Presbyvestibulopathy

By Marcello Cherchi, MD PhD

For patients

Presbyvestibulopathy refers to disequilibrium that is due only to loss of inner ear balance function from normal heathy aging. If your doctor suspects this diagnosis, they may consider checking several tests of balance function, and in some cases may also try to assess whether any other diseases are present that might interfere with your equilibrium. If no other explanation is found, then the management strategy for presbyvestibulopathy is vestibular rehabilitation therapy.

For clinicians

Overview

The term “presbyvestibulopathy” refers to disequilibrium that is only attributable to age-related reduction of vestibular function. Diagnostic criteria specify quantitative vestibular test results for this diagnosis. Histopathological studies have shown clear evidence of what appears to be age-related degeneration of most structures along the vestibular pathway (otoconia, vestibular hair cells, vestibular ganglion, vestibular nerve, vestibular nuclei), which is the likely mechanism underlying both the abnormal responses in quantitative vestibular function tests and the symptom of disequilibrium. A clinician should bear in mind that healthy aging is also associated with attrition of other sensoria (presbyopia, reduced proprioception), so in many if not most instances, reduced vestibular function is actually only one of several contributors to the symptom of disequilibrium, and thus multifactorial disequilibrium is more commonly encountered than “pure” presbyvestibulopathy. A trial of vestibular rehabilitation therapy is appropriate.

Introduction

The idea that the symptom of disequilibrium can arise exclusively from age-related deterioration of the vestibular system is not new (Matheson et al. 1999), but a formal definition was proposed only relatively recently.

Agrawal and colleagues (Agrawal et al. 2019) authored a consensus paper for the Barany Society’s classification committee proposing diagnostic criteria for presbyvestibulopathy, which they define as, “Mild or incomplete vestibular losses attributable to the normative aging process.” They purposefully choose this term to designate incomplete vestibular loss, analogous to terms such as “presbyopia” (age-related vision decline but not complete blindness) and “presbycusis” (age-related hearing loss but not complete deafness).

The specific diagnostic criteria they propose for presbyvestibulopathy are:

1. Chronic vestibular syndrome (at least 3 months duration) with at least 2 of the following symptoms:
   • Postural imbalance or unsteadiness
   • Gait disturbance
   • Chronic dizziness
   • Recurrent falls
2. Mild bilateral peripheral vestibular hypofunction documented by at least 1 of the following:
   • VOR [vestibulo-ocular reflex] gain measured by video-HIT [head impulse testing] between 0.6 and 0.8 bilaterally.
   • VOR gain between 0.1 and 0.3 upon sinusoidal stimulation on rotatory chair (0.1 Hz, V_max = 50˚-60˚/sec).
   • Reduced caloric response (sum of bithermal maximum peak SPV [slow phase velocity] on each side between 6˚ and 25˚/sec).
3. Age ≥ 60 years.
4. Not better accounted for by another disease or disorder.

Epidemiology

The epidemiology of presbyvestibulopathy per the Barany Society criteria is unknown. Many studies cite the increase of fall risk with age (Zalewski 2015), but this is not a proxy for presbyvestibulopathy itself.

Pathophysiological mechanism of disease

If one takes the working definition of presbyvestibulopathy proposed by Agrawal and colleagues (Agrawal et al. 2019), the mechanism is reduced vestibular function due to the natural attrition that occurs in normal healthy aging. Data from histopathological studies to support this idea (see below).

In addition, the neural plasticity mechanisms (which usually can help compensate to some extent for sensory deficits) become less effective with age (Paige 1992), so this “rescue mechanism” becomes progressively less available over time.

Clinical presentation

Patients diagnosed with presbyvestibulopathy often describe an insidious onset of imbalance or unsteadiness, and because of the gradual onset they may have difficulty pinpointing the start of symptoms. If a patient describes apoplectic onset of disequilibrium, then other diagnoses should be considered.

Physical examination

In patients meeting the Barany Society criteria (Agrawal et al. 2019) for presbyvestibulopathy and carry no other diagnosis, physical examination is generally unrevealing. These patients perform poorly on unsighted tandem Romberg testing, but this is non-specific since performance on that test declines with age in healthy individuals (Agrawal et al. 2011).

