Persistent arm and neck pain can occur following whiplash injury to the neck. In some patients, principally those with arm symptoms, the problem may not resolve and many patients suffer disability associated with chronic pain (Suissa et al., 2001). In such patients standard neurological examination is normal and no deficits can be found in nerve conduction (Alpar et al., 2002; Barnsley et al., 1998). There is much dispute regarding the reasons for the persistence of disabling symptoms (Awerbach, 1992; Schrader et al., 1996), which has led some authors to suggest a major psychological component for chronic pain following whiplash (e.g. Gorman, 1979).
There are similarities between chronic arm pain post-whiplash and the chronic pain condition non-specific arm pain (NSAP). The pathology of NSAP is unclear and the diagnosis is made by exclusion of specific upper limb pathologies (Harrington et al., 1998). Characteristically, NSAP patients have many positive sensory symptoms but no indication of nerve damage (e.g. on examination of nerve conduction). Subtle changes in median nerve function (altered C, Aβ and autonomic fibre responses) have been demonstrated in these patients (Greening et al., 2003) indicating a possible neuropathic origin.
In both patient groups there are clinical signs of altered nerve movement and changes in neural mechanosensitivity. Painful responses following physical tests designed to increase tension in the brachial plexus (e.g. upper limb tension test 1 (ULTT1)) have been reported following whiplash injury and in patients with NSAP (Bring and Westman, 1991; Byng, 1997; Greening et al., 2001; Ide et al., 2001; Quintner, 1989; Sterling et al., 2002a). Both patient groups also showed signs of brachial plexus irritation (i.e. positive Tinels sign at the supraclavicular fossa) and decreased pain thresholds to digital pressure over upper limb nerve trunks have also been demonstrated (Ide et al., 2001; Sterling et al., 2002b), as well as signs of thoracic outlet syndrome (TOS) (Kai et al., 2001; Lynn et al., 2002). In addition, MRI studies and high frequency ultrasound imaging have demonstrated a reduction in transverse median nerve sliding in response to wrist flexion in NSAP (Greening et al., 1999, 2001), while median nerve entrapment at the carpal tunnel has also been suggested as a component of chronic arm pain following whiplash injury (Alpar et al., 2002).
In the present study, high frequency ultrasound imaging was used to investigate longitudinal median nerve sliding in response to maximum inspiration in patients with neck and arm pain following whiplash and also patients with NSAP. In the whiplash group transverse sliding of the median nerve at the carpal tunnel was examined to investigate possible similarities with NSAP and carpal tunnel syndrome (CTS). Signs of increased mechanosensitivity along the median nerve course were also examined.
2.1. Whiplash patients
Nine patients (5 female and 4 male) complaining of neck and arm pain following whiplash injury were included in the study. Examination of these patients included moderate digital pressure over the median nerve to look for mechanical allodynia at the carpal tunnel, just proximal to the carpal tunnel and over the cords of the brachial plexus at the supraclavicular fossa. Allodynic responses were recorded for those subjects who reported local or referred symptoms to this moderate pressure. The ULTT1 and a clinical test for TOS (Roo's Test (Roos, 1976)) were also used. The ULTT1 consists of 90° shoulder abduction, elbow and wrist extension, and has been shown to tension the median nerve and brachial plexus (Kleinrensink et al., 2000). A positive test is one that reproduces symptoms and demonstrates a restriction in the range of elbow and wrist extension. Roo's test involves the subject positioning their upper limb at 90° shoulder abduction, lateral rotation and 90° elbow flexion, and performing active flexion and extension of the digits for 30s. Reproduction of patient symptoms indicates a positive result. Height, weight and demographic details were recorded. Eight control subjects (4 female and 4 male) were also examined (Table 1). Clinical screening to exclude patients with signs of cervical radiculopathy, tendonopathy, a previous history of CTS, upper limb/rib fracture or asthma was carried out. In addition, subjects were questioned in general terms regarding site, extent and characteristics of any symptoms, which was recorded on a standardized body chart. This was used to determine the most affected side. Control subjects were also screened to exclude any cervical spine or upper limb pathology or a previous history of whiplash, NSAP or asthma. All subjects were screened by senior physiotherapy staff at Livingstone Hospital Dartford, Kent UK (Dartford, Gravesham and Swanley Primary Care Trust). The experimenter was blind to subject status.
