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Vestibular Infant Screening – Flanders: The implementation of a standard vestibular screening protocol for hearing-impaired children in Flanders
International Journal of Pediatric Otorhinolaryngology 120 (2019) 196–201
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International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Vestibular Infant Screening – Flanders: The implementation of a standard vestibular screening protocol for hearing-impaired children in Flanders
T
Sarie Martensa,∗, Ingeborg Dhoogeb,c, Cleo Dhondtc, Laura Leyssensa, Marieke Sucaeta, Saartje Vanaudenaerdeb, Lotte Rombautb, Leen Maesa,b a
Faculty of Medicine and Health Sciences, Department of Rehabilitation Sciences, Ghent University, Corneel Heymanslaan 10 (2P1), 9000, Ghent, Belgium Department of Oto-rhino-laryngology, Ghent University Hospital, Corneel Heymanslaan 10 (1P1), 9000, Ghent, Belgium c Faculty of Medicine and Health Sciences, Department of Head and Skin, Corneel Heymanslaan 10 (1P1), Ghent University, 9000, Ghent, Belgium b
ARTICLE INFO
ABSTRACT
Keywords: Vestibular infant screening Vestibular function Hearing-impaired children Neonatal hearing loss Vestibular Evoked Myogenic Potential (VEMP)
Objectives: The Vestibular Infant Screening – Flanders (VIS-Flanders) project aims to implement and refine a vestibular screening protocol for all children with neonatal hearing loss in Flanders (Belgium) to limit the impact of a vestibular dysfunction on the motor, cognitive and psychosocial development of hearing-impaired children. Methods: Each child with a confirmed neonatal hearing loss in Flanders will undergo a vestibular screening at the age of 6 months in the reference centers involved in the neonatal hearing screening program. The cervical Vestibular Evoked Myogenic Potential (cVEMP) test will be used as a screening tool. The test is short, childfriendly, feasible at a young age and highly correlated with motor and balance performance. The results of an extensive follow-up protocol at the Ghent University Hospital will enable further refinement of the screening protocol. Results: Data collection in all reference centers has started since June 2018. This paper outlines the rationale for the screening and the set-up of this four-year project. Conclusions: Current available literature strongly favors vestibular assessment in congenitally hearing-impaired children. A standard vestibular screening for these children should lead to early identification of vestibular deficits and subsequent prompt referral for further motor assessment and rehabilitation, in order to limit the impact of a vestibular dysfunction in developing children and improve their quality of life.
1. Introduction Hearing-impaired children are at risk for a vestibular impairment [1–6]. This is not surprising, since the close anatomical and embryological relationship of the auditory and vestibular structures assumes that the underlying etiology of the hearing loss may also affect the vestibular end-organs [7,8]. Table 1 provides an overview of the occurrence of vestibular deficits in hearing-impaired children. Depending on the vestibular test protocol, and the etiology and degree of hearing loss, vestibular deficits occur in approximately 38–91% of the children with sensorineural hearing loss [1,7,9–24]. Even mild and unilateral hearing losses can be accompanied with impaired vestibular function [21,25,26]. The vestibular system is an important sensory input system, required for normal balance control. Several studies have indicated a
decreased motor and balance performance in vestibular-impaired children [4,15,25,27–30]. In infants, this manifests itself in delayed gross motor development [1–3,11,16,18,31,32]. Moreover, the combination of hearing loss, vestibular deficit and reduced motor function may have a negative impact on the development of more advanced skills such as spatial orientation, self-concept and joint attention [27]. As a result, vestibular dysfunctions could have an indirect impact on the cognitive and psychosocial development [33–37], and reading, writing and learning abilities [28,38,39]. This implies possible constraining consequences on the child's future educational level, professional opportunities and quality of life [30]. Since many decades, a Universal Newborn Hearing Screening Program (UNHSP) [40,41] is installed in many countries resulting in early detection and timely rehabilitation of hearing impairment [42–44]. Although literature suggests that a significant number of
Corresponding author. E-mail addresses: [email protected] (S. Martens), [email protected] (I. Dhooge), [email protected] (C. Dhondt), [email protected] (L. Leyssens), [email protected] (M. Sucaet), [email protected] (S. Vanaudenaerde), [email protected] (L. Rombaut), [email protected] (L. Maes). ∗
https://doi.org/10.1016/j.ijporl.2019.02.033 Received 21 October 2018; Received in revised form 9 January 2019; Accepted 20 February 2019 Available online 25 February 2019 0165-5876/ © 2019 Elsevier B.V. All rights reserved.
