Impacts of ventriculoperitoneal shunt on hearing threshold and speech discrimination among hydrocephalic children
Marwa Abdelhafeez1, Reem Elbeltagy2
1 Department of Otorhinolaryngology, Faculty of Medicine, Minia University, Minia, Egypt
2 Department of Otorhinolaryngology, Audiovestibular Medicine, Faculty of Medicine, Zagazig University, Zagazig, Egypt; Department of Health Communication sciences. College of Health and Rehabilitation Sciences, Princess Nourah bint Abdulrahman University, KSA
Correspondence Address:
Dr. Marwa Abdelhafeez
Department of Otorhinolaryngology, Faculty of Medicine, Minia University, Minia
Egypt
Source of Support: None, Conflict of Interest: None
CheckDOI: 10.4103/indianjotol.indianjotol_107_22
Purpose: The purpose of this study was to determine the prevalence of hearing loss (HL) in children with hydrocephalus (HCP) and to assess the impact of the ventriculoperitoneal (VP) shunt on their hearing threshold and speech discrimination percentage. Methodology: This was a case–control study. A total of 20 children who experienced HCP and 20 healthy controls were recruited. All participants in the study were subjected to a systematic clinical examination including otomicroscopic, audiometric (Pure-tone audiometry and speech audiometry), and tympanometric examination before and after VP shunt. Results: The mean age ± standard deviation for the HCP children and the control group was 5.4 ± 0.994 and 5.8 ± 1.196 years, respectively. The prevalence of HL in hydrocephalic children was 40%, and they had raising mild-to-moderate sensorineural HL. Children with HCP (preoperative) had a statistically significantly higher pure-tone threshold at 250, 500, 1000, 2000, and 4000 Hz than the control group. They also had a statistically significantly lower speech discrimination percentage than the control group. There was a statistically significant difference between the preoperative and the postoperative groups in pure-tone thresholds at 250, 500, 1000, and 2000 Hz. There is also a statistically significant difference between the preoperative and the postoperative groups in speech discrimination percentage. Conclusion: Early diagnosis in children with HCP is important. The results of the current study add further evidence of hearing impairment in hydrocephalic children and improvement in hearing after shunt operation. Auditory assessment is highly recommended for all hydrocephalic children as a routine examination.
Keywords: Hydrocephalus, sensorineural hearing loss, speech discrimination, ventriculoperitoneal shunt
Hydrocephalus (HCP) is not defined as an isolated disease but rather as a clinical condition. Specifically, it is an imbalance between the production and absorption of cerebrospinal fluid (CSF) and/or obstruction of the CSF circulation pathway due to enlargement of the ventricles, which often creates high intracranial pressure (ICP) syndrome.[1] HCP is an important health issue, with a reported prevalence of 0.5–2/1000 pregnancies worldwide. It is estimated that over 300,000 cases occur worldwide each year.[2]
Proper inner ear function depends on a delicate balance between the fluids of the inner ear. It is believed that symptoms may arise due to the pressure difference between endolymph and perilymph, which leads to deformation of the neural bearing membranes and, thus, to system dysfunction.[3] The literature reports sensorineural hearing loss (SNHL) in patients with HCP, and the proposed mechanism is that increased ICP is transmitted to the perilymph via the cochlear aqueduct resulting in relative perilymphatic hydrops. This hydrodynamics leads to SNHL.[4] One of the documents supporting the presence of SNHL associated with HCP is the case report of Sammons et al.[5] They report a patient with HCP and SNHL who experienced resolution of SNHL after the insertion of a ventriculoperitoneal (VP) shunt.
