|Year : 2016 | Volume
| Issue : 2 | Page : 95-100
Hearing profile and postural sensory integration deficits in Parkinson's disease
Gehan A Al Zarea, Ali A Ali, Ahmed M.A. Mahmoud, Ahmed I Abbas
Audiology Unit, Department of ENT, Al-Alzhar University, Cairo, Egypt
|Date of Submission||07-Jun-2016|
|Date of Acceptance||17-Jun-2016|
|Date of Web Publication||21-Oct-2016|
Ahmed I Abbas
Benha, 15 Farid Nada St. postal code 15311
Source of Support: None, Conflict of Interest: None
The objectives of this study were to evaluate auditory function and postural instability in Parkinson’s disease (PD) patients, and to correlate audiological findings and postural instability with the severity and duration of PD.
Patients and methods
The severity of motor symptoms and staging were ascertained with the Unified Parkinson’s Disease Rating Scale and the Hoehn and Yahr Scale, with identification of the side most affected by PD and the disease duration. Audiologic evaluation consisted of history taking, otoscopic examination, pure-tone audiometry, acoustic immittance measures, speech audiometry, and brainstem auditory-evoked potentials. Sensory Organization Test was also conducted. Of 55 PD patients, 31 were enrolled in this study, along with 31 healthy age-matched and sex-matched controls.
Results and conclusion
Our PD patients showed high-frequency, age-dependent unilateral or bilateral hearing loss, significant increase in wave V peak latency and I–V and III–V interpeak latencies, and significant decrease in composite score, vestibular score, and visual score and significant increase in preferential visual score in comparison with controls. All these findings were significantly correlated to disease severity and duration.
Keywords: auditory brainstem response, Parkinson’s disease, postural instability, pure-tone audiometry, Sensory Organization Test
|How to cite this article:|
Al Zarea GA, Ali AA, Mahmoud AM, Abbas AI. Hearing profile and postural sensory integration deficits in Parkinson's disease. Al-Azhar Assiut Med J 2016;14:95-100
|How to cite this URL:|
Al Zarea GA, Ali AA, Mahmoud AM, Abbas AI. Hearing profile and postural sensory integration deficits in Parkinson's disease. Al-Azhar Assiut Med J [serial online] 2016 [cited 2018 May 23];14:95-100. Available from: http://www.azmj.eg.net/text.asp?2016/14/2/95/192651
| Introduction|| |
Parkinson’s disease (PD) was first described by James Parkinson in 1817. It is a neurodegenerative disease with degeneration of neurons in the substantia nigra and accumulation of aggregated α-synuclein in the brainstem. This degeneration results in a shortage of dopamine  and in the presence of Lewy bodies in the remaining cells. The pathological changes in PD are seen not only in the substantia nigra but also in many brainstem and cortical regions. This widespread neuropathology is responsible for various motor and nonmotor symptoms of PD . Both incidence and prevalence rates of PD increase with aging. As life expectancy of the general population arises, both the occurrence and prevalence of PD are likely to increase dramatically .
The exact cause of PD is unknown. An overall 15–20% of PD patients have a close relative who has also experienced parkinsonian symptoms. This leads us to believe that there may be a genetic component involved in PD. But development of the disease is dependent on the influence of environmental factors .
Mutations of α-synuclein, LRRK2, and PINK1 are the most important genetic factors associated with PD . PD is characterized by four cardinal motor manifestations: resting tremor, bradykinesia, rigidity, and postural instability (PI) with impairment of postural reflexes . Motor symptoms usually begin asymmetrically but gradually spread to the contralateral side . The side of initial involvement tends to remain the most severely affected throughout the course of the disease .
A variety of nonmotor symptoms and disorders are common in PD, such as depression, autonomic dysfunction, olfactory dysfunction, cognitive impairment, dementia, and psychosis . PD can be staged with different scales such as the Hoehn and Yahr (H&Y) Scale  and The Unified Parkinson’s Disease Rating Scale (UPDRS) .
