Motor control integrated into muscle strengthening exercises has more effects on scapular muscle activities and joint range of motion before initiation of radiotherapy in oral cancer survivors with neck dissection: A randomized controlled trial

Yueh-Hsia Chen, Chi-Rung Lin, Wei-An Liang, Cheng-Ya Huang, Yueh-Hsia Chen, Chi-Rung Lin, Wei-An Liang, Cheng-Ya Huang

Abstract

Background: Accessory nerve shoulder dysfunction is common after neck dissection in oral cancer survivors. This study aimed to investigate the short-term effects of scapular muscle strengthening exercises with motor-control techniques on neck dissection-related shoulder dysfunction in oral cancer survivors before the initiation of radiotherapy.

Methods: Thirty-eight participants were randomly allocated into the motor-control and regular-exercise groups. Each group received conventional physical therapy and specific scapular muscle strengthening exercises for 1 month immediately after neck dissection. Motor control techniques were integrated with scapular strengthening exercises for the motor-control group. Shoulder pain, active range of motion (AROM) of shoulder abduction, and scapular muscle activities including upper trapezius (UT), middle trapezius (MT), lower trapezius (LT), and serratus anterior (SA) when performing maximal voluntary isometric contraction (MVIC) and scapular muscle exercises were evaluated at baseline and after 1 month of training.

Results: Both groups reduced shoulder pain and increased muscle activity of maximum voluntary isometric contraction (MVIC) of each muscle after the intervention. Increased AROM of shoulder abduction was only observed in the motor-control group (95% CI 3.80 to 20.51, p = 0.004). Relative to baseline evaluation, muscle activities of UT decreased in the motor-control group when performing shoulder shrug with 1-kg weight (95% CI -33.06 to -1.29, p = 0.034). Moreover, the SA activity decreased in the motor-control group (95% CI -29.73 to -27.68, p<0.001) but increased in the regular-exercise group (95% CI 28.16 to 30.05, p<0.001) when performing shoulder horizontal adduction and flexion.

Conclusion: Early strengthening exercise with motor control techniques has greater benefits for improving AROM of shoulder abduction, muscle economy, and reducing compensatory scapular muscle activities in patients with neck dissection-related shoulder dysfunction before the initiation of radiotherapy.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1. CONSORT flow diagram.
Fig 1. CONSORT flow diagram.
Fig 2. The EMG activities under the…
Fig 2. The EMG activities under the 4 MVIC conditions.
(A) Upper trapezius. (B) Middle trapezius. (C) Lower trapezius. (D) Serratus anterior. The p values are shown if any significant difference (p<0.05) between the groups or pre-post tests in that muscle.
Fig 3. Muscle activites in each muscle…
Fig 3. Muscle activites in each muscle to perform shoulder shrug.
(A) Upper trapezius. (B) Middle trapezius. (C) Lower trapezius. (D) Serratus anterior. The p values are shown if any significant difference (p<0.05) between the groups or pre-post tests in that muscle.
Fig 4. Muscle activites in each muscle…
Fig 4. Muscle activites in each muscle to perform horrizontal adduction and flexion.
(A) Upper trapezius. (B) Middle trapezius. (C) Lower trapezius. (D) Serratus anterior. The p values are shown if any significant difference (p<0.05) between the groups or pre-post tests in that muscle.
Fig 5. Muscle activites in each muscle…
Fig 5. Muscle activites in each muscle to perform one-arm row.
(A) Upper trapezius. (B) Middle trapezius. (C) Lower trapezius. (D) Serratus anterior. The p values are shown if any significant difference (p<0.05) between the groups or pre-post tests in that muscle.

