ ⫽ .10. In addition, the differences between the trials appear to be clinically trivial in magnitude. † ICC ⫽ 0 represents no agreement between trials; ICC ⫽ 1.00 represents perfect agreement.

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EFFECT OF NECK PAIN ON VERTICALITY PERCEPTION, Grod Table 4: Between-Test Comparisons by Using the Tukey Post Hoc Test

Table 2: Means and SDs for Each Test Test

Asymptomatic

Symptomatic

1 2 3

1.2 ⫾ 1.34 5.02 ⫾ 2.97 .55 ⫾ .62

2.95 ⫾ 3.61 7.16 ⫾ 3.65 2.63 ⫾ 3.01

Tests Compared

each consisting of 3 trials would be administered. Only the rod would be visible on the first tests and a rod within a square frame would be visible on the second and third tests. The subject was asked to close his/her eyes. Initially, the frame portion was not exposed. The subject made 3 trials with the rod set at 10° to begin each test. When the subject was satisfied that the rod was vertical, the deviation from true vertical was measured. In the second test, the frame was set at 10° and the rod at 30°. Again, there were 3 attempts. The third test had the frame set at 0° and the rod at 30°. Assessment was made by measuring the degrees of discrepancy between the subject’s estimate of vertical and the true vertical. The 3 trials per test per subject (table 1) were analyzed with a repeated-measures analysis of variance (ANOVA) to ascertain whether an average of each of the 3 trials was acceptable. The mean values of the 2 groups were compared. We considered values of P less than .05 to be statistically significant. RESULTS Repeated-measures ANOVA and interclass correlation coefficients supported the use of the averages of the 3 trials in all further analyses. A 2-way ANOVA showed statistically significant differences in judging vertical between symptomatic and asymptomatic subjects (F ⫽ 13.37, P ⫽ .001) (table 1). There were significant differences between the 3 test situations (F ⫽ 12.44, P ⫽ .001) (table 2). Unpaired t tests for each test situation and a Tukey post hoc test showed statistical differences for both the asymptomatic and symptomatic groups between test 1 and test 2 (P ⬍ .001) and test 1 and test 3 (P ⬍ .001) (tables 3, 4). DISCUSSION In this study, the RFT was used for the first time to measure differences in the perception of verticality between an asymptomatic group and subjects with mechanical neck pain. Use of the RFT proved to be simple, relatively time efficient, and reliable. The results showed that the symptomatic group, as a whole, had greater error in judging the true vertical. It also showed that both test 1 and test 3 were useful in this way. Test 2, which tested for field dependence and independence, did not discriminate between symptomatic and asymptomatic subjects.

Table 3: Between-Symptom Comparisons (asymptomatic vs symptomatic) Test

Mean 兩⌬兩

t Statistic (1-tailed unpaired t test)

P

1 2 3

1.75 (2.95–1.2) 2.14 (7.16–5.02) 2.08 (2.63–.55)

⫺1.97 ⫺1.94 ⫺2.94

.61* .61* .008†

* Statistically significant at the ␣ ⫽ .10 level (where P must be ⱕ .10 and a maximum 10% probability that the difference between symptom groups will be tolerated). Not statistically significant at the ␣ ⫽ .05 (most commonly used) level. † Statistically significant at both the ␣ ⫽ .10 and ␣ ⫽ .05 levels.

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1 2 1 1 2 1

vs vs vs vs vs vs

2 3 3 2 3 3

A A A S S S

Actual Mean 兩⌬兩

Minimum Required Mean 兩⌬兩

P Value Corresponding to Minimum Required Mean 兩⌬兩

3.82 4.47 .67 4.21 4.53 0.32

兩⌬兩 ⫽ 2.56 兩⌬兩 ⫽ 2.56 .73 ⬎ 兩⌬兩 ⬎ .64 兩⌬兩 ⫽ 3.67 兩⌬兩 ⫽ 4.30 兩⌬兩 ⫽ .49

⬍.001* ⬍.001* .5 ⬍ P ⬍ .6† ⬍.005* ⬍.001* ⬎.900†

Abbreviations: A, asymptomatic; S, symptomatic. * Statistically significant difference between the tests at both the ␣ ⫽ .05 and ␣ ⫽ .10 levels. † No statistically significant difference between the tests at either the ␣ ⫽ .05 or ␣ ⫽ .10 levels.

