DÄ internationalArchive29-30/2021Sensory Dysfunction in Old Age

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Sensory Dysfunction in Old Age

Dtsch Arztebl Int 2021; 118: 512-20. DOI: 10.3238/arztebl.m2021.0212

Völter, C; Thomas, J P; Maetzler, W; Guthoff, R; Grunwald, M; Hummel, T

Background: The senses serve as the crucial interface between the individual and the environment. They are subject to aging and disease processes.

Methods: This review is based on pertinent publications retrieved by a selective search in the Medline and Cochrane Library databases.

Results: Approximately 40% of persons aged 70 to 79 manifest dysfunction in at least one, and more than 25% in multiple senses. Sensory changes are accompanied by diverse comorbidities which depend on the particular sense(s) affected. The presence of sensory deficits is associated with an increased risk of developing dementia (OR: 1.49 [95% confidence interval: 1.12; 1.98] for dysfunction in a single sensory modality, 2.85 [1.88; 4.30] for dysfunction in three or more sensory modalities). The risk of developing depressive symptoms is elevated as well (OR 3.36 [2.28; 4.96]). The individual’s ability to cope with the demands of everyday life is largely determined by the ability to carry out multisensory integration, in which the perceptions of the different senses are bound together. This function itself is subject to age-related changes that can be either adaptive or maladaptive; it can, therefore, serve as an indicator for pathological aging processes.

Conclusion: Sensory dysfunction in old age should be detected as early as possible. This implies the need for close collaboration of all of the involved disciplines. It would be desirable to develop sensory screening tests as well as a procedure for testing multisensory integration in routine clinical practice.

LNSLNS

Sensory perception, whether normal or impaired, has an enormous impact on our lives. The elderly often suffer a marked decline in one or more sensory systems. Most studies on this subject to date have focused on only one sensory system per study (e1). It has been determined, however, that 39.2% of persons aged 70 to 79 have an objectively demonstrable functional impairment in a single sensory modality, 20.1% in two, and approximately 6% in three or four modalities (e2).

Learning objectives

This article is intended to enable the reader to:

  • know the basic changes to which each sensory modality is subject in old age,
  • gain an overview of current scientific evidence on the effects of sensory impairment in old age, and
  • understand how central integration of the different sensory modalities is affected by normal and pathological aging processes.

Hearing impairment

Even in otologically healthy persons, the auditory threshold rises by an average of 1 dB per year from age 60 onward (Figure 1) (e3). Hearing impairment as defined by the WHO criteria is present in 20.3% of persons in their seventh decade, 42.2% of persons in their eighth, and 71.5% of persons aged 80 and above (e4). Elderly persons often do not notice their hearing impairment until long after its onset, or else accept it as a supposedly inevitable part of aging (e5, e6). As a result, even though good treatment options are available (e7, e8), hearing aids are worn by only 5.8% of hearing-impaired persons in Germany who are in their seventh decade, and by 32.6% of hearing-impaired 80-year-olds (e4). There are similar estimates from the USA and Sweden with respect to the provision of cochlear implants (e9, e10).

Median values of expected changes of the auditory threshold
Figure 1
Median values of expected changes of the auditory threshold

Hearing loss is associated with a variety of diseases. Above all, the relation between hearing loss and cognitive impairment has been the object of numerous studies. As early as 2011, a longitudinal study revealed that the risk of dementia appearing within 11.9 years is elevated by a factor of 1.89 (95% confidence interval: [1.00; 3.58]) in persons with mild hearing impairment, threefold [1.43; 6.30] in persons with moderate hearing impairment, and by a factor of 4.94 [1.09; 22.40] in persons with severe hearing impairment (e11). This was confirmed in a recent meta-analysis of 36 studies. A mild, but statistically significant correlation was found between age-associated hearing impairment and dysfunction in multiple cognitive domains (global cognition: r = −0.15 [−0.18; −0.11]). The odds ratio (OR) for incident dementia among persons with hearing loss is 2.42 [1.24; 4.72] in cross-sectional studies and 1.28 [1.02; 1.59] in longitudinal studies (1). Similarly, a longitudinal study based on data from over 150,000 insurees of the AOK health insurance carrier in Germany aged 65 and above revealed an elevated risk of dementia in persons with bilateral hearing impairment (hazard ratio [HR] = 1.43, p < 0.01) (e12).

