Estimating Muscle Forces for Breast Cancer Survivors During Functional Tasks

in Journal of Applied Biomechanics

Click name to view affiliation

Angelica E. LangUniversity of Saskatchewan

Search for other papers by Angelica E. Lang in
Current site
Google Scholar
PubMed
Close
*
,
Soo Y. KimUniversity of Saskatchewan

Search for other papers by Soo Y. Kim in
Current site
Google Scholar
PubMed
Close
*
,
Stephan MilosavljevicUniversity of Saskatchewan

Search for other papers by Stephan Milosavljevic in
Current site
Google Scholar
PubMed
Close
*
, and
Clark R. DickersonUniversity of Waterloo

Search for other papers by Clark R. Dickerson in
Current site
Google Scholar
PubMed
Close
*
Restricted access

Breast cancer survivors have known scapular kinematic alterations that may be related to the development of secondary morbidities. A measure of muscle activation would help understand the mechanisms behind potential harmful kinematics. The purpose of this study was to define muscle force strategies in breast cancer survivors. Shoulder muscle forces during 6 functional tasks were predicted for 25 breast cancer survivors (divided by impingement pain) and 25 controls using a modified Shoulder Loading Analysis Module. Maximum forces for each muscle were calculated, and 1-way analysis of variance (P < .05) was used to identify group differences. The differences between maximum predicted forces and maximum electromyography were compared with repeated-measures analysis of variance (P < .05) to evaluate the success of the model predictions. Average differences between force predictions and electromyography ranged from 7.3% to 31.6% but were within the range of previously accepted differences. Impingement related pain in breast cancer survivors is associated with increased force of select shoulder muscles. Both pectoralis major heads, upper trapezius, and supraspinatus peak forces were higher in the pain group across all tasks. These force prediction differences are also associated with potentially harmful kinematic strategies, providing a direction for possible rehabilitation strategies.

Lang is with the Department of Health Sciences, College of Medicine, University of Saskatchewan, Saskatoon, SK, Canada. Kim and Milosavljevic are with the School of Rehabilitation Science, College of Medicine, University of Saskatchewan, Saskatoon, SK, Canada. Dickerson is with the Department of Kinesiology, Faculty of Applied Health Sciences, University of Waterloo, Waterloo, ON, Canada.

Dickerson (cdickers@uwaterloo.ca) is corresponding author.
  • Collapse
  • Expand
  • 1.

    Lang AE, Murphy M, Dickerson CR, Stavness I, Kim SY. Factors related to shoulder dysfunction in breast cancer survivors. Rehabil Oncol. 2020.

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

    Verbelen H, Tjalma W, Meirte J, Gebruers N. Long-term morbidity after a negative sentinel node in breast cancer patients. Eur J Cancer Care. 2019;28(5):e13077. PubMed ID: 31050088 doi:10.1111/ecc.13077

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

    Lee CH, Chung SY, Kim WY, Yang SN. Effect of breast cancer surgery on chest tightness and upper limb dysfunction. Medicine. 2019;98(19):e15524. PubMed ID: 31083196 doi:10.1097/MD.0000000000015524

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    De Groef A, Van Kampen M, Tieto E, et al. Arm lymphoedema and upper limb impairments in sentinel node-negative breast cancer patients: a one year follow-up study Arm lymphoedema and upper limb impairments in sentinel node-negative breast cancer patients: a one year follow-up study. Breast. 2016;29:102108. PubMed ID: 27479040 doi:10.1016/j.breast.2016.07.021

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

    Ebaugh D, Spinelli B, Schmitz KH. Shoulder impairments and their association with symptomatic rotator cuff disease in breast cancer survivors. Med Hypotheses. 2011;77(4):481487. PubMed ID: 21764521 doi:10.1016/j.mehy.2011.06.015

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

    Yang EJ, Park WB, Seo KS, Kim SW, Heo CY, Lim JY. Longitudinal change of treatment-related upper limb dysfunction and its impact on late dysfunction in breast cancer survivors: a prospective cohort study. J Surg Oncol. 2010;101(1):8491. PubMed ID: 19924721 doi:10.1002/jso.21435