2.2. Non-specific arm pain patients
Eight female patients, who all attributed their symptoms to prolonged and intensive keyboard use, were screened to ensure they conformed to the diagnostic criteria for NSAP (Harrington et al., 1998). The examination included digital pressure over nerve trunks to assess mechanical allodynia at three locations: two over the median nerve (just proximal to the carpal tunnel and over the pronator teres muscle) and over the cords of the brachial plexus in the supraclavicular fossa. In addition, the ULTT1 and Roo's Test were performed. Height, weight and demographic details were recorded. Eight female control subjects were also examined (Table 2). Clinical examination was carried by one of the authors (JG) to ensure that patients conformed to the subjective criteria for non-specific arm pain (NSAP) and that they were not suffering with any other upper limb pathologies, for example, CTS, tenosynovitis, tendonitis or asthma (Harrington et al., 1998). All symptoms were recorded on a standardised body chart, which was used to determine the most affected side. Control subjects were also screened to exclude any cervical spine or upper limb pathology or a previous history of NSAP, whiplash or asthma. Controls were also excluded if they used display screen equipment for more than 40% of their working week.
2.3. Longitudinal median nerve imaging
In the whiplash group, patients (n=9) and controls (n=8) were imaged whilst lying supine with their shoulder abducted to 30°, the elbow fully extended and the forearm supinated. The arm was supported on a Perspex plate, the wrist and digits maintained in neutral. Since the experimenter was blind to subject status, nerve movement was examined bilaterally in both groups. Image evaluation was carried out in a blind fashion.
Imaging in the NSAP group (patients (n=8) and controls (n=7)) was carried out as in the whiplash group. Imaging was performed over the most symptomatic side in the patients, which was also their dominant side. Therefore, the dominant arm was imaged in the control group. Since NSAP patients were not examined blind, spirometry was used during imaging to measure recumbent vital capacity, to ensure that each subject produced a maximum inspiration.
In all subjects the median nerve was imaged in longitudinal section at one location approximately mid forearm during maximal inspiration following forced expiration. A practise session prior to imaging was carried out to ensure that all subjects could produce a pain-free maximal inspiration. During the inspiration phase, sequences of ultrasound images were captured as a cine loop at 10frames/s using a Diasus ultrasound system (Dynamic Imaging, Livingston, Scotland, UK) with a 10–22MHz, 26mm linear array transducer. The image sequences were analysed offline using software developed in Matlab (Mathworks, USA) that employs a frame-by-frame cross-correlation algorithm (Dilley et al., 2001, 2003). Resolution of the images was 0.09mm/pixel and image size was 280 by 440pixels. The procedure was repeated three times.
2.4. Transverse nerve movement in whiplash patients
Transverse images were obtained on the palmer surface of the wrist at the distal wrist crease. Subjects were lying supine with their shoulder abducted to 30°, with the elbow fully extended and the forearm supinated. The forearm was supported on a Perspex plate and the hand was attached to a separate plate using Velcro strapping. The digits and metacarpophalangeal joints were maintained in neutral for each movement. Images were taken with the wrist in 30° extension and 30° flexion. Adjustable stops ensured that the degree of wrist extension/flexion was not exceeded. The surface of the skin was marked using thin (2mm wide) strips of tape (Fixamull, Beirsdorf) applied along the long axis of the palmer surface of the wrist. Two strips were positioned 10–17mm apart and could be seen on the ultrasound images as bright lines which cast an acoustic shadow across the image. Median nerve location was measured relative to these markers using the tpsDig program (F. James Rohlf, Department of Ecology and Evolution State University of New York). Change in nerve position was measured by subtracting the values in extension from those in the flexed wrist position.
Local ethical approval was obtained for both studies. Written informed consent was obtained from all participants.
2.5. Statistical analysis
Comparisons between nerve movements in patients and controls were carried out using student's t-test. Error values are for standard errors of the means.
