Abstract
Auditory processing difficulties and hearing loss have been reported among stroke survivors, but is largely neglected. Post-stroke hearing impairment may affect communication between stroke survivors and healthcare professionals, thereby restricting rehabilitation and long-term patient outcome. In this prospective pilot study, we sought to determine the prevalence and pattern of hearing loss in stroke patients when compared to age and sex matched controls. 50 consecutive patients with first-ever stroke, both hemorrhagic and ischemic, and a comparison cohort of 50 age and sex matched controls were assessed. Pure Tone Audiogram was performed in all patients within 15 days of stroke onset and mean hearing loss was determined. Mean audiometric threshold was significantly higher in both ears in stroke patients (mean 44.0 ± 12.1 dB) when compared to the control subjects (36.1 ± 11.4 dB; p = 0.001). After adjusting for Diabetes mellitus and hypertension, sensorineural hearing loss was more common and severe in stroke compared to controls (p < 0.005). Most of the strokes were ischemic and involved middle cerebral artery territory. A modest correlation between hearing threshold and stroke severity in both ears was seen (mean B 0.775, R2 0.54, CI 0.122–1.427, p = 0.020). Our pilot study shows significant hearing impairment in patients with stroke, compared to age and sex matched controls with similar prevalence of cardiovascular risk factors, interestingly seen in a predominantly anterior circulation stroke population. Undetected hearing loss may impact post stroke functional recovery. Hence, current rehabilitation guidelines should include auditory screening in all patients of stroke for detection of hearing loss.
Keywords: Stroke, Hearing impairment, Sensorineural hearing loss, Pure tone audiogram
Introduction
Stroke is a leading driver of neurological disability and placement in long-term care. A third of stroke survivors are functionally dependent on others even one year after stroke onset [1]. Hearing loss and auditory processing difficulties have also been reported among stroke survivors [2]. Approximately two-thirds of stroke survivors may suffer from a communication problem that may be related to listening, speaking, reading or writing [3]. In addition to dysphasia and dysarthria, these communication problems may affect production of speech prosody, mainly related to impaired auditory processing after stroke [4–6]. Stroke occurs more commonly in older individuals, among whom hearing impairment is widely prevalent, but studies indicate that compared to the healthy individuals, stroke survivors have higher rates of hearing impairment [1, 7]. There is evidence for increased cardiovascular risk in adults with hearing loss, especially among those with high frequency hearing loss [8]. This might contribute towards the higher observed hearing loss after stroke. “Guidelines for Adult Stroke Recovery and Rehabilitation” American Heart Association/American Stroke Association (AHA/ASA) 2016 state that “Stroke rehabilitation requires a sustained and coordinated effort from a large team, including doctors, physiotherapist, occupational therapist, family and friends. Communication and coordination among these team members are paramount in maximizing the effectiveness and efficiency of rehabilitation” [9]. Hearing loss may hinder communication between stroke survivors and healthcare professionals, thereby restricting participation in rehabilitation programs and limiting improvements in physical performance and may even predict long-term patient outcome after stroke.
While post-stroke visual deficits have been investigated extensively, auditory deficits remain scarcely studied. Accordingly, the current guidelines for auditory function assessments after stroke remain limited [10]. Although sudden hearing loss after stroke is rare, auditory processing and perceptual deficits are probably less well studied [11, 12]. Sudden hearing loss, defined as deterioration of hearing thresholds by 30 dB in at least three frequencies noted over 72 h may occur in acute stroke involving anterior inferior cerebellar artery or posterior inferior cerebellar artery [11]. Such hearing loss is more peripheral in mechanism and mainly unilateral. Stroke however may affect all levels of the auditory pathway, but owing to its multiple decussations and redundancy from the periphery to the cortex, both reception or perception deficits may be subtle and easily overlooked[2, 13]
In this prospective pilot study, we sought to determine the prevalence and pattern of hearing loss in our stroke patients when compared to age and sex matched controls.
Materials and Methods
This prospective pilot study was conducted at a tertiary care centre in India over a six month period between July and December 2019. Consecutive patients with first-ever stroke, both hemorrhagic and ischemic, were recruited. Patients with previous history of stroke were excluded. Diagnosis and severity of stroke were assessed by clinical features, National Institute of Health Stroke Scale (NIHSS) and neuroimaging. Demographic characteristics and prevailing vascular risk factors were recorded. Stroke patients who were conscious and oriented, enough to respond to pure tone audiogram (PTA) were included in the study.