It is still unclear how hearing impairment and cognitive changes influence each other (e13, e14). Various hypotheses are under discussion, but none of them have yet been definitively confirmed by scientific evidence:

  • an underlying pathological change affecting both the ascending auditory pathway and the multimodal cortex
  • a decline of cognitive resources because of primary, longstanding impoverishment of auditory stimulation
  • overloading of cognitive reserves by the increased effort required for useful hearing under difficult acoustic circumstances
  • damage to the medial portion of the temporal lobe, which is affected in early-stage Alzheimer’s disease and is also responsible for so-called auditory cognition, resulting in simultaneous impairment of cognitive function as well as hearing and/or auditory processing (2, 3).

No data on the temporal course of the appearance of these sensory and cognitive changes are yet available that would support inferences about causation (e15). The mechanisms underlying these changes are the crucial determinants of whether auditory rehabilitation in middle age, in the form of a hearing aid or cochlear implant, might be able to prevent cognitive decline and dementia in old age, as postulated by Livingstone (4). While a few non-randomized studies have revealed improvement in various cognitive domains 6 and 12 months after cochlear implantation, the evidence remains insufficient (5, e16, e17). Prospective, clinically controlled longitudinal trials are hard to conduct for both ethical and practical reasons, not least because middle-aged persons are often reluctant to accept hearing aids (e18). Initial multicenter trials have begun; their results are pending (6).

In persons already suffering from Alzheimer dementia (AD), wearing a hearing aid for 6 months seems not to cause any significant change in cognitive function, according to the findings of an initial randomized and placebo-controlled trial carried out on 38 patients with AD aged 68 and above (e19). An intervention of this type might, however, lower the probability of a transition from mild cognitive impairment (MCI) to dementia, as suggested by a recent retrospective data analysis based on subjective assessments of hearing status (HR 0.73 [0.61; 0.89]) (e20).

Moreover, hearing impairment is associated with a higher frequency of mental symptoms and illnesses (e21). For instance, women aged 60 to 69 with an untreated hearing impairment suffer more frequently from social isolation: the odds ratio (OR) rises by 3.49 [1.91; 6.39] per 25 dB worsening of hearing, averaged over the range 500–4000 Hz (e22). Hearing impairment is also associated with depression: the relative risk of depression is 1.41 [1.26; 1.58] five years after the onset of a hearing impairment, and 6.88 [4.62; 9.14] at 10 years (e23). According to a meta-analysis of 35 studies, a significant association of hearing impairment with depression has been revealed both by cross-sectional studies (OR: 1.54 [1.31; 1.80]) and by longitudinal studies (OR: 1.39 [1.16; 1.67]) (7). It remains unknown whether this is due to behavioral changes alone or to structural changes in the limbic system as well (8).

Elderly persons with at least 25 dB of hearing loss also have a 1.4-fold [1,3; 1,5] elevation of the risk of falling (e24). This association was recently confirmed in a meta-analysis of four studies, after adjustment for other risk factors (OR: 1.72 [1.07; 2.37]) (9).

Impairment of balance

The elderly often suffer from impaired balance because of multifactorial deficits in vestibular, proprioceptive, visual, and somatosensory function (e25). Many age-dependent degenerative changes have been demonstrated in the vestibular system at the cellular and neuronal level, but these often cannot be correlated with clinical manifestations, because the physiology of the central vestibular system is complex (10). The clinical relevance of physiological aging processes in this sensory system is, therefore, difficult to determine.

When interpreting data on the prevalence of age-associated impairment of balance, one must bear in mind that the common lay term “dizziness” can refer both to apparent relative motion of the subject and the environment (i.e., true vertigo) and, more broadly, to an unsystematic feeling of unsteadiness. Data on the prevalence of balance disturbances are mainly derived from questionnaires and may not differentiate between these two senses of the word. A study by Gassmann revealed an increasing prevalence of impaired balance with increasing age (27% in persons aged 65 to 70, 54% in persons aged 90 and above) (11). Women have a higher prevalence of impaired balance than men (at age 70, 36% vs. 29%; at age 90, 51% vs. 45%).

