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.
Similar content being viewed by others
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
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
Boyle J, Negus V (1998) Joint position sense in the recurrently sprained ankle. Aust J Physiother 44:1998
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
Clancy E, Morin E, Merletti R (2002) Sampling, noise-reduction and amplitude estimation issues in surface electromyography. J Electromyogr Kinesiol 12:1–16
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
Docherty CL, Arnold BL (2008) Force sense deficits in functionally unstable ankles. J Orthop Res 26:1489–1493
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
Eils E, Rosenbaum D (2001) A multi-station proprioceptive exercise program in patients with ankle instability. Med Sci Sports Exerc 33:1991–1998
Ferran NA, Maffulli N (2006) Epidemiology of sprains of the lateral ankle ligament complex. Foot Ankle Clin 11:659–662
Freeman M (1965) Instability of the foot after injuries to the lateral ligament of the ankle. J Bone Joint Surg 47:669–677
Freeman M, Dean M, Hanham I (1965) The etiology and prevention of functional instability of the foot. J Bone Joint Surg 49:678–683
Garn SN, Newton RA (1988) Kinesthetic awareness in subjects with multiple ankle sprains. Phys Ther 68:1667–1671
Glencross D, Thornton E (1981) Position sense following joint injury. J Sport Med Phys Fit 21:23–27
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
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
Hertel J (2002) Functional anatomy, pathomechanics, and pathophysiology of lateral ankle instability. J Athl Train 37:364–375
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
Jackson LT, Dunaway LJ, Lundeen GA (2017) Acute tears of the tibialis posterior tendon following ankle sprain. Foot Ankle Int 38:752–759
Kamen G, Caldwell GE (1996) Physiology and interpretation of the electromyogram. Clin Neurophysiol 13:366–384
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
Khasnis A, Gokula RM (2003) Romberg’s test. J Postgrad Med 49:169
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
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
Konradsen L (2002) Factors contributing to chronic ankle instability: kinesthesia and joint position sense. J Athl Train 37:381–385
Konradsen L, Ravn JB (1990) Ankle instability caused by prolonged peroneal reaction time. Acta Orthop Scand 61:388–390
Konradsen L, Ravn JB (1991) Prolonged peroneal reaction time in ankle instability. Int J Sports Med 12:290–292
Lai CHY, Li-Tsang CWP (2009) Validation of the Pliance X System in measuring interface pressure generated by pressure garment. Burns 35:845–851
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
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
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
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
Peetrons P, Creteur V, Bacq C (2004) Sonography of ankle ligaments. J Clin Ultrasound 32(9):491–499
Perotto A, Delagi E, Iazetti J, Morrison D (1997) Anatomical guide for the electromyographer—the limbs and trunk. Charles C Thomas, Springfield
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
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
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
Sarrafian SK (1993) Anatomy of the foot and ankle descriptive, topographic, functional. Lippincott, Phiadelphia
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
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
Soderberg GL, Cook TM (1984) Electromyography in biomechanics. Phys Ther 64:1813–1820
Solomonow M (2006) Sensory—motor control of ligaments and associated neuromuscular disorders. J Electromyogr Kinesiol 16:549–567
Solomonow M, Lewis J (2002) Reflex from the ankle ligaments of the feline. J Electromyogr Kinesiol 12:193–198
Taube W, Gruber M, Gollhofer A (2008) Spinal and supraspinal adaptations associated with balance training and their functional relevance. Acta Physiol 193:101–116
Tropp H (1986) Pronator muscle weakness in functional instability of the ankle joint. Int J Sports Med 7:291–294
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
Yeung M, Chan K, So C, Yuan W (1994) An epidemiological survey on ankle sprain. Br J Sports Med 28:112–116
Zipp P (1982) Recommendations for the standardization of lead positions in surface electromyography. Eur J Appl Physiol Occup Physiol 50:41–54
Zwipp H (1986) Die anterolaterale Rotationsinstabilität des oberen Sprunggelenkes. Hefte Unfallheilkd 177:41–59
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.
Author information
Authors and Affiliations
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
Ethics declarations
Conflict of interest
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.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00167-020-06232-w