3.1. Clinical results
The clinical findings for all subjects are summarised in Tables 1 and 2. Eight of nine patients in the whiplash group and all NSAP patients (n=8) showed signs of mechanical allodynia of the median nerve trunk or chords of the brachial plexus. Six of nine whiplash and 7 of 8 NSAP patients had positive results on testing the thoracic outlet. The ULLT1 was positive in all patients.
3.2. Longitudinal nerve movement in whiplash patients
In all control subjects (n=8) the median nerve moved proximally during maximum inspiration. There was no significant difference between right and left side (P=0.89, paired t-test), and therefore the results were combined (mean=1.32±0.17mm (95% CI=0.91–1.73mm)). In the whiplash injured patients (n=9) nerve movement on the symptomatic or more symptomatic side was greatly reduced (a 71% reduction) compared to the control group (mean=0.38±0.08mm (95% CI=0.20–0.56mm), P<0.05 (unpaired t-test)). One patient had equal bilateral symptoms, and therefore the results for both sides were averaged. Nerve movement on the most symptomatic side in the remaining subjects was also reduced (a 52% reduction) compared to the less symptomatic or non-symptomatic side (n=8; symptomatic mean=0.32±0.06mm (95% CI=0.46–0.18); less/non-symptomatic mean=0.66±0.12mm (95% CI=0.39–0.93mm); P<0.05 (paired t-test)). Nerve movement on the non or less symptomatic side remained reduced compared to controls (P<0.05 (unpaired t-test)). These results are summarised in Fig. 1.
3.3. Longitudinal nerve movement in NSAP patients
Recumbent vital capacity measured by spirometry was not significantly different between patient and control groups (NSAP patients mean=2.70±0.13l; control mean2.80±0.18l, P=0.65, unpaired t-test). In control subjects the mean nerve movement was 1.55±0.19mm (95% CI=1.09–2.00mm). In 7 of 8 patients, nerve movement was markedly reduced (a 68% reduction; mean=0.49±0.19mm (95% CI=−0.02–1.00mm, P<0.05, unpaired t-test)) (Fig. 2). There was no significant difference in nerve movement between NSAP or whiplash controls (P=0.40, unpaired t-test).
3.4. Transverse nerve movement in whiplash patients
In the control group (n=7) the results for transverse median nerve movement during 30° wrist extension to 30° flexion were variable. There were no side differences and therefore the results were combined (P=0.86, paired t-test). Nerve movement ranged from −5.09mm in an ulna direction to 3.59mm radially (movement in the ulna direction is expressed as a negative result). The mean translation was −0.39±0.52mm ulna (95% CI=−1.66–0.88mm). In the whiplash group, results on the symptomatic side averaged 2.57±0.80mm in a radial direction (95% CI=0.61–4.54mm). One patient had equal bilateral symptoms, and therefore the results for both sides were averaged. This result was significantly different compared to the control average (P<0.05, unpaired t-test). There was no significant difference between symptomatic and non-symptomatic sides (n=6; symptomatic mean=2.93±0.85mm (95% CI=0.74–5.12mm); non-symptomatic mean=2.29±1.02mm (95% CI=−0.35–4.93mm); P=0.36 (paired t-test)).
4.1. Indications of altered nerve sliding
The present results demonstrate a proximal change in nerve sliding in both the whiplash and NSAP patient groups. Spirometry measures in the NSAP patients showed a similar recumbent vital capacity compared to controls indicating a similar level of inspiration between both groups. In the whiplash study, experimenter blinding to subject status ensured no bias towards the depth of deep breathing each subject was encouraged to make. None of the subjects had problems taking a maximal deep inspiration. Control subjects in both groups demonstrated a similar degree of nerve sliding. Only female subjects were examined in the NSAP control group, since all patients were also female. Female/male differences in nerve movement have not been previously observed (Greening, Dilley, Lynn, unpublished observations).
