Muscle–tendon tissue properties in the hypermobility type of Ehlers‐Danlos syndrome
Abstract
Objective: To investigate the passive properties of the plantar flexors muscle–tendon tissue in patients with the hypermobility type of Ehlers‐Danlos syndrome (EDS‐HT). Methods: Twenty‐five women with EDS‐HT and 25 sex‐ and age‐matched healthy control subjects participated in the study. Passive resistive torque (PRT) of the plantar flexors was measured with an isokinetic dynamometer during 2 standardized stretch protocols to obtain the passive muscle tension. Protocol 1 consisted of 4 continuous cycles to a predetermined angle of 10° dorsiflexion. Protocol 2 consisted of a slow stretch to the onset of pain. Torque, angle, and electromyography were simultaneously recorded during the tests. To take muscle thickness into account, muscle cross‐sectional area (MCSA) was obtained with peripheral quantitative computed tomography. Stiffness of the Achilles tendon was assessed using a dynamometer in combination with ultrasonography. Results: The results demonstrate a significantly larger maximal joint angle in the EDS‐HT patients accompanied by a similar PRT compared to the control subjects (protocol 2), indicating a lower passive muscle tension in the patient group. PRT for the predetermined angle (protocol 1) was the same for both groups and there was no difference in MSCA. Furthermore, a significantly lower Achilles tendon stiffness was seen in the patient group than in the control group. Conclusion: This study is the first to provide evidence for altered passive properties of the muscle–tendon unit in EDS‐HT patients. These changes are thought to be associated with structural modifications in connective tissue.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Fear of provoking pain and sustaining injury potentially leads to decreased levels of physical activity, hastening deconditioning and exercise intolerance in patients with HSDs.
“Fear of provoking pain and sustaining injury potentially leads to decreased levels of physical activity, hastening deconditioning and exercise intolerance.[8,33]”
From Hypermobility spectrum disorders: A review (2023) · cites this paper as [33]
Generalized hyperalgesia is common in HSDs and believed to be mediated by central sensitization.
“Generalized hyperalgesia is common and believed to be mediated by central sensitization.”
From Hypermobility spectrum disorders: A review (2023) · cites this paper as [33]
Cites
The Stabilizing System of the Spine. Part I. Function, Dysfunction, Adaptation, and Enhancement
Panjabi, M. M. (1992) · Journal of Spinal Disorders · doi:10.1097/00002517-199212000-00001 · Cited by 2,180 · see citing works
Muscles Alive—their functions revealed by electromyography
(1963) · Postgraduate Medical Journal · doi:10.1136/pgmj.39.449.162-b · Cited by 1,780 · see citing works
The Stabilizing System of the Spine. Part II. Neutral Zone and Instability Hypothesis
Panjabi, M. M. (1992) · Journal of Spinal Disorders · doi:10.1097/00002517-199212000-00002 · Cited by 1,576 · see citing works
The sensorimotor system, part I: the physiologic basis of functional joint stability.
Riemann, B. L., & Lephart, S. M. (2002) · PubMed · Cited by 956 · see citing works
Passive extensibility of skeletal muscle: review of the literature with clinical implications
Gajdosik, R. L. (2001) · Clinical Biomechanics · doi:10.1016/s0268-0033(00)00061-9 · Cited by 532 · see citing works
Proprioception and neuromuscular control in joint stability
Lephart, S. M., & Fu, F. H. (2000) · Cited by 501 · see citing works
Increasing Muscle Extensibility: A Matter of Increasing Length or Modifying Sensation?
Weppler, C. H., & Magnusson, S. P. (2010) · Physical Therapy · doi:10.2522/ptj.20090012 · Cited by 435 · see citing works
A mechanism for altered flexibility in human skeletal muscle.
Magnusson, S. P., Simonsen, E. B., Aagaard, P., Sørensen, H., & Kjaer, M. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021768 · Cited by 406 · see citing works
Steinmann, B., Royce, P. M., & Superti‐Furga, A. (2002) · Connective Tissue and Its Heritable Disorders · doi:10.1002/0471221929.ch9 · Cited by 358 · see citing works
Joint hypermobility and genetic collagen disorders: are they related?
