Central neuromuscular dysfunction of the deltoid muscle in patients with chronic rotator cuff tears

Alexander Berth, Géza Pap, Wolfram Neuman, Friedemann Awiszus, Alexander Berth, Géza Pap, Wolfram Neuman, Friedemann Awiszus

Abstract

Background: Previous surface electromyogram (EMG) studies have shown that chronic rotator cuff tears (RCT) may be associated with a altered activation of adjacent shoulder muscles. The effect of RCT on central neuromuscular control mechanisms of the shoulder girdle muscles such as the deltoideus muscle (DM), a key muscle of shoulder function, has as not yet been studied in detail.

Materials and methods: This study investigated the corticospinal excitability of the DM to assess the effects of RCT on the central neuromuscular function of proximal upper limb muscles. The motor-evoked potentials (MEP) in response to transcranial magnetic stimulation of DM on both sides were obtained from patients with unilateral RCT and compared with healthy control subjects.

Results: In patients, stimulus response curves of DM demonstrated a bilateral hyperexcitability at rest and a hypoexcitability during voluntary activation (F = 3.82, P = 0.007).

Conclusions: The DM hyperexcitability may be related to alterations in the sensory output from the shoulder. The insufficient facilitation of the DM points toward a bilateral central activation deficit. These findings seem to be assigned to adaptive changes in the motor cortex as a consequence of chronic RCT, and the neuromuscular alteration of the DM should be considered when treating patients with RCT.

Figures

Fig. 1
Fig. 1
Experimental setup of the study (investigation of the right side). The motor-evoked potentials (MEP) of the deltoid muscle (DM) and first dorsal interosseus muscle (FDI) were recorded after transcranial magnetic stimulation (TMS) over the scalp during rest and slight voluntary activation of the DM. Voluntary effort of the DM was exerted with a constant abduction of the arm against resistance (strap) at an angle of 40°
Fig. 2
Fig. 2
Motor-evoked potential (MEP) recruitment curves of the deltoideus muscle (DM), both sides averaged, at rest (a) and low-level muscular activity of the DM in slight voluntary abduction of the shoulder against resistance (b) in patients (filled circles) and control subjects (open circles) after transcranial magnetic stimulation (TMS) at five different stimulus levels. T individual resting motor threshold for first dorsal interosseus muscle (FDI); T+ increasing stimulus intensities given in percentage of the magnetic stimulator output (MSO)

