Electromyographic assessment of muscle fatigue in massive rotator cuff tear
Introduction
Effective shoulder function is essential for many activities of daily living. Coordinated synchronous activity of shoulder girdle muscles is required to limit translation of the humeral head on the shallow glenoid fossa (Bey et al., 2008, Poppen and Walker, 1978). Rotator cuff muscle activity plays a fundamental role in maintaining glenohumeral joint (GHJ) stability (Burkhart, 1991, Inman et al., 1944, Yanagawa et al., 2008), ‘stiffening’ the GHJ to establish a stable fulcrum (David et al., 2000).
Rotator cuff tears are prevalent in the elderly (Sher et al., 1995, Tempelhof et al., 1999). A tear larger than 5 cm or involving 2 or more rotator cuff tendons is defined as a ‘massive rotator cuff tear’ (MRCT) (Cofield, 1981, Gerber et al., 2000). An MRCT often has significant impact on quality of life due to impaired shoulder strength and range of movement, and consequently reduced ability to perform essential daily activities. A MRCT disrupts the glenohumeral fulcrum, leading to abnormal superior translation of the humeral head on the glenoid fossa during arm elevation as the destabilising force generated by the deltoid muscle is unopposed (Terrier et al., 2007, Yamaguchi et al., 2000). The altered joint mechanics results in a disabling condition which can impact on functional capacity and quality of life. However, despite this anatomical deficit, some patients with a MRCT are able to maintain function. This has led to the hypothesis that alternative muscle activation strategies can compensate for the deficient rotator cuff to establish a stable glenohumeral fulcrum for arm movement (Hansen et al., 2008, Steenbrink et al., 2006, Steenbrink et al., 2009).
The outcome of surgical interventions for MRCT depends on several factors such as age, activity level, joint stability, and associated degenerative changes (Dines et al., 2006, Gerber et al., 2011). High rates of re-tear follow rotator cuff repair (Galatz et al., 2004) and tendon transfer or shoulder arthroplasty are the main options when the tear is irreparable (Boes et al., 2006). Physiotherapy has been suggested as a key alternative intervention in the management of MRCT when tear is irreparable and symptomatic (Ainsworth and Lewis, 2007). However, evidence is lacking to support the development of effective rehabilitation protocols which target compensatory muscle activation strategies and fatigue-susceptible muscles. While a few studies have investigated the activation pattern of shoulder girdle muscles in MRCT, their fatigability not been studied. Identification of potentially fatigable muscles in the upper limb kinetic chain is needed to support the development of tailored rehabilitation protocols.
Muscular fatigue is a time-dependent process occurring during muscular contraction, resulting in manifestations such as tremor, pain and inability to achieve a desired force output (De Luca, 1984). Its importance in MRCT is that altered muscle force generation caused by deficient rotator cuff function may contribute to decreased GHJ stability. Shoulder muscle fatigue has been studied using electromyography (EMG) in healthy subjects during isometric arm elevation tasks, in which the greatest fatigue is observed in the deltoid and rotator cuff muscles (Minning et al., 2007, Nieminen et al., 1995). However, appropriate measurement of muscle fatigue in painful conditions such as MRCT presents a significant challenge.
Shoulder pain directly alters muscle activation strategies, partly to protect painful structures (Diederichsen et al., 2009) and partly as movement avoidance due to fear of pain (Alizadehkhaiyat et al., 2007). These factors complicate comparisons with healthy controls, so an alternative approach is required. Hand grip tasks activate key shoulder girdle muscles by exploiting the principles of the kinetic chain (Alizadehkhaiyat et al., 2011, Sporrong et al., 1995, Sporrong et al., 1996, Sporrong et al., 1998). This can provide a practical way of studying shoulder muscle fatigue, albeit only in a particular position, in patients with MRCT while limiting pain and potential sources of confounding.
Shoulder muscle fatigue has not been measured before in MRCT. Hence, the central aim of the present study was to determine and compare the fatigability of key shoulder girdle muscles in groups of MRCT patients and healthy controls during a pain-free task representative of daily activities. We further aimed to evaluate the functional impact of MRCT on patients’ quality of life using validated scores. The combined results are intended to provide a base of knowledge for future clinical studies aiming to compare current rehabilitation protocols and promote the development of effective evidence-based programmes.
Section snippets
Participants
The control group (CG) comprised 14 healthy subjects with no history of upper limb painful conditions or surgery, and normal upper limb clinical examination. The mean (±SD) age was 36 ± 15 year, height 175 ± 10 cm and mass 77 ± 15 kg. The arm tested was randomly selected. The MRCT group (MRCTG) including 12 patients were recruited from a specialised Upper Limb Unit in a major orthopaedic centre during 2009–2011. Patients typically presented with shoulder pain and loss of both strength and range of
Results
All subjects completed the study protocol, with no dropout due to pain or other factors. There were no significant intra-session effects with regard to the normalised MDF slope or initial MDF for any of the muscles studied.
