Neurol India Home 
 

ORIGINAL ARTICLE
Year : 2022  |  Volume : 70  |  Issue : 2  |  Page : 554--562

Impact of Hearing Loss on Cognitive Abilities in Subjects with Tinnitus

Anuradha Sharma1, Manju Mohanty2, Naresh Panda1, Sanjay Munjal1,  
1 Department of Otolaryngology, Speech and Hearing Unit, New OPD, Post Graduate Institute of Medical Education and Research, Chandigarh, India
2 Department of Neurosurgery, New OPD, Post Graduate Institute of Medical Education and Research, Chandigarh, India

Correspondence Address:
Dr. Anuradha Sharma
Department of Otolaryngology, Speech and Hearing Unit, New OPD, Post Graduate Institute of Medical Education and Research, Chandigarh - 160 012
India

Abstract

Background: This study aimed to delineate the underlying pathophysiology of tinnitus between normal hearing and hearing loss subjects. Objective: The study aimed to characterize the neuropsychological aspects of two types of groups with tinnitus having variable hearing thresholds. Materials and Methods: The study sample comprises 75 subjects in a group with tinnitus and normal hearing, and 100 subjects in the tinnitus and hearing loss group. Subjects were matched to their respective controls for age, gender, and education levels. Subjects underwent verbal learning and memory tasks, visual learning, memory, listening attention, sustained visual attention, work memory, category control, phonemic mastery, response inhibition, and data processing velocity. Results and Conclusions: Subjects having hearing loss with bilateral tinnitus showed significantly reduced performance on total learning capacity (P = 0.02) and recognition (P = 0.05) (Rey's auditory verbal learning test), auditory attention tasks, digit forward span test (DFST) (P = 0.03), digit span test score (P = 0.01), and working memory (P = 0.02) (digit backward span test). For response inhibition tasks and Stroop interference (P = 0.03), subjects with normal hearing with bilateral tinnitus displayed lower performance. This study proves a relationship between poor working memory, auditory memory, total learning capacity, and recognition due to hearing impairment in bilateral Tinnitus subjects. The study has substantial implications for effective assessment and treatment recommendations in hearing loss with bilateral tinnitus subjects.



How to cite this article:
Sharma A, Mohanty M, Panda N, Munjal S. Impact of Hearing Loss on Cognitive Abilities in Subjects with Tinnitus.Neurol India 2022;70:554-562


How to cite this URL:
Sharma A, Mohanty M, Panda N, Munjal S. Impact of Hearing Loss on Cognitive Abilities in Subjects with Tinnitus. Neurol India [serial online] 2022 [cited 2022 Aug 18 ];70:554-562
Available from: https://www.neurologyindia.com/text.asp?2022/70/2/554/344654


Full Text



The cognitive ineffectiveness in tinnitus has become increasingly apparent in recent times. Wang et al.[1] reported severe cognitive deficits in subjects having tinnitus. Further reports highlight that even early stages of mild hearing loss contributes enormously to cognitive decline.[2] Researchers established that even 25-dB hearing loss may affect cognitive functioning equivalent to 7 years of aging.[3] Thus, it is questionable whether slippages and cognitive errors are a characteristic of tinnitus or an overall reflection of hearing loss in subjects with tinnitus. This study investigated the impact of hearing loss on cognitive domains in groups with and without tinnitus.

 Materials and Methods



Research design

The study had a cross-sectional research design [[Figure 1]: Experimental design]. Seventy-five subjects (42 males and 33 females) with tinnitus and normal hearing (group 1) and 100 subjects (70 males and 30 females) with a bilateral mild-moderate level of hearing loss with tinnitus (group 2) were identified. The age group for the study was 18–55. Data associated with the perception of tinnitus included the pitch, location, and nature of tinnitus. Subjects with severe bilateral sensory hearing loss (61–80-dB HL loss) and those over 55 years were excluded from the study to minimize the influence of hearing loss on the assessment.{Figure 1}

The exclusion criteria included subjects with external or middle ear pathology, systemic disorders, psychiatric illnesses, neurological disorders, noise exposure, and the use of mobile phones for more than 2 hours a day. The Hospital Anxiety and depression (HADS) scale evaluated the symptoms of anxiety and depression; tinnitus subjects with scores above the cutoff score were excluded from the study. The institute's ethics committee endorsed the study before its commencement (in accordance with the Helsinki Declaration, 1975). Informed consent was taken obtained from every subject prior to the commencement of the study.

