The effect of muscle fatigue on wrist joint position sense in healthy adults

Journal of Hand Therapy xxx (2019) 1e9

Contents lists available at ScienceDirect

Journal of Hand Therapy journal homepage: www.jhandtherapy.org

The effect of muscle fatigue on wrist joint position sense in healthy adults Christos Karagiannopoulos MPT, PhD, ATC, CHT *, Jessica Watson PT, DPT, Sarah Kahan PT, DPT, Danielle Lawler PT, DPT DeSales University, Doctor of Physical Therapy Program, Center Valley, PA, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 9 May 2018 Received in revised form 4 March 2019 Accepted 4 March 2019 Available online xxx

Study design: Pretest and posttest experimental study. Introduction: The effect of muscle fatigue on wrist joint position sense (JPS) has yet to be determined. Purpose of the Study: The primary aim was to determine whether muscle fatigue affects wrist JPS in healthy adults. The secondary aims were to compare the effect of muscle fatigue on younger and older adults JPS and determine the association between JPS rate of change and total muscle fatigue (TMF) rates postexercise. Methods: Forty male and female healthy adults were assigned into younger (18-40 years) and older (4165 years) groups. Preexercise and postexercise testing consisted of active wrist JPS, handgrip, and wrist extensor strength assessments. Muscle fatigue was induced via a calibrated gripper and wrist extension dumbbell exercises. Dependent variables were the JPS rate of change (ie, preexercise and postexercise), TMF rate (ie, grip and wrist extension average strength decline), and Borg Rating of Perceived Exertion scale scores. Results: Postexercise wrist JPS test scores were significantly higher than preexercise. Exercises induced statistically significant TMF rates and Borg Rating of Perceived Exertion scores among all participants. No statistically significant age-group differences on JPS rate of change, and TMF rate was found. A statistically significant mild correlation (r ¼ 0.425) existed between JPS rate of change and TMF rates. Discussion: Postexercise fatigue significantly impairs wrist JPS in both younger and older adults. On average, an 18% muscle strength decline led to 215% wrist JPS deficit. Conclusions: Significant wrist proprioception deficits persist for 5 min following exertional exercises, regardless of age level. Ó 2019 Hanley & Belfus, an imprint of Elsevier Inc. All rights reserved.

Keywords: Muscle fatigue Wrist JPS deficit Healthy Adults

Introduction The sensorimotor (SM) control system provides the fundamental basis for human body kinesis.1,2 Its function relies on continuous influx of afferent proprioceptive input, which is integrated within the central nervous system to regulate limb motion recognition, and joint neuromuscular control.2-5 The unconscious SM control sense regulates reflexive neuromuscular responses toward joint dynamic control.3,6 Its function depends on an intact conscious SM control sense,4,6 which provides the body with a

Conflictn of interest: All named authors hereby declare no financial involvement or conflict of interest with the subject of matter presented in this research manuscript. * Corresponding authorDeSales University, Doctor of Physical Therapy Program, 2755 Station Avenue, Center Valley, PA 18034-9568, USA. Tel.: þ1 610 282 1100; fax: þ1 610 282 2663. E-mail address: [email protected] (C. Karagiannopoulos).

distinct ability to recognize joint position (ie, joint position sense [JPS]) via input from skin and muscle mechanoreceptors.2,6 Muscle spindle, the primary regulatory mechanoreceptor for JPS,6-8 is vulnerable to muscle fatigue,9-11 leading to decreased JPS following rigorous activity. The critical role of JPS on proper wrist joint dynamic control and function has been recently recognized in the literature.12-14 Wrist JPS deficit has been determined to be a clinically meaningful indicator for functional impairment following distal radius fracture, regardless of age and hand dominance.12 Wrist JPS deficit can be measured via the active wrist JPS test, which psychometric properties have been established in terms of reliability and responsiveness levels among healthy adults and patients with distal radius fracture.12,15,16 Muscle fatigue is defined as the incapability of a muscle to retain its maximal force output potential following a single maximum or multiple submaximal muscle contractions.17,18 The Borg Rating of Perceived Exertion (RPE) scale19,20 is a validated self-reported

0894-1130/$ e see front matter Ó 2019 Hanley & Belfus, an imprint of Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jht.2019.03.004

2

C. Karagiannopoulos et al. / Journal of Hand Therapy xxx (2019) 1e9

outcome tool to assess upper and lower extremity muscle fatigue following exercises.21-24 Research studies have pointed out that muscle fatigue negatively affects ankle, knee, elbow, and shoulder JPS and function.7,9,25-33 Immediately after exercise, a critical threshold of 20% to 30% of muscle strength decline is associated with significant JPS deficit at the elbow and knee among healthy adults.8,30,31 Similarly, a 50% postexercise muscle strength decline has been linked to significant JPS impairment at the shoulder and ankle.32,33 Although it is unknown how quickly wrist JPS deficit rebounds to normal levels following exertional exercises, high variability exists for other joints. At the elbow, up to 4 days is required for JPS deficit to gradually return to preexercise levels.34 However, shoulder JPS deficit tends to recover within 40 min following exercises.35 The main clinical concern is safety during long rehabilitation programs and repetitive daily activities that would predispose a patient to significant fatigue accumulation and extended proprioceptive deficit during function. Current research has suggested that JPS deficit is associated with significant wrist functional disability following wrist trauma.12 Thus, it can be speculated that JPS deficit could also lead to greater risk for a new injury or reinjury among patients. Another important matter is the timing for assessing wrist proprioception in the clinic, preferably before exercises, thus avoiding the confounding effects of muscle fatigue on patients’ ability to reliably perform proprioception testing. Currently, there are several clinically relevant unanswered questions regarding the effect of exercise-induced muscle fatigue on wrist JPS. This study has attempted to provide evidence for the following two main clinical concerns: (1) whether there is a relationship between wrist muscle fatigue and wrist JPS impairment and (2) how this relationship is affected by age levels among young and old adults. Determining these two fundamental questions would support future clinical research toward the effect of muscle fatigue on wrist proprioception among various patient populations. Clinical knowledge on the effect of muscle fatigue on wrist proprioception would enable clinicians to direct rehabilitation activities within safe levels of exercise intensity, avoiding significant JPS deficits before functional or proprioceptive testing. Patient education could also be advanced, deterring patients from engaging in demanding daily activities immediately after rigorous exercises to avoid possible risk for reinjury. Essentially, better recognition of a JPS decline critical level following rigorous strengthening exercises could instill safer clinical practice while promoting injury prevention. Study aims and hypotheses The primary aim of this study was to determine whether exercise-induced muscle fatigue can affect wrist JPS among healthy adults. The secondary aims were to (1) compare the effect of exercise-induced muscle fatigue on wrist JPS between younger and older healthy adults and (2) determine the association strength between exercise-induced muscle fatigue and wrist JPS among younger and older healthy adults. The study hypotheses were that (1) exercise-induced muscle fatigue would significantly increase postexercise wrist JPS deficit, (2) there would be no age-group difference on postexercise wrist JPS deficit due to muscle fatigue, and (3) there will be a significant association between postexercise wrist JPS deficit and total muscle fatigue (TMF) among healthy adults. Methods Study design and participants A two-group pretest and posttest experimental study design was used. A convenience sample of 42 male and female healthy

