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The evaluation of the tendon and muscle changes of lower extremity in patients with acromegaly

Pituitary volume 23, pages 338–346 (2020)Cite this article

Abstract

Purpose

Although it is well known that acromegaly causes enlargement in the extremities, studies investigating the effects of acromegaly on tendons, muscles and soft tissue are limited. The aims of our study were to investigate tendons, the presence of enthesitis, soft tissue, muscle groups in terms of thickness and pennation angle (PA) which is an indicator of microstructure and strength of the muscle, of the lower extremities.

Methods

Thirty-nine patients with acromegaly and thirty-nine healthy control subjects similar for age, sex and body mass index were enrolled. Lower extremity tendons, skin, muscle groups were evaluated by ultrasound.

Results

The thicknesses of heel skin, heel pad, plantar fascia and Achilles tendon were higher in acromegaly than the control group (p < 0.05). The incidence of Achilles enthesitis were increased in the acromegaly group (p < 0.05). The thicknesses of the gastrocnemius medial head, vastus medialis, lateralis muscles for both sides and the left rectus femoris muscle were found to be lower in the acromegaly patients than controls (p < 0.05). However, thicknesses of vastus intermedius, gastrocnemius lateral head and soleus were similar between the acromegaly and control groups (p > 0.05). PA values of the right and left vastus medialis and the right vastus lateralis were found to be decreased in the acromegaly group (p < 0.05). Myostatin levels were lower in acromegaly group (p < 0.05).

Conclusions

Acromegaly may cause to an increase in tendon and soft tissue thickness, enthesitis formation, decrease in the thickness of some muscles, and deterioration in microstructures in lower extremity.

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References

  1. De herder WW (2016) The history of acromegaly. Neuroendocrinology 103(1):7–17

    CAS  PubMed  Google Scholar 

  2. Freda PU, Shen W, Reyes-vidal CM, Geer EB, Arias-Mendoza F, Gallagher D, Heymsfield SB (2009) Skeletal muscle mass in acromegaly assessed by magnetic resonance imaging and dual-photon X-ray absorptiometry. J Clin Endocrinol Metab 94(8):2880–2886

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Nagulesparen M, Trickey R, Davies MJ, Jenkins JS (1976) Muscle changes in acromegaly. Br Med J 2(6041):914–915

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Mastaglia FL, Barwich DD, Hall R (1970) Myopathy in acromegaly. Lancet 2(7679):907–909

    CAS  PubMed  Google Scholar 

  5. Fields ML, Greenberg BH, Burkett LL (1967) Roentgenographic measurement of skin and heel-pad thickness in the diagnosis of acromegaly. Am J Med Sci 254(4):528–533

    CAS  PubMed  Google Scholar 

  6. Velloso CP (2008) Regulation of muscle mass by growth hormone and IGF-I. Br J Pharmacol 3:557–568

    Google Scholar 

  7. Strasser EM, Draskovits T, Praschak M, Quittan M, Graf A (2013) Association between ultrasound measurements of muscle thickness, pennation angle, echogenicity and skeletal muscle strength in the elderly. Age (Dordr) 35(6):2377–2388

    Google Scholar 

  8. Abe T, Kawakami Y, Suzuki Y, Gunji A, Fukunaga T (1997) Effects of 20 days bed rest on muscle morphology. J Gravit Physiol 4(1):S10–S14

    CAS  PubMed  Google Scholar 

  9. Aagaard P, Andersen JL, Dyhre-poulsen P, Leffers AM, Wagner A, Magnusson SP, Halkjaer-Kristensen J, Simonsen EB (2001) A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture. J Physiol (Lond) 534(Pt. 2):613–623

    CAS  Google Scholar 

  10. Silva CRS, Costa ADS, Rocha T, De lima DAM, Do nascimento T, De moraes SRA (2018) Quadriceps muscle architecture ultrasonography of individuals with type 2 diabetes: reliability and applicability. PLoS ONE 13(10):e0205724

    PubMed  PubMed Central  Google Scholar 

  11. Nozoe M, Kanai M, Kubo H, Kitamura Y, Yamamoto M, Furuichi A, Takashima S, Mase K, Shimada S (2016) Changes in quadriceps muscle thickness, disease severity, nutritional status, and c-reactive protein after acute stroke. J Stroke Cerebrovasc Dis 25(10):2470–2474

    PubMed  Google Scholar 

  12. Cruz-montecinos C, Guajardo-rojas C, Montt E, Contreras-Briceño F, Torres-Castro R, Díaz O, Cuesta-Vargas A (2016) Sonographic measurement of the quadriceps muscle in patients with chronic obstructive pulmonary disease: functional and clinical implications. J Ultrasound Med 35(11):2405–2412

