|
 
 |
| ORIGINAL ARTICLE |
|
| Year : 2019 | Volume
: 25
| Issue : 2 | Page : 90-96 |
|
Central auditory function in multiple sclerosis patients
Reem Elbeltagy1, Nahla Hassan Gad2, Mohamed Hamdy Ismail3
1 Department of ENT, Audio-Vestibular Medicine, Faculty of Medicine, Zagazig University, Zagazig, El Sharkia, Egypt; Department of Audiology and Balance, College of Health and Rehabilitation Science, Princess Nourah Bint Abdulrahman University, Riyadh, KSA
2 Department of ENT, Audio.Vestibular Medicine, Faculty of Medicine, Zagazig University, Zagazig, El Sharkia, Egypt
3 Department of Neurology, Faculty of Medicine, Zagazig University, Zagazig, El Sharkia, Egypt
| Date of Web Publication | 16-Aug-2019 |
Correspondence Address:
Dr. Reem Elbeltagy
Department of ENT, Audio-Vestibular Medicine, Faculty of Medicine, Zagazig University, Zagazig, El Sharkia
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/indianjotol.INDIANJOTOL_80_18
Objectives: To evaluate central auditory functions in multiple sclerosis (MS) patients. Subjects and Methods: Twenty Egyptian MS patients involved in the study and 20 healthy controls who were matched to MS group in age, gender, and literacy. They ranged in age from 30 to 50 years with a mean age 37.6 ± 5 in the study group versus 37.3 ± 4.2 in the control group. In this study, four screening tests were conducted for the assessment of central auditory processing: Gaps In Noise test (GIN), Arabic dichotic digits test (DDT), Pitch Pattern Sequence test (PPS), and last Arabic Speech In Noise test (SPIN). Results: The study showed elevated GIN test approximate threshold and depressed total score in MS patients compared to the control group, with no significant difference between both right and left ears. There was statistical significant depressed scores in study groups at PPS, speech intelligibility in noise, and DDTs. Conclusion The findings of the current study add more evidence to the involvement of central auditory processing abilities in patients with MS. The assessment of central auditory function is highly recommended for all MS patients as a routine examination and can be used for monitoring the effectiveness of medication and related therapies for these patients.
Keywords: Behavioral tests, central auditory function, multiple sclerosis
How to cite this article:
Elbeltagy R, Gad NH, Ismail MH. Central auditory function in multiple sclerosis patients. Indian J Otol 2019;25:90-6 |
| Introduction | |  |
Multiple sclerosis (MS) is a chronic inflammatory demyelinating disease affecting the central nervous system (CNS). Disseminated neurological symptoms caused by acute and chronic inflammation include loss or alteration of sensation (numbness, paresthesia), of motor function (typically spastic paresis or complete paralysis), visual symptom such as blurring of vision, transient blindness, disorder of conjugate eye movements, bladder, bowel dysfunction, and cognitive impairment. MS patients require enduring medical and rehabilitative care. Fatigue is one of the most common symptoms reported by patients with MS, which is reported to affect between 50% and 80% of patients.[1]
The diagnosis of MS is based on representing evidence of inflammatory-demyelinating harm within the CNS that is disseminated in both time and space. Diagnosis is through a combination of the clinical history, neurologic examination, magnetic resonance imaging, and the exclusion of other diagnostic possibilities. Other so-called “para-clinical” tests, including the examination of the cerebrospinal fluid, the usage of evoked potentials, urodynamic studies of bladder function, and ocular coherence tomography, may be helpful in forming the diagnosis of MS, but are often unnecessary.[2]
MS is characterized by episodes (“attacks” or “relapses”) of neurologic dysfunction. The symptoms caused by these attacks vary significantly between patients and depend on the site of neurologic involvement. Commonly, patients may complain of numbness, tingling, weakness, vision loss, gait impairment, incoordination, imbalance, and bladder dysfunction. Between these attacks, in the relapsing-remitting (RR) phase of the illness, patients are neurologically stable.[3]
Many patients who begin with RRMS progress to the secondary progressive phase of the illness, in which they have marked worsening of function and increasing of neurologic disability not related to any acute attacks that may or may not occur. About 66% of RRMS patients developed SPMS at an average time of 15 years,[4] while in a British Columbia cohort study, 58% of patients with relapsing MS advanced to SPMS after an average time of 19.1 years.[5]
About 10%–20% of the patients experience a clinical course of primary progressive (PP) MS, in which they started by insidious deterioration and never have acute relapses. About 5% of the PPMS patients can experience clinical episodes and now this type is known as progressive relapsing MS.[3]
Central auditory processing could be affected in MS patients. Difficulty in speech perception in background noise was reported by many researches.[6] Temporal resolution, dichotic listening, and performance with competing acoustic signals were evaluated in these patients through gaps in noise (GIN) test, dichotic digits test (DDT) (both versions), and speech in noise for adults (respectively).
