Skip to main content
Top
Published in: BMC Musculoskeletal Disorders 1/2022

Open Access 01-12-2022 | Neurotomy | Research

Shoulder muscle changes in patients with type 2 diabetes mellitus who have a painful shoulder: a quantitative muscle ultrasound study

Authors: Login Ahmed S. Alabdali, Bjorn Winkens, Geert-Jan Dinant, Nens van Alfen, Ramon P. G. Ottenheijm

Published in: BMC Musculoskeletal Disorders | Issue 1/2022

Login to get access

Abstract

Background

It is assumed that in patients with diabetic neuropathy, muscle denervation can result in shoulder disorders. Muscle denervation will lead to changes in muscle architecture, which can be assessed by quantitative muscle ultrasound (QMUS). The aim was to investigate whether increased muscle echogenicity, as a sign of neuropathy, is more often present in patients with shoulder pain who have type 2 diabetes mellitus (T2DM) than in those without.

Methods

Sixty-six patients with T2DM and 23 patients without diabetes mellitus (DM) having shoulder pain were included. Quantitative muscle ultrasound images were obtained bilaterally from the biceps brachii, deltoid, and supra- and infraspinatus muscles. The mean echogenicity (muscle ultrasound grey value) was transformed into z-scores and compared to reference values obtained from 50 healthy participants. Associations between muscle echogenicity and clinical variables were explored.

Results

In painful shoulders of both patients with T2DM and patients without DM, mean echogenicity z-scores of all muscles were significantly increased compared to healthy controls. No significant differences in echogenicity between patients with T2DM and those without DM were found. In patients with T2DM, a distal symmetric polyneuropathy was significantly associated with increased echogenicity of all muscles except the infraspinatus muscle.