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Table 1 Brief overview of the occurrence of vestibular deficits in hearing-impaired children. Subject characteristics
Occurrence of vestibular end-organ dysfunction a
N°
Age range
Etiology of SNHL (CI)
Degree of SNHL
Overall
Otolith dysfunction
Canal dysfunction
Tribukait et al. (2004) [22]
36
15-17 y
Bilateral profound
70%
12 20
2-7 y 2.6–8.1 y
Bilateral profound Bilateral severe-profound
50% 85%
42% (cVEMP) 42% (SVH) 50% (cVEMP) 50% (cVEMP)
30% (Cal.)
Jin et al. (2006) [19] Shinjo et al. (2007) [10]
≠ etiologies (N/A: use of sign language) ≠ etiologies (All pre-CI) ≠ etiologies (All pre-CI)
Zagólski (2007) [23]
18
3m
Non-syndromic hereditary
78%
67% (cVEMP)
Cushing et al. (2008) [1]
40
3-19.3 y
≠ etiologies (Unilateral CI)
Bilateral moderateprofound Bilateral severe-profound
≥38%
38% (cVEMP)
Jacot et al. (2009) [13] Shall et al. (2009) [18] Zhou et al. (2009) [24]
224 33 23
7 m-16.5 y 4-7 y 2-16 y
≠ etiologies (All pre-CI) ≠ etiologies (5 uni-& 14 bilateral CI) ≠ etiologies (7 uni-& 14 bilateral CI)
± 50% 87% 91%
45% (cVEMP) 87% (cVEMP) 91% (cVEMP)
Jafari et al. (2011) [15] Cushing et al. (2013) [7]
30 153
6-9.4 y 3.6–20 y
≠ etiologies (N/A) ≠ etiologies (119 unilateral CI)
Bilateral profound Bilateral severe-profound Bilateral moderateprofound Bilateral profound Bilateral profound
53% ± 50%
53% (cVEMP) 51% (cVEMP)
Inoue et al. (2013) [16]
89
1.6–8.1 y
≠ etiologies (All pre-CI)
Bilateral profound
57%
42% (cVEMP)
Maes et al. (2014) [20] Sokolov et al. (2018) [21]
39 20
3.7–12.8 y 5.1–12.5 y
≠ etiologies (7 uni-& 8 bilateral CI) ≠ etiologies (No CI)
Bilateral mild-profound Unilateral mild-profound
74% 60%
3 m-15 y
≠ etiologies (721 no CI, 302 pre-CI)
Uni-& bilateral mildprofound
55%
60% (cVEMP) 17% (cVEMP) 33% (oVEMP) N/A
Wiener-Vacher et al. (2018) [17] 1022
N/A 50% (Cal.) 30% (Rot.) 67% (Cal.) 50% (Cal.) 38% (Rot.) 51% (Cal., Rot. & HIT) N/A N/A N/A 50% (Cal.) 47% (Rot.) 41% (Cal.) 20% (Rot.) 49% (Rot.) 48% (Cal.) 35% (vHIT) N/A
N° = Number of subjects; y = Years; m = Months; ≠ = Different; N/A = Not applicable; SNHL = Sensorineural hearing loss; CI = Cochlear Implant; cVEMP = cervical Vestibular Evoked Myogenic Potential; oVEMP = ocular Vestibular Evoked Myogenic Potential; Rot. = Rotatory test; Cal. = Caloric test; SVH = Subjective Visual Horizontal for utricle testing; (v)HIT = (video) Head Impulse Test. a According to BIAP criteria (International Bureau for Audiophonology).
responses or MAICO test) and are subjected to a diagnostic auditory evaluation (i.e. auditory brainstem responses (ABR)) in one of the 25 audiological reference centers in Flanders (Fig. 2: step 3). Annually, a permanent (sensorineural, mixed or conductive) hearing loss is confirmed in about 120–140 of these children. The VIS-Flanders project adds a basic vestibular screening protocol to the existing UNHSP (Fig. 2: step 4). All children with some form of permanent, unilateral or bilateral congenital hearing loss will undergo the vestibular screening at the age of six months in one of the reference centers. In order to collect the test results of all subjects in Flanders, a multicenter overarching approval of the local ethic committees of all participating centers is obtained. In accordance to the Helsinki Declaration, each parent will be requested to sign the informed consent before data collection. The cervical Vestibular Evoked Myogenic Potential (cVEMP) test is applied as standard vestibular screening test. A bone conduction stimulus (i.e. 500 Hz tone bursts (1-2-1 ms) with an intensity of 59 dB nHL (129 dB SPL) and a stimulus repetition rate of 5 Hz) is used to circumvent middle ear disorders which are common in young children [52]. Electromyographic activity is recorded with Neuro-Audio (version 2010, Neurosoft, Ivanovo, Russia) equipment in all reference centers by placing a ground electrode on the forehead, active electrodes on both sternocleidomastoid muscle bellies and a reference electrode on the sternum. During the test, the child is placed in supine position with the upper body upon a sloping pillow (Fig. 3). The examiner turns the child's head to the other side, where the parent is distracting the child with a toy or movie. A bilateral two-peaked reproducible response of the cVEMP with response parameters within the normative data range is required to ‘pass’ the vestibular screening. In case the result is considered unreliable (e.g. due to insufficient tension of the sternocleidomastoid muscle), the screening is rescheduled within three months. No further follow-up is provided in case of a ‘pass’ on the vestibular screening. Patients with a ‘refer’ are referred to a physiotherapist for motor assessment to evaluate if physiotherapy is necessary. Additionally, the VIS-Flanders website provides general information for parents and caregivers.
