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ROBERT J. NEE, PT, MAppSc1 • GWENDOLEN A. JULL, PT, PhD2 • BILL VICENZINO, PT, PhD2 • MICHEL W. COPPIETERS, PT, PhD3

The Validity of Upper-Limb Neurodynamic Tests for Detecting Peripheral Neuropathic Pain

U

tralateral neck sidebending inpper-limb neurodynamic tests (ULNTs) (FIGURE 1, creases a sensory response in the ONLINE VIDEOS) use a series of movements to apply forearm).12,38 Moving a distant SUPPLEMENTAL mechanical forces to a portion of the nervous system.12,38 VIDEO ONLINE body part to evaluate a ULNT reULNTs also load nonneural tissues.12,38 Therefore, when sponse is referred to as structural central pain mechanisms are not the primary reason for a patient’s differentiation.12,38,45 pain experience, a ULNT response could be related to neural or Peripheral neuropathic pain (PNP) nonneural tissue sensitivity. In these situations, a ULNT response is thought to be related to neural tissue sensitivTTSYNOPSIS: The validity of upper-limb neurody-

namic tests (ULNTs) for detecting peripheral neuropathic pain (PNP) was assessed by reviewing the evidence on plausibility, the definition of a positive test, reliability, and concurrent validity. Evidence was identified by a structured search for peerreviewed articles published in English before May 2011. The quality of concurrent validity studies was assessed with the Quality Assessment of Diagnostic Accuracy Studies tool, where appropriate. Biomechanical and experimental pain data support the plausibility of ULNTs. Evidence suggests that a positive ULNT should at least partially reproduce the patient’s symptoms and that structural differentiation should change these symptoms. Data indicate that this definition of a positive ULNT is reliable when used clinically. Limited evidence suggests that the median nerve test, but not the radial nerve test, helps determine whether a patient has cervical radiculopathy. The median nerve test does not help diagnose carpal tunnel syndrome.

ity when it changes with movement of a distant body part that further loads or unloads the nervous system (eg, conThese findings should be interpreted cautiously, because diagnostic accuracy might have been distorted by the investigators’ definitions of a positive ULNT. Furthermore, patients with PNP who presented with increased nerve mechanosensitivity rather than conduction loss might have been incorrectly classified by electrophysiological reference standards as not having PNP. The only evidence for concurrent validity of the ulnar nerve test was a case study on cubital tunnel syndrome. We recommend that researchers develop more comprehensive reference standards for PNP to accurately assess the concurrent validity of ULNTs and continue investigating the predictive validity of ULNTs for prognosis or treatment response. J Orthop Sports Phys Ther 2012;42(5):413-424, Epub 8 March 2012. doi:10.2519/jospt.2012.3988

TTKEY WORDS: carpal tunnel syndrome, cervical radiculopathy, cubital tunnel syndrome, reliability

is pain that arises as a direct result of a lesion or disease affecting the somatosensory component of the peripheral nervous system.99 Clinicians use ULNTs to help determine whether patients have PNP conditions such as cervical radiculopathy,110 carpal tunnel syndrome,104,111 and cubital tunnel syndrome.20,85 The rationale for the use of ULNTs is that they are considered capable of detecting the increased nerve mechanosensitivity associated with these conditions.12,38,42,45,112 Other clinical tests proposed for detecting these conditions, such as the Spurling test,92 Phalen’s test,75 and the elbow flexion-pressure test,68 use the same rationale. While ULNTs can also be used to guide treatment selection,12,38,45 a specific assessment of their diagnostic validity is important. Guidelines recommend that clinicians use these tests when examining patients with symptoms affecting the neck or upper limb,1,16 and expert physical

PhD candidate, Division of Physiotherapy and NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Australia. 2Professor, Division of Physiotherapy and NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Australia. 3Associate Professor, Division of Physiotherapy and NHMRC Centre of Clinical Research Excellence in Spinal Pain, Injury and Health, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Australia. Robert J. Nee was funded by an Endeavour International Postgraduate Research Scholarship from the Australian Government and a Research Scholarship from The University of Queensland. Address correspondence to Dr Michel W. Coppieters, Division of Physiotherapy, School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia. E-mail: m.coppieters@uq.edu.au 1

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therapists and pain consultants rely heavily on neurodynamic tests for making a clinical diagnosis of PNP.90 The validity of ULNTs to detect PNP can be assessed by answering 4 questions.41,58,80,87 First, are ULNTs plausible tests for detecting PNP? Second, what criteria should be used to define a positive ULNT? Third, can clinicians make reliable decisions about a positive ULNT? Fourth, are ULNTs accurate for detecting PNP clinically (concurrent validity)? This clinical commentary reviews the available evidence to help answer these questions.