Hearing loss is one of the nonmotor features in PD that may precede motor impairment . The finding that α-synuclein is located predominately in the efferent neuronal system within the inner ear raises the possibility that α-synuclein dysfunction could play a role in susceptibility to noise-induced hearing loss or presbycusis . It is possible that the combined effect of the natural aging process and neurodegenerative changes intrinsic to PD might interfere with cochlear transduction mechanisms, thus anticipating presbycusis . Thus, evaluation of auditory function in PD is an important issue.
PI is one of the hallmarks of PD, even in the early stages of presentation. The inability to maintain balance predisposes affected patients to loss of equilibrium and falls . This is due to a dysfunction of postural reflexes, orthostatic hypotension, age-related sensory changes, and ability to integrate visual, vestibular, and proprioceptive inputs .
Researchers have reported that 38–68% of individuals with PD have fallen in the recent past and 13% fell more than once a week . Previous studies have found that balance impairment is a primary risk factor for falls . On the basis of these studies, accurate assessment of PI is a significant issue in the PD population.
| Patients and methods|| |
Fifty-five PD patients were examined; 24 of them were excluded for different reasons. Written consents were taken from all patients and approved by Al Azhar University medical committee. The remaining 31 patients were enrolled in this study with 31 healthy age-matched and sex-matched individuals taken as controls. In both cases and controls we excluded those with definitive ear diseases (e.g. tympanic perforation, chronic otitis media, or other causes of conductive hearing loss), other neurological diseases, or other medical disorders known to negatively affect the hearing function (such as cardiovascular diseases, metabolic diseases, autoimmune diseases, and diabetes). Among cases we excluded those with atypical parkinsonism such as multiple system atrophy, progressive supranuclear palsy, and corticobasal degeneration, as well as those with severe disability (stages IV and V).
All participants were examined at the Audiology Unit, El Hussein University Hospital. Cases were referred from the outpatient neurology clinic after examination by a neurologist. Controls were chosen from those accompanying patients attending the Audiology Unit, El Hussein Hospital, and from among spouses and other nongenetically related people accompanying PD patients.
PD patients were submitted to PD scaling (using UPDRS Section-III and H&Y Scale) and assessment of disease duration (DD) and of the most affected PD side (MAS-PD). Both groups were submitted to full history taking, otoscopic examination, basic audiological evaluation, neuro-otologic auditory brainstem response (ABR), and Sensory Organization Test.
Statistical analysis was conducted using range, mean, SD, and standard error for quantitative data, and numbers and percentage for qualitative data. We conducted χ2-tests, the Mann–Whitney test, the Npar test, and the Kruskal–Wallis test with SPSS, Chicago, IL, USA (version 17).
| Results|| |
Participants were divided into two groups: 31 patients with a clinical diagnosis of PD and 31 healthy age-matched and sex-matched controls ([Table 1]).
|Table 1: Pure-tone audiometry (right+left ears) thresholds at different frequencies in the two groups|
Click here to view
PD patients had significantly high pure-tone audiometry (PTA) thresholds at frequencies of 4000, 6000, and 8000 Hz ([Figure 1]).
|Figure 1: Correlation between pure-tone audiometry scores (right+left ears) and disease duration.|
Click here to view
There was a strong significant correlation between PTA scores and DD ([Table 2]).
|Table 2: Auditory brainstem response (right+left ears) wave latencies and interpeak latencies in the two groups|
Click here to view
There was statistically significant increase in wave V, high-repetition wave V peak latencies, and I–V and III–V interpeak latencies (IPLs) for PD patients in comparison with controls ([Table 3]).
|Table 3: Correlation between auditory brainstem response latencies (right+left ears) and age, disease duration, Hoehn and Yahr Scale, and Unified Parkinson’s Disease Rating Scale Section-III|
Click here to view
There was no correlation between wave I peak latency and DD, H&Y Scale, and UPDRS-III, but there was significant correlation between waves III and V, high-repetition wave V peak latency, and I–III, III–V, and I–V IPLs, and DD, H&Y Scale, and UPDRS-III. Also there was significant correlation between all waves and IPLs, and age ([Table 4]).