A gap in noise test is a simple sensitive test for temporal resolution ability. It has a sensitivity of 67%, a specificity of 94%, and a high test–retest reliability, which is important for the clinical use of the test.[6] Temporal resolution ability is the ability to follow rapid changes in a sound over time which is very important in speech perception. It is one of central auditory abilities through which the central pathway till auditory cortex could be assessed.
Dichotic listening is another central auditory ability that could assessed through many psychological tests. One of them is DDT which has two versions; the first is two digit one in each ear while the second version consisted of four digits two in each ears. It investigates the integration of binaural inputs within the auditory system. Specifically, it is a behavioral test for hemispheric lateralization of speech sound perception.[7] The main object of this study was to evaluate the central auditory function in MS patients.
| Subjects and Methods | | |
Subjects
A descriptive case–control study in which a group of 20 Egyptian MS patients of both genders involved in the study and 20 apparently healthy controls who were matched to MS group in age, gender, and literacy. They ranged in age from 30 to 50 years. MS patients were recruited from neurology department to Audio-Vestibular Medicine Unit, ORL Department, Zagazig University.
All particpants attained the following criteria:
- Age between 30 and 50 years
- RR MS type
- Expanded disability severity scale of the patients <6.
Exclusion criteria:
- Any other neurological and otological disorders
- History of cranial and otological operation
- History of ototoxic, sedative, and hypnotic drugs.
Patients divided into two age-matched subgroups:
- Study group (n = 20) MS patients
- Control group (n = 20) normal age-matched individuals.
Equipment and materials
Basic audiological evaluations included
- Pure-tone audiometry using orbiter 922 (GM Otomtrix, Denmark): this included air conduction (air conduction hearing thresholds were determined by frequency range 0.250 and 8 K Hz) and bone conduction (bone conduction hearing thresholds were determined by frequency range 0.500 and 4 K Hz). Hearing thresholds >25 dB were considered as HL
- Speech audiometry (speech reception threshold [SRT] using Arabic spondee words)[8] and the word discrimination scores using Arabic phonetically balanced words[9]
- Immittancemetry using Amplaid 724 (Amplifon, Italy). This included tympanometry and acoustic reflex threshold measurement (ANSI, 1969).[10]
The audiometer was connected to dual channel audiocassette and CD player to deliver the recorded materials for central auditory testing. Audio tapes of screening central auditory tests included an Arabic version of DDT[11] and an Arabic version of speech intelligibility in noise (SPIN) test for adults.[12] Moreover, a CD for GIN test was used.[6] Individuals were examined in a sound-treated booth, and test stimuli were presented through TDH-39 headphones.
Procedures
Examinations required about 2 h in one day (breaks may be in between to avoid expected patient's fatigue could possibly influence results while testing).
The study started with detailed history taking including personal history, history of hearing loss, tinnitus, discharge, earache, headache or vertigo, past history of systemic disease, physical trauma, ototoxic drug or previous operations, and family history followed by an otoscopic examination of the external auditory canal and tympanic membraneand the basic audiological evaluation.
