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Rehabilitation of dynamic visual acuity in patients with unilateral vestibular hypofunction: earlier is better

  • Otology
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European Archives of Oto-Rhino-Laryngology Aims and scope Submit manuscript

Abstract

Purpose

Patients with acute peripheral unilateral hypofunction (UVH) complain of vertigo and dizziness and show posture imbalance and gaze instability. Vestibular rehabilitation therapy (VR) enhances the functional recovery and it has been shown that gaze stabilization exercises improved the dynamic visual acuity (DVA). Whether the effects of VR depend or not on the moment when it is applied remains however unknown, and investigation on how the recovery mechanisms could depend or not on the timing of VR has not yet been tested.

Methods

Our study investigated the recovery of DVA in 28 UVH patients whose unilateral deficit was attested by clinical history and video head impulse test (vHIT). Patients were tested under passive conditions before (pre-tests) and after (post-tests) being subjected to an active DVA rehabilitation protocol. The DVA protocol consisted in active gaze stabilization exercises with two training sessions per week, each lasting 30 min, during four weeks. Patients were sub-divided into three groups depending on the time delay between onset of acute UVH and beginning of VR. The early DVA group (N = 10) was composed of patients receiving the DVA protocol during the first 2 weeks after onset (mean = 8.9 days), the late group 1 (N = 9) between the 3rd and the 4th week (mean = 27.5 days after) and the late group 2 (N = 9) after the 1st month (mean: 82.5 days). We evaluated the DVA score, the angular aVOR gain, the directional preponderance and the percentage of compensatory saccades during the HIT, and the subjective perception of dizziness with the Dizziness Handicap Inventory (DHI). The pre- and post-VR tests were performed with passive head rotations done by the physiotherapist in the plane of the horizontal and vertical canals.

Results

The results showed that patients submitted to an early DVA rehab improved significantly their DVA score by increasing their passive aVOR gain and decreasing the percentage of compensatory saccades, while the late 1 and late 2 DVA groups 1 and 2 showed less DVA improvement and an inverse pattern, with no change in the aVOR gain and an increase in the percentage of compensatory saccades. All groups of patients exhibited significant reductions of the DHI score, with higher improvement in subjective perception of dizziness handicap in the patients receiving the DVA rehab protocol in the first month.

Conclusion

Our data provide the first demonstration in UVH patients that earlier is better to improve DVA and passive aVOR gain. Gaze stabilization exercises would benefit from the plastic events occurring in brain structures during a sensitive period or opportunity time window to elaborate optimal functional reorganizations. This result is potentially very important for the VR programs to restore the aVOR gain instead of recruiting compensatory saccades assisting gaze stability.

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References

  1. Herdman SJ, Tusa RJ, Blatt PJ, Suzuki A, Venuto PJ, Roberts D (1998) Computerized dynamic visual acuity test in the assessment of vestibular deficits. Am J Otol 19:790–796

    CAS  PubMed  Google Scholar 

  2. Dieringer N (1988) Immediate saccadic substitution for deficits in dynamic vestibular reflexes of frogs with selective peripheral lesions. Prog Brain Res 76:403–409

    Article  CAS  Google Scholar 

  3. Berthoz A (1988) The role of gaze in compensation of vestibular disfunction: the gaze substitution hypothesis. Prog Brain Res 76:411–420. https://doi.org/10.1016/S0079-6123(08)64528-8

    Article  CAS  PubMed  Google Scholar 

  4. Schubert MC, Migliaccio AA, Clendaniel RA, Allak A, Carey JP (2008) Mechanisms of dynamic visual acuity recovery with vestibular rehabilitation. Arch Phys Med Rehabil 89:500–507. https://doi.org/10.1016/j.apmr.2007.11.010

    Article  PubMed  PubMed Central  Google Scholar 

  5. Kazai T, Zee DS (1978) Eye-head coordination in labyrinthine-defective human beings. Brain Res 144:123–141. https://doi.org/10.1016/0006-8993(78)90439-0