References

    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1007/s001320050534', 'is_inner': False, 'url': 'https://doi.org/10.1007/s001320050534'}, {'type': 'PubMed', 'value': '11142903', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/11142903/'}]}
    2. Gohlke F (2000) Biomechanics of the shoulder. Orthopade 29:834–844
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '2703509', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/2703509/'}]}
    2. Norwood LA, Barrack R, Jacobson KE (1989) Clinical presentation of complete tears of the rotator cuff. J Bone Joint Surg Am 71:499–505
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/S0140-6736(00)04161-1', 'is_inner': False, 'url': 'https://doi.org/10.1016/s0140-6736(00)04161-1'}, {'type': 'PubMed', 'value': '11253973', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/11253973/'}]}
    2. Murrell GA, Walton JR (2001) Diagnosis of rotator cuff tears. Lancet 357:769–770
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '10798229', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/10798229/'}]}
    2. Habermeyer P, Lehmann L, Lichtenberg S (2000) Rotator cuff tears: diagnosis and therapy. Orthopade 29:196–208
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1055/s-2002-24250', 'is_inner': False, 'url': 'https://doi.org/10.1055/s-2002-24250'}, {'type': 'PubMed', 'value': '11935482', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/11935482/'}]}
    2. Dietz SO, Habermeyer P, Magosch P (2002) Current concepts in treatment of rotator cuff tears. Zentralbl Chir 127:194–202
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1007/s001320050538', 'is_inner': False, 'url': 'https://doi.org/10.1007/s001320050538'}, {'type': 'PubMed', 'value': '11142907', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/11142907/'}]}
    2. Loew M (2000) Traumatic development of rotator cuff lesion. Scientific principles and consequences for expert assessment. Orthopade 29:881–887
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '7706351', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/7706351/'}]}
    2. Milgrom C, Schaffler M, Gilbert S, van Holsbeeck M (1995) Rotator-cuff changes in asymptomatic adults. The effect of age, hand dominance and gender. J Bone Joint Surg Br 77:296–298
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.math.2006.07.004', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.math.2006.07.004'}, {'type': 'PubMed', 'value': '16890886', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16890886/'}]}
    2. Steenbrink F, de Groot JH, Veeger HE et al (2006) Pathological muscle activation patterns in patients with massive rotator cuff tears, with and without subacromial anaesthetics. Man Ther 11:231–237
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.jse.2004.06.010', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.jse.2004.06.010'}, {'type': 'PubMed', 'value': '15789010', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15789010/'}]}
    2. Kelly BT, Williams RJ, Cordasco FA et al (2005) Differential patterns of muscle activation in patients with symptomatic and asymptomatic rotator cuff tears. J Shoulder Elbow Surg 14:165–171
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.clinph.2006.02.005', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.clinph.2006.02.005'}, {'type': 'PubMed', 'value': '16564206', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16564206/'}]}
    2. Malcolm MP, Triggs WJ, Light KE et al (2006) Reliability of motor cortex transcranial magnetic stimulation in four muscle representations. Clin Neurophysiol 117:1037–1046
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '3791738', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/3791738/'}]}
    2. Constant CR, Murley AH (1987) A clinical method of functional assessment of the shoulder. Clin Orthop Relat Res 214:160–164
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1002/(SICI)1097-0274(199606)29:6<602::AID-AJIM4>3.0.CO;2-L', 'is_inner': False, 'url': 'https://doi.org/10.1002/(sici)1097-0274(199606)29:6<602::aid-ajim4>3.0.co;2-l'}, {'type': 'PubMed', 'value': '8773720', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/8773720/'}]}
    2. Hudak PL, Amadio PC, Bombardier C (1996) Development of an upper extremity outcome measure: the DASH (disabilities of the arm, shoulder and hand) [corrected]. The Upper Extremity Collaborative Group (UECG). Am J Ind Med 29:602–608
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/0028-3932(77)90067-7', 'is_inner': False, 'url': 'https://doi.org/10.1016/0028-3932(77)90067-7'}, {'type': 'PubMed', 'value': '896019', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/896019/'}]}
    2. Bryden MP (1977) Measuring handedness with questionnaires. Neuropsychologia 15:617–624
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/S0140-6736(85)92413-4', 'is_inner': False, 'url': 'https://doi.org/10.1016/s0140-6736(85)92413-4'}, {'type': 'PubMed', 'value': '2860322', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/2860322/'}]}
    2. Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex. Lancet 1:1106–1107
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1111/j.1460-9568.2004.03835.x', 'is_inner': False, 'url': 'https://doi.org/10.1111/j.1460-9568.2004.03835.x'}, {'type': 'PubMed', 'value': '15654863', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15654863/'}]}
    2. Tyc F, Boyadjian A, Devanne H (2005) Motor cortex plasticity induced by extensive training revealed by transcranial magnetic stimulation in human. Eur J Neurosci 21:259–266
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/S1567-424X(09)70205-3', 'is_inner': False, 'url': 'https://doi.org/10.1016/s1567-424x(09)70205-3'}, {'type': 'PubMed', 'value': '14677378', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/14677378/'}]}
    2. Awiszus F (2003) TMS and threshold hunting. Suppl Clin Neurophysiol 56:13–23
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PubMed', 'value': '2059424', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/2059424/'}]}
    2. Rothwell JC, Thompson PD, Day BL et al (1991) Stimulation of the human motor cortex through the scalp. Exp Physiol 76:159–200
