Hearing loss and cortical atrophy in a population-based study on non-demented women
SIR—Age-related hearing loss (ARHL) is common and may cause difficulties in perception and understanding speech. ARHL is influenced by ageing, genetic factors, noise and other environmental factors [1]. Age-related brain atrophy is related to reductions in the number of neurons, and decreased cortical synaptic density. Brain atrophy may potentially damage hearing capacity through the impairment of primary and secondary auditory centres which are located in the temporal lobe. To our knowledge, no study has examined the relationship between brain atrophy and ARHL.In a population-based sample of non-demented women, we examined whether there is an association between ARHL and brain atrophy, and whether this relationship is influenced by cognitive function.
Population
This study is part of the representative Gerontological and Geriatric Population Study in Gothenburg [2], and the Prospective Population Study of Women [3]. In 1992–93, 70-year-old women were examined (n = 299). Pure tone audiometry was performed in 163 randomly selected participants [4], of whom 80 had a brain computerised tomography (CT) scan. In 2000–01, 70-year-old women were examined (n = 523). Pure tone audiometry was performed in 42 randomly selected women, of whom 31 had a brain CT scan. Since there were no differences of hearing capacity and brain atrophy between these two groups, they were pooled. One hundred and eleven in the study population were comprised of 70-year-old women. None were demented according to criteria of the Diagnostic and Statistical Manual of Mental Disorders, Revised Third Edition [5].
Five right ears with pronounced hearing impairment of peripheral origin, not related to ageing, were excluded from the study. Three had conductive hearing loss (two chronic otitis media, and one otosclerosis), and two had severe, unilateral sensorineural hearing loss (one Ménière's disease, one sudden deafness). In all these cases, the otological condition was unilateral, and the contralateral, non-affected ear was included in the study. One woman lacked hearing in the right ear, leaving 111 left ears and 105 right ears for analyses. The study was approved by the Ethics Committee of Göteborg University. All subjects gave informed consent to participate, in accordance with the provisions of the Helsinki Declaration.
Audiometry
Pure tone audiometry was performed in a quiet office room by trained clinical audiologists. Madsen OB 70 audiometers, calibrated according to internationally accepted ISO standards, were used. Before testing, an otoscopic examination of the external meatus was done and occluding cerumen was removed. The pure tone test included measurements of air conduction thresholds at octave and half-octave intervals between 0.25 and 8 kHz using the ascending method [6].
Computerised tomography (CT) of brain
CT scans (without contrast enhancement) were rated by radiologists and neurologists blinded to the subjects' clinical characteristics [7, 8]. Cortical atrophy of occipital, parietal, frontal and temporal lobes was categorised using a three-point scale according to the extent of sulcal widening (normal, moderate and severe) [8, 9]. Lateral ventricle size was measured in three linear distances: (i) the bifrontal span, (ii) the width of the head of the caudate nucleus, and (iii) the minimum width of the bodies at the waist. Ratios for (i), (ii), and (iii) were determined by dividing the obtained values by the internal diameter of the skull at the level of the measurement, giving the following ratios: bifrontal ratio, bicaudate ratio, and cella media ratio.
Mini mental state examination (MMSE)
Cognitive function was assessed by Mini mental state examination (MMSE) [10] which assesses global cognitive function including orientation, registration, attention, calculation, visual-spatial, recall and language. It scores from 0 to 30, lower scores implying worse cognitive function.
Statistical analysis
As few women had severe cortical atrophy, cortical atrophy was analysed as a dichotomous variable (present/absent). A paired sample t-test was used to examine differences of hearing capacity between left and right ear. An independent sample t-test was used to study the differences of hearing capacity between women with and without cortical atrophy. The association between hearing capacity and lateral ventricle index was tested by Spearman's rank correlation coefficient (bicaudate ratio and cella media ratio) or Pearson's correlation coefficient (bifrontal ratio). As cognitive impairment may influence performance on hearing tests, the relationship between hearing capacity and cortical atrophy was further studied by stratifying the sample by MMSE score (
28 and >28). Two-tailed tests of significance were used.
Among the 111 70-year-old women, 72 had cortical atrophy (34 one lobe, 17 two lobes, 13 three lobes, 8 four lobes). The pure tone thresholds were poorer in the left ear than in the right ear at frequencies 6 and 8 kHz with a difference of 2.2 dB (P = 0.05) and 2.7 dB (P = 0.03), respectively.