volunteer adults (18-65 years of age) was recruited for this study. Recruiting methods included posting of research flyers and wordto-mouth communication regarding the study purpose. Participants were assigned to one of the two independent groups based on age level. The younger adult group consisted of 22 participants of 18 to 39 years of age. The older adult group consisted of 20 participants of 40 to 65 years of age. All potential study participants were screened to assess their qualification for participation in the study based on specific inclusion and exclusion criteria. Inclusion criteria included the following conditions: being an adult (male or female) of 18 to 65 years of age, able to participate in wrist and hand exercises free of pain, present full functional ability to grasp with the dominant arm free of pain, and have pain-free functional wrist and hand active range of motion (ROM). Functional wrist active ROM was defined as the ability to demonstrate flexion near 50 , extension near 60 , radial deviation near 20 , and ulnar deviation near 40 .36 Functional hand active ROM was defined as the ability to touch fingers’ pulp to palm.37 Participants’ eligibility was not based on specific ROM inclusion criteria and functional active ROM was not assessed goniometrically. Rather, functional active ROM was screened via gross visual inspection. Exclusion criteria included failure to meet the study age requirements; inability to communicate in English; incapability to demonstrate functional wrist and hand active ROM due to painful conditions (eg, chronic deformities, rheumatoid disease, or osteoarthritis); dominant upper extremity edema or pain due to 6-month-old musculoskeletal trauma; motor or sensory deficits due to neurological disease within the last 6 months; pregnancy; blindness; and cognitive impairment that will prevent safe study participation. A total of 40 participants completed the study. Two participants from the older adult group were disqualified as they reported elbow and wrist pain during testing. The study was approved by the DeSales University Institutional Review Board. Measures Data recording forms Three exclusive data recording forms were used in the study: participant personal information, data collection form, and RPE scale form19 (Appendix A). The participant personal information form was used to obtain patient’s demographic information (ie, age, gender, and hand dominance) and past medical history. This form was used to determine each participant’s study eligibility. The data collection form was used to document information during all testing procedures (ie, pretest and posttesting, and exercise fatigue protocol). The RPE scale form was used to record self-reported fatigue levels during exercise from each participant. This is a 15-point numerical scale (ie, from 6 to 20) that grades an individual’s perceived exertion or increasing level of fatigue. In this scale, a score of 6 represents no exertion, scores of 15 to 16 represent hard effort, and the highest scores of 17 represent very hard to maximal exertion levels. In this study, an RPE score of 15/20 was considered a level of significant muscle fatigue.21 Wrist joint position sense The active wrist JPS test was used to test wrist conscious proprioception at each participant’s dominant arm in a standardized way prior and immediately after exercises. Each participant was seated with the elbow resting on a table in a flexed position, forearm in upright neutral position, wrist in neutral position, and fingers in a resting and slightly flexed position. Test protocol followed three consecutive steps while participants’ eyes were closed. First, a volarly placed plastic wrist goniometer was used by the tester to passively place the participant’s wrist in 20 of extension (ie, reference angle). The goniometer’s moving arm was aligned