Discussion
Peripheral (muscular) (Merton, 1954) and central (central nervous system) (Brasil-Neto et al., 1994, Brasil-Neto et al., 1993) factors contribute to localised muscular fatigue according to the particular demands of the motor task. EMG has been extensively used to study muscular fatigue, and its consistent lower-frequency shift during a sustained contraction underlies the application of the MDF slope as a fatigue index (Hof, 1991, Stulen and DeLuca, 1981).
Fatigue has been studied in normal
Conflict of interest
None.
Acknowledgement
We are grateful to Mr. P. Watt for his technical assistance. None of the authors report any conflict of interest.
D.H. Hawkes gained his primary medical degree from the University of Liverpool in 2010. He received his MPhil in Musculoskeletal Science from the same institute for work on rotator cuff tears. He embarked upon his orthopaedic surgical training in 2012 and gained Membership to the Royal College of Surgeons in 2013. His research interests focus on the multimodaility assessment of shoulder pathology particularly using complex signal analysis techniques for electromyographic data.
References (69)
- et al.
Assessment of functional recovery in tennis elbow
J Electromyogr Kinesiol
(2009) - et al.
Shoulder muscle activation and fatigue during a controlled forceful hand grip task
J Electromyogr Kinesiol
(2011) - et al.
Methods to reduce the variability of EMG power spectrum estimates
J Electromyogr Kinesiol
(1998) - et al.
Measuring dynamic in-vivo glenohumeral joint kinematics: technique and preliminary results
J Biomech
(2008) - et al.
EMG and strength correlates of selected shoulder muscles during rotations of the glenohumeral joint
Clin Biomech (Bristol, Avon)
(2000) - et al.
Interpretation of EMG changes with fatigue: facts, pitfalls, and fallacies
J Electromyogr Kinesiol
(2003) - et al.
Assessment of low back muscle fatigue by surface EMG signal analysis: methodological aspects
J Electromyogr Kinesiol
(2003) - et al.
The upper limb functional index: development and determination of reliability, validity, and responsiveness
J Hand Therap
(2006) - et al.
Treatment options for massive rotator cuff tears
J Shoulder Elbow Surg
(2011) - et al.
Forearm extensor and flexor muscle exertion during simulated gripping work – an electromyographic study
Clin Biomech (Bristol, Avon)
(1997)
Roles of deltoid and rotator cuff muscles in shoulder elevation
Clin Biomech (Bristol, Avon)
The impact of rotator cuff pathology on isometric and isokinetic strength, function, and quality of life
J Shoulder Elbow Surg
Reliability and validity of grip and pinch strength evaluations
J Hand Surg Am
Suprascapular nerve block disrupts the normal pattern of scapular kinematics
Clin Biomech (Bristol, Avon)
Indices of muscle fatigue
J Electromyogr Kinesiol
EMG analysis of shoulder muscle fatigue during resisted isometric shoulder elevation
J Electromyogr Kinesiol
Muscular synergy in the shoulder during a fatiguing static contraction
Clin Biomech (Bristol, Avon)
An electromyographic analysis of functional differentiation in human pectoralis major muscle
J Electromyogr Kinesiol
The effect of light manual precision work on shoulder muscles – an EMG analysis
J Electromyogr Kinesiol
Pathological muscle activation patterns in patients with massive rotator cuff tears, with and without subacromial anaesthetics
Man Ther
Glenohumeral stability in simulated rotator cuff tears
J Biomech
Age-related prevalence of rotator cuff tears in asymptomatic shoulders
J Shoulder Elbow Surg
Effect of supraspinatus deficiency on humerus translation and glenohumeral contact force during abduction
Clin Biomech (Bristol, Avon)
Measurement of human muscle fatigue
J Neurosci Methods
Glenohumeral motion in patients with rotator cuff tears: a comparison of asymptomatic and symptomatic shoulders
J Shoulder Elbow Surg
Physiotherapy rehabilitation in patients with massive, irreparable rotator cuff tears
Musculoskelet Care
Exercise therapy for the conservative management of full thickness tears of the rotator cuff: a systematic review
Br J Sports Med
Pain, functional disability, and psychologic status in tennis elbow
Clin J Pain
Neuromuscular fatigue and aging: central and peripheral factors
Muscle Nerve
Age-related differences in muscle fatigue vary by contraction type: a meta-analysis
Phys Ther
Muscles alive: their functions revealed by electromyography
Diagnosis and management of massive rotator cuff tears: the surgeon’s dilemma
Instr Course Lect
Hand-grip dynamometry predicts future outcomes in aging adults
J Geriatr Phys Ther
Postexercise depression of motor evoked potentials: a measure of central nervous system fatigue
Exp Brain Res
Cited by (17)
Mechanical characteristic of supraspinatus muscle changes independent of its size and intramuscular fat in patient with rotator cuff repair
2023, Journal of Electromyography and KinesiologyChanges in shoulder muscle activities and glenohumeral motion after rotator cuff repair: an assessment using ultrasound real-time tissue elastography
2021, Journal of Shoulder and Elbow SurgeryElectromyographic analysis of selected shoulder muscles during a series of exercises commonly used in patients with symptomatic degenerative rotator cuff tears
2020, Journal of Shoulder and Elbow SurgeryCitation Excerpt :It is unclear whether different muscle activity patterns would be apparent in the presence of an RC tear. It is known that patients with RC tears have different muscle recruitment mainly of the deltoid compared with healthy controls during elevation movements.2,11 Future studies should examine muscle activity patterns during shoulder rehabilitation exercises in this specific population.