hearing-impaired children are at risk for a vestibular impairment, vestibular assessment in hearing-impaired children is not routinely performed [30]. It is often mainly restricted to cochlear implant candidates [7,13,45–47] and a small number of children with vertigo or balance disorders [27,48,49]. Even though vestibular testing in children is challenging and time-consuming, it is shown to be feasible in children if some adjustments are made [50,51]. The aim of the Vestibular Infant Screening – Flanders (VIS-Flanders) project is to overcome the current lack of vestibular assessment in hearing-impaired children, by providing an early vestibular screening for all children with a congenital hearing loss and by increasing awareness of the impact of vestibular problems. This way, early diagnosis of a vestibular deficit will lead to adequate referral for extensive vestibular testing, motor assessment and rehabilitation if necessary. Additionally, the comparison of the screening results with those of an extensive vestibular follow-up protocol at the Ghent University Hospital will demonstrate the sensitivity and enable further refinement of the vestibular screening protocol. 2. Material and methods Since the official start of the project in June 2018, VIS-Flanders has implemented a vestibular screening protocol in all reference centers in Flanders. A more extensive follow-up protocol is applied for all hearingimpaired children in the Ghent University Hospital. An overview of the two test protocols and cohorts to reach the main objectives is provided in Fig. 1. 2.1. Vestibular screening protocol In Flanders, the UNHSP is organized by the infant welfare agency ‘Child & Family’ (‘Kind en Gezin’) within the first weeks of life for all newborn infants ( ± 60.000 annually) (Fig. 2: step 1 and 2). Each year, approximately 1.2% of these infants ( ± 700) have a ‘refer’ on the second neonatal hearing screening (i.e. automated auditory brainstem 197
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Fig. 1. Overview of the VIS-Flanders project. (FU = follow-up).
equipment is not available or not adapted to children in the majority of the Flemish reference centers. In contrast to the caloric and rotatory test, the (video) Head Impulse Test ((v)HIT) is a short and child-friendly test to examine all semicircular canals. Unfortunately, not many centers have the equipment (with a stand-alone registering camera) to objectively perform this test in infants. Performing the clinical HIT is an alternative. However, the extensive experience that is required for reliable application of the clinical HIT in infants is currently not present in the majority of the reference centers. Ideally, the vestibular screening should be performed, where applicable, before cochlear implant surgery, which is generally scheduled after the age of 8 months [56]. Moreover, an early screening will ensure that rehabilitative measures can be taken in time to limit the impact of a vestibular deficit on the child's development [56,57]. Scheduling the screening not too early, i.e. around the age of six months, has the advantage that the gross motor milestones may already give an indication of the child's vestibular function [4] and most children will have acquired enough head control to build up sufficient tension in the sternocleidomastoid muscle to ensure a reliable interpretation of the cVEMP responses [52]. Also, the permanent character of the hearing loss is generally already confirmed at the age of 6 months [42]. Therefore, this age is assumed to be the ideal timing for the vestibular screening. Unfortunately, by screening only once at the age of six months, children with a delayed-onset or progressive hearing or vestibular loss will be missed. Secondly, although previous studies have suggested a higher occurrence of saccular compared to semicircular canal dysfunctions in hearing-impaired children [20,22,23] and abnormal cVEMP responses have been reported in about half of the included hearing-impaired children [1,7,10,13,16,18–20,22–24,58,59], subjects with isolated semicircular canal dysfunctions will be missed by using only the cVEMP as screening test. Furthermore, the study of Bernard et al. (2015) even demonstrated higher percentages of semicircular dysfunctions in children with a profound hearing loss caused by the congenital cytomegalovirus infection [58]. However, the results of this study (and all others mentioned in Table 1) cannot be generalized to all hearing-impaired children, as the subjects often have bilaterally