Grahame, R. (1999) · Archives of Disease in Childhood · doi:10.1136/adc.80.2.188 · Cited by 344 · see citing works
Human Tendons: Anatomy, Physiology, and Pathology
Józsa, L., & Kannus, P. (1997) · Cited by 334 · see citing works
Human Tendons: Anatomy, Physiology and Pathology
G.Kleiner, D. (1998) · Journal of Athletic Training · Cited by 307 · see citing works
In vivo moment arm calculations at the ankle using magnetic resonance imaging (MRI)
Rugg, S., Gregor, R. J., Mandelbaum, B. R., & Chiu, L. T. (1990) · Journal of Biomechanics · doi:10.1016/0021-9290(90)90305-m · Cited by 303 · see citing works
Tinkle, B. T., Bird, H. A., Grahame, R., Lavallee, M., Levy, H. P., & Sillence, D. (2009) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.33070 · Cited by 290 · see citing works
Gender differences in the viscoelastic properties of tendon structures
Kubo, K., Kanehisa, H., & Fukunaga, T. (2003) · European Journal of Applied Physiology · doi:10.1007/s00421-002-0744-8 · Cited by 282 · see citing works
Purslow, P. P. (1989) · Journal of Biomechanics · doi:10.1016/0021-9290(89)90181-4 · Cited by 267 · see citing works
Mechanical properties of tendon and aponeurosis of human gastrocnemius muscle in vivo
Muramatsu, T., Muraoka, T., Takeshita, D., Kawakami, Y., Hirano, Y., & Fukunaga, T. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.5.1671 · Cited by 263 · see citing works
Nonisometric behavior of fascicles during isometric contractions of a human muscle
Ito, M., Kawakami, Y., Ichinose, Y., Fukashiro, S., & Fukunaga, T. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.85.4.1230 · Cited by 258 · see citing works
Ehlers-Danlos syndromes and Marfan syndrome
Callewaert, B., Malfait, F., Loeys, B., & De Paepe, A. (2008) · Best Practice & Research Clinical Rheumatology · doi:10.1016/j.berh.2007.12.005 · Cited by 257 · see citing works
Self-citationMagnusson, S. P., Simonsen, E. B., Aagaard, P., Boesen, J., Johannsen, F. E., & Kjær, M. (1997) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.1997.tb00139.x · Cited by 251 · see citing works
Rombaut, L., Malfait, F., Cools, A., De Paepe, A., & Calders, P. (2010) · Disability and Rehabilitation · doi:10.3109/09638280903514739 · Cited by 236 · see citing works
Self-citationLanne, R. D. (1952) · Acta Clinica Belgica · doi:10.1080/17843286.1952.11717220 · Cited by 211 · see citing works
Connective tissue and its heritable disorders. Molecular, genetic and medical aspects
Olavesen, A. H. (1993) · FEBS Letters · doi:10.1016/0014-5793(93)80460-c · Cited by 198 · see citing works
Gajdosik, R. L., Linden, D. W. V., & Williams, A. K. (1999) · Physical Therapy · doi:10.1093/ptj/79.9.827 · Cited by 170 · see citing works
Neuromuscular involvement in various types of Ehlers–Danlos syndrome
Voermans, N. C., van Alfen, N., Pillen, S., Lammens, M. M. Y., Schalkwijk, J., Zwarts, M. J., van Rooij, I. A. L. M., Hamel, B. C. J., & van Engelen, B. G. M. (2009) · Annals of Neurology · doi:10.1002/ana.21643 · Cited by 168 · see citing works
Ultrasonography gives directly but noninvasively elastic characteristic of human tendon in vivo
Fukashiro, S., Rob, M., Ichinose, Y., et al. (1995) · European Journal of Applied Physiology · doi:10.1007/bf00238560 · Cited by 163 · see citing works
Is passive stiffness in human muscles related to the elasticity of tendon structures?
Kubo, K., Kanehisa, H., & Fukunaga, T. (2001) · European Journal of Applied Physiology · doi:10.1007/s004210100463 · Cited by 143 · see citing works
Effect of Eccentric Training on the Plantar Flexor Muscle-Tendon Tissue Properties
Mahieu, N., McNair, P. J., Cools, A. M. J., D'HAEN, C., VANDERMEULEN, K., & Witvrouw, E. (2008) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181599254 · Cited by 121 · see citing works
Self-citationOrthopaedic Manifestations of Ehlers-Danlos Syndrome
Stanitski, D. F., Nadjarian, R. K., Stanitski, C. L., Bawle, E., & Tsipouras, P. (2000) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-200007000-00029 · Cited by 115 · see citing works
Rombaut, L., Paepe, A. D., Malfait, F., Cools, A., & Calders, P. (2010) · Clinical Rheumatology · doi:10.1007/s10067-009-1320-y · Cited by 104 · see citing works
Self-citationKirschner, J., Haußer, I., Zou, Y., Schreiber, G., Christen, H. ‐., Brown, S., Anton‐Lamprecht, I., Francesco Muntoni, A., Hanefeld, F. A., & Bönnemann, C. G. (2004) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.30443 · Cited by 104 · see citing works
Effects of transient muscle contractions and stretching on the tendon structures in vivo
Kubo, K., Kanehisa, H., & Fukunaga, T. (2002) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2002.00976.x · Cited by 102 · see citing works