The effects of repetitive bouts of a fatiguing exertion (with breaks) on the slope of EMG measures of localized muscle fatigue
2020, Journal of Electromyography and KinesiologyCitation Excerpt :One area of the EMG fatigue response that has not yet been explored is the effect of repetitive bouts of a fatiguing exertion (with intermittent breaks) on the slope of these EMG-based measures of localized muscle fatigue. As noted above there have been a number of studies (e.g. Lindstrӧm et al., 1977; Doheny et al., 2008; Evans et al., 2018; da Silva et al., 2015; Hawkes et al., 2015; Pereira et al., 2011; Merletti et al., 1984) that have considered the use of the time-dependent slope of these EMG parameters as a way of assessing the rate of development of fatigue. However, none of these studies have explored how intermittent breaks might influence the rate of fatigue development in individual bouts.
Evolution of a capacitive electromyography contactless biosensor: Design and modelling techniques
2019, Measurement: Journal of the International Measurement ConfederationCan grip strength be used as a surrogate marker to monitor recovery from shoulder fatigue?
2018, Journal of Electromyography and Kinesiology
D.H. Hawkes gained his primary medical degree from the University of Liverpool in 2010. He received his MPhil in Musculoskeletal Science from the same institute for work on rotator cuff tears. He embarked upon his orthopaedic surgical training in 2012 and gained Membership to the Royal College of Surgeons in 2013. His research interests focus on the multimodaility assessment of shoulder pathology particularly using complex signal analysis techniques for electromyographic data.
O. Alizadehkhaiyat received his MD from the Tabriz University of Medical Science, Iran in 1995, and his PhD in musculoskeletal sciences/sports medicine from the University of Liverpool, UK in 2006. Following a 7-year clinical research work at the University of Liverpool, he joined Liverpool Hope University in 2013, where he is an Associate Professor in the School of Health Sciences (Sport and Exercise Science). His main research interests include evaluation of Neuromuscular Function in healthy population, sporting activities, and patients with musculoskeletal conditions with a special interest in the use of electromyographic (EMG) and kinematics.
G.J. Kemp qualified in medicine at the University of Oxford in 1980. After specializing in clinical biochemistry he undertook full-time laboratory and clinical research work first at the University of Sheffield and then at the Medical Research Council Biochemical and Clinical Magnetic Resonance Research Unit at Oxford. In 1996, he joined the University of Liverpool, where he is a Professor in the Department of Musculoskeletal Biology. His research interests include several aspects of muscle function and biochemistry, with a special interest in the use of magnetic resonance and other non-invasive techniques in biomedical research.
Professor A.C. Fisher is a Consultant Clinical Scientist and Head of Department (Medical Physics and Clinical Engineering) at the Royal Liverpool University Hospital and Director of the Merseyside Training Consortium in Medical Physics and Clinical Engineering. He is a Fellow of the Institute of Engineering and Technology (FIET CEng) and a Fellow of the Institute of Physics and Engineering in Medicine (FIPEM CSci). He holds an MSc in Biomedical Engineering (Surrey) and a PhD in Medical Physics and Bioengineering (Liverpool). His principal research interests include biomedical signal processing, mathematical modelling, artificial intelligence, and instrumentation.
Dr. M.M. Roebuck received her BA in Physiological Science from the University of Oxford in 1976 and her MA and D.Phil. from the University of Oxford in 1982. She is currently a research fellow in the Musculoskeletal Science Research Group at the University of Liverpool. Her primary research interests are aseptic loosening of joint implants, osteoarthritis, upper limb pathologies such as rotator cuff disorders or subacromial impingement syndrome and soft tissue sarcoma.
S.P. Frostick received his BA in Physiological Science from University of Oxford in 1975, his FRCS from Royal College of Surgeons in 1983, and his MA and DM from University of Oxford in 1983 and 1988, respectively. He is currently a Professor of Orthopaedics at the University of Liverpool and the director of Musculoskeletal Science Research Group. His primary research interest is in musculoskeletal diseases and injuries with an emphasis on upper limb, particularly peripheral nerve injuries, malignancy, thrombophilia, and rotator cuff disorders