Responses to a Clinical Test of Mechanical Provocation
of Nerve Tissue in Whiplash Associated DisorderThis section is compiled by Frank M. Painter, D.C.
Send all comments or additions to: Frankp@chiro.org
FROM: Manual Therapy 2002 (May); 7 (2): 89–94 ~ FULL TEXT
Sterling M, Treleaven J, Jull G.
Department of Physiotherapy,
The University of Queensland,
St Lucia, Australia
Involvement of nerve tissue may contribute to the persistence of pain following a whiplash injury. This study aimed to investigate responses to the brachial plexus provocation test (BPPT) in 156 subjects with chronic whiplash associated disorder (WAD) with and without associated arm pain and 95 asymptomatic control subjects. The range of elbow extension (ROM) and visual analogue scale (VAS) pain scores were measured.
Subjects with chronic WAD demonstrated significantly less ROM and higher VAS scores with the BPPT than the asymptomatic subjects (P<0.001). These effects occurred bilaterally. Within the whiplash population, subjects whose arm pain was reproduced by the BPPT demonstrated significantly less ROM on both the symptomatic and asymptomatic sides when compared to the whiplash subjects whose arm pain was not reproduced by the BPPT (P=0.003) and significantly less ROM and higher VAS scores than those whiplash subjects with no arm pain (P=0.003, 0.01). Only the whiplash subjects whose arm pain was reproduced by the BPPT demonstrated differences between the symptomatic and asymptomatic sides. These generalized hyperalgesic responses to the BPPT support the hypothesis of central nervous system hypersensitivity as contributing to persistent pain experienced by WAD patients.
INTRODUCTION
The majority of patients experiencing neck pain following a whiplash injury will recover in 2–3 months (Maimaris et al. 1988; Gargan & Bannister 1990) although the development of persistent neck pain is not uncommon and is believed to occur in 20–40% of cases (Barnsley et al. 1994). Despite poor identification of specific pathologies with current radiological methods (Riley et al. 1995), evidence from cadaveric and animal studies indicate that a variety of lesions are possible. These include damage to zygapophyseal joints, discs, ligaments, muscles and nerve tissue (Davis et al. 1991; Jonsson et al. 1991; Barnsley et al. 1995; Taylor & Taylor 1996). With respect to nerve tissue, primary injuries have been shown to occur to the cervical nerve roots, dorsal root ganglia and spinal cord following a whiplash injury (Taylor & Taylor 1996). Nerve tissue may also become irritated as a consequence of inflammatory processes in adjacent structures such as the intervertebral disc or zygapophyseal joint (Taylor & Taylor 1996; Bove & Light 1997; Eliav et al. 1999).
The predominant symptom of subjects suffering from a persistent whiplash associated disorder (WAD) is neck pain, but other symptoms suggestive of nerve tissue involvement, such as upper limb pain and weakness, paraesthesia and anaesthesia, are also common (Barnsley et al. 1994). Despite the common occurrence of arm pain, overt neurological signs and diagnosis of impaired nerve conduction are not common in WAD (Barnsley et al. 1998). However, pain arising from nerve tissue may not necessarily be accompanied by signs of nerve conduction loss (Greening & Lynn 1998). Irritation of nerve tissue renders it sensitive to mechanical stimulation due to sensitization of C-fibres from axons in continuity producing ectopic discharge with little or no neuronal degeneration such that nerve conduction remains intact (Tal 1999; Eliav et al. 1999, 2001). Sensitization of nociceptors within the nervi nervorum may also play a role although it is believed that activity from this source is quite small and not sufficient to generate neuropathic type pain (Eliav et al. 1999).
Sensitized nerve tissue has been shown to demonstrate hyperalgesic responses to mechanical stimulation (Hall & Quintner 1996; Ochoa 1997). In the clinical setting, the brachial plexus provocation test (BPPT) is commonly used by physiotherapists to mechanically provoke the nerve tissue of the upper limb (Elvey 1979). This test involves the application of controlled longitudinal provocative stimuli to test for mechanical sensitivity of nerve tissue and peripheral nerves in the upper limb. A pathological response is determined by the reproduction of the patient’s pain (Hall & Elvey 1999) coinciding with a decrease in range of movement (usually elbow extension) that is thought to be related to the onset of protective muscle activity (Hall et al. 1993; Balster & Jull 1997; Elvey 1997).
