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.