ULNT1MEDIAN • Shoulder girdle stabilization • Shoulder abduction • Wrist/finger extension • Forearm supination • Shoulder external rotation • Elbow extension • Structural differentiation - Cervical sidebending - Release wrist extension ULNT2MEDIAN • Shoulder girdle depression • Elbow extension • Shoulder external rotation and forearm supination • Wrist/finger extension • Shoulder abduction • Structural differentiation - Cervical sidebending - Release shoulder girdle depression - Release wrist extension

SEARCH STRATEGY

S

earch terms were entered into PubMed, CINAHL, EMBASE, Scopus, and Web of Science to find peerreviewed articles published in English before May 2011. Titles and abstracts were screened, and full-text articles of all potentially relevant publications were retrieved for further assessment. Reference lists of retrieved articles were hand searched for additional publications. Cadaveric studies measuring nerve strain (percent elongation) and nerve sliding (longitudinal displacement) during ULNT movements had to use whole-body or transthoracic specimens that maintained the nerve root attachments to the spinal cord.124 Biomechanical studies focusing only on moving individual digits were excluded, because the hand and wrist are normally moved together during ULNTs.12,38 FIGURE 2 summarizes the search.

DIAGNOSING PERIPHERAL NEUROPATHIC PAIN

A

reference standard for diagnosing PNP is needed to interpret results from clinical studies on ULNT validity. Treede et al99 proposed that their criteria for “probable” neuropathic pain would be sufficient for making a neuropathic pain diagnosis. For PNP, probable means that (1) the patient’s symptoms fit a nerve-related distribution, (2) the history of symptoms is

ULNTRADIAL • Shoulder girdle depression • Elbow extension • Shoulder internal rotation and forearm pronation • Wrist/finger flexion • Shoulder abduction • Structural differentiation - Cervical sidebending - Release shoulder girdle depression - Release wrist flexion ULNTULNAR • Wrist/finger extension • Forearm pronation • Elbow flexion • Shoulder external rotation • Shoulder girdle depression • Shoulder abduction • Structural differentiation - Cervical sidebending - Release shoulder girdle depression - Release wrist extension FIGURE 1. Standard sequence of joint movements and suggested structural differentiation maneuvers for each ULNT.12 Joint movements for each ULNT can be applied in different sequences (ONLINE VIDEOS).12,38 Abbreviation: ULNT, upper-limb neurodynamic test.

consistent with a nerve-related problem, and either (3a) a clinical neurological examination shows positive or negative sensory signs that match the innervation territory of the suspected nerve problem, or (3b) diagnostic tests, such as imaging or electrophysiological studies, confirm an injury or disease that explains the distribution of PNP.99

PLAUSIBILITY OF ULNTs

B

iomechanical studies on nerve strain, sliding, and compression help answer whether ULNTs are plausible tests for detecting PNP. Cadaveric studies show that joint movements used in the me-

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Median nerve Radial nerve Ulnar nerve Brachial plexus Spinal nerve roots Spinal nerves Nerve roots

“AND” biomechanics (English, humans)* “AND” excursion (English, humans)* “AND” sliding (English, humans)*

Brachial plexus tension test Brachial plexus provocation test Neural tissue provocation test Upper-limb tension test Upper-limb neural tension test Upper-limb neurodynamic test Neurodynamic(s) “AND” test (English)*

PubMed, 932 records CINAHL, 237 records† EMBASE, 622 records Scopus, 1388 records Web of Science, 293 records Excluded, 3360 including duplicates Full-text articles retrieved, 112 Excluded, 46 • Cadaver limbs only, 13 • Finger motion only, 8 • Validity questions not addressed, 25

Relevant articles from hand search of reference lists, 12 Articles included in review, 78

Biomechanical studies, 40

Cadaver studies, 23

Clinical studies, 38

In vivo studies, 17

FIGURE 2. Search strategy and results. *Limits used for each search. †Nerve structure terms were searched in isolation because combining each term with biomechanics, excursion, or sliding revealed no records.

