Year 2021,
Volume: 3 Issue: 3, 102 - 108, 29.07.2021
Hale Turnaoğlu
,
Feride Altay
Feride Kural Rahatlı
,
Yusuf Bozkuş
,
Özlem Turhan İyidir
,
Kemal Murat Haberal
Supporting Institution
Başkent Üniversitesi
References
- 1. Oliva F, Piccirilli E, Berardi AC, Frizziero A, Tarantino U, Maffulli N. Hormones and tendinopathies: the current evidence. Br Med Bull. 2016 Mar;117(1):39-58. doi: 10.1093/bmb/ldv054.
- 2. Knopp WD, Bohm ME, McCoy JC. Hypothyroidism presenting as tendinitis. Phys Sportmed. 1997 Jan;25(1):47-55. doi: 10.3810/psm.1997.01.1094.
- 3. Pantazis K, Roupas ND, Panagopoulos A, Theodoraki S, Tsintoni A, Kyriazopoulou V. Spontaneous rupture of the long head of the biceps tendon in a woman with hypothyroidism: a case report. J Med Case Rep. 2016 Jan;10:2. doi: 10.1186/s13256-015-0794-2.
- 4. Balaban M, Idilman IS, Ipek A, Ikiz SS, Bektaser B, Gumus M. Elastographic findings of Achilles tendons in asymptomatic professional male volleyball players. J Ultrasound Med. 2016 Dec;35(12):2623-8. doi: 10.7863/ultra.15.11077.
- 5. Fu S, Cui L, He X, Sun Y. Elastic characteristics of the normal Achilles tendon assessed by virtual touch imaging quantification shear wave elastography. J Ultrasound Med. 2016 Sep;35(9):1881-7. doi: 10.7863/ultra.16.01052.
- 6. Paavola M, Paakkala T, Kannus P , Jarvinen M. Ultrasonography in the differential diagnosis of Achilles tendon injuries and related disorders. A comparison between pre-operative ultrasonography and surgical findings. Acta Radiol. 1998 Nov;39(6):612-9. doi: 10.3109/02841859809175485.
- 7. Khan KM, Forster BB, Robinson J, Cheong Y, Louis L, Maclean L, Taunton JE. Are ultrasound and magnetic resonance imaging of value in assessment of Achilles tendon disorders? A two year prospective study. Br J Sports Med. 2003 Apr;37(2):149-53. doi: 10.1136/bjsm.37.2.149.
- 8. Ruan Z, Zhao B, Qi H, Zhang Y, Zhang F, Wu M, Shao G. Elasticity of healthy Achilles tendon decreases with the increase of age as determined by acoustic radiation force impulse imaging. Int J Clin Exp Med. 2015 Jan;8(1):1043-50.
- 9. Chen XM, Cui LG, He P , Shen WW, Qian YJ, Wang JR. Shear wave elastographic characterization of normal and torn Achilles tendons: a pilot study. J Ultrasound Med. 2013 Mar;32(3):449-55. doi: 10.7863/jum.2013.32.3.449.
- 10. Sporea I, Sirli R, Popescu A, Danila M. Acoustic Radiation Force Impulse (ARFI)-a new modality for the evaluation of liver fibrosis. Med Ultrason. 2010 Mar;12(1):26-31.
- 11. Yilmaz B. Achilles tendon elasticity decreases with intermittent claudication in patients by Acoustic Radiation Force Impulse Imaging (ARFI). J Pak Med Assoc. 2018 Jan;68(1):16-20.
- 12. Kural Rahatli F, Turnaoglu H, Haberal KM, Kirnap M, Fidan C, Sayın CB, Uslu N, Haberal M. Acoustic Radiation Force Impulse Elastography Findings of Achilles Tendons in Patients on Chronic Hemodialysis and in Renal Transplant Patients. Exp Clin Transplant. 2018 Nov. doi: 10.6002/ect.2018.0015.