References

    1. Ewing MR, Martin H. Disability following radical neck dissection; an assessment based on the postoperative evaluation of 100 patients. Cancer. 1952;5(5):873–83.
    1. Erisen L, Basel B, Irdesel J, Zarifoglu M, Coskun H, Basut O, et al. Shoulder function after accessory nerve-sparing neck dissections. Head & neck. 2004;26(11):967–71.
    1. Gane EM, Michaleff ZA, Cottrell MA, McPhail SM, Hatton AL, Panizza BJ, et al. Prevalence, incidence, and risk factors for shoulder and neck dysfunction after neck dissection: A systematic review. Eur J Surg Oncol. 2017;43(7):1199–218. 10.1016/j.ejso.2016.10.026
    1. Carr SD, Bowyer D, Cox G. Upper limb dysfunction following selective neck dissection: a retrospective questionnaire study. Head & neck. 2009;31(6):789–92.
    1. Dijkstra PU, van Wilgen PC, Buijs RP, Brendeke W, de Goede CJ, Kerst A, et al. Incidence of shoulder pain after neck dissection: a clinical explorative study for risk factors. Head & neck. 2001;23(11):947–53.
    1. McGarvey AC, Osmotherly PG, Hoffman GR, Chiarelli PE. Impact of neck dissection on scapular muscle function: a case-controlled electromyographic study. Archives of physical medicine and rehabilitation. 2013;94(1):113–9. 10.1016/j.apmr.2012.07.017
    1. Lima LP, Amar A, Lehn CN. Spinal accessory nerve neuropathy following neck dissection. Braz J Otorhinolaryngol. 2011;77(2):259–62. 10.1590/s1808-86942011000200017
    1. Orhan KS, Demirel T, Baslo B, Orhan EK, Yucel EA, Guldiken Y, et al. Spinal accessory nerve function after neck dissections. J Laryngol Otol. 2007;121(1):44–8. 10.1017/S0022215106002052
    1. McNeely ML, Parliament M, Courneya KS, Seikaly H, Jha N, Scrimger R, et al. A pilot study of a randomized controlled trial to evaluate the effects of progressive resistance exercise training on shoulder dysfunction caused by spinal accessory neurapraxia/neurectomy in head and neck cancer survivors. Head & neck. 2004;26(6):518–30.
    1. McNeely ML, Parliament MB, Seikaly H, Jha N, Magee DJ, Haykowsky MJ, et al. Effect of exercise on upper extremity pain and dysfunction in head and neck cancer survivors: a randomized controlled trial. Cancer. 2008;113(1):214–22. 10.1002/cncr.23536
    1. McGarvey AC, Hoffman GR, Osmotherly PG, Chiarelli PE. Maximizing shoulder function after accessory nerve injury and neck dissection surgery: A multicenter randomized controlled trial. Head & neck. 2015;37(7):1022–31.
    1. McGarvey AC, Osmotherly PG, Hoffman GR, Chiarelli PE. Scapular muscle exercises following neck dissection surgery for head and neck cancer: a comparative electromyographic study. Phys Ther. 2013;93(6):786–97. 10.2522/ptj.20120385
    1. Kibler WB, Sciascia A. Current concepts: scapular dyskinesis. Br J Sports Med. 2010;44(5):300–5. 10.1136/bjsm.2009.058834
    1. 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):877–85. 10.1136/bjsports-2013-092425
    1. Cools AM, Declercq GA, Cambier DC, Mahieu NN, Witvrouw EE. Trapezius activity and intramuscular balance during isokinetic exercise in overhead athletes with impingement symptoms. Scand J Med Sci Sports. 2007;17(1):25–33. 10.1111/j.1600-0838.2006.00570.x
    1. Struyf F, Cagnie B, Cools A, Baert I, Brempt JV, Struyf P, et al. Scapulothoracic muscle activity and recruitment timing in patients with shoulder impingement symptoms and glenohumeral instability. J Electromyogr Kinesiol. 2014;24(2):277–84. 10.1016/j.jelekin.2013.12.002
    1. Chen YH, Liang WA, Hsu CY, Guo SL, Lien SH, Tseng HJ, et al. Functional outcomes and quality of life after a 6-month early intervention program for oral cancer survivors: a single-arm clinical trial. PeerJ. 2018;6:e4419 10.7717/peerj.4419
    1. Carvalho AP, Vital FM, Soares BG. Exercise interventions for shoulder dysfunction in patients treated for head and neck cancer. Cochrane Database Syst Rev. 2012;4:CD008693.
    1. Cheng YJ, Tsai MH, Chiang CJ, Tsai ST, Liu TW, Lou PJ, et al. Adjuvant radiotherapy after curative surgery for oral cavity squamous cell carcinoma and treatment effect of timing and duration on outcome-A Taiwan Cancer Registry national database analysis. Cancer Med. 2018.