Conclusions

These findings indicate that patients with painful shoulders, irrespective of having T2DM, seem to have abnormal shoulder muscles. Future studies are needed to elucidate whether neuropathy or other conditions lead to these muscle changes.
Appendix
Available only for authorised users
Literature
2.
go back to reference Abate M, Schiavone C, Salini V. Sonographic evaluation of the shoulder in asymptomatic elderly subjects with diabetes. BMC Musculoskelet Disord. 2010;11:278.PubMedPubMedCentralCrossRef Abate M, Schiavone C, Salini V. Sonographic evaluation of the shoulder in asymptomatic elderly subjects with diabetes. BMC Musculoskelet Disord. 2010;11:278.PubMedPubMedCentralCrossRef
3.
go back to reference Arkkila PE, Gautier JF. Musculoskeletal disorders in diabetes mellitus: an update. Best Pract Res Clin Rheumatol. 2003;17(6):945–70.PubMedCrossRef Arkkila PE, Gautier JF. Musculoskeletal disorders in diabetes mellitus: an update. Best Pract Res Clin Rheumatol. 2003;17(6):945–70.PubMedCrossRef
4.
go back to reference Abourazzak FE, Akasbi N, Houssaini GS, Bazouti S, Bensbaa S, Hachimi H, et al. Articular and abarticular manifestations in type 2 diabetes mellitus. Eur J Rheumatol. 2014;1(4):132–4.PubMedPubMedCentralCrossRef Abourazzak FE, Akasbi N, Houssaini GS, Bazouti S, Bensbaa S, Hachimi H, et al. Articular and abarticular manifestations in type 2 diabetes mellitus. Eur J Rheumatol. 2014;1(4):132–4.PubMedPubMedCentralCrossRef
5.
go back to reference Gwilym SE, Oag HCL, Tracey I, Carr AJ. Evidence that central sensitisation is present in patients with shoulder impingement syndrome and influences the outcome after surgery. J Bone Joint Surg (Br). 2011;93-B(4):498–502.CrossRef Gwilym SE, Oag HCL, Tracey I, Carr AJ. Evidence that central sensitisation is present in patients with shoulder impingement syndrome and influences the outcome after surgery. J Bone Joint Surg (Br). 2011;93-B(4):498–502.CrossRef
6.
go back to reference Boer BC, Boetje J, Stevens M, van den Akker-Scheek I, van Raay J. Adaptation, validity and reliability of the modified painDETECT questionnaire for patients with subacromial pain syndrome. PLoS One. 2019;14(2):e0211880.PubMedPubMedCentralCrossRef Boer BC, Boetje J, Stevens M, van den Akker-Scheek I, van Raay J. Adaptation, validity and reliability of the modified painDETECT questionnaire for patients with subacromial pain syndrome. PLoS One. 2019;14(2):e0211880.PubMedPubMedCentralCrossRef
7.
go back to reference Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, et al. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care. 2010;33(10):2285–93.PubMedPubMedCentralCrossRef Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, et al. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care. 2010;33(10):2285–93.PubMedPubMedCentralCrossRef
8.
go back to reference Pop-Busui R, Boulton AJ, Feldman EL, Bril V, Freeman R, Malik RA, et al. Diabetic neuropathy: a position statement by the American Diabetes Association. Diabetes Care. 2017;40(1):136–54.PubMedCrossRef Pop-Busui R, Boulton AJ, Feldman EL, Bril V, Freeman R, Malik RA, et al. Diabetic neuropathy: a position statement by the American Diabetes Association. Diabetes Care. 2017;40(1):136–54.PubMedCrossRef
9.
go back to reference Boulton AJ. Diabetic neuropathy: classification, measurement and treatment. Curr Opin Endocrinol Diabetes Obes. 2007;14(2):141–5.PubMedCrossRef Boulton AJ. Diabetic neuropathy: classification, measurement and treatment. Curr Opin Endocrinol Diabetes Obes. 2007;14(2):141–5.PubMedCrossRef
10.
go back to reference Patel K, Horak H, Tiryaki E. Diabetic neuropathies; 2020. Patel K, Horak H, Tiryaki E. Diabetic neuropathies; 2020.
11.