2.2. Extensive follow-up protocol Infants diagnosed with a permanent hearing loss in the Ghent University Hospital (ca. 20 to 30 subjects each year) are followed prospectively with an extensive protocol until the age of three years old. This consists of a complete age-dependent vestibular test battery (Table 2) [50], an ocular motor assessment and a motor assessment. Parents are also questioned about the gross motor milestones. If the motor assessment is abnormal, children are referred for physiotherapy. The ethic committee of the Ghent University Hospital approved the data collection of the extensive follow-up protocol in our research center by using an informed consent for parents, according to the Helsinki Declaration. 3. Results and discussion 3.1. Results During the test period from June 2018 until May 2021, approximately 400 infants will be referred for the vestibular screening. 3.2. Discussion - Strengths and opportunities for improvement Since a screening test should be short, sensitive, objective and in this case also child-friendly, the cVEMP is selected as standard vestibular screening test [15,18,24,25,48,53–55]. Moreover, literature suggests a higher occurrence of saccular deficits, which the cVEMP examines [52], compared to semicircular canal dysfunctions in hearingimpaired children [20,22,23]. This is probably linked to a common embryologic origin of the saccule and the cochlea in the pars inferior of the labyrinth [7,8]. Additionally, Maes et al. (2014) demonstrated a strong correlation between the cVEMP results and the motor performance in hearing-impaired children [4,25]. The use of the cVEMP makes this screening also more accessible as ABR equipment, which mostly contains a cVEMP module, is available in most participating centers. The caloric and the rotatory test are not recommended as basic pediatric vestibular screening tests. Currently, this expensive 198
International Journal of Pediatric Otorhinolaryngology 120 (2019) 196–201
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Fig. 2. Addition of the vestibular screening to the Universal Neonatal Hearing Screening Program in Flanders (UNHSP). (ABR = Auditory Brainstem Responses; MAICO test = Automated ABR; cVEMP = cervical Vestibular Evoked Myogenic Potential test).
profound hearing losses, cochlear implants, different ages and different etiologies of hearing loss. Moreover, limited information is provided about the number of children with an isolated semicircular canal dysfunction and the test protocol varies from study to study [14].
At the Ghent University Hospital, an extensive longitudinal protocol is implemented. This protocol includes a follow-up examination of the motor, oculomotor, otolith and semicircular canal function until the age of three (Table 2), as children normally reach the most important gross
Fig. 3. Test setup of the vestibular screening (in a normal-hearing child). 199
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centers, the thirteen rehabilitation centers and more than thirty private physiotherapists in Flanders for their participation in this project.
Table 2 Overview of the extensive longitudinal vestibular assessment at the Ghent University Hospital. Vestibular assessment
(General specifications)
6 months 1 year 2 years
vHIT Rotatory test cVEMP
(Stand-alone registering camera) (ENG registration) (Bone conduction)
3 years
+ Caloric Test + oVEMP
(Air insufflation at 24 °C and 48 °C) (Mini-shaker)
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vHIT = video Head Impulse Test; cVEMP = cervical Vestibular Evoked Myogenic Potential test; oVEMP = ocular Vestibular Evoked Myogenic Potential test; ENG = Electronystagmography.
