Skip to main content
Top
Published in: European Journal of Trauma and Emergency Surgery 2/2021

01-04-2021 | Painful Arc | Original Article

Muscle fat content in the intact infraspinatus muscle correlates with age and BMI, but not critical shoulder angle

Authors: Helen Anwander, Fabian Fuhrer, Gaëlle Diserens, Beat Kaspar Moor, Chris Boesch, Peter Vermathen, Waldo Valenzuela, Matthias A. Zumstein

Published in: European Journal of Trauma and Emergency Surgery | Issue 2/2021

Login to get access

Abstract

Purpose

Muscle fat content of the rotator cuff increases after a tear. In the healthy rotator cuff, the influence of age, body mass index (BMI) and critical shoulder angle (CSA) on muscle fat content is unknown. The primary aim was to correlate muscle fat content with age, BMI and CSA. The secondary aims were (1) to correlate muscle fat content in the entire muscle and slice Y (most lateral sagittal slice with scapular spine) and (2) assessed the reliability for CSA measurement in MRI.

Methods

In 26 healthy shoulders (17 subjects), aged 40–65 years, BMI 20–35 kg/m2, Goutallier grade 0, Dixon MRI was applied. The CSA was > 35° in 14 shoulders and < 30° in 12 shoulders. Muscle fat content was calculated from Dixon MRI.

Results

Infraspinatus muscle fat content correlates moderately with age (r = 0.553; p = 0.003) and BMI (r = 0.517; p = 0.007). Supraspinatus muscle fat content does not correlate with age (r = 0.363, p = 0.069) and BMI (r = 0.342, p = 0.087). No correlation between CSA and muscle fat content was found. Muscle fat content measurement in the entire muscle correlates strongly with measurement in slice Y (intraclass correlation coefficient supraspinatus muscle: 0.757; infraspinatus muscle: 0.794). CSA intermethod analysis between radiography and MR images shows very high reliability (intraclass correlation coefficient > 0.9) and no systematical deviation in Bland–Altman analysis.

Conclusion

Muscle fat content in the healthy infraspinatus muscle does correlate with age and BMI, but not with the CSA. Muscle fat content measurement in the rotator cuff using Dixon MRI showed a high reliability between slice Y and the entire muscle.