The frequency distribution of diagnosed causes of impaired balance is highly dependent on the particular medical specialty performing the diagnostic assessment (e26). An interdisciplinary approach and thorough history-taking are thus very important. The patient should be asked about the nature and duration of the difficulty with balance, precipitating factors, accompanying symptoms and concomitant illnesses, and medication use, as well as about any falls that may have occurred and any further risk factors for falling that may be present.

In the elderly, dizziness as a symptom is a major risk factor for falling (e27). A recent meta-analysis determined that, in the presence of dizziness, the relative risk of falling is 1.32 [1.10; 1.59] (13). Moreover, dizziness is also associated with elevated mortality after risk adjustment (adjusted OR: 1.7 [1.36; 2.18]) (e28).

With regard to peripheral vestibular disturbances, bilateral vestibulopathy should be considered as a possible cause in any patient with chronically impaired balance. The typical clinical manifestation is movement-dependent unsteadiness that worsens in darkness and when the patient walks on an uneven surface. A cause can be identified in only 49% of cases (e.g., vestibulotoxic drugs, bilateral Ménière’s disease) (e29). The term “presbyvestibulopathy” refers to bilateral mild reduction of vestibular function, as determined by objective measurement. Further diagnostic criteria for it include age 60 or above, unsteadiness, gait impairment, chronic dizziness, and recurrent falls that are not explained by another disorder (14). The recommended treatment is daily balance training, particularly with rotation of the head in all three axes, in order to train the vestibulo-ocular reflex (level I evidence) (e30), supplemented by fall prevention under physiotherapeutic guidance (15). A combination of balance, strength, and gait training can lower the risk of falling by 23 % (level I evidence) (e31).

Visual impairment

Visual disturbances become more common in old age. The prevalence of visual impairment and blindness in Germany is 0.4% overall (431.5 per 100 000 persons), 0.7% (735.4/100 000) in persons aged 65 to 74, and 2.4% (2391.4/100 000) in persons aged 75 and above (16). The most common causes of blindness in Germany are associated with aging, namely, age-associated macular degeneration (AMD) and glaucoma (e32).

In contrast to diseases such as AMD, the normal, continuous aging processes of the various tissue systems of the eye have only mild symptoms at first. Contrast perception declines slowly, as does the ability to adapt to different lighting conditions. Physiological changes of the lens play a major role at first; the declining accommodation ability of the lens from age 45 onward (presbyopia) is due to structural changes of the lens itself, its zonular fibers (suspensory apparatus), the ciliary muscle tendons, and the ciliary muscle (e33). Presbyopia can be corrected with spectacles, multifocal contact lenses, or microsurgically implanted intraocular lenses of various types (17). There are nonetheless more than 800 million persons around the world with inadequate access (or none at all) to presbyopia correction. This constitutes a major socioeconomic problem, particularly in rural areas (18).

Progressive destabilization of lens proteins in old age leads to turbidity of the lens and ultimately to a pathological cataract (19). Depending on the morphology of the turbidity/opacification, the symptoms may consist of lessened contrast sensitivity, increased sensitivity to glare, and/or impaired visual acuity (20). Cataract is the main preventable cause of blindness around the world (e34).

There are various reasons for the lessened central visual acuity and impaired vision in dim light that accompany normal aging. The pupils become narrower, allowing less light to reach the retina (19). The retinal ganglion-cell layer in the macular region becomes approximately 3% thinner with each additional decade of life (Figure 2) (20). The number of rod cells, which are responsible for vision in dim light, also diminishes between the ages of 60 and 70 (21). Adaptation to darkness becomes harder as the amount of the photopigment rhodopsin in the photoreceptors lessens and phototransduction processes for rod-cell regeneration become slower. Thus, the normal switching from cone to rod vision in dim light is slowed. Lastly, transport processes for vitamin A, a necessary component of the visual cycle, are impaired by changes in the retinal pigment epithelium (RPE), by the accumulation of extracellular materials between Bruch’s membrane and the RPE (drusen), and by thickening of Bruch’s membrane itself. This can be a transitional stage to the development of diseases of old age, such as age-associated macular degeneration (AMD) (e35).

