Shoulder ultrasound imaging in the post-stroke population: a systematic review and meta-analysis
DOI:
https://doi.org/10.2340/jrm.v55.13432Keywords:
hemiplegia, rotator cuff, pain, ultrasonography, rehabilitationAbstract
Objective: Post-stroke shoulder pain is a serious challenge for stroke survivors. The aim of this meta-analysis was to review the literature to confirm information on structural changes in post-stroke shoulders detected by ultrasound examination.
Methods: PubMed, Embase, Web of Science and ClinicalTrials.gov were searched until 7 December 2022, for studies describing shoulder sonographic findings in stroke patients. Two independent authors selected the studies, extracted the data, and performed the critical appraisal.
Results: A total of 23 clinical studies were included. The most prevalent pathologies in hemiplegic shoulders pertained to the biceps long head tendon (41.4%), followed by the supraspinatus tendon (33.2%), subdeltoid bursa (29.3%), acromioclavicular joint (15.0%), and subscapularis tendon (9.2%). The common pathological findings encompassed bicipital peritendinous effusion (39.2%), biceps tendinopathy (35.5%), subdeltoid bursitis (29.3%) and supraspinatus tendinopathy (24.6%). Biceps long head tendon and supraspinatus tendon abnormalities were observed significantly more in the hemiplegic (vs contralateral) shoulders, with odds ratios of 3.814 (95% confidence interval 2.044–7.117) and 2.101 (95% confidence interval 1.257–3.512), respectively. No correlation was observed between motor function and shoulder pathology.
Conclusion: Ultrasonography enabled the identification of common shoulder pathologies after stroke. Further research is needed to establish the association between these changes and the clinical course of stroke patients.
Downloads
References
Feigin VL, Stark BA, Johnson CO, Roth GA, Bisignano C, Abady GG, et al. Global, regional, and national burden of stroke and its risk factors, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet Neurol 2021; 20: 795-820.
https://doi.org/10.1016/S1474-4422(21)00252-0 DOI: https://doi.org/10.1016/S1474-4422(21)00252-0
Murie-Fernández M, Iragui MC, Gnanakumar V, Meyer M, Foley N, Teasell R. Painful hemiplegic shoulder in stroke patients: causes and management. Neurologia 2012; 27: 234-244. DOI: https://doi.org/10.1016/j.nrleng.2012.05.002
https://doi.org/10.1016/j.nrl.2011.02.010 DOI: https://doi.org/10.1016/j.nrl.2011.02.010
Dromerick AW, Edwards DF, Kumar A. Hemiplegic shoulder pain syndrome: frequency and characteristics during inpatient stroke rehabilitation. Arch Phys Med Rehabil 2008; 89: 1589-1593.
https://doi.org/10.1016/j.apmr.2007.10.051 DOI: https://doi.org/10.1016/j.apmr.2007.10.051
Prescher A. Anatomical basics, variations, and degenerative changes of the shoulder joint and shoulder girdle. Eur J Radiol 2000; 35: 88-102.
https://doi.org/10.1016/S0720-048X(00)00225-4 DOI: https://doi.org/10.1016/S0720-048X(00)00225-4
Kalichman L, Ratmansky M. Underlying pathology and associated factors of hemiplegic shoulder pain. Am J Phys Med Rehabil 2011; 90.
https://doi.org/10.1097/PHM.0b013e318214e976 DOI: https://doi.org/10.1097/PHM.0b013e318214e976
Adey-Wakeling Z, Liu E, Crotty M, Leyden J, Kleinig T, Anderson CS, et al. Hemiplegic shoulder pain reduces quality of life after acute stroke: a prospective population-based study. Am J Phys Med Rehabil 2016; 95: 758-763.
https://doi.org/10.1097/PHM.0000000000000496 DOI: https://doi.org/10.1097/PHM.0000000000000496
Turner-Stokes L, Jackson D. Shoulder pain after stroke: a review of the evidence base to inform the development of an integrated care pathway. Clin Rehabil 2002; 16: 276-298.