Level of evidence

III.
Literature
1.
go back to reference Kuzel BR, Grindel S, Papandrea R, Ziegler D. Fatty infiltration and rotator cuff atrophy. J Am Acad Orthop Surg. 2013;21(10):613–23.CrossRef Kuzel BR, Grindel S, Papandrea R, Ziegler D. Fatty infiltration and rotator cuff atrophy. J Am Acad Orthop Surg. 2013;21(10):613–23.CrossRef
2.
go back to reference Melis B, Wall B, Walch G. Natural history of infraspinatus fatty infiltration in rotator cuff tears. J Shoulder Elbow Surg. 2010;19(5):757–63.CrossRef Melis B, Wall B, Walch G. Natural history of infraspinatus fatty infiltration in rotator cuff tears. J Shoulder Elbow Surg. 2010;19(5):757–63.CrossRef
3.
go back to reference Meyer DC, Hoppeler H, von Rechenberg B, Gerber C. A pathomechanical concept explains muscle loss and fatty muscular changes following surgical tendon release. J Orthopaed Res. 2004;22(5):1004–7.CrossRef Meyer DC, Hoppeler H, von Rechenberg B, Gerber C. A pathomechanical concept explains muscle loss and fatty muscular changes following surgical tendon release. J Orthopaed Res. 2004;22(5):1004–7.CrossRef
4.
go back to reference Barry JJ, Lansdown DA, Cheung S, Feeley BT, Ma CB. The relationship between tear severity, fatty infiltration, and muscle atrophy in the supraspinatus. J Shoulder Elbow Surg. 2013;22(1):18–25.CrossRef Barry JJ, Lansdown DA, Cheung S, Feeley BT, Ma CB. The relationship between tear severity, fatty infiltration, and muscle atrophy in the supraspinatus. J Shoulder Elbow Surg. 2013;22(1):18–25.CrossRef
5.
go back to reference Gumucio JP, Korn MA, Saripalli AL, Flood MD, Phan AC, Roche SM, et al. Aging-associated exacerbation in fatty degeneration and infiltration after rotator cuff tear. J Shoulder Elbow Surg. 2014;23(1):99–108.CrossRef Gumucio JP, Korn MA, Saripalli AL, Flood MD, Phan AC, Roche SM, et al. Aging-associated exacerbation in fatty degeneration and infiltration after rotator cuff tear. J Shoulder Elbow Surg. 2014;23(1):99–108.CrossRef
6.
go back to reference Melis B, Nemoz C, Walch G. Muscle fatty infiltration in rotator cuff tears: descriptive analysis of 1688 cases. OTSR. 2009;95(5):319–24.PubMed Melis B, Nemoz C, Walch G. Muscle fatty infiltration in rotator cuff tears: descriptive analysis of 1688 cases. OTSR. 2009;95(5):319–24.PubMed
7.
go back to reference Pfirrmann CW, Schmid MR, Zanetti M, Jost B, Gerber C, Hodler J. Assessment of fat content in supraspinatus muscle with proton MR spectroscopy in asymptomatic volunteers and patients with supraspinatus tendon lesions. Radiology. 2004;232(3):709–15.CrossRef Pfirrmann CW, Schmid MR, Zanetti M, Jost B, Gerber C, Hodler J. Assessment of fat content in supraspinatus muscle with proton MR spectroscopy in asymptomatic volunteers and patients with supraspinatus tendon lesions. Radiology. 2004;232(3):709–15.CrossRef
8.
go back to reference Moor BK, Bouaicha S, Rothenfluh DA, Sukthankar A, Gerber C. Is there an association between the individual anatomy of the scapula and the development of rotator cuff tears or osteoarthritis of the glenohumeral joint? A radiological study of the critical shoulder angle. Bone Joint J. 2013;95-B(7):935–41. Moor BK, Bouaicha S, Rothenfluh DA, Sukthankar A, Gerber C. Is there an association between the individual anatomy of the scapula and the development of rotator cuff tears or osteoarthritis of the glenohumeral joint? A radiological study of the critical shoulder angle. Bone Joint J. 2013;95-B(7):935–41.
9.
go back to reference Goutallier D, Postel JM, Bernageau J, Lavau L, Voisin MC. Fatty muscle degeneration in cuff ruptures. Pre- and postoperative evaluation by CT scan. Clinical orthopaedics and related research. 1994(304):78–83. Goutallier D, Postel JM, Bernageau J, Lavau L, Voisin MC. Fatty muscle degeneration in cuff ruptures. Pre- and postoperative evaluation by CT scan. Clinical orthopaedics and related research. 1994(304):78–83.
10.
go back to reference Fuchs B, Weishaupt D, Zanetti M, Hodler J, Gerber C. Fatty degeneration of the muscles of the rotator cuff: assessment by computed tomography versus magnetic resonance imaging. J Shoulder Elbow Surg. 1999;8(6):599–605.CrossRef Fuchs B, Weishaupt D, Zanetti M, Hodler J, Gerber C. Fatty degeneration of the muscles of the rotator cuff: assessment by computed tomography versus magnetic resonance imaging. J Shoulder Elbow Surg. 1999;8(6):599–605.CrossRef
11.
go back to reference Zanetti M, Gerber C, Hodler J. Quantitative assessment of the muscles of the rotator cuff with magnetic resonance imaging. Invest Radiol. 1998;33(3):163–70.CrossRef Zanetti M, Gerber C, Hodler J. Quantitative assessment of the muscles of the rotator cuff with magnetic resonance imaging. Invest Radiol. 1998;33(3):163–70.CrossRef
12.