C. Karagiannopoulos et al. / Journal of Hand Therapy xxx (2019) 1e9

palmary between the 3rd and 4th metacarpals, the stationary arm was placed over the volar midline of the distal forearm, and its axis (ie, with 2 increments) was placed over the volar wrist.12 The participant was instructed to actively hold for 3 s and memorize the reference angle. Next, the participant was instructed to relax by fully flexing the wrist away from the memorized angle. Finally, the participant was asked to actively reproduce the angle of reference. When the participant verbally confirmed that the memorized angle has been met, the same plastic wrist goniometer was used again to measure the participant reproduced wrist angle (ie, indicator angle). The difference between the reference and indicator wrist angles represented a wrist JPS deficit. A score value of zero indicated an exact replication of the reference angle, inferring no JPS deficit. Positive or negative score values (ie, overshooting or undershooting the reference angle) indicated wrist JPS errors. The test was repeated twice, and the absolute mean score value was used to determine the final active wrist JPS score or deficit. The preexercise and postexercise JPS scores were compared to determine the JPS rate of change, which was calculated by subtracting the preexercise and postexercise JPS score values, dividing it by the initial preexercise JPS score value, and multiplying by 100. JPS scores and the final value of JPS rate of change were used toward the statistical analysis. Hand and wrist dynamometry A Jamar (Jamar, Pakistan) hand-held dynamometer was used to assess grip strength of each participant’s dominant arm prior and immediately after exercises, following a standardized protocol as described by the American Society of Hand Therapists practice guidelines.38 Maximum handgrip voluntary isometric contraction (MVIC) was tested in a seated (ie, armless chair) position with the elbow unsupported, fully adducted, and flexed to 90 . The forearm was in neutral position, and the dynamometer handle was set on the second position. This test was performed twice with a 30second rest period between each trial. The mean value of two trials was used toward data analysis. A MicroFet dynamometer (HOGGAN Scientific, LLC, Salt Lake City, UT) was used to assess strength of each participant’s dominant arm wrist extensor group prior and immediately after exercise, following a standardized protocol.39,40 The make-test method41 was used to assess wrist extension MVIC values. Participants were seated next to a table with an erect posture, hips and knees flexed at a 90 angle, and both feet flat on the ground. The dominant arm rested on the table with the shoulder resting in neutral position, elbow flexed, forearm in a pronated position, and the wrist extending off the edge of the table in a neutral position. The MicroFet dynamometer was held by the tester in a static position against the dorsum of the participant’s hand, using both arms with elbows extended (Fig. 1). Each participant was instructed to exert maximum force by pushing the dorsum of the hand against the MicroFet dynamometer for 5 s. The standardized instructions that were given to participants were as follows: “Push as hard as you can, harder, harder, and relax”. This test was repeated twice with a 30-second rest period between each trial. The mean value of two trials was used toward data analysis. Testers and procedures The study’s research team consisted of the primary investigator and five 2nd year Doctor of Physical Therapy student coinvestigators. A single-tester approach for each measure was used in the study. The primary investigator, who is a physical therapist and certified hand therapist with 18 years of clinical experience, completed all preexercise and postexercise wrist JPS testing. Similarly, a single Doctor of Physical Therapy student coinvestigator was

3

Fig. 1. MicroFet assessment of wrist extension strength.

used to complete all preexercise and postexercise strength testing. This student had fully completed all musculoskeletal classes and had been trained on handgrip and wrist dynamometry. Exercises and data recordings were directed by the remaining student coinvestigators. Study recruitment, testing, and exercising took place at the DeSales University, Doctor of Physical Therapy Program (Center Valley, PA) research laboratory. Participants’ eligibility was determined via completion of the patient demographic form. Those participants who met all inclusion criteria and were free of all exclusion criteria were given a consent form to read and sign. Once the procedure was explained to the participant, preexercise testing was completed. During preexercise testing, the active wrist JPS test was completed first, followed by handgrip and wrist extensor muscle strength testing. A 3-minute rest period was utilized between preexercise testing and to determine the 10 repetition maximum (RM) values for the grip and wrist extension exercises. Following a 5-minute rest period, the exercises session was commenced with the hand gripping preceding the wrist extension exercise. Postexercise testing took place immediately following the exercise session (ie, 5 min). During postexercise testing, grip strength was assessed first followed by wrist extension strength and active wrist JPS testing. All preexercise and postexercise testing values were recorded in the data recording form. A stopwatch was used throughout all testing procedures to monitor testing and rest periods for all participants. Exercise session An exercise session was used to induce muscle fatigue to participants’ dominant hand intrinsic and extrinsic hand flexor and wrist extensor muscle groups. This exercise session took place immediately after all initial testing and included the following two exercises: gripping a calibrated hand gripper (AliMed, Dedham, MA) and performing wrist extension curls with a dumbbell. The calibrated hand gripper offered various resistance settings to fatigue the hand flexor muscles via three calibrated springs that range from 10 to 100 pounds (Fig. 2). Dumbbell hand weights were used to fatigue the wrist extensor group. Exercise resistance was based on each participant 10 RM level for each of the aforementioned exercises, which was established before exercises. A 50% to

4

C. Karagiannopoulos et al. / Journal of Hand Therapy xxx (2019) 1e9

Data analysis

Fig. 2. Calibrated hand gripper.

75% range of the grip and wrist extension strength MVIC values was used for determining a 10 RM point for each exercise.42-44 A 10 RM value represented the greatest exercise resistance a participant could sustain for 10 repetitions before failure due to muscle fatigue. During testing, participants performed 3 sets of 10 or more repetitions until maximum fatigue was reached for each exercise. This approach provided assurance that full physiological fatigue levels were reached. A digitally displayed metronome was used to keep exercise repetitions timing (ie, 1-2 sec/repetition) consistent among all participants. A 30-second rest period was used between exercises and exercise sets. The RPE scale was used to record each participant’s self-reported fatigue levels following each exercise set for both exercises.

Descriptive and inferential statistics were used to complete the study data analysis. The independent variables of the study were assessment time (ie, preexercise and postexercise) and age levels (ie, younger and older). The dependent variables consisted of active wrist JPS score, JPS rate of change, grip and wrist extension strength scores, TMF rate, and final RPE score following exercises. The primary aim hypothesis was analyzed via a paired t-test to compare preexercise and postexercise mean active wrist JPS test scores for all participants. Similarly, paired t-test was used to determine preexercise and postexercise muscle strength (ie, grip and wrist extension) differences among all participants. The secondary aim 1 hypothesis was analyzed using the independent t-test to compare the two age groups on wrist JPS scores and JPS rate of change. Similarly, independent t-test was used to determine muscle strength (ie, grip and wrist extension) differences and TMF rate between the two age groups. The secondary aim 2 hypothesis was analyzed using Spearman correlation coefficient to determine the relationship between JPS rate of change and TMF rate. To correlate these two heterogeneous variables, a common categorical scale of low, moderate, and high level was used. A t-test sample size table was used for a one-tail .80 a priory analysis,45 which determined that a sample size of 40 participants (20 participants per group) with a .05 alpha level and expected .80 (large) effect size are sufficient for the study to reach statistical significance. The Statistical Package for the Social Sciences, version 20.0 (SPSS, Chicago, IL) was used for all data analyses, with a statistical significance level set at P  .05 for all study aims. Results

Fatigue rate assessment Both the physiological and self-reported exercise-induced muscle fatigue was determined following exercises. Physiological fatigue was determined by comparing the preexercise and postexercise grip and wrist extension strength values. The rate of strength reduction (ie, percent value) for each muscle group was determined. The average rate of strength reduction for both grip and wrist extension represented the TMF rate postexercise, which was used toward the statistical analysis of the study. Self-reported muscle fatigue was determined via the RPE scale for each exercise. The final RPE value following the third set of each exercise was used toward the statistical analysis.