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1111/j.1460-9568.2006.04760.x', 'is_inner': False, 'url': 'https://doi.org/10.1111/j.1460-9568.2006.04760.x'}, {'type': 'PubMed', 'value': '16706853', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16706853/'}]}
    2. Devanne H, Cassim F, Ethier C et al (2006) The comparable size and overlapping nature of upper limb distal and proximal muscle representations in the human motor cortex. Eur J Neurosci 23:2467–2476
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1007/PL00005641', 'is_inner': False, 'url': 'https://doi.org/10.1007/pl00005641'}, {'type': 'PubMed', 'value': '9166922', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/9166922/'}]}
    2. Devanne H, Lavoie BA, Capaday C (1997) Input–output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/S0924-980X(97)00041-6', 'is_inner': False, 'url': 'https://doi.org/10.1016/s0924-980x(97)00041-6'}, {'type': 'PubMed', 'value': '9362997', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/9362997/'}]}
    2. Ridding MC, Rothwell JC (1997) Stimulus/response curves as a method of measuring motor cortical excitability in man. Electroencephalogr Clin Neurophysiol 105:340–344
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/S0165-0270(97)02242-5', 'is_inner': False, 'url': 'https://doi.org/10.1016/s0165-0270(97)02242-5'}, {'type': 'PubMed', 'value': '9219881', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/9219881/'}]}
    2. Rothwell JC (1997) Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods 74:113–122
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PMC', 'value': 'PMC1192555', 'is_inner': False, 'url': 'http://www.ncbi.nlm.nih.gov/pmc/articles/pmc1192555/'}, {'type': 'PubMed', 'value': '3079553', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/3079553/'}]}
    2. Hess CW, Mills KR, Murray NM (1987) Responses in small hand muscles from magnetic stimulation of the human brain. J Physiol 388:397–419
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1038/35018000', 'is_inner': False, 'url': 'https://doi.org/10.1038/35018000'}, {'type': 'PubMed', 'value': '10910346', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/10910346/'}]}
    2. Hallett M (2000) Transcranial magnetic stimulation and the human brain. Nature 406:147–150
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1097/00004691-200208000-00005', 'is_inner': False, 'url': 'https://doi.org/10.1097/00004691-200208000-00005'}, {'type': 'PubMed', 'value': '12436087', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/12436087/'}]}
    2. Abbruzzese G, Trompetto C (2002) Clinical and research methods for evaluating cortical excitability. J Clin Neurophysiol 19:307–321
    1. None
    2. Awiszus F (2005) Quantification of motoneuron pool responses to transcranial magnetic stimulation with surface electromyography. Biocybern Biomed Eng 25:3–10
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.clinph.2005.04.019', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.clinph.2005.04.019'}, {'type': 'PubMed', 'value': '15982928', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15982928/'}]}
    2. Barden JM, Balyk R, Raso VJ et al (2005) Atypical shoulder muscle activation in multidirectional instability. Clin Neurophysiol 116:1846–1857
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.clinph.2003.12.033', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.clinph.2003.12.033'}, {'type': 'PubMed', 'value': '15134693', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/15134693/'}]}
    2. Zanette G, Manganotti P, Fiaschi A, Tamburin S (2004) Modulation of motor cortex excitability after upper limb immobilization. Clin Neurophysiol 115:1264–1275
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1007/s00221-007-0920-5', 'is_inner': False, 'url': 'https://doi.org/10.1007/s00221-007-0920-5'}, {'type': 'PubMed', 'value': '17361426', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/17361426/'}]}
    2. Roberts DR, Ricci R, Funke FW et al (2007) Lower limb immobilization is associated with increased corticospinal excitability. Exp Brain Res 181(2):213–220
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PMC', 'value': 'PMC6792672', 'is_inner': False, 'url': 'http://www.ncbi.nlm.nih.gov/pmc/articles/pmc6792672/'}, {'type': 'PubMed', 'value': '9547251', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/9547251/'}]}
    2. Chen R, Corwell B, Yaseen Z et al (1998) Mechanisms of cortical reorganization in lower-limb amputees. J Neurosci 18:3443–3450
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'PMC', 'value': 'PMC6792752', 'is_inner': False, 'url': 'http://www.ncbi.nlm.nih.gov/pmc/articles/pmc6792752/'}, {'type': 'PubMed', 'value': '9437031', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/9437031/'}]}
    2. Ziemann U, Corwell B, Cohen LG (1998) Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci 18:1115–1123
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.clinph.2007.04.028', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.clinph.2007.04.028'}, {'type': 'PubMed', 'value': '17576095', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/17576095/'}]}
    2. Marconi B, Pecchioli C, Koch G, Caltagirone C (2007) Functional overlap between hand and forearm motor cortical representations during motor cognitive tasks. Clin Neurophysiol 118:1767–1775
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/j.neures.2006.02.002', 'is_inner': False, 'url': 'https://doi.org/10.1016/j.neures.2006.02.002'}, {'type': 'PubMed', 'value': '16584795', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/16584795/'}]}
    2. Oliviero A, Profice P, Tonali PA et al (2006) Effects of aging on motor cortex excitability. Neurosci Res 55:74–77
    1. {'text': '', 'ref_index': 1, 'ids': [{'type': 'DOI', 'value': '10.1016/S1388-2457(02)00144-X', 'is_inner': False, 'url': 'https://doi.org/10.1016/s1388-2457(02)00144-x'}, {'type': 'PubMed', 'value': '12088713', 'is_inner': True, 'url': 'http://pubmed.ncbi.nlm.nih.gov/12088713/'}]}
    2. Wassermann EM (2002) Variation in the response to transcranial magnetic brain stimulation in the general population. Clin Neurophysiol 113:1165–1171

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