- 13. Iyidir OT, Rahatlı FK, Bozkus Y, Ramazanova L, Turnaoglu H, Nar A, Tutuncu NB. Acoustic Radiation Force Impulse Elastography and Ultrasonographic Findings of Achilles Tendon in Patients With and Without Diabetic Peripheral Neuropathy: A Cross-Sectional Study. Exp Clin Endocrinol Diabetes. 2019 Feb. doi: 10.1055/a-0840-3292.
- 14. De Zordo T, Chhem R, Smekal V, Feuchtner G, Reindl M, Fink C, Faschingbauer R, Jaschke W, Klauser AS. Real-time sonoelastography: findings in patients with symptomatic Achilles tendons and comparison to healthy volunteers. Ultraschall Med. 2010 Aug;31(4):394-400. doi: 10.1055/s-0028-1109809.
- 15. Klauser AS, Miyamoto H, Tamegger M, Faschingbauer R, Moriggl B, Klima G, Feuchtner GM, Kastlunger M, Jaschke WR. Achilles tendon assessed with sonoelastography: histologic agreement. Radiology. 2013 Jun;267(3):837-42. doi: 10.1148/radiol.13121936.
- 16. Turan A, Tufan A, Mercan R, Teber MA, Tezcan ME, Bitik B, Goker B, Haznedaroglu S. Real-time sonoelastography of Achilles tendon in patients with ankylosing spondylitis. Skeletal Radiol. 2013 Aug;42(8):1113-8. doi: 10.1007/s00256-013-1637-0.
- 17. Karatekin YS, Karaismailoglu B, Kaynak G, Ogut T, Dikici AS, Ure Esmerer E, Aydingoz O, Botanlioglu H. Does elasticity of Achilles tendon change after suture applications? Evaluation of repair area by acoustic radiation force impulse elastography. J Orthop Surg Res. 2018 Mar;13(1):45. doi: 10.1186/s13018-018-0751-z.
- 18. Maffulli N, Margiotti K, Longo UG, Loppini M, Fazio VM, Denaro V. The genetics of sports injuries and athletic performance. Muscles Ligaments Tendons J. 2013 Aug;3(3):173-89.
- 19. Oliva F, Misiti S, Maffulli N. Metabolic diseases and tendinopathies: the missing link. Muscles Ligaments Tendons J. 2014 Nov;4(3):273-4.
- 20. Oliva F, Berardi AC, Misiti S, Verga Falzacappa C, Lacone A, Maffulli N. Thyroid hormones enhance growth and counteract apoptosis in human tenocytes isolated from rotator cuff tendons. Cell Death Dis. 2013 Jul;4(7):e705. doi: 10.1038/cddis.2013.229.
- 21. Berardi AC, Oliva F, Berardocco M, la Rovere M, Accorsi P, Maffulli N. Thyroid hormones increase collagen I and cartilage oligomeric matrix protein (COMP) expression in vitro human tenocytes. Muscles Ligaments Tendons J. 2014 Nov;4(3):285-91.
- 22. Dorwart BB, Schumacher HR. Joint effusions, chondrocalcinosis and other rheumatic manifestations in hypothyroidism. A clinicopathologic study. Am J Med. 1975 Dec;59(6):780-90. doi: 10.1016/0002-9343(75)90463-5.
- 23. Mackley JR, Ando J, Herzyk P, Winder SJ. Phenotypic responses to mechanical stress in fibroblasts from tendon, cornea and skin. Biochem J. 2006 Jun;396(2):307-16. doi: 10.1042/BJ20060057.
- 24. Dutta D, Garg A, Khandelwal D, Kalra S, Mittal S, Chittawar S. Thyroid symptomatology across the spectrum of hypothyroidism and impact of levothyroxine supplementation in patients with severe primary hypothyroidism. Indian J Endocrinol Metab. 2019 May-Jun;23(3):373-378. doi: 10.4103/ijem.IJEM_78_19.
- 25. Lankhaar JA, de Vries WR, Jansen JA, Zelissen PM, Backx FJ. Impact of overt and subclinical hypothyroidism on exercise tolerance: a systematic review. Res Q Exerc Sport. 2014 Sep;85(3):365-89. doi: 10.1080/02701367.2014.930405.