Composite, visual, and vestibular scores of the PD patients were significantly lower than those of controls. Somatosensory score of the PD patients was not significantly lower than that of controls, whereas the preferential visual score of the PD patients was significantly higher than that of controls ([Table 5]).
|Table 5: Correlation between composite scores and sensory ratios and age, disease duration, Hoehn and Yahr Scale, and Unified Parkinson’s Disease Rating Scale Section-III|
Click here to view
There was a strong significant negative correlation between composite, visual, and vestibular scores and age, DD, H&Y Scale, and UPDRS-III, with no correlation between somatosensory and preference scores and age, DD, H&Y Scale, or UPDRS-III.
| Discussion|| |
The median age at onset of PD is 60 years and the mean duration of the disease from diagnosis to death is 15 years . The patients’ ages in this study ranged from 42 to 76 years, and the mean age was 63.10±9.44 years.
Although good evidence exists that men are about 1.5 times more likely than women to develop PD, this difference is not the same across different studies. PD is not related to race or creed . Sex distribution in this study was 19 (61.3%) men versus 12 (38.7%) women.
In this study, mean DD was 7.10±4.02 years (range, 1–15 years). The mean overall UPDRS-III score was 14.10±8.42 (range, 3–30). The mean H&Y Scale was 1.77±0.62 (range, stages I−III). There was no statistically significant difference between male and female subgroups of PD patients as regards DD, UPDRS-III, and H&Y Scale. The MAS-PD was the left (19 cases), and then the right (12 cases), with no statistically significant difference between right and left.
In the present study, PD patients were reported to have significantly high PTA thresholds at frequencies of 4000, 6000, and 8000 Hz but not at hearing thresholds of lower frequencies of 250, 500, 1000, and 2000 Hz compared with controls, which is in agreement with the findings of Yýlmaz et al.  and Vitale et al. . Fradis et al.  reported no statistically significant difference in PTA results in 500–8000 Hz frequencies of PD patients compared with healthy controls. These discrepancies might be the result of the small size of the study populations in the study by Fradis et al. . In the current study, there was no correlation between PTA scores and sex or MAS-PD, but there was a strong significant correlation between PTA scores and other clinical demographic variables such as age, DD, UPDRS-III, and H&Y Scale at all frequencies, which is in agreement with the results of Vitale et al. .
α-Synuclein could be the link between hearing loss and PD . α-Synuclein is a 140-amino-acid protein that is the main component of Lewy bodies and are found in all patients with PD . Aggregation of α-synuclein is thought to be a key event in dopaminergic neuronal cell death in PD . The finding that α-synuclein is located predominately in the efferent neuronal system within the inner ear raises the possibility that α-synuclein dysfunction could play a role in susceptibility to noise-induced hearing loss or presbycusis . The localization of α-synuclein within the stria vascularis, also a well-known site of age-related hearing loss , supports this notion. It is possible that the combined effect of the natural aging process and neurodegenerative changes intrinsic to PD might interfere with cochlear transduction mechanisms, thus anticipating presbycusis .
ABR results showed a statistically significant increase in wave V peak latency and I–V and III–V IPLs with no statistically significant difference in waves I and III peak latencies or I–III IPL for PD patients in comparison with controls. Tachibana et al.  reported the same results. On the one hand, Gawel et al.  reported prolongation of wave V peak latency, which was also reported by Yýlmaz et al. , in addition to prolonged I−V IPL, whereas Alexa et al.  reported prolongation of II−V wave latencies and III–V IPL. On the other hand, Tsuji et al. , Chiappa , Prasher and Bannister , Vitale et al. , and Fabre et al.  have reported normal ABR results in patients with PD.