Testing: vestibular

The only quantitative factors included in the diagnostic criteria proposed by Agrawal and colleagues (Agrawal et al. 2019) are video head impulse testing, caloric testing (on videonystagmography) and slow harmonic acceleration (on rotatory chair testing). Two of these tests are reasonably widely available (video head impulse testing, videonystagmography), while one is not (rotatory chair testing).

However, there is compelling evidence that responses on each clinical vestibular test deteriorate in normal healthy aging (Bermudez Rey et al. 2016):

• Vestibulo-ocular reflexes:
  • Vestibulo-ocular reflex (low end of the vestibular tuning frequency spectrum) of the horizontal semicircular canal, as measured on caloric testing (Agrawal et al. 2012; Hajioff et al. 2000; Maes et al. 2010; Peterka et al. 1990b).
  • Vestibulo-ocular reflex (middle of the vestibular tuning frequency spectrum), as measured on rotatory chair testing (Baloh et al. 1993; Chan et al. 2016; Peterka et al. 1990a).
  • Vestibulo-ocular reflex gain (high-end of the vestibular tuning frequency spectrum), as measured on video head impulse testing (Guerra Jimenez and Perez Fernandez 2016; Kim and Kim 2018; Matino-Soler et al. 2015; Mossman et al. 2015).
  • Step velocity testing as measured on rotatory chair testing (DiZio and Lackner 1990).
• Saccadic function: Saccadic latency, velocity and accuracy, as measured on oculography (Irving and Lillakas 2019; Warabi et al. 1984).
• Pursuit: Smooth pursuit, as measured on oculography (Kato et al. 1995; Sakuma et al. 2000; Sharpe and Sylvester 1978; Spooner et al. 1980; Zackon and Sharpe 1987).
• Optokinetic responses:
  • Horizontal optokinetic responses, as measured on rotatory chair testing (Baloh et al. 1993; Lynch et al. 1985).
  • Torsional optokinetic responses (Farooq et al. 2008).
• Otolith responses:
  • Cervical vestibular evoked myogenic potentials’ latencies, thresholds and amplitudes (Agrawal et al. 2012; Bi et al. 2016; Janky and Shepard 2009; Maes et al. 2010; Ochi and Ohashi 2003; Su et al. 2004; Welgampola and Colebatch 2001).
  • Ocular vestibular evoked myogenic potentials’ latencies, thresholds and amplitudes (Agrawal et al. 2012; Bi et al. 2016; Singh and Firdose 2021).
  • Subjective visual vertical (Baccini et al. 2014; Cakrt et al. 2016; Fukata et al. 2017; Toupet et al. 2015; Zakaria et al. 2019).
• Postural responses, as measured on computerized dynamic posturography (Peterka and Black 1990a, b).

Despite the current limited definition of presbyvestibulopathy promulgated by the Barany Society (Agrawal et al. 2019), in clinical practice we take into account results of all vestibular tests when attempting to secure this diagnosis. We anticipate that future revisions of the diagnostic criteria for presbyvestibulopathy are likely to do the same.

Histopathology

Histopathological studies of the temporal bone and brain clearly document age-related changes in vestibular structures in otherwise healthy individuals, including:

• Labyrinth:
  • Reduced number of otoconia, degenerated otoconia (Walther and Westhofen 2007).
  • Accumulation of lipofuscin inclusions in vestibular hair cells (Walther and Westhofen 2007) and sustentacular cells (Rosenhall and Rubin 1975).
  • Deformation of cilia (Rosenhall and Rubin 1975; Walther and Westhofen 2007).
  • Decreasing hair cell counts (Rauch et al. 2001) (Walther and Westhofen 2007) of both type I and type II vestibular hair cells (Merchant et al. 2000) and therefore decreasing hair cell densities.
• Vestibular ganglion: Decreasing number of nerve cells in Scarpa’s ganglion (Richter 1980).
• Vestibular nerve: Decreasing number of vestibular fibers (Rasmussen 1940).
• Brainstem: Loss of neurons in the vestibular nuclei (Lopez et al. 1997).

Differential diagnosis

To this point we have discussed presbyvestibulopathy in the sense intended by the Barany Society’s diagnostic criteria (Agrawal et al. 2019), which is to say that exclusively vestibular deficits account for disequilibrium (“Not better accounted for by another disease or disorder”).