    Article  Google Scholar 

  6. Schubert MC, Das V, Tusa RJ, Herdman SJ (2004) Cervico-ocular reflex in normal subjects and patients with unilateral vestibular hypofunction. Otol Neurotol 25:65–71

    Article  Google Scholar 

  7. Bockisch CJ, Straumann D, Hess K, Haslwanter T (2004) Enhanced smooth pursuit eye movements in patients with bilateral vestibular deficits. NeuroReport 15:2617–2620

    Article  Google Scholar 

  8. Gauthier GM, Robinson DM (1975) Adaptation of the human vestibulo-ocular reflex to magnifying lenses. Brain Res 92:331–335

    Article  CAS  Google Scholar 

  9. Schubert MC, Della Santina CC, Shelhamer M (2008) Incremental angular vestibulo-ocular adaptation to active head rotation. Exp Brain Res 191:435–446

    Article  Google Scholar 

  10. Migliaccio AA, Schubert MC (2013) Unilateral adaptation of the human angular vestibulo-ocular reflex. J Assoc Res Otol 14:29–36. https://doi.org/10.1007/s10162-012-0359-7

    Article  Google Scholar 

  11. Migliaccio AA, Schubert MC (2014) Pilot study of a new rehabilitation tool: improved unilateral short-term adaptation of the human angular vestibulo-ocular reflex. Otol Neurotol 35:310–316. https://doi.org/10.1097/MAO.00000000000000539

    Article  Google Scholar 

  12. Crane BT, Schubert MC (2018) An adaptive vestibular rehabilitation technique. Laryngoscope 128:713–718. https://doi.org/10.1002/lary.26661

    Article  PubMed  Google Scholar 

  13. Sadeghi NG, Azad BS, Rassian N, Sadeghi SG (2018) Rebalancing the vestibular system by unidirectional rotations in patients with chronic vestibular dysfunction. Front Neurol. https://doi.org/10.3389/fneur.2018.01196

    Article  PubMed  Google Scholar 

  14. Ushio M, Minor LB, Della Santina CC, Lasker DM (2011) Unidirectional rotations produce asymmetric changes in horizontal VOR gain before and after unilateral labyrinthectomy in macaques. Exp Brain Res 210:651–660. https://doi.org/10.1007/s00221-011-2622-2

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hillier SL, McDonnell M (2011) Vestibular rehabilitation for unilateral peripheral vestibular dysfunction. Cochrane Database Syst Rev 2:CD005397. https://doi.org/10.1002/14651858.CD005397.pub4

    Article  Google Scholar 

  16. Hillier SL, McDonnell M (2016) Is vestibular rehabilitation effective in improving dizziness and function after unilateral peripheral vestibular hypofunction? an abridged version of a Cochrane review. Eur J Phys Rehab Med 52:541–556. https://doi.org/10.1002/14651858.CD005397.pub4

    Article  Google Scholar 

  17. Herdman SJ, Schubert MC, Das VE, Tusa RJ (2003) Recovery of dynamic visual acuity in unilateral vestibular hypofunction. Arch Otolaryngol Head Neck Surg 129:819–824. https://doi.org/10.1001/archotol.129.8.819

    Article  PubMed  Google Scholar 

  18. Jacobson GP, Newman CW (1990) The development of the dizziness handicap inventory. Arch Otolaryngol Head Neck Surg 116:424–427. https://doi.org/10.1001/archotol.1990.01870040046011

    Article  CAS  PubMed  Google Scholar 

  19. Herdman SJ, Hall CD, Schubert MC, Das VE, Tusa RJ (2007) Recovery of dynamic visual acuity in bilateral vestibular hypofunction. Arch Otolaryngol Head Neck Surg 133:383–389. https://doi.org/10.1001/archotol.133.4.383