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

    Lang AE, Dickerson CR, Kim SY, Stobart J, Milosavljevic S. Impingement pain affects kinematics of breast cancer survivors in work-related functional tasks. Clin Biomech. 2019;70:223230. PubMed ID: 31669920 doi:10.1016/j.clinbiomech.2019.10.001

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

    Ludewig PM, Reynolds JF. The association of scapular kinematics and glenohumeral joint pathologies. J Orthop Sports Phys Ther. 2009;39(2):90104. PubMed ID: 19194022 doi:10.2519/jospt.2009.2808

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Campbell ST, Ecklund KJ, Chu EH, McGarry MH, Gupta R, Lee TQ. The role of pectoralis major and latissimus dorsi muscles in a biomechanical model of massive rotator cuff tear. J Shoulder Elbow Surg. 2014;23(8):11361142. PubMed ID: 24560467 doi:10.1016/j.jse.2013.11.030

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

    Hotta GH, Santos AL, McQuade KJ, de Oliveira AS. Scapular-focused exercise treatment protocol for shoulder impingement symptoms: three-dimensional scapular kinematics analysis. Clin Biomech. 2018;51:7681. PubMed ID: 29245139 doi:10.1016/j.clinbiomech.2017.12.005

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

    Chopp-Hurley JN, Brookham RL, Dickerson CR. Identification of potential compensatory muscle strategies in a breast cancer survivor population: a combined computational and experimental approach. Clin Biomech. 2016;40:6367. PubMed ID: 27825052 doi:10.1016/j.clinbiomech.2016.10.015

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

    Lemieux PO, Nuño N, Hagemeister N, Tétreault P. Mechanical analysis of cuff tear arthropathy during multiplanar elevation with the AnyBody shoulder model. Clin Biomech. 2012;27(8):801806. PubMed ID: 22652501 doi:10.1016/j.clinbiomech.2012.04.008

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Dalberg K, Krawiec K, Sandelin K. Eleven-year follow-up of a randomized study of pectoral fascia preservation after mastectomy for early breast cancer. World J Surg. 2010;34(11):25392544. PubMed ID: 20730429 doi:10.1007/s00268-010-0737-4

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    de Haan A, Toor A, Hage JJ, Veeger HEJ, Woerdeman LAE. Function of the pectoralis major muscle after combined skin-sparing mastectomy and immediate reconstruction by subpectoral implantation of a prosthesis. Ann Plast Surg. 2007;59(6):605610. PubMed ID: 18046138 doi:10.1097/SAP.0b013e31803429dd

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

    Shamley DR, Srinanaganathan R, Weatherall R, et al. Changes in shoulder muscle size and activity following treatment for breast cancer. Breast Cancer Res Treat. 2007;106(1):1927. PubMed ID: 17221154 doi:10.1007/s10549-006-9466-7

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

    Dickerson CR, Chaffin DB, Hughes RE. A mathematical musculoskeletal shoulder model for proactive ergonomic analysis. Comput Methods Biomech Biomed Engin. 2007;10(6):389400. PubMed ID: 17891574 doi:10.1080/10255840701592727

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

    de Groot JH, Brand R. A three-dimensional regression model of the shoulder rhythm. Clin Biomech. 2001;16(9):735743. PubMed ID: 11714550 doi:10.1016/S0268-0033(01)00065-1

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

    Grewal TJ, Dickerson CR. A novel three-dimensional shoulder rhythm definition that includes overhead and axially rotated humeral postures. J Biomech. 2013;46(3):608611. PubMed ID: 23141955 doi:10.1016/j.jbiomech.2012.09.028

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

    Wu W, Lee PVS, Ackland DC. The sensitivity of shoulder muscle and joint force predictions to changes in joint kinematics: a Monte-Carlo analysis. Gait Posture. 2017;54:8792. PubMed ID: 28279851 doi:10.1016/j.gaitpost.2017.02.027

