Motor Control, 2014, 18, 395-404 http://dx.doi.org/10.1123/mc.2013-0067 © 2014 Human Kinetics, Inc.

Acute Experimentally Induced Neck Pain Does Not Affect Fatigability of the Peripheral Biceps Brachii Muscle Laurie Y. Hung, Emmalee Maracle, John Z. Srbely, and Stephen H.M. Brown Evidence has shown that upper limb muscles peripheral to the cervical spine, such as the biceps brachii, can demonstrate functional deficits in the presence of chronic neck pain. However, few studies have examined how neck pain can affect the fatigability of upper limb muscles; therefore we were motivated to investigate the effects of acutely induced neuropathic neck pain on the fatigability of the biceps brachii muscle during isometric contraction to exhaustion. Topical capsaicin was used to induce neck pain in 11 healthy male participants. Surface EMG signals were recorded from the biceps brachii during an isometric elbow flexion fatigue task in which participants held a weight equivalent to 30% of their MVC until exhaustion. Two experimental sessions, one placebo and one capsaicin, were conducted separated by two days. EMG mean power frequency and average normalized activation values were calculated over the course of the fatigue task. In the presence of pain, there was no statistically significant effect on EMG parameters during fatigue of the biceps brachii. These results demonstrate that acutely induced neuropathic neck pain does not affect the fatigability, under the tested conditions, of the biceps brachii. Keywords: neck pain, cervical spine, muscle fatigue, capsaicin, electromyography, chronic pain

Neck pain affects 30–50% of people within a given calendar year, depending on the country of residence (Hogg-Johnson et al., 2008), and as a chronic disability in the United States ranks second only to low back pain (Wright, Mayer, & Gatchel, 1999). The chronic form of neck pain has been associated with a number of differences in the morphology and functional characteristics of neck muscles (e.g., Gogia & Sabbahi, 1994; Falla, Rainoldi, Merletti, & Jull, 2003; Falla, Jull, Rainoldi, & Merletti, 2004; Johnston, Jull, Souvlis, & Jimmieson, 2008; Elliott, 2011). While differentiation in neck muscle function in comparison with healthy controls have been clearly established, other research has also suggested that chronic neck pain can affect peripheral muscles in the upper limb. Suter and McMorland (2002) The authors are with the Dept. of Human Health and Nutritional Sciences, University of Guelph, Guelph, Canada. Address author correspondence to Stephen H.M. Brown at [email protected].   395

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demonstrated distinct force-generating inhibition of the biceps brachii muscle in patients diagnosed with chronic neck pain. This inhibition was eliminated immediately following directed manipulation to the cervical spine, suggesting a potential neuropathic mechanism for the altered biceps brachii function. Further evidence of a relationship between chronic neck pain and biceps brachii functional characteristics is provided by Lundblad, Elert, and Gerdle (1998). They demonstrated that the fatigue characteristics of the biceps brachii muscle, as quantified with the measure of electromyographic (EMG) mean power frequency (MPF), helped explain some variance in predicting which patients would improve neck pain scores over time. Specifically, they found that individuals who display greater drops in MPF in the biceps brachii and other shoulder region muscles are more likely to show improvements in neck pain over time. This suggests that studying the activation profile of biceps brachii may provide insight into early onset of neck pain disorders, and/or may be used to help predict patient recovery over time. Increased fatiguability of neck muscles, as characterized by greater reductions in EMG MPF during fatigue tests, has been observed in patients with chronic neck pain compared with healthy individuals (Gogia & Sabbahi, 1994; Falla et al., 2003; Falla et al., 2004). Falla et al. (2003) hypothesized that this increased fatigability was related to the changing of muscle fiber types in the chronic pain patients toward faster-twitch type II (Uhlig et al., 1995). Interestingly, Lundblad et al. (1998) examined a group of patients suffering from chronic neck pain and found that a greater reduction in MPF of the trapezius muscle during a dynamic fatiguing protocol predicted greater improvements in neck pain one year later. They suggested, based on their EMG findings, the possibility that patients who did not improve pain scores over time did not demonstrate the normal changing of fiber types toward type II, and instead maintained a high proportion of type I fibers. These studies suggest that chronic pathological changes to muscle morphology may contribute to the altered fatigability of neck muscles in patients suffering from neck pain. Research investigating the effects of acute experimental pain on muscle function is equivocal. Investigations using acute experimental pain models have been able to replicate muscle functional deficits, thought mainly to be of neuro-adaptive origin, which are seen in chronic pain conditions (e.g., Zedka et al., 1999; Hodges et al., 2003; Farina et al., 2004; Falla et al., 2007). In contrast, acute experimental neck muscle pain was not able to demonstrate any changes in the fatigue characteristics of neck muscles that have been reported in the chronic pain literature (Falla et al., 2008). Recent studies have demonstrated altered motor unit recruitment in the presence of experimentally induced acute pain (Tucker et al., 2009; Jegatheeswaran, 2011; Tucker et al., 2012) and, similarly, even in the anticipation of pain (Tucker et al., 2012). Interestingly, Jegatheeswaran (2011) demonstrated altered motor unit recruitment during low level (20% MVC) nonfatiguing contractions in the first dorsal interosseous, peripheral to the site of pain in the cervical region, using the topical application of capsaicin. Thus, we were interested in the question of whether similar motor changes occur in larger muscle groups (biceps brachii) and under more demanding physiological conditions (fatiguing contraction). This would potentially provide a mechanism to induce functionally relevant changes to motor unit fatiguing properties that could approximate those seen in clinical conditions. The purpose of this study was to investigate the effects of acutely induced neuropathic neck pain on the fatigability of the biceps brachii muscle during