Audiological assessment

Pure tone thresholds were acquired at conventional (250 Hz–8 kHz) octave frequencies. The computation of the PTA average of 500, 1000, 2000, and 4000 Hz permitted a comparison between the respective groups. A subject with a PTA of <25-dB HL was considered normal hearing, from 26–40 dB was considered a mild hearing loss, and 41–55 dB was considered a moderate hearing loss.[4] A valid and adapted inventory of Hindi Tinnitus handicap (English Tinnitus handicap inventory (THI) by Craig W. Newman)[5] was also administered to the two groups.[6]

Neuropsychological tests

The following tests from the NIMHANS neuropsychological battery[7] were included: Rey's auditory verbal learning test (RAVLT),[8] Rey's complex figure test (RCFT),[9] digit vigilance test (DVT),[9] verbal N back test,[10] controlled oral word association test (COWA),[9] animal names test (ANT),[9] digit symbol substitution test (DSST),[11] and digit span test (DST) from the Wechsler memory scale-III (India)[12] and the Stroop test.[13]

Not all hearing-impaired individuals use hearing aids regularly on a daily basis. As the subjects in hearing loss with tinnitus were not accustomed to hearing aids, they were fitted with adequate amplification (from sample hearing aids available in the department) during testing for the appropriate commencement of the neuropsychological tests. Hearing loss was compensated by amplification only during neuropsychological testing. The subjects were provided with amplification 2–3 days before the test session for acclimatization with the aids. The hearing aid fitting was finalized utilizing real-ear insertion gain testing and further confirming the benefit from the hearing aid with the help of speech discrimination scores (with and without hearing aid assistance). The study group subjects were provided sufficient training over 2–3 days to get accustomed to listening through the device and wore hearing aids during neuropsychological testing leading to effortless and more precise outcomes.

Statistical analysis

Data were analyzed using version 23 of Statistical Package for Social Sciences (SPSS). Shapiro–Wilk's test of normalcy revealed the non-normal distribution of data for groups. As a result, the non-parametric statistical test Mann–Whitney was applied. Descriptive statistics were employed to obtain the mean, standard deviation for continuous variables, and frequency and percentages for the discontinuous variables.

 Results



A total of 175 subjects (G1- 75 subjects, G2 -100 subjects) were enrolled for the study. [Table 1] shows the demographic details of the subjects. The scores of THI revealed that group 1 and group 2 had maximum subjects in mild and moderate category (37% had a mild handicap, 39% fell in the moderate category for group 1, and 32% mild and 38% moderate for group 2), 14% and 18% in the severe group, and 10% and 12% in catastrophic category for group 1 and group 2, respectively. Subjects of hearing loss with tinnitus group had a mild to moderate bilateral hearing loss that existed for at least 1 month to 1 year. [Table 2] shows the pure tone thresholds across both groups.{Table 1}{Table 2}

Clinical profile of tinnitus subjects

Tinnitus was predominantly present in the left ear (40% in G1 and 39% in G2), followed by binaural tinnitus (26.7% and 33%) and tinnitus on the right side (29.3% and 26%). Subjects in G1 and G2 showed preponderance for high-pitched tinnitus (72% in G1 and 72% in G2). The vast majority of subjects had a “hissing” type of tinnitus (45.3% in G1 and 38% in G2), followed by the “buzzing” type (14.7% in G1 and 20% in G2). The tinnitus pitch and loudness characteristics of subjects in both groups are displayed in [Table 1].

Neuropsychology tests in mixed tinnitus groups

[Table 3] shows that there was no significant difference between the two groups regarding the RAVLT, RCFT, DST, N back, DVT, and verbal fluency measures (COWA and ANT); only the DVT error score showed a significant difference [Table 4]. In the Stroop test, a significant difference was observed only in the word score (P = 0.02) and not in the color score and color word score. However, the information processing speed measured through DSST was lower (P = 0.006) in the G2 as compared to the G1 [Table 3]. The age-adjusted means did not show a significant result on DSST.{Table 3}{Table 4}

