The Effect of Shoulder Muscle Fatigue on Acromiohumeral Distance and Scapular Dyskinesis in Women With Generalized Joint Hypermobility

in Journal of Applied Biomechanics
Restricted access

Purchase article

USD  $24.95

Student 1 year subscription

USD  $87.00

1 year subscription

USD  $116.00

Student 2 year subscription

USD  $165.00

2 year subscription

USD  $215.00

Muscle fatigue is considered to be one cause of shoulder pain, and subjects with generalized joint hypermobility (GJH) are affected more by shoulder pain. The purpose of this study was to examine the effects of muscle fatigue on acromiohumeral distance (AHD) and scapular dyskinesis in women with GJH. Thirty-six asymptomatic participants were assigned to either a GJH (n = 20) or control group (n = 16) using the Beighton scale. Before and after elevation fatigue trials, AHD was measured with ultrasonography at rest and when the arm was in 90° active elevation. A scapular dyskinesis test was used to visually observe alterations in scapular movement. Our results showed that in both groups, the fatigue reduced AHD in the 90° elevation position and increased the presence of scapular dyskinesis; however, no differences were found between the two groups. Although GJH has been identified as a factor for developing musculoskeletal disorders, generalized joint hypermobility did not result in changes to scapular dyskinesis or AHD, even after an elevation fatigue task. More studies are needed to evaluate the effects of muscle fatigue in subjects with GJH and a history of shoulder instability.

Alibazi and Moghadam are with the Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran. Cools is with the Department of Rehabilitation Sciences and Physiotherapy, University Hospital Ghent, Gent, Belgium. Bakhshi is with the Department of Statistics, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran. Ahari is with the Department of Radiology, Iran University of Medical Science, Tehran, Iran.

Address author correspondence to Afsun Nodehi Moghadam at Afsoonnodehi@gmail.com; Nodehi@uswr.ac.ir.
  • 1.

    Remvig L , Jensen DV , Ward RC . Epidemiology of general joint hypermobility and basis for the proposed criteria for benign joint hypermobility syndrome: review of the literature. J Rheumatol. 2007;34(4):804–809. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Simmonds JV , Keer RJ . Hypermobility and the hypermobility syndrome, part 2: assessment and management of hypermobility syndrome: illustrated via case studies. Man Ther. 2008;13(2):1–11. PubMed doi:10.1016/j.math.2007.11.001

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Beynnon BD , Murphy DF , Alosa DM . Predictive factors for lateral ankle sprains: a literature review. J Athl Train. 2002;37(4):376–380. PubMed

  • 4.

    Bin Abd Razak HR , Bin Ali N , Howe TS . Generalized ligamentous laxity may be a predisposing factor for musculoskeletal injuries. J Sci Med Sport. 2014;17(5):474–478. PubMed doi:10.1016/j.jsams.2013.11.001

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Ramesh R , Von Arx O , Azzopardi T , Schranz PJ . The risk of anterior cruciate ligament rupture with generalised joint laxity. J Bone Joint Surg Br. 2005;87(6):800–803. PubMed doi:10.1302/0301-620X.87B6.15833

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Blasier RB , Carpenter JE , Huston LJ . Shoulder proprioception. Effect of joint laxity, joint position, and direction of motion. Orthop Rev. 1994;23(1):45–50. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Smith TO , Jerman E , Easton V , et al. Do people with benign joint hypermobility syndrome (BJHS) have reduced joint proprioception? A systematic review and meta-analysis. Rheumatol Int. 2013;33(11):2709–2716. PubMed doi:10.1007/s00296-013-2790-4

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Simpson MR . Benign joint hypermobility syndrome: evaluation, diagnosis, and management. J Am Osteopath Assoc. 2006;106(9):531–536. PubMed

  • 9.

