Advertisement
Journal of Shoulder and Elbow Surgery

Bilateral shoulder proprioception deficit in unilateral anterior shoulder instability

Published:November 28, 2018DOI:https://doi.org/10.1016/j.jse.2018.08.034

      Hypothesis and background

      Proprioception is an important element of shoulder dynamic stability. It has been shown to be affected in cases of capsular or labral injuries of the glenohumeral joint. Therefore, this study was conducted to investigate bilateral shoulder proprioception by active reproduction of joint position both in patients with post-traumatic recurrent unilateral shoulder instability and in normal healthy volunteers.

      Methods

      We compared 41 patients, comprising 11 female and 30 male patients with an average age of 25.6 years (range, 18-39 years), with post-traumatic unilateral anterior shoulder instability with a control group of 27 healthy volunteers with no history of shoulder problems and with normal shoulder function during examination. All patients were examined using a high-accuracy computer-controlled electronic goniometer (Propriometer). The error of active reproduction of joint position (EARJP) was measured in abduction, flexion, external rotation, and internal rotation in both shoulders.

      Results

      We observed a significant deficit in the EARJP in the unstable shoulders within the instability group. Surprisingly, similar results were recorded for the contralateral, unaffected shoulders within this group of patients compared with the control group. Joint acuity increased with higher elevation of the arm position.

      Conclusion

      Unilateral shoulder injuries, resulting in instability, affect proprioception in both shoulders, as demonstrated by an increased EARJP. This is the first report of unilateral shoulder instability coexisting with inferior proprioception in both shoulders.