https://doi.org/10.1191/0269215502cr491oa DOI: https://doi.org/10.1191/0269215502cr491oa
Lo S-F, Chen S-Y, Lin H-C, Jim Y-F, Meng N-H, Kao M-J. Arthrographic and clinical findings in patients with hemiplegic shoulder pain. Arch Phys Med Rehabil 2003; 84: 1786-1791.
https://doi.org/10.1016/S0003-9993(03)00408-8 DOI: https://doi.org/10.1016/S0003-9993(03)00408-8
Kim YH, Jung SJ, Yang EJ, Paik NJ. Clinical and sonographic risk factors for hemiplegic shoulder pain: a longitudinal observational study. J Rehabil Med 2014; 46: 81-87.
https://doi.org/10.2340/16501977-1238 DOI: https://doi.org/10.2340/16501977-1238
Özçakar L, Kara M, Chang K-V, Çarl AB, Akkaya N, Tok F, et al. Nineteen reasons why physiatrists should do musculoskeletal ultrasound: EURO-MUSCULUS/USPRM recommendations. Am J Phys Med Rehabil 2015; 94: e45-e49.
https://doi.org/10.1097/PHM.0000000000000223 DOI: https://doi.org/10.1097/PHM.0000000000000223
De Jesus JO, Parker L, Frangos AJ, Nazarian LN. Accuracy of MRI, MR arthrography, and ultrasound in the diagnosis of rotator cuff tears: a meta-analysis. AJR Am J Roentgenol 2009; 192: 1701-1707.
https://doi.org/10.2214/AJR.08.1241 DOI: https://doi.org/10.2214/AJR.08.1241
Zappia M, Di Pietto F, Aliprandi A, Pozza S, De Petro P, Muda A, et al. Multi-modal imaging of adhesive capsulitis of the shoulder. Insights Imaging 2016; 7: 365-371.
https://doi.org/10.1007/s13244-016-0491-8 DOI: https://doi.org/10.1007/s13244-016-0491-8
Pong YP, Wang LY, Wang L, Leong CP, Huang YC, Chen YK. Sonography of the shoulder in hemiplegic patients undergoing rehabilitation after a recent stroke. J Clin Ultrasound 2009; 37: 199-205.
https://doi.org/10.1002/jcu.20573 DOI: https://doi.org/10.1002/jcu.20573
Huang YC, Liang PJ, Pong YP, Leong CP, Tseng CH. Physical findings and sonography of hemiplegic shoulder in patients after acute stroke during rehabilitation. J Rehabil Med 2010; 42: 21-26.
https://doi.org/10.2340/16501977-0488 DOI: https://doi.org/10.2340/16501977-0488
Kim N-H, Pyun S-B, Kwon H-K. Ultrasonographic finding of painful hemiplegic shoulder associated with motor recovery after stroke. Brain Neurorehabil 2011; 4: 44-49.
https://doi.org/10.12786/bn.2011.4.1.44 DOI: https://doi.org/10.12786/bn.2011.4.1.44
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Int J Surg 2021; 88: 105906.
https://doi.org/10.1016/j.ijsu.2021.105906 DOI: https://doi.org/10.1016/j.ijsu.2021.105906
Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010; 25: 603-605.
https://doi.org/10.1007/s10654-010-9491-z DOI: https://doi.org/10.1007/s10654-010-9491-z
Borenstein M, Hedges LV, Higgins JP, Rothstein HR. Fixed-effect versus random-effects models. Introduction to Meta-analysis 2009; 77: 85.
https://doi.org/10.1002/9780470743386.ch13 DOI: https://doi.org/10.1002/9780470743386.ch13
Higgins JP, Li T, Deeks JJ. Choosing effect measures and computing estimates of effect. Cochrane Handbook for Systematic Reviews of Interventions. Chichester (UK): John Wiley & Sons, 2019: 143-176.
https://doi.org/10.1002/9781119536604.ch6 DOI: https://doi.org/10.1002/9781119536604.ch6
Higgins JP, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, et al. Assessing risk of bias due to missing results in a synthesis. Cochrane Handbook for Systematic Reviews of Interventions: John Wiley & Sons; 2019.