For purposes of research it is desirable to isolate a single variable (in this case, “vestibular function”) and observe its activity while keeping all other variables unchanged. In a complex biological system this is rarely achievable.

Thus, we appreciate the Barany Society’s proposal of a definition for presbyvestibulopathy as a theoretical construct. In practice, a clinician would rarely encounter an elderly person presenting with a chief complaint of disequilibrium who turns out to have only mild vestibular weakness and no other pathology at all. Even if an individual carries no other formal diagnoses, all sensory modalities undergo attrition with normal healthy aging. For example, it is well established that in normal healthy aging there is progressive decline in vision (Erdinest et al. 2021) and proprioception (Robbins et al. 1995; Skinner et al. 1984).

In other words, in clinical practice, presbyvestibulopathy in isolation is probably rarely, if ever, encountered. The more likely scenario is that when an older person complains of disequilibrium, there are several factors contributing to that presentation (Tuunainen et al. 2011), of which reduced vestibular function is only one. Thus, the otoneurologist and neuro-otologist should keep the likelihood of multifactorial disequilibrium in mind.

In such patients it is also important to consider common vestibular diseases, such as benign paroxysmal positional vertigo, whose incidence increases with age.

Treatment

For a patient who meets the Barany Society’s diagnostic criteria of presbyvestibulopathy (Agrawal et al. 2019), it is always reasonable to attempt a trial of vestibular rehabilitation therapy.

Prognosis

A process of age-related deterioration tends to be progressive, and this likely also applies to the clinical manifestations of presbyvestibulopathy.

References

Agrawal Y, Carey JP, Hoffman HJ, Sklare DA, Schubert MC (2011) The modified Romberg Balance Test: normative data in U.S. adults. Otol Neurotol 32: 1309-11. doi: 10.1097/MAO.0b013e31822e5bee

Agrawal Y, Van de Berg R, Wuyts F, Walther L, Magnusson M, Oh E, Sharpe M, Strupp M (2019) Presbyvestibulopathy: Diagnostic criteria Consensus document of the classification committee of the Barany Society. J Vestib Res 29: 161-170. doi: 10.3233/VES-190672

Agrawal Y, Zuniga MG, Davalos-Bichara M, Schubert MC, Walston JD, Hughes J, Carey JP (2012) Decline in semicircular canal and otolith function with age. Otol Neurotol 33: 832-9. doi: 10.1097/MAO.0b013e3182545061

Baccini M, Paci M, Del Colletto M, Ravenni M, Baldassi S (2014) The assessment of subjective visual vertical: comparison of two psychophysical paradigms and age-related performance. Atten Percept Psychophys 76: 112-22. doi: 10.3758/s13414-013-0551-9

Baloh RW, Jacobson KM, Socotch TM (1993) The effect of aging on visual-vestibuloocular responses. Exp Brain Res 95: 509-16.

Bermudez Rey MC, Clark TK, Wang W, Leeder T, Bian Y, Merfeld DM (2016) Vestibular Perceptual Thresholds Increase above the Age of 40. Front Neurol 7: 162. doi: 10.3389/fneur.2016.00162

Bi X, Zhou HF, Su J, Zhang J, Wang MX (2016) [The normative values of vestibular evoked myogenic potential in different age-groups]. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 30: 1016-1020. doi: 10.13201/j.issn.1001-1781.2016.13.003

Cakrt O, Slaby K, Kmet J, Kolar P, Jerabek J (2016) Subjective visual and haptic vertical in young and elderly. J Vestib Res 25: 195-9. doi: 10.3233/VES-150562

Chan FM, Galatioto J, Amato M, Kim AH (2016) Normative data for rotational chair stratified by age. Laryngoscope 126: 460-3. doi: 10.1002/lary.25497

DiZio P, Lackner JR (1990) Age differences in oculomotor responses to step changes in body velocity and visual surround velocity. J Gerontol 45: M89-94.