      Level of evidence

      Keywords

      To read this article in full you will need to make a payment

      References

        • Ager A.L.
        • Roy J.S.
        • Roos M.
        • Belley A.F.
        • Cools A.
        • Hébert L.J.
        Shoulder proprioception: how is it measured and is it reliable? A systematic review.
        J Hand Ther. 2017; 30: 221-231
        • Alstermark B.
        • Isa T.
        • Pettersson L.G.
        • Sasaki S.
        The C3-C4 propriospinal system in the cat and monkey: a spinal pre-motoneuronal centre for voluntary motor control.
        Acta Physiol (Oxf). 2007; 189: 123-140
        • Anderson V.B.
        • Wee E.
        Impaired joint proprioception at higher shoulder elevations in chronic rotator cuff pathology.
        Arch Phys Med Rehabil. 2011; 92: 1146-1151
        • Aydin T.
        • Yildiz Y.
        • Yanmis C.
        • Kalyon T.
        Shoulder proprioception: a comparison between the shoulder joint in healthy and surgically repaired shoulders.
        Arch Orthop Trauma Surg. 2001; 121: 422-425
        • Badagliacco J.A.
        • Karduna A.
        College pitchers demonstrate directional differences in shoulder joint position sense compared to controls.
        J Sport Rehabil. 2017; 17: 1-19
        • Bank P.J.
        • Peper C.E.
        • Marinus J.
        • Beek P.J.
        • van Hilten J.J.
        Motor consequences of experimentally induced limb pain: a systematic review.
        Eur J Pain. 2013; 17: 145e57
        • Barden J.M.
        • Balyk R.
        • Raso V.J.
        • Moreau M.
        • Bagnall K.
        Dynamic upper limb proprioception in multidirectional shoulder instability.
        Clin Orthop Relat Res. 2004; 420: 181-189
        • Blasier R.B.
        • Carpenter J.E.
        • Huston L.J.
        Shoulder proprioception: effect of joint laxity, joint position, and direction of motion.
        Orthop Rev. 1994; 23: 45-50
        • Brunt D.
        • Andersen J.C.
        • Huntsman B.
        • Reinhert L.B.
        • Thorell A.L.
        • Sterling J.C.
        Postural responses to lateral perturbation in healthy subjects and ankle sprain patients.
        Med Sci Sports Exerc. 1992; 24: 171-176
        • Burkhead Jr, W.Z.
        • Rockwood Jr, C.A.
        Treatment of instability of the shoulder with an exercise program.
        J Bone Joint Surg Am. 1992; 74: 890-896
        • Derscheid G.L.
        • Brown W.C.
        Rehabilitation of the ankle.
        Clin Sports Med. 1985; 4: 527-544
        • Dilek B.
        • Gulbahar S.
        • Gundogdu M.
        • Ergin B.
        • Manisali M.
        • Ozkan M.
        • et al.
        Efficacy of proprioceptive exercises in patients with subacromial impingement syndrome: a single-blinded randomized controlled study.
        Am J Phys Med Rehabil. 2016; 95: 169-182
        • Dos Santos G.L.
        • Salazar L.F.
        • Lazarin A.C.
        • de Russo T.L.
        Joint position sense is bilaterally reduced for shoulder abduction and flexion in chronic hemiparetic individuals.
        Top Stroke Rehabil. 2015; 22: 271-280
        • Emery C.A.
        • Roy T.O.
        • Whittaker J.L.
        • Nettel-Aguirre A.
        • van Mechelen W.
        Neuromuscular training injury prevention strategies in youth sport: a systematic review and meta-analysis.
        Br J Sports Med. 2015; 49: 865-870
        • Etty Griffin L.Y.
        Neuromuscular training and injury prevention in sports.
        Clin Orthop Relat Res. 2003; 409: 53-60
        • Fortier S.
        • Basset F.A.
        The effects of exercise on limb proprioceptive signals.
        J Electromyogr Kinesiol. 2012; 22: 795-802
        • Freeman M.A.
        • Wyke B.
        Articular contributions to limb muscle reflexes. The effects of partial neurectomy of the knee-joint on postural reflexes.
        Br J Surg. 1966; 53: 61-68
        • Fremerey R.
        • Bosch U.
        • Freitag N.
        • Lobenhoffer P.
        • Wippermann B.
        Proprioception and EMG pattern after capsulolabral reconstruction in shoulder instability: a clinical and experimental study.
        Knee Surg Sports Traumatol Arthrosc. 2006; 14: 1315-1320
        • Fyhr C.
        • Gustavsson L.
        • Wassinger C.
        • Sole G.
        The effects of shoulder injury on kinaesthesia: a systematic review and meta-analysis.
        Man Ther. 2015; 20: 28-37
        • Goble D.J.
        Proprioceptive acuity assessment via joint position matching: from basic science to general practice.
        Phys Ther. 2010; 90: 1176-1184
        • Goble D.J.
        • Coxon J.P.
        • Van Impe A.
        • Geurts M.
        • Doumas M.
        • Wenderoth N.
        • et al.
        Brain activity during ankle proprioceptive stimulation predicts balance performance in young and older adults.
        J Neurosci. 2011; 31: 16344-16352
        • Haik M.N.
        • Camargo P.R.
        • Zanca G.G.
