A review of the fatigue’s effect on shoulder proprioception

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REVIEW ARTICLE

Hippokratia 2024, 28(2): 45-49

Hadjisavvas S, Themistocleous IC, Papamichael E, Michailidou C
Department of Health Sciences, Physiotherapy Program, University of Nicosia, Cyprus

Abstract

Background: Fatigue is considered a significant contributing factor to shoulder injuries that most commonly happen at the later phases of a competitive game, possibly due to reduced proprioception. The main objective of the current review was to provide information based on the available literature regarding fatigue’s impact on shoulder proprioception.

Methods: We performed a literature search via the EBSCO, PubMed, and Scopus electronic databases using the keywords (“muscle fatigue” OR “muscular fatigue” OR “fatigue exercise” OR “fatiguing activity”) AND (“proprioception”) AND (“shoulder”). The studies incorporated in this review were required to meet the Population, Intervention, Comparison, Outcome, and Study design (PICOS) criteria.

Results: A total of 12 studies fulfilled the inclusion criteria, examining the impact of tiredness on shoulder joint repositioning sense (n =9), the threshold for detecting passive movement (n =2), and the sense of force reproduction (n =1).

Conclusions: Exercise-induced fatigue can cause considerable impairment of shoulder joint position sense. The other subcategories of proprioception, including kinesthesia and sense of force reproduction, are also affected due to fatigue. HIPPOKRATIA 2024, 28 (2):45-49.

Keywords: Muscle fatigue, proprioception, joint position sense, kinesthesia, shoulder

Corresponding author: Stelios Hadjisavvas, BSc, MSc, PhD, Adjunct faculty Department of Health Sciences, Physiotherapy Program, University of Nicosia, 46 Makedonitissas Avenue, CY-2417, Nicosia, Cyprus, tel: +35722841500, e-mail: hadjisavvas.s@unic.ac.cy

Background

Shoulder disorders are a common source of musculoskeletal pain and impairment1. In addition, shoulder pain ranks as the third most prevalent musculoskeletal condition, following low back and cervical pain2. The prognosis for persons experiencing musculoskeletal shoulder discomfort exhibits significant variation among individuals. On average, over 50 % of individuals with shoulder pain continue to report symptoms six months after seeking primary care3. In 68.8 % of the athletes who reported shoulder pain, training, and competition were most often linked to the development of pain4. The increased incidence of shoulder pain may have been caused by the training load and lack of recuperation between events, as most sports injuries in adolescents happened through indirect processes4,5. Athletes of elite level who perform overhead sports engage in high-intensity activities that could result in transient and end-match neuromuscular fatigue, which may explain the high prevalence of injuries during the latter half of a game or the final part of a training session6.

Fatigue, defined as a decline in the muscle’s capacity to produce force or power due to exercise, is influenced by both peripheral and central factors7. This decline is associated with an elevation in perceived exertion, which refers to the level of subjective effort, strain, discomfort, or fatigue experienced during physical activity8. Muscle fatigue has been postulated to hinder proprioceptive acuity through the elevation of muscle spindle discharge threshold and the disruption of afferent feedback9. The observed decline in proprioception following fatigue-induced exercise may be attributed to increased metabolites and inflammatory substances within the muscles. These substances directly influence the release pattern of muscle spindles and the activation of alpha-gamma receptors10,11.

Proprioception refers to the collective neural input received by the central nervous system from mechanoreceptors, which are specialized nerve endings situated in various anatomical structures such as joints, capsules, ligaments, muscles, tendons, and skin12,13. Proprioception is commonly categorized into three subcategories: sense of tension (resistance), sense of movement, and sense of joint position14. The evaluation of proprioception is conducted with specific tests15,16 that use either passive conditions, which involve biasing joint mechanoreceptors, or active conditions involving activating joint and muscle-tendon mechanoreceptors15,17. According to Lephart et al18 and Benjaminse et al19, joint position sense tests evaluate the level of precision or accuracy in repositioning a joint at a preset target angle. Kinesthesia assessments evaluate an individual’s capacity to perceive joint movement, measured through various methods such as threshold to detection of passive motion (TTDPM)18,19, movement discrimination tests20,21, or the acuity of a tracking task22. Force sense tests evaluate an individual’s capacity to perceive and generate a preset and controlled amount of force below the maximum threshold19,23,24.