Participants’ characteristics and descriptive statistical data are presented in Tables 1 and 2. The majority of the study participants were right-hand dominant females. The mean age for the younger and older adult groups was 24 and 54 years, respectively. Postexercise active wrist JPS test scores were significantly (t ¼ 9.79, P ¼ .000) higher than the preexercise scores among all participants (Fig. 3), regardless of age level. No statistically significant age-group difference existed on preexercise (t ¼ .664, P ¼ .511) and postexercise (t ¼ 1.64, P ¼ .109) active wrist JPS scores. Similarly, no statistically significant age-group difference existed on postexercise active wrist JPS change (t ¼ 1.26, P ¼ .115) and JPS rate of change (t ¼ .678, P ¼ .502). On average, participants’ JPS deficit scores

Table 1 Participant descriptive data and differences between participants groups Characteristics

Young adults

Older adults

All ages

Mean age (range) Males/females R/L handedness Pre-Exer JPS score (mean) Post-Exer JPS score (mean) JPS score change (mean) JPS rate of change (mean %) Pre-Grip (mean) Post-Grip (mean) Grip change (mean) Pre-Ext strength (mean) Post-Ext strength (mean) Ext strength change (mean) TMF rate (mean %) Final postexercise RPE (mean)

24.48 (19-39) 3/18 20/1 4.52 9.42 4.90 188.67 75.83 58.33 17.50 29.62 24.13 5.48 18.71 16.95

54.63 (41-64) 7/12 19/0 5.10 11.26 6.26 246.11 81.45 64.21 17.24 36.85 31.21 6.45 18.92 16.87

38.80 (19-64) 10/30 39/1 4.80 10.30 5.55 215.95 78.50 61.13 17.38 33.06 27.49 5.94 18.82 16.91

P-value

511 109 115 502 394 220 922 011a 001b 448 929

Ext ¼ extension; JPS ¼ joint position sense; Post-Ext ¼ postexercise extension strength; Post-Grip ¼ postexercise grip strength; Pre-Exer ¼ preexercise; Pre-Ext ¼ preexercise extension strength; Pre-Grip ¼ preexercise grip strength; R/L ¼ right/left; RPE ¼ Borg Rating of Perceived Exertion Scale; TMF ¼ total muscle fatigue. a Significant at  0.05. b Significant at  0.001.

Table 2 Preexercise and postexercise participants’ descriptive data Variables

Preexercise

Postexercise

P-value

JPS score (mean) Young adults JPS (mean) Old adults JPS (mean) Combined groups JPS (mean) Grip (mean) Grip young (mean) Grip old (mean) Ext strength (mean) Ext young (mean) Ext old (mean)

4.80 4.52 5.11 4.80 78.50 75.83 81.44 33.06 29.62 36.85

10.30 9.43 11.26 10.30 61.13 58.33 64.21 27.49 24.12 31.21

.000a .000a .000a .000a .000a .000a .000a .000a .000a .000a

Ext ¼ extension; JPS ¼ joint position sense score. a Significant at  0.05.

Discussion The SM control system plays a critical role on joint stability and coordination during functional mobility. Considering the degree of

800.00

695.14 %

600.00 400.00 151.96 %

200.00 13.89 % 0.00 Low (n=9)

Moderate (n=24)

wrist proprioception decline following exertional wrist and hand exercises is important for safety before performing demanding functional activities. To the best of our knowledge, this is the first study to determine that exercise-induced fatigue has a significant adverse effect on wrist proprioception as reflected by the active wrist JPS rate of change between preexercise and postexercise among healthy adults, regardless of their age level. On average, a 215% JPS rate of change was significantly correlated to a critical level of 19% postexercise TMF. These results corroborate that better recognition of wrist proprioception decline following rigorous exercises could optimize patient safety and advance clinical practice. This study’s results are in agreement with previous research studies that have determined the negative effect of muscle fatigue on JPS at the elbow,11 shoulder,7 knee,8,22,31 and ankle.32,33 Similarly, this study findings align with previous reports that have linked a critical level of 25% to 30% postexercise fatigue to significant elbow JPS impairment among healthy adults.30,46

Instrumentation The active wrist JPS test has been supported by recent studies as a clinically meaningful assessment tool for wrist conscious proprioception impairment.12,15 This test utilizes a standardized goniometric protocol to measure someone’s ability to reproduce a specific wrist reference angle with vision occluded. During this test, ipsilateral matching accuracy is determined by estimating the difference between a memorized (ie, reference) and reproduced (ie, indicator) angle at the same wrist.15,16 The advantages to this test consist of its simple and clinically available instrumentation and strong psychometric properties (ie, high intratester reliability [ICC ¼ .85] and responsiveness values [effect size ¼ 1.22-2.75, standardized response mean ¼ 1.43-2.36] up to 12 weeks following wrist fractures).15 Under normal resting conditions, small accuracy errors are expected when JPS testing is conducted. At the wrist, a 3 to 4 of JPS accuracy error is considered normal among healthy

10.3

4.8

80 70 60 50 40 30 20 10 0

78.5 61.13

33.06

Grip

Pre

High (n=7)

JPS Test Score Rate of Change Classification Levels

Force (Lbs)

Degrees of MoƟon

5

Fig. 4. Categorization of postexercise active wrist JPS rate of change. JPS, joint position sense.