Furthermore, a study by Barlas et al.[6] described bilateral low-frequency SNHL that resolved after shunt placement. Another study found that 68.75% of patients with HCP have SNHL, and this increase in threshold may reflect a neurological condition rather than peripheral hearing loss (HL).[7]
Early diagnosis and treatment of HCP and its associated HL is crucial. Because HL can affect speech and language development, even mild HL can affect academic achievement and cause psychological and social problems.[8] The development of the maximum level of hearing and communication skills in infants is essential for the development of the nervous system. During the 1st year of life, billions of basic neural connections are formed and neurons in the auditory brainstem mature. At this time, the thalamus and auditory brainstem are just beginning to connect to the auditory cortex. Interruption of sensory input into the auditory nervous system leads to disruption of the functional properties of neurons and the morphology of the central auditory system.[9]
The standard treatment for HCP is the insertion of a shunting device, which helps remove excess CSF and maintain more normal ICP. VP shunting is the preferred procedure because the incidence of serious complications is lower.[10] The mechanism of HL after loss of CSF and VP bypass surgery is largely unknown, but it is suspected that the cochlear duct is the source of pressure change in the inner ear. Decreased CSF pressure can cause the cochlear endolymph to expand through the open cochlear aqueduct, although evidence remains insufficient.[11],[12]
Karabağli et al. report on a pediatric patient with HCP and bilateral SNHL whose ICP range dropped to normal levels after a series of surgeries. The study of Karabağli et al. highlights that the intracochlear pressure can be reduced by treating the increased CSF pressure and that SNHL can be reversed.[13]
Since there are few studies on the role of the VP shunt on hearing threshold and speech discrimination percentage in children with HCP, the present study was conducted to determine the prevalence of HL in children with HCP and to assess the impact of the VP shunt on their hearing threshold and speech discrimination percentage.
MethodologyStudy design and subjects
This was a descriptive case–control study, which involved a group of 20 children with HCP of both sexes and 20 apparently healthy children (control group), who were matched to the hydrocephalic group by age, sex, and literacy. Their age ranged from 4 to 8 years. Hydrocephalic children were recruited from the neurology department to the otorhinolaryngology department of the university hospital.
Inclusion criteria
Children between the ages of 4 and 8 yearsChildren with good reliability during hearing assessmentThe presence of macrocephaly (head circumference >97th percentile) plus ventriculomegaly or, progressive enlargement of the ventricles, even if the head was not macrocephalicSigns of increased intracranial pressure in the presence of ventriculomegaly as confirmed by computed tomography (CT).Exclusion criteria
Any children with neurodegenerative diseases that may cause HL or intracranial space-occupying lesions, intracranial hemorrhage, malformations, or other pathological findings were excluded from the study. Furthermore, HCP developing secondary to midline defects such as myeloschisis, meningocele, myelomeningocele, and encephalocele, low Apgar score at birth, meconium aspiration, and cranial trauma due to forceps/vacuum use at birth were excluded from the studyAny children with a chronic middle ear infection (e.g., chronic suppurative otitis media and cholesteatoma)Any children with poor reliabilityAny children using a hearing aid to reduce the variability between childrenAny children have had language problem or learning disability that may affect their speech tests.Procedure
All participants in the study were subjected to the following:
Full history takingPersonal history (age, name, and sex)History of HL, tinnitus, discharge, earache, and headacheHistory of increased intracranial pressure symptoms (headache and vomiting)Past history of systemic disease, physical trauma, acoustic trauma, ototoxic drug, and operationsFamily history of congenital diseaseOtological examination: preauricular region, ear pinna, postauricular region, and tympanic membraneImmittancemetry: using Amplaid 724 (Amplifon, Italy) including tympanometry and acoustic reflex threshold measurementAudiometric examinationPure-tone audiometry using orbiter 922 GM Otomtrix, Denmark:Air conduction: Air conduction hearing thresholds were determined by the frequency range of 0.250 and 8K HzBone conduction: Bone conduction hearing thresholds were determined by the frequency range of 0.500 and 4K HzHearing thresholds >20 dB were considered HLSpeech audiometry: Speech reception threshold[14] using the Arabic spondee words and the word discrimination scores using Arabic phonetically balanced words[15]A comprehensive audiological assessment was performed. All children were taught to play a listening game, such as putting a peg in a board, when they heard a soundAll children were taught to repeat the words that they listened while performing speech testExaminations required about 3 h in 1 day. Serial evaluations were performed to develop reliable assessment of hearing thresholdsAll hydrocephalic children in the study group were evaluated twice: 1 week before surgery (preoperative group) and 3 months after surgery (postoperative group)All audiological evaluations were performed under the same condition and using the same equipmentThe hearing thresholds exceeded 20 dB; it was considered HL.[16]Ethical consideration
All ethical considerations were fulfilled prior to the study. Ethical approval has been requested from the university hospital research center. Agreement with written knowledgeable consent was gained from the children's parents or caretakers for children's participation in this study. The consent form contained the objectives of the study, the steps in carrying it out, and its risks and benefits. Furthermore, the confidentiality of data was guaranteed by the signing of the confidentiality agreement by the researchers.