    Article  PubMed  Google Scholar 

  20. Lacour M (2006) Restoration of vestibular function: basic aspects and practical advances for rehabilitation. Curr Med Res Opin 22:1651–1659. https://doi.org/10.1185/030079906X115694

    Article  PubMed  Google Scholar 

  21. Lacour M, Tighilet B (2010) Plastic events in the vestibular nuclei during vestibular compensation: the brain orchestration of a deafferentation code. Rest Neurol Neurosci 28:19–35. https://doi.org/10.3233/RNN-2010-0509

    Article  Google Scholar 

  22. Lacour M, Bernard-Demanze L (2014) Interaction between vestibular compensation mechanisms and vestibular rehabilitation therapy. 10 recommendations for optimal functional recovery. Front Neurol 5:285

    PubMed  Google Scholar 

  23. Lacour M, Helmchen C, Vidal PP (2015) Vestibular compensation: the neuro-otologist’s best friend. J Neurol. https://doi.org/10.1007/s00415-015-7903-4

    Article  PubMed  Google Scholar 

  24. Hall CD, Herdman SJ, Whitney SL, Cass SP, Clendaniel RA, Fife TD, Furman JM, Getchius TS, Goebel JA, Shepard NT, Woodhouse SN (2016) Vestibular rehabilitation for peripheral vestibular hypofunction: an evidence-based clinical practice guidelines. J Neurol Phys Ther 40:124–155. https://doi.org/10.1097/NPT.000000000120

    Article  PubMed  PubMed Central  Google Scholar 

  25. Strupp M, Magnusson M (2015) Acute unilateral vestibulopathy. Neurol Clin 33:669–685. https://doi.org/10.1016/J.ncl.2015.04.012

    Article  PubMed  Google Scholar 

  26. Kunel’s skaya NL, Naibakova EV, Guseva AL, Nikitkina YY, Chugunova MA, Manaenkova EA (2018) The compensation of the vestibulo-ocular reflex during rehabilitation of the patients presenting with vestibular neuritis. Vestn Otorinolaringol 83:27–31. https://doi.org/10.17116/otorino201883127-31

    Article  Google Scholar 

  27. Wai Yip C, Strupp M (2018) The dizziness handicap inventory does not correlate with vestibular function tests: a prospective study. J Neurol 265:1210–1218. https://doi.org/10.1007/s00415-018-8834.7

    Article  Google Scholar 

  28. Szturm T, Ireland DJ, Lessing-Turner M (1994) Comparison of different exercise programs in the rehabilitation of patients with chronic peripheral vestibular dysfunction. J Vest Res 4:461–479

    Article  CAS  Google Scholar 

  29. Lee HJ, Kim SH, Jung J (2018) Long-term changes in video head impulse and caloric tests in patients with unilateral vestibular neuritis. Korean J Otolaryng Head Neck Surg. https://doi.org/10.3342/kjorl-hns.2017.01081

    Article  Google Scholar 

  30. Allred RP, Kim SY, Jones TA (2014) Use it and/or lose it—experience effects on brain remodeling across time after stroke. Front Human Neurosci. https://doi.org/10.3389/fnhum.2014.00379

    Article  Google Scholar 

  31. Tian J, Shubayev I, Demer JL (2007) Dynamic visual acuity during passive and self-generated transient head rotation in normal and unilaterally vestibulopathic humans. Exp Brain Res 142:486–495. https://doi.org/10.1007/s00221-001-0959-7

    Article  Google Scholar 

  32. Kunel’skaya NL, Baibakova EV, Guseva AL, Nikitkina YY, Chugunova MA, Manaenkova EA (2018) The compensation of the vestibule-ocular reflex during rehabilitation of the patients presenting with vestibular neuritis. Vestn Otorinolaringol 83:27–31. https://doi.org/10.17116/otorino201883127-31