go back to reference Khoury V, Cardinal E, Brassard P. Atrophy and fatty infiltration of the supraspinatus muscle: sonography versus MRI. AJR American journal of roentgenology. 190. United States. 2008. pp 1105–11. Khoury V, Cardinal E, Brassard P. Atrophy and fatty infiltration of the supraspinatus muscle: sonography versus MRI. AJR American journal of roentgenology. 190. United States. 2008. pp 1105–11.
13.
go back to reference Dixon WT. Simple proton spectroscopic imaging. Radiology. 1984;153(1):189–94.CrossRef Dixon WT. Simple proton spectroscopic imaging. Radiology. 1984;153(1):189–94.CrossRef
14.
go back to reference Fischer MA, Nanz D, Shimakawa A, Schirmer T, Guggenberger R, Chhabra A, et al. Quantification of muscle fat in patients with low back pain: comparison of multi-echo MR imaging with single-voxel MR spectroscopy. Radiology. 2013;266(2):555–63.CrossRef Fischer MA, Nanz D, Shimakawa A, Schirmer T, Guggenberger R, Chhabra A, et al. Quantification of muscle fat in patients with low back pain: comparison of multi-echo MR imaging with single-voxel MR spectroscopy. Radiology. 2013;266(2):555–63.CrossRef
15.
go back to reference Fischer MA, Pfirrmann CW, Espinosa N, Raptis DA, Buck FM. Dixon-based MRI for assessment of muscle-fat content in phantoms, healthy volunteers and patients with achillodynia: comparison to visual assessment of calf muscle quality. Eur Radiol. 2014;24(6):1366–75.CrossRef Fischer MA, Pfirrmann CW, Espinosa N, Raptis DA, Buck FM. Dixon-based MRI for assessment of muscle-fat content in phantoms, healthy volunteers and patients with achillodynia: comparison to visual assessment of calf muscle quality. Eur Radiol. 2014;24(6):1366–75.CrossRef
16.
go back to reference Bouaicha S, Ehrmann C, Slankamenac K, Regan WD, Moor BK. Comparison of the critical shoulder angle in radiographs and computed tomography. Skeletal Radiol. 2014. Bouaicha S, Ehrmann C, Slankamenac K, Regan WD, Moor BK. Comparison of the critical shoulder angle in radiographs and computed tomography. Skeletal Radiol. 2014.
17.
go back to reference Valenzuela W, Vermathen P, Boesch C, Nolte L, Reyes M. iSix (Image Segmentation in OsiriX). ESMRMB Annual Meeting 30th. 2013. Valenzuela W, Vermathen P, Boesch C, Nolte L, Reyes M. iSix (Image Segmentation in OsiriX). ESMRMB Annual Meeting 30th. 2013.
18.
go back to reference Campell M, TDV S. Statistics at square one. Hoboken: Wiley; 2011. Campell M, TDV S. Statistics at square one. Hoboken: Wiley; 2011.
19.
go back to reference Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86(2):420–8.CrossRef Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86(2):420–8.CrossRef
20.
go back to reference Munro IC, Ford RA, Kennepohl E, Sprenger JG. Correlation of structural class with no-observed-effect levels: a proposal for establishing a threshold of concern. Food Chem Toxicol. 1996;34(9):829–67.CrossRef Munro IC, Ford RA, Kennepohl E, Sprenger JG. Correlation of structural class with no-observed-effect levels: a proposal for establishing a threshold of concern. Food Chem Toxicol. 1996;34(9):829–67.CrossRef
21.
go back to reference Gumina S, Candela V, Passaretti D, Latino G, Venditto T, Mariani L, et al. The association between body fat and rotator cuff tear: the influence on rotator cuff tear sizes. J Shoulder Elbow Surg. 2014;23(11):1669–744.CrossRef Gumina S, Candela V, Passaretti D, Latino G, Venditto T, Mariani L, et al. The association between body fat and rotator cuff tear: the influence on rotator cuff tear sizes. J Shoulder Elbow Surg. 2014;23(11):1669–744.CrossRef
22.
go back to reference Bredella MA, Ghomi RH, Thomas BJ, Miller KK, Torriani M. Comparison of 3.0 T proton magnetic resonance spectroscopy short and long echo-time measures of intramyocellular lipids in obese and normal-weight women. J Magn Reson Imaging. 2010;32(2):388–93. Bredella MA, Ghomi RH, Thomas BJ, Miller KK, Torriani M. Comparison of 3.0 T proton magnetic resonance spectroscopy short and long echo-time measures of intramyocellular lipids in obese and normal-weight women. J Magn Reson Imaging. 2010;32(2):388–93.
23.
go back to reference Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, et al. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes. 1997;46(6):983–8.CrossRef Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, et al. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes. 1997;46(6):983–8.CrossRef
24.
go back to reference St-Onge MP, Newcomer BR, Buchthal S, Aban I, Allison DB, Bosarge A, et al. Intramyocellular lipid content is lower with a low-fat diet than with high-fat diets, but that may not be relevant for health. Am J Clin Nutr. 2007;86(5):1316–22.CrossRef St-Onge MP, Newcomer BR, Buchthal S, Aban I, Allison DB, Bosarge A, et al. Intramyocellular lipid content is lower with a low-fat diet than with high-fat diets, but that may not be relevant for health. Am J Clin Nutr. 2007;86(5):1316–22.CrossRef
25.