Assessment with screening tests for central auditory processing
Gaps in noise test
The GIN test contained four lists: only list 1 and 2 are used, one list for each ear randomly. The list contained six-second white noise segments with each segment contained zero to three mute gaps lasting 2, 3, 4, 5, 6, 8, 10, 12, 15, or 20 ms. Each gap's duration was repeated six times with a total gaps number of 60 within the list. Ten segments were used as practice before the test.[6] The list presented monaurally at 50 dBSL through a single channel. The second channel was connected to a bone vibrator at an intensity of −10 dBSL. This channel was needed to give the examiner clue about the incidence of gaps. The test required about 10 min to be completed in each ear. All participants were instructed to raise one hand each time the gap was detected. The results of GIN test included the approximate gap detection threshold (the shortest gap's duration that was detected at least four times) and the percentage of correct score detections out of the 60 gaps presented for each ear.
Arabic speech intelligibility in noise test
Twenty-five monosyllabic words were heard in a noisy background at 5 dB signal to noise ratio. Both sentence and its noise were applied monaurally at a level of 50 dBSL (referenced to SRT). Scoring included the percentage of correctly recognized words for each ear separately.[12]
Pitch pattern sequence test
This test included 30 items: each of them had a paradigm of three tones. Each paradigm contained two different patterns of frequencies (high [1122 Hz] and low [880 Hz]). All items were presented monaurally at 50 dBSL (referenced to SRT). The percentage of correct responses calculated for each ear apart.[13]
Arabic dichotic digits test
It consists of two subtests: the first subtest consisted of 20 items that were presented at 50 dBSL (referenced to SRT). Each item of the first subtest contains two digits that were presented simultaneously as one for each ear, whereas the second subtest consisted of 40 items in which four digits are applied simultaneously as a pair of digits for each ear. Scoring based on the percentage of correct responses for each ear, which are 20 and 40 for the first and second subtests, respectively.[11]
Ethical consideration
In the present study, all the testing procedures were performed using noninvasive techniques and adhering to the conditions of the ethical approval committee of the institute. All participants were given their written consent form before participating in the study.
Statistical analysis
Data was analyzed using Statistical Package of Social Science (SPSS), software version 24.0 (SPSS Inc., 2016), Chicago, Illinois, USA. Continuous variables were presented as the mean ± standard deviation or median (range). Categorical variables were presented by the count and percentage. Normality was checked by a Kolmogorov–Smirnov test. Independent-samples t-test is used to determine if a difference exists between the means of two independent groups on a continuous dependent variable. Mann–Whitney U-test is a non-parametric alternative to independent-samples t-test. Wilcoxon–signed-rank test (nonparametric alternative to paired t-test) is used to compare two sets of data that come from the same participants. Chi-squared test of association is used to discover if there is a relationship between two categorical variables. The differences were considered significant at P < 0.05. All statistical comparisons were two-tailed.
| Results | | |
Baseline characteristics of the control and patient groups
Ages ranged between 20 and 50 years with a mean age of control group 37.3 ± 4.2 and 37.6 ± 5 of the study group. They were 12 females (60%) and 8 males (40%) in the control group, and in the study group, it was 17 females (85%) and 3 males (15%). Baseline characteristics (age and sex) were similar between the control and patient groups (P > 0.05) as shown in [Table 1].