Neuropsychological test results for unilateral and bilateral tinnitus groups

Furthermore, the comparison between unilateral tinnitus groups did not yield significant results for any of the neuropsychological domains [Table 5]. However, hearing loss with bilateral tinnitus showed significant differences in RAVLT measures, that is, learning capacity (P = 0.02), the total number of words recalled in five trials (P = 0.03), and recognition (P = 0.05) of normal hearing with the bilateral tinnitus group. We found significant evidence of auditory attention deficits (DST) (P = 0.03 and 0.01) and memory impairment (DBST) with P = 0.02 between bilateral tinnitus with normal and hearing loss groups. There was a direct association between increased error score (P = 0.02) on DVT in the normal hearing with bilateral tinnitus subjects. Executive functioning also showed a negative association with subjects having mild to moderate hearing loss and bilateral tinnitus. Significant differences were recorded G2 and G1 on color naming (P = 0.01) and Stroop interference tasks (P = 0.03) on the age-adjusted means.{Table 5}

The groups revealed no statistically significant difference in the comparison of age-adjusted means on visual memory (RCFT), visual attention (DVT), working memory (N back), and verbal fluency (ANT and COWA) scores [Table 6].{Table 6}

 Discussion



A well-known fact is that tinnitus and hearing loss are nested; consequently, it is of paramount importance to define the impact of hearing loss on the cognition of tinnitus subjects. Perhaps one of the most striking outcomes is that bilateral tinnitus subjects with hearing loss exhibited poorer executive functioning, including working memory and auditory attention, total learning capacity, and recognition compared to bilateral tinnitus with normal hearing.

The presence of continuous tinnitus, considered irrelevant, interferes with selective attention (DST) and alters cognitive performance as far as possible by automatically focusing attention on the tinnitus ear. The attention captured by tinnitus causes a reduction in performance toward the signals presented to the ear of tinnitus.[14] Furthermore, studies on tinnitus using the evoked potential have also highlighted that chronic tinnitus impedes the shift of attention towards any external task requiring attention.[15] This evidence indicates that tinnitus has a significant effect on attention shift. The literature also has many supporting studies toward the effects of even mild hearing impairment on the cognitive domain because untreated hearing loss utilizes a large processing capacity to cope with the hearing disorder.[16] Thus, when bilateral tinnitus subjects struggled during attention tasks, a degraded auditory signal and higher language requirements due to hearing loss would further influence the cognitive performance during tasks requiring auditory attention.[17] Thus, the cumulative effect of hearing loss with bilateral tinnitus can add to the existing burden on central executive function.

Working memory is evaluated through tasks involving storage and processing capacity at the same time. DBST measures the working memory where the task was based on immediately recalling the digits in reverse order. The results of this study indicate that bilateral hearing loss in bilateral tinnitus subjects poses a great demand on working memory capacity, a fundamental component of many higher-order processes. The working memory domains (represented in the anterior dorsal cingulate gyrus) observed across the DBST scores showed a significant divergence between the groups studied. Previous researchers have established that tinnitus impairs the phonological loop's ability to retain auditory verbal information and decreases the capacity to carry on other tasks on the same lines as hearing loss.[18] Various other studies involving tinnitus subjects revealed that they were slower than their respective controls under very demanding conditions and indicated tinnitus reduced cognitive efficiency.[19] However, according to the information degradation hypothesis, subjects with hearing difficulties require more effortful listening, and greater demands are placed on working memory as mental resources are diverted towards perception[20]. Thus, bilateral tinnitus increases the demands on auditory processing; however, the hearing loss further adds to the working memory loads by diminishing the remaining capacity for conducting other tasks. Thus, the present study results also add to the literature that hearing loss in bilateral tinnitus subjects significantly alters the working memory with a significant contribution from the hearing loss itself.

The RAVLT test indicated that bilateral tinnitus with hearing loss significantly reduced total learning ability and recognition scores than bilateral tinnitus with normal hearing. The findings of lower scores in bilateral tinnitus with hearing loss group on RAVLT (a measure of auditory verbal learning and memory) were in agreement with many previous studies[19], indicating the weakness of the associative memory in the tinnitus group with hearing loss. The low recognition memory in subjects with bilateral tinnitus shows that it distorts the interaction between the lexical memory and associative process, explicitly disrupting “the interaction between parietal cortex attention region and frontal cortex regions associated with retrieval.”[21] Results from earlier studies have illustrated that as tinnitus disrupts attention to tasks, subjects must deploy varied strategies to attend to memory for retrieval compared to healthy controls.[22] Additionally, we have also found evidence of further depletion of cognitive performance on total learning capacity and recognition that might be connected with mild to moderate hearing loss in tinnitus subjects, as has also been previously described.[23] Therefore, this study suggests a significant decline in total learning ability and recognition due to bilateral hearing loss in bilateral tinnitus subjects.

