Abstract
Purpose
The effects of acromegaly on soft tissues, bones and joints are well-documented, but information on its effects on muscle mass and quality remains limited. The primary goal of this study is to assess the sonoelastographic features of forearm muscles in patients with acromegaly.
Method
Forty-five patients with acromegaly and 45 healthy controls similar in terms of gender, age, and body mass index (BMI) were included in a single-center, multidisciplinary, cross-sectional study. The body composition was analyzed using bioelectrical impedance analysis (BIA), and height-adjusted appendicular skeletal muscle index (hSMI) was calculated. The dominant hand’s grip strength was also measured. Two radiologists specialized in the musculoskeletal system employed ultrasound shear wave elastography (SWE) to assess the thickness and stiffness of brachioradialis and biceps brachii muscles.
Results
The acromegaly group had significantly higher thickness of both the biceps brachii (p = 0.034) and brachioradialis muscle (p = 0.046) than the control group. However, the stiffness of the biceps brachii (p = 0.001) and brachioradialis muscle (p = 0.001) was lower in the acromegaly group than in the control group. Disease activity has not caused a significant difference in muscle thickness and stiffness in the acromegaly group (p > 0.05). The acromegaly group had a higher hSMI (p = 0.004) than the control group. The hand grip strength was similar between the acromegaly and control group (p = 0.594).
Conclusion
The patients with acromegaly have an increased muscle thickness but decreased muscle stiffness in the forearm muscles responsible for elbow flexion. Acromegaly can lead to a permanent deterioration of the muscular structure regardless of the disease activity.
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Data availability
The data used to support the findings of this research are available from the corresponding author upon request.
References
Katznelson L, Laws ER, Melmed S et al (2014) Acromegaly: an endocrine society clinical practice guideline. J Clin Endocrinol Metab 99(11):3933–3951. https://doi.org/10.1210/jc.2014-2700
Gadelha MR, Kasuki L, Lim DST, Fleseriu M (2018) Systemic complications of acromegaly and the impact of the current treatment landscape: an update. Endocr Rev 40(1):268–332. https://doi.org/10.1210/er.2018-00115
Giustina A, Barkan A, Beckers A et al (2020) A consensus on the diagnosis and treatment of acromegaly comorbidities: an update. J Clin Endocrinol Metab 105(4):E937–E946. https://doi.org/10.1210/clinem/dgz096
Miller A, Doll H, David J, Wass J (2008) Impact of musculoskeletal disease on quality of life in long-standing acromegaly. Eur J Endocrinol 158(5):587–593. https://doi.org/10.1530/EJE-07-0838
Martel-Duguech L, Alonso-Pérez J, Bascuñana H et al (2021) Intramuscular fatty infiltration and physical function in controlled acromegaly. Eur J Endocrinol 185(1):167–177. https://doi.org/10.1530/EJE-21-0209
Shiina T, Nightingale KR, Palmeri ML et al (2015) WFUMB guidelines and recommendations for clinical use of ultrasound elastography: part 1: basic principles and terminology. Ultrasound Med Biol 41(5):1126–1147. https://doi.org/10.1016/j.ultrasmedbio.2015.03.009
Creze M, Nordez A, Soubeyrand M, Rocher L, Maître X, Bellin MF (2018) Shear wave sonoelastography of skeletal muscle: basic principles, biomechanical concepts, clinical applications, and future perspectives. Skeletal Radiol 47(4):457–471. https://doi.org/10.1007/s00256-017-2843-y
Phan A, Lee J, Gao J (2019) Ultrasound shear wave elastography in assessment of skeletal muscle stiffness in senior volunteers. Clin Imaging 58:22–26. https://doi.org/10.1016/j.clinimag.2019.06.006
Taljanovic MS, Gimber LH, Becker GW et al (2017) Shear-wave elastography: basic physics and musculoskeletal applications. Radiographics 37(3):855–870. https://doi.org/10.1148/rg.2017160116
