Introduction
Neurodynamic maneuvers are clinical evaluation tools and part of manual therapy. They are used in various patients with disorders of the neuromuscular system [
1, 2, 3]. Nerve problems can result from an extraneural (e.g. narrowing of the nerve context due to pressure caused by edema) or intraneural (e.g. following diabetes) pathology [
4, 5, 6, 7].
Neurodynamic tests in the lower and upper limbs are used in clinical evaluations of a wide range of patients to examine the mechanical sensitivity of the nerve. Positive responses to these tests usually appear as sensory perceptions, like changes in pain or paresthesia [
8, 9, 10]. Of course, it should be noted that pain and sensory manifestations in response to neurodynamic tests can be seen both in patients with musculoskeletal problems [
7,
11, 12] and in healthy people [
13, 14, 15], and it is not always easy to determine whether the response to the test is normal or abnormal [
8,
16, 17]. This reason shows why recent studies have investigated the validity of these techniques [
18].
There are four neurodynamic tests in the upper limb [
1]. Kleinrensink and his colleagues showed that median, radial, and ulnar nerve tension is more sensitive than other upper limb neurodynamic tests [
7]. Hines and his colleagues found a low reproducibility between testers in the first resistance in performing the neurodynamic test [
19]. Coppieters and colleagues showed strong intra-tester and inter-tester reproducibility in asymptomatic subjects and patients in one session [
20]. In another study, Leoni and colleagues found that measuring the range between the moment of pain onset and submaximal pain has a higher reproducibility than the moment of pain onset and submaximal pain during neurodynamic evaluation [
21].
A limited number of studies have examined the reproducibility of neurodynamic tests of the upper limb, and most of these studies have examined the reproducibility of the median nerve [
14,
21, 22, 23]. There is little information about the reproducibility of the radial and ulnar nerves. In addition, there is no single method for measuring joint angles in radial and ulnar nerve examination [
24, 25, 26, 27]. Little information and the lack of a single measurement method cannot be a good criterion for review studies on the reproducibility of the radial and ulnar nerves [
24, 25, 26,
28]. Therefore, this study investigates the reproducibility of upper limb neurodynamic tests, including the median, radial, and ulnar nerves, using a simple and clinical tool to measure the joint range of motion (mechanical goniometer). If these tests have good reproducibility, they can be used as a diagnostic method for evaluating therapeutic effects in patients with neurodynamic disorders.
Materials and Methods
This cross-sectional study was observational, and study samples were collected by a simple, non-random method. A total of 25 asymptomatic people (9 women, 16 men) participated in this study. This study was conducted from February 7, 2020, to April 21, 2021, at the physiotherapy clinic of Shahid Beheshti Hospital in Babol City, Iran.
The inclusion criteria included people aged 19 to 45 years with a full and pain-free range of motion in the separate assessment of upper limb joints. The exclusion criteria include a history of the following problems or diseases: neck and upper limb pain in the past 6 months, upper limb surgery, chemotherapy or radiation therapy, diabetes, cognitive disorders, fractures of the upper limb, infection, neck radiculopathy, and peripheral neuropathies of the upper limb and other diseases of the nervous system [
14,
21,
29].
The evaluation team consisted of two physiotherapists with at least 5 years of experience in the field of manual therapy and nerve mobilization. They were named tester 1 (E1) and tester 2 (E2). The reproducibility of upper limb neurodynamic tests was investigated in one intra-session and two inter-sessions. In the first session, tester 1 and then tester 2 repeated each test twice. There was a 1-minute rest period between each repetition of each test. In the second session and after 24 hours, at first, tester 2 and then tester 1 repeated each test once. The tests were conducted in the second session, similar to the first session.
The neurodynamic evaluation was performed using the standard method provided by Butler and Shacklock for the median (
Figure 1), radial (
Figure 2), and ulnar (
Figure 3) nerves bilaterally for both upper limbs [
4,
30].
Randomization was performed to select the evaluated side. Sealed envelopes were used for this purpose. Before starting the neurodynamic assessment, the participants were instructed to report the moment of onset of pain and submaximal pain in the relevant area (sensory distribution area of the relevant nerve) by saying the words "now" and "stop" during the assessment. In assessing the median nerve, the target area for reporting pain was the anterior forearm, wrist, and fingers. In evaluating the radial nerve, the target area for reporting pain was the outside of the elbow and forearm and the back of the wrist and fingers. In assessing the ulnar nerve, this area was the inside the elbow and forearm [
30]. During the assessment, the moment of pain onset was considered when the minimal painful stretch was felt, and the moment of submaximal pain was when the painful stretch increased and became clear, and the participant wanted to stop the assessment [
15]. If the participants did not report submaximal pain during the available range of motion or if they had sensory manifestations, such as tingling, they would be excluded from the study.
Joint angles were measured using a standard goniometer according to the method of Covill and Martinez (
Figures 4,
5, and
6) [
24,
31].
During the evaluation, the testers were unaware of each other's test results and joint angles. In the evaluation of the median and radial nerves, the extension angle of the elbow joint, the evaluation of the ulnar nerve, and the abduction angle of the shoulder joint were the measurement criteria.