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

    Calis¸ M, Akgün K, Birtane M, Karacan I, Calis¸ H, Tüzün F. Diagnostic values of clinical diagnostic tests in subacromial impingement syndrome. Ann Rheum Dis. 2000;59(1):4447. PubMed ID: 10627426 doi:10.1136/ard.59.1.44

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

    Moen MH, de Vos RJ, Ellenbecker TS, Weir A. Clinical tests in shoulder examination: how to perform them. Br J Sports Med. 2010;44(5):370375. PubMed ID: 20371563 doi:10.1136/bjsm.2010.071928

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

    Wu G, van der Helm FC, Veeger HE, et al. ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motion—part II: shoulder, elbow, wrist and hand. J Biomech. 2005;38(5):981992. PubMed ID: 15844264 doi:10.1016/j.jbiomech.2004.05.042

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

    Lang AE, Kim SY, Milosavljevic S, Dickerson CR. The utility of the acromion marker cluster (AMC) in a clinical population. J Electromyogr Kinesiol. 2019 ;102298. PubMed ID: 31006518 doi:10.1016/j.jelekin.2019.04.002

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

    van Andel C, van Hutten K, Eversdijk M, Veeger D, Harlaar J. Recording scapular motion using an acromion marker cluster. Gait Posture. 2009;29(1):123128. PubMed ID: 18815043 doi:10.1016/j.gaitpost.2008.07.012

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

    Brookham RL, Cudlip AC, Dickerson CR. Quantification of upper limb electromyographic measures and dysfunction of breast cancer survivors during performance of functional dynamic tasks. Clin Biomech. 2018;52:713. PubMed ID: 29306754 doi:10.1016/j.clinbiomech.2017.12.011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Cram JR, Kasman GS. Cram’s Introduction to Surface Electromyography. 2nd ed. Mississauga, Canada: Jones and Bartlett Publishers; 1998.

    • Search Google Scholar
    • Export Citation
  • 27.

    Lafayette Instrument. Purdue Pegboard Test. 2002:142. Lafayette, IN: Lafayette Instruments.

  • 28.

    Lafayette Instrument. The Minnesota Dexterity Test Examiners Manual. 1998. Lafayette, IN: Lafayette Instruments.

  • 29.

    Reneman MF, Soer R, Gerrits EHJ. Basis for an FCE methodology for patients with work-related upper limb disorders. J Occup Rehabil. 2005;15(3):353363. PubMed ID: 16119226 doi:10.1007/s10926-005-5942-x

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

    Winter DA. Biomechanics and Motor Control of Human Movement. 4th ed. Hoboken, NJ: John Wiley & Sons; 2009.

  • 31.

    Drake JDM, Callaghan JP. Elimination of electrocardiogram contamination from electromyogram signals: an evaluation of currently used removal techniques. J Electromyogr Kinesiol. 2006;16(2):175187. PubMed ID: 16139521 doi:10.1016/j.jelekin.2005.07.003

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

    Dickerson CR, Hughes RE, Chaffin DB. Experimental evaluation of a computational shoulder musculoskeletal model. Clin Biomech. 2008;23(7):886894. PubMed ID: 18502010 doi:10.1016/j.clinbiomech.2008.04.004

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

    Högfors C, Sigholm G, Herberts P. Biomechanical model of the human shoulder—I. Elements. J Biomech. 1987;20(2):157166. PubMed ID: 3571296 doi:10.1016/0021-9290(87)90307-1

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

    Dul J, Johnson GE, Shiavi R, Townsend MA. Muscular synergism-II. A minimum-fatigue criterion for load sharing between synergistic muscles. J Biomech. 1984;17(9):675684. PubMed ID: 6501327 doi:10.1016/0021-9290(84)90121-0

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

    Howarth SJ, Callaghan JP. Compressive force magnitude and intervertebral joint flexion/extension angle influence shear failure force magnitude in the porcine cervical spine. J Biomech. 2012;45(3):484490. PubMed ID: 22196209 doi:10.1016/j.jbiomech.2011.11.051