Pompa A, Clemenzi A, Troisi E, Di Mario M, Tonini A, Pace L, et al. Enhanced-MRI and ultrasound evaluation of painful shoulder in patients after stroke: a pilot study. Eur Neurol 2011; 66: 175-181.
https://doi.org/10.1159/000330657 DOI: https://doi.org/10.1159/000330657
Zaiton F, Tantawy HI, Elsharkawy KAM, Sanad G. Painful poststroke shoulder: Comparison of magnetic resonance imaging and high frequency ultrasonography. Egypt J Radiol Nucl Med 2011; 42: 47-55.
https://doi.org/10.1016/j.ejrnm.2011.01.003 DOI: https://doi.org/10.1016/j.ejrnm.2011.01.003
Pong YP, Wang LY, Huang YC, Leong CP, Liaw MY, Chen HY. Sonography and physical findings in stroke patients with hemiplegic shoulders: a longitudinal study. J Rehabil Med 2012; 44: 553-557.
https://doi.org/10.2340/16501977-0987 DOI: https://doi.org/10.2340/16501977-0987
Rah UW, Yoon SH, Moon DJ, Kwack KS, Hong JY, Lim YC, et al. Subacromial corticosteroid injection on poststroke hemiplegic shoulder pain: a randomized, triple-blind, placebo-controlled trial. Arch Phys Med Rehabil 2012; 93: 949-956.
https://doi.org/10.1016/j.apmr.2012.02.002 DOI: https://doi.org/10.1016/j.apmr.2012.02.002
Doğun A, Karabay İ, Hatipoğlu C, Özgirgin N. Ultrasound and magnetic resonance findings and correlation in hemiplegic patients with shoulder pain. Top Stroke Rehabil 2014; Suppl 1: S1-7.
https://doi.org/10.1310/tsr21S1-S1 DOI: https://doi.org/10.1310/tsr21S1-S1
Huang YC, Chang KH, Liou TH, Cheng CW, Lin LF, Huang SW. Effects of Kinesio taping for stroke patients with hemiplegic shoulder pain: a double-blind, randomized, placebo-controlled study. J Rehabil Med 2017; 49: 208-215.
https://doi.org/10.2340/16501977-2197 DOI: https://doi.org/10.2340/16501977-2197
Huang YC, Leong CP, Tso HH, Chen MJ, Liaw MY, Hsieh HC, et al. The long-term effects of hyaluronic acid on hemiplegic shoulder pain and injury in stroke patients A randomized controlled study. Medicine (Baltimore) 2018; 97: 7.
https://doi.org/10.1097/MD.0000000000012078 DOI: https://doi.org/10.1097/MD.0000000000012078
Lin PH. Sonographic findings of painful hemiplegic shoulder after stroke. J Chin Med Assoc 2018; 81: 657-661.
https://doi.org/10.1016/j.jcma.2017.07.018 DOI: https://doi.org/10.1016/j.jcma.2017.07.018
Korkmaz N, Yaşar E, Demir Y, Tezen Ö, Gurcay E. Sonographic predictors in patients with hemiplegic shoulder pain: a cross-sectional study. J Stroke Cerebrovasc Dis 2020; 29: 105170.
https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.105170 DOI: https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.105170
Arya KN, Pandian S, Bhatnagar N, Sharma A. Rehabilitation of the shoulder subluxation based on ultrasonographic findings among post stroke subjects: a case series. Neurol India 2021; 69: 1309-1317.
El-Sonbaty HAE, Abou Elmaaty AA, Zarad CA, El-Bahnasawy AS. Clinical and radiological assessment of hemiplegic shoulder pain in stroke patients. Egypt J Neurol Psychiatr Neurosurg 2022; 58: 15.
https://doi.org/10.1186/s41983-022-00474-w DOI: https://doi.org/10.1186/s41983-022-00474-w
Lee CL, Chen TW, Weng MC, Wang YL, Cheng HS, Huang MH. Ultrasonographic findings in hemiplegic shoulders of stroke patients. Kaohsiung J Med Sci 2002; 18: 70-76.