Data collection
In this study, the range between the moment of pain onset and submaximal pain was measured and reported. This range was shown as R1E1MN, R2E1MN, and R3E1MN for tester 1 and the median nerve, which indicated the first and second repetition of the test in the first session and the repetition of the test in the second session, respectively.
Statistical analysis
Data were analyzed using SPSS software v.26. To determine the relative repeatability, the intraclass correlation coefficient-test (ICC) and 95% confidence interval (95% CI) were used [
32]. To find out the absence of systematic bias, a paired t-test was used in the pre- and post-measurement of each tester, and an independent binomial t-test was used to compare the two testers. P˂0.05 was considered significant for all analyses. The average repetitions of each test by the testers in the first session and the average of the same test in the second session were used to calculate intra-tester reproducibility. To calculate the reproducibility of inter-testers in one session, the average repetitions of each test were used by tester 1 and tester 2 in the first session, and to calculate the reproducibility of intra-tester in two sessions, the average repetitions of each test by tester 1 was used in the first session, and the average repetitions of the same test by tester 2 were used in the second session [
20,
22]. To check the absolute reproducibility of the standard error of measurement, it was calculated based on a function of sharing the standard deviation of groups and ICC (SEM=SDPooled×√(1-ICC)) [
33].
Results
Table 1 presents the characteristics and demographic information of the participants, and
Table 2 presents the mean and range of the measurements.
After randomization in selecting the evaluated side, it was evaluated in 14 right-handed and 11 left-handed participants.
The reproducibility values of the inter-tester 1 were 0.94 for the median nerve (P=0.942, 95% CI: 0.88-0.97: 95%) with a standard error of measurement of 2˚, 0.56 for the radial nerve (P=0.784, 95% CI: 0.78-0.22) with a standard error of measurement of 6.36˚, and 0.42 the ulnar nerve (P=0.355, 95% CI: 0.69-0.04) with a standard error of measurement 3.27˚. These values were calculated for tester 2 as 0.89 for median nerve (P=0.98, 95% CI: 0.78-0.95), 0.93 for radial nerve (P=0.056, 95% CI: 0.96-0.84), and 0.79 for the ulnar nerve (P=0.359, 95% CI: 0.9-0.57) with standard errors of measurements of 2.85˚, 1.82˚, and 1.42˚, respectively. In addition to the reproducibility between the average values of the first and second day, the reproducibility between two evaluations (with an interval of one minute) has been calculated. The results were 0.94 and 0.96 for the median nerve (E1 and E2, respectively), with standard errors of measurements of 2.05 and 1.78; 0.83 and 0.94 for the radial nerve, with standard errors of measurements of 4.61 and 1.69; and 0.87 and 0.7 for the ulnar nerve, with standard errors of measurements of 1.8 and 1.86. The results of the paired t-test showed no statistically significant difference between the average measurements of tester 1 and tester 2 for the median, radial, and ulnar nerves.
Reproducibility rates between two testers in one session were 0.84 for median nerve (P=0.942, 95% CI: 0.93-0.68), 0.54 for radial nerve (P=0.415, 95% CI: 0.77-0.2), and 0.55 for the ulnar nerve (P=0.626, 95% CI: 0.2-0.77) with standard errors of measurements of 3.44˚, 6.1˚, and 2.75˚, respectively. The reproducibility rates between two testers in two sessions were 0.97 for median nerve (P=0.933, 95% CI: 0.93-0.98, 0.97), 0.69 for radial nerve (P=0.683, 95% CI: 0.41-0.85), and 0.51 for the ulnar nerve (P=0.412, 95% CI: 0.15-0.75), respectively with standard errors of measurements of 1.43˚, 5.06˚ and 2.8˚. According to the independent binomial t-test results, no statistically significant difference was observed between the average measurements between the two testers for the median, radial, and ulnar nerves.
Discussion
In the evaluations conducted by two testers, no significant difference was found between the average measurements of elbow joint extension angle and shoulder joint abduction in one session and between two sessions. The reproducibility of neurodynamic tests of median, radial, and ulnar nerves was investigated in one session and between two sessions as intra-tester and inter-testers. To interpret the ICC in this study, Coppieters et al.’s criteria were used [
20]. ICC less than 0.4 was considered poor, between 0.4 and 0.69 fair, between 0.7 and 0.89 good, and more than 0.9 excellent reproducibility.
The results showed moderate to excellent inter-examiner reproducibility in all three nerves; however, the median nerve has higher reproducibility than the other two nerves. In examining the reproducibility between two testers in one session, the highest reproducibility was obtained for the median, then ulnar and radial nerves, respectively. Similar to the findings of Leoni et al., in the present study, the reproducibility of the neurodynamic test of the median nerve increased between two sessions compared to one session [
21]. The slight improvement in reproducibility can be attributed to better coordination and cooperation between the tester and the participant during the implementation of the neurodynamic test.