dian (ULNTMEDIAN),13,18,21,56,57,61,66,67,119,124,127 radial (ULNTRADIAL),122 and ulnar (ULNTULNAR)2,3,13,21,47,66,72,83,98,123 nerve tests increase strain in the corresponding nerve. Each test preferentially loads its corresponding nerve at the elbow and wrist,13,56 suggesting that mechanosensitivity of a particular nerve near these joints may be most readily assessed by the corresponding ULNT. ULNTs cannot selectively test mechanosensitivity of individual nerve roots.55 Shoulder girdle stabilization/depression and shoulder abduction involved in all ULNTs increase strain

throughout the brachial plexus.55 Cadaveric13,18,21,67,118,122-124 and in vivo22,29,30,32,33,35, 49,52,65,100,101 studies also show that ULNT movements produce sliding between the nerve and surrounding tissues. A nerve segment slides toward the moving joint as each ULNT movement lengthens the nerve bed. Strain and sliding produced by a joint movement are greatest in nerve segments closest to the moving joint.18,30,32,52,56,57,122-124 However, when the limb is in the end ULNT position, biomechanical effects from wrist movement or

neck sidebending spread along the entire nerve.18,21,22,30,52,56,57,61,65,119,122,124 These data support the concept of structural differentiation. The spread of biomechanical effects along the nerve is a plausible explanation for why movement of a distant body part can change sensory responses at the end of a ULNT. Transfer of strain through the fascial network in the neck and upper limb91,93 may also explain why moving a distant body part changes sensory responses at the end of a neurodynamic test.5 However, a separate literature search did

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[ ULNT1MEDIAN and ULNT2MEDIAN

clinical commentary

ULNTRADIAL Anterior view

ULNTRADIAL Posterior view

x

x

FIGURE 3. The most common areas where asymptomatic individuals reported sensory responses at the end of ULNT1MEDIAN,23,54,63 ULNT2MEDIAN,63,77 and ULNTRADIAL.73,126 Abbreviation: ULNT, upper-limb neurodynamic test.

not identify any studies that specifically measured whether strain produced by a structural differentiation maneuver, such as contralateral neck sidebending, might be transferred to distant parts of this fascial network. ULNT movements also compress nerves. For example, wrist extension compresses the median nerve in the carpal tunnel114,115; the combination of elbow extension, forearm pronation, and wrist flexion compresses the deep branch of the radial nerve in the radial tunnel39,62; and the combination of elbow flexion and wrist extension compresses the ulnar nerve in the cubital tunnel.69 Based on these biomechanical data, ULNTs appear to be plausible tests for detecting PNP. Strain and compression from ULNT movements will likely provoke mechanically sensitive neural tissues in patients with PNP. Furthermore, the ability for wrist or neck movement in the end ULNT position to produce biomechanical effects throughout the nerve supports using structural differentiation to determine whether an ULNT response is related to nerve mechanosensitivity. An experimental pain model further supports the plausibility of ULNTs. Coppieters et al19 induced experimental pain in the thenar muscles of asymptomatic volunteers and showed that ULNT1MEdid not change the distribution or DIAN

intensity of muscle-related pain. This suggests that ULNT1MEDIAN can potentially distinguish pain related to muscle irritation from pain related to increased nerve mechanosensitivity. Although biomechanical and experimental pain data support using ULNTs to detect PNP, it must be remembered that plausibility is the lowest level of test validity.87

DEFINING A POSITIVE ULNT

S

ensory responses, resistance to movement, and range of motion during a ULNT are assessed to determine whether a patient shows signs of increased nerve mechanosensitivity.12,38 To be useful criteria for defining a positive test, ULNT responses should exhibit 2 properties.80 First, the ULNT responses must discriminate patients with PNP from asymptomatic individuals. Second, concurrent validity studies must show that these ULNT responses also discriminate patients with PNP from patients who present with competing diagnoses. This section addresses the potential ability of ULNT responses to discriminate patients with PNP from asymptomatic individuals and proposes criteria for defining a positive ULNT. Evidence on the concurrent validity of ULNTs is presented later in this clinical commentary.

]

Sensory Responses FIGURE 3 shows the most common areas in

which asymptomatic individuals reported sensory responses at the end of ULNT1ME,23,54,63 ULNT2MEDIAN,63,77 and ULNTRADIAN .73,126 There were no equivalent studies DIAL for ULNTULNAR. Sensory responses were predominantly described as stretch, ache, pain, burning, and tingling.23,54,63,73,77,102,126 Structural differentiation with contralateral neck sidebending increased limb responses in more than 85% of participants.54,73,77,126 This suggests that asymptomatic individuals have a certain level of nerve mechanosensitivity. The variety of responses reported by asymptomatic individuals signifies the need to be specific about the type of sensory response that qualifies as a positive ULNT in symptomatic populations. To be confident that a sensory response distinguishes a patient with PNP from asymptomatic individuals and, therefore, potentially discriminates patients with PNP from those with competing diagnoses, the ULNT needs to reproduce at least part of the patient’s symptoms. For example, if a patient reports pain in the neck that spreads down 1 limb past the elbow, the ULNT should reproduce this pain at least somewhere in the neck, upper arm, or forearm.