- 26. Klein IK, Levey GS. Unusual manifestations of hypothyroidism. Arch lntern Med. 1984 Jan;144(1):123-8.
- 27. Wilke WS, Sheeler LR, Makarowski WS. Hypothyroidism with presenting symptoms of fibrositis. J Rheumat. 1981 Jul-Aug;8(4):626-31.
- 28. Carette S, Lefrancois L. Fibrositis and primary hypothyroidism. J Rheumatol. 1988 Sep;15(9):1418-21.
- 29. Keenan GF, Ostrov BE, Goldsmith DP, Athreya BH. Rheumatic symptoms associated with hypothyroidism in children. J Pediatr. 1993 Oct;123(4):586-8. doi: 10.1016/s0022-3476(05)80957-6.
- 30. Smith TJ, Bahn RS, Gorman CA. Connective tissue, glycosaminoglycans, and diseases of the thyroid. Endocr Rev. 1989 Aug;10(3):366-91. doi: 10.1210/edrv-10-3-366.
- 31. Gibbon WW, Cooper JR, Radcliffe GS. Distribution of sonographically detected tendon abnormalities in patients with a clinical diagnosis of chronic Achilles tendinosis. J Clin Ultrasound. 2000 Feb;28(2):61-6. doi: 10.1002/(sici)1097-0096(200002)28:2<61::aid-jcu1>3.0.co;2-r.
Acoustic radiation force impulse elastography findings of achilles tendon in patients with hypothyroidism
Year 2021,
Volume: 3 Issue: 3, 102 - 108, 29.07.2021
Hale Turnaoğlu
,
Feride Altay
Feride Kural Rahatlı
,
Yusuf Bozkuş
,
Özlem Turhan İyidir
,
Kemal Murat Haberal
Abstract
Introduction
The aim of our study was to investigate the effect of thyroid dysfunction on tendons and the contribution of Acoustic Radiation Force Impulse (ARFI) elastography to the diagnosis of tendinopathy.
Methods
Eighty Achilles tendons of 40 patients under levothyroxine treatment, who had previously known hypothyroidism but high serum thyroid stimulating hormone levels, and 80 Achilles tendons of 40 healthy individuals were evaluated with ARFI (Virtual Touch Quantification®). 19 of 40 of the patients with hypotiroidism’ Achilles tendons were re-evaluated after thyroid stimulating hormone levels reached to normal limits following the adjustments in thyroid hormone replacement therapy. The middle portion of the each Achilles tendon was chosen for the examination. Every examination consisted of three to five independent measurements (shear wave velocity- meters per second). The mean shear wave velocity value was calculated for each tendon, and used for statistical analysis.
Results
The stiffness values of both left and right Achilles tendons, represented as shear wave velocity, were similar in patients with hypothyroidism and control group. There was no significant difference between the Achilles tendon shear wave velocity measurements of 19 of 40 hypothyroidism patients who were re-evaluated after the adjustments in thyroid hormone replacement therapy.
Conclusions
The lack of significant difference in Achilles tendon stiffness between non-naive hypothyroid patients and the control group may be explained as a positive clinical effect of thyroid hormone replacement therapy.
References
- 1. Oliva F, Piccirilli E, Berardi AC, Frizziero A, Tarantino U, Maffulli N. Hormones and tendinopathies: the current evidence. Br Med Bull. 2016 Mar;117(1):39-58. doi: 10.1093/bmb/ldv054.
- 2. Knopp WD, Bohm ME, McCoy JC. Hypothyroidism presenting as tendinitis. Phys Sportmed. 1997 Jan;25(1):47-55. doi: 10.3810/psm.1997.01.1094.
- 3. Pantazis K, Roupas ND, Panagopoulos A, Theodoraki S, Tsintoni A, Kyriazopoulou V. Spontaneous rupture of the long head of the biceps tendon in a woman with hypothyroidism: a case report. J Med Case Rep. 2016 Jan;10:2. doi: 10.1186/s13256-015-0794-2.
- 4. Balaban M, Idilman IS, Ipek A, Ikiz SS, Bektaser B, Gumus M. Elastographic findings of Achilles tendons in asymptomatic professional male volleyball players. J Ultrasound Med. 2016 Dec;35(12):2623-8. doi: 10.7863/ultra.15.11077.