Erdinest N, London N, Lavy I, Morad Y, Levinger N (2021) Vision through Healthy Aging Eyes. Vision (Basel) 5. doi: 10.3390/vision5040046

Farooq SJ, Gottlob I, Benskin S, Proudlock FA (2008) The effect of aging on torsional optokinetic nystagmus. Invest Ophthalmol Vis Sci 49: 589-93. doi: 10.1167/iovs.07-0899

Fukata K, Amimoto K, Fujino Y, Inoue M, Inoue M, Takahashi Y, Makita S, Takahashi H (2017) The effects of aging on the subjective vertical in the frontal plane in healthy adults. J Phys Ther Sci 29: 1950-1953. doi: 10.1589/jpts.29.1950

Guerra Jimenez G, Perez Fernandez N (2016) Reduction in posterior semicircular canal gain by age in video head impulse testing. Observational study. Acta Otorrinolaringol Esp 67: 15-22. doi: 10.1016/j.otorri.2014.12.002

Hajioff D, Barr-Hamilton RM, Colledge NR, Lewis SJ, Wilson JA (2000) Re-evaluation of normative electronystagmography data in healthy ageing. Clin Otolaryngol Allied Sci 25: 249-52. doi: coa361 [pii]

Irving EL, Lillakas L (2019) Difference between vertical and horizontal saccades across the human lifespan. Exp Eye Res 183: 38-45. doi: 10.1016/j.exer.2018.08.020

Janky KL, Shepard N (2009) Vestibular evoked myogenic potential (VEMP) testing: normative threshold response curves and effects of age. J Am Acad Audiol 20: 514-22. doi: 10.3766/jaaa.20.8.6

Kato I, Sakuma A, Ogino S, Takahashi K, Okada T (1995) Aging effects upon pursuit eye movements. Acta Otolaryngol Suppl 520 Pt 2: 293-4. doi: 10.3109/00016489509125252

Kim TH, Kim MB (2018) Effect of aging and direction of impulse in video head impulse test. Laryngoscope 128: E228-E233. doi: 10.1002/lary.26864

Lopez I, Honrubia V, Baloh RW (1997) Aging and the human vestibular nucleus. J Vestib Res 7: 77-85.

Lynch SJ, Nayak US, Isaacs B (1985) Positional and optokinetic nystagmus in healthy old people. Age Ageing 14: 122-4. doi: 10.1093/ageing/14.2.122

Maes L, Dhooge I, D’Haenens W, Bockstael A, Keppler H, Philips B, Swinnen F, Vinck BM (2010) The effect of age on the sinusoidal harmonic acceleration test, pseudorandom rotation test, velocity step test, caloric test, and vestibular-evoked myogenic potential test. Ear Hear 31: 84-94. doi: 10.1097/AUD.0b013e3181b9640e

Matheson AJ, Darlington CL, Smith PF (1999) Dizziness in the elderly and age-related degeneration of the vestibular system. NZ J Psychol 28: 10-6.

Matino-Soler E, Esteller-More E, Martin-Sanchez JC, Martinez-Sanchez JM, Perez-Fernandez N (2015) Normative data on angular vestibulo-ocular responses in the yaw axis measured using the video head impulse test. Otol Neurotol 36: 466-71. doi: 10.1097/MAO.0000000000000661

Merchant SN, Velazquez-Villasenor L, Tsuji K, Glynn RJ, Wall C, 3rd, Rauch SD (2000) Temporal bone studies of the human peripheral vestibular system. Normative vestibular hair cell data. Ann Otol Rhinol Laryngol Suppl 181: 3-13. doi: 10.1177/00034894001090s502

Mossman B, Mossman S, Purdie G, Schneider E (2015) Age dependent normal horizontal VOR gain of head impulse test as measured with video-oculography. J Otolaryngol Head Neck Surg 44: 29. doi: 10.1186/s40463-015-0081-7

Ochi K, Ohashi T (2003) Age-related changes in the vestibular-evoked myogenic potentials. Otolaryngol Head Neck Surg 129: 655-659. doi: 10.1016/s0194-5998(03)01578-x

Paige GD (1992) Senescence of human visual-vestibular interactions. 1. Vestibulo-ocular reflex and adaptive plasticity with aging. J Vestib Res 2: 133-51.

Peterka RJ, Black FO (1990a) Age-related changes in human posture control: motor coordination tests. J Vestib Res 1: 87-96.

Peterka RJ, Black FO (1990b) Age-related changes in human posture control: sensory organization tests. J Vestib Res 1: 73-85.

