DISCUSSION
With the increasing rate of bilateral CI implementation in children with IEMs, vestibular function development has received significant attention. However, studies on this subject remain limited. Due to the close anatomical and developmental relationship between otolith end-organs and the cochlear, hearing impairment may lead to vestibular disorder[13], but vestibular assessment is not routinely performed[14, 15]. One of the reasons for this is the lack of clinically appropriate and effective assessment methods in the pediatric group and a gold standard test for the assessment of balance and postural control in children[16]. Another reason is that vestibular dysfunction can be compensated by other systems, and notably, abnormality in gait and motor coordination is not observed in children with IEMs[17]. The current study aimed to describe the difference in gross motor development in patients with SNHL, and to investigate the otolith functional modifications after CI between children with and without IEMs.
Otoliths are important receptors of the vestibulospinal reflex pathway, which helps to maintain balance and is significantly important for the human body to control the erect head and the spatial orientation of the body[18]. Balance and motor development in early childhood are delayed in patients with IEMs, as observed in children with severe congenital hearing loss[19]. In patients with IEMs, otolith function may be significantly compromised, and these patients often present with impairments in balance control, such as delays in head control and independent walking, because such functions are related to abnormal inner ear structures[20, 21]. Consistent with previous studies[22, 23], we reported that children with IEMs performed worse than those in the control group with regards to gross motor development. The mean ages of head control and independent walking in the IEM group were 3.73±0.86 months and 15.39±4.5 months, respectively. While follow-up research continues,, even when these children were able to walk, their balance ability, such as performance on the single-leg standing test, remained tardive. Moreover, they also had a higher risk of falling during advanced balance activities, such as bicycle riding, than the normal children.
Farideh et al.[24] reported that 68.2% and 14.3% of children with IEMs and SNHL (normal cochlear anatomy), respectively, presented with vestibular dysfunction after CI. Hosseinzadeh et al.[6] used the Bruininks–Oseretsky motor ability test (BOT) and sensory organization test for postures to test the standing/walking stability of four patients with common cavity deformity (CCD) under open and closed eyes conditions. Their results indicated that the balance function of the patients with CCD was more delayed than that of other patients with SNHL. We evaluated the gross motor development preliminarily because in our study, most of the CI candidates had not reached the standard BOT-2 assessment age (>4 years). In our study, the gross motor development of children with IEMs was significantly more delayed compared with that of the control group. Specifically, the mean age of independent walking in the IEM group was 15.39 months. This result is similar to those of previous studies, which indicate that the otolith end-organ plays an essential role in obtaining gross motor abilities before the age of 2 years. If any postoperative balance damage is identified, such as instability after surgery, the solution of early rehabilitation should be recommended for the best and most rapid balance recovery.
The VEMP test is a noninvasive test that can sensitively identify otolith function variation in younger children. Some studies have shown that VEMP plays an important role in evaluating the otolith function and vestibular nerve integrity of patients before and after CI[25, 26]. However, assessment of otolith function in children with SNHL, especially in IEMs, remains limited. In this study, we aimed to analyze the difference in VEMP between children with IEMs and children with SNHL with normal cochlear anatomy.
Previous findings have revealed that the function of the saccular and utricle may receive certain damage by CI, and this damage can last for a long period of time and the cVEMP response rate is more likely influenced by CI than oVEMP, because the saccule is anatomically closer to the cochlea and has a major risk of CI[27]. To determine the real variation of otolith function in relation to CI, we analyzed the VEMP variation only in the ears that had a present response for cVEMP and oVEMP preoperatively. In the present study, 40% of patients lost the cVEMP response and this variation may suggest the risk of injury during CI, specifically during intracochlear port electrode insertion, which may seriously affect the saccular neuroepithelium.
The higher postoperative cVEMP loss rate in our study might be related to the patients’ age. The youngest children assessed for waveform were 9 and 12 months old in the normal cochlear group and IEM group, respectively. It was not easy for children to maintain an adequate SCM tone during the whole test process. The second factor is that the electrical stimulation of the CI device can have an effect on VEMP responses[28-30]. However, the VEMP tests in our study were performed in CI-off conditions to prevent the electrical stimulation from having an effect on the responses to evaluate the actual residual otolith function only. Another factor is different surgical techniques. Studies on this matter, that is whether the surgical approach can induce VEMP loss, remain inconclusive. Some studies have indicated that cochleostomy might be more likely traumatic for the otolith end-organ than the round window approach[31]. In this study, the approach used for most patients was the round window approach, except for children with CCD, who underwent the slotted labyrinthotomy approach. The latter can significantly shorten the surgery duration and effectively reduce the rate of postoperative cerebrospinal fluid leakage and vertigo probability[32]. Similarly, Cozma et al.[33] reported normal saccular function in 73.3% of the CI ears using the round window approach and in 68.42% of ears using the cochleostomy approach, which suggests that the round window port electrode insertion is the recommended strategy to avoid saccular impairment. In this study, all children underwent AC-cVEMP tests, and previous studies have revealed that CI can induce peripheral mechanical changes, leading to air–bone gaps, which can lead to absent AC-cVEMP responses without underlying vestibular deficit[34, 35]. Moreover, inaccuracies in measurement methods can also lead to a higher rate of VEMP loss.