Normal age-related changes in the thickness
Figure 2
Normal age-related changes in the thickness

In general, elderly persons with impaired vision suffer more often from cognitive impairment (relative risk [RR]: 1.47 [1.36; 1.60]) and dementia (RR 1.35 [1.28; 1.41]) (22). Visual acuity often improves markedly after cataract surgery in elderly persons with cognitive impairment, who often have very advanced lenticular opacification. The visual improvement may also have a beneficial effect on cognition.

Impairment of smell

Anosmia, i.e., the total lack of olfactory perception, affects 3.6% of the general population (23, e36). It has wide-ranging consequences for the perception of dangers in everyday life (smoke, poisonous substances). 45% of persons with anosmia, but only 19% of persons with a normal sense of smell, report having had accidents of types that may have to do with olfactory perception (e37). Moreover, the inability to smell the aroma of food may impair the enjoyment of eating and the rewarding character of the eating experience (e38). A depressive mood disturbance is found in approximately one-third of patients with impaired olfaction (24, e39), and most suffer from a lowered quality of life.

The sense of smell declines with age and is practically absent in at least one-third of persons aged 80 and above (25, e40). The loss of smell apparently reflects the summed effect of changes at various levels of olfactory perception (26). The olfactory epithelium can regenerate itself, but this ability declines over a lifetime (e41, e42). The olfactory bulb also possesses plasticity (e43, e44), which can be seen in imaging studies as a change of volume (Figure 3) (e45). The mean volume of the olfactory bulb is 71.6 mm3 in persons under age 40 and 59.6 mm3 in persons over age 60 (27). The activation of the brain by odors declines as well, mainly in the secondary olfactory cortex (e46).

Age-dependence of olfaction
Figure 3
Age-dependence of olfaction

Various methods are available for the assessment of olfactory function. Self-assessment of the general ability to smell is erroneous in approximately one-third of cases (e47). For clinical olfactory testing, Sniffin’ Sticks can be used as a screening test (e48) or for more detailed testing (e49). If the ability to tell odors apart and the perceptory threshold for odors are affected to varying extents, the cause probably lies in a disturbance at either the central nervous or the peripheral nasal level (e50, e51); a variety of treatments are available (23, e52). In persons with age-associated impairment of smell, the plasticity of the olfactory system can be stimulated by regular smell training. In one study carried out on 91 healthy subjects, improvement was seen in 20% of the smell-training group and in 10% of the control group (e53).

At any age, olfactory disturbances of unclear cause may be an early symptom of a neurodegenerative diseases such as idiopathic Parkinson syndrome (IPS). Although unexplained olfactory loss has a positive predictive value of only 0.09, olfactory testing may be helpful in the differential diagnosis of IPS (28). Moreover, up to 94% of patients with manifest IPS have impaired olfaction (e54), which suggests that reconsideration of the diagnosis of IPS may be advisable in patients with a normal sense of smell.

Impairment of taste

Impaired gustatory perception (sweet, sour, salty, bitter, umami) affects approximately 5% of the population (e55). It may be idiopathic, or else due to a reduced number of papillae in the mouth, altered production and composition of the saliva, or impaired central nervous processing (e56, e57). Moreover, a declining sense of smell leads indirectly to lessened reinforcement of gustatory function (e58). Hardly any treatment is available for impaired taste (e59).

Somatosensory impairment

The somatosensory system, with its component modalities (exteroception, proprioception, interoception), is responsible from intrauterine development onward for both active (haptic) and passive (tactile) somatic sensation. Somatosensory performance varies greatly between individuals and changes over the course of any single individual’s lifetime as well (29, 30, 31) (e60).