In this study, there was no statistically significant relation between ABR latencies and sex or MAS-PD. There was also no correlation between wave I peak latency and DD, UPDRS-III, and H&Y Scale, but there was a strong significant correlation between waves III and V peak latency, I–III, III–V, and I–V IPLs and DD, UPDRS-III, and H&Y Scale.
These results prove that the auditory nerve transmission is normal with a central conduction delay at the brainstem level in PD patients; this delay may be related to the neurodegenerative changes occurring in these patients . The strong correlation between waves III and V peak latencies and DD, UPDRS-III, and H&Y Scale, with no correlation between wave I peak latency and DD, UPDRS-III, and H&Y Scale, strengthens the notion: affection of PD is not peripheral but mainly on the brainstem. Also, dopamine deficiencies in PD may affect the autonomic nervous system in the form of disturbed thermoregulation and hypothermia; in turn, the hypothermia will increase the latency of ABR waves, especially later ones .
Results of Sensory Organization Test showed that the composite score of the PD population was significantly lower than that of controls, which is in agreement with McGuirk . The mean vestibular score of the PD patients was significantly lower than those of controls, which is in agreement with Jagielski et al. , while Pastor et al.  concluded that postural deficits in mildly or moderately affected PD patients are not explained by vestibular dysfunction. Although the vestibular system interacts with the basal ganglia indirectly through its input into the cerebellum and thalamus, then through polysynaptic pathways arriving at the sensory integration cerebral cortex, which then feeds forward into the basal ganglia, identification of vestibular dysfunction remains problematic in PD and it cannot be considered a nonmotoric sign of the disease process per se.
The mean visual score of the PD patients was significantly lower than those of controls, which is in agreement with McGuirk , and in contrast to the results of Bronstein et al. . Patients with PD may develop a range of visual problems during the course of the disease as dopamine is an important neurotransmitter in the retina and is present in amacrine cells and along the inner border of the inner nuclear layer, and may be involved in the organization of the ganglion cell and bipolar cell receptive fields and appears to modulate the physical activity of the photoreceptors. In addition, dopamine is involved in the coupling of the horizontal and amacrine lateral system .
The mean preferential visual score of the PD patients was significantly greater in comparison with controls, which is in agreement with Rinalduzzi et al. . Accordingly, PD patients will use the visual system more than other sensory systems when compared with a healthy population, which may represent a compensatory mechanism to the deficit of other sensory systems .
The mean somatosensory score of the PD patients was not significantly lower than that of controls, which is in agreement with McGuirk , whereas Maschke et al.  suggested that an intact corticobasal ganglion loop is essential for awareness of the limb position and that the basal ganglia play a selective role in kinesthesis (the conscious perception of active or passive motion and direction of movements); thus it is reasonable that in PD kinesthetic defects may impair the patients’ ability to perform postural responses ‘adequate’ to external perturbations, thereby contributing to PI.
There was strong significant negative correlation between composite, visual, and vestibular scores and age, DD, H&Y Scale, and UPDRS-III, with no correlation between somatosensory and preference scores and age, DD, H&Y Scale, or UPDRS-III.
| Conclusion|| |
PD patients are more affected by high-frequency, age-dependent unilateral or bilateral hearing loss compared with controls. Further, they may have hearing loss even in the absence of self-reported audiologic symptoms. PD affects the high brainstem region as it affects later waves of ABR. Although motor symptoms of PD tend to remain more severe at the side of initial involvement throughout the course of the disease, PD affects auditory function on both sides equally. PD affects vestibular and visual systems with over-reliance (excessive dependence) on the visual system. There is a strong significant correlation between degree of hearing loss, prolongation of waves III and V latency, I–III, III–V, and I–V IPLs, visual and vestibular scores, and PD severity and duration.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Hanato T, Hattori N. Etiology and pathogenesis of Parkinson’s disease. In: QayyumRana A, editor. Chapter one of text book etiology and psychophysiology of parkinson disease. Tokyo, Japan: InTech; 2011. 1–14.