    Kronberg M , Brostrom LA , Nemeth G . Differences in shoulder muscle activity between patients with generalized joint laxity and normal controls. Clin Orthop Relat Res. 1991(269):181–192.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Cameron KL , Duffey ML , DeBerardino TM , Stoneman PD , Jones CJ , Owens BD . Association of generalized joint hypermobility with a history of glenohumeral joint instability. J Athl Train. 2010;45(3):253–258. PubMed doi:10.4085/1062-6050-45.3.253

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    McFarland EG , Campbell G , McDowell J . Posterior shoulder laxity in asymptomatic athletes. Am J Sports Med. 1996;24(4):468–471. PubMed doi:10.1177/036354659602400410

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Lugo R , Kung P , Ma CB . Shoulder biomechanics. Eur J Radiol. 2008;68(1):16–24. PubMed doi:10.1016/j.ejrad.2008.02.051

  • 13.

    Lucas DB . Biomechanics of the shoulder joint. Arch Surg. 1973;107(3):425–432. PubMed doi:10.1001/archsurg.1973.01350210061018

  • 14.

    Karduna AR , Williams GR , Williams JL , Iannotti JP . Kinematics of the glenohumeral joint: influences of muscle forces, ligamentous constraints, and articular geometry. J Orthop Res. 1996;14(6):986–993. PubMed doi:10.1002/jor.1100140620

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    McClure PW , Michener LA , Sennett BJ , Karduna AR . Direct 3-dimensional measurement of scapular kinematics during dynamic movements in vivo. J Shoulder Elbow Surg. 2001;10(3):269–277. PubMed doi:10.1067/mse.2001.112954

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Wadsworth DJ , Bullock-Saxton JE . Recruitment patterns of the scapular rotator muscles in freestyle swimmers with subacromial impingement. Int J Sports Med. 1997;18(8):618–624. PubMed doi:10.1055/s-2007-972692

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Bagg SD , Forrest WJ . Electromyographic study of the scapular rotators during arm abduction in the scapular plane. Am J Phys Med. 1986;65(3):111–124. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Bjelle A , Hagberg M , Michaelson G . Occupational and individual factors in acute shoulder-neck disorders among industrial workers. Br J Ind Med. 1981;38(4):356–363. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Bosch T , de Looze MP , Kingma I , Visser B , van Dieen JH . Electromyographical manifestations of muscle fatigue during different levels of simulated light manual assembly work. J Electromyogr Kinesiol. 2009;19(4):e246–e256. PubMed doi:10.1016/j.jelekin.2008.04.014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    van der Windt DA , Thomas E , Pope DP , et al. Occupational risk factors for shoulder pain: a systematic review. Occup Environ Med. 2000;57(7):433–442. PubMed doi:10.1136/oem.57.7.433

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Ludewig PM , Cook TM . Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys Ther. 2000;80(3):276–291. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Leclerc A , Chastang JF , Niedhammer I , Landre MF , Roquelaure Y ; Study Group on Repetitive Work. Incidence of shoulder pain in repetitive work. Occup Environ Med. 2004;61(1):39–44. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Chen SK , Simonian PT , Wickiewicz TL , Otis JC , Warren RF . Radiographic evaluation of glenohumeral kinematics: a muscle fatigue model. J Shoulder Elbow Surg. 1999;8(1):49–52. PubMed doi:10.1016/S1058-2746(99)90055-1

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Chopp JN , O’Neill JM , Hurley K , Dickerson CR . Superior humeral head migration occurs after a protocol designed to fatigue the rotator cuff: a radiographic analysis. J Shoulder Elbow Surg. 2010;19(8):1137–1144. PubMed doi:10.1016/j.jse.2010.03.017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Kibler WB . The role of the scapula in athletic shoulder function. Am J Sports Med. 1998;26(2):325–337. PubMed doi:10.1177/03635465980260022801

  • 26.

    Tsai NT , McClure PW , Karduna AR . Effects of muscle fatigue on 3-dimensional scapular kinematics. Arch Phys Med Rehabil. 2003;84(7):1000–1005. PubMed doi:10.1016/S0003-9993(03)00127-8

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Chopp JN , Dickerson CR . Resolving the contributions of fatigue-induced migration and scapular reorientation on the subacromial space: an orthopaedic geometric simulation analysis. Hum Mov Sci. 2012;31(2):448–460. PubMed doi:10.1016/j.humov.2011.09.005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Ebaugh DD , McClure PW , Karduna AR . Effects of shoulder muscle fatigue caused by repetitive overhead activities on scapulothoracic and glenohumeral kinematics. J Electromyogr Kinesiol. 2006;16(3):224–235. PubMed doi:10.1016/j.jelekin.2005.06.015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Johannessen EC , Reiten HS , Lovaas H , Maeland S , Juul-Kristensen B . Shoulder function, pain and health related quality of life in adults with joint hypermobility syndrome/Ehlers-Danlos syndrome-hypermobility type. Disabil Rehabil. 2016;38(14):1382–1390. PubMed doi:10.3109/09638288.2015.1102336