significantly increased from a preexercise level of 4.8 to a postexercise level of 10.3 . This indicated an average of 215% of JPS rate of change. JPS rate of change was classified as low (0%-49%), moderate (50%-350%), and high (350%). Distribution data on participants’ JPS rate of change levels are presented in Figure 4. Postexercise grip and wrist extension strength were significantly (t ¼ 13.11, P ¼ .000 and t ¼ 7.87, P ¼ .000) lower than their respective preexercise values (Fig. 5), regardless of age level. On average, preexercise grip force decreased from 78.5 to 61.12 lbs after exercise. Similarly, preexercise wrist extension force decreased from 33.05 to 27.49 lbs after exercise. No statistically significant agegroup difference existed on preexercise (t ¼ .843, P ¼ .394) and postexercise (t ¼ 1.246, P ¼ .220) grip strength scores. In contrast, older adults presented significantly higher preexercise (t ¼ 2.66, P ¼ .011) and postexercise (t ¼ 3.69, P ¼ .001) wrist extension strength values than their younger counterparts. However, no statistically significant age-group difference existed on strength reduction of grip (t ¼ .098, P ¼ .922), wrist extension (t ¼ .766, P ¼ .448), and TMF rates (t ¼ .09, P ¼ .929) postexercise. On average, an 18.82% level of TMF rate was observed postexercise among all participants. TMF rate was classified as low (0%-7.9%), moderate (8.0%-18.9%), and high (19%). Distribution data on participants’ TMF rate levels are presented in Figure 6. Statistically significant postexercise perceived exertion (ie, RPE > 15 points) levels were observed among all participants, regardless of age level. On average, all participants reported a final RPE score of 16.9/20 points postexercise. A statistically significant (P ¼ .007) fair (r ¼ 0.420) correlation was found between the JPS rate of change and TMF rate (Fig. 7). In this study, the intratester reliability level for the MicroFet wrist extension make-test strength assessment was determined to be high [Intraclass Correlation Coefficient (ICC (3,1) ¼ .97)].

12 11 10 9 8 7 6 5 4 3 2 1 0

Rate of Change (Mean %)

C. Karagiannopoulos et al. / Journal of Hand Therapy xxx (2019) 1e9

Post

Fig. 3. Preexercise and postexercise active wrist JPS test score mean values. JPS, joint position sense.

27.49

Ex t en si o n

Pre

Post

Fig. 5. Preexercise and postexercise hand grip and wrist extension strength mean values.

C. Karagiannopoulos et al. / Journal of Hand Therapy xxx (2019) 1e9

Total Muscle Fatigue Rate (Mean %)

6

30 25 20 15 10 5 0

24.53 % 15.10 % 5.03 %

Low (n=3)

Moderate (n=18)

High (n=19)

Total Muscle Fatigue Rate Classification Levels Fig. 6. Categorization of postexercise total muscle fatigue rates.

adults.12,15 Similar JPS accuracy errors of approximately 3 , 4 , 5 to 6 , and 1 to 2 have been reported at the elbow (ie, flexionextension),11 shoulder (ie, abduction),7 knee (ie, flexion-extension),8,22,31 and ankle (ie, inversion and eversion),32,33 respectively. Although the underlying physiological mechanism is not fully understood, these accuracy errors have been attributed to fluctuating skin receptors sensory input47 and have altered muscle spindle sensitivity levels in the contracting agonist and antagonist muscle groups8,10,11,25 during active JPS testing. Normal muscle contraction and relaxation may lead to predictable muscle spindle sensitivity level changes (ie, intrafusal passive tension) that produce illusionary sensory inputs. When such inputs are centrally interpreted, it produces a feeling of the muscle being longer or shorter than normal.8,30 This faulty central interpretation on muscle length leads to faulty cortical feedforward motor commands46 and matching errors (ie, underestimation or overestimation) during active JPS reference angle reproduction.8,30 When significant levels of muscle fatigue occur, the level of these errors significantly increase as neuromuscular function is declined,46,48 leading to even greater levels of muscle spindle sensitivity distortion8,49 and cortical joint position misinterpretation (ie, central fatigue).31,46,50 Additionally, the presence of accumulating local metabolites (eg, lactic acid, arachidonic acid, bradykinin, and prostaglandins) in a fatigued muscle can alter further muscle spindles’ function,49,51 leading to increased errors during JPS testing. Currently, it is unknown how long it takes for the impaired wrist JPS to rebound after exercises. Based on the study design, which intended to measure the effect of muscle fatigue on wrist JPS

immediately after exercises only, it can be inferred that JPS deficit does not rebound immediately. Specifically, during the postexercise testing sequence (ie, grip strength, wrist extension strength, wrist proprioception), active wrist JPS testing was conducted last within a period of 5 min from the termination of the exercise program. This implies that significant wrist JPS deficit could persist for at least 5 min following vigorous exercises, which is consistent with research findings at the elbow where similar JPS errors persists for at least 15 min after exercise.11 Self-reported fatigue rate was assessed in this study via the RPE scale. This 15-point (6-20) scale is a validated instrument to rate physiological fatigue during exertional upper extremity exercises.23 In this study, a 15/20 RPE score was considered the critical threshold point for reaching a significant fatigue level. This is consistent with previous research, which has associated this RPE score level with significant upper extremity muscle fatigue levels due to accumulation of local metabolic byproducts in muscle and rapid changes in respiratory and heart rates during exercise.24 Previous studies have used the same score to denote significant muscle fatigue following upper and lower extremity exercises.21,22 The advantage of utilizing the RPE scale is its simple clinical utility to objectively assess self-reported fatigue levels, incorporating a participant’s perspective. In this study, all participants exceeded the RPE score of 15/20 as they reported an average of 16.2 and 17.6 scores following the 3rd trial of the hand gripper and wrist extension exercises, respectively. This finding provides strong evidence that all participants subjectively felt that they reached significant fatigue levels upon exercise completion, corroborating that the main study intent to induce significant exercise-induced muscle fatigue was met. The make-test method was used to assess wrist extensors muscle strength using the MicroFet dynamometer. This standardized method has been described by previous studies41 as a reliable method to objectively measure muscle strength. During this method, the examiner holds the dynamometer stationary against the body while the subject is instructed to independently exert a maximum isometric force against the instrument. The advantage of this method is to better isolate the patient’s ability to produce force with minimal potential bias from any tester’s contribution. Originally, the wrist extension make-test was established with the subject lying supine, shoulder at the neutral position, elbow flexed at 90 , and forearm and wrist at neutral positions while the dynamometer was placed against the dorsum of the hand and the tester manually stabilized the distal forearm.52,53 Test-retest reliability for this method has been determined to be high (ICC ¼ .97.98).52 A modified wrist extension make-test was instituted in this study. Participants were seated next to a table with the elbow and forearm resting in a flexed and pronated position, respectively. The wrist was extended off the edge of the table in a neutral position, and the dynamometer was placed against the dorsum of the hand while the tester manually stabilized the distal forearm. A high (ICC ¼ .97) test-retest reliability was established for this modified method, which is in agreement with its previously established psychometrics. The advantage of the modified method is its more functional and easily attainable patient position in a clinical setting. Exercise protocol