Resistance to Movement Resistance to movement during ULNT1MEDIAN has been quantified by relating shoulder girdle elevation force24,25 and torque resisting passive elbow extension50 to elbow extension range of motion. Only shoulder girdle elevation force has been assessed in a symptomatic population.25 Patients with nerve-related neck and unilateral arm pain showed increased shoulder girdle elevation force at earlier stages of elbow extension in the symptomatic limb. These findings cannot be generalized to everyday clinical practice, because a load cell was used to measure shoulder girdle elevation force. Two studies used clinically feasible methods for quantifying resistance to movement during ULNT1MEDIAN.48,105 Examiners identified the onset of resistance

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during elbow extension in asymptomatic participants and measured this angle with a standard goniometer48 or an electrogoniometer.105 Intraclass correlation coefficients (ICC2,1)86 for interexaminer reliability were 0.42 (calculated from reported data)48 and 0.48.105 The standard error of measurement36 for both studies was 10° (calculated from reported data). This translates to a smallest detectable difference at a 95% confidence level (SDD95)36 of 28°. This amount of measurement error suggests that onset of resistance probably cannot be sensitive enough to discriminate patients with PNP from asymptomatic individuals and is, therefore, unlikely to be a useful criterion for a positive ULNT1MEDIAN.

Range of Motion ULNT range of motion is usually quantified by the joint angle at pain onset or pain tolerance (eg, ULNT1MEDIAN elbow extension or ULNTRADIAL shoulder abduction). Patients with PNP are expected to exhibit less range of motion in their symptomatic limb compared to their asymptomatic limb or asymptomatic individuals. Several studies have compared ULNT1MEDIAN14,15,17,26,84,94-97,103,121 or ULNTRADI71,73,106,107,121,125 range of motion between AL patients’ symptomatic and asymptomatic limbs or between patients and asymptomatic individuals. Only Chien et al15 included patients with PNP who met the diagnostic criteria of Treede et al.99 Patients with cervical radiculopathy had less ULNT1MEDIAN range of motion at pain onset in the symptomatic limb compared to the asymptomatic limb or asymptomatic individuals (FIGURE 4). However, significant differences in range of motion for group data do not help determine whether an individual patient has an abnormal deficit in ULNT range of motion. One strategy for determining whether an individual patient has an abnormal deficit in ULNT range of motion is to identify an absolute cut-off for the symptomatic limb. Davis et al28 proposed that, when the neck is in contralateral side-

(n = 38) (n = 38)

Chien et al15

(n = 31) (n = 10)

Coppieters et al17

(n = 20)

Sterling et al94

(n = 20)

Sterling et al95

(n = 36)

Vanti et al105

0

10

20

30

40

50

60

Deficit in Elbow Extension at Onset of Pain, deg Symptomatic limb of patients with cervical radiculopathy Asymptomatic limb of patients with cervical radiculopathy Asymptomatic individuals

FIGURE 4. Average deficit in elbow extension range of motion at the onset of pain during ULNT1MEDIAN (cervical spine in neutral). Error bars represent 1 standard deviation and provide an indication of the variability in range-ofmotion deficit among participants. Abbreviation: ULNT, upper-limb neurodynamic test.

bending before applying ULNT1MEDIAN, elbow extension deficits greater than 60° at pain onset could be classified as abnormal. Because this proposed cut-off is based on asymptomatic data only, its ability to discriminate patients with PNP from asymptomatic individuals needs to be tested. Despite this proposed cut-off, data suggest that it is very difficult to find an absolute range-of-motion cut-off that successfully identifies patients with PNP. ULNT1MEDIAN range of motion at pain onset is highly variable in asymptomatic individuals17,94,95,105 and patients with cervical radiculopathy (FIGURE 4).15 There is also considerable overlap in ULNT1MEDIAN range of motion between these 2 groups. Comparing asymptomatic and cervical radiculopathy data is appropriate, because these studies15,17,94,95,105 used similar methods for applying ULNT1MEDIAN. Range-of-motion variability and overlap highlight the difficulty in distinguishing normal from abnormal range of motion in an individual patient. Measurement error adds to the difficulty in finding an effective absolute range-of-motion cutoff. SDD95 estimates for elbow extension