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Warner JJ , Lephart S , Fu FH . Role of proprioception in pathoetiology of shoulder instability. Clin Orthop Relat Res. 1996(330):35–39.

    • Search Google Scholar
    • Export Citation
  • 31.

    Desmeules F , Minville L , Riederer B , Cote CH , Fremont P . Acromio-humeral distance variation measured by ultrasonography and its association with the outcome of rehabilitation for shoulder impingement syndrome. Clin J Sport Med. 2004;14(4):197–205. PubMed doi:10.1097/00042752-200407000-00002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Maenhout A , Dhooge F , Van Herzeele M , Palmans T , Cools A . Acromiohumeral distance and 3-dimensional scapular position change after overhead muscle fatigue. J Athl Train. 2015;50(3):281–288. PubMed doi:10.4085/1062-6050-49.3.92

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Seitz AL , McClure PW , Lynch SS , Ketchum JM , Michener LA . Effects of scapular dyskinesis and scapular assistance test on subacromial space during static arm elevation. J Shoulder Elbow Surg. 2012;21(5):631–640. PubMed doi:10.1016/j.jse.2011.01.008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    McCreesh K , Adusumilli P , Evans T , Riley S , Davies A , Lewis J . Validation of ultrasound measurement of the subacromial space using a novel shoulder phantom model. Ultrasound Med Biol. 2014;40(7):1729–1733. PubMed doi:10.1016/j.ultrasmedbio.2013.12.015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    McCreesh KM , Crotty JM , Lewis JS . Acromiohumeral distance measurement in rotator cuff tendinopathy: is there a reliable, clinically applicable method? A systematic review. Br J Sports Med. 2013. doi:10.1136/bjsports-2012-092063

    • Search Google Scholar
    • Export Citation
  • 36.

    Myer GD , Ford KR , Paterno MV , Nick TG , Hewett TE . The effects of generalized joint laxity on risk of anterior cruciate ligament injury in young female athletes. Am J Sports Med. 2008;36(6):1073–1080. PubMed doi:10.1177/0363546507313572

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Quatman CE , Ford KR , Myer GD , Paterno MV , Hewett TE . The effects of gender and pubertal status on generalized joint laxity in young athletes. J Sci Med Sport. 2008;11(3):257–263. PubMed doi:10.1016/j.jsams.2007.05.005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Beighton P , Solomon L , Soskolne CL . Articular mobility in an African population. Ann Rheum Dis. 1973;32(5):413–418. PubMed doi:10.1136/ard.32.5.413

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Grahame R , Bird HA , Child A . The revised (Brighton 1998) criteria for the diagnosis of benign joint hypermobility syndrome (BJHS). J Rheumatol. 2000;27(7):1777–1779. PubMed

    • Search Google Scholar
    • Export Citation
  • 40.

    Wang HK , Lin JJ , Pan SL , Wang TG . Sonographic evaluations in elite college baseball athletes. Scand J Med Sci Sports. 2005;15(1):29–35. PubMed doi:10.1111/j.1600-0838.2004.00408.x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Azzoni R , Cabitza P , Parrini M . Sonographic evaluation of subacromial space. Ultrasonics. 2004;42(1–9):683–687. PubMed doi:10.1016/j.ultras.2003.11.015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Girometti R , De Candia A , Sbuelz M , Toso F , Zuiani C , Bazzocchi M . Supraspinatus tendon US morphology in basketball players: correlation with main pathologic models of secondary impingement syndrome in young overhead athletes. Preliminary report. Radiol Med. 2006;111(1):42–52. PubMed doi:10.1007/s11547-006-0005-8