Few studies have investigated the mechanosensitivity of nerve tissue of the upper limb nerve trunks in WAD, despite suggestions of the potential involvement of nerve tissue as contributing to symptoms in this patient group (Koelbaek-Johansen et al. 1999; Munglani 2000). Quintner (1989) investigated the responses to the BPPT in chronic whiplash subjects with arm pain and paraesthesia and suggested the involvement of sensitive cervical nerve tissues in 89% of subjects. More recently, Ide et al. (2001) demonstrated signs of brachial plexus irritation (positive Tinel sign and reproduction of arm symptoms with passive manoeuvres aimed at provoking nerve tissue) in 38% of whiplash subjects at l–12 weeks post injury. Mechanical hyperalgesia of peripheral nerve tissue has also been identified, using pressure algometry, in chronic WAD. This study revealed lowered pressure pain thresholds over the upper limb peripheral nerve trunks in subjects with or without arm pain (Sterling et al. 2002).
Furthermore, a global decrease in mechanical pain thresholds was demonstrated at sites both local and remote to the site of injury, suggestive of central nervous system hypersensitivity (Sterling et al. 2002). Other studies have also supported the involvement of altered central pain processing mechanisms in WAD (Koelbaek-Johansen et al. 1999; Moog et al. 1999). If peripheral nerves of the upper limb demonstrate mechanosensitivity to pressure and should central nervous system hypersensitivity be a component of persistent pain in WAD, these factors together may influence findings of the BPPT and clinical interpretation of such findings. It was the aim of this study to investigate the responses to the BPPT, a test of mechanical provocation of nerve tissue in subjects with chronic WAD when compared to healthy asymptomatic control subjects. A secondary aim was to further investigate these responses in WAD subjects both with and without reported symptoms of arm pain.
METHOD
Subjects One hundred and fifty-six subjects (29 male, 127 female, mean age 37.4379.3years) who were referred to the Whiplash Research Unit in the Department of Physiotherapy, The University of Queensland participated in the study. All subjects were classified as WAD II or III as per the Quebec Task Force classification (Spitzer et al. 1995) and had experienced pain for longer than 3mon ths following the accident. Ninety-five asymptomatic subjects (45 male, 50 female, mean age 38.95714.47 years) were also recruited following appeals to the general community for volunteers. These subjects were included provided they had never experienced any prior pain or trauma to the cervical spine, head or upper quadrant. Ethical clearance for the study was gained from the Medical Research Ethics Committee of The University of Queensland and all subjects gave written informed consent to participate.
Measurements
Clinical neurological examination
A clinical neurological examination including tests for sensation, tendon reflexes and muscle power of the upper limbs was performed on all WAD subjects.
Brachial plexus provocation test (BPPT)
In this study, the BPPT was performed in the following sequence: gentle shoulder girdle depression, glenohumeral abduction and external rotation in the coronal plane, wrist and finger extension and elbow extension. A method previously described by Edgar et al. (1994) was used to standardize the amount of shoulder girdle depression applied at the commencement of the BPPT. An air-filled pressure sensor (Stabiliser, Chattanooga, Pacific) was inserted between the superior aspect of the subject’s shoulder and the examiner’s forearm. The sensor was inflated to a baseline of 40mmHg and shoulder girdle depression was applied to increase pressure to a standard 60mmHg at the commencement of the test. The range of elbow extension during the BPPT was measured using a standard goniometer aligned along the mid-humeral shaft, medial epicondyle and ulnar styloid (Clarkson & Gilewich 1989; Balster & Jull 1997). The subjects’ pain and other symptoms were respected at all times during the test. Elbow extension was taken to a tolerable pain level, defined as the level of pain that the subject was prepared to experience knowing that the test was to be performed several times. A similar measure has been used previously in studies of the BPPT (Coppieters et al. 2001a, b). If no pain was experienced elbow extension was continued to the normal end of range. At the completion of this test, the subjects were asked to rate any pain on a visual analogue scale (VAS).