Based on the study findings, the reproducibility of the median nerve neurodynamic test was higher than the radial and ulnar nerves; this finding is consistent with the results of previous studies that reported the highest reproducibility of the median nerve test among upper limb neurodynamic tests [
7,
34, 35], which may be due to the more specific and easier implementation and control of the sequence of this test compared to the radial and ulnar nerve tests [
7]. The sequence of the median nerve neurodynamic test is similar to the activities of the upper limbs of people in daily activities; also, therapists often use this test in evaluation and treatment and are more skilled in its implementation.
The lower reproducibility of the radial and ulnar nerves between two testers may be due to the participants’ lack of familiarity with the test sequence of the radial and ulnar nerves. In other words, these test sequences are not usually used in daily activities compared to the median nerve. Alternatively, the sequence of these tests is more difficult, for example, due to the difference in the amount of depression force applied on the shoulder belt by the testers. These factors cause the intrinsic changes of the radial and ulnar nerves to be higher than the median nerve. Also, if the shoulder girdle goes into protraction in the ulnar nerve test during the flexion phase of the elbow joint, it can affect the test result. Reproducibility of the radial and ulnar nerve test is probably related to the experience and clinical skill of the testers; recent studies have shown that the reproducibility rate is slightly higher for experienced testers [
14,
29]. Measurement of the abduction angle of the shoulder joint is another factor that can contribute to the low reproducibility of the ulnar nerve test because it is more difficult to place and keep the goniometer on the shoulder joint during evaluation than on the elbow joint. However, the reproducibility of the ulnar nerve was moderate between the two testers. The present study’s findings showed that similar to the results of Pithak and Reisch’s study [
29,
36], in examining the reproducibility of the nerves of the upper limbs, the measurement of the elbow joint extension angle and shoulder joint abduction has moderate to excellent reproducibility.
The standard error of measurement is usually used to calculate the error related to repeated measurements [
37, 38, 39]. In other words, by using the standard error of measurement, the very range is determined that is expected to be in the actual score of people by considering the amount of error associated with repeated measurements [
40]. The smaller the measurement standard error, the higher the absolute reproducibility and the more stable the measurement [
39].
The standard error of measurement of the intra-tester for the median nerve was calculated as 2° and 2.85°, which is similar to the results of the study by Talebi and Coppieters [
20,
22]. Contrary to the findings of Coppieters et al., in the present study, the standard error of measurement between two testers for the median nerve calculated in one session was more than that in two sessions [
20]. The standard error of measurement for the median nerve test was lower than other nerves, which shows that the median nerve neurodynamic test is more stable. As far as we know, the standard errors of measurements for radial and ulnar nerve neurodynamic tests have not been reported in previous studies; therefore, comparing the obtained results with other studies is impossible.
Similar to the findings of Leoni et al., the results of this study show that the moment of occurrence of pain and submaximal pain has good reproducibility, but the range between them has higher reproducibility [
21]. In addition, the standard error of measurement for these two points is greater than the range between them. The results of this study show that the reproducibility and standard error of measurement for neurodynamic tests of the median, radial, and ulnar nerves are acceptable; therefore, we can use the neurodynamic tests, with confidence in the reproducibility of the aforementioned measurement method, for initial evaluation as well as checking the effects of treatment in patients with suspected neurological disorders.
Study limitations
Due to the COVID-19 pandemic, some samples were excluded from the study and the sampling period lasted longer than usual. Another limitation of this study was the small and constant consideration of rest time between the repetitions of tests. According to the possible effect of repeating the test and creating a therapeutic effect on the results of subsequent repetitions, it is suggested to increase the rest time.
Suggestions for future research
It is suggested that in future studies, the sample size be increased, and people with symptoms, such as musculoskeletal pain syndromes, undergo neurodynamic evaluations to clarify the role and contribution of neurological disorders in the development of symptoms in these patients.
Ethical Considerations
Compliance with ethical guidelines
This study was approved by the Ethics Committee of Babol University of Medical Sciences (Code: IR.MUBABOL.REC.1400.063). The participants were given the permission to cancel their participation at any stage of study. All participants were aware of the research process. Their information was kept confidential.
Funding
The paper was extracted from the MSc. thesis of the first author in Department of Physiotherapy, Babol University of Medical Sciences, Babol, Iran. Also, this study was supported of Vice President of Research and Technology of Babol University of Medical Sciences.
Authors' contributions
Conceptualization: Milad Taheri, Ghadamali Talebi, Mohammad Taghipour; Methodology and validation: Milad Taheri, Ghadamali Talebi, Mohammad Taghipour, Massoud Bahrami; Analysis and research: All authors; writing-original draft: Milad Taheri; Editing and finalization: Ghadamali Talebi, Mohammad Taghipour; Funding and resources: Vice President of Research and Technology Babol University of Medical Sciences.
Conflict of interest
The authors declared no conflict of interest.
Acknowledgments
The authors express their gratitude from the research participants and physiotherapy department staff of Shahid Beheshti hospital, specially physiotherapist Mahdi Hosseinpour. The authors are also grateful for assistance and support of Vice President of Research and Technology of Babol University of Medical Sciences.
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