PTA was performed in all patients within 15 days of the stroke-onset. Pure Tone Audiogram was carried out for both ears, for air and bone conduction according to the recommended guidelines [14]. Air conduction was tested for 250 Hz, 500 Hz, 1000 Hz, 2000 Hz, 4000 Hz and 6000 Hz frequencies and 250 Hz, 500 Hz, 1000 Hz, 2000 Hz and 4000 Hz for bone conduction. Mean hearing loss was determined for the above frequencies. Patients with a pre-existing history or otoscopic evidence of ear disease were excluded from the study. Impedance audiometry was carried out in all study participants and the type of tympanogram noted. A comparison cohort of 50 age and sex matched controls underwent audiometric assessment with a similar protocol.
Hearing loss was defined as a pure-tone average reduction by > 25 dB. Mild, moderate, severe and profound hearing loss were defined as 26–40, 41–60, 61–80, and > 81 dB, respectively. Disabling hearing loss was defined as hearing loss greater than 40 dB in the better hearing ear in adults. Potential co-variates for hearing loss as well as stroke (specifically hypertension and diabetes mellitus) were recorded in study participants as well as controls.
An institutional ethics committee approval was obtained for this study and written informed consent was obtained from all patients.
Statistical Analyses
Demographic and baseline variables were analyzed descriptively. Chi-square test was used for categorical predictors, while 2 sample t-test was used for continuous predictors. Descriptive statistics have been presented with mean, range, and standard deviation of the variables. Pearson's correlation and linear regression were used to assess various associations. All the data were analyzed using SPSS statistical software version 20.0 (SPSS Inc, IBM, Chicago).
Results
A total of 100 patients were included in the study, comprising of 50 patients with first-ever stroke and 50 age and sex matched controls. Mean age of the stroke patients was 60 years (SD 13.1), which was comparable (58.1 ± 11 years) to the control group. Male and female subjects were equal in number in both groups. Baseline characteristics of stroke patients and control groupare summarized in Table 1. Briefly, hypertension was the commonest vascular risk factor in 32 (64%) stroke patients followed by dyslipidemia in 27 (54%). The vascular risk factors showed similar prevalence between stroke patients and the control group.
Table 1.
Baseline characteristics of the study populations (n = 100)
| Variables | All (n = 100) | Stroke (n = 50) | Controls(n = 50) | p value |
|---|---|---|---|---|
| Baseline demographics | ||||
| Age (years), mean (SD) | 59.1 (12.1) | 60.0 (13.1) | 58.1 (11.0) | 0.420 |
| Male gender, n (%) | 52 (52.0) | 25 (50.0) | 27 (54.0) | 0.689 |
| Co-morbidities, n (%) | ||||
| Diabetes mellitus | 31 (31.0) | 15 (48.4) | 16 (51.6) | 0.829 |
| Hypertension | 59 (59.0) | 32 (64.0) | 27 (54.0) | 0.309 |
| Dyslipidemia | 49 (49.0) | 27 (54.0) | 22 (44.0) | 0.317 |
| Ischemic heart disease | 24 (24.0) | 11 (22.0) | 13 (26.0) | 0.815 |
| Atrial fibrillation | 16 (16.0) | 8 (16.0) | 8 (16.0) | 1.000 |
| 8 (8%) | 5 (10%) | 3 (6%) | 0.263 | |
| Audiometry parameters | ||||
| Hearing threshold, mean (SD) | ||||
| Right ear | 40.3 (12.6) | 44.2 (12.2) | 36.4 (11.8) | 0.002 |
| Left ear | 39.9 (12.3) | 43.9 (12.2) | 35.8 (11.1) | 0.001 |
| Mean | 40.1 (12.4) | 44.0 (12.1) | 36.1 (11.4) | 0.001 |
Most of the patients in both groups (47/50 stroke patients and 48/50 controls) showed type A tympanogram in both ears, indicating negligible middle ear pathology in the study population.