Procedure
All subjects were requested to disrobe and expose their upper limbs. A clinical neurological examination was performed on all WAD subjects.
The subjects were requested to lie supine. A folded towel was placed under the head to position the cervical spine in a neutral position. A neutral position was visually determined by a horizontal face position between the forehead and chin and observing that a line bisecting the neck longitudinally was parallel to the treatment couch. A research assistant was present to ensure that the subjects’ head remained in this position. The contralateral arm lay resting by the side with the forearm resting on the subject’s abdomen throughout testing. The BPPT was performed once prior to the actual test in order to familiarize the subject with the procedure. The experimental BPPT was then performed and the range of elbow extension recorded at the subject’s nominated tolerable pain level. If the subject did not experience pain, the test was continued to the normal end of range. Once the test was completed, the subject reported where the pain was felt and whether it was their familiar arm pain (whiplash subjects). The subjects then rated the pain intensity felt during the test on the VAS. The BPPT was first performed on the left arm and then repeated on the right arm.
Data management and analysis
Data were analysed using SPSS 10.0 statistical software package. A mixed model ANCOVA was first performed to investigate differences between the WAD subjects and the asymptomatic control subjects. The dependent variables were the range of elbow extension (ROM) and pain intensity determined in the BPPT (VAS) with the within-subjects factor being side (right or left). The independent variable was subject group. Age and gender were used as covariates in the analysis.
Following primary analysis of the total population, further analysis was performed on the data from the whiplash subjects based on the presence or the absence of arm pain as part of their whiplash syndrome. The WAD subjects were categorized into one of three groups. Group 1 were those subjects whose arm pain of which they complained was reproduced by the BPPT. Group 2 were those subjects whose arm pain was not reproduced by the BPPT. Group 3wer e the whiplash subjects with no arm pain. Mixed model ANCOVAS were performed to investigate differences in ROM and pain intensity (VAS) between Groups 1 and 2, Groups 1 and 3and Groups 2 and 3. In these analyses, the dependent variables were ROM and VAS during the BPPT with the within-subjects factor being side (asymptomatic or symptomatic). Six subjects in Group 1 were subsequently found to have bilateral arm pain and the pain in both arms was reproduced by the BPPT. In order to prevent confounding results with respect to the symptomatic and asymptomatic sides, the data from these subjects were not included in these analyses. As subjects in Group 3did not have arm pain and therefore no symptomatic or asymptomatic side, the mean values of both right and left sides were used in the analysis. Again age and gender were used as covariates in both these analyses. Due to the number of analyses performed and to avoid a Type I error, a conservative alpha level was set at Po0.01.
RESULTS
The results of the initial mixed model ANCOVA comparing the asymptomatic control and WAD populations demonstrated that there was a significant difference between the pain reported (VAS) by the WAD group compared to the control group during BPPT as well as a difference in the range of elbow extension (Table 1). There was no significant effect of side (right or left) (F2.250 = 2.05, P = 0.19) and no interaction effect between side and group (F2.250 = 2.16, P = 0.118). There was no significant effect of either age or gender on VAS (F1.250 = 2.92, P = 0.091; F1.250 = 4.46, P = 0.056) or ROM (F1.250 = 1.31, P = 0.253; F1.250 = 2.9, P = 0.089). The marginal means and 95% confidence intervals for ROM and VAS are presented in Table 1. Whiplash subjects had less range of elbow extension and higher pain intensity in the BPPT as compared to the asymptomatic control group.
The WAD subjects were then allocated to either Group 1,2 or 3on pre-referenced criteria for planned posthoc comparisons. Of the 156 WAD subjects, 40 subjects were allocated to Group 1, 54 to Group 2 and 62 to Group 3. Twenty-three subjects (15% of total whiplash population) demonstrated clinical neurological signs, all of whom were members of Group 1. Six subjects were removed from Group 1 for analysis as planned, leaving a total of 34 subjects in this group.