Mahieu, N., Cools, A. M. J., Wilde, B. D., Boon, M., & Witvrouw, E. (2009) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2008.00815.x · Cited by 93 · see citing works
Self-citationHeritable disorders of connective tissue
Grahame, R. (2000) · Best Practice & Research Clinical Rheumatology · doi:10.1053/berh.1999.0069 · Cited by 82 · see citing works
Molecular nosology of heritable disorders of connective tissue
Beighton, P., Paepe, A. D., Hall, J. G., Hollister, D. W., Pope, F. M., Pyeritz, R. E., Steinmann, B. U., & Tsipouras, P. (1992) · American Journal of Medical Genetics · doi:10.1002/ajmg.1320420406 · Cited by 61 · see citing works
Biomechanical Behavior of the Plantar Flexor Muscle-Tendon Unit after an Achilles Tendon Rupture
Bressel, E., & McNair, P. J. (2001) · The American Journal of Sports Medicine · doi:10.1177/03635465010290031201 · Cited by 59 · see citing works
Magnusson, S. P., Julsgaard, C., Aagaard, P., Zacharie, C., Ullman, S., Kobayasi, T., & Kjær, M. (2001) · PubMed · Cited by 41 · see citing works
Muscle pain: Animal and human experimental and clinical studies
Marchettini, P. (1993) · Muscle & Nerve · doi:10.1002/mus.880161006 · Cited by 38 · see citing works
Reduced quantitative muscle function in tenascin-X deficient Ehlers-Danlos patients
Voermans, N. C., Altenburg, T. M., Hamel, B. C., de Haan, A., & van Engelen, B. G. (2007) · Neuromuscular Disorders · doi:10.1016/j.nmd.2007.04.004 · Cited by 36 · see citing works
Berglund, B., Nordström, G. M., Hagberg, C., & Mattiasson, A. (2005) · Disability and Rehabilitation · doi:10.1080/09638280400009352 · Cited by 34 · see citing works
Muscle formation in Ehlers-Danlos syndrome.
Bilkey, W. J., Baxter, T., Kottke, F. J., & Mundale, M. O. (1981) · PubMed · Cited by 19 · see citing works
The Ehlers-Danlos syndrome causing lacerations in tendons and muscles
P�lv�lgyi, R., B�lint, B. J., & J�zsa, L. (1979) · Archives of Orthopaedic and Trauma Surgery · doi:10.1007/bf00460115 · Cited by 19 · see citing works
Mahieu, N., Witvrouw, E., Stevens, V. K., Willems, T. M., Vanderstraeten, G., & Cambier, D. C. (2004) · Isokinetics and Exercise Science · doi:10.3233/ies-2004-0172 · Cited by 12 · see citing works
Self-citationEhlers-Danlos syndromes: Revised nosology, Villefranche, 1997
Beighton, P., Paepe, A. D., Steinmann, B., Tsipouras, P., & Wenstrup, R. J. (1998) · American Journal of Medical Genetics · doi:10.1002/(sici)1096-8628(19980428)77:1
Flagged first, then by citations
Cited by
Sorted by citations
Joint Hypermobility Syndrome: Recognizing a Commonly Overlooked Cause of Chronic Pain
Kumar, B., & Lenert, P. (2017) · The American Journal of Medicine · doi:10.1016/j.amjmed.2017.02.013 · Cited by 153 · see citing works
Scheper, M., de Vries, J. E., Verbunt, J., & Engelbert, R. H. H. (2015) · Journal of Pain Research · doi:10.2147/jpr.s64251 · Cited by 105 · see citing works
Scheper, M. C., Nicholson, L. L., Adams, R. D., Tofts, L., & Pacey, V. (2017) · Rheumatology · doi:10.1093/rheumatology/kex148 · Cited by 68 · see citing works
Hypermobility spectrum disorders: A review
Carroll, M. B. (2023) · Rheumatology and Immunology Research · doi:10.2478/rir-2023-0010 · Cited by 45 · see citing works
- Authors
- Rombaut, L., Malfait, F., De Wandele, I., Mahieu, N., Thijs, Y., Segers, P., De Paepe, A., & Calders, P.
- Affiliations
- Ghent University (BE)
- Ghent University Hospital (BE)
- Venue
- Arthritis Care & Research
- Publisher
- Wiley
- Published
- 2012-04-23
- Volume
- 64
- Issue
- 5
- Pages
- 766-772
- ISSN
- 0893-7524 (ISSN-L)
- 2151-464X
- 2151-4658
- OpenAlex
- W2137757650
- Cited by
- 71
- References
- 44
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 3 · 2023: 7 · 2022: 9 · 2021: 3 · 2020: 17 · 2019: 2 · 2018: 2 · 2017: 3 · 2016: 6 · 2015: 3 · 2014: 2 · 2013: 5 · 2012: 2
- FWCI
- 2.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Arthritis Care & Research (publishedVersion)
- PubMed (publishedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Connective tissue disorders research
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Tendon Structure and Treatment
- Physical Sciences › Engineering › Biomedical Engineering › Lower Extremity Biomechanics and Pathologies
- Keywords
- muscle-tendon unit, plantar flexors, Achilles tendon stiffness, joint hypermobility, connective tissue, muscle cross-sectional area
- MeSH terms
- Achilles Tendon, Adult, Ehlers-Danlos Syndrome, Female, Humans, Joint Instability, Middle Aged, Muscle Tonus, Surveys and Questionnaires, Muscle, Skeletal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