Mean audiometric threshold was significantly higher in both ears in stroke patients (mean 44.0 ± 12.1 dB) when compared to the control subjects (36.1 ± 11.4 dB; p = 0.001). This difference in hearing threshold was more pronounced in higher frequencies (2000–6000 Hz) between stroke patients (55 dB ± 5) and controls (38.33 ± 7.63 dB; p = 0.001) Most of the strokes were ischemic and involved middle cerebral artery (MCA) territory (Table 2). Hearing loss in stroke patients was sensorineural(SNHL), bilateral and symmetrical irrespective of the side involved by stroke (Fig. 1). The difference in the hearing threshold in both ears in the same patient was less than 10 dB, thus ruling out any laterality or unilateral involvement. Mid and higher frequencies were involved more than the lower frequencies. None of the stroke patients complained of sudden reduction or loss of hearing in any ear. Moderate to severe SNHL was more common amongst stroke patients while mild hearing loss was more common in controls. After adjusting for Diabetes mellitus and hypertension, which can also lead to SNHL, hearing loss was found to be more common and more severe amongst stroke patients compared to controls (p < 0.005).In order to test the goodness-of-fit measure, linear regression was performed, which showed a modest correlation between hearing threshold and stroke severity in both ears (mean B 0.775, R2 0.54, CI 0.122–1.427, p = 0.020) (Tables 3, 4).
Table 2.
Stroke types, location, vascular territory and severity (n = 50)
| Variables | Stroke characteristics (n = 50) |
|---|---|
| Type of stroke, n (%) | |
| Ischaemic | 43 (86.0) |
| Haemorrhagic | 7 (14.0) |
| Side of stroke, n (%) | |
| Right anterior | 19 (38.0) |
| Left anterior | 23 (46.0) |
| Posterior | 8 (16.0) |
| Vascular territory, n (%) | |
| MCA | 43 (86.0) |
| ACA | 2 (4.0) |
| Posterior | 5 (10.0) |
| NIHSS score, median (IQR) | 1 (IQR = 0–7) |
| Day PTA done from symptom onset (day), mean (SD) | 7 (3) |
Fig. 1.
47 year old hypertensive male patient showing left middle cerebral artery (MCA) infarct on MRI. Impedance audiometry of the same patient showing a type A tympanogram. PTA done on day 5 after stroke onset shows bilateral SNHL involving higher frequencies more than lower frequencies. Mean hearing threshold was about 45 dB in both ears
Table 3.
Relationship between hearing threshold and stroke location (n = 50)
| Side of stroke | Right anterior (n = 19) | Left anterior (n = 23) | Posterior (n = 8) | No stroke (n = 50) | p value |
|---|---|---|---|---|---|
| Hearing threshold, mean (SD) | |||||
| Right ear | 42.0 (11.1) | 43.5 (11.7) | 51.3 (15.1) | 36.4 (11.9) | 0.004 |
| Left ear | 42.8 (10.7) | 43.1 (11.7) | 49.0 (16.8) | 35.8 (11.1) | 0.004 |
| Mean | 42.4 (10.8) | 43.4 (11.6) | 50.1 (15.8) | 36.1 (11.4) | 0.004 |
| Vascular territory | MCA (n = 43) | ACA (n = 2) | Posterior (n = 5) | No stroke (n = 50) | p value |
|---|---|---|---|---|---|
| Hearing threshold, mean (SD) | |||||
| Right ear | 43.3 (11.7) | 50.0 (7.1) | 49.0 (18.2) | 36.4 (11.8) | 0.010 |
| Left ear | 42.9 (11.1) | 52.5 (3.5) | 49.4 (21.0) | 35.8 (11.1) | 0.003 |
| Mean | 43.1 (11.3) | 51.3 (5.3) | 49.2 (19.6) | 36.1 (11.4) | 0.005 |
ACA, anterior cerebral artery; MCA, middle cerebral artery; NIHSS, National Institute of Health Stroke Scale; PTA, pure tone audiometry
Table 4.
Correlation between hearing threshold and stroke severity (Pearson’s correlation)
| Variable | B | R2 | Confidence interval (CI) | P value |
|---|---|---|---|---|
| Right ear | 0.784 | 0.053 | 0.019–1.449 | 0.021 |
| Left ear | 0.765 | 0.021 | 0.116–1.414 | 0.021 |
| Mean | 0.775 | 0.020 | 0.122–1.427 | 0.020 |
Discussions
Our pilot study shows that significant disabling hearing impairment occurs in patients with stroke, when compared to age and sex matched controls with similar prevalence of cardiovascular risk factors. Interestingly, this observation was noted in a predominantly anterior circulation stroke population.