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Disselhorst-klug C, Schmitz-rode T, Rau G. Surface electromyography and muscle force: limits in sEMG—force relationship and new approaches for applications. Clin Biomech. 2009;24(3):225235. PubMed ID: 18849097 doi:10.1016/j.clinbiomech.2008.08.003

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

    Blache Y, Dal Maso F, Desmoulins L, Plamondon A, Begon M. Superficial shoulder muscle co-activations during lifting tasks: influence of lifting height, weight and phase. J Electromyogr Kinesiol. 2015;25(2):355362. PubMed ID: 25483204 doi:10.1016/j.jelekin.2014.11.004

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

    Lindstroem R, Graven-Nielsen T, Falla D. Current pain and fear of pain contribute to reduced maximum voluntary contraction of neck muscles in patients with chronic neck pain. Arch Phys Med Rehabil. 2012;93(11):20422048. PubMed ID: 22546536 doi:10.1016/j.apmr.2012.04.014

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

    Phadke V, Camargo PR, Ludewig PM. Scapular and rotator cuff muscle activity during arm elevation: a review of normal function and alterations with shoulder impingement. Rev Bras Fisioter. 2009;13(1):19. PubMed ID: 20411160 doi:10.1590/S1413-35552009005000012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Paine R, Voight ML. The role of the scapula. Int J Sports Phys Ther. 2013;8(5):617629. PubMed ID: 24175141

  • 41.

    Galiano-Castillo N, Fernández -Lao C, Cantarero-Villanueva I, Fernández-de-Las-Peñas C, Menjón-Beltrán S, Arroyo-Morales M. Altered pattern of cervical muscle activation during performance of a functional upper limb task in breast cancer survivors. Am J Phys Med Rehabil. 2011;90(5):349355. PubMed ID: 21765253 doi:10.1097/PHM.0b013e318214e406

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

    Leidenius M, Leppänen E, Krogerus L, Von Smitten K. Motion restriction and axillary web syndrome after sentinel node biopsy and axillary clearance in breast cancer. Am J Surg. 2003;185(2):127130. PubMed ID: 12559441 doi:10.1016/S0002-9610(02)01214-X

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

    Kuehn T, Klauss W, Darsow M, et al. Long-term morbidity following axillary dissection in breast cancer patients—clinical assessment, significance for life quality and the impact of demographic, oncologic and therapeutic factors. Breast Cancer Res Treat. 2000;64(3):275286. PubMed ID: 11200778 doi:10.1023/A:1026564723698

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

    Braman JP, Engel SC, LaPrade RF, Ludewig PM. In vivo assessment of scapulohumeral rhythm during unconstrained overhead reaching in asymptomatic subjects. J Shoulder Elbow Surg. 2009;18(6):960967. PubMed ID: 19395283 doi:10.1016/j.jse.2009.02.001

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

    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):269277. PubMed ID: 11408911 doi:10.1067/mse.2001.112954

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

    Roren A, Nguyen C, Palazzo C, et al. Kinematic analysis of the shoulder complex after anatomic and reverse total shoulder arthroplasty: a cross-sectional study. Musculoskelet Sci Pract. 2017;29:8490. PubMed ID: 28347934 doi:10.1016/j.msksp.2017.03.006

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

    Seitz AL, Mcclure PW, Finucane S, Boardman ND, Michener LA. Clinical Biomechanics Mechanisms of rotator cuff tendinopathy: intrinsic, extrinsic, or both? Clin Biomech. 2011;26(1):112. PubMed ID: 20846766 doi:10.1016/j.clinbiomech.2010.08.001

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

    Michener LA, McClure PW, Karduna AR. Anatomical and biomechanical mechanisms of subacromial impingement syndrome. Clin Biomech. 2003;18(5):369379. PubMed ID: 12763431 doi:10.1016/S0268-0033(03)00047-0

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

    Dark A, Ginn KA, Halaki M. Shoulder muscle recruitment patterns during commonly used rotator cuff exercises: an electromyographic study. Phys Ther. 2007;87(8):10391046. PubMed ID: 17578940 doi:10.2522/ptj.20060068

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 2412 898 104
Full Text Views 59 10 0
PDF Downloads 53 15 0