go back to reference Pica EC, Verma KK. Bilateral brachial plexopathy as an initial presentation in a newly-diagnosed, uncontrolled case of diabetes mellitus. Singap Med J. 2008;49(2):e29–32. Pica EC, Verma KK. Bilateral brachial plexopathy as an initial presentation in a newly-diagnosed, uncontrolled case of diabetes mellitus. Singap Med J. 2008;49(2):e29–32.
12.
go back to reference Ogawa K, Sasaki H, Kishi Y, Yamasaki H, Okamoto K, Yamamoto N, et al. A suspected case of proximal diabetic neuropathy predominantly presenting with scapulohumeral muscle weakness and deep aching pain. Diabetes Res Clin Pract. 2001;54(1):57–64.PubMedCrossRef Ogawa K, Sasaki H, Kishi Y, Yamasaki H, Okamoto K, Yamamoto N, et al. A suspected case of proximal diabetic neuropathy predominantly presenting with scapulohumeral muscle weakness and deep aching pain. Diabetes Res Clin Pract. 2001;54(1):57–64.PubMedCrossRef
13.
go back to reference Wada Y, Yanagihara C, Nishimura Y, Oka N. A case of diabetic amyotrophy with severe atrophy and weakness of shoulder girdle muscles showing good response to intravenous immune globulin. Diabetes Res Clin Pract. 2007;75(1):107–10.PubMedCrossRef Wada Y, Yanagihara C, Nishimura Y, Oka N. A case of diabetic amyotrophy with severe atrophy and weakness of shoulder girdle muscles showing good response to intravenous immune globulin. Diabetes Res Clin Pract. 2007;75(1):107–10.PubMedCrossRef
14.
go back to reference Kabadi UM. Diabetic amyotrophy with primary involvement of shoulder girdle. Postgrad Med. 1982;71(6):71–2, 4.PubMedCrossRef Kabadi UM. Diabetic amyotrophy with primary involvement of shoulder girdle. Postgrad Med. 1982;71(6):71–2, 4.PubMedCrossRef
15.
go back to reference Alabdali LAS, Jaeken J, van Alfen N, Dinant G-J, Borghans RA, Ottenheijm RPJJoCM. What Is the Diagnosis in Patients with Type 2 Diabetes Who Have a Painful Shoulder? Results from a Prospective Cross-Sectional Study. J Clin Med. 2020;9(12):4097.PubMedCentralCrossRef Alabdali LAS, Jaeken J, van Alfen N, Dinant G-J, Borghans RA, Ottenheijm RPJJoCM. What Is the Diagnosis in Patients with Type 2 Diabetes Who Have a Painful Shoulder? Results from a Prospective Cross-Sectional Study. J Clin Med. 2020;9(12):4097.PubMedCentralCrossRef
16.
17.
go back to reference Pillen S, Arts IM, Zwarts MJ. Muscle ultrasound in neuromuscular disorders. Muscle Nerve. 2008;37(6):679–93.PubMedCrossRef Pillen S, Arts IM, Zwarts MJ. Muscle ultrasound in neuromuscular disorders. Muscle Nerve. 2008;37(6):679–93.PubMedCrossRef
18.
go back to reference Pillen S, van Keimpema M, Nievelstein RAJ, Verrips A, van Kruijsbergen-Raijmann W, Zwarts MJ. Skeletal muscle ultrasonography: Visual versus quantitative evaluation. Ultrasound Med Biol. 2006;32(9):1315–21.PubMedCrossRef Pillen S, van Keimpema M, Nievelstein RAJ, Verrips A, van Kruijsbergen-Raijmann W, Zwarts MJ. Skeletal muscle ultrasonography: Visual versus quantitative evaluation. Ultrasound Med Biol. 2006;32(9):1315–21.PubMedCrossRef
19.
go back to reference Wijntjes J, van Alfen N. Muscle ultrasound: present state and future opportunities. Muscle Nerve. 2020. Wijntjes J, van Alfen N. Muscle ultrasound: present state and future opportunities. Muscle Nerve. 2020.
20.
go back to reference Zaidman CM, van Alfen N. Ultrasound in the assessment of Myopathic disorders. J Clin Neurophysiol. 2016;33(2):103–11.PubMedCrossRef Zaidman CM, van Alfen N. Ultrasound in the assessment of Myopathic disorders. J Clin Neurophysiol. 2016;33(2):103–11.PubMedCrossRef
22.
go back to reference Nijboer-Oosterveld J, Van Alfen N, Pillen S. New normal values for quantitative muscle ultrasound: Obesity increases muscle echo intensity. Muscle Nerve. 2011;43(1):142–3.PubMedCrossRef Nijboer-Oosterveld J, Van Alfen N, Pillen S. New normal values for quantitative muscle ultrasound: Obesity increases muscle echo intensity. Muscle Nerve. 2011;43(1):142–3.PubMedCrossRef