Gap in noise test and total gap in noise scores of the control group versus patient group
Patients had highly statistically significantly lower GIN total correct scores and total GIN Scores in both ears than the control group (P < 0.001). Comparing right ears with left ears, GIN total correct scores and total GIN scores were statistically significantly similar in both ears in controls and cases (P > 0.05) as shown in [Table 2] and [Figure 1]. | Table 2: Gap in noise test and total gaps in noise scores of the control group versus patient group
Click here to view |
 | Figure 1: Box-and-whisker plot of gaps in noise approximate threshold in the control group versus patient group
Click here to view |
Gap in noise approximate threshold of the control group versus patient group
Patients had highly statistically significantly higher GIN approximate threshold in both ears than the control group (P < 0.001). Comparing right ears with left ears, GIN approximate threshold was statistically significantly similar in both ears in controls and cases (P > 0.05) as shown in [Table 3] and [Figure 1]. | Table 3: Gaps in noise approximate threshold of the control group versus patient group
Click here to view |
Speech intelligibility in noise test of the control group versus patient group
Patients had statistically significantly lower SPIN test in both ears than the control group (P < 0.001). Comparing right ears with left ears, SPIN test was statistically significantly similar in right and left ears in cases (P > 0.05) as shown in [Table 4] and [Figure 2]. | Table 4: Speech intelligibility in noise test of the control group versus patient group
Click here to view |
 | Figure 2: Box-and-whisker plot of speech intelligibility in noise test in the control group versus patient group
Click here to view |
Pitch pattern sequence test of the control group versus patient group
Patients had statistically significantly lower pitch pattern sequence (PPS) test in both ears than the control group (P < 0.001). Comparing right ears with left ears, PPS test was statistically significantly similar in both ears in controls and cases (P > 0.05) as shown in [Table 5]. | Table 5: Pitch pattern sequence test of the control group versus patient group
Click here to view |
Dichotic digits test (version 1 and version 2) of the control group version patient group
Patients had statistically significantly lower DDT % (version 1 and version 2 in both ears) than the control group (P < 0.05). Comparing right ears with left ears, DDT% (version 1 and version 2) was statistically significantly higher in right ears than left ears in controls and cases (P < 0.05) as shown in [Table 6]. | Table 6: Dichotic digits test (version 1 and version 2) of the control group versus patient group
Click here to view |
| Discussion | | |
It is known that the auditory system consists of a peripheral and central part; there is a series of connection between both parts that allows processing of the signal sound from peripheral to the central part. Any disruption of these signal will diminish the reception of the information.[14]
In this study, ages ranged between 20 and 50 years with a mean age of control group 37.3 ± 4.2 and 37.6 ± 5 of the study group. They were 12 females (60%) and 8 males (40%) in the control group, and in the study group, it was 17 females (85%) and 3 males (15%). Baseline characteristics were similar between the control and patient groups [Table 1].
In the present study, the approximate threshold and percent of correct answers of GIN test were significantly higher in MS patients than the normal individuals Table and [Figure 1], a similar result was reported by El-Zarea et al.[15] who reported elevated threshold and reduction of the percent of correct answer obtained from GIN test in MS Egyptian patients.
Furthermore, Valadbeigi et al.[16] evaluated 52 individuals – 26 apparently healthy controls and 26 patients with MS. Both groups were matched in age and gender. They observed a significant difference in GIN test between the two groups. Also, the current result is consistent with the study conducted by Rappaport et al.[17] They founded 40% of patients with MS had abnormal performance in GIN test.
Another study conducted in 2005, in which GIN test was studied in 50 healthy controls and 18 patients complaining of significant lesions in central auditory processing system; results showed that the average approximate threshold in the right ear was 8.5 ms and 7.8 for the left ear that indicated weaker performance of temporal resolution in people with auditory processing disorder.[6]
Sanches et al.[18] studied the GIN test on 44 normal hearing individuals with and without tinnitus. They concluded that there was a significant difference between the two groups in detection thresholds and duration interval. They explained their result as tinnitus can damage the cochlea causing a series of changes in the central auditory system that lead to lack of afferent information.
On the other hand, there was a non-significant difference between the right and left ear in both groups [Table 3] and [Figure 1]. This is matched with previous studies of Valadbeigi et al.[16] and Samelli and Schochat.[19]
According to the results of the GIN test, it became obvious that MS patients are likely to have a poor temporal resolution performance.