go back to reference Nove-Josserand L, Edwards TB, O'Connor DP, Walch G. The acromiohumeral and coracohumeral intervals are abnormal in rotator cuff tears with muscular fatty degeneration. Clin Orthop Relat Res. 2005;433:90–6.CrossRef Nove-Josserand L, Edwards TB, O'Connor DP, Walch G. The acromiohumeral and coracohumeral intervals are abnormal in rotator cuff tears with muscular fatty degeneration. Clin Orthop Relat Res. 2005;433:90–6.CrossRef
26.
go back to reference Collin P, Matsumura N, Ladermann A, Denard PJ, Walch G. Relationship between massive chronic rotator cuff tear pattern and loss of active shoulder range of motion. J Shoulder Elbow Surg Am Shoulder Elbow Surg. 2014;23(8):1195–202.CrossRef Collin P, Matsumura N, Ladermann A, Denard PJ, Walch G. Relationship between massive chronic rotator cuff tear pattern and loss of active shoulder range of motion. J Shoulder Elbow Surg Am Shoulder Elbow Surg. 2014;23(8):1195–202.CrossRef
27.
go back to reference Gerber C, Meyer DC, Frey E, von Rechenberg B, Hoppeler H, Frigg R, et al. Neer Award 2007: Reversion of structural muscle changes caused by chronic rotator cuff tears using continuous musculotendinous traction. An experimental study in sheep. J Shoulder Elbow Surg Am Shoulder Elbow Surg. 2009;18(2):163–71. Gerber C, Meyer DC, Frey E, von Rechenberg B, Hoppeler H, Frigg R, et al. Neer Award 2007: Reversion of structural muscle changes caused by chronic rotator cuff tears using continuous musculotendinous traction. An experimental study in sheep. J Shoulder Elbow Surg Am Shoulder Elbow Surg. 2009;18(2):163–71.
28.
go back to reference Meyer DC, Jacob HA, Nyffeler RW, Gerber C. In vivo tendon force measurement of 2-week duration in sheep. J Biomech. 2004;37(1):135–40.CrossRef Meyer DC, Jacob HA, Nyffeler RW, Gerber C. In vivo tendon force measurement of 2-week duration in sheep. J Biomech. 2004;37(1):135–40.CrossRef
29.
go back to reference Kuenzler MB, Nuss K, Karol A, Schär MO, Hottiger M, Raniga S, et al. Neer Award 2016: reduced muscle degeneration and decreased fatty infiltration after rotator cuff tear in a poly(ADP-ribose) polymerase 1 (PARP-1) knock-out mouse model. J Shoulder Elbow Surg. 2017;26(5):733–44.CrossRef Kuenzler MB, Nuss K, Karol A, Schär MO, Hottiger M, Raniga S, et al. Neer Award 2016: reduced muscle degeneration and decreased fatty infiltration after rotator cuff tear in a poly(ADP-ribose) polymerase 1 (PARP-1) knock-out mouse model. J Shoulder Elbow Surg. 2017;26(5):733–44.CrossRef
30.
go back to reference Kim HM, Galatz LM, Lim C, Havlioglu N, Thomopoulos S. The effect of tear size and nerve injury on rotator cuff muscle fatty degeneration in a rodent animal model. J Shoulder Elbow Surg. 2012;21(7):847–58.CrossRef Kim HM, Galatz LM, Lim C, Havlioglu N, Thomopoulos S. The effect of tear size and nerve injury on rotator cuff muscle fatty degeneration in a rodent animal model. J Shoulder Elbow Surg. 2012;21(7):847–58.CrossRef
31.
go back to reference Spiegl UJ, Horan MP, Smith SW, Ho CP, Millett PJ. The critical shoulder angle is associated with rotator cuff tears and shoulder osteoarthritis and is better assessed with radiographs over MRI. Knee Surg Sports Traumatol Arthrosc. 2015. Spiegl UJ, Horan MP, Smith SW, Ho CP, Millett PJ. The critical shoulder angle is associated with rotator cuff tears and shoulder osteoarthritis and is better assessed with radiographs over MRI. Knee Surg Sports Traumatol Arthrosc. 2015.
32.
go back to reference Agten CA, Rosskopf AB, Gerber C, Pfirrmann CW. Quantification of early fatty infiltration of the rotator cuff muscles: comparison of multi-echo Dixon with single-voxel MR spectroscopy. Eur Radiol. 2015. Agten CA, Rosskopf AB, Gerber C, Pfirrmann CW. Quantification of early fatty infiltration of the rotator cuff muscles: comparison of multi-echo Dixon with single-voxel MR spectroscopy. Eur Radiol. 2015.
33.
go back to reference Lee S, Lansdown DA, Lucas R, Nardo L, Lai A, Ma B, et al. Rotator cuff fatty infiltration is correlated with tendon tear size, tendon retraction and patient age: a quantitative MR Evaluation using the IDEAL sequence. ORS Annual Meeting2014. Lee S, Lansdown DA, Lucas R, Nardo L, Lai A, Ma B, et al. Rotator cuff fatty infiltration is correlated with tendon tear size, tendon retraction and patient age: a quantitative MR Evaluation using the IDEAL sequence. ORS Annual Meeting2014.
Metadata
Title
Muscle fat content in the intact infraspinatus muscle correlates with age and BMI, but not critical shoulder angle
Authors
Helen Anwander
Fabian Fuhrer
Gaëlle Diserens
Beat Kaspar Moor
Chris Boesch
Peter Vermathen
Waldo Valenzuela
Matthias A. Zumstein
Publication date
01-04-2021
Publisher
Springer Berlin Heidelberg
Keyword
Painful Arc
Published in
European Journal of Trauma and Emergency Surgery / Issue 2/2021
Print ISSN: 1863-9933
Electronic ISSN: 1863-9941
DOI
https://doi.org/10.1007/s00068-019-01246-7

Other articles of this Issue 2/2021

European Journal of Trauma and Emergency Surgery 2/2021 Go to the issue