Our results showed that the RFT may be useful for measuring some of the symptoms other than pain that are experienced by patients with cervical injuries. The perception of verticality comes partially from internal cues. These internal cues are produced by all the spinal proprioceptive receptors (most important, those in the cervical spine). Operating collectively, multiple arrays of these receptors in cervical synovial joints and related musculature provide the CNS with the repetitive sensory information necessary for the perception of verticality. Cervical synovial joints and the inherent segmental musculature are also equipped with numerous nociceptive receptor nerve endings with different behavioral properties and distributions. These nociceptors can adversely affect the functioning of the proprioceptive arrays.15 Such disturbances may make it more difficult to perceive the vertical and give rise to some of the other sensations of disturbed spatial orientation that are present in neck pain patients. Several areas of research follow from these preliminary results. It is not known if neck pain subjects who actually complain of dizziness or other symptoms of disturbed spatial orientation have greater difficulty in perceiving the vertical than do those who complain only of neck pain. Also, there are other means of detecting disturbed spatial orientation that measure an ability to reproduce a neutral head position, the ability to reproduce a chosen head position, forceplate evaluations of body balancing, and the ability to locate accurately a digit placed out of sight.10,20-22 Each of these methods may, in fact, be testing different aspects of spatial orientation. It is not known if results from these different methods would correlate with each other or whether some or all of the methods correlate with the actual symptomatology. The RFT has been used for years to measure field dependence. The extent to which an individual may be functionally impaired by disturbances of spatial orientation may depend on the extent to which his/her perceptual style depends on internal cues. The concept that difficulty with perception of verticality, or any of the other measures of spatial orientation dysfunction, may be affected by perceptual style (ie, field dependence and independence), should be explored. CONCLUSION The results of this study indicate that there may be a direct connection between the structures that provide internal cues for the body’s ability to sense verticality and nociceptive influences affecting the afference of these structures. The overshoot of the neck pain group (symptomatic) could indicate the search for additional proprioceptive information.

EFFECT OF NECK PAIN ON VERTICALITY PERCEPTION, Grod

Because the cervical spine is of primary importance in the functioning of the entire body, it is reasonable to theorize that change in proprioceptive abilities is a conceivable explanation for the statistically significant difference between asymptomatic and symptomatic groups. The RFT is an easy tool to use. The test can be administered effortlessly and can quantify changes in verticality perception. Further studies will attempt to assess if manual therapy, such as spinal manipulative treatment, changes the results in the 2 groups (asymptomatic vs symptomatic). Subsequent studies will shed more light on vertical discernment and perhaps provide another tool for measuring other effects of neck pain. References 1. Bovim G, Schrader H, Sand T. Neck pain in the general population. Spine 1994;19:1307-9. 2. Makela M, Heliovaana M, Sievers K, Impinaana O, Knekt P, Aromaa A. Prevalence, determinants and consequences of chronic neck pain in Finland. Am J Epidemiol 1991;134:1356-67. 3. Deans GT, Magalliard JN, Kerr M, Rutherford WH. Neck sprain: a major cause of disability following car accidents. Injury 1987; 18:10-2. 4. Pearce JM. Whiplash injury: a reappraisal. J Neurol Neurosurg Psychiatry 1998;52:1329-31. 5. Croft AC. Soft tissue injury: long and short-term effects. In: Forman SM, Croft AC, editors. Whiplash injuries: the cervical acceleration/deceleration syndrome. Baltimore: Williams & Wilkins; 1988. p 323. 6. Chester JB. Whiplash, postural control and the inner ear. Spine 1991;16:716-20. 7. Barnsley L, Bogduk N. Clinical review: whiplash injury. Pain 1994;58:283-307. 8. Baloh RW, Honrubia V. Clinical neurophysiology of the vestibular system. 2nd ed. Philadelphia: FA Davis; 1989. p 91-2.

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9. McCouch GP, Deering ID, Ling TH. Location of receptors for tonic neck reflexes. J Neurophysiol 1951;14:191-5. 10. McPartland JM, Brodeur RR, Hallgren RC. Chronic neck pain, standing balance and suboccipital muscle atrophy: a pilot study. J Manipulative Physiol Ther 1997;20:24-9. 11. Bakker DA, Richmond FJ. Muscle spindle complexes in muscles around upper cervical vertebrae in the cat. J Neurophysiol 1982; 48:62-70. 12. Richmond FJ, Bakker DA. Anatomical organization and sensory receptor content of soft tissues surrounding upper cervical vertebrae in the cat. J Neurophysiol 1982;48:49-61. 13. Kuffler SW. Discharge patterns and functional organization of the mammalian retina. J Neurophysiol 1953;16:37-68. 14. Wyke B. Neurology of the cervical spinal joints. Physiotherapy 1979;65(3):72-6. 15. Bogduk N. Cervical causes of headache and dizziness. In: Grieve G, editor. Modern manual therapy of the vertebral column. Edinburgh: Churchill-Livingstone; 1986. p 280-302. 16. Dwyer A, Aprill C, Bogduk N. Cervical zygapophyseal joint pain patterns I: a study in normal volunteers. Spine 1990;15:453-7. 17. Adevai G, McGough WE. Retest reliability of rod-and-frame scores during early adulthood. Percept Mot Skills 1968;26:1306. 18. Lester G. The rod-and-frame test: some comments on methodology. Percept Mot Skills 1968;26:1307-14. 19. Applebaum H. Stability of portable rod-and-frame test scores. Percept Mot Skills 1978;47:1153-4. 20. Christensen HW, Nilsson N. The ability to reproduce the neutral zero position of the head. J Manipulative Physiol Ther 1999;22: 26-8. 21. Revel M, Andre-Deshays C, Minguet M. Cervicocephalic kinesthetic sensibility in patients with cervical pain. Arch Phys Med Rehabil 1991;72:288-91. 22. Rogers RG. The effects of spinal manipulation on cervical kinesthesia in patients with chronic neck pain: a pilot study. J Manipulative Physiol Ther 1997;20:80-5.

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