range of motion at pain onset during ULNT1MEDIAN in asymptomatic17,105 and symptomatic103 individuals range from 14° to 20° (calculated from reported data). In light of the variability and overlap in range of motion for these populations, this amount of measurement error makes it unlikely that an absolute cut-off can accurately discriminate patients with PNP from asymptomatic individuals. It is, therefore, questionable whether an absolute range-of-motion cut-off could be a meaningful criterion for a positive ULNT1MEDIAN. Another strategy for detecting abnormal deficits in ULNT range of motion is to identify a relative cut-off that requires a certain difference in range of motion between the symptomatic and asymptomatic limbs in an individual patient. PNP conditions in which bilateral involvement is common are the exception (eg, more than 50% of individuals with carpal tunnel syndrome have the condition bilaterally10). Despite this exception, no data currently exist on the difference in range of motion between limbs that would normally be expected in as-

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ymptomatic individuals. It is unknown whether a certain difference in range of motion between limbs may discriminate patients with PNP from asymptomatic individuals. In summary, due to the measurement error for resistance to movement and the lack of discriminatory cut-offs for range of motion, current evidence does not support these components of the test response to decide whether a patient’s ULNT is positive. At this time, the suggested criteria for a positive ULNT are (1) at least partial reproduction of the patient’s symptoms and (2) a change in these symptoms with structural differentiation. Reproducing the patient’s symptoms is necessary because asymptomatic individuals report a wide variety of sensations in response to ULNTs. Changing the patient’s symptoms with structural differentiation is necessary to show that these symptoms are at least partly related to increased nerve mechanosensitivity.

RELIABILITY OF A POSITIVE ULNT

T

he next question is whether this definition of a positive ULNT is reliable when used clinically. Most reports of ULNT reliability in asymptomatic 14,17,27,43,48,63,70,74,77,105,126 and symptomatic 17,84,103 populations have focused on measuring range of motion, not whether examiners agreed on a positive test. Four studies assessed reliability for identifying a positive ULNT.9,82,108,110 Only Schmid et al82 required that a positive test reproduce the patient’s symptoms and that structural differentiation change these symptoms. Each ULNT was applied to 31 patients with unilateral arm and/or neck pain that had been present for at least 4 weeks. According to cut-offs proposed by Landis and Koch,59 interexaminer reliability was moderate (κ = 0.41-0.60) for ULNT1MEDIAN, ULNT2MEDIAN, and ULNTRADIAL, and fair (κ = 0.21-0.40) for ULNTULNAR (TABLE 1).82 Kappa values can

Interexaminer Reliability   for a Positive ULNT 82*

TABLE 1 Test

]

Kappa Value (95% CI)

Prevalence Index†

Bias Index†

ULNT1MEDIAN

0.54 (0.19, 0.89)

0.19

0.10

ULNT2MEDIAN

0.46 (0.11, 0.81)‡

0.23

0.06

ULNTRADIAL

0.44 (0.09, 0.79)‡

0.29

0.06

ULNTULNAR

0.36 (0.01, 0.71)‡

0.32

0.10

All ULNTs combined

0.45 (0.27, 0.63)

...

...

Abbreviations: CI, confidence interval; ULNT, upper-limb neurodynamic test. *A positive ULNT required at least partial reproduction of a patient’s symptoms and a change in these symptoms with structural differentiation. † Calculated from original data obtained from Schmid et al,82 according to formulas proposed by Sim and Wright.88 ‡ Confidence interval calculated as 1.96 times reported standard error. The standard error of the kappa value for each ULNT was 0.18.82

be reduced by a high or low proportion of positive tests (prevalence) or inflated by a high level of disagreement between examiners on the proportion of positive tests (bias).88 Prevalence and bias indices88 (calculated from original data obtained from the authors) were low (TABLE 1), indicating that these issues did not affect the kappa values reported by Schmid et al.82 Additional studies are needed to improve the precision of these reliability estimates, because 95% confidence intervals for each ULNT’s kappa value ranged from less than 0.20 to greater than 0.70 (TABLE 1). Nevertheless, clinical tests with fair to moderate reliability can still have sufficient concurrent validity to help make a diagnosis.41,109

CONCURRENT VALIDITY OF ULNTs

E

vidence on the concurrent validity of ULNTs came from diagnostic accuracy studies on cervical radiculopathy110 and carpal tunnel syndrome,104,111 and a case study on cubital tunnel syndrome.85 The methodological quality of the diagnostic accuracy studies was assessed with the Quality Assessment of Diagnostic Accuracy Studies (QUADAS) tool.116,117