    1. Gallagher KK, Sacco AG, Lee JS, Taylor R, Chanowski EJ, Bradford CR, et al. Association Between Multimodality Neck Treatment and Work and Leisure Impairment: A Disease-Specific Measure to Assess Both Impairment and Rehabilitation After Neck Dissection. JAMA Otolaryngol Head Neck Surg. 2015;141(10):888–93. 10.1001/jamaoto.2015.2049
    1. Sun Q, Guo S, Wang D, Xu N, Fang QG. Shoulder Dysfunction After Radiotherapy in Surgically and Nonsurgically Treated Necks: A Prospective Study. Medicine (Baltimore). 2015;94(30):e1229.
    1. Chepeha DB, Taylor RJ, Chepeha JC, Teknos TN, Bradford CR, Sharma PK, et al. Functional assessment using Constant's Shoulder Scale after modified radical and selective neck dissection. Head & neck. 2002;24(5):432–6.
    1. Chen AM, Wang PC, Daly ME, Cui J, Hall WH, Vijayakumar S, et al. Dose—volume modeling of brachial plexus-associated neuropathy after radiation therapy for head-and-neck cancer: findings from a prospective screening protocol. Int J Radiat Oncol Biol Phys. 2014;88(4):771–7. 10.1016/j.ijrobp.2013.11.244
    1. McNeely ML, Campbell K, Ospina M, Rowe BH, Dabbs K, Klassen TP, et al. Exercise interventions for upper-limb dysfunction due to breast cancer treatment. Cochrane Database Syst Rev. 2010(6):CD005211 10.1002/14651858.CD005211.pub2
    1. Wong CK, Levine WN, Deo K, Kesting RS, Mercer EA, Schram GA, et al. Natural history of frozen shoulder: fact or fiction? A systematic review. Physiotherapy. 2017;103(1):40–7. 10.1016/j.physio.2016.05.009
    1. Cools AM, Dewitte V, Lanszweert F, Notebaert D, Roets A, Soetens B, et al. Rehabilitation of scapular muscle balance: which exercises to prescribe? Am J Sports Med. 2007;35(10):1744–51. 10.1177/0363546507303560
    1. Cricchio M, Frazer C. Scapulothoracic and scapulohumeral exercises: a narrative review of electromyographic studies. J Hand Ther. 2011;24(4):322–33; quiz 34. 10.1016/j.jht.2011.06.001
    1. Andersen CH, Zebis MK, Saervoll C, Sundstrup E, Jakobsen MD, Sjogaard G, et al. Scapular muscle activity from selected strengthening exercises performed at low and high intensities. J Strength Cond Res. 2012;26(9):2408–16. 10.1519/JSC.0b013e31823f8d24
    1. Schory A, Bidinger E, Wolf J, Murray L. A Systematic Review of the Exercises That Produce Optimal Muscle Ratios of the Scapular Stabilizers in Normal Shoulders. Int J Sports Phys Ther. 2016;11(3):321–36.
    1. Worsley P, Warner M, Mottram S, Gadola S, Veeger HE, Hermens H, et al. Motor control retraining exercises for shoulder impingement: effects on function, muscle activation, and biomechanics in young adults. J Shoulder Elbow Surg. 2013;22(4):e11–9. 10.1016/j.jse.2012.06.010
    1. Huang TS, Du WY, Wang TG, Tsai YS, Yang JL, Huang CY, et al. Progressive conscious control of scapular orientation with video feedback has improvement in muscle balance ratio in patients with scapular dyskinesis: a randomized controlled trial. J Shoulder Elbow Surg. 2018;27(8):1407–14. 10.1016/j.jse.2018.04.006
    1. Roy JS, Moffet H, Hebert LJ, Lirette R. Effect of motor control and strengthening exercises on shoulder function in persons with impingement syndrome: a single-subject study design. Man Ther. 2009;14(2):180–8. 10.1016/j.math.2008.01.010
    1. Shumway-Cook A. Motor control: theory and practical applications. 2nd ed Woollacott MH, editor. Philadelphia: Lippincott Williams & Wilkins; 2001.
    1. Goldstein DP, Ringash J, Bissada E, Jaquet Y, Irish J, Chepeha D, et al. Scoping review of the literature on shoulder impairments and disability after neck dissection. Head & neck. 2014;36(2):299–308.
    1. Chan JY, Wong ST, Chan RC, Wei WI. Shoulder Dysfunction after Selective Neck Dissection in Recurrent Nasopharyngeal Carcinoma. Otolaryngol Head Neck Surg. 2015;153(3):379–84. 10.1177/0194599815590589
    1. Norkin CC, White DJ. Measurement Of Joint Motion: A Guide To Goniometry: F.A. Davis Company; 2016.
    1. Beretta-Piccoli M, Cescon C, Barbero M, D'Antona G. Reliability of surface electromyography in estimating muscle fiber conduction velocity: A systematic review. J Electromyogr Kinesiol. 2019;48:53–68. 10.1016/j.jelekin.2019.06.005