However, another intriguing finding was that the DSST scores (a measure of information processing speed; has a neural basis in the fronto-hippocampal region) were not statistically different between the two groups. The existing evidence also indicates that probably only moderate-severe hearing loss contributes significantly to cognitive impairment.[24] The methodological variation that only subjects with mild-moderate loss were included in the written report could have led to differences. Moreover, evidence from the present study could also propose that tinnitus could have brought significant alterations in information processing speed that did not further accentuate due to bilateral hearing loss in tinnitus and hearing loss subjects.

The results drawn from the error score in visually sustained attention tasks pinpoint that tinnitus subjects with normal hearing were probably more distracted by the environmental noise and the internal noise, which contributed to a more significant error score. Sustained attention means the ability to attend to a task for an extended period. It is required to fulfill tasks requiring repetition, which depletes significantly in the tinnitus subjects with normal hearing.[25] These results imply that bilateral tinnitus with normal hearing is more prone to errors, even in tasks requiring sustained visual attention.

The present study also found a significant difference in the age-adjusted means on Stroop interference task and color-naming task between bilateral tinnitus subjects with hearing loss and bilateral tinnitus subjects with normal hearing. Stroop test not only tests the response inhibition but also requires attention from subjects. Our Stroop test findings uncover that normal hearing is more distracted by bilateral tinnitus and unable to pay attention to tasks involving executive control of attention than hearing loss with bilateral tinnitus subjects. Generally, in tinnitus subjects, more attention resources are required to complete a dual-task paradigm (fewer attention resources for the secondary task).[25] Degeest et al.[26] also demonstrated increased listening effort in subjects suffering from mild tinnitus and normal hearing for executive function tasks. They also suggested that chronic tinnitus subjects devote unconscious attention to this annoying sound while carrying out demanding tasks, leading to the deterioration of their performance. Our findings also display that subjects with bilateral tinnitus and normal hearing showed poorer performance on age-adjusted means for response inhibition tasks (tasks without acoustic requirements) than subjects with hearing loss with bilateral tinnitus. Future research is required to investigate whether any confounding factors such as age, length of time with hearing impairment, degree of hearing impairment, and procedure used to calculate the Stroop effect lead to the impact.

The deficits in total learning capacity, auditory attention, and working memory appearing on neuropsychological tests in hearing loss with bilateral tinnitus subjects could be distinctly associated with hearing loss leading to deficient acoustic or language comprehension requirements. In contrast, Stroop, having a minimum hearing requirement, showed lower scores for the normal hearing with bilateral tinnitus subjects. However, in subjects with bilateral tinnitus and hearing loss, most of the other neuropsychological tests, namely RCFT (visuo-constructive ability and visual short and long term memory), DVT (visual attention), COWA and ANT (verbal fluency), and N back (working memory) did not show any significant alterations.

 Conclusion



Conjointly, our data suggest that when peripheral hearing loss exists along with tinnitus, only auditory-based higher-order cognitive functioning (total learning capacity, auditory attention, and working memory) shows a significant impact.

Limitations of the study

Subjects with hearing loss with tinnitus did not regularly wear hearing aids. If the hearing aids were worn, it would have significantly affected their hearing-related quality of life and, in turn, their neuropsychological aspects. Additionally, the study did not examine the emotional aspects of tinnitus, that is, bothersome or non-bothersome tinnitus, which could also influence the outcome of the study.

Declaration of Patient Consent

Informed consent was taken obtained from every subject prior to the commencement of the study. The patient's identity has been adequately anonymized.