Women with cortical atrophy at any lobe had poorer hearing capacity of the left ear at the frequencies 6 kHz (mean value: 42.3 versus 50.1 dBHL) and 8 kHz (mean value: 49.0 versus 60.2 dBHL) than women without cortical atrophy. Women with atrophy of three or four lobes had poorer hearing of the left ear than those with atrophy of one or two lobes, and women without atrophy at frequencies 2, 4, 6 and 8 kHz (Figure 1). The findings for the right ear were in the same direction, but non-significant. Women with isolated temporal lobe atrophy (n = 17) had similar hearing capacity as women with isolated atrophy of the other three lobes (n = 17). Hearing capacity was not related to lateral ventricle index, (i.e. bicaudate ratio, bifrontal ratio and cella media ratio).
|
The mean MMSE score for the total group was 28.3 ± 1.4 (range 21–30). The relationship between cortical atrophy and hearing capacity was stronger in women with better cognitive function (MMSE 29–30, n = 56) than in other women (MMSE
28, n = 55) (Table 1). In those with better cognitive function, cortical atrophy at any cerebral lobe was related to poorer hearing of the left ear at frequencies of 1, 2, 4, 6 and 8 kHz. In those with poorer cognitive function, cortical atrophy was related to hearing capacity of the left ear at the frequency 8 kHz.
|
Discussion
We found a relationship between general cortical atrophy and poorer hearing in the high-frequency range of the left ear in a population-based sample of 70-year-old women. The relation between pure tone thresholds and brain atrophy was correlated to the extension of cortical atrophy, but not to specific location (temporal lobe). Most correlations were found in women with high cognitive function.
There are possible explanations for our findings. First, the relationship may represent expressions of common, age-related degenerative processes, as poor hearing was related to general cerebral atrophy, not to individual lobes. Second, although pure tone audiometry is supposed to reflect peripheral hearing, and not believed to be influenced by central auditory processing, we cannot exclude the possibility that a small part of the observed differences of pure tone thresholds in our study may reflect influences of central auditory processing, as primary and secondary auditory centres are located in the temporal lobe. Finally, the cross-sectional design of our study cannot elucidate the direction of the associations. It is thus possible that hearing loss may accelerate cerebral atrophy through impaired social contact and auditory stimulation.
The associations were more pronounced for the left ear than for the right. One explanation could be that brain atrophy might be more severe in the right hemisphere than in the left, but we could not test this hypothesis, as we had no measurement of atrophied side. Another explanation is ear asymmetry with slightly poorer high-frequency thresholds of the left ear [11]. It has been suggested that the right cochlea is more sensitive to noise than the left [12]. Hearing loss was associated with cortical, but not central, atrophy, which seems logical as the cochlear sensory cells are more equivalent to grey than to white matter.
Cognitive function may alter capacity to perform hearing tests. Cognitive decline has been related to problems to perceive stimuli to the left ear during dichotic listening [13], and central auditory speech-processing deficits has been suggested to precede onset of Alzheimer's disease by many years [14]. However, the observed association between hearing loss and cortical atrophy was most pronounced in those with high cognitive function.
Among the strengths of the study are the population-based sample, and comprehensive examinations. Limitations include, first, the sample size which is relatively small. The findings therefore need to be confirmed in larger studies. Second, although inter-rater reliability was good, subjective rating of cortical atrophy on CT scan is a crude method, which likely underestimated the associations. Third, the cross-sectional design precludes conclusions about the directions of the associations. Fourth, there are differences between men and women regarding hearing loss and brain atrophy [6,15,16]. We only examined women, and thus, cannot generalise our findings to men. Finally, multiple comparisons were made, which may lead to false positive findings. The finding that all significant associations were in the expected direction supports our conclusion, but further confirmation is needed.
In conclusion, our study suggests a possible association between general brain atrophy and hearing loss, but causality cannot yet be inferred due to cross-sectional study design.
- Women with cortical brain atrophy had poorer hearing in the high-frequency range of the left ear.
- The relation between brain atrophy and poorer hearing was correlated to the extension, not to the location, of the cortical atrophy.
- The relation between brain atrophy and poorer hearing was stronger in women with high cognitive function.
No conflicts of interest exist.
