Vestibular assessment in children aged zero to twelve years: an integrative review

Objective To describe the main vestibular assessment tests performed in children aged zero to twelve years and the main causes of referral for vestibular assessment. Methods The review was guided by the following question: What are the main vestibular assessment tests performed in children aged zero to twelve years and the main causes of referral for vestibular assessment? The PVO strategy was used, being defined as: Population (P) – newborns and children; study Variable (V) – causes of referral for vestibular assessment; study Outcome (O): the main vestibular assessment tests and the main findings. This study was carried out using the main available databases in the months of July, August and September 2021, with no restrictions regarding language and publication date, namely: PubMed, Web of Science, Scientific Electronic Library Online (SciELO), Latin-American and Caribbean Literature in Health Sciences (LILACS), ScienceDirect, Cochrane Library and Embase. The descriptors were obtained from the MeSH database: newborn, infant, child, children, vestibular screening, vestibular infant screening, vestibular newborn screening, test, vestibular function, vestibular function test. Results A total of 7,078 studies were identified. After reading the titles and abstracts, 107 of them were selected, with 101 remaining after the exclusion of duplicates. After the full-text reading, 31 articles were included. It was observed that the most frequently used tests were: rotational tests, caloric stimulation and cervical vestibular evoked myogenic potential and the main causes of referral for vestibular evaluation were hearing loss and vestibular screening. Conclusion The main tests for vestibular screening and/or assessment of children aged zero to twelve years are the rotary chair testing, caloric stimulation and cervical-vestibular evoked myogenic potential. Consequently, performing these procedures is extremely important, since the presence of vestibular dysfunction is quite common in the studied population.


Introduction
For a good body balance, the joint action of the visual, locomotor and vestibular system activities is crucial, as well as the integration of these systems' activity with the central nervous system (CNS). 1 When conflicting information occurs in one or more of the aforementioned systems, dizziness and body instability are the symptoms that usually appear in the affected subjects. 2 A child with vestibular dysfunction can also show alterations in communication skills, changes in cognitive impairment, psychological disorders such as social isolation, as well as poor school performance. Moreover, most of the time, children do not know how to report or describe the body changes caused by such dysfunctions. 3,4 Vestibular screening is the most adequate way to identify early changes related to balance in newborns (NB). As children grow, the neurotological assessment becomes more complete and can be performed with more complex and age-appropriate tests. 2,5 Since the 1980s, there has gradually been a growing awareness of possible vertigo syndromes in the pediatric population and, as a result, the need to increasingly understand about vestibular function in this age group has emerged. 6 The area of vestibular assessment in children has become popular in audiology and otorhinolaryngology clinics in recent years. If there is a slightest suspicion of vestibular involvement, due to any suspicious symptomatology, the child should be referred for appropriate neurotological evaluation, in an attempt to establish a correct diagnosis and then initiate a more appropriate treatment, if necessary. 7,8 Similarly to the early recognition of hearing impairment, the early identification of vestibular disorders has been developed in the pediatric population, since the earlier the identification, the earlier intervention strategies can be implemented. 7 It is important to note that a good choice of vestibular tests is necessary, as most tests are based on visual motor skills that are only fully developed by 14 to 18 years of age. 6,9 Researchers, audiologists and physicians have increasingly contributed with valuable information both about vestibular disorders in the pediatric population and in relation to vestibular assessment techniques that are useful for children.
The present integrative review aimed to describe the main vestibular assessment tests performed in children aged zero to twelve years and the main causes of referral for vestibular assessment.

Methods
This study is an integrative review, which was guided by the following question: What are the main vestibular assessment tests performed in children aged zero to twelve years and the main causes of referral for vestibular evaluation? The study was carried out in July, August and September 2021, through a search in the main available databases, namely: PubMed, Web of Science, Scientific Electronic Library Online (SciELO), Latin-American and Caribbean Literature in Health Sciences (LILACS), ScienceDirect, Cochrane Library and Embase.
There were no language and publication date restrictions. To obtain a larger number of articles, a search key associated with the Boolean operators AND and OR was used, namely: (newborn OR infant OR child OR children) AND (vestibular screening OR vestibular infant screening OR vestibular newborn screening OR test, vestibular function OR vestibular function test). All descriptors used in the search keys were obtained from the Medical Subject Headings (MeSH) database.