23.
go back to reference Kim HM, Dahiya N, Teefey SA, Keener JD, Galatz LM, Yamaguchi K. Relationship of tear size and location to fatty degeneration of the rotator cuff. J Bone Joint Surg Am. 2010;92(4):829–39.PubMedPubMedCentralCrossRef Kim HM, Dahiya N, Teefey SA, Keener JD, Galatz LM, Yamaguchi K. Relationship of tear size and location to fatty degeneration of the rotator cuff. J Bone Joint Surg Am. 2010;92(4):829–39.PubMedPubMedCentralCrossRef
24.
go back to reference van Seventer R, Vos C, Giezeman M, Meerding WJ, Arnould B, Regnault A, et al. Validation of the Dutch version of the DN4 diagnostic questionnaire for neuropathic pain. Pain Pract. 2013;13(5):390–8.PubMedCrossRef van Seventer R, Vos C, Giezeman M, Meerding WJ, Arnould B, Regnault A, et al. Validation of the Dutch version of the DN4 diagnostic questionnaire for neuropathic pain. Pain Pract. 2013;13(5):390–8.PubMedCrossRef
25.
go back to reference Van Seventer R, Vos C, Meerding W, Mear I, Le Gal M, Bouhassira D, et al. Linguistic validation of the DN4 for use in international studies. Eur J Pain. 2010;14(1):58–63.PubMedCrossRef Van Seventer R, Vos C, Meerding W, Mear I, Le Gal M, Bouhassira D, et al. Linguistic validation of the DN4 for use in international studies. Eur J Pain. 2010;14(1):58–63.PubMedCrossRef
26.
go back to reference Spallone V, Morganti R, D'Amato C, Greco C, Cacciotti L, Marfia GA. Validation of DN4 as a screening tool for neuropathic pain in painful diabetic polyneuropathy. Diabet Med. 2012;29(5):578–85.PubMedCrossRef Spallone V, Morganti R, D'Amato C, Greco C, Cacciotti L, Marfia GA. Validation of DN4 as a screening tool for neuropathic pain in painful diabetic polyneuropathy. Diabet Med. 2012;29(5):578–85.PubMedCrossRef
27.
go back to reference Van Eijk JJ, Groothuis JT, Van Alfen N. Neuralgic amyotrophy: an update on diagnosis, pathophysiology, and treatment. Muscle Nerve. 2016;53(3):337–50.PubMedCrossRef Van Eijk JJ, Groothuis JT, Van Alfen N. Neuralgic amyotrophy: an update on diagnosis, pathophysiology, and treatment. Muscle Nerve. 2016;53(3):337–50.PubMedCrossRef
28.
go back to reference Geraets JJ, de Jongh AC, Boeke AJ, Buis PA, Spinnewijn WE, Geijer RM, et al. Summary of the practice guideline for shoulder complaints from the Dutch College of General Practitioners. Ned Tijdschr Geneeskd. 2009;153:A164.PubMed Geraets JJ, de Jongh AC, Boeke AJ, Buis PA, Spinnewijn WE, Geijer RM, et al. Summary of the practice guideline for shoulder complaints from the Dutch College of General Practitioners. Ned Tijdschr Geneeskd. 2009;153:A164.PubMed
29.
go back to reference England JD, Gronseth GS, Franklin G, Miller RG, Asbury AK, Carter GT, et al. Distal symmetric polyneuropathy: a definition for clinical research: report of the American Academy of Neurology, the American Association of Electrodiagnostic Medicine, and the American Academy of physical medicine and rehabilitation. Neurology. 2005;64(2):199–207.PubMedCrossRef England JD, Gronseth GS, Franklin G, Miller RG, Asbury AK, Carter GT, et al. Distal symmetric polyneuropathy: a definition for clinical research: report of the American Academy of Neurology, the American Association of Electrodiagnostic Medicine, and the American Academy of physical medicine and rehabilitation. Neurology. 2005;64(2):199–207.PubMedCrossRef
30.
go back to reference Mineoka Y, Ishii M, Hashimoto Y, Hata S, Tominaga H, Nakamura N, et al. Limited joint mobility of the hand correlates incident hospitalisation with infection in patients with type 2 diabetes. Diabetes Res Clin Pract. 2020;161:108049.PubMedCrossRef Mineoka Y, Ishii M, Hashimoto Y, Hata S, Tominaga H, Nakamura N, et al. Limited joint mobility of the hand correlates incident hospitalisation with infection in patients with type 2 diabetes. Diabetes Res Clin Pract. 2020;161:108049.PubMedCrossRef
