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Alterated ligamento-muscular reflex pattern after stimulation of the anterior talofibular ligament in functional ankle instability

  • Ankle
  • Published:
Knee Surgery, Sports Traumatology, Arthroscopy Aims and scope

Abstract

Purpose

Ligamento-muscular reflex pattern following stimulation of the anterior talofibular ligament (ATFL) was examined.

Methods

The peroneus longus (PL), the tibialis anterior (TA), and tibialis posterior (TP) muscles were investigated in sixteen patients with functional ankle instability (FAI) and 16 age- and gender-matched controls. The ATFL was stimulated with a fine wire electrode while electromyographic (EMG) activities were recorded during isometric foot contraction of 20% maximal force in plantarflexion, dorsiflexion, supination and pronation. The complete measurement was repeated after a peroneal block anesthesia.

Results

Statistically significant changes in post-stimulus EMG activity were observed in all three muscles and all four tested foot positions. In supination, the PL showed no reactions in both groups before and after anesthesia. The post-stimulus inhibition of the TA seen after 80 and 180 ms disappeared in controls after anesthesia. The TP had similar inhibitory responses in both groups.

Conclusion

Ligamento-muscular reflex pattern is alterated in FAI. While early reactions are essential in protecting the ankle joint in sudden movements, the later responses indicate a supraspinal control of neuromuscular stability of the ankle joint. Proprioceptive rehabilitation of the PL, TA, and TP is crucial in FAI to compensate for post-traumatic ligamentomuscular reflex deficiencies.

Level of evidence

II.

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Abbreviations

ATFL:

Anterior talofibular ligament

CFL:

Calcaneofibular ligament

EMG:

Electromyography

FAI:

Functional ankle instability

PL:

Peroneus longus muscle

TA:

Tibialis anterior muscle

TP:

Tibialis posterior muscle

References

  1. Bahr R, Pena F, Shine J, Lew WD, Engebretsen L (1998) Ligament force and joint motion in the intact ankle: a cadaveric study. Knee Surg Sport Traumatol Arthrosc 6:115–121

    CAS  Google Scholar 

  2. Boyle J, Negus V (1998) Joint position sense in the recurrently sprained ankle. Aust J Physiother 44:1998

    Google Scholar 

  3. Brunt D, Andersen JC, Huntsman B, Reinhert LB, Thorell AC, Sterling JC (1992) Postural responses to lateral perturbation in healthy subjects and ankle sprain patients. Med Sci Sports Exerc 24(2):171–176

    CAS  PubMed  Google Scholar 

  4. Clancy E, Morin E, Merletti R (2002) Sampling, noise-reduction and amplitude estimation issues in surface electromyography. J Electromyogr Kinesiol 12:1–16

    CAS  PubMed  Google Scholar 

  5. Diederichsen LP, Nørregaard J, Krogsgaard M, Fischer-Rasmussen T, Dyhre-Poulsen P (2004) Reflexes in the shoulder muscles elicited from the human coracoacromial ligament. J Orthop Res 22:976–983

    PubMed  Google Scholar 

  6. Docherty CL, Arnold BL (2008) Force sense deficits in functionally unstable ankles. J Orthop Res 26:1489–1493

    PubMed  Google Scholar 

  7. Dyhre-Poulsen P, Krogsgaard MR (2000) Muscular reflexes elicited by electrical stimulation of the anterior cruciate ligament in humans. J Appl Physiol 89:2191–2195

    CAS  PubMed  Google Scholar 

  8. Eils E, Rosenbaum D (2001) A multi-station proprioceptive exercise program in patients with ankle instability. Med Sci Sports Exerc 33:1991–1998

    CAS  PubMed  Google Scholar 

  9. Ferran NA, Maffulli N (2006) Epidemiology of sprains of the lateral ankle ligament complex. Foot Ankle Clin 11:659–662

    PubMed  Google Scholar 

  10. Freeman M (1965) Instability of the foot after injuries to the lateral ligament of the ankle. J Bone Joint Surg 47:669–677

    CAS  Google Scholar 

  11. Freeman M, Dean M, Hanham I (1965) The etiology and prevention of functional instability of the foot. J Bone Joint Surg 49:678–683

    Google Scholar 

  12. Garn SN, Newton RA (1988) Kinesthetic awareness in subjects with multiple ankle sprains. Phys Ther 68:1667–1671

    CAS  PubMed  Google Scholar 

  13. Glencross D, Thornton E (1981) Position sense following joint injury. J Sport Med Phys Fit 21:23–27

    CAS  Google Scholar 

  14. Granacher U, Gruber M, Förderer D, Strass D, Gollhofer A (2010) Effects of ankle fatigue on functional reflex activity during gait perturbations in young and elderly men. Gait Posture 32:107–112