Schapira AH, Jenner P. Etiology and pathogenesis of Parkinson’s disease. Mov Disord 2011; 26:1049–1055.
Pringsheim T, Jette N, Frolkis A, Steeves TDL. The prevalence of Parkinson’s disease: a systemic review and meta-analysis. Mov Disord 2014; 29:1583–1590.
Kasper DL, Fauci AS, Hauser S, Longo DL, Jameson JL, Loscalzo J. Parkinson’s disease and other movement disorders. In: Olanow CW. and Schapira A.H.V part 17, chapter 372, Harrison’s principles of internal medicine
. 18th ed. New York, NY: McGraw-Hill; 2015.
Olanow CW, Brundin P. Parkinson’s disease and alpha synuclein: is Parkinson’s disease a prion-like disorder? Mov Disord 2013; 28:31–40
Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W et al.
MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 2015; 30:1591–1601
Simuni T. Diagnosis and management of Parkinson’s disease. Medscape Neurol 2007; 1:10.
Frank C, Pari G, Rossiter JP. Approach to diagnosis of Parkinson disease. Can Fam Physician 2006; 52:862–868.
Hoehn M, Yahr M. Parkinsonism: onset, progression and mortality. Neurology 1967; 17:427–442.
Goetz CG, Poewe W, Rascol O, Sampaio C, Stebbins GT, Fahn S et al.
Movement Disorder Society Task Force on Rating Scales for Parkinson’s Disease The Unified Parkinson’s Disease Rating Scale (UPDRS): status and recommendations. Mov Disord 2003; 18:738–750.
Mehndiratta M, Garg RK, Pandey S. Nonmotor symptom complex of Parkinson’s disease-an under-recognized entity. J Assoc Physicians India 2011; 59:302–308.
Zhu X, Vasilyeva ON, Kim S, Jacobson M, Romney J, Waterman MS et al.
Auditory efferent feedback system deficits precede age-related hearing loss: contralateral suppression of otoacoustic emissions in mice. J Comp Neurol 2007; 503:593–604.
Benskey MJ, Perez RG, Manfredsson FP. The contribution of alpha synuclein to neuronal survival and function − Implications for Parkinson’s disease. J Neurochem 2016; 137:331–359.
Lee HK, Altmann LJ, McFarland N, Hass CJ. The relationship between balance confidence and control in individuals with Parkinson’s disease. Parkinsonism Relat Disord 2016; 26:24–28.
Jankovic J. Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry 2008; 79:368–376.
Wood BH, Bilclough JA, Bowron A, Walker RW. Incidence and prediction of falls in Parkinson’s disease: a prospective multidisciplinary study. J Neurol Neurosurg Psychiatry 2002; 72:721–725.
Rochester L, Hetherington V, Jones D, Nieuwboer A, Willems AM, Kwakkel G, Van Wegen E. Attending to the task: interference effects of functional tasks on walking in Parkinson’s disease and the roles of cognition, depression, fatigue, and balance. Arch Phys Med Rehabil 2004; 85:1578–1585.
Katzenschlager R, Head J, Schrag A, Ben-Shlomo Y, Evans A, Lees AJ, Parkinson’s Disease Research Group of the United Kingdom. Fourteen-year final report of the randomized PDRG-UK trial comparing three initial treatments in PD. Neurology 2008; 71:474–480.
Yýlmaz S, Karalý E, Tokmak A, Güçlü E, Koçer A, Oztürk O. Auditory evaluation in Parkinsonian patients. Eur Arch Otorhinolaryngol 2009; 266:669–671.
Vitale C, Marcelli V, Allocca R, Santangelo G, Riccardi P, Erro R et al.
Hearing impairment in Parkinson’s disease: expanding the nonmotor phenotype. Mov Disord 2012; 27:1530–1535.