Search strategy
The PVO strategy was used, being defined as follows: Population (P) ---newborns and children; study Variable (V) ---causes of referral for vestibular evaluation; study Outcome (O): the main vestibular assessment tests and the main findings. 10

Selection criteria
Two independent reviewers initially selected the articles by reading the title and abstract and, finally, by reading the full-text article, according to the pre-established inclusion and exclusion criteria. Discrepancies regarding study selection and data extraction were discussed between the reviewers at the end of each step, aiming to reach a consensus, and in the absence of agreement, a third evaluator was consulted.
The studies were included without restrictions regarding the design type, as follows: (1) Description of human patients, either newborns and/or children, aged between zero and twelve years, submitted to any type of vestibular evaluation and/or or self-perception questionnaire related to vestibular function. The exclusion criteria adopted for the review were: (1) Literature review; (2) Book chapters; (3) Studies involving children with vestibular disorders of neurological origin; (4) Course Completion Works, dissertations and theses; (5) Animal studies.

Data analysis
The reviewers independently extracted data from the selected articles in digital format, namely: article title, authors' names, year of publication, country, type of study, study objective, sample size, age range of the studied group, performed exams, vestibular alterations, complaints for referral, main conclusions provided by the studies and level of evidence. Aiming to synthesize the information from the articles, the data extracted from the studies were descriptively recorded into a previously prepared table, which facilitated the identification and reformulation of thematic categorizations.
The studies were also classified based on the new evidence pyramid, where studies are classified into five levels: level one (systematic reviews/meta-analysis), level two (randomized clinical trials), level three (non-randomized clinical trials), level four (observational studies) and level five (case studies/reports). 11

Results
A total of 7,078 studies were identified in the initial search, of which 107 were selected after reading the titles and abstracts. Of the 107 studies selected by reading the titles and abstracts, six articles were removed because they were duplicates, leaving 101 articles to be read in full, according to the described selection steps. Finally, 32 articles were selected after excluding the ones that did not meet the pre-established eligibility criteria.
It is important to highlight that the exclusion of the 69 articles that occurred after full-text reading was due to lack of clarity or missing information in the abstract, being better described only throughout the text, such as: age group outside the one established by the study, articles involving children with vestibular disorders of neurological origin and literature reviews (Fig. 1).
The aims of the studies were quite varied. The three most frequently used tests were the ones that used RCT, caloric stimulation and cVEMP.
Most studies aimed at using RCT as a type of vestibular assessment of the Vestibulo-Ocular Reflex (VOR) in children with Hearing Loss (HL), 15,20,23,40,41 maturation of the vestibular system, 28,31 infants and children with CMV infection, 25,27 vestibular function in newborns at neurological risk, 16 IE malformations, 31 and finally, children with ADHD. 38 The use of caloric stimulation comes second, with some studies using bithermal stimulation ---stimulation with hot and cold temperatures, 15,25,35 some studies using only cold water 13,22 and others using ice-cold water. 23,32 Caloric stimulation has been used to assess the vestibular system in children with HL, 13,15,23 at-risk infants, 22 migraine, 15 CMV infection, 25 the assessment of the vestibular system maturation, 32 and BPCV(benign paroxysmal vertigo of childhood ). 35 All studies showed some ype of vestibular impairment through the results of caloric stimulation. 15,22,23,25,32 The vast majority showed some type of peripheral vestibular alteration, such as hyporeflexia and areflexia, 23 uniand bilateral hypoexcitability, and bilateral absence of excitability 22 and weaker nystagmus reactions with cold stimulation. 13  Finally, cVEMP, as a form of vestibular screening in newborns, 5,36 sacculo-collic reflex maturation, 37 ADHD, 38 and, finally, to verify vestibular function in at-risk infants (preterm, neurological disorders or CMV infection). 12,25,27 Because it is an objective test and capable of assessing the vestibular system and sacculo-collic pathways, cVEMP has been considered a very promising test for the evaluation of the pediatric population, especially in relation to vestibular screening in newborns 17 (Table 1).