Fig. 7. Association between TMF rate and JPS change of rate. JPS, joint position sense; TMF, total muscle fatigue.

The study’s methodological approach to utilize the 10 RM method for determining each participant’s maximum exercise resistance is consistent with previous studies that utilized this method to improve muscle strength at the shoulder42 and wrist43 among healthy participants. These studies demonstrated that the 10 RM is an effective way to induce sufficient muscle overload via a significant physiological response of muscle fatigue. Unlike

C. Karagiannopoulos et al. / Journal of Hand Therapy xxx (2019) 1e9

previous reports, in this study, the 10 RM method was complemented by allowing each participant to add extra repetitions beyond the predetermined 10 RM level until maximum fatigue was reached. In fact, most participants in this study exceeded their predetermined 10 RM levels, performing on average 17 to 12 and 12 to 8 reps during the 3 consecutive sets of hand gripper and wrist extension free weights, respectively. The advantage of this approach was that it allowed all participants to exercise up to a point of actual performance failure, attaining maximum physiological and self-reported muscle fatigue levels. This approach minimized a potential source of error (ie, failure to reach maximum fatigue) that could have affected the study’s internal validity. The study’s standardized exercise protocol was effective on inducing significant physiological postexercise muscle fatigue in all muscle groups. The exercises targeted the wrist extensor group as well as the intrinsic and extrinsic hand flexor muscles. Physiological muscle fatigue was assessed by determining the rate of postexercise strength reduction for these muscle groups, using reliable and standardized dynamometry methods. Postexercise grip and wrist extension strength levels were significantly reduced by an average of 22.2% and 16.6%, respectively, leading to a TMF rate of 18.8% for both exercises. Thus, the observed exercise-induced TMF was linked to significant wrist JPS deficits following exercises. This finding is in agreement with previous studies that indicated 20% to 30% postexercise muscle fatigue levels accompany significant JPS deficit at the elbow and knee among healthy populations.8,30,31

Results The study finding of a significant positive association between the wrist JPS score change and the muscle fatigue rates postexercise is a unique outcome as no previous study, to the best of our knowledge, has explored this relationship. The results of this study imply that the higher the postexercise muscle fatigue, the higher the JPS deficit and JPS rate of change expected at the wrist. Essentially, low, moderate, and high TMF rates are expected to be associated with low, moderate, and high JPS rate of change, respectively. The determined strength level (ie, fair) of this association could possibly be attributed to the influence from various other confounding elements (eg, biological, psychological, and external environment) that this study did not intent to assess. Specifically, participants’ gender, training level, muscle endurance, personal judgment, attention span, and room noise or temperature could have been influential to the tested variables of TMF and JPS rate of change. Another noteworthy factor that could have influenced this association is exercise timing. Recruited participants were tested at various times of the day (ie, morning or afternoon, before or after work hours, before or after meals) that could have altered their individual levels of muscle strength and endurance as well as psychological status. This study did not control for possible confounding influences from all the aforementioned factors. Participant’s age level was not found to influence the study’s outcomes as there were no significant age-group differences on JPS scores, JPS rate of change, grip and wrist extension strength, and TMF rate. To the best of our knowledge, no previous studies have investigated age-based differences on wrist JPS deficit due to exercise-induced muscle fatigue. These findings imply that age should not be influencing the level of wrist JPS deficit due to muscle fatigue. However, this finding should also be interpreted with some caution as only two very broad age-level categories (ie, 18-39 and 40-65 years) were compared. Future research is needed to further explore this relationship with smaller age subcategories, including age groups of >65 years.

7

Study strengths The most significant strength of this study is its pioneer findings of the effect of exercise-induced muscle fatigue on wrist JPS. In addition, the utilization of a healthy population provided a unique advantage, allowing this study to fulfill its exploratory objectives among a more stable population. This study’s well-structured methodology helped to minimize experimental bias or errors. Assigning specific roles for all research members throughout data collection, standardizing the protocol for completing objective tests by a single tester, and the use of a metronome and a stopwatch provided methodological consistency and strengthened this study’s internal validity. Assessing fatigue levels via both dynamometry and self-reported measures allowed for capturing a more holistic dimension (ie, both physiological and self-reflective elements) of muscle fatigue. This approach strengthened the validity of the study. Finally, the study was strengthened by the efficacy of its exercise protocol. This study followed a unique approach for inducing muscle fatigue via the use of readily available equipment and exercises (ie, calibrated hand gripper and dumbbell weights) in an attempt to better extrapolate its results to today’s clinical environment. In addition, the exercise protocol entailed exercising beyond the 10 RM values if needed, successfully ensuring the development of true maximal muscle fatigue. Study limitations The study’s findings need to be interpreted with caution due to several study weaknesses. A relatively small sample size and the utilization of a single research site may have influenced the extrapolating power of the study’s results. However, the study’s sample size met the original power analysis criteria (ie, 40 participants) with minimal attrition as 95% of participants completed the study. Post hoc testing indicated a high (ie, 1.55) effect size and power (ie, 1.0) levels for the study’s primary aim, validating its results. Although the study’s approach to recruit healthy participants was consistent with previous research, it can be considered both a weakness and strength. Clearly, its results could not be extrapolated with full confidence into other injured populations. Further research is needed to determine the effect of exercise-induced muscle fatigue on wrist JPS deficits following wrist injury. However, recruitment of healthy participants benefited this novel study to efficiently test its primary hypotheses in a more stable population, while avoiding other confounding effects caused by musculoskeletal injury (ie, reduced muscle strength, endurance, and neuromuscular control). It is reasonable to assume that an injured population would be more easily fatigued and present more pronounced JPS and strength deficits following exercises. Another study weakness by design was its inability to determine the full duration of the observed wrist JPS impairment postexercise. Although this was not one of the study aims, it limits its clinical interpretation. Further research is needed to determine the required length of time (ie, beyond 5 min) for wrist JPS deficit to recover following exertional exercise. Finally, using a gripper with preset resistance settings could have introduced some minor testing error as 10 RM levels were estimated based on the available gripper force increments. Conclusion Exercise-induced fatigue significantly affects wrist JPS levels as a significant association exists between postexercise TMF rate and JPS deficit among healthy adults. Specifically, a near 20% postexercise hand and wrist fatigue levels could lead to near 200% wrist JPS deficit for at least 5 min following exercise termination in