From age 20 onward, the quality of perception of tactile stimuli at the fingertips declines by approximately 1% per year. This is due not only to an age-dependent loss of Meissner and Merkel receptors, but also to a loss of neurons (e61). The perception of passively applied, high-frequency (>100 Hz) vibratory stimuli worsens with age, while that of lower-frequency vibratory stimuli (< 40 Hz) remains unimpaired even in old age. The decline of perception of high-frequency vibratory stimuli is thought to be due to structural changes in the Pacinian corpuscles (32, e62, e63).

The active, haptic capacity to recognize objects regularly declines in old age, but later than passive, tactile somatosensory perception. The decline of active, haptic ability is more closely correlated with cognitive changes than with the declining number of somatosensory receptors in old age (Figure 4) (e64, e65). The age-related decline of proprioceptive ability is often associated with impaired balance; the degree of resulting functional impairment depends on the individual’s prior motor experience and level of physical activity (e66, e67). Nonetheless, as all somatosensory dimensions are trainable even in old age, proprioceptive training can help lower the frequency of falls in elderly patients (e68, e69).

Drawings made after haptic object recognition of real bas-reliefs
Figure 4
Drawings made after haptic object recognition of real bas-reliefs

There are also changes in some aspects of intero-ception from age 50 onward. Painful visceral stimuli are processed less adequately; nonetheless, the elderly complain of pain more commonly than younger persons. This is thought to be the result of summation effects due to pain located at multiple bodily sites simultaneously in old age, as well as to a decline of inhibitory mechanisms and a stronger emotional-motivational component (e70).

Despite the decline of somatosensory function, the elderly have an unchanged need for bodily social interaction. Studies have shown a positive effect of social physical contact on perceived loneliness (e71, e72), depression, and anxiety, as well as improved food intake and diminution of aggressive and agitated behaviors in persons with dementia (33, e73, e74).

Interactions between the sensory systems

The consequences of sensory impairment are more severe if multiple sensory systems are affected. The degree of sensory impairment, as measured with the Global Sensory Impairment Index, is significantly correlated with activities of daily living (OR 1.26 [1.10; 1.46]), physical mobility (OR 1.32 [1.17; 1.50]), and 5-year mortality (OR 1.45 [1.19; 1.76]) (e1). Moreover, the OR for the appearance of dementia is 1.49 [1.12; 1.98] with functional impairment in a single sensory modality, 1.91 [1.39; 2.63] with impairment in two, and 2.85 [1.88; 4.30] with impairment in three or more modalities (e2). The simultaneous dysfunction of multiple sensory systems is associated with poorer physical performance ability (e75), and the risk of developing depression is elevated by a factor of 3.36 [2.28; 4.96] if three or more sensory systems are impaired (34).

These effects can be well explained as being due to altered multisensory integration (MSI). As part of everyday life, the brain has the task of generating a single, holistic perception out of the voluminous data that are conveyed to it uninterruptedly by the various sensory systems, in all of their differing and more or less correlated temporal, spatial, textual, and semantic aspects. These data must be matched to each other in such a way as to give the individual a maximally realistic picture of the environment, so that his or her ensuing behavior will be situationally appropriate, with the lowest possible chance of bringing harm. It is presumed that, in order to carry out this enormously complex integrative task, the brain performs the equivalent of computing Bayesian probabilities (35, e76). Bayes’s Theorem enables the continuous computation of a posteriori probabilities of hypotheses, as in the following example from the visual domain: the hypothesis “The two headlights that I see coming my way in the dark as I drive down this wet road belong to a car that is coming toward me” has an a priori probability (derived from pre-existing knowledge about approaching headlights in comparable situations) that can be corrected for current circumstances (e.g., a dirty windshield).

MSI can improve the perceptions of our senses adaptively, or else it can have maladaptive effects, causing perceptual illusions. The precise mechanisms are imperfectly known to date (36, 37, e76). Imaging studies and neurophysiological studies provide evidence that the capacity for MSI not only remains intact over an individual’s lifetime but actually improves, mainly in the processing of congruent stimuli (37, e77, e78). Thus, MSI may be able to compensate for age-associated impairment of particular peripheral sensory functions (e79). On the other hand, some aspects of MSI seem to worsen with age, with adverse consequences for everyday life. For instance, impaired visuo-somatosensory integration has been found to be associated with poorer balance (p < 0.05) and an elevated risk of falling (HR : 0.24, p = 0.01) (38). The extent of impairment of MSI may also be an early indicator of pathological aging processes (e80, 36).