Cervical Radiculopathy Wainner and colleagues110 developed a

clinical prediction rule to diagnose cervical radiculopathy from 81 patients referred for electrophysiological testing for suspected cervical radiculopathy or carpal tunnel syndrome. ULNT1MEDIAN and ULNTRADIAL were 2 of several clinical tests considered as potential predictors for the diagnostic prediction rule. Needle electromyography was the reference standard for diagnosing cervical radiculopathy. Only 1 of the following 3 criteria was required for a ULNT to be positive: (1) the ULNT reproduced the patient’s symptoms, (2) the difference between limbs in elbow extension (ULNT1MEDIAN) or wrist flexion (ULNTRADIAL) was greater than 10°, or (3) contralateral neck sidebending increased symptoms or ipsilateral neck sidebending decreased symptoms. The methodological quality of this study was high (11/14 QUADAS items).116,117 The data from Wainner and colleagues110 suggest that ULNT1MEDIAN, but not ULNTRADIAL, may help determine whether a patient has cervical radiculopathy. The negative likelihood ratio (LR) of 0.12 indicated that a negative ULNT1MEDIAN would essentially rule out cervical radiculopathy.51,110 A positive ULNT1MEcombined with positive findings on DIAN the 3 other clinical tests in the diagnostic prediction rule (ipsilateral cervical rotation less than 60°, reduction of symptoms with the supine distraction test,

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TABLE 2 Test

Diagnostic Accuracy of ULNT1 MEDIAN and ULNT RADIAL for Cervical Radiculopathy 110 Sensitivity (95% CI)

Specificity (95% CI)

Positive LR (95% CI)

Negative LR (95% CI)

ULNT1MEDIAN*

0.97 (0.90, 1.00)

0.22 (0.12, 0.33)

1.30 (1.10, 1.50)

0.12 (0.01, 1.90)

ULNTRADIAL*

0.72 (0.52, 0.93)

0.33 (0.21, 0.45)

1.10 (0.77, 1.50)

0.85 (0.37, 1.90)

Diagnostic CPR†‡

0.24 (0.05, 0.43)

0.99 (0.97, 1.00)

30.30 (1.70, 538.20)

...

Abbreviations: CI, confidence interval; CPR, clinical prediction rule; LR, likelihood ratio; ULNT, upper-limb neurodynamic test. *ULNT positive if 1 or more of the following criteria are present: ULNT reproduces the patient’s symptoms, greater than 10° difference between limbs in elbow extension (ULNT1MEDIAN) or wrist flexion (ULNTRADIAL) at the end of the test, contralateral neck sidebending increased symptoms or ipsilateral neck sidebending decreased symptoms when performed at the end position of the ULNT on the symptomatic limb. † All 4 of the following variables are present: positive ULNT1MEDIAN, ipsilateral cervical rotation less than 60°, supine cervical distraction test alleviates symptoms, and ipsilateral Spurling test provokes symptoms. ‡ Negative LR not reported because the focus of the CPR was to identify patients who were most likely to have cervical radiculopathy confirmed by electrophysiological testing.

TABLE 3 Test

Diagnostic Accuracy of ULNT1 MEDIAN and ULNT RADIAL for Carpal Tunnel Syndrome 104,111 Sensitivity (95% CI)

Specificity (95% CI)

Positive LR (95% CI)

ULNT1MEDIAN111*

0.75 (0.58, 0.92)

0.13 (0.04, 0.22)

0.86 (0.67, 1.10)

Negative LR (95% CI) 1.90 (0.72, 5.10)

ULNT1MEDIAN104*

0.92 (0.74, 0.98)

0.15 (0.05, 0.36)

1.08 (0.38, 3.08)

0.56 (0.19, 1.59)

ULNT1MEDIAN104†

0.54 (0.35, 0.72)

0.70 (0.48, 0.85)

1.81 (1.13, 2.88)

0.65 (0.41, 1.04)

ULNTRADIAL111*

0.64 (0.45, 0.83)

0.30 (0.17, 0.42)

0.91 (0.65, 1.30)

1.20 (0.62, 2.40)

Abbreviations: CI, confidence interval; LR, likelihood ratio; ULNT, upper-limb neurodynamic test. *ULNT positive if 1 or more of the following criteria are present: ULNT reproduces the patient’s symptoms, greater than 10° difference between limbs in elbow extension (ULNT1MEDIAN) or wrist flexion (ULNTRADIAL) at the end of the test, contralateral neck sidebending increased symptoms or ipsilateral neck sidebending decreased symptoms when performed at the end position of the ULNT on the symptomatic limb. † Same criteria for a positive ULNT, but symptoms had to be reproduced in the first 3 digits (median nerve distribution).