    PubMed  Google Scholar 

  15. Hagert E, Persson JKE, Werner M, Ljung BO (2009) Evidence of wrist proprioceptive reflexes elicited after stimulation of the scapholunate interosseous ligament. J Hand Surg Am 34:642–651

    PubMed  Google Scholar 

  16. Hertel J (2002) Functional anatomy, pathomechanics, and pathophysiology of lateral ankle instability. J Athl Train 37:364–375

    PubMed  PubMed Central  Google Scholar 

  17. Jaber H, Lohman E, Daher N, Bains G, Nagaraj A, Mayekar P, Shanbhag M, Alameri M (2018) Neuromuscular control of ankle and hip during performance of the star excursion balance test in subjects with and without chronic ankle instability. PLoS One 13:1–16

    Google Scholar 

  18. Jackson LT, Dunaway LJ, Lundeen GA (2017) Acute tears of the tibialis posterior tendon following ankle sprain. Foot Ankle Int 38:752–759

    PubMed  Google Scholar 

  19. Kamen G, Caldwell GE (1996) Physiology and interpretation of the electromyogram. Clin Neurophysiol 13:366–384

    CAS  Google Scholar 

  20. Kazemi K, Arab AM, Abdollahi I, López-López D, Calvo-Lobo C (2017) Electromiography comparison of distal and proximal lower limb muscle activity patterns during external perturbation in subjects with and without functional ankle instability. Hum Mov Sci 55:211–220

    PubMed  Google Scholar 

  21. Khasnis A, Gokula RM (2003) Romberg’s test. J Postgrad Med 49:169

    CAS  PubMed  Google Scholar 

  22. Kim K-M, Kim J-S, Cruz-Díaz D, Ryu S, Kang M, Taube W (2019) Changes in spinal and corticospinal excitability in patients with chronic ankle instability: a systematic review with meta-analysis. J Clin Med 8:1037

    PubMed Central  Google Scholar 

  23. Konrad P (2005) The ABC of EMG—a practical introduction to kinesiological electromyography. Noraxon Inc., Scottsdale. https://www.noraxon.com/wp-content/uploads/2014/12/ABC-EMG-ISBN.pdf

  24. Konradsen L (2002) Factors contributing to chronic ankle instability: kinesthesia and joint position sense. J Athl Train 37:381–385

    PubMed  PubMed Central  Google Scholar 

  25. Konradsen L, Ravn JB (1990) Ankle instability caused by prolonged peroneal reaction time. Acta Orthop Scand 61:388–390

    CAS  PubMed  Google Scholar 

  26. Konradsen L, Ravn JB (1991) Prolonged peroneal reaction time in ankle instability. Int J Sports Med 12:290–292

    CAS  PubMed  Google Scholar 

  27. Lai CHY, Li-Tsang CWP (2009) Validation of the Pliance X System in measuring interface pressure generated by pressure garment. Burns 35:845–851

    PubMed  Google Scholar 

  28. Löfvenberg R, Kärrholm J, Sundelin G, Ahlgren O (1995) Reaction time in patients with chronic lateral instability of the ankle prolonged. Am J Sport Med 23:414–417

    Google Scholar 

  29. Martina IS, van Koningsveld R, Schmitz PI, van der Meché FG, van Doorn PA (1998) Measuring vibration threshold with a graduated tuning fork in normal aging and in patients with polyneuropathy. European Inflammatory Neuropathy Cause and Treatment (INCAT) Group. J Neurol Neurosurg Psychiatry 65:743–747

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Mobargha N, Rein S, Hagert E (2019) Ligamento-muscular reflex patterns following stimulation of a thumb carpometacarpal ligament: an electromyographic study. J Hand Surg Am 44:248.e1–248.e9

    Google Scholar 

  31. Papegaaij S, Taube W, Baudry S, Otten E, Hortobágyi T (2014) Aging causes a reorganization of cortical and spinal control of posture. Front Aging Neurosci 6:1–15

    Google Scholar 

  32. Peetrons P, Creteur V, Bacq C (2004) Sonography of ankle ligaments. J Clin Ultrasound 32(9):491–499

    PubMed  Google Scholar 

  33. Perotto A, Delagi E, Iazetti J, Morrison D (1997) Anatomical guide for the electromyographer—the limbs and trunk. Charles C Thomas, Springfield

    Google Scholar 

  34. Phillips D, Petrie S, Solomonow M, Zhou BH, Guanche C, D’Ambrosia R (1997) Ligamentomuscular protective reflex in the elbow. J Hand Surg Am Surg 22(3):473–478

    CAS  Google Scholar 

  35. Rein S, Hagert E, Hanisch U, Lwowski S, Fieguth A, Zwipp H (2013) Immunohistochemical analysis of sensory nerve endings in ankle ligaments: a cadaver study. Cells Tissues Organs 197:64–76