motor milestones in the first three years of life. These results will demonstrate the sensitivity of the cVEMP as vestibular screening test in detecting vestibular dysfunctions in hearing-impaired infants and enable further refinement of the screening protocol in the future. For example, the VIS-Flanders project may try to implement the vHIT widely to detect semicircular canal dysfunctions or to adapt the screening protocol according to the etiology of the hearing loss. In the meantime, VIS-Flanders will induce increasing awareness of pediatric vestibular deficits within the participating centers (e.g. by providing guidance, information sessions and professional manuals) and among parents with hearing-impaired children (e.g. by providing adequate counseling, information brochures with tips, red flags and contact details in case of a suspicion of vestibular problems). As a consequence, it is hoped that children with undetected vestibular deficits (because of a possible false negative result on the vestibular screening) will be noticed by caregivers or the child's family and find their way to vestibular testing and appropriate therapy after all. 4. Conclusion Although hearing-impaired children have a higher risk of vestibular deficits, which can influence the child's motor, cognitive and psychosocial development, vestibular assessment of very young hearing-impaired children in clinical practice is still uncommon. The VIS-Flanders project aims to minimize the impact of vestibular dysfunctions on a child's development by implementing a standard vestibular screening protocol at the age of six months for all congenitally hearing-impaired children in Flanders. By providing widespread access to this basic vestibular screening, this pioneer work will increase awareness and lead to early identification of vestibular deficits in hearing-impaired infants and subsequent referral for motor assessment and rehabilitation. As such, the project aims to set an example for other regions worldwide. VIS-Flanders website https://vis-flanders.be/en/ (accessed 26/02/2019). Conflicts of interest There are no conflicts of interest to disclose for all authors. Funding source This work was supported by funding from the Research Foundation – Flanders (FWO TBM project T000917N). Acknowledgments The authors would like to thank the agency ‘Child & Family’, the ‘Federation of Centers for Ambulatory Rehabilitation’, the parent organization ‘VLOK-CI’, the ENT departments of the twenty-five reference 200
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Vestibular Infant Screening – Flanders: The implementation of a standard vestibular screening protocol for hearing-impaired children in Flanders
T
Sarie Martensa,∗, Ingeborg Dhoogeb,c, Cleo Dhondtc, Laura Leyssensa, Marieke Sucaeta, Saartje Vanaudenaerdeb, Lotte Rombautb, Leen Maesa,b a
Faculty of Medicine and Health Sciences, Department of Rehabilitation Sciences, Ghent University, Corneel Heymanslaan 10 (2P1), 9000, Ghent, Belgium Department of Oto-rhino-laryngology, Ghent University Hospital, Corneel Heymanslaan 10 (1P1), 9000, Ghent, Belgium c Faculty of Medicine and Health Sciences, Department of Head and Skin, Corneel Heymanslaan 10 (1P1), Ghent University, 9000, Ghent, Belgium b
ARTICLE INFO
ABSTRACT
Keywords: Vestibular infant screening Vestibular function Hearing-impaired children Neonatal hearing loss Vestibular Evoked Myogenic Potential (VEMP)
Objectives: The Vestibular Infant Screening – Flanders (VIS-Flanders) project aims to implement and refine a vestibular screening protocol for all children with neonatal hearing loss in Flanders (Belgium) to limit the impact of a vestibular dysfunction on the motor, cognitive and psychosocial development of hearing-impaired children. Methods: Each child with a confirmed neonatal hearing loss in Flanders will undergo a vestibular screening at the age of 6 months in the reference centers involved in the neonatal hearing screening program. The cervical Vestibular Evoked Myogenic Potential (cVEMP) test will be used as a screening tool. The test is short, childfriendly, feasible at a young age and highly correlated with motor and balance performance. The results of an extensive follow-up protocol at the Ghent University Hospital will enable further refinement of the screening protocol. Results: Data collection in all reference centers has started since June 2018. This paper outlines the rationale for the screening and the set-up of this four-year project. Conclusions: Current available literature strongly favors vestibular assessment in congenitally hearing-impaired children. A standard vestibular screening for these children should lead to early identification of vestibular deficits and subsequent prompt referral for further motor assessment and rehabilitation, in order to limit the impact of a vestibular dysfunction in developing children and improve their quality of life.
1. Introduction Hearing-impaired children are at risk for a vestibular impairment [1–6]. This is not surprising, since the close anatomical and embryological relationship of the auditory and vestibular structures assumes that the underlying etiology of the hearing loss may also affect the vestibular end-organs [7,8]. Table 1 provides an overview of the occurrence of vestibular deficits in hearing-impaired children. Depending on the vestibular test protocol, and the etiology and degree of hearing loss, vestibular deficits occur in approximately 38–91% of the children with sensorineural hearing loss [1,7,9–24]. Even mild and unilateral hearing losses can be accompanied with impaired vestibular function [21,25,26]. The vestibular system is an important sensory input system, required for normal balance control. Several studies have indicated a
decreased motor and balance performance in vestibular-impaired children [4,15,25,27–30]. In infants, this manifests itself in delayed gross motor development [1–3,11,16,18,31,32]. Moreover, the combination of hearing loss, vestibular deficit and reduced motor function may have a negative impact on the development of more advanced skills such as spatial orientation, self-concept and joint attention [27]. As a result, vestibular dysfunctions could have an indirect impact on the cognitive and psychosocial development [33–37], and reading, writing and learning abilities [28,38,39]. This implies possible constraining consequences on the child's future educational level, professional opportunities and quality of life [30]. Since many decades, a Universal Newborn Hearing Screening Program (UNHSP) [40,41] is installed in many countries resulting in early detection and timely rehabilitation of hearing impairment [42–44]. Although literature suggests that a significant number of
Corresponding author. E-mail addresses: [email protected] (S. Martens), [email protected] (I. Dhooge), [email protected] (C. Dhondt), [email protected] (L. Leyssens), [email protected] (M. Sucaet), [email protected] (S. Vanaudenaerde), [email protected] (L. Rombaut), [email protected] (L. Maes). ∗
https://doi.org/10.1016/j.ijporl.2019.02.033 Received 21 October 2018; Received in revised form 9 January 2019; Accepted 20 February 2019 Available online 25 February 2019 0165-5876/ © 2019 Elsevier B.V. All rights reserved.