        • Alburquerque-Sendín F.
        • Salvini T.F.
        • Mattiello-Rosa S.M.
        Joint position sense is not altered during shoulder medial and lateral rotations in female assembly line workers with shoulder impingement syndrome.
        Physiother Theory Pract. 2013; 29: 41-50
        • Haller S.
        • Cunningham G.
        • Laedermann A.
        • Hofmeister J.
        • Van De Ville D.
        • Lovblad K.O.
        • et al.
        Shoulder apprehension impacts large-scale functional brain networks.
        AJNR Am J Neuroradiol. 2014; 35: 691-697
        • Han J.
        • Waddington G.
        • Adams R.
        • Anson J.
        • Liu Y.
        Assessing proprioception: a critical review of methods.
        J Sport Health Sci. 2016; 5: 80-90
        • Hasan Z.
        • Stuart D.G.
        Animal solutions to problems of movement control: the role of proprioceptors.
        Annu Rev Neurosci. 1988; 11: 199-223
        • Hodges P.
        • van den Hoorn W.
        • Dawson A.
        • Cholewicki J.
        Changes in the mechanical properties of the trunk in low back pain may be associated with recurrence.
        J Biomech. 2009; 42: 61e6
        • Hung Y.J.
        • Darling W.G.
        Shoulder position sense during passive matching and active positioning tasks in individuals with anterior shoulder instability.
        Phys Ther. 2012; 92: 563-573
        • 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
        • Itoi E.
        • Hsu H.
        • An K.
        Biomechanical investigation of glenohumeral joint.
        J Shoulder Elbow Surg. 1996; 5: 407-424
        • Jaggi A.
        • Lambert S.
        Rehabilitation for shoulder instability.
        Br J Sports Med. 2010; 44: 333-340
        • Jankowska E.
        Interneuronal relay in spinal pathways from proprioceptors.
        Prog Neurobiol. 1992; 38: 335-378
        • Janwantanakul P.
        • Magarey M.E.
        • Jones M.A.
        • Dansie B.R.
        Variation in shoulder position sense at mid and extreme range of motion.
        Arch Phys Med Rehabil. 2001; 82: 840-844
        • Jerosch J.
        • Thorwesten L.
        • Steinbeck J.
        • Reer R.
        Proprioceptive function of shoulder girdle in healthy volunteers.
        Knee Surg Sports Traumatol Arthrosc. 1996; 3: 219-225
        • Kim S.H.
        • Park J.C.
        • Park J.S.
        • Oh I.
        Painful jerk test: a predictor of success in nonoperative treatment of posteroinferior instability of the shoulder.
        Am J Sports Med. 2004; 32: 1849-1855
        • Koralewicz L.M.
        • Engh G.A.
        Comparison of proprioception in arthritic and age-matched normal knees.
        J Bone Joint Surg Am. 2000; 82: 1582-1588
        • Lephart S.M.
        • Myers J.B.
        • Bradley J.P.
        • Fu F.H.
        Shoulder proprioception and function following thermal capsulorraphy.
        Arthroscopy. 2002; 18: 770-778
        • Lephart S.M.
        • Warner J.
        • Borsa P.
        Proprioception of the shoulder joint in healthy, unstable, and surgically repaired shoulders.
        J Shoulder Elbow Surg. 1994; 3: 371-380
        • Lin Y.L.
        • Karduna A.
        Errors in shoulder joint position sense mainly come from the glenohumeral joint.
        J Appl Biomech. 2017; 33: 32-38
        • Lubiatowski P.
        • Ogrodowicz P.
        • Wojtaszek M.
        • Kaniewski R.
        • Stefaniak J.
        • Dudzinski W.
        • et al.
        Measurement of active shoulder proprioception: dedicated system and device.
        Eur J Orthop Surg Traumatol. 2013; 23: 177-183
        • Lubiatowski P.
        • Olczak I.
        • Lisiewicz E.
        • Ogrodowicz P.
        • Bręborowicz M.
        • Romanowski L.
        Elbow joint position sense after total elbow arthroplasty.
        J Shoulder Elbow Surg. 2014; 23: 693-700
        • Machner A.
        • Merk H.
        • Becker R.
        • Rohkohl K.
        • Wissel H.
        • Pap G.
        Kinesthetic sense of the shoulder in patients with impingement syndrome.
        Acta Orthop Scand. 2003; 1: 85-88
        • Markey K.L.
        Functional rehabilitation of the anterior cruciate ligament deficient knee.
        Sports Med. 1991; 12: 407-417
        • Myers J.B.
        • Lephart S.M.
        The role of the sensorimotor system in the athletic shoulder.
        J Athl Train. 2000; 35: 351-363
        • Myers J.B.
        • Oyama S.
        Sensorimotor factors affecting outcome following shoulder injury.
        Clin Sports Med. 2008; 27: 481-490
        • Oldfield R.C.
        The assessment and analysis of handedness: the Edinburgh inventory.
        Neuropsychologia. 1971; 9: 97-113
        • Pettersson L.G.
        • Alstermark B.
        • Blagovechtchenski E.
        • Isa T.
        • Sasaski S.
        Skilled digit movements in feline and primate-recovery after selective spinal cord lesions.
        Acta Physiol (Oxf). 2007; 189: 141-154
        • Pollock R.