MS patient revealed no problem with word discrimination in the quiet environment. However, there was a significant difference in word discrimination in noise environment as observed in the SPIN test. Comparing right ears with left ears, SPIN test was statistically significantly similar in the right and left ears in MA patient [Table 4] and [Figure 2]. This result matched to the study of El-Zarea et al.;[15] they studied WD in quiet and in noise, and they observed a significant difference between WD in both conditions. They explained this difference due to MS disease that may affect any part of CNS. The auditory system and integrity of auditory nerve may be affected as a part of the CNS. Furthermore, basal ganglia, cerebral cortex, and cerebellum may be affected in MS patient as reported by Mauk and Buonomano.[20]
Speech is considered as one of the most complex pattern recognitions which requires normal temporal and spatial processing function.[15] Hence, the affection of the central processing system, mainly in ordering pattern, temporal resolution, and word discrimination that occur in MS patient may be the cause of different speech disorders such as dyslexia, speech with low speed, vague and difficult speech production and understanding.[21] About 40%–55% of MS patients have speech disorders as reported by Klugman and Ross.[22] Furthermore, demyelination of many pons structures such as the superior olives and inferior colliculi can occur, both are responsible for processing speech in noise.[16]
MS patients had statistically significantly lower PPS test in both ears than control group, comparing right ears with left ears; PPS test was statistically significantly similar in both ears in controls and cases [Table 5] and [Figure 3]. Furthermore, El-Zarea et al.[15] who studied different auditory memory domains reported a significant difference between MS patients and their control group; the most significant difference was in sequence memory. Musiek[23] reported that some MS patient can perform well humming, but not verbally in frequency pattern test; he refers that problem to deficits in the interhemispheric transfer. | Figure 3: Box-and-whisker plot of pitch pattern sequence test in the control group versus patient group
Click here to view |
In the current study, MS patient had statistically significant lower dichotic digit test percentage (version 1 and version 2 in both ears) than the control group. A significant difference between the right and left ears was observed in MS patient in DDT [Table 6]. Also, El-Zarea et al.[15] and Musiek et al.[24] found that a significant number of MS patients showed abnormalities on DDT test. DDT test was considered as one of the most important tests for detecting CAP in MS patients.
Jacobson et al.[25] reported that the abnormalities in dichotic listening may be increased in MS patients because about 10% of MS patients had abnormalities on the Staggered Spondaic Word, 25% had abnormal results on the Synthetic Sentence Inventory–Ipsilateral Competing Message in addition to 80% exceeded the norm for a right-ear advantage on the Dichotic Consonant-Vowel Nonsense Syllable test (Kresge Hearing Research Laboratory South). In another study conducted by Hendler et al.,[26] they studied dichotic listening and gap detection thresholds in CAP patients; they observed abnormal MLD findings and elevated gap-detection thresholds in 13% of the patients.
Myelin sheath covers the nerve fibers and protects them. Furthermore, it allows the conduction of electrical impulses to and from the brain; so, if it is damaged, the conductivity of nerve impulses will be disrupted. The deficit of dichotic listening occurs in MS patients could be attributed to demyelination of corpus callosum which is considered as a highly myelinated structure. Transmission of the signal between the cerebral hemispheres through the corpus callosum is important for dichotic listening.[25]
From all previous results, it becomes clear that MS had clear impacts on central auditory processing functions such as temporal resolution, sequence memory, and speech discrimination in noise. Hence, it is very important for all patients complaining of MS.
| Conclusion | | |
The findings of the current study add more evidence to the involvement of central auditory processing abilities in patients with MS. Central auditory processing assessment is highly recommended for all MS patients as a routine examination and can be used for monitoring the effectiveness of medication and related therapies for these patients.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Lerdal A, Celius EG, Krupp L, Dahl AA. A prospective study of patterns of fatigue in multiple sclerosis. Eur J Neurol 2007;14:1338-43.  |