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Table 1 Brief overview of the occurrence of vestibular deficits in hearing-impaired children. Subject characteristics
Occurrence of vestibular end-organ dysfunction a
N°
Age range
Etiology of SNHL (CI)
Degree of SNHL
Overall
Otolith dysfunction
Canal dysfunction
Tribukait et al. (2004) [22]
36
15-17 y
Bilateral profound
70%
12 20
2-7 y 2.6–8.1 y
Bilateral profound Bilateral severe-profound
50% 85%
42% (cVEMP) 42% (SVH) 50% (cVEMP) 50% (cVEMP)
30% (Cal.)
Jin et al. (2006) [19] Shinjo et al. (2007) [10]
≠ etiologies (N/A: use of sign language) ≠ etiologies (All pre-CI) ≠ etiologies (All pre-CI)
Zagólski (2007) [23]
18
3m
Non-syndromic hereditary
78%
67% (cVEMP)
Cushing et al. (2008) [1]
40
3-19.3 y
≠ etiologies (Unilateral CI)
Bilateral moderateprofound Bilateral severe-profound
≥38%
38% (cVEMP)
Jacot et al. (2009) [13] Shall et al. (2009) [18] Zhou et al. (2009) [24]
224 33 23
7 m-16.5 y 4-7 y 2-16 y
≠ etiologies (All pre-CI) ≠ etiologies (5 uni-& 14 bilateral CI) ≠ etiologies (7 uni-& 14 bilateral CI)
± 50% 87% 91%
45% (cVEMP) 87% (cVEMP) 91% (cVEMP)
Jafari et al. (2011) [15] Cushing et al. (2013) [7]
30 153
6-9.4 y 3.6–20 y
≠ etiologies (N/A) ≠ etiologies (119 unilateral CI)
Bilateral profound Bilateral severe-profound Bilateral moderateprofound Bilateral profound Bilateral profound
53% ± 50%
53% (cVEMP) 51% (cVEMP)
Inoue et al. (2013) [16]
89
1.6–8.1 y
≠ etiologies (All pre-CI)
Bilateral profound
57%
42% (cVEMP)
Maes et al. (2014) [20] Sokolov et al. (2018) [21]
39 20
3.7–12.8 y 5.1–12.5 y
≠ etiologies (7 uni-& 8 bilateral CI) ≠ etiologies (No CI)
Bilateral mild-profound Unilateral mild-profound
74% 60%
3 m-15 y
≠ etiologies (721 no CI, 302 pre-CI)
Uni-& bilateral mildprofound
55%
60% (cVEMP) 17% (cVEMP) 33% (oVEMP) N/A
Wiener-Vacher et al. (2018) [17] 1022
N/A 50% (Cal.) 30% (Rot.) 67% (Cal.) 50% (Cal.) 38% (Rot.) 51% (Cal., Rot. & HIT) N/A N/A N/A 50% (Cal.) 47% (Rot.) 41% (Cal.) 20% (Rot.) 49% (Rot.) 48% (Cal.) 35% (vHIT) N/A
N° = Number of subjects; y = Years; m = Months; ≠ = Different; N/A = Not applicable; SNHL = Sensorineural hearing loss; CI = Cochlear Implant; cVEMP = cervical Vestibular Evoked Myogenic Potential; oVEMP = ocular Vestibular Evoked Myogenic Potential; Rot. = Rotatory test; Cal. = Caloric test; SVH = Subjective Visual Horizontal for utricle testing; (v)HIT = (video) Head Impulse Test. a According to BIAP criteria (International Bureau for Audiophonology).