It is only in the last few years that multisensory integration has attracted increased scientific attention (e81). In view of the functional importance of MSI, the changes and adaptations in this capability over an individual’s lifetime, and, especially, its susceptibility to impairment by age-associated neurological diseases, it appears important that testing procedures for MSI should be developed for use in the routine clinical evaluation of elderly patients in particular (36, e80). The essential prerequisite is an intensive collaboration of geriatrics with the other relevant specialties in both the clinical and the scientific domain.

Overview

Impairments in single sensory systems have far-reaching consequences for the individual. These are even more marked when multiple sensory systems are affected. The multisensory integration of sensory perceptions plays a crucial role in enabling elderly persons to continue going about their everyday activities. In the future, early detection of sensory impairments in the elderly would be a desirable component of preventive medical check-ups, as it might help lessen severe long-term consequences. Moreover, multimodal therapeutic approaches might help slow aging processes by stimulating the plasticity of the brain (e81, e82).

Conflict of interest statement
Prof. Völter has received reimbursement of scientific meeting participation fees and accommodation expenses, as well as honoraria for preparing continuing medical education events and funding for a research project that she initiated, from MED-EL.

PD Thomas has received reimbursement of scientific meeting participation fees and travel expenses from MED-EL. From the same company, he has received honoraria for preparing continuing medical education events, as well as payment for carrying out clinical trials.

Rainer Guthoff has received lecture honoraria from Hoffmann La Roche AG and reimbursement of scientific meeting participation fees and travel expenses from Bayer AG and DORC GmbH. He has received payment for carrying out clinical trials from Bayer AG, Novartis Pharma, Hoffmann La Roche AG, and Samsung.

Prof. Hummel has received funding for a research project that he initiated from Smell and Taste, Geneva, and from Sony and Takasago.

The remaining authors state that they have no conflict of interest.

Manuscript received on 14 April 2020; revised version accepted on 14 April 2021.

Translated from the original German by Ethan Taub, M.D:

Correspondence address
Prof. Dr. med. Christiane Völter
Klinik für HNO-Heilkunde, Kopf- und Halschirurgie
Ruhr-Universität Bochum
Katholisches Klinikum Bochum, St. Elisabeth Hospital
Bleichstr. 15, D-44787 Bochum, Germany
christiane.voelter@rub.de

Cite this as:
Völter C, Thomas JP, Maetzler W, Guthoff R, Grunwald M, Hummel T: Sensory dysfunction in old age. Dtsch Arztebl Int 2021; 118: 512–20. DOI: 10.3238/arztebl.m2021.0212

Supplementary material

eReferences
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* Joint first authors
Hearing Competence Center, St. Elisabeth- Hospital, Department of Otorhinolaryngology, Head and Neck Surgery, Ruhr University of Bochum: Prof. Dr. med. Christiane Völter
Department of Otorhinolaryngology, Head and Neck Surgery, St.-Johannes-Hospital, Dortmund: PD Dr. med. Jan Peter Thomas
Department of Neurology, Faculty of Medicine, University of Kiel: Prof. Dr. med. Walter Maetzler
Department of Ophthalmology, Düsseldorf University Hospital: Prof. Dr. med. Rainer Guthoff
Haptic Research Lab, Paul Flechsig Institute of Brain Research, Medical Faculty of the Universität Leipzig: Prof. Dr. phil. habil. Dipl.-Psych. Martin Grunwald
Otorhinolaryngology, Head and Neck Surgery, Universitätsklinikum Carl Gustav Carus, Dresden: Prof. Dr. med. Thomas Hummel
Median values of expected changes of the auditory threshold
Figure 1
Median values of expected changes of the auditory threshold
Normal age-related changes in the thickness
Figure 2
Normal age-related changes in the thickness
Age-dependence of olfaction
Figure 3
Age-dependence of olfaction
Drawings made after haptic object recognition of real bas-reliefs
Figure 4
Drawings made after haptic object recognition of real bas-reliefs
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