Fradis M, Samet A, Ben-David J, Podoshin L, Sharf B, Wajsbort J et al.
Brainstem auditory evoked potentials to different stimulus rates in parkinsonian patients. Eur Neurol 1988; 28:81–186.
Lee VM, Trojanowski JQ. Mechanisms of Parkinson’s disease linked to pathological alpha-synuclein: new targets for drug discovery. Neuron 2006; 52:33–38.
Spicer SS, Schulte BA. Pathologic changes of presbycusis begin in secondary processes and spread to primary processes of strial marginal cells. Hear Res 2005; 205:225–240.
Tachibana H, Takeda M, Sugita M. Short-latency somatosensory and brainstem auditory evoked potentials in patients with Parkinson’s disease. Int J Neurosci 1989; 44:321–326.
Gawel MJ, Das P, Vincent S, Rose FC. Visual and auditory evoked responses in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 1981; 44:227–232.
Alexa D, Alexa L, Popa L, Paduraru DN, Igant B, Constantinescu A et al.
Brainstem auditory evoked potentials in Parkinson’s disease patients. Rom J Neurol 2013; XII:198–201.
Tsuji S, Muraoka S, Kuroiwa Y, Chen KM, Gajdusek CD. Auditory brainstem evoked response (ABSR) of Parkinson-dementia complex and amyotrophic lateral sclerosis in Guam and Japan (author’s transl). Rinsho Shinkeigaku 1981; 21:37–41.
Chiappa KH. Short-latency somatosensory evoked potentials: methodology. In: Chiappa K II editor. Evoked potential in clinical medicine. New York, NY: Raven Press; 1983. 204–313.
Prasher D, Bannister R. Brain stem auditory evoked potentials in patients with multiple system atrophy with progressive autonomic failure (Shy-Drager syndrome). J Neurol Neurosurg Psychiatry 1986; 49:278–289.
Fabre LA, Loyola JGG, Montiel HLH, Montiel CH, Martinez LM, Malagon GV, Valdes RFR. Brainstem auditory evoked potentials in Parkinson’s disease. Mexican J Neurol 2015; 16:14–20.
Norrix LW, Trepanier S, Atlas M, Kim D. The auditory brainstem response: latencies obtained in children while under general anesthesia. J Am Acad Audiol 2012; 23:57–63.
McGuirk TE. The use of computerized dynamic posturography to assess the balance in individuals with Parkinson’s disease [thesis]. Richmond, VA: Virginia Commonwealth University Scholars Compass; 2005.
Jagielski J, Kubiczek-Jagielska M, Sobstyl M, Koziara H, Błaszczyk J, Zabek M, Zaleski M. Posturography as objective evaluation of the balance system in Parkinson’s disease patients after neurosurgical treatment. A preliminary report. Neurol Neurochir Pol 2006; 40:127–133.
Pastor MA, Day BL, Marsden CD. Vestibular induced postural responses in Parkinson’s disease. Brain 1993; 116(Pt 5):1177–1190.
Bronstein AM, Hood JD, Gresty MA, Panagi C. Visual control of balance in cerebellar and parkinsonian syndromes. Brain 1990; 113(Pt 3):767–779.
Armstrong RA. Visual symptoms in Parkinson’s disease. Parkinsons Dis 2011; 2011:908306.
Rinalduzzi S, Trompetto C, Marinelli L, Alibardi A, Missori P, Fattapposta F et al.
Balance dysfunction in Parkinson’s disease. Biomed Res Int 2015; 2015:434683.
Vaugoyeau M, Viel S, Assaiante C, Amblard B, Azulay JP. Impaired vertical postural control and proprioceptive integration deficits in Parkinson’s disease. Neuroscience 2007; 146:852–863.
Maschke M, Gomez CM, Tuite PJ, Konczak J. Dysfunction of the basal ganglia, but not the cerebellum, impairs kinaesthesia. Brain 2003; 126:2312–2322.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]