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    McClure P , Tate AR , Kareha S , Irwin D , Zlupko E . A clinical method for identifying scapular dyskinesis, part 1: reliability. J Athl Train. 2009;44(2):160–164. PubMed doi:10.4085/1062-6050-44.2.160

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Tate AR , McClure P , Kareha S , Irwin D , Barbe MF . A clinical method for identifying scapular dyskinesis, part 2: validity. J Athl Train. 2009;44(2):165–173. PubMed doi:10.4085/1062-6050-44.2.165

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Borg G . Psychophysical scaling with applications in physical work and the perception of exertion. Scand J Work Environ Health. 1990;16(suppl 1):55–58. doi:10.5271/sjweh.1815

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Bigliani LU , Kelkar R , Flatow EL , Pollock RG , Mow VC . Glenohumeral stability. Biomechanical properties of passive and active stabilizers. Clin Orthop Relat Res. 330, 1996(330):13–30. doi:10.1097/00003086-199609000-00003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47.

    Michener LA , McClure PW , Karduna AR . Anatomical and biomechanical mechanisms of subacromial impingement syndrome. Clin Biomech (Bristol, Avon). 2003;18(5):369–379. doi:10.1016/S0268-0033(03)00047-0

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Dickerson CR , Jaclyn NC , Stephanie PB . Simulation of fatigue-initiated subacromial impingement: clarifying mechanisms. Procedia IUTAM. 2011;2:35–57. doi:10.1016/j.piutam.2011.04.005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 49.

    Itoi E , Kido T , Sano A , Urayama M , Sato K . Which is more useful, the “full can test” or the “empty can test,” in detecting the torn supraspinatus tendon? Am J Sports Med. 1999;27(1):65–68. PubMed doi:10.1177/03635465990270011901

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    Michener LA , Subasi Yesilyaprak SS , Seitz AL , Timmons MK , Walsworth MK . Supraspinatus tendon and subacromial space parameters measured on ultrasonographic imaging in subacromial impingement syndrome. Knee Surg Sports Traumatol Arthrosc. 2015;23(2):363–369. PubMed doi:10.1007/s00167-013-2542-8

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Leong HT , Tsui S , Ying M , Leung VY , Fu SN . Ultrasound measurements on acromio-humeral distance and supraspinatus tendon thickness: test-retest reliability and correlations with shoulder rotational strengths. J Sci Med Sport. 2012;15(4):284–291. PubMed doi:10.1016/j.jsams.2011.11.259

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52.

    Moghadam AN , Salimee MM . A comparative study on scapular static position between females with and without generalized joint hyper mobility. Med J Islam Repub Iran. 2012;26(3):97–102. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    Huang TS , Ou HL , Huang CY , Lin JJ . Specific kinematics and associated muscle activation in individuals with scapular dyskinesis. J Shoulder Elbow Surg. 2015;24(8):1227–1234. PubMed doi:10.1016/j.jse.2014.12.022

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54.

    Thomas SJ , Swanik CB , Kaminski TW , Higginson JS , Swanik KA , Nazarian LN . Assessment of subacromial space and its relationship with scapular upward rotation in college baseball players. J Sport Rehabil. 2013;22(3):216–223. PubMed doi:10.1123/jsr.22.3.216

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 55.

    Silva RT , Hartmann LG , Laurino CF , Bilo JP . Clinical and ultrasonographic correlation between scapular dyskinesia and subacromial space measurement among junior elite tennis players. Br J Sports Med. 2010;44(6):407–410. PubMed doi:10.1136/bjsm.2008.046284

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56.

    Giphart JE , van der Meijden OA , Millett PJ . The effects of arm elevation on the 3-dimensional acromiohumeral distance: a biplane fluoroscopy study with normative data. J Shoulder Elbow Surg. 2012;21(11):1593–1600. PubMed doi:10.1016/j.jse.2011.11.023

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 57.

    Kibler WB , Ludewig PM , McClure PW , Michener LA , Bak K , Sciascia AD . Clinical implications of scapular dyskinesis in shoulder injury: the 2013 consensus statement from the ‘Scapular Summit’. Br J Sports Med. 2013;47(14):877–885. PubMed doi:10.1136/bjsports-2013-092425

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 122 122 15
Full Text Views 6 6 2
PDF Downloads 3 3 1