Bastijns S, De Cock AM, Vandewoude M, Perkisas S (2020) Usability and pitfalls of Shear-Wave Elastography for evaluation of muscle quality and its potential in assessing Sarcopenia: a review. Ultrasound Med Biol 46(11):2891–2907. https://doi.org/10.1016/j.ultrasmedbio.2020.06.023
Scacchi M, Andrioli M, Carzaniga C et al (2009) Elastosonographic evaluation of thyroid nodules in acromegaly. Eur J Endocrinol 161(4):607–613. https://doi.org/10.1530/EJE-09-0558
Burulday V, Doğan A, Şahan MH, Arıkan Ş, Güngüneş A (2018) Ultrasound elastography of the median nerve in patients with acromegaly: a case-control study. J Ultrasound Med 37(10):2371–2377. https://doi.org/10.1002/jum.14591
Karataş A, Artaş H, Uğur K, Koca SS (2022) Sonoelastrographic finding of Achilles tendon in patients with ankylosing spondylitis and acromegaly. Diagn Interv Radiol (Ankara Turkey) 9(3):122–125. https://doi.org/10.5152/eujrheum.2022.21132
Bankir M, Sumbul HE, Koc AS, Demirtas D, Acibucu F (2019) Elastography detected solid organ stiffness increased in patients with acromegaly. Med (United States) 98(3). https://doi.org/10.1097/MD.0000000000014212
Kleiber T, Kunz L, Disselhorst-Klug C (2015) Muscular coordination of biceps brachii and brachioradialis in elbow flexion with respect to hand position. Front Physiol 6(Aug):139652. https://doi.org/10.3389/fphys.2015.00215
Mercado M, Abreu C, Vergara-López A et al (2020) Surgical and pharmacological outcomes in acromegaly: real-life data from the mexican acromegaly registry. J Clin Endocrinol Metab 105(12). https://doi.org/10.1210/clinem/dgaa664
Lee PH, Macfarlane DJ, Lam TH, Stewart SM (2011) Validity of the international physical activity questionnaire short form (IPAQ-SF): a systematic review. Int J Behav Nutr Phys Activity 8. https://doi.org/10.1186/1479-5868-8-115
Landin D, Thompson M, Jackson MR (2017) Actions of the Biceps Brachii at the shoulder: a review. J Clin Med Res 9(8):667–670. https://doi.org/10.14740/jocmr2901w
Lung BE, Bisogno M (2019) Anatomy, shoulder and Upper Limb, Forearm Brachioradialis muscle. StatPearls Publishing
Kim KM, Jang HC, Lim S (2016) Differences among skeletal muscle mass indices derived from height-, weight-, and body mass index-adjusted models in assessing sarcopenia. Korean J Intern Med 31(4):643–650. https://doi.org/10.3904/kjim.2016.015
Leong DP, Teo KK, Rangarajan S et al (2015) Prognostic value of grip strength: findings from the prospective Urban Rural Epidemiology (PURE) study. The Lancet 386(9990):266–273. https://doi.org/10.1016/S0140-6736(14)62000-6
Ibrahim K, May C, Patel HP, Baxter M, Sayer AA, Roberts H (2016) A feasibility study of implementing grip strength measurement into routine hospital practice (GRImP): study protocol. Pilot and Feasibility Studies 2(1). https://doi.org/10.1186/s40814-016-0067-x
Unal I (2017) Defining an optimal cut-point value in ROC analysis: An alternative approach. Computational and Mathematical Methods in Medicine. ;2017. https://doi.org/10.1155/2017/3762651
Roberts TJ (2016) Contribution of elastic tissues to the mechanics and energetics of muscle function during movement. J Exp Biol 219(2):266–275. https://doi.org/10.1242/jeb.124446
Alfuraih AM, O’Connor P, Tan AL et al (2019) Muscle shear wave elastography in idiopathic inflammatory myopathies: a case–control study with MRI correlation. Skeletal Radiol 48(8):1209–1219. https://doi.org/10.1007/s00256-019-03175-3
Hagert E, Lluch A, Rein S (2016) The role of proprioception and neuromuscular stability in carpal instabilities. J Hand Surgery: Eur Volume 41(1):94–101. https://doi.org/10.1177/1753193415590390
He X, Huang WY, Leong HT et al (2021) Decreased passive muscle stiffness of vastus medialis is associated with poorer quadriceps strength and knee function after anterior cruciate ligament reconstruction. Clin Biomech Elsevier Ltd 82. https://doi.org/10.1016/j.clinbiomech.2021.105289