8

C. Karagiannopoulos et al. / Journal of Hand Therapy xxx (2019) 1e9

healthy adults, regardless of age level. Thus, declined wrist proprioception following exertional wrist and hand exercises may necessitate caution to prevent injury. Acknowledgments In addition to all study participants, the authors sincerely thank our research group members Mike Anastasiou, Doctor of Physical Therapy and Eric Louis, DPT for their imperative collaboration and support toward study completion. They are grateful to their front office coordinator Heidi Troxell for her vital assistance during participant recruitment and scheduling. References 1. Riemann BL, Lephart SM. The sensorimotor system, Part I: the physysiologic basis of functional joint stability. J Athl Train. 2002;37(1):71e79. 2. Hagert E. Proprioception of the Wrist Joint: a review of current concepts and possible implications on the rehabilitation of the wrist. J Hand Ther. 2010;23(1):2e17. 3. Riemann BL, Lephart SM. The sensorimotor system, Part II: the role of proprioception in motor control and functional joint stability. J Athl Train. 2002;37(1):80e84. 4. Smith JL, Crawford M, Proske U, Taylor JL, Gandevia SC. Signals of motor commands bias joint position sense in the presence of feedback from proprioceptors. J Appl Physiol. 2009;106(3):950e958. 5. Gandevia SC, Smith JL, Crawford M, Proske U, Taylor JL. Motor commands contribute to human position sense. J Physiol. 2006;571(3):703e710. 6. Proske U, Gandevia SC. The kinesthetic senses. J Physiol. 2009;587(17):4139e 4146. 7. Voight ML, Hardin JA, Blackburn TA, Tippett S, Canner GC. The effects of muscle fatigue on and the relationship of arm dominance to shoulder proprioception. J Orthop Sports Phys Ther. 1996;23(6):348e352. 8. Ribeiro F, Mota J, Oliveira J. Effect of exercise-induced fatigue on position sense of the knee in the elderly. Eur J Appl Physiol. 2007;99(4):379e385. 9. Myers JB, Guskiewicz KM, Schneider RA, Prentice WE. Proprioception and neuromuscular control of the shoulder after muscle fatigue. J Athl Train. 1999;34(4):362e367. 10. Hiemstra LA, Lo IK, Fowler PJ. Effect of fatigue on knee proprioception: implications for dynamic stabilization. J Orthop Sports Phys Ther. 2001;31(10): 598e605. 11. Allen TJ, Proske U. Effect of muscle fatigue on the sense of limb position and movement. Exp Brain Res. 2006;170(1):30e38. 12. Karagiannopoulos C, Sitler M, Michlovitz S, Tierney R. A descriptive study on wrist and hand sensori-motor impairment and function following distal radius fracture intervention. J Hand Ther. 2013;26(3):204e214. 13. Valdes K, Naughton N, Algar L. Sensorimotor interventions and assessments for the hand and wrist: a scoping review. J Hand Ther. 2014;27(4):272e286. 14. Hincapie OL, Elkins JS, Vasquez-Welsh L. Proprioception retraining for a patient with chronic wrist pain secondary to ligament injury with no structural instability. J Hand Ther. 2016;29(2):183e190. 15. Karagiannopoulos C, Sitler M, Michlovitz S, Tucker C, Tierney R. Responsiveness of the active wrist joint position sense test after distal radius fracture intervention. J Hand Ther. 2016;29(4):474e481. 16. Karagiannopoulos C, Michlovitz S. Rehabilitation strategies for wrist sensorimotor control impairment: from theory to practice. J Hand Ther. 2016;29(2): 154e165. 17. Chaffin DB. Localized muscle fatigue: definition and measurement. J Occup Med. 1973;15(4):346e354. 18. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev. 2001;81(4):1725e1789. 19. Borg G. Psychophysical bases of perceived exertion. Med Sci Sports Exerc. 1982;14(5):377e381. 20. Buckley JP, Borg GA. Borg’s scales in strength training; from theory to practice in young and older adults. Appl Phys Nutr Metab. 2011;36(5):682e692. 21. Tripp BL, Boswell L, Gansneder BM, Shultz SJ. Functional fatigue decreases 3dimensional multijoint position reproduction acuity in the overhead-throwing athlete. J Athl Train. 2004;39(4):316e320. 22. Changela PK, Selvamani K. A study to evaluate the effect of fatigue on knee joint proprioception and balance in healthy individuals. Indian J Phys Occup Ther. 2013;7(1):213e217. 23. Kang J, Chaloupka EC, Mastrangelo MA, Donnelly MS, Martz WP, Robertson RJ. Regulating exercise intensity using ratings of perceived exertion during arm and leg ergometry. Eur J Appl Physiol Occup Physiol. 1998;78(3):241e246.