Biceps Brachii Fatigue  397

isometric contraction to exhaustion. The biceps brachii muscle is innervated by the musculocutaneous nerve (originates from the C5–6 nerve roots), therefore we hypothesized that inducing pain via a neuropathic mechanism in the neck region would increase the apparent fatigability (e.g., decrease time to fatigue, increase slope of EMG mean power frequency drop) of this muscle.

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Participants 11 volunteers (males) participated in the study after providing informed consent. Participants (aged 18–24 years) did not have any current neck or upper limb pain or injuries, and had no history of neurological disorders. Participants were not currently experiencing any bodily pain (e.g., lower limbs, lower back), and did not perform any strength training of the upper limbs 72 hr before or in between test days. Testing occurred for each participant on two separate days, separated by 48 hr; all experimental procedures were identical on each day except the application of either capsaicin or placebo topical cream was randomized between days. A flowchart detailing a summary of the experimental protocol is found in Figure 1. This study was approved by the University of Guelph Research Ethics Board (ethics certificate number: 11JL027).

Electromyography Upon arrival in the laboratory, the participants’ skin was prepared by gentle cleaning with rubbing alcohol. Next, bipolar Ag/AgCl adhesive surface EMG electrodes were

Figure 1 — Flowchart providing a summary of the experimental protocol followed on each of the two testing days. Details of each of the stages can be found in the text.

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placed over the right biceps brachii and triceps brachii muscles with an approximate 3 cm interelectrode distance, and oriented parallel to the direction of the muscle fibers. Biceps brachii was assessed as the primary muscle of interest (generating the agonist moment at the elbow joint) and the triceps brachii was assessed as a cocontracting partner (generating the antagonist moment at the elbow joint). This was done to account for the possibility that sources other than neck pain, namely changes in the antagonistic activation of the triceps muscle, could affect biceps fatigability. Myoelectric signals were amplified with a gain of 1000–1500 (AMT-8, Bortec Biomedical, Calgary AB; bandwidth 10–1000 Hz; CMRR = 115 dB at 90 Hz; input impedance = 10 GW), sampled at 2048 Hz, and digitally converted via a 14 bit analog to digital converter.

Maximum Voluntary Contractions Maximum voluntary contractions (MVCs) were collected from the right biceps brachii and triceps brachii muscles. For each contraction, participants were instructed to gradually ramp up force until they reached their absolute maximum, hold it for 2–3 s, and then gradually relax. At baseline, three of each of biceps and triceps contractions were performed, and approximately 3 min of rest were given between each MVC. For the biceps muscle, participants were seated with the shoulder in a neutral posture and the elbow flexed to 90 degrees, and produced a maximum isometric elbow flexion contraction while holding onto a handle attached to a Vernier force plate (Vernier Software & Technology, Beaverton, OR) mounted on the underside of a solid laboratory bench. Force was sampled at 100 Hz. Thirty percent of the maximum steady-state force was used to establish the fatiguing biceps load. Two additional biceps MVC contractions were performed, the first immediately before the fatigue trial and the second immediately after the fatigue trial. For the triceps muscle, participants stood with the shoulder in a neutral position, the elbow flexed to 90 degrees and the forearm supinated, and produced a maximum isometric elbow extension effort against manual resistance. Participants were given verbal encouragement to generate maximal effort during the MVC trials.

Experimental Neck Pain Experimental cervical spine pain was induced by the application of topical capsaicin (Zostrix, 0.025%; Hi-Tech Pharmacal, Amityville, NY) to an area defined by the hairline superiorly, the sternocleidomastoid muscle laterally, and a transverse line transecting the acromioclavicular joints bilaterally. A thick layer of capsaicin or placebo cream (depending on the day) was applied to the defined area and rubbed in until visually absorbed. The use of topical capsaicin to induce pain has been demonstrated previously (Petersen et al., 2000; Governo et al., 2006; Srbely et al., 2010; Martucci et al., 2012). Herbacin hand cream (REHA Enterprises Ltd., Mississauga ON) was used as a control cream. Before cream application, the skin over the defined area was heated for 10 min with wet hot towels (40 °C, towels changed every minute). Cream application (capsaicin or placebo) was randomized for each experimental session and participants were blinded to the creams. Participants were told that one or both of the creams might cause some discomfort or pain. Participants were asked to rate their pain on a 10 cm visual analog scale (VAS). Pain ratings were obtained at baseline, and at 3, 5, and 9 min post cream application.