and provocation of symptoms with the Spurling test) would confirm the presence of cervical radiculopathy (positive LR, 30.30).51,110 These findings should be interpreted cautiously because of the wide 95% confidence intervals (TABLE 2). Additionally, prediction rule performance should be confirmed in a second patient sample before it is considered ready for widespread clinical application.64 ULNTRADIAL does not help detect cervical radiculopathy, because LRs were between 0.5 and 2.0 (TABLE 2).51,110 LRs in this range mean that clinical test results do not lead to important shifts in pretestto-posttest probability of the target condition being present.51

Carpal Tunnel Syndrome Wainner and colleagues111 used the same sample of patients to develop a diagnostic prediction rule for carpal tunnel syndrome. Nerve conduction tests were the reference standard for diagnosing carpal tunnel syndrome, and the aforementioned criteria were used for a positive ULNT. ULNT1MEDIAN and ULNTRADIAL were not considered helpful for either making or ruling out a diagnosis of carpal tunnel syndrome, because LRs for each test were between 0.5 and 2.0 (TABLE 3).51,111 Combining ULNT1MEDIAN or ULNTRADIAL with other clinical tests did not improve diagnostic accuracy, because neither test was included in the di-

agnostic prediction rule for carpal tunnel syndrome.111 The diagnostic accuracy of ULNT1MEfor detecting carpal tunnel syndrome DIAN was also assessed by Vanti et al.104 They studied 44 consecutive patients referred for nerve conduction tests for possible carpal tunnel syndrome. The methodological quality of this study was also high (12/14 QUADAS items).116,117 Two separate analyses were performed that involved slightly different definitions of a positive ULNT1MEDIAN. First, a positive test required the presence of only 1 of the 3 criteria used by Wainner and colleagues.110,111 Second, the “symptom reproduction” criterion was modified so that symptoms had to be reproduced in the first 3 digits of the hand (typical median nerve distribution), but still only 1 of the 3 criteria was required for a positive test. ULNT1MEDIAN was not considered helpful for either making or ruling out a diagnosis of carpal tunnel syndrome with either definition of a positive test, because LRs were between 0.5 and 2.0 (TABLE 3).51,104

Cubital Tunnel Syndrome The only evidence on concurrent validity for ULNTULNAR came from a case study of a patient with suspected cubital tunnel syndrome.85 ULNTULNAR was considered positive because it reproduced the patient’s symptoms and structural differentiation changed these symptoms. Surgical confirmation of ulnar nerve entrapment at the elbow and alleviation of the patient’s forearm and hand symptoms after surgical release confirmed a diagnosis of PNP. A corresponding improvement in the ULNTULNAR response after surgery supported the concurrent validity of this test.85 However, conclusions about the diagnostic accuracy of ULNTULNAR cannot be made from a case study.41

Potential for Bias in Diagnostic Accuracy Studies Despite the high QUADAS scores for the diagnostic accuracy studies on cervical radiculopathy110 and carpal tunnel syn-

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drome,104,111 2 significant methodological concerns make it necessary to carefully interpret diagnostic accuracy findings. The first is the definition of a positive ULNT. Only 1 of 3 criteria—symptom reproduction, a greater-than-10° difference in range of motion between limbs, or a change in symptoms with neck sidebending—was required for a positive ULNT.104,110,111 This is a liberal definition of a positive test. No data support a difference greater than 10° in ULNT range of motion between limbs as able to distinguish symptomatic patients from asymptomatic individuals. More importantly, changing symptoms with structural differentiation (neck sidebending) was not required for a positive ULNT. QUADAS scoring does not address this methodological issue.116,117 It is unclear whether this liberal definition of a positive ULNT influenced diagnostic accuracy because the number of patients with a positive test whose symptoms did not change with structural differentiation was not reported. The second concern is the potential limitation of an electrophysiological reference standard of conduction loss. This reference standard assumes that conduction loss is consistently present in PNP. However, clinical studies of cervical radicular pain89 and carpal tunnel syndrome120 have demonstrated that increased nerve mechanosensitivity may contribute to PNP even when impulse conduction is normal. The pathophysiology of PNP helps explain the potential discrepancy between increased nerve mechanosensitivity and electrophysiological evidence of conduction loss. Increased mechanosensitivity is related to increased excitability of small-diameter afferents,6,11,31,37 central nervous system pathways,6 and nociceptors in the nervi nervorum and sinu-vertebral nerves that innervate the nervous system’s connective tissues.4,53,81 These pathophysiological changes cannot be detected by electrophysiological tests that focus on damage or conduction loss in large-diameter fibers.60 Consequently, patients with PNP who present with in-