    Article  PubMed  Google Scholar 

  33. Gall C, Lynch G (1981) The regulation of axonal sprouting in the adult hippocampus: some insights from developmental studies. In: Lesion-induced neuronal plasticity in sensorimotor systems. Flohr H, Precht W (Eds). Springer-Verlag, Berlin, Heidelberg. 10.1007/978-3-462-68074-8

  34. Dieringer N, Precht W (1979) Mechanisms of compensation for vestibular deficits in the frog. I. Modifications of the excitatory commissural system. Exp Brain Res 36:311–328. https://doi.org/10.1007/BF00238914

    Article  CAS  PubMed  Google Scholar 

  35. Dieringer N, Precht W (1979) Mechanisms of compensation for vestibular deficits in the frog. I. Modifications of the inhibitory pathways. Exp Brain Res 36:329–341. https://doi.org/10.1007/BF00238915

    Article  CAS  PubMed  Google Scholar 

  36. Segal BN, Katsarkas A (1988) Goal directed vestibulo-ocular function in man: gaze stabilization by slow-phase and saccadic eye movements. Exp Brain Res 70:26–32

    CAS  PubMed  Google Scholar 

  37. Bloomberg J, Melvill Jones G, Segal B (1991) Adaptive plasticity in the gaze stabilizing synergy of slow and saccadic eye movements. Exp Brain Res 84:35–46

    CAS  PubMed  Google Scholar 

  38. Trinidad-Ruiz G, Martinez JR, Batuecas-Caletrio A, Perez-Fernandez N (2018) Visual performance and perception as a target of saccadic strategies in patients with unilateral vestibular loss. Ear Hear. https://doi.org/10.1097/AUD.00000576

    Article  PubMed  Google Scholar 

  39. McGarvie LA, McDougall HG, Halmagyi GM, Burgess AM, Weber KP, Curthoys IS (2015) The video head impulse test (vHIT) of semicircular canal function-age-dependent normative values of VOR gain in healthy subjects. Front Neurol 6:154. https://doi.org/10.3389/fneur.2015.00154

    Article  PubMed  PubMed Central  Google Scholar 

  40. Cowand JL, Wrisley DM, Walker M, Strasnick B, Jacobson JT (1998) Efficacy of vestibular rehabilitation. Otolaryngol Head Neck Surg 118:49–54. https://doi.org/10.1016/S0194-5998(98)70374-2

    Article  CAS  PubMed  Google Scholar 

  41. Topuz O, Topuz B, Ardic FN, Sarhus M, Ogmen G, Ardic F (2004) Efficacy of vestibular rehabilitation on chronic unilateral vestibular hypofunction. Clin Rehabil 18:76–83. https://doi.org/10.1191/0269215504cr704oa

    Article  PubMed  Google Scholar 

  42. Ramachandran R, Lisberger SG (2008) Neural substrates for modified and unmodified pathways for learning in monkey vestibule-ocular reflex. J Neurophysiol 100:1868–1878. https://doi.org/10.1152/jn.90498.2008

    Article  PubMed  PubMed Central  Google Scholar 

  43. Van Nechel C, Bostan A, Duquesne U, Hautefort C, Toupet M (2019) Visual input is the main trigger and parametric determinant for catch-up saccades during video head impulse test in bilateral vestibular loss. Front Neurol 4(9):1138. https://doi.org/10.3389/fneur.2018.01138.eCollection2018

    Article  Google Scholar 

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Acknowledgments

We thank all the patients for their active participation in the study

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Contributions

LT diagnosed and selected the patients included in the study; AT did the vestibular rehabilitation of the patients; ML, AT and LT elaborated the experimental protocol; ML wrote the paper; and LT, AT and ML corrected together the manuscript.

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Correspondence to Lacour Michel.

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Michel, L., Laurent, T. & Alain, T. Rehabilitation of dynamic visual acuity in patients with unilateral vestibular hypofunction: earlier is better. Eur Arch Otorhinolaryngol 277, 103–113 (2020). https://doi.org/10.1007/s00405-019-05690-4

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