Several studies were designed to examine the impact of exercise-induced fatigue on several aspects of proprioception, such as joint position sense and kinesthesia, due to its detrimental effect on shoulder proprioception12,13,25-27. However, fewer studies have been conducted on the shoulder compared to knee and ankle joints. To date, no review has been conducted that exclusively investigates the effect of the exercise-induced fatigue on shoulder proprioception.

This review aimed to provide information from existing literature on fatigue’s effect on shoulder proprioception and discuss possible outcomes based on this information.

Methods

The literature search was performed via the EBSCO, Pubmed, and Scopus electronic databases using the keywords (“muscle fatigue” OR “muscular fatigue” OR “fatigue exercise” OR “fatiguing activity”) AND (“proprioception”) AND (“shoulder”). We operated the exact sequence of the above keywords in each database. There were no restrictions regarding the publication date of the studies. We used the reference management software RefWorks (Proquest LLC, Ann Arbor, MI, USA) to screen, select, and eliminate duplicate articles. Furthermore, the studies incorporated in this review were required to meet the Population, Intervention, Comparison, Outcome, and Study design (PICOS) criteria (Table 1). We excluded from the analysis books, case reports, case series, review articles, conference abstracts, study protocols, and studies that involved patients with neurological diseases, or lacked sufficient information about the muscle fatigue protocol. We specified no specific limitations on the publication date.

Results

Fatigue and joint repositioning sense (JRS)

Nine studies12,25-32 investigated the impact of fatigue on the shoulder JRS. All studies used the active repositioning (ARP) method to detect the target angles, while five12,26-28,30 used passive repositioning (PRP) method. In one study29, elite and amateur overhead throwers participated, while the remaining studies enrolled healthy, non-mentioned athletes. In total, 290 individuals participated in the studies (156 males, 53.79 %, and 98 females, 33.79 %). One study29 did not mention the participant’s gender. Six studies12,25,27,30-32 used the isokinetic dynamometer to assess the JRS; two26,28 used the isokinetic dynamometer with other proprioception testing devices, and one32 used the digital inclinometer. Most included studies evaluated the JRS of the shoulder external or/internal rotation, while one32 assessed JRS in shoulder flexion. Despite the target angles during the JRS assessment, Chang et al30 assessed four target angles (5° from full internal rotation, 5° from full external rotation, mid-point of full range of motion for shoulder internal rotation, and mid-point of full range of motion for shoulder external rotation). Kablan et al29 evaluated six target angles (10°, 15°, and 20° in internal and external rotation). Lee et al26 used two replicated angles (45° of internal and 75° of external rotation). Lida et al27 examined two target angles (mid-range for internal and external rotation). Myers et al25 utilized three target angles (30° of internal and 30° of external rotation. Spargoli31 assessed only one target angle (30° of external rotation). Sterner et al28 examined the mid-range angle of both internal and external rotation, and Voight et al12 assessed a solitary replicated angle (75° of external rotation). Guo et al32 examined three target angles (30°, 60°, and 120° of shoulder flexion). The initial participants’ positions for the proprioceptive assessments were sitting12,27,29,30,32, supine25,26,28, and standing31. Studies that used an isokinetic dynamometer for fatigue induction applied angular speeds of 180°/sec12,25,26,31, 60°/sec29, and 90°/sec30. In addition, these studies performed continuous maximal isokinetic contractions for fatigue confirmation until the peak torque was reduced to a specific percentage value for three consecutive repetitions. All studies involved a protocol of concentric-induced fatigue with the isokinetic dynamometer. Nevertheless, one study31 utilized eccentric exercise-induced fatigue protocol. Guo et al32 used a fatigue protocol, a repetitive exercise using dumbbells loaded at roughly 80 % of the participant’s maximum force. Then, fatigue was confirmed when the recorded maximum force was reduced to 50 % below the initial maximum force. Six studies12,25-27,29,30 confirmed the impairment of shoulder JRS due to fatigue, while three studies did not demonstrate any significant difference in angular error scores pre- and post-fatigue intervention28,31,32. The main characteristics of the above studies are described in Table 2.