creased nerve mechanosensitivity rather than conduction loss may often be incorrectly classified by needle electromyography and nerve conduction tests as not having PNP. This potential misclassification of patients with PNP might have biased estimates of the diagnostic accuracy of ULNT1MEDIAN and ULNTRADIAL.78

ultrasound imaging on its own is positive in an individual patient can be difficult.40,44 Therefore, more work is needed to develop composite reference standards for different PNP conditions. When an ideal reference standard for a diagnostic label is unavailable, research on predictive validity for prognosis or treatment response provides alternative information on how ULNT results can be used clinically.41,78 Raney et al76 provided this type of information on ULNT1MEDI. They developed a clinical prediction AN rule to identify patients with neck pain who will improve after cervical traction and exercise. The reference standard was whether a patient reported being at least “a great deal better” after 6 treatments. A positive ULNT1MEDIAN was retained as 1 of 5 variables in the rule. A positive test reproduced the patient’s symptoms, and neck sidebending changed these symptoms. Further studies are needed to determine whether this rule may predict a preferential response to cervical traction and exercise, or whether patients who are positive on the rule may respond equally well to other interventions.46 Researchers should continue investigating the predictive validity of ULNTs.

Alternate Strategies for a Reference Standard The potential incorrect classification of patients with PNP who present with increased nerve mechanosensitivity rather than conduction loss suggests that an electrophysiological reference standard of conduction loss may not be comprehensive enough to judge the diagnostic accuracy of clinical tests of nerve mechanosensitivity.113 One way to address this problem is to create a composite reference standard by combining needle electromyography and nerve conduction tests with other tests.78 Quantitative sensory testing can assess the function of smalldiameter afferents and provide evidence of sensory hypersensitivity.44,79 Magnetic resonance neurography34 and ultrasound imaging7,40 can identify signs of nerve irritation and nerve thickening. Therefore, quantitative sensory testing, magnetic resonance neurography, or ultrasound imaging might be options for a composite reference standard for various PNP conditions. The composite reference standard approach has its own methodological challenges. The combination(s) of test results necessary to conclude that the target condition is present must be determined in advance.78 For example, Beekman et al8 assessed the diagnostic accuracy of provocation tests for ulnar neuropathy at the elbow with a reference standard of positive electrophysiological findings or evidence of nerve thickening on ultrasound imaging. Identifying these combinations also requires that each test within the composite reference standard be labeled as positive or negative in an individual patient. However, deciding whether quantitative sensory testing or

]

CONCLUSION

T

he available evidence was reviewed to assess the validity of using ULNTs to detect PNP conditions such as cervical radiculopathy, carpal tunnel syndrome, and cubital tunnel syndrome. Aspects of validity that were assessed included plausibility, the definition of a positive test, reliability, and concurrent validity (diagnostic accuracy). ULNTs are plausible tests for detecting PNP. A positive ULNT should at least partially reproduce the patient’s symptoms, and structural differentiation should change these symptoms. This definition of a positive ULNT is reliable when used clinically. However, concurrent validity studies need to determine whether this specific definition of a positive test may improve the diagnostic ac-

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curacy of ULNTs. The minimal evidence available prevents any definitive statements about the diagnostic accuracy of ULNTs for detecting PNP. Evidence shows that, when using a liberal definition of a positive test, ULNT1MEDIAN, but not ULNTRADIAL, can help determine whether a patient has cervical radiculopathy. When using similar criteria, ULNT1MEDIAN does not help diagnose carpal tunnel syndrome. Contrasting results in the diagnostic accuracy of ULNT1MEDIAN for detecting cervical radiculopathy and carpal tunnel syndrome suggest that diagnostic accuracy of the same ULNT may be different for different PNP conditions. Diagnostic accuracy findings should be interpreted cautiously, because results may be distorted by the liberal definition of a positive test. Furthermore, patients with PNP who presented with increased nerve mechanosensitivity rather than conduction loss might have been incorrectly classified by electrophysiological reference standards as not having PNP. Researchers should try to develop more comprehensive reference standards for PNP to accurately assess the concurrent validity of ULNTs and continue investigating whether ULNTs have predictive validity for prognosis or treatment response. t

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Nerve Testing - Detecting Upper Extremity Peripheral Neuropathic Pain