responses or MAICO test) and are subjected to a diagnostic auditory evaluation (i.e. auditory brainstem responses (ABR)) in one of the 25 audiological reference centers in Flanders (Fig. 2: step 3). Annually, a permanent (sensorineural, mixed or conductive) hearing loss is confirmed in about 120–140 of these children. The VIS-Flanders project adds a basic vestibular screening protocol to the existing UNHSP (Fig. 2: step 4). All children with some form of permanent, unilateral or bilateral congenital hearing loss will undergo the vestibular screening at the age of six months in one of the reference centers. In order to collect the test results of all subjects in Flanders, a multicenter overarching approval of the local ethic committees of all participating centers is obtained. In accordance to the Helsinki Declaration, each parent will be requested to sign the informed consent before data collection. The cervical Vestibular Evoked Myogenic Potential (cVEMP) test is applied as standard vestibular screening test. A bone conduction stimulus (i.e. 500 Hz tone bursts (1-2-1 ms) with an intensity of 59 dB nHL (129 dB SPL) and a stimulus repetition rate of 5 Hz) is used to circumvent middle ear disorders which are common in young children [52]. Electromyographic activity is recorded with Neuro-Audio (version 2010, Neurosoft, Ivanovo, Russia) equipment in all reference centers by placing a ground electrode on the forehead, active electrodes on both sternocleidomastoid muscle bellies and a reference electrode on the sternum. During the test, the child is placed in supine position with the upper body upon a sloping pillow (Fig. 3). The examiner turns the child's head to the other side, where the parent is distracting the child with a toy or movie. A bilateral two-peaked reproducible response of the cVEMP with response parameters within the normative data range is required to ‘pass’ the vestibular screening. In case the result is considered unreliable (e.g. due to insufficient tension of the sternocleidomastoid muscle), the screening is rescheduled within three months. No further follow-up is provided in case of a ‘pass’ on the vestibular screening. Patients with a ‘refer’ are referred to a physiotherapist for motor assessment to evaluate if physiotherapy is necessary. Additionally, the VIS-Flanders website provides general information for parents and caregivers.
hearing-impaired children are at risk for a vestibular impairment, vestibular assessment in hearing-impaired children is not routinely performed [30]. It is often mainly restricted to cochlear implant candidates [7,13,45–47] and a small number of children with vertigo or balance disorders [27,48,49]. Even though vestibular testing in children is challenging and time-consuming, it is shown to be feasible in children if some adjustments are made [50,51]. The aim of the Vestibular Infant Screening – Flanders (VIS-Flanders) project is to overcome the current lack of vestibular assessment in hearing-impaired children, by providing an early vestibular screening for all children with a congenital hearing loss and by increasing awareness of the impact of vestibular problems. This way, early diagnosis of a vestibular deficit will lead to adequate referral for extensive vestibular testing, motor assessment and rehabilitation if necessary. Additionally, the comparison of the screening results with those of an extensive vestibular follow-up protocol at the Ghent University Hospital will demonstrate the sensitivity and enable further refinement of the vestibular screening protocol. 2. Material and methods Since the official start of the project in June 2018, VIS-Flanders has implemented a vestibular screening protocol in all reference centers in Flanders. A more extensive follow-up protocol is applied for all hearingimpaired children in the Ghent University Hospital. An overview of the two test protocols and cohorts to reach the main objectives is provided in Fig. 1. 2.1. Vestibular screening protocol In Flanders, the UNHSP is organized by the infant welfare agency ‘Child & Family’ (‘Kind en Gezin’) within the first weeks of life for all newborn infants ( ± 60.000 annually) (Fig. 2: step 1 and 2). Each year, approximately 1.2% of these infants ( ± 700) have a ‘refer’ on the second neonatal hearing screening (i.e. automated auditory brainstem 197
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Fig. 1. Overview of the VIS-Flanders project. (FU = follow-up).