Self disclosure

The authors hereby certify that the work shown here is genuine, original, and not submitted anywhere, either in part or full. All the necessary permissions from the patient, hospital, and institution have been taken for submitting to neurology India.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1Wang Y, Zhang JN, Hu W, Li JJ, Zhou JX, Zhang JP, et al. The characteristics of cognitive impairment in subjective chronic tinnitus. Brain Behav 2018;8:e00918.
2Amieva H, Ouvrard C, Giulioli C, Meillon C, Rullier L, Dartigues JF. Self-reported hearing loss, hearing aids, and cognitive decline in elderly adults: A 25-year study. J Am Geriatr Soc 2015;63:2099-104.
3Lin FR. Hearing loss and cognition among older adults in the United States. Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences 2011;66:1131-6.
4Goodman AC. LXXX new observations on changes in hearing in the temporal course of Meniere's disease. Ann Otol Rhinol Laryngol 1965;74:991-1010.
5Newman CW, Jacobson GP, Spitzer JB. Development of the tinnitus handicap inventory. Arch Otol Head Neck Surg 1996;122:143-8.
6Sharma A. Evaluation of audiological, neurocognitive and scintigraphic characteristics of tinnitus. PhD thesis unpublished, Post Graduate Institute of Medical Education and Research, Chandigarh, India;2018.
7Rao SL, Subbakrishna DK, Gopukumar K. NIMHANS. Neuropsychological Battery-Manual. Bangalore: National Institute of Mental Health and Neurosciences; 2004.
8Maj M, D'Elia L, Satz P, Janssen R, Zaudig M, Uchiyama C, et al. Evaluation of two new neuropsychological tests designed to minimize cultural bias in the assessment of HIV-1 seropositive persons: A WHO study. Arch Clin Neuropsychol 1993;8:123-35.
9Lezak MD, Howieson DB, Loring DW, Fischer JS. Neuropsychological Assessment. USA: Oxford University Press; 2004.
10Smith EE, Jonides J. Storage and executive processes in the frontal lobes. Science 1999;283:1657-61.
11Wechsler, David. Wechsler adult intelligence scale. Archives of Clinical Neuropsychology;1955.
12Chlebowski, Colby. Wechsler Memory Scale All Versions. Kreutzer, Jeffrey S. DeLuca, John Caplan, Bruce. Encyclopedia of Clinical Neuropsychology. New York, NY. Springer New York.2688-2690;2011.
13Jensen AR, Rohwer WD Jr. The Stroop color-word test: A review. Acta Psychol 1966;25:36-93.
14Cuny C, Norena A, El Massioui F, Chéry-Croze S. Reduced attention shift in response to auditory changes in subjects with tinnitus. Audiol Neurotol 2004;9:294-302.
15Delb W, Strauss DJ, Low YF, Seidler H, Rheinschmitt A, Wobrock T, et al. Alterations in event related potentials (ERP) associated with tinnitus distress and attention. Appl Psychophysiol Biofeedback 2008;33:211-21.
16Taljaard DS, Olaithe M, Brennan-Jones CG, Eikelboom RH, Bucks RS. The relationship between hearing impairment and cognitive function: A meta-analysis in adults. Clin Otolaryngol 2016;41:718-29.
17Peelle JE, Troiani V, Grossman M, Wingfield A. Hearing loss in older adults affects neural systems supporting speech comprehension. J Neurosci 2011;31:12638-43.
18Andersson G, McKenna L. Contributions of clinical psychology in audiology: Hearing impairment and tinnitus. Clinical Psychology & Psychotherapy: An International Journal of Theory and Practice 1997;4:42-50.
19Stevens C, Walker G, Boyer M, Gallagher M. Severe tinnitus and its effect on selective and divided attention: Acufeno severo y sus efectos sobre la atención selectiva y dividida. Int J Audiol 2007;46:208-16.
20Lehericy S, Baulac M, Chiras J, Piérot L, Martin N, Pillon B, et al. Amygdalohippocampal MR volume measurements in the early stages of Alzheimer disease. Am J Neuroradiol 1994;15:929-37.
21Ciaramelli E, Grady CL, Moscovitch M. Top-down and bottom-up attention to memory: A hypothesis (AtoM) on the role of the posterior parietal cortex in memory retrieval. Neuropsychologia 2008;46:1828-51.
22Hallam R, McKenna L, Shurlock L. Tinnitus impairs cognitive efficiency. Int J Audiol 2004;43:218-26.
23Ray J, Popli G, Fell G. Association of cognition and age-related hearing impairment in the English longitudinal study of ageing. JAMA Otolaryngol Head Neck Surg 2018;144:876-82.
24Mohamad N, Hoare DJ, Hall DA. The consequences of tinnitus and tinnitus severity on cognition: A review of the behavioural evidence. Hear Res 2016;332:199-209.
25Tai Y, Husain FT. The role of cognitive control in tinnitus and its relation to speech-in-noise performance. J Audiol Otol 2019;23:1-7.
26Degeest S, Keppler H, Corthals P. The effect of tinnitus on listening effort in normal-hearing young adults: A preliminary study. J Speech Lang Hear Res 2017;60:1036-45.