    PubMed  Google Scholar 

  13. Mcpherron AC, Lawler AM, Lee SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387(6628):83–90

    CAS  PubMed  Google Scholar 

  14. Longobardi S, Keay N, Ehrnborg C, Cittadini A, Rosén T, Dall R, Boroujerdi MA, Bassett EE, Healy ML, Pentecost C, Wallace JD, Powrie J, Jørgensen JO, Saccà L (2000) Growth hormone (GH) effects on bone and collagen turnover in healthy adults and its potential as a marker of GH abuse in sports: a double blind, placebo-controlled study. The GH-2000 Study Group. J Clin Endocrinol Metab 85(4):1505–1512

    CAS  PubMed  Google Scholar 

  15. Giustina A, Chanson P, Bronstein MD, Klibanski A, Lamberts S, Casanueva FF, Trainer P, Ghigo E, Ho K, Melmed S (2010) A consensus on criteria for cure of acromegaly. J Clin Endocrinol Metab 95(7):3141–3148

    CAS  PubMed  Google Scholar 

  16. Gooding GA, Stress RM, Graf PM, Grunfeld C (1985) Heel pad thickness: determination by high-resolution ultrasonography. J Ultrasound Med 4(4):173–174

    CAS  PubMed  Google Scholar 

  17. Schmidt WA, Schmidt H, Schicke B, Gromnica-ihle E (2004) Standard reference values for musculoskeletal ultrasonography. Ann Rheum Dis 63(8):988–994

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Arampatzis A, De monte G, Karamanidis K, Morey-klapsing G, Stafilidis S, Brüggemann GP (2006) Influence of the muscle-tendon unit's mechanical and morphological properties on running economy. J Exp Biol 209(Pt 17):3345–3357

    PubMed  Google Scholar 

  19. Fukunaga T, Ichinose Y, Ito M, Kawakami Y, Fukashiro S (1997) Determination of fascicle length and pennation in a contracting human muscle in vivo. J Appl Physiol 82(1):354–358

    CAS  PubMed  Google Scholar 

  20. Webb SM, Prieto L, Badia X, Albareda M, Catalá M, Gaztambide S, Lucas T, Páramo C, Picó A, Lucas A, Halperin I, Obiols G, Astorga R (2002) Acromegaly Quality of Life Questionnaire (ACROQOL) a new health-related quality of life questionnaire for patients with acromegaly: development and psychometric properties. Clin Endocrinol 57(2):251–258

    CAS  Google Scholar 

  21. Badia X, Webb SM, Prieto L, Lara N (2004) Acromegaly quality of life questionnaire (AcroQoL). Health Qual Life Outcomes 2:13

    PubMed  PubMed Central  Google Scholar 

  22. Yildirim Y, Ergin G (2013) A validity and reliability study of the Turkish Multidimensional Assessment of Fatigue (MAF) scale in chronic musculoskeletal physical therapy patients. J Back Musculoskelet Rehabil 26(3):307–316

    PubMed  Google Scholar 

  23. Jørgensen JO, Pedersen SA, Thuesen L, Ingemann-Hansen T, Pedersen S, Jørgensen J, Skakkebaek N, Christiansen JS (1989) Beneficial effects of growth hormone treatment in GH-deficient adults. Lancet 1(8649):1221–1225

    PubMed  Google Scholar 

  24. Woodhouse LJ, Asa SL, Thomas SG, Ezzat S (1999) Measures of submaximal aerobic performance evaluate and predict functional response to growth hormone (GH) treatment in GH-deficient adults. J Clin Endocrinol Metab 84(12):4570–4577

    CAS  PubMed  Google Scholar 

  25. Brummer RJ, Lönn L, Kvist H, Grangård U, Bengtsson BA, Sjöström L (1993) Adipose tissue and muscle volume determination by computed tomography in acromegaly, before and 1 year after adenomectomy. Eur J Clin Invest 23(4):199–205

    CAS  PubMed  Google Scholar 

  26. Kostka T, Rahmani A, Berthouze SE, Lacour JR, Bonnefoy M (2000) Quadriceps muscle function in relation to habitual physical activity and VO2max in men and women aged more than 65 years. J Gerontol A Biol Sci Med Sci 55(10):B481–B488

    CAS  PubMed  Google Scholar 

  27. Forghany S, Nester CJ, Richards B, Hatton AL, Liu A (2014) Rollover footwear affects lower limb biomechanics during walking. Gait Posture 39(1):205–212

    PubMed  Google Scholar 

  28. Lopes AJ, Guedes da silva DP, Ferreira Ade S, Kasuki L, Gadelha MR, Guimarães FS (2015) What is the effect of peripheral muscle fatigue, pulmonary function, and body composition on functional exercise capacity in acromegalic patients? J Phys Ther Sci 27(3):719–724