Our stroke patients suffered from a hearing impairment that was sensorineural, bilateral, symmetrical and affected higher frequencies. Even after adjusting for diabetes mellitus and hypertension, SNHL and the degree of hearing impairment was higher in patients with stroke. Our findings are consistent with previous studies [7, 8]. Kuo et al. in a nationwide study based on 44,460 patients for 5 years observed that stroke survivors were 1.71 times more likely to develop SNHL than patients without stroke [1]. Furthermore, they observed a remarkable increase in risk of SNHL in stroke patients within 1-year of follow-up. Similar relationship between stroke risk and hearing loss was reported among African-Americans in the Jackson Heart Study where stroke risk showed a positive predictive relationship with hearing pure-tone threshold [15].
Apart from stroke involving the vertebrobasilar territory in which hearing loss may be striking and immediate[1, 11] sudden changes in hearing threshold are usually not seen immediately after stroke, probably due multiple sources of blood supply to various parts of the auditory pathway, such as the cochlear nucleus, inferior colliculus and medial geniculate body [1, 12, 14]. Additionally, strong bilateral representation of the auditory pathway above the level of the cochlear nuclei contributes to this observation. In our study, none of the patient complained of sudden and acute reduction in hearing, probably due to the absence of anterior inferior cerebellar artery (AICA) infarct in the study cohort. In most of our stroke patients hearing loss after stroke if present, were subtle, when compared to other features like dysphasia, loss of motor function or visual deficits suggesting a longstanding cause.
Performing a proper pure tone audiogram in a soundproof room may not be feasible among stroke patients suffering from cognitive or functional impairments. Furthermore, widespread bilateral lesions of the brain and auditory pathway may render the patients unable to respond to standard PTA. Perhaps, this is responsible for the debatable and underreporting of the incidence of SNHL in stroke patients [8, 10, 16]. A systematic review and meta-analysis, which investigated the risk factors for adult SNHL, indicated that developing SNHL involves a complex pathogenetic process with multiple contributing factors notably, inherited cardiovascular risk factors, smoking and alcohol consumption. Even genetic mutations associated with greater risk of thromboembolic events have been implicated [17]. The underlying causal mechanism relating stroke with SNHL, mainly anterior circulation stroke is complex and not well understood but nevertheless exists.
According to the current global burden of disease data on stroke, in 2016 there were almost 116 million DALYs (disability adjusted life years) due to stroke. [18] Hearing loss that is not immediately apparent after stroke may remain undetected and uncorrected affecting the overall communication of the patient. Therefore, post stroke rehabilitation protocols should include screening for hearing before the patient leaves the stroke ward, including a simple set of hearing-related questions and a screening audiogram to address the hearing needs of stroke survivors [19]. Accordingly, in stroke patients with hearing impairment, the rehabilitation team may be informed to follow a modified protocol to ascertain optimal patient participation.
Clinical implications of the present study are important. The National Institute for Health and Care Excellence in the United Kingdom recommends performing a full medical assessment of the person with stroke including functional ability and communication. Uncorrected hearing loss may affect outcome of speech, language assessment and related therapies and impact on functional recovery after stroke [20, 21]. In addition, individuals with hearing loss may have an increased rate of developing dementia or rapid cognitive decline [22, 23]. Although, this is perhaps the first study that evaluated hearing impairment in stroke patients in India, we acknowledge certain limitation of our study. First, a small sample size is a major limitation to draw any reliable conclusions. Second there were very few patients with posterior circulation stroke, in whom hearing impairments may be more pronounced However, this was a pilot study for Indian stroke patients and our findings would serve as a template for larger multicenter studies to define the impact of ischemic stroke and associated hearing impairment on stroke rehabilitation and functional outcome and further ascertain its impact on cognitive functions, relationship to stroke etiology, age, location and size of infarct, all of which are known factors to affect hearing abilities.
Conclusion
In conclusion, significant hearing impairment occurs among Indian patients with stroke, irrespective of the type, location and cause of stroke. Larger and multicenter studies are recommended to evaluate various components of this association.
Authors’ Contribution
SS: design and analysis of study, collection of data, writing and editing the paper. VP: contributed data (provided patients of stroke for analysis, diagnosis and classification of stroke) editing of the paper. AS: contributed data (provided patients of stroke for analysis, diagnosis and classification of stroke), editing of the paper. BYQT: performed the statistical analysis. VKS: conceived and designed the study, writing and editing the paper. The paper was drafted revised and finalized by all authors. All authors were involved in conceptualization, methodology, data analysis, writing and editing of the manuscript. All authors have read and approved the final manuscript.
Compliance with Ethical Standards
Conflict of interest
The authors declare no conflict of interest related to this work. The authors declare no financial support or interest related to this study.
Footnotes
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