Fatigue and TTDPM

Two studies13,28 investigated TTDPM of the shoulder (Table 2). Both studies evaluated the TTDPM for shoulder internal and external rotation, with all trials employing an identical starting shoulder position of 90° shoulder abduction and 90° flexion, while the participants were in a seated position. However, the angular speed of the passive movement varied throughout the investigations. Sterner et al28 employed an angular speed of 0.5°/sec, whereas Carpenter et al13 utilized an angular speed of 1°/sec. Both investigations used the same protocol to produce fatigue. The results varied in both investigations as Sterner et al28 discovered no notable disparities in TTDPM before and after the fatigue intervention. In contrast, Carpenter et al13 found a noteworthy rise in TTDPM following the fatigue intervention.

Fatigue and sense of force reproduction

Only one study33 assessed the impact of fatigue on the sense of force reproduction (Table 2), in which seventeen healthy males participated.  Before and after a fatigue procedure, each participant had to replicate a specific target in three consecutive trials. Before fatigue’s onset, the force exerted by the participants did not show a significant difference compared to the desired value (p =0.073). Nevertheless, following the fatiguing procedure, the magnitude of this force was much lower than the intended objective. No significant interactions were identified when repeated for external rotation (p =0.425).

Discussion

This review aimed to provide the existing evidence in the current literature regarding the impact of muscle fatigue on shoulder proprioception. The primary findings of this review indicate that muscular fatigue adversely impacts the JRS of the shoulder. The prevailing consensus among the majority of studies (66.66 %) supports this hypothesis. Nevertheless, conflicting findings and insufficient evidence exist regarding the impact of fatigue on shoulder kinesthesia and the sense of force reproduction.

The observed decline in shoulder JRS following fatigue-induced exercise may be attributed to increased levels of several metabolites and inflammatory substances within the muscles. These substances directly influence the release pattern of muscle spindles and the activation of alpha-gamma receptors10,11.

Only two studies13,28 have examined the impact of muscular fatigue on the TTDPM of the shoulder, and they yielded conflicting results. Carpenter et al13 found that following the fatigue intervention, the mean TTDPM (combined internal and external rotation) increased to 73 %, while no significant differences in TTDPM by Sterner et al28, before and after a fatigue intervention. The methodological differences (initial participant’s assessment position, angular speed, sample) between the two investigations may account for the conflicting results. It is hypothesized that fatigue decreases the kinesthetic information, reducing the sensitivity of muscle spindles, commonly acknowledged as the main receptors for kinesthesia9. Further evidence from a separate source confirms that muscle spindles have a crucial role in kinesthesia. This evidence comes from the observation that passive tension in muscles, both in and outside the eye, depends on the previous muscle contractions and changes in length, a phenomenon known as muscle thixotropy9.

Due to the limited number of studies, there is limited evidence regarding the impact of exercise-induced fatigue of the rotator cuff on sense of force reproduction. Coskun et al33 observed that the individuals demonstrated a significantly higher proficiency in recreating external rotation forces compared to their ability to reproduce internal rotation forces. A plausible rationale for this disparity, which the researchers gave, can be attributed to the testing position. The participants were examined in a maximum range of motion (ROM) position, specifically a complete external rotation and 90° of abduction. This position, similar to the final stage of cocking in overhead sports, generates specific tension in the ligaments of the front shoulder and offers proprioceptive feedback34. When a muscle is stretched passively, it causes the muscle spindles within the muscle to become active and produce brain impulses35,36. Greater elongation of the muscles, specifically the internal rotators, towards the end of the range of motion can lead to a higher quantity of stimulated muscle spindles in these muscles37,38. The simultaneous application of increased stress on ligaments, capsular structures, and the internal rotators can enhance proprioceptive feedback, improving accuracy in force reproduction39.

Clinical recommendations

Physically active people are advised to incorporate well-organized training routines in order to enhance their endurance and develop a higher level of resistance to fatigue.

It is advisable to assess shoulder proprioception using reliable measurement equipment, such as an isokinetic dynamometer, in order to detect any proprioceptive abnormalities.