    PubMed  Google Scholar 

  36. Rivera MJ, Winkelmann ZK, Powden CJ, Games KE (2017) Proprioceptive training for the prevention of ankle sprains: an evidence-based review. J Athl Train 52:1065–1067

    PubMed  PubMed Central  Google Scholar 

  37. Sarrafian SK (1993) Anatomy of the foot and ankle descriptive, topographic, functional. Lippincott, Phiadelphia

    Google Scholar 

  38. Schmidt R, Gerngroß H, Friemert B, Herbst A, Claes L (2005) The peroneal reaction time (PRT)—reference data in a healthy sample population. Foot Ankle Int 26:382–386

    PubMed  Google Scholar 

  39. Semple R, Murley GS, Woodburn J, Turner DE (2009) Tibialis posterior in health and disease: a review of structure and function with specific reference to electromyographic studies. J Foot Ankle Res 2:24

    PubMed  PubMed Central  Google Scholar 

  40. Soderberg GL, Cook TM (1984) Electromyography in biomechanics. Phys Ther 64:1813–1820

    CAS  PubMed  Google Scholar 

  41. Solomonow M (2006) Sensory—motor control of ligaments and associated neuromuscular disorders. J Electromyogr Kinesiol 16:549–567

    CAS  PubMed  Google Scholar 

  42. Solomonow M, Lewis J (2002) Reflex from the ankle ligaments of the feline. J Electromyogr Kinesiol 12:193–198

    PubMed  Google Scholar 

  43. Taube W, Gruber M, Gollhofer A (2008) Spinal and supraspinal adaptations associated with balance training and their functional relevance. Acta Physiol 193:101–116

    CAS  Google Scholar 

  44. Tropp H (1986) Pronator muscle weakness in functional instability of the ankle joint. Int J Sports Med 7:291–294

    CAS  PubMed  Google Scholar 

  45. Tropp H, Odenrick P, Gillquist J (1985) Stabilometry recordings in functional and mechanical instability of the ankle joint. Int J Sports Med 6:180–182

    CAS  PubMed  Google Scholar 

  46. Yeung M, Chan K, So C, Yuan W (1994) An epidemiological survey on ankle sprain. Br J Sports Med 28:112–116

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Zipp P (1982) Recommendations for the standardization of lead positions in surface electromyography. Eur J Appl Physiol Occup Physiol 50:41–54

    Google Scholar 

  48. Zwipp H (1986) Die anterolaterale Rotationsinstabilität des oberen Sprunggelenkes. Hefte Unfallheilkd 177:41–59

    Google Scholar 

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Acknowledgements

We thank Ursula Range (Institute for Medical Informatics and Biometry, University Hospital ‘‘Carl Gustav Carus’’, Dresden, Germany) for statistical support, Jonas K. E. Persson, MD, PhD (Department of Clinical Neuroscience, Section of Neurophysiology, Stockholm, Sweden), Thomas Albrecht and Heiko Lange (Center for Orthopedics and Trauma Surgery, University Hospital ‘‘Carl Gustav Carus), and Christian Retschke (Leipzig) for logistic support as well as Jochen Schäfer, MD, and Martin Pette, MD, PhD (Department of Neurology, University Hospital „Carl Gustav Carus“, Dresden, Germany). Furthermore, we thank Axel Kalpen (novel biomechanic laboratory, https://www.novel.de, Ismaninger Straße 51, 81675 Munich, Germany) for technical support.

Funding

This study has been financially supported by Bauerfeind AG, Zeulenroda-Triebes, Germany (Grant no.: 100_3380). The authors disclose any financial conflicts of interest that may influence the interpretation of this study and/or results.

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Contributions

All authors made substantive intellectual contributions to this study, in conception and design (SR, EH, TSH), acquisition of data (SR, TSH), analysis and interpretation of data (SR, EH, TSH), drafting and revising the manuscript (SR, EH, TSH), as well as final approval of the version to be submitted (SR, EH, TSH). All authors have read and approved the final submitted manuscript.

Corresponding author

Correspondence to Susanne Rein.

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The authors declare that they have no competing interests.

Ethical approval

The local ethical committee of the Medical Faculty of the Technical University Dresden approved this study under the processing number: EK34022012.

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Informed consent was obtained from all individual participants included in the study.

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Rein, S., Hagert, E. & Sterling-Hauf, T. Alterated ligamento-muscular reflex pattern after stimulation of the anterior talofibular ligament in functional ankle instability. Knee Surg Sports Traumatol Arthrosc 29, 1544–1553 (2021). https://doi.org/10.1007/s00167-020-06232-w

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