- 5. Fu S, Cui L, He X, Sun Y. Elastic characteristics of the normal Achilles tendon assessed by virtual touch imaging quantification shear wave elastography. J Ultrasound Med. 2016 Sep;35(9):1881-7. doi: 10.7863/ultra.16.01052.
- 6. Paavola M, Paakkala T, Kannus P , Jarvinen M. Ultrasonography in the differential diagnosis of Achilles tendon injuries and related disorders. A comparison between pre-operative ultrasonography and surgical findings. Acta Radiol. 1998 Nov;39(6):612-9. doi: 10.3109/02841859809175485.
- 7. Khan KM, Forster BB, Robinson J, Cheong Y, Louis L, Maclean L, Taunton JE. Are ultrasound and magnetic resonance imaging of value in assessment of Achilles tendon disorders? A two year prospective study. Br J Sports Med. 2003 Apr;37(2):149-53. doi: 10.1136/bjsm.37.2.149.
- 8. Ruan Z, Zhao B, Qi H, Zhang Y, Zhang F, Wu M, Shao G. Elasticity of healthy Achilles tendon decreases with the increase of age as determined by acoustic radiation force impulse imaging. Int J Clin Exp Med. 2015 Jan;8(1):1043-50.
- 9. Chen XM, Cui LG, He P , Shen WW, Qian YJ, Wang JR. Shear wave elastographic characterization of normal and torn Achilles tendons: a pilot study. J Ultrasound Med. 2013 Mar;32(3):449-55. doi: 10.7863/jum.2013.32.3.449.
- 10. Sporea I, Sirli R, Popescu A, Danila M. Acoustic Radiation Force Impulse (ARFI)-a new modality for the evaluation of liver fibrosis. Med Ultrason. 2010 Mar;12(1):26-31.
- 11. Yilmaz B. Achilles tendon elasticity decreases with intermittent claudication in patients by Acoustic Radiation Force Impulse Imaging (ARFI). J Pak Med Assoc. 2018 Jan;68(1):16-20.
- 12. Kural Rahatli F, Turnaoglu H, Haberal KM, Kirnap M, Fidan C, Sayın CB, Uslu N, Haberal M. Acoustic Radiation Force Impulse Elastography Findings of Achilles Tendons in Patients on Chronic Hemodialysis and in Renal Transplant Patients. Exp Clin Transplant. 2018 Nov. doi: 10.6002/ect.2018.0015.
- 13. Iyidir OT, Rahatlı FK, Bozkus Y, Ramazanova L, Turnaoglu H, Nar A, Tutuncu NB. Acoustic Radiation Force Impulse Elastography and Ultrasonographic Findings of Achilles Tendon in Patients With and Without Diabetic Peripheral Neuropathy: A Cross-Sectional Study. Exp Clin Endocrinol Diabetes. 2019 Feb. doi: 10.1055/a-0840-3292.
- 14. De Zordo T, Chhem R, Smekal V, Feuchtner G, Reindl M, Fink C, Faschingbauer R, Jaschke W, Klauser AS. Real-time sonoelastography: findings in patients with symptomatic Achilles tendons and comparison to healthy volunteers. Ultraschall Med. 2010 Aug;31(4):394-400. doi: 10.1055/s-0028-1109809.
- 15. Klauser AS, Miyamoto H, Tamegger M, Faschingbauer R, Moriggl B, Klima G, Feuchtner GM, Kastlunger M, Jaschke WR. Achilles tendon assessed with sonoelastography: histologic agreement. Radiology. 2013 Jun;267(3):837-42. doi: 10.1148/radiol.13121936.
- 16. Turan A, Tufan A, Mercan R, Teber MA, Tezcan ME, Bitik B, Goker B, Haznedaroglu S. Real-time sonoelastography of Achilles tendon in patients with ankylosing spondylitis. Skeletal Radiol. 2013 Aug;42(8):1113-8. doi: 10.1007/s00256-013-1637-0.