        Role of shoulder stabilization relative to restoration of neuromuscular control in joint kinematics.
        in: Lephart S. Fu F. Proprioception and neuromuscular control in joint stability. 1st ed. Human Kinetics, Champaign, IL2000: 265-275
        • Pötzl W.
        • Thorwesten L.
        • Götze C.
        • Garmann S.
        • Steinbeck J.
        Proprioception of the shoulder joint after surgical repair for instability: a long-term follow up study.
        Am J Sports Med. 2004; 32: 425-430
        • Relph N.
        • Herrington L.
        The effect of conservatively treated a ACL injury on knee joint position sense.
        Int J Sports Phys Ther. 2016; 11: 536-543
        • Roberts D.
        • Fridén T.
        • Stomberg A.
        • Lindstrand A.
        • Moritz U.
        Bilateral proprioceptive defects in patients with a unilateral anterior cruciate ligament reconstruction: a comparison between patients and healthy individuals.
        J Orthop Res. 2000; 18: 565-571
        • Roga M.
        • Lubiatowski P.
        • Lisiewicz E.
        • Romanowski L.
        Analysis of normal glenohumeral joint proprioception.
        Issue Rehabil Orthop Neurophysiol Sport Promot. 2013; 5: 15-30
        • Safran M.R.
        • Borsa P.A.
        • Lephart S.M.
        • Fu F.H.
        • Warner J.J.
        Shoulder proprioception in baseball pitchers.
        J Shoulder Elbow Surg. 2001; 10: 438-444
        • Sahin E.
        • Dilek B.
        • Baydar M.
        • Gundogdu M.
        • Ergin B.
        • Manisali M.
        • et al.
        Shoulder proprioception in patients with subacromial impingement syndrome.
        J Back Musculoskelet Rehabil. 2017; 30: 857-862
        • Salles J.I.
        • Velasques B.
        • Cossich V.
        • Nicoliche E.
        • Ribeiro P.
        • Amaral M.V.
        • et al.
        Strength training and shoulder proprioception.
        J Athl Train. 2015; 50: 277-280
        • Shitara H.
        • Shimoyama D.
        • Sasaki T.
        • Hamano N.
        • Ichinose T.
        • Yamamoto A.
        • et al.
        The neural correlates of shoulder apprehension: a functional MRI study.
        PLoS One. 2015; 10 (e0137387)
        • Smetacek V.
        • Mechsner F.
        Making sense.
        Nature. 2004; 432: 21
        • Sole G.
        • Osborne H.
        • Wassinger C.
        The effect of experimentally-induced subacromial pain on proprioception.
        Man Ther. 2015; 20: 166-170
        • 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
        • Sullivan J.A.
        • Hoffman M.A.
        • Harter R.A.
        Shoulder joint position sense after thermal, open, and arthroscopic capsulorrhaphy for recurrent anterior instability.
        J Shoulder Elbow Surg. 2008; 17: 389-394
        • Suprak D.N.
        • Osternig L.R.
        • van Donkelaar P.
        • Karduna A.R.
        Shoulder joint position sense improves with elevation angle in a novel, unconstrained task.
        J Orthop Res. 2006; 24: 559-568
        • Takasaki H.
        • Lim E.C.
        • Soon B.
        The effect of shoulder muscle fatigue on active repositioning acuity and scapulothoracic resting alignment: a systematic review with meta-analysis.
        Phys Ther Sport. 2016; 20: 61-78
        • Tibone J.E.
        • Fechter J.
        • Kao J.T.
        Evaluation of a proprioception pathway in patients with stable and unstable shoulders with somatosensory cortical evoked potentials.
        J Shoulder Elbow Surg. 1997; 6: 440-443
        • Tripp B.L.
        • Yochem E.M.
        • Uhl T.L.
        Functional fatigue and upper extremity sensorimotor system acuity in baseball athletes.
        J Athl Train. 2007; 42: 90-98
        • Vafadar A.K.
        • Côté J.N.
        • Archambault P.S.
        Sex differences in the shoulder joint position sense acuity: a cross-sectional study.
        BMC Musculoskelet Disord. 2015; 16: 273
        • Wassinger C.A.
        • Myers J.B.
        • Gatti J.M.
        • Conley K.M.
        • Lephart S.M.
        Proprioception and throwing accuracy in the dominant shoulder after cryotherapy.
        J Athl Train. 2007; 42: 84-89
        • Yasuda K.
        • Sato Y.
        • Iimura N.
        • Iwata H.
        Allocation of attentional resources toward a secondary cognitive task leads to compromised ankle proprioceptive performance in healthy young adults.
        Rehabil Res Pract. 2014; 2014: 7
        • Zanchi D.
        • Cunningham G.
        • Lädermann A.
        • Ozturk M.
        • Hoffmeyer P.
        • Haller S.
        Structural white matter and functional connectivity alterations in patients with shoulder apprehension.
        Sci Rep. 2017; 7: 42327
        • Zuckerman J.D.
        • Gallagher M.A.
        • Cuomo F.
        • Rokito A.
        The effect of instability and subsequent anterior shoulder repair on proprioceptive ability.
        J Shoulder Elbow Surg. 2003; 12: 105-109