In our study, the rate of VEMP response was significantly different between the two groups, but there were no significant differences in changes within various P1-N1 parameters (Tables 2–4). It is possible that patients with IEMs in this study had a more severe degree of deformity and that they presented little difference in waveforms after CI. Additionally, because the test is performed in young children who do not have typical amplitudes, the differences between the two groups are subtle. Currently, there is no consensus protocol for the quantitative assessment of the P1-N1 parameters wave complex in children. However, the type of change in VEMPs can indicate severity of IEMs affecting the utricle and saccule. Xu et al.[30] reported that cVEMP disappearance occurred more frequently on the CI-implanted ear and that waveform parameter showed abnormal changes, such as decreased amplitude, forward movement of P1 and N1, and shortened interpeak latency at 1 month after CI, suggesting that cVEMP waveforms can reflect the degree of damage to the saccule caused by CI.
The present study consisted of 11 children with CCD, all of which showed no VEMP response before surgery on either cVEMP or oVEMP. In contrast, most patients with IEMs presented with concomitant symptoms with cochleovestibular nerve deficiency and abnormal development of vestibular sensory cells. Hence, patients with IEMs are more likely to have abnormal VEMP response rate and waveform than those without IEMs. In 2006, Jin et al.[28] tested 12 patients with IEMs using VEMP and found that saccule function was more likely damaged after CI, as reflected in the absence of cVEMP waveform in short pure tone stimulation. Our results are consistent with those of previous studies. In the current study, the otolith function in the IEM group was significantly more compromised than that of the control group, which suggests that the VEMPs of IEMs might be more susceptible to influence by CI.
Vestibular sensory cells of the semicircular canals and otolith organs or primary vestibular afferent neurons are possibly present in patients with IEMs to maintain a basic balance function, particularly CCD. These patients do not have difficulty in general activities that require dynamic balance and mobility[36]. In an embryological study, in the human fetal developmental stage, the vestibular system develops earlier than the cochlear system[37][38]. Children with hearing loss who are at high risk for vestibular dysfunction can develop a new sensory distribution process in which visual and somatosensory information becomes essential for postural control when vestibular input is impaired[3, 39]. The above can explain why VEMP can still be present in patients with severe IEMs and how they can acquire balance function at 3–4 years of age. In the present study, one patient with CCD presented with cVEMP waveform 6 months after CI. Considering the small sample size, long-term changes in cVEMP parameters should be analyzed through follow-up.
Additionally, six patients with large vestibular aqueduct syndrome (LVAs) presented with normal VEMP waveform before surgery and normal performance of balance function. These results are similar to those of preceding studies. Patients with LVAs often complain of subjective symptoms of balance disorders, such as dizziness and unsteady walking, but may have normal waveform on VEMP tests[40, 41]. Due to the small differences between the different types of malformations and the small sample size, there were no statistical differences between different types of malformations.
This study also observed that, IEM group has two children presented with vertigo and slight unsteadiness. all symptoms resolved within 48 h. We analyzed that this may be due to otolith function. In these patients, the balloon and utricle are not fully developed, with strong plasticity, and the otoconia injury has a strong compensatory mechanism and central system adaptability. Another reason is that the operation is gentle, which greatly avoids damage to the vestibular system. Therefore, it is still necessary to understand the otolith function of postoperative patients. Long-term follow-up is needed to determine whether such patients are at risk for vestibular decline along with age growth.
Our study has some limitations. First, recall bias exsist due to the retrospective methodology of determining gross motor delays. Second,the mean follow-up time was 1–3 months after CI. Patients develop or compensate their vestibular function from the visual and central nervous systems rapidly during the age of 1–5 years, which would affect the results of the VEMP tests. Moreover, the otolith function test method was primarily performed; thus, a further vestibular function test battery is required.