Park GY, Kim JM, Sohn SI, Shin IH, Lee MY. Ultrasonographic measurement of shoulder subluxation in patients with post-stroke hemiplegia. J Rehabil Med 2007; 39: 526-530.
https://doi.org/10.2340/16501977-0099 DOI: https://doi.org/10.2340/16501977-0099
Baek S-R, Jung SH, Oh B-M, Chung SG, Sim YJ, Han TR. Ultrasonographic and physical examination to investigate the cause of painful hemiplegic shoulder. Brain Neurorehabil 2009; 2: 140-145.
https://doi.org/10.12786/bn.2009.2.2.140 DOI: https://doi.org/10.12786/bn.2009.2.2.140
Lee IS, Shin YB, Moon TY, Jeong YJ, Song JW, Kim DH. Sonography of patients with hemiplegic shoulder pain after stroke: correlation with motor recovery stage. Am J Roentgenol 2009; 192: W40-44.
https://doi.org/10.2214/AJR.07.3978 DOI: https://doi.org/10.2214/AJR.07.3978
Huang SW, Liu SY, Tang HW, Wei TS, Wang WT, Yang CP. Relationship between severity of shoulder subluxation and soft-tissue injury in hemiplegic stroke patients. J Rehabil Med 2012; 44: 733-739.
https://doi.org/10.2340/16501977-1026 DOI: https://doi.org/10.2340/16501977-1026
Pop T. Subluxation of the shoulder joint in stroke patients and the influence of selected factors on the incidence of instability. Ortop Traumatol Rehabil 2013; 15: 259-267.
https://doi.org/10.5604/15093492.1058421 DOI: https://doi.org/10.5604/15093492.1058421
Yi Y, Shim JS, Kim K, Baek SR, Jung SH, Kim W, et al. Prevalence of the rotator cuff tear increases with weakness in hemiplegic shoulder. Ann Rehabil Med 2013; 37: 471-478.
https://doi.org/10.5535/arm.2013.37.4.471 DOI: https://doi.org/10.5535/arm.2013.37.4.471
Mohamed RE, Amin MA, Aboelsafa AA. Ultrasonographic and clinical study of post-stroke painful hemiplegic shoulder. Egypt J Radiol Nucl Med 2014; 45: 1163-1170.
https://doi.org/10.1016/j.ejrnm.2014.06.011 DOI: https://doi.org/10.1016/j.ejrnm.2014.06.011
Idowu BM, Ayoola OO, Adetiloye VA, Komolafe MA. Sonographic evaluation of structural changes in post-stroke hemiplegic shoulders. Pol J Radiol 2017; 82: 141-148.
https://doi.org/10.12659/PJR.899684 DOI: https://doi.org/10.12659/PJR.899684
Elser F, Braun S, Dewing CB, Giphart JE, Millett PJ. Anatomy, function, injuries, and treatment of the long head of the biceps brachii tendon. Arthroscopy 2011; 27: 581-592.
https://doi.org/10.1016/j.arthro.2010.10.014 DOI: https://doi.org/10.1016/j.arthro.2010.10.014
Favorito PJ, Harding WG, 3rd, Heidt RS, Jr. Complete arthroscopic examination of the long head of the biceps tendon. Arthroscopy 2001; 17: 430-432.
https://doi.org/10.1053/jars.2001.22360 DOI: https://doi.org/10.1053/jars.2001.22360
Friedman DJ, Dunn JC, Higgins LD, Warner JJP. Proximal biceps tendon: injuries and management. Sports Med Arthrosc Rev 2008; 16.
https://doi.org/10.1097/JSA.0b013e318184f549 DOI: https://doi.org/10.1097/JSA.0b013e318184f549
Chang K-V, Wu W-T, Özçakar L. Association of bicipital peritendinous effusion with subacromial impingement: a dynamic ultrasonographic study of 337 shoulders. Sci Rep 2016; 6: 38943.
https://doi.org/10.1038/srep38943 DOI: https://doi.org/10.1038/srep38943
Chang K-V, Chen W-S, Wang T-G, Hung C-Y, Chien K-L. Associations of sonographic abnormalities of the shoulder with various grades of biceps peritendinous effusion (BPE). Ultrasound Med Biol 2014; 40: 313-321.