    PubMed  PubMed Central  Google Scholar 

  29. Lieber RL, Fridén J (2000) Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23(11):1647–1666

    CAS  PubMed  Google Scholar 

  30. Lee D, Li Z, Sohail QZ, Jackson K, Fiume E, Agur A (2015) A three-dimensional approach to pennation angle estimation for human skeletal muscle. Comput Methods Biomech Biomed Eng 18(13):1474–1484

    Google Scholar 

  31. Colao A, Marzullo P, Vallone G, Giaccio A, Ferone D, Rossi E, Scarpa R, Smaltino F, Lombardi G (1999) Ultrasonographic evidence of joint thickening reversibility in acromegalic patients treated with lanreotide for 12 months. Clin Endocrinol 51(5):611–618

    CAS  Google Scholar 

  32. 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 Ultrason 18(1):30–35

    PubMed  Google Scholar 

  33. Koçak M (2015) Ultrasonographic assessment of soft tissues in patients with acromegaly. Arch Rheumatol 30(2):138–143

    Google Scholar 

  34. Abrahamsson SO, Lundborg G, Lohmander LS (1991) Recombinant human insulin-like growth factor-I stimulates in vitro matrix synthesis and cell proliferation in rabbit flexor tendon. J Orthop Res 9(4):495–502

    CAS  PubMed  Google Scholar 

  35. Abrahamsson SO, Lohmander S (1996) Differential effects of insulin-like growth factor-I on matrix and DNA synthesis in various regions and types of rabbit tendons. J Orthop Res 14(3):370–376

    CAS  PubMed  Google Scholar 

  36. Doessing S, Holm L, Heinemeier KM, Feldt-Rasmussen U, Schjerling P, Qvortrup K, Larsen JO, Nielsen RH, Flyvbjerg A, Kjaer M (2010) GH and IGF1 levels are positively associated with musculotendinous collagen expression: experiments in acromegalic and GH deficiency patients. Eur J Endocrinol 163(6):853–862

    CAS  PubMed  Google Scholar 

  37. Galdiero M, Auriemma RS, Pivonello R, Colao A (2014) Cushing, acromegaly, GH deficiency and tendons. Muscles Ligaments Tendons J 4(3):329–332

    PubMed  PubMed Central  Google Scholar 

  38. Colao A, Pivonello R, Scarpa R, Vallone G, Ruosi C, Lombardi G (2005) The acromegalic arthropathy. J Endocrinol Invest 28(8 Suppl):24–31

    CAS  PubMed  Google Scholar 

  39. Fonseca R, Fernández-martínez A, Miguélez R, Uson J (2018) Ultrasound and radiographic abnormalities in a patient with chronic severe acromegaly. Reumatol Clin 14(4):236–238

    PubMed  Google Scholar 

  40. Steinbach HL, Russell W (1964) Measurement of the heel-pad as an aid to diagnosis of acromegaly. Radiology 82(3):418–423

    CAS  PubMed  Google Scholar 

  41. Kho KM, Wright AD, Doyle FH (1970) Heel pad thickness in acromegaly. Br J Radiol 43(506):119–125

    CAS  PubMed  Google Scholar 

  42. Gonticas SK, Ikkos DG, Stergiou LH (1969) Evaluation of the diagnostic value of heel-pad thickness in acromegaly. Radiology 92(2):304–307

    CAS  PubMed  Google Scholar 

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Acknowledgement

Authors would like to thank Nazmiye Kursun from Ankara University Department of Biostatistics for her assistance with statistical analysis.

Funding

This study was supported by Endocrinology and Metabolism Education and Coordination Association.

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Authors and Affiliations

  1. Department of Internal Medicine, Gazi University Faculty of Medicine, Ankara, Turkey

    Birsen Ozturk Gokce & Onur Gokce

  2. Department of Physical Medicine and Rehabilitation, Division of Rheumatology, Gazi University Faculty of Medicine, Ankara, Turkey

    Feride Gogus & Duygu Tecer

  3. Department of Internal Medicine, Division of Endocrinology and Metabolism, Gazi University Faculty of Medicine, Ankara, 06560, Turkey

    Basak Bolayir, Alev Eroglu Altinova, Fusun Balos Toruner & Mujde Akturk

Authors
  1. Birsen Ozturk Gokce
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  2. Feride Gogus
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  5. Onur Gokce
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Correspondence to Basak Bolayir.

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The authors have no conflict of interest.

Ethical approval

The study was approved by Ankara Numune Training and Research Hospital ethics committee and all participants gave written informed consent to a protocol adhering to the 1964 Declaration of Helsinki.

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Ozturk Gokce, B., Gogus, F., Bolayir, B. et al. The evaluation of the tendon and muscle changes of lower extremity in patients with acromegaly. Pituitary 23, 338–346 (2020). https://doi.org/10.1007/s11102-020-01037-z

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  • DOI: https://doi.org/10.1007/s11102-020-01037-z

Keywords

  • Acromegaly
  • Ultrasound
  • Muscle thickness
  • Tendon