| 2. | Polman CH, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald criteria”. Ann Neurol 2005;58:840-6. |
| 3. | Lublin FD, Reingold SC. Defining the clinical course of multiple sclerosis: Results of an international survey. National Multiple Sclerosis Society (USA) Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology 1996;46:907-11. |
| 4. | Scalfari A, Neuhaus A, Daumer M, Muraro PA, Ebers GC. Onset of secondary progressive phase and long-term evolution of multiple sclerosis. J Neurol Neurosurg Psychiatry 2014;85:67-75. |
| 5. | Tremlett H, Yinshan Z, Devonshire V. Natural history of secondary-progressive multiple sclerosis. Mult Scler 2008;14:314-24. |
| 6. | Musiek FE, Shinn JB, Jirsa R, Bamiou DE, Baran JA, Zaida E, et al. GIN (Gaps-in-noise) test performance in subjects with confirmed central auditory nervous system involvement. Ear Hear 2005;26:608-18. |
| 7. | Ingram-John CL. Neurolinguistics: An Introduction to Spoken Language Processing and its Disorders. 3 rd ed. Cambridge: Cambridge University Press; 2007. p. 381. |
| 8. | Soliman S. Speech discrimination audiometry using - Arabic Phonetically-Balanced Words. Ain Shams Medical Journal 1976;27:27-30. |
| 9. | Soliman S, Fathalla A, Shehata W. Development of the Arabic Staggered Spondaic Words (SSW) Test. Proceedings of the 8th Annual Ain Shams Congress 1985;2:1220-46. |
| 10. | American National Standard Acoustical Terminology. American National Standards Institute X3L2 Committee Records (ANSI1969). New York: American National Standard Acoustical Terminology; 1969-1975. |
| 11. | Tawfik S, Abdel-Maksoud A, Weiheha H. Standardization of two Binaural Dichotic Digits and Dichotic Rhyme Tests on Normal Children, Unpublished Master Thesis. Egypt: Ain Shams University; 2008. |
| 12. | Tawfik S, Shalaby A. Development and Standardization of Arabic Central Test Battery for Children. Proceeding of XXIII World Congress of the International Association of Logopedics and Phoniatric; 1995. p. 416-9. |
| 13. | Pinheiro M, Patcek P. Reversals in the perception of noise and tone patterns. J Acoust Soc Am 1971;49:1178-82. |
| 14. | Magnano I, Aiello I, Piras MR. Cognitive impairment and neurophysiological correlates in MS. J Neurol Sci 2006;245:117-22. |
| 15. | El-Zarea GA, Shalaby AA, Hussin HM, Ali1 MS. evaluation of central auditory processing in Egyptian multiple sclerosis patients. EJHM 2018;71:3667-75. |
| 16. | Valadbeigi A, Weisi F, Rohbakhsh N, Rezaei M, Heidari A, Rasa AR, et al. Central auditory processing and word discrimination in patients with multiple sclerosis. Eur Arch Otorhinolaryngol 2014;271:2891-6. |
| 17. | Rappaport JM, Gulliver JM, Phillips DP, Van Dorpe RA, Maxner CE, Bhan V, et al. Auditory temporal resolution in multiple sclerosis. J Otolaryngol 1994;23:307-24. |
| 18. | Sanches SG, Samelli AG, Nishiyama AK, Sanchez TG, Carvallo RM. GIN test (Gaps-in-noise) in normal listeners with and without tinnitus. Pro Fono 2010;22:257-62. |
| 19. | Samelli AG, Schochat E. Study of the right ear advantage on gap detection tests. Braz J Otorhinolaryngol 2008;74:235-40. |
| 20. | Mauk MD, Buonomano DV. The neural basis of temporal processing. Annu Rev Neurosci 2004;27:307-40. |
| 21. | White CP, White MB, Russell CS. Invisible and visible symptoms of multiple sclerosis: Which are more predictive of health distress? J Neurosci Nurs 2008;40:85-95, 102. |
| 22. | Klugman TM, Ross E. Perceptions of the impact of speech, language, swallowing, and hearing difficulties on quality of life of a group of South African persons with multiple sclerosis. Folia Phoniatr Logop 2002;54:201-21. |
| 23. | Musiek F. The frequency pattern test: A guide. Hear J 2002;55:8. |
| 24. | Musiek FE, Gollegly KM, Kibbe KS, Reeves AG. Electrophysiologic and behavioral auditory findings in multiple sclerosis. Am J Otol 1989;10:343-50. |
| 25. | Jacobson JT, Deppe U, Murray TJ. Dichotic paradigms in multiple sclerosis. Ear Hear 1983;4:311-7. |
| 26. | Hendler T, Squires NK, Emmerich DS. Psychophysical measures of central auditory dysfunction in multiple sclerosis: Neurophysiological and neuroanatomical correlates. Ear Hear 1990;11:403-16. |
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]
|
Users Online: 250
Search Pubmed for