31.
go back to reference Beggs IBS, Bueno A, Cohen M, Court-Payen M, Grainger A, Kainberger F, et al. Musculoskeletal Ultrasound Technical Guidelines, Shoulder. Eur Soc MusculoSkeletal Radiol. 2016. Beggs IBS, Bueno A, Cohen M, Court-Payen M, Grainger A, Kainberger F, et al. Musculoskeletal Ultrasound Technical Guidelines, Shoulder. Eur Soc MusculoSkeletal Radiol. 2016.
32.
go back to reference Ottenheijm RP, Joore MA, Walenkamp GH, Weijers RE, Winkens B, Cals JW, et al. The Maastricht ultrasound shoulder pain trial (MUST): ultrasound imaging as a diagnostic triage tool to improve management of patients with non-chronic shoulder pain in primary care. BMC Musculoskelet Disord. 2011;12:154.PubMedPubMedCentralCrossRef Ottenheijm RP, Joore MA, Walenkamp GH, Weijers RE, Winkens B, Cals JW, et al. The Maastricht ultrasound shoulder pain trial (MUST): ultrasound imaging as a diagnostic triage tool to improve management of patients with non-chronic shoulder pain in primary care. BMC Musculoskelet Disord. 2011;12:154.PubMedPubMedCentralCrossRef
33.
go back to reference Scholten RR, Pillen S, Verrips A, Zwarts MJ. Quantitative ultrasonography of skeletal muscles in children: normal values. Muscle Nerve. 2003;27(6):693–8.PubMedCrossRef Scholten RR, Pillen S, Verrips A, Zwarts MJ. Quantitative ultrasonography of skeletal muscles in children: normal values. Muscle Nerve. 2003;27(6):693–8.PubMedCrossRef
34.
go back to reference Pillen S, Morava E, Van Keimpema M, Ter Laak HJ, De Vries MC, Rodenburg RJ, et al. Skeletal muscle ultrasonography in children with a dysfunction in the oxidative phosphorylation system. Neuropediatrics. 2006;37(3):142–7.PubMedCrossRef Pillen S, Morava E, Van Keimpema M, Ter Laak HJ, De Vries MC, Rodenburg RJ, et al. Skeletal muscle ultrasonography in children with a dysfunction in the oxidative phosphorylation system. Neuropediatrics. 2006;37(3):142–7.PubMedCrossRef
35.
go back to reference Hanewinckel R, Drenthen J, van Oijen M, Hofman A, van Doorn PA, Ikram MA. Prevalence of polyneuropathy in the general middle-aged and elderly population. Neurology. 2016;87(18):1892–8.PubMedCrossRef Hanewinckel R, Drenthen J, van Oijen M, Hofman A, van Doorn PA, Ikram MA. Prevalence of polyneuropathy in the general middle-aged and elderly population. Neurology. 2016;87(18):1892–8.PubMedCrossRef
36.
go back to reference Pillen S, Verrips A, van Alfen N, Arts IM, Sie LT, Zwarts MJ. Quantitative skeletal muscle ultrasound: diagnostic value in childhood neuromuscular disease. Neuromuscul Disord. 2007;17(7):509–16.PubMedCrossRef Pillen S, Verrips A, van Alfen N, Arts IM, Sie LT, Zwarts MJ. Quantitative skeletal muscle ultrasound: diagnostic value in childhood neuromuscular disease. Neuromuscul Disord. 2007;17(7):509–16.PubMedCrossRef
37.
go back to reference Pillen S, Scholten RR, Zwarts MJ, Verrips A. Quantitative skeletal muscle ultrasonography in children with suspected neuromuscular disease. Muscle Nerve. 2003;27(6):699–705.PubMedCrossRef Pillen S, Scholten RR, Zwarts MJ, Verrips A. Quantitative skeletal muscle ultrasonography in children with suspected neuromuscular disease. Muscle Nerve. 2003;27(6):699–705.PubMedCrossRef
Metadata
Title
Shoulder muscle changes in patients with type 2 diabetes mellitus who have a painful shoulder: a quantitative muscle ultrasound study
Authors
Login Ahmed S. Alabdali
Bjorn Winkens
Geert-Jan Dinant
Nens van Alfen
Ramon P. G. Ottenheijm
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2022
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/s12891-022-05627-9

Other articles of this Issue 1/2022

BMC Musculoskeletal Disorders 1/2022 Go to the issue