The nerve movement observed in the forearm of control subjects during maximum inspiration is likely to occur because of the close association of the medial cord of the brachial plexus (which contributes to the formation of the median nerve) to the first rib. Elevation of the first rib during maximum inspiration is likely to stretch the medial cord as the nerve bed increases in length, resulting in proximal sliding of the nerve in the arm and forearm. However, in both patient groups the movements seen in the forearm were markedly reduced.
Decreased proximal nerve gliding in the patient groups in response to deep inspiration may be caused by a number of different factors, including a restriction in motion of the first rib. In the NSAP patients, poor and prolonged cervical spine posture might result in shortening of the scalene muscles (Pascarelli and Hsu, 2001), which could cause an elevated first rib. During whiplash injury the first rib may also be elevated (based on clinical observations by digital palpation of both first ribs (Greening, unpublished observations)), possibly due to the excessive stretch applied to the scalene muscles and their subsequent reflex shortening. Furthermore, first rib elevation may restrict the space around the neurovascular bundle at the thoracic outlet, altering the ability for the nerve to slide through the shoulder region during upper limb movements.
There were significant differences in transverse movement of the median nerve at the wrist in the whiplash injured patients compared to controls indicating distal changes. Interestingly the transverse median nerve movement was increased in the patient group, always in a radial direction, compared to the more random movement observed in the controls. These results are difficult to interpret since movements in both patients and controls were dissimilar to the results for NSAP, which showed a reduction in transverse movement compared to controls (Greening et al., 2001). This is likely to be due to the different arm positions used, since in the present study the forearm was positioned in supine, whereas in the NSAP study the forearm was pronated. Despite these differences both studies indicate changes at the wrist in whiplash and NSAP patients.
4.2. Distributed signs and symptoms
Both whiplash and NSAP patients demonstrate similar diffuse symptoms in the neck and upper limb. Correspondingly, in both patient groups the present results show a change in nerve sliding at both proximal and distal locations. Both groups also show distributed signs of mechanical allodynia to digital pressure over sites along the median nerve and cords of the brachial plexus. Such diffuse symptoms may be the result of a change in nerve environment at the thoracic outlet and the carpal tunnel, which may lead to localised inflammation. For example, there is evidence that whiplash injury can lead to significant soft tissue injury, exposing nerve roots and spinal nerves to inflammatory mediators (reviewed in Greening, 2005). Inflammation of the nerve or its environment can lead to increased mechanosensitivity of C and Aβ fibres (Bove et al., 2003; Dilley and Lynn, 2004; Eliav et al., 2001). In the clinical situation, inflammatory changes might contribute to nerve allodynia with digital pressure along the nerve course. Mechanosensitivity to nerve stretch within the physiological range has also been demonstrated following nerve inflammation (Dilley and Lynn, 2004). Clinically, positive results to the ULTT1 are likely to be in part due to increased nerve mechanosensitivity following inflammation.
This study has shown small nerve movements in the forearm in response to deep breathing that are reduced in both whiplash and NSAP patients. Whiplash injured patients have changed nerve sliding at the wrist, indicating a more distributed problem than has been previously considered for this group. In both these diffuse chronic pain conditions, the change in nerve sliding may reflect underlying nerve pathology that could play a part in causing pain symptoms. Ultrasound imaging may provide a useful addition to the methods available for diagnosing NSAP and chronic whiplash disorders and for monitoring treatment.
All physiotherapists and staff at Livingstone Hospital Physiotherapy Department Dartford Kent UK for their help in recruiting and screening patients and control subjects.
Alpar EK, Onuoha G, Killampali VV, Waters R. Management of chronic pain in whiplash injury. J Bone Joint Surg Br
Awerbach MS. Whiplash in Australia; illness or injury? Med J Aust
Barnsley L, Lord S, Bogduk N. The pathophysiology of whiplash. Spine: State of the Art Reviews
Bove GM, Ransil BJ, Lin HC, Leem JG. Inflammation induces ectopic mechanical sensitivity in axons of nociceptors innervating deep tissues. J Neurophysiol
Bring G, Westman G. Chronic post-traumatic syndrome after whiplash injury: a pilot study of 22 patients. Scand J Prim Health Care
Byng J. Overuse syndromes of the upper limb and the upper limb tension test: a comparison between patients, asymptomatic keyboard workers and asymptomatic non-keyboard workers. Man Ther
Dilley A, Lynn B. Stretch responses of axons in regions of local inflammation in rat peripheral nerves. Comp Biochem Physiol A Mol Integr Physiol. 2004;137(suppl. 1):S111-S112.