    1. McIntosh KC, Gabriel DA. Reliability of a simple method for determining muscle fiber conduction velocity. Muscle Nerve. 2012;45(2):257–65. 10.1002/mus.22268
    1. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol. 2000;10(5):361–74. 10.1016/s1050-6411(00)00027-4
    1. Ekstrom RA, Soderberg GL, Donatelli RA. Normalization procedures using maximum voluntary isometric contractions for the serratus anterior and trapezius muscles during surface EMG analysis. J Electromyogr Kinesiol. 2005;15(4):418–28. 10.1016/j.jelekin.2004.09.006
    1. Zeger SL, Liang KY. Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 1986;42(1):121–30.
    1. Paik MC. The generalized estimating equation approach when data are not missing completely at random. Journal of the American Statistical Association. 1997;92(440):1320–9.
    1. Birhanu T, Molenberghs G, Sotto C, Kenward MG. Doubly robust and multiple-imputation-based generalized estimating equations. J Biopharm Stat. 2011;21(2):202–25. 10.1080/10543406.2011.550096
    1. Ma Y, Mazumdar M, Memtsoudis SG. Beyond repeated-measures analysis of variance: advanced statistical methods for the analysis of longitudinal data in anesthesia research. Reg Anesth Pain Med. 2012;37(1):99–105. 10.1097/AAP.0b013e31823ebc74
    1. McGarvey AC, Chiarelli PE, Osmotherly PG, Hoffman GR. Physiotherapy for accessory nerve shoulder dysfunction following neck dissection surgery: a literature review. Head & neck. 2011;33(2):274–80.
    1. Struyf F, Nijs J, Mollekens S, Jeurissen I, Truijen S, Mottram S, et al. Scapular-focused treatment in patients with shoulder impingement syndrome: a randomized clinical trial. Clinical rheumatology. 2013;32(1):73–85. 10.1007/s10067-012-2093-2
    1. Park SI, Choi YK, Lee JH, Kim YM. Effects of shoulder stabilization exercise on pain and functional recovery of shoulder impingement syndrome patients. J Phys Ther Sci. 2013;25(11):1359–62. 10.1589/jpts.25.1359
    1. Muir SW, Corea CL, Beaupre L. Evaluating change in clinical status: reliability and measures of agreement for the assessment of glenohumeral range of motion. N Am J Sports Phys Ther. 2010;5(3):98–110.
    1. Frikha M, Chaari N, Elghoul Y, Mohamed-Ali HH, Zinkovsky AV. Effects of Combined Versus Singular Verbal or Haptic Feedback on Acquisition, Retention, Difficulty, and Competence Perceptions in Motor Learning. Percept Mot Skills. 2019;126(4):713–32. 10.1177/0031512519842759
    1. Johnson G, Bogduk N, Nowitzke A, House D. Anatomy and actions of the trapezius muscle. Clin Biomech (Bristol, Avon). 1994;9(1):44–50.
    1. Ludewig PM, Cook TM, Nawoczenski DA. Three-dimensional scapular orientation and muscle activity at selected positions of humeral elevation. The Journal of orthopaedic and sports physical therapy. 1996;24(2):57–65. 10.2519/jospt.1996.24.2.57
    1. Del Balso C, Cafarelli E. Adaptations in the activation of human skeletal muscle induced by short-term isometric resistance training. J Appl Physiol (1985). 2007;103(1):402–11.
    1. Gabriel DA, Kamen G, Frost G. Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Med. 2006;36(2):133–49. 10.2165/00007256-200636020-00004
    1. Camargo PR, Alburquerque-Sendin F, Avila MA, Haik MN, Vieira A, Salvini TF. Effects of Stretching and Strengthening Exercises, With and Without Manual Therapy, on Scapular Kinematics, Function, and Pain in Individuals With Shoulder Impingement: A Randomized Controlled Trial. The Journal of orthopaedic and sports physical therapy. 2015;45(12):984–97. 10.2519/jospt.2015.5939
    1. Turgut E, Duzgun I, Baltaci G. Effects of Scapular Stabilization Exercise Training on Scapular Kinematics, Disability, and Pain in Subacromial Impingement: A Randomized Controlled Trial. Archives of physical medicine and rehabilitation. 2017;98(10):1915–23 e3. 10.1016/j.apmr.2017.05.023
    1. Sale DG. Neural adaptation to resistance training. Med Sci Sports Exerc. 1988;20(5 Suppl):S135–45. 10.1249/00005768-198810001-00009
    1. Didesch JT, Tang P. Anatomy, Etiology, and Management of Scapular Winging. The Journal of hand surgery. 2019;44(4):321–30. 10.1016/j.jhsa.2018.08.008

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