The mixed model ANCOVA performed on data from the WAD Groups 1 and 2 revealed that ROM was significantly less in Group 1 than Group 2 (9.487, P = 0.003) although the difference in pain intensity (VAS) failed to reach significance (F1.84 = 4.176, P = 0.044). There was no main effect of side tested (F2.83 = 0.156, P = 0.856) but there was a significant interaction between side and group (F2.83 = 6.993. P = 0.002). Subjects in Group 1 demonstrated less range of movement and a higher pain intensity in the symptomatic arm. Figures 1 and 2 present the marginal means and 95% confidence intervals for elbow extension ROM and pain scores, respectively, for each group of WAD subjects. The mixed model ANCOVA performed on data from the WAD Groups 1 and 3 reveal ed that ROM was significantly less (F1.151 = 9.03, P = 0.003) and pain intensity (VAS) was significantly greater (F1.151 = 5.51, P = 0.0l) in Group 1 compared to Group 3. There was no main effect of side tested (F2.150 = 2.055, P = 0.132), but there was an interaction effect between side and group (F2.150 = 10.49, Po0.001) reflecting the differences between sides in Group 1 previously discussed.
The mixed model ANCOVA performed on data from WAD Groups 2 and 3reveal ed no significant difference for ROM or pain intensity (VAS) between groups (F1.117 = 1.45, P = 0.232, F1.117 = 0.161, P = 0.689). There was no main effect of side tested (F2.116 = 1.56, P = 0.215) nor any interaction between side and group (F2.116 = 0.657, P = 0.52) (Figs. 1 and 2).
DISCUSSION
The results of this study indicate that subjects with persistent WAD demonstrate hyperalgesic responses to the BPPT (a clinical test of mechanical provocation of nerve tissue). Hyperalgesic responses were manifested by decreased range of elbow extension and higher reports of pain with the test, as compared to asymptomatic control subjects, and the responses were bilateral. They occurred in all WAD subjects regardless of whether the subjects reported arm pain as a symptom of their condition or if that arm pain was reproduced by the BPPT.
Decreased range of movement during the BPPT has been proposed to be due to increased muscle activity, directly related to an evoked pain response, as a protective mechanism for mechanosensitive nerve tissue (Balster & Jull 1997; Elvey 1997; Hall & Elvey 1999). This muscle activity is likely recruited via central nervous system processes to prevent pain associated with the mechanical provocation of nerve tissue (Wright et al. 1994; Hall & Quintner 1996). It is known from animal and human studies that facilitation of the flexor withdrawal reflex occurs in the presence of ongoing C-fibre afferent input from a variety of tissues including muscle, joint and nerve tissue (Wall & Woolf 1984; Ferrell et al. 1988; Gronroos & Pertovaara 1993; Hu et al. 1995). It occurs as a consequence of changes in dorsal horn interneurons involved in reflex pathways to a motor neurones (Cook et al. 1986). The bilateral loss of elbow extension in the whiplash subjects seen in this study may reflect a facilitated flexor withdrawal reflex occurring as a result of central nervous system hyperexcitability. In addition to facilitated motor responses, indicating a decreased threshold to mechanical stimulation, VAS pain scores indicating an increased response to mechanical stimulation were also significantly higher in all WAD subjects. These concomitant hyperalgesic sensory responses are also suggestive of central nervous system sensitization. The findings of this study would support the hypothesis that hypersensitivity is a feature of chronic WAD (Koelbaek-Johansen et al. 1999; Moog et al. 1999; Sterling et al. 2002).
Central nervous system hyperexcitability or central sensitization is believed to be initiated by peripheral nociceptive input following injury (Gracely et al. 1992; Coderre & Katz 1997). The mechanisms by which this central nervous system hyperexcitability is maintained are unclear; however, it has been suggested that an ongoing nociceptive afferent barrage is required (Gracely et al. 1992; Devor 1997). In the case of WAD, it is possible that this ongoing nociceptive input may arise from injured musculoskeletal structures or in some patients, the irritation or injury of nerve tissue.