Dilley A, Greening J, Lynn B, Leary R, Morris V. The use of cross-correlation analysis between high-frequency ultasound images to measure longitudinal median nerve
movement. Ultrasound Med Biol
Dilley A, Lynn B, Greening J, Deleon N. Quantitative in vivo studies of median nerve
sliding in response to wrist, elbow, shoulder and neck movements. Clin Biomech (Bristol, Avon)
Eliav E, Benoliel R, Tal M. Inflammation with no axonal damage of the rat saphenous nerve trunk induces ectopic discharge and mechanosensitivity in myelinated axons. Neurosci Lett
Gorman RF. ‘Whiplash’ fictive or factual. Bull Am Acad Psychiatry Law
Greening J. How inflammation and minor nerve injury contribute to pain in nerve root and peripheral neuropathies. In: Boyling J, Jull G, editors. Modern Manual Therapy Of the Vertebral Column. 3rd ed.; Amsterdam: Elsevier, 2005. pp. 205–214.
Greening J, Smart S, Leary R, O'Higgins P, Hall-Craggs M, Lynn B. Reduced movement of the median nerve
at the carpal tunnel during wrist flexion in patients with non-specific forearm pain: a magnetic imaging study. Lancet
Greening J, Lynn B, Leary R, Warren L, O'Higgins P, Hall-Craggs M. The use of ultrasound imaging to demonstrate reduced movement of the median nerve
during wrist flexion in patients with non-specific arm pain. J Hand Surg [Br]
Greening J, Lynn B, Leary R. Sensory and autonomic function and ultrasound nerve imaging in RSI patients and keyboard workers. Pain
Harrington JM, Carter JT, Birrell L, Gompertz D. Surveillance case definitions for work related upper limb pain syndromes. Occup Environ Med
Ide M, Ide J, Yamagam M, Takagik K. Symptoms and signs of irritation of the brachial plexus in whiplash injuries. J Bone Joint Surg Br
Kai Y, Oyama M, Kurose S, Inadome T, Oketani Y, Masuda Y. Neurogenic thoracic outlet syndrome in whiplash injury. J Spinal Disord
Kleinrensink GJ, Stoeckart R, Mulder PG, Broek T, Vleeming A, Snijders CJ. Upper limb tension tests as tools in the diagnosis of nerve and plexus lesions. Anatomical and biomechanical aspects. Clin Biomech (Bristol, Avon)
Lynn B, Greening J, Leary R. Sensory and autonomic function and ultrasound nerve imaging in RSI patients and keyboard workers. Health and Safety Executive Contract Report UK 2002;417/2002.
Pascarelli EF, Hsu YP. Understanding work-related upper extremity disorders: clinical findings in 485 computer users, musicians, and others. J Occup Rehabil
Quintner J. A study of upper limb pain and paraesthesia following neck injury in motor vehicle accidents: assessment of brachial plexus tension test of Elvey. Br J Rheumatol
Roos DB. Congenital anomalies associated with thoracic outlet syndrome: anatomy, diagnosis and treatment. Am J Surg
Schrader H, Obelienene D, Bovim G, Surkiene D, Mickevciene D, Mickevciene I, Sand T. Natural evolution of the late whiplash syndrome outside the medicolegal context. Lancet
Sterling M, Treleaven J, Jull G. Responses to a clinical test of mechanical provocation of nerve tissue in whiplash associated disorder. Man Ther
Sterling M, Treleaven J, Edwards S, Jull G. Pressure pain thresholds in chronic whiplash associated disorder: further evidence of altered central pain processing. J Musculoskelet Pain
Suissa S, Harder S, Veilleux M. The relation between initial symptoms and signs and the prognosis of whiplash. Eur Spine J