- 17. Karatekin YS, Karaismailoglu B, Kaynak G, Ogut T, Dikici AS, Ure Esmerer E, Aydingoz O, Botanlioglu H. Does elasticity of Achilles tendon change after suture applications? Evaluation of repair area by acoustic radiation force impulse elastography. J Orthop Surg Res. 2018 Mar;13(1):45. doi: 10.1186/s13018-018-0751-z.
- 18. Maffulli N, Margiotti K, Longo UG, Loppini M, Fazio VM, Denaro V. The genetics of sports injuries and athletic performance. Muscles Ligaments Tendons J. 2013 Aug;3(3):173-89.
- 19. Oliva F, Misiti S, Maffulli N. Metabolic diseases and tendinopathies: the missing link. Muscles Ligaments Tendons J. 2014 Nov;4(3):273-4.
- 20. Oliva F, Berardi AC, Misiti S, Verga Falzacappa C, Lacone A, Maffulli N. Thyroid hormones enhance growth and counteract apoptosis in human tenocytes isolated from rotator cuff tendons. Cell Death Dis. 2013 Jul;4(7):e705. doi: 10.1038/cddis.2013.229.
- 21. Berardi AC, Oliva F, Berardocco M, la Rovere M, Accorsi P, Maffulli N. Thyroid hormones increase collagen I and cartilage oligomeric matrix protein (COMP) expression in vitro human tenocytes. Muscles Ligaments Tendons J. 2014 Nov;4(3):285-91.
- 22. Dorwart BB, Schumacher HR. Joint effusions, chondrocalcinosis and other rheumatic manifestations in hypothyroidism. A clinicopathologic study. Am J Med. 1975 Dec;59(6):780-90. doi: 10.1016/0002-9343(75)90463-5.
- 23. Mackley JR, Ando J, Herzyk P, Winder SJ. Phenotypic responses to mechanical stress in fibroblasts from tendon, cornea and skin. Biochem J. 2006 Jun;396(2):307-16. doi: 10.1042/BJ20060057.
- 24. Dutta D, Garg A, Khandelwal D, Kalra S, Mittal S, Chittawar S. Thyroid symptomatology across the spectrum of hypothyroidism and impact of levothyroxine supplementation in patients with severe primary hypothyroidism. Indian J Endocrinol Metab. 2019 May-Jun;23(3):373-378. doi: 10.4103/ijem.IJEM_78_19.
- 25. Lankhaar JA, de Vries WR, Jansen JA, Zelissen PM, Backx FJ. Impact of overt and subclinical hypothyroidism on exercise tolerance: a systematic review. Res Q Exerc Sport. 2014 Sep;85(3):365-89. doi: 10.1080/02701367.2014.930405.
- 26. Klein IK, Levey GS. Unusual manifestations of hypothyroidism. Arch lntern Med. 1984 Jan;144(1):123-8.
- 27. Wilke WS, Sheeler LR, Makarowski WS. Hypothyroidism with presenting symptoms of fibrositis. J Rheumat. 1981 Jul-Aug;8(4):626-31.
- 28. Carette S, Lefrancois L. Fibrositis and primary hypothyroidism. J Rheumatol. 1988 Sep;15(9):1418-21.
- 29. Keenan GF, Ostrov BE, Goldsmith DP, Athreya BH. Rheumatic symptoms associated with hypothyroidism in children. J Pediatr. 1993 Oct;123(4):586-8. doi: 10.1016/s0022-3476(05)80957-6.
- 30. Smith TJ, Bahn RS, Gorman CA. Connective tissue, glycosaminoglycans, and diseases of the thyroid. Endocr Rev. 1989 Aug;10(3):366-91. doi: 10.1210/edrv-10-3-366.
- 31. Gibbon WW, Cooper JR, Radcliffe GS. Distribution of sonographically detected tendon abnormalities in patients with a clinical diagnosis of chronic Achilles tendinosis. J Clin Ultrasound. 2000 Feb;28(2):61-6. doi: 10.1002/(sici)1097-0096(200002)28:2<61::aid-jcu1>3.0.co;2-r.