Peterka RJ, Black FO, Schoenhoff MB (1990a) Age-related changes in human vestibulo-ocular and optokinetic reflexes: pseudorandom rotation tests. J Vestib Res 1: 61-71.

Peterka RJ, Black FO, Schoenhoff MB (1990b) Age-related changes in human vestibulo-ocular reflexes: sinusoidal rotation and caloric tests. J Vestib Res 1: 49-59.

Rasmussen AT (1940) Studies of the VIIIth cranial nerve of man. Laryngoscope 50: 67-83.

Rauch SD, Velazquez-Villasenor L, Dimitri PS, Merchant SN (2001) Decreasing hair cell counts in aging humans. Ann N Y Acad Sci 942: 220-7.

Richter E (1980) Quantitative study of human Scarpa’s ganglion and vestibular sensory epithelia. Acta Otolaryngol 90: 199-208. doi: 10.3109/00016488009131716

Robbins S, Waked E, McClaran J (1995) Proprioception and stability: foot position awareness as a function of age and footwear. Age Ageing 24: 67-72. doi: 10.1093/ageing/24.1.67

Rosenhall U, Rubin W (1975) Degenerative changes in the human vestibular sensory epithelia. Acta Otolaryngol 79: 67-80.

Sakuma A, Ogino S, Takahashi K, Kato I (2000) Aging effects upon smooth pursuit induced by step-ramp stimulation. Auris Nasus Larynx 27: 195-200. doi: 10.1016/s0385-8146(00)00051-1

Sharpe JA, Sylvester TO (1978) Effect of aging on horizontal smooth pursuit. Invest Ophthalmol Vis Sci 17: 465-8.

Singh NK, Firdose H (2021) Characterizing the impact of advancing age on 500 Hz tone-burst evoked ocular-vestibular evoked myogenic potentials. Eur Arch Otorhinolaryngol. doi: 10.1007/s00405-020-06542-2

Skinner HB, Barrack RL, Cook SD (1984) Age-related decline in proprioception. Clin Orthop Relat Res: 208-11.

Spooner JW, Sakala SM, Baloh RW (1980) Effect of aging on eye tracking. Arch Neurol 37: 575-6. doi: 10.1001/archneur.1980.00500580071012

Su HC, Huang TW, Young YH, Cheng PW (2004) Aging effect on vestibular evoked myogenic potential. Otol Neurotol 25: 977-980. doi: 10.1097/00129492-200411000-00019

Toupet M, Van Nechel C, Grayeli AB (2015) Subjective Visual Vertical Tilt Attraction to the Side of Rod Presentation: Effects of Age, Sex, and Vestibular Disorders. Otol Neurotol 36: 1074-80. doi: 10.1097/MAO.0000000000000771

Tuunainen E, Poe D, Jantti P, Varpa K, Rasku J, Toppila E, Pyykko I (2011) Presbyequilibrium in the oldest old, a combination of vestibular, oculomotor and postural deficits. Aging Clin Exp Res 23: 364-71. doi: 10.1007/BF03337761

Walther LE, Westhofen M (2007) Presbyvertigo-aging of otoconia and vestibular sensory cells. J Vestib Res 17: 89-92.

Warabi T, Kase M, Kato T (1984) Effect of aging on the accuracy of visually guided saccadic eye movement. Ann Neurol 16: 449-54. doi: 10.1002/ana.410160405

Welgampola MS, Colebatch JG (2001) Vestibulocollic reflexes: normal values and the effect of age. Clin Neurophysiol 112: 1971-9.

Zackon DH, Sharpe JA (1987) Smooth pursuit in senescence. Effects of target acceleration and velocity. Acta Otolaryngol 104: 290-7. doi: 10.3109/00016488709107331

Zakaria MN, Salim R, Tahir A, Zainun Z, Mohd Sakeri NS (2019) The influences of age, gender and geometric pattern of visual image on the verticality perception: A subjective visual vertical (SVV) study among Malaysian adults. Clin Otolaryngol 44: 166-171. doi: 10.1111/coa.13255

Zalewski CK (2015) Aging of the Human Vestibular System. Semin Hear 36: 175-96. doi: 10.1055/s-0035-1555120