Evaluation of proprioception should also be conducted before and immediately following fatigue.

If a notable proprioceptive problem is detected during the assessment, targeted exercises should be implemented to improve proprioception.

Proprioception-enhancing exercises should be utilized even when experiencing fatigue to enhance mechanoreceptors’ sensitivity in these situations.

Conclusion

Exercise-induced fatigue can cause significant impairment of shoulder joint position sense. The other subcategories of proprioception, including kinesthesia and sense of force reproduction also seem to be affected due to fatigue. Nevertheless, given the scarcity of existing studies, additional research is needed to establish more secure results.

Conflict of Interest

Authors declare no conflicts of interest.

Acknowledgement

Authors thank Mrs Georgia Christodoulou (lead librarian) for her help in the search process.

References

  1. Lucas J, van Doorn P, Hegedus E, Lewis J, van der Windt D. A systematic review of the global prevalence and incidence of shoulder pain. BMC Musculoskelet Disord. 2022; 23: 1073.
  2. Urwin M, Symmons D, Allison T, Brammah T, Busby H, Roxby M, et al. Estimating the burden of musculoskeletal disorders in the community: the comparative prevalence of symptoms at different anatomical sites, and the relation to social deprivation. Ann Rheum Dis. 1998; 57: 649-655.
  3. Kuijpers T, van der Windt DAWM, van der Heijden GJMG, Bouter LM. Systematic review of prognostic cohort studies on shoulder disorders. Pain. 2004; 109: 420-431.
  4. Johansson F, Cools A, Gabbett T, Fernandez-Fernandez J, Skillgate E. Association Between Spikes in External Training Load and Shoulder Injuries in Competitive Adolescent Tennis Players: The SMASH Cohort Study. Sports Health. 2022; 14: 103-110.
  5. Henschke N, Harrison C, McKay D, Broderick C, Latimer J, Britt H, et al. Musculoskeletal conditions in children and adolescents managed in Australian primary care. BMC Musculoskelet Disord. 2014; 15: 164.
  6. Póvoas SC, Ascensão AA, Magalhães J, Seabra AF, Krustrup P, Soares JM, et al. Analysis of fatigue development during elite male handball matches. J Strength Cond Res. 2014; 28: 2640-2648.
  7. Phillips RO. A review of definitions of fatigue – And a step towards a whole definition. Transp Res Part F Traffic Psychol Behav. 2015; 29: 48-56.
  8. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev. 2001; 81: 1725-1789.
  9. Proske U. Exercise, fatigue and proprioception: a retrospective. Exp Brain Res. 2019; 237: 2447-2459.
  10. Pedersen J, Sjölander P, Wenngren BI, Johansson H. Increased intramuscular concentration of bradykinin increases the static fusimotor drive to muscle spindles in neck muscles of the cat. Pain. 1997; 70: 83-91.
  11. Pedersen J, Lönn J, Hellström F, Djupsjöbacka M, Johansson H. Localized muscle fatigue decreases the acuity of the movement sense in the human shoulder. Med Sci Sports Exerc. 1999; 31: 1047-1052.
  12. 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: 348-352.
  13. Carpenter JE, Blasier RB, Pellizzon GG. The effects of muscle fatigue on shoulder joint position sense. Am J Sports Med. 1998; 26: 262-265.
  14. Franco PG, Santos KB, Rodacki AL. Joint positioning sense, perceived force level and two-point discrimination tests of young and active elderly adults. Braz J Phys Ther. 2015; 19: 304-310.
  15. 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: 80-84.
  16. Proske U, Gandevia SC. The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol Rev. 2012; 92: 1651-1697.
  17. Clark NC, Röijezon U, Treleaven J. Proprioception in musculoskeletal rehabilitation. Part 2: Clinical assessment and intervention. Man Ther. 2015; 20: 378-387.