When the subgroups of WAD subjects were considered, it was found that those whiplash subjects with the classic clinical signs of nerve tissue mechanosensitivity (arm pain reproduced with the BPPT, Group 1) demonstrated greater responses than the other whiplash subjects (Group 2 arm pain not reproduced by the BPPT, Group 3no arm pain). The ROM was less and VAS scores higher in Group 1 subjects compared to those in Groups 2 and 3. Furthermore, only subjects in Group 1 demonstrated greater responses in the symptomatic arm. Even though WAD Groups 2 and 3wer e significantly different from asymptomatic subjects in pain, range and bilateral responses, they were not different from each other. Therefore, it seems that provocation of potentially injured or sensitized nerve tissue (Group 1) induces protective muscle activity over and above that occurring as a result of apparent general hypersensitivity.
Reproduction of arm pain by the BPPT (Group 1) is suggestive of the presence of mechanosensitive nerve tissue (Hall & Elvey 1999). Only 23W AD subjects, who were all members of Group 1, had clinical neurological signs indicative of conduction loss (decreased sensation, loss of muscle power or absent/diminished tendon reflexes). Therefore, approximately one-third of subjects in Group 1 demonstrated signs of nerve tissue sensitization or irritation without apparent conduction loss. This may reflect the presence of relatively minor axonal damage or nerve sheath inflammation undetected by the clinical neurological examination (Greening & Lynn 1998). This may occur as a consequence of inflammatory processes in injured adjacent structures (Taylor & Taylor 1996; Bove & Light 1997) causing sensitization of C-fibres from axons in continuity producing ectopic discharge (Tal 1999; Eliav et al. 2001) or from sensitization of the nervi nervorum (Bove & Light 1997; Sauer et al. 1999). Nevertheless, as primary injury to nerve tissue has been shown to occur with a whiplash injury (Taylor & Taylor 1996), this cannot be ruled out as a cause of the nerve tissue responses seen in this study.
The results of this study have implications for both clinical examination and treatment of patients with persistent WAD. The global decrease in range of movement in the BPPT found in all WAD subjects indicates that caution is required with the interpretation of nerve tissue provocation tests in these patients. Loss of range of movement during these tests may merely reflect generalized hyperalgesic motor responses to a provocative stimulus as opposed to specific pathology of nerve tissue. It is suggested that a clinical diagnosis of nerve tissue mechanosensitivity in WAD should not rest on nerve provocation tests in isolation but involve a more thorough examination process as has been advocated by other authors (Elvey 1997; Hall & Elvey 1999). Evidence from this study supports the possible presence of central nervous system hypersensitivity as a contributor to symptoms in chronic WAD (Sheather-Reid & Cohen 1998; Koelbaek-Johansen et al. 1999; Moog et al. 1999). Treatment of chronic WAD should in consequence be non-provocative and pain free in nature such that this hypersensitivity is not further facilitated. Central sensitization is thought to be maintained by ongoing peripheral nociceptive afferent input (Gracely et al. 1992; Devor 1997), which could include the non-judicious application of pain producing manipulative therapy or exercise. Hall & Elvey (1999) have suggested that treatment techniques involving the movement of nerve tissue, either indirectly or directly, should be gentle and not involve stretching or lengthening techniques. The results of this study strongly support this approach in the treatment of WAD patients.
CONCLUSION
This study provides further support for the contribution of central nervous system hyperexcitability as contributing to symptoms in WAD subjects with persistent symptoms. Although whiplash subjects whose arm pain was reproduced by the BPPT demonstrated greater responses to the nerve tissue provocation test of BPPT, heightened responses were evident in all WAD subjects. This clouds the objective value of this test in isolation for the clinical diagnosis of nerve tissue mechanosensitivity in WAD. These findings suggest the importance of careful assessment in the clinical diagnosis of sensitive nerve tissue in WAD and emphasize the need for nonprovocative treatment in this patient group.
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