This study has been supported by grants from the Karolinska University Hospital/County of Stockholm, the Foundation Tysta Skolan, the Alzheimer's Association Stephanie B. Overstreet Scholars (IIRG-00-2159), the Swedish Council for Working Life and Social Research, the Swedish Research Council, The Bank of Sweden Tercentenary Foundation, The Alzheimer's Association Zenith Award (ZEN-01-3151), Stiftelsen för Gamla Tjänarinnor, and Handlanden Hjalmar Svenssons Forskningsfond.
1 Department of Psychiatry, Sahlgrenska University Hospital, SE-413 45 Göteborg, Sweden
2 Department of Audiology, Karolinska University Hospital, SE 141 86 Stockholm, Sweden
3 Department of Neurological and Psychiatric Sciences, University of Florence, Viale Morgagni 85, 50134 Firenze, Italy
* To whom correspondence should be addressed E-mail: xinxin.guo{at}neuro.gu.se
References
- Willott JF, Hnath Chisolm T, Lister JJ. Modulation of presbycusis: current status and future directions. Audiol Neurootol (2001) 6:231–49.[CrossRef][Medline]
- Steen B, Djurfeldt H. The gerontological and geriatric population studies in Gothenburg, Sweden. Z Gerontol (1993) 26:163–9.[Web of Science][Medline]
- Bengtsson C, Ahlqwist M, Andersson K, et al. The prospective population study of women in Gothenburg, Sweden, 1968–69 to 1992–93. A 24-year follow-up study with special reference to participation, representativeness, and mortality. Scand J Prim Health Care (1997) 15:214–9.[Web of Science][Medline]
- Jönsson R, Rosenhall U, Gause-Nilsson I, et al. Auditory function in 70 and 75-year-olds of four age cohorts. A cross-sectional and time-lag study of presbyacusis. Scand Audiol (1998) 27:81–93.[CrossRef][Web of Science][Medline]
- American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders (1987) 3rd edition. Washington, DC: American Psychiatric Association.
- Jönsson R, Rosenhall U. Hearing in advanced age. A study of presbyacusis in 85-, 88- and 90 year-old people. Audiology (1998) 37:207–18.[CrossRef][Web of Science][Medline]
- Guo X, Pantoni L, Simoni M, et al. Midlife respiratory function related to white matter lesions and lacunar infarcts in late life: the prospective population study of women in Gothenburg, Sweden. Stroke (2006) 37:1658–62.
[Abstract/Free Full Text] - Gustafson D, Lissner L, Bengtsson C, et al. A 24-year follow-up of body mass index and cerebral atrophy. Neurology (2004) 63:1876–81.
[Abstract/Free Full Text] - de Leon MJ, Ferris SH, George AE, et al. Computed tomography evaluations of brain-behavior relationships in senile dementia of the Alzheimer's type. Neurobiol Aging (1980) 1:69–79.[CrossRef][Web of Science][Medline]
- Folstein MF, Folstein SE, McHugh PR. "Mini-Mental State" A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res (1975) 12:189–98.[CrossRef][Web of Science][Medline]
- Pirila T, Sorri M, Jounio-Ervasti K, et al. Hearing symmetry among occupationally noise-exposed men and women under 60 years of age. Scand Audiol (1991) 20:217–22.[Web of Science][Medline]
- Job A, Grateau P, Picard J. Intrinsic differences in hearing performance between ears revealed by the asymmetrical shooting posture in the army. Hear Res (1998) 122:119–24.[CrossRef][Web of Science][Medline]
- Hallgren M, Larsby B, Lyxell B, et al. Cognitive effects in dichotic speech testing in elderly persons. Ear Hear (2002) 22:120–9.[CrossRef][Web of Science]
- Gates GA, Beiser A, Rees TS, et al. Central auditory dysfunction may precede the onset of clinical dementia in people with probable Alzheimer's disease. J Am Geriatr Soc (2002) 50:482–8.[CrossRef][Web of Science][Medline]
- Coffey CE, Lucke JF, Saxton JA, et al. Sex differences in brain aging: a quantitative magnetic resonance imaging study. Arch Neurol (1998) 55:169–79.
[Abstract/Free Full Text] - Cowel PE, Turetsky BI, Gur RC, et al. Sex differences in aging of the human frontal and temporal lobes. J Neurosci (1994) 14:4748–55.[Abstract]
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||