  18. Lephart SM, Warner JJ, Borsa PA, Fu FH. Proprioception of the shoulder joint in healthy, unstable, and surgically repaired shoulders. J Shoulder Elbow Surg. 1994; 3: 371-380.
  19. Benjaminse A, Sell TC, Abt JP, House AJ, Lephart SM. Reliability and precision of hip proprioception methods in healthy individuals. Clin J Sport Med. 2009; 19: 457-463.
  20. Waddington G, Adams R, Jones A. Wobble board (ankle disc) training effects on the discrimination of inversion movements. Aust J Physiother. 1999; 45: 95-101.
  21. Waddington G, Seward H, Wrigley T, Lacey N, Adams R. Comparing wobble board and jump-landing training effects on knee and ankle movement discrimination. J Sci Med Sport. 2000; 3: 449-59.
  22. Kristjansson E, Oddsdottir GL. “The Fly”: a new clinical assessment and treatment method for deficits of movement control in the cervical spine: reliability and validity. Spine (Phila Pa 1976). 2010; 35: E1298-E1305.
  23. Dover G, Powers ME. Reliability of Joint Position Sense and Force-Reproduction Measures During Internal and External Rotation of the Shoulder. J Athl Train. 2003; 38: 304-310.
  24. O’Leary SP, Vicenzino BT, Jull GA. A new method of isometric dynamometry for the craniocervical flexor muscles. Phys Ther. 2005; 85: 556-564.
  25. Myers JB, Guskiewicz KM, Schneider RA, Prentice WE. Proprioception and neuromuscular control of the shoulder after muscle fatigue. J Athl Train. 1999; 34: 362-367.
  26. Lee HM, Liau JJ, Cheng CK, Tan CM, Shih JT. Evaluation of shoulder proprioception following muscle fatigue. Clin Biomech (Bristol). 2003; 18: 843-847.
  27. Iida N, Kaneko F, Aoki N, Shibata E. The effect of fatigued internal rotator and external rotator muscles of the shoulder on the shoulder position sense. J Electromyogr Kinesiol. 2014; 24: 72-77.
  28. Sterner RL, Pincivero DM, Lephart SM. The effects of muscular fatigue on shoulder proprioception. Clin J Sport Med. 1998; 8: 96-101.
  29. Kablan N, Ertan H, Ünver F, Kirazci S, Korkusuz F. Factors affecting the shoulder proprioceptive sense among male volleyball players. Isokinet Exerc Sci. 2004; 12: 193-198.
  30. Chang HY, Chen CS, Wei SH, Huang CH. Recovery of Joint Position Sense in the Shoulder after Muscle Fatigue. J Sport Rehabil. 2006; 15: 312-325.
  31. Spargoli G. The acute effects of concentric versus eccentric muscle fatigue on shoulder active repositioning sense. Int J Sports Phys Ther. 2017; 12: 219-226.
  32. Guo LY, Lin CF, Yang CH, Hou YY, Chen SK, Wu WL. Evaluation of internal rotator muscle fatigue on shoulder and scapular proprioception. J Mech Med Biol. 2011; 11: 663-674.
  33. Coskun G, Talu B, Cools A. Proprioceptive force-reproduction of the rotator cuff in healthy subjects before and after muscle fatigue. Isokinet Exerc Sci. 2018; 26: 175-181.
  34. Kuhn JE. Adaptive pathology: new insights into the physical examination and imaging of the thrower’s shoulder and elbow. J Shoulder Elbow Surg. 2024; 33: 474-493.
  35. Lan N, Li Y, Sun Y, Yang FS. Reflex regulation of antagonist muscles for control of joint equilibrium position. IEEE Trans Neural Syst Rehabil Eng. 2005; 13: 60-71.
  36. Blum KP, Lamotte D’Incamps B, Zytnicki D, Ting LH. Force encoding in muscle spindles during stretch of passive muscle. PLoS Comput Biol. 2017; 13: e1005767.
  37. Matthews PB. Proprioceptors and their contribution to somatosensory mapping: complex messages require complex processing. Can J Physiol Pharmacol. 1988; 66: 430-438.
  38. Banks RW, Ellaway PH, Prochazka A, Proske U. Secondary endings of muscle spindles: Structure, reflex action, role in motor control and proprioception. Exp Physiol. 2021; 106: 2339-2366.
  39. Janwantanakul P, Magarey ME, Jones MA, Dansie BR. Variation in shoulder position sense at mid and extreme range of motion. Arch Phys Med Rehabil. 2001; 82: 840-844.