Ozturk Gokce B, Gogus F, Bolayir B et al (2020) The evaluation of the tendon and muscle changes of lower extremity in patients with acromegaly. Pituitary 23(4):338–346. https://doi.org/10.1007/s11102-020-01037-z
Onal ED, Ipek A, Evranos B, Idilman IS, Cakir B, Ersoy R (2016) Structural tendon changes in patients with acromegaly: Assessment of Achilles tendon with sonoelastography. Med Ultrasonography 18(1):30–35. https://doi.org/10.11152/mu.2013.2066.181.edo
Tiwana MS, Charlick M, Varacallo M (2022) Anatomy, shoulder and Upper Limb, biceps muscle. StatPearls Publishing
Nagulesparen M, Trickey R, Davies MJ, Jenkins JS (1976) Muscle changes in acromegaly. BMJ 2(6041):914–915. https://doi.org/10.1136/bmj.2.6041.914
Arlien-Søborg MC, Dal J, Madsen MA et al (2023) Whole-body and forearm muscle protein metabolism in patients with acromegaly before and after treatment. The Journal of clinical endocrinology and metabolism. Published online April 10, https://doi.org/10.1210/clinem/dgad190
Janssen I, Heymsfield SB, Baumgartner RN, Ross R (2000) Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol 89(2):465–471. https://doi.org/10.1152/jappl.2000.89.2.465
Lopes AA, Albuquerque L, Fontes M, Rego D, Bandeira F (2022) Body composition in Acromegaly according to Disease activity – performance of dual X-Ray Absorptiometry and Multifrequency Bioelectrical Impedance Analysis. Front Endocrinol 13. https://doi.org/10.3389/fendo.2022.866099
Fernandez AM, LeRoith D (2005) Skeletal muscle. Adv Exp Med Biol 567:117–147. https://doi.org/10.1007/0-387-26274-1_5
Katznelson L (2009) Alterations in body composition in acromegaly. Pituitary 12(2):136–142. https://doi.org/10.1007/s11102-008-0104-8
Jorgensen JOL, Thuesen L, Muller J, Ovesen P, Skakkebaek NE, Christiansen JS (1994) Three years of growth hormone treatment in growth hormone-deficient adults: Near normalization of body composition and physical performance. Eur J Endocrinol 130(3):224–228. https://doi.org/10.1530/eje.0.1300224
BRUMMER R -J M, LÖNNS L, KVIST H, GRANGÅRD U, ‐A BENGTSSONB (1993) Adipose tissue and muscle volume determination by computed tomography in acromegaly, before and I year after adenomectomy. Eur J Clin Invest 23(4):199–205. https://doi.org/10.1111/j.1365-2362.1993.tb00762.x
Guo X, Gao L, Shi X et al (2018) Pre- and Postoperative Body Composition and Metabolic Characteristics in Patients with Acromegaly: A Prospective Study. International Journal of Endocrinology. ;2018. https://doi.org/10.1155/2018/4125013
Füchtbauer L, Olsson DS, Bengtsson BA, Norrman LL, Sunnerhagen KS, Johannsson G (2017) Muscle strength in patients with acromegaly at diagnosis and during long-term follow-up. Eur J Endocrinol 177(2):217–226. https://doi.org/10.1530/EJE-17-0120
Acknowledgements
We are grateful to Nurse Selma Avcu and Health Technician Semra Aydogan, who provided body composition analysis and hand grip strength measurements in.
the study group. We thank all the participants in the study.
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All authors contributed to the study’s conception and design. M.C., H.N.S., M.N.C., A.B., E.T.C., M.M.Y., A.E.A., M.A., M.A.K., and F.B.T. have performed material preparation, data collection and analysis. M.C., F.B.T. wrote the first draft of the manuscript, and all authors commented on previous versions. All authors read and approved the final manuscript.
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Coskun, M., Sendur, H.N., Cerit, M.N. et al. Assessment of forearm muscles with ultrasound shear wave elastography in patients with acromegaly. Pituitary 26, 716–724 (2023). https://doi.org/10.1007/s11102-023-01352-1
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DOI: https://doi.org/10.1007/s11102-023-01352-1