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Fatigue Protocol Ten minutes posttopical cream application, a biceps brachii fatigue trial was conducted. To fatigue the biceps muscle, participants stood upright with the shoulder in a neutral position and the right elbow in 90 degrees of flexion. Participants held a weight that represented 30% of their mean biceps brachii (elbow flexion) MVC force value. Participants held this isometric contraction until exhaustion (fatigue), which was deemed to occur when they felt they could no longer maintain the contraction, or when the experimenters deemed by visual estimation that the participant could no longer maintain the intended 90 degrees of elbow flexion. Participants were given verbal encouragement, and cuing to maintain the proper positioning, throughout the fatigue trial. Immediately following the completion of the fatigue trial participants completed a Borg CR-10 rating of perceived exertion scale.

Data Analysis To analyze muscle activation levels, EMG signals were full-wave rectified and low pass filtered (Butterworth 2nd order 2.5 Hz). These signals were normalized to the maximum obtained during the baseline MVC trials. Average biceps and triceps normalized activation levels, and biceps mean power frequency (MPF; calculated from the raw data) were calculated over 4 s windows every 20 s (16 s in between each window) to quantify fatigue over the course of the entire fatigue trial. If the end of the trial (exhaustion) did not occur at the end of one of these windows, a final window was calculated over the final 4 s of the trial. MPF was plotted over all time points and a linear slope was calculated. Percent changes in MPF and activation level, between the first and last 4 s window were also calculated. Percent change in force output between the prefatigue and postfatigue biceps MVC trial was also calculated. Dependent variables were compared between capsaicin and placebo days using paired t tests. Significance was set at p < .05.

Results Fatigue Assessment No statistically significant effects of capsaicin were found for any of the biceps brachii fatigue variables (Table 1). MPF decreased by 37% and 35%, and force output by 34% and 25%, in capsaicin and placebo conditions respectively, indicating that similar magnitudes of fatigue occurred under both conditions. Endurance times (245 s and 239 s for capsaicin and placebo, respectively) were also similar, and ratings of perceived exertion, as indicated by the Borg CR-10 scale, were identical under the two conditions (9.2 for both capsaicin and placebo).

Activation Strategies No statistically significant effects of capsaicin on biceps brachii, nor triceps brachii, activation strategies were uncovered during fatigue (Table 2).

Perceived Pain and Sensitivity Visual analog pain scores were statistically different (p < .0001) between the capsaicin (VAS = 4.4 cm) and placebo (VAS = 0.3 cm) conditions (Table 3).

Table 1  Mean (SD) of Variables Used to Assess Fatigue of the Biceps Brachii for Both the Capsaicin and Placebo Cream Conditions

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Capsaicin Mean (SD)

Placebo Mean (SD)

P

MPF change (%)

–37.2 (12.7)

–34.6 (13.5)

.12

MPF slope (%/sec)

–0.13 (0.14)

–0.15 (0.11)

.55

Endurance time (sec)

245.4 (100.3)

239.3 (104.1)

.56

Force change (%)

–33.9 (16.4)

–25.1 (10.7)

.19

RPE (Borg CR-10)

9.2 (0.6)

9.2 (0.7)

.93

Note. RPE = rating of perceived exertion.

Table 2  Mean (SD) of Variables Associated with Biceps Brachii and Triceps Brachii Activation Strategies During the Biceps Fatigue Protocol for Both the Capsaicin and Placebo Cream Conditions Capsaicin Mean (SD)

Placebo Mean (SD)

P

Initial biceps MPF (Hz)

93.2 (14.9)

91.3 (16)

.59

Biceps activation change (%)

166.3 (118.6)

169.1 (145.6)

.95

Initial normalized biceps AL (%MVC)

12.8 (2.5)

12.9 (3.8)

.90

Triceps activation change (%)

47.0 (97.1)

51.5 (87.0)

.70

Initial normalized triceps AL (%MVC)

8.6 (3.7)

9.7 (2.7)

.33

Note. AL = activation level.

Table 3  Mean (SD) Visual Analog Pain Scores at Baseline, 3 Min, 5 Min and 9 Min Post Cream Application. Bolded P-Values Indicate Statistical Significant Differences Between the Capsaicin and Placebo Cream Conditions Capsaicin Mean (SD)

Placebo Mean (SD)

P

VAS at baseline (cm)

0.3 (0.6)

0.2 (0.4)

.09

VAS at 3 min post (cm)

3.2 (1.2)

0.3 (0.5)

< .0001

VAS at 5 min post (cm)

4.1 (1.2)

0.3 (0.5)

< .0001

VAS at 9 min post (cm)

4.4 (1.1)

0.3 (0.5)

Acute experimentally induced neck pain does not affect fatigability of the peripheral biceps brachii muscle.

Evidence has shown that upper limb muscles peripheral to the cervical spine, such as the biceps brachii, can demonstrate functional deficits in the pr...
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