Statistical analysis
The data were analyzed using the Statistical Package for the Social Sciences (SPSS) for Windows (version 24.0; IBM Corp, Armonk, NY, USA.). Continuous variables were presented as the mean, standard deviation (SD), and range. Discrete variables were presented by the count and percentage. The independent-samples t-test was used to determine if a difference exists between the means of two independent groups (preoperative hydrocephalic and control) on a continuous variable. Paired sample t-test was used to determine if a difference exists between the means of two dependent groups (preoperative hydrocephalic and postoperative hydrocephalic). Chi-squared test of association was used to discover if there was a relationship between two categorical variables. The differences were considered significant at P < 0.05. All statistical comparisons were two-tailed.
ResultsBaseline characteristics of the study and control groups
The age ranged from 4 to 8 years; the average age of children was 5.4 ± 0.99 years in the study group and 5.8 ± 1.19 years in the control group. In the study group, there were 8 females (40%) and 12 males (60%), and in the control group, there were 9 females (45%) and 11 males (55%). Baseline characteristics (age and gender) were similar between the study group and the control group (P > 0.05), as shown in [Table 1].
Basic audiological assessment
All hydrocephalic children had Type A tympanometry with preserved acoustic reflex.
The prevalence of HL in hydrocephalic children was 40% (5% mild, 25% moderate, and 10% moderately severe). Hydrocephalic children had raising mild-to-moderate SNHL, as shown in [Table 2] and [Table 3].
Table 2: Distribution of type and grade of hearing loss among hydrocephalic childrenTable 3: Mean, standard deviation, and range of pure-tone thresholds (dB HL) of hydrocephalic children with hearing loss (Group A)The study group was divided into two groups according to the hearing threshold:
Group A: Hydrocephalic children with HLGroup B: Hydrocephalic children with normal hearing threshold.Comparison between pure-tone thresholds and speech tests in the study and control groups
The hydrocephalic children (preoperative) had statistically significantly higher pure-tone thresholds in dB HL in right and left ears when compared to the control group. There was a statistically significant difference in the pure-tone threshold between the two groups at 250, 500, 1000, 2000, and 4000 Hz, as shown in [Table 4]. The hydrocephalic children (preoperative) had statistically significantly lower speech reception threshed and lower speech discrimination score in right and left ears when compared with the control group, as shown in [Table 5].
Table 4: Mean and standard deviation of pure-tone thresholds (dB HL) of the study (preoperative) group and control groupTable 5: Mean and standard deviation of speech reception threshold and speech discrimination percentage of the study (preoperative) group and control groupComparison between pure-tone thresholds and speech tests in the study groups (preoperative and postoperative)
[Table 6] shows the mean and SD of the pure-tone thresholds in dB HL in right and left ears of the study groups (preoperative and postoperative). There was a statistically significant difference in the pure-tone threshold between the two groups at 250, 500, 1000, and 2000 Hz. [Table 7] shows the mean and SD of speech tests in right and left ears of the study groups (preoperative and postoperative). There was a statistically significant difference between the two groups.