Discussion
According to the studies included in the review, children considered at risk deserve special attention regarding the evaluation of the vestibular system. Infants at neurological risk may have altered vestibular sensitivity; thus, vestibular tests are considered very useful for this assessment. 18,22 Vestibular disorders are frequent and severe in children infected with CMV. 25 These children may present with unilateral or bilateral, limited or extensive, stable or progressive, early or delayed vestibular alteration. As the vestibular function can deteriorate over time in children infected with CMV, the vestibular assessment should be part of the otorhinolaryngology follow-up in all children infected with CMV. 27 Children with ADHD may have greater gains in VOR and poor ocular fixation reflex capacity when compared to typically developing children. Additionally, cerebellar dysfunction in these patients has also been documented in the literature, and the findings of the cVEMP and rotational chair test (RCT) for children with ADHD showed impaired vestibular function as the results, based on increased VOR gain values and the decreased ocular fixation reflex capacity. 38 Thus, the assessed study established a relationship between both ADHD and the vestibular system, and between poor school performance and possible vestibular alterations. 38 Regarding preterm infants 12,40 and the vestibular system maturation, 37 cVEMP may show prolonged and/or absent results. Prolonged and/or absent cVEMP findings reflect incomplete maturity of the sacculo-collic reflex. The myelination process is one of the main causes. 12,37,40 Another relevant aspect is that some studies 20,21,24 report that the development of the delayed motor aspect can be correlated with reduced vestibular function, in which the vestibular function can be acquired through to the maturation of the sensory hair cells of the vestibular system and the vestibular nerve of the inner ear (IE). 20 The association between hearing loss and motor efficiency deficit has also been highlighted, which may require good balance in addition to abnormal responses in vestibular tests, such as cold caloric stimulation, RCT and cVEMP. 15,23 Although the literature mentions that the vestibular assessment can be difficult in infants and children, RCT is widely used, since it is one of the most frequently used tests, as it stimulates the semicircular canals and otoliths in both ears. Hence, it can detect responses even with a weak VOR. 21 Finally, the association between structural IE malformations and reduced vestibular function and delayed motor development has also been highlighted, 20 showing a higher incidence of reduced VOR in children with vestibular and semicircular canal malformations. 31 Of note, the cerebellar connections with the vestibular system help to maintain VOR balance, contributing to postural balance and limb coordination. 42 Moreover, VOR gain is interceded by the inferior olivary nucleus, in addition to being controlled by the cerebellum, 43 which raises the hypothesis that central inhibition of vestibular function via the cerebellum may be deficient in children with ADHD, thus resulting in greater VOR gains.
Regarding the scenario of low school performance, dizziness, nausea, reading and copying difficulties showed a statistically significant relationship with the studied variables. Dizziness was the most common general complaint, reported by 36% of children and headache was the most common symptom, reported by 50% of participants in the school environment. 34 A study reports that symptoms such as nausea, malaise and headache are common, demonstrating the involvement of alterations in the vestibular system. 44 Regarding the vestibular alterations found in children with poor school performance, they had an irritative peripheral origin, showing a statistically significant relationship between vestibular alterations and school performance. 33,34 As balance is a vital neurological function in the process of maintaining adequate postures, being an essential factor in learning and a sign of neurological maturity. Vestibular alterations can compromise this school process, since learning is a complex and dynamic process, structured through the relationship between motor and perception skills, which, when cortically processed, give rise to cognition. 33 A relevant aspect to consider is related to the vestibular findings of children with migraine. Findings from one study state that all children participating in the study who had migraine had abnormalities on VECTO vestibular tests, from calibration to caloric testing. The results and their analyses indicate that the functional status of the structures that make up the visual-ocular and vestibulo-ocular structures were altered in all migraine patients assessed in the study. Additionally, pathological findings mainly suggest a central location of vestibular dysfunction in children with migraine. 15 Finally, regarding caloric stimulation; this is one of the few clinically proven tests that assess vestibular function separately in newborns. Its results represent the continuity of the VOR, starting in the lateral vestibular canal. It is worth noting that changes can be diagnosed in 20% to 70% of newborns who undergo the test and these changes are most often found in infants with perinatal pathology, multiple birth defects, and administration of aminoglycosides. 13

Conclusion
The most frequently used tests were RCT, caloric stimulation and cVEMP, because they are highly feasible tests that have the capacity to explore the vestibular system and maturation of the sacculo-collic pathway and reflexes, being the most common causes of referral for hearing loss assessment and vestibular screening.