https://doi.org/10.1016/j.ultrasmedbio.2013.10.002 DOI: https://doi.org/10.1016/j.ultrasmedbio.2013.10.002
de Witte PB, Werner S, ter Braak LM, Veeger HEJ, Nelissen RGHH, de Groot JH. The supraspinatus and the deltoid - not just two arm elevators. Hum Mov Sci 2014; 33: 273-283.
https://doi.org/10.1016/j.humov.2013.08.010 DOI: https://doi.org/10.1016/j.humov.2013.08.010
Kibler BW, McMullen J. Scapular dyskinesis and its relation to shoulder pain. J Am Acad Orthop Surg 2003; 11: 142-151.
https://doi.org/10.5435/00124635-200303000-00008 DOI: https://doi.org/10.5435/00124635-200303000-00008
Paci M, Nannetti L, Taiti P, Baccini M, Pasquini J, Rinaldi L. Shoulder subluxation after stroke: relationships with pain and motor recovery. Physiother Res Int 2007; 12: 95-104.
https://doi.org/10.1002/pri.349 DOI: https://doi.org/10.1002/pri.349
Ward SR, Hentzen ER, Smallwood LH, Eastlack RK, Burns KA, Fithian DC, et al. Rotator cuff muscle architecture: implications for glenohumeral stability. Clin Orthop Relat Res 2006; 448: 157-163.
https://doi.org/10.1097/0000214443.87645.bb DOI: https://doi.org/10.1097/0000214443.87645.bb
Draghi F, Scudeller L, Draghi AG, Bortolotto C. Prevalence of subacromial-subdeltoid bursitis in shoulder pain: an ultrasonographic study. J Ultrasound 2015; 18: 151-158.
https://doi.org/10.1007/s40477-015-0167-0 DOI: https://doi.org/10.1007/s40477-015-0167-0
van Holsbeeck M, Strouse PJ. Sonography of the shoulder: evaluation of the subacromial-subdeltoid bursa. Am J Roentgenol 1993; 160: 561-564.
https://doi.org/10.2214/ajr.160.3.8430553 DOI: https://doi.org/10.2214/ajr.160.3.8430553
Awerbuch MS. The clinical utility of ultrasonography for rotator cuff disease, shoulder impingement syndrome and subacromial bursitis. Med J Aust 2008; 188: 50-53.
https://doi.org/10.5694/j.1326-5377.2008.tb01507.x DOI: https://doi.org/10.5694/j.1326-5377.2008.tb01507.x
Daghir AA, Sookur PA, Shah S, Watson M. Dynamic ultrasound of the subacromial-subdeltoid bursa in patients with shoulder impingement: a comparison with normal volunteers. Skeletal Radiol 2012; 41: 1047-1053.
https://doi.org/10.1007/s00256-011-1295-z DOI: https://doi.org/10.1007/s00256-011-1295-z
Precerutti M, Garioni E, Madonia L, Draghi F. US anatomy of the shoulder: pictorial essay. J Ultrasound 2010; 13: 179-187. Hollister MS, Mack LA, Patten RM, Winter TC, 3rd, Matsen FA, 3rd, Veith RR. Association of sonographically detected subacromial/subdeltoid bursal effusion and intraarticular fluid with rotator cuff tear. Am J Roentgenol 1995; 165: 605-608.
https://doi.org/10.2214/ajr.165.3.7645478 DOI: https://doi.org/10.2214/ajr.165.3.7645478
Additional Files
Published
How to Cite
License
Copyright (c) 2023 Ting-Yu Lin, Peng-Chieh Shen, Ke-Vin Chang, Wei-Ting Wu, Levent Özçakar
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
All digitalized JRM contents is available freely online. The Foundation for Rehabilitation Medicine owns the copyright for all material published until volume 40 (2008), as from volume 41 (2009) authors retain copyright to their work and as from volume 49 (2017) the journal has been published Open Access, under CC-BY-NC licences (unless otherwise specified). The CC-BY-NC licenses allow third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material for non-commercial purposes, provided proper attribution to the original work.
From 2024, articles are published under the CC-BY licence. This license permits sharing, adapting, and using the material for any purpose, including commercial use, with the condition of providing full attribution to the original publication.