Table 6: Mean and standard deviation of pure-tone thresholds (dB HL) of the study groups (preoperative and postoperative)Table 7: Mean and standard deviation of speech reception threshold and speech discrimination percentage of the study groups (preoperative and postoperative) DiscussionConflicting studies reported a relationship between HCP and HL or improvement in hearing after VP shunting. Previously, the pathophysiology which clarified HL associated with HCP was contradictory.[17]
In the present study, 40% of hydrocephalic children had rising mild-to-moderate SNHL, as shown in [Table 2] and [Table 3]. A similar result was obtained by Lim et al.[18] who found the same percentage of HL in patients with HCP. Lim et al.[18] considered that a threshold elevation of at least 15 dB at one or more frequencies is a HL. In addition, Verma et al. reported that 60% of patients with HCP had SNHL, which was common at low and high frequencies compared to mid-frequencies.[19] In the current study, hydrocephalic children show a significant difference in pure-tone threshold and speech discrimination percentages when compared to their control group, as shown in [Table 4] and [Table 5]. A previous study revealed that hydrocephalic patients had bilateral low-frequency SNHL that was resolved following shunt operation. This can be explained by the fact that HCP has a pathophysiology similar to that of endolymphatic hydrops with fluctuating HL.[20]
Even a minimal change in CSF pressure can be transmitted to the cochlea via the cochlear aqueduct, resulting in endolymph production, resorption mismatch, or decrease in the perilymph volume. These mechanisms can cause collapse and rupture of the Reissner's membrane and cochlear damage.[21] Another theory about the cause of HCP-related HL is compression of the cochlear nerve or nuclei by the cerebellar tonsils, resulting in transmission of abnormal CSF pressures to the cochlea.[22],[23],[24] Sano et al. studied postmortem HCP temporal bone specimens, focusing on cases secondary to a ventricular mass. Sano et al. found damage to the basal turn of the organ of Corti, while the apical part did not have any pathological changes, which may explain the low-frequency SNHL in HCP in the early stages.[25]
Speech affection was observed in the current study, where speech discrimination percentages were significantly different compared to the control group, as shown in [Table 5]. In this study, children who underwent shunt surgery were found to have better hearing function. There was a statistically significant difference between preoperative and postoperative groups in pure-tone thresholds at 250, 500, 1000, and 2000 Hz, as shown in [Table 6]. In line with this finding, the study of Ozturk et al. also showed an improvement of hearing thresholds in all patients who underwent shunt surgery.[26] According to Tandon et al., the prevalence of HL among hydrocephalic patients was 81.5%.[27] Likewise, Dixon and Jones found an improvement in hearing threshold in a 14-year-old patient complaining of HCP associated with sudden unilateral SNHL.[28]
Furthermore, Lim et al. found a 40% improvement in pure-tone thresholds in hydrocephalic patients after shunt operation. Lim et al. revealed that this improvement in the thresholds is associated with decreased CSF pressure causing a decrease in perilymphatic pressure through the patent cochlear aqueduct.[18] In contrast to this study, Spirakis and Hurley reported ipsilateral high-frequency SNHL after a shunt operation in 83% of patients with HCP.[10] This deterioration after shunting is unclear, but there are two theories to explain it: the first identified HL due to retrocochlear dysfunction caused by overshunting, which leads to overdrainage of CSF and produces hypoplasia of the skull base with the involvement of the brain stem, which defines a retrocochlear dysfunction.[29] The second is hypertension resulting from undershunting.[30]
When comparing speech discrimination between the preoperative and postoperative groups, a statistically significant difference was found, as shown in [Table 7]. Since the auditory system has both sensory and motor inputs, the association between hearing recovery and improved speech intelligibility can be explained by a possible improvement and enhancement of cerebral plasticity caused by Alternating and Filtering Auditory Training.[31] In addition, early auditory stimulation after shunt surgery should be recommended to improve the neural organization of the recovering brain.[32] Early auditory stimulation after shunt surgery will also help to avoid maladaptive reorganization of the auditory cortex, especially after unilateral SNHL.[33]
ConclusionThe results of this study add further evidence of hearing impairment in hydrocephalic children and improvement in hearing after shunt operation. Auditory evaluation is highly recommended for all hydrocephalic children as a routine examination. This is especially important in infants and children, in whom self-reporting is unreliable and hearing is vital for speech and language development.
Acknowledgment
The authors appreciate the assistance of all children who participated in this work.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References
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