24. Pandolf KB, Billing DS, Drolfi LL, Pimentiial NA, Sawka MN. Differentiated ratings of perceived exertion and various physiological responses during prolonged upper and lower body exercise. Eur J Appl Physiol Occup Physiol. 1984;53(1):5e11. 25. Skinner HB, Wyatt MP, Hodgdon JA, Conard DW, Barrack RL. Effect of fatigue on joint position sense of the knee. J Orthop Res. 1986;4(1):112e118. 26. Blasier RB, James EC, Laura JH. Shoulder proprioception: effect of joint laxity, joint position, direction of motion, and muscle fatigue. Orthop Rev. 1993;23: 45e50. 27. Marks R. Effect of exercise-induced fatigue on position sense of the knee. Aust Physiother. 1994;40(3):175e181. 28. Carpenter JE, Blasier RB, Pellizzon GG. The effects of muscle fatigue on shoulder joint position sense. Am J Sports Med. 1998;26(2):262e265. 29. Forestier N, Teasdale N, Nougier V. Alteration of the position sense at the ankle induced by muscular fatigue in humans. Med Sci Sports Exerc. 2002;34(1):117e 122. 30. Allen TJ, Ansems GE, Proske U. Effects of muscle conditioning on position sense at the human forearm during loading or fatigue of elbow flexors and the role of the sense of effort. J Physiol. 2007;580(2):423e434. 31. Givoni NJ, Pham T, Allen TJ, Proske U. The effect of quadriceps muscle fatigue on position matching at the knee. J Physiol. 2007;584(1):111e119. 32. Sandrey MA, Kent TE. The effects of eversion fatigue on frontal plane joint position sense in the ankle. J Sport Rehabil. 2008;17(3):257e268. 33. Mohammadi F, Roozdar A. Effects of fatigue due to contraction of evertor muscles on the ankle joint position sense in male soccer players. Am J Sports Med. 2010;38(4):824e828. 34. Brockett C, Warren N, Gregory JE, Morgan DL, Proske U. A comparison of the effects of concentric versus eccentric exercise on force and position sense at the human elbow joint. Brain Res. 1997;771:251e258. 35. Chang HY, Chen CS, Wei SH, Huang CH. Recovery of joint position sense in the shoulder after muscle fatigue. J Sport Rehabil. 2006;15(4):312e325. 36. Ryu J, Cooney WP, Askew LJ, An KN, Chao EYS. Functional ranges of motion of the wrist joint. J Hand Surg. 1991;16(3):409e419. 37. MacDermid JC, Fox E, Richards RS, Roth JH. Validity of pulp-to-palm distance as a measure of finger flexion. J Hand Surg Br. 2001;26(5):432e435. 38. Schectman O, Sindhu BS. Grip strength. In: MacDermid JC, ed. Clinical Assessment Recommendations. 3rd ed. Mt laurel, NJ: The American Society of Hand Therapists; 2015:2e8. 39. Stratford PW, Balsor BE. A comparison of make and break tests using a handheld dynamometer and the Kin-Com. J Orthop Sports Phys Ther. 1994;19(1): 28e32. 40. Chou PH, Feng CK, Chiu FY, Chen TH. Isometric measurement of wrist-extensor power following surgical treatment of displaced lateral condylar fracture of the humerus in children. Int Orthop. 2008;32(5):679e684. 41. Bohannon RW. Make tests and break tests of elbow flexor muscle strength. Phys Ther. 1988;68(2):193e194. 42. Reinold MM, Wilk KE, Fleisig GS, et al. Electromyographic analysis of the rotator cuff and deltoid musculature during common shoulder external rotation exercises. J Orthop Sports Phys Ther. 2004;34(7):385e394. 43. Szymanski DJ, Szymanski JM, Molloy JM, Pascoe DD. Effect of 12 weeks of wrist and forearm training on high school baseball players. J Strength Cond Res. 2004;18(3):432e440. 44. Brzycki M. Strength testing e predicting a one-rep max from reps to fatigue. J Phys Edu Rec Dance. 1993;64(1):88e90. 45. Portney LG, Watkins MP. Foundations of Clinical Research: Applications to Practice. 3rd ed. Philadelphia, PA: FA Davis; 2015. 46. Allen TJ, Leung M, Proske U. The effect of fatigue from exercise on human limb position sense. J Physiol. 2010;588(8):1369e1377. 47. Collins DF, Refshauge KM, Todd G, Gandevia SC. Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. J Neurophysiol. 2005;94(3):1699e1706. 48. Pasquet B, Carpentier A, Duchateau J, Hainaut K. Muscle fatigue during concentric and eccentric contractions. Muscle Nerve. 2000;23(11):1727e 1735. 49. Pedersen J, LOnn J, Hellstrom FR, Djupsjobacka MA, Johansson H. Localized muscle fatigue decreases the acuity of the movement sense in the human shoulder. Med Sci Sports Exerc. 1999;31(7):1047e1052. 50. Taylor JL, Todd G, Gandevia SC. Evidence for a supraspinal contribution to human muscle fatigue. Clin Exp Pharmacol Physiol. 2006;33(4):400e 405. 51. Djupsjobacka M, Johansson H, Bergenheim M. Influences on the g-muscle-spindle system from muscle afferents stimulated by increased intramuscular concentrations of arachidonic acid. Brain Res. 1994;663(2):293e 302. 52. Bohannon RW. Test-retest reliability of hand-held dynamometry during a single session of strength assessment. Phys Ther. 1986;66(2):206e209. 53. Andrews AW, Thomas MW, Bohannon RW. Normative values for isometric muscle force measurements obtained with hand-held dynamometers. Phys Ther. 1996;76(3):248e259.

C. Karagiannopoulos et al. / Journal of Hand Therapy xxx (2019) 1e9

Appendix A

9