equipment is not available or not adapted to children in the majority of the Flemish reference centers. In contrast to the caloric and rotatory test, the (video) Head Impulse Test ((v)HIT) is a short and child-friendly test to examine all semicircular canals. Unfortunately, not many centers have the equipment (with a stand-alone registering camera) to objectively perform this test in infants. Performing the clinical HIT is an alternative. However, the extensive experience that is required for reliable application of the clinical HIT in infants is currently not present in the majority of the reference centers. Ideally, the vestibular screening should be performed, where applicable, before cochlear implant surgery, which is generally scheduled after the age of 8 months [56]. Moreover, an early screening will ensure that rehabilitative measures can be taken in time to limit the impact of a vestibular deficit on the child's development [56,57]. Scheduling the screening not too early, i.e. around the age of six months, has the advantage that the gross motor milestones may already give an indication of the child's vestibular function [4] and most children will have acquired enough head control to build up sufficient tension in the sternocleidomastoid muscle to ensure a reliable interpretation of the cVEMP responses [52]. Also, the permanent character of the hearing loss is generally already confirmed at the age of 6 months [42]. Therefore, this age is assumed to be the ideal timing for the vestibular screening. Unfortunately, by screening only once at the age of six months, children with a delayed-onset or progressive hearing or vestibular loss will be missed. Secondly, although previous studies have suggested a higher occurrence of saccular compared to semicircular canal dysfunctions in hearing-impaired children [20,22,23] and abnormal cVEMP responses have been reported in about half of the included hearing-impaired children [1,7,10,13,16,18–20,22–24,58,59], subjects with isolated semicircular canal dysfunctions will be missed by using only the cVEMP as screening test. Furthermore, the study of Bernard et al. (2015) even demonstrated higher percentages of semicircular dysfunctions in children with a profound hearing loss caused by the congenital cytomegalovirus infection [58]. However, the results of this study (and all others mentioned in Table 1) cannot be generalized to all hearing-impaired children, as the subjects often have bilaterally
2.2. Extensive follow-up protocol Infants diagnosed with a permanent hearing loss in the Ghent University Hospital (ca. 20 to 30 subjects each year) are followed prospectively with an extensive protocol until the age of three years old. This consists of a complete age-dependent vestibular test battery (Table 2) [50], an ocular motor assessment and a motor assessment. Parents are also questioned about the gross motor milestones. If the motor assessment is abnormal, children are referred for physiotherapy. The ethic committee of the Ghent University Hospital approved the data collection of the extensive follow-up protocol in our research center by using an informed consent for parents, according to the Helsinki Declaration. 3. Results and discussion 3.1. Results During the test period from June 2018 until May 2021, approximately 400 infants will be referred for the vestibular screening. 3.2. Discussion - Strengths and opportunities for improvement Since a screening test should be short, sensitive, objective and in this case also child-friendly, the cVEMP is selected as standard vestibular screening test [15,18,24,25,48,53–55]. Moreover, literature suggests a higher occurrence of saccular deficits, which the cVEMP examines [52], compared to semicircular canal dysfunctions in hearingimpaired children [20,22,23]. This is probably linked to a common embryologic origin of the saccule and the cochlea in the pars inferior of the labyrinth [7,8]. Additionally, Maes et al. (2014) demonstrated a strong correlation between the cVEMP results and the motor performance in hearing-impaired children [4,25]. The use of the cVEMP makes this screening also more accessible as ABR equipment, which mostly contains a cVEMP module, is available in most participating centers. The caloric and the rotatory test are not recommended as basic pediatric vestibular screening tests. Currently, this expensive 198
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Fig. 2. Addition of the vestibular screening to the Universal Neonatal Hearing Screening Program in Flanders (UNHSP). (ABR = Auditory Brainstem Responses; MAICO test = Automated ABR; cVEMP = cervical Vestibular Evoked Myogenic Potential test).
profound hearing losses, cochlear implants, different ages and different etiologies of hearing loss. Moreover, limited information is provided about the number of children with an isolated semicircular canal dysfunction and the test protocol varies from study to study [14].
At the Ghent University Hospital, an extensive longitudinal protocol is implemented. This protocol includes a follow-up examination of the motor, oculomotor, otolith and semicircular canal function until the age of three (Table 2), as children normally reach the most important gross
Fig. 3. Test setup of the vestibular screening (in a normal-hearing child). 199
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centers, the thirteen rehabilitation centers and more than thirty private physiotherapists in Flanders for their participation in this project.
Table 2 Overview of the extensive longitudinal vestibular assessment at the Ghent University Hospital. Vestibular assessment
(General specifications)
6 months 1 year 2 years
vHIT Rotatory test cVEMP
(Stand-alone registering camera) (ENG registration) (Bone conduction)
3 years
+ Caloric Test + oVEMP
(Air insufflation at 24 °C and 48 °C) (Mini-shaker)
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vHIT = video Head Impulse Test; cVEMP = cervical Vestibular Evoked Myogenic Potential test; oVEMP = ocular Vestibular Evoked Myogenic Potential test; ENG = Electronystagmography.
motor milestones in the first three years of life. These results will demonstrate the sensitivity of the cVEMP as vestibular screening test in detecting vestibular dysfunctions in hearing-impaired infants and enable further refinement of the screening protocol in the future. For example, the VIS-Flanders project may try to implement the vHIT widely to detect semicircular canal dysfunctions or to adapt the screening protocol according to the etiology of the hearing loss. In the meantime, VIS-Flanders will induce increasing awareness of pediatric vestibular deficits within the participating centers (e.g. by providing guidance, information sessions and professional manuals) and among parents with hearing-impaired children (e.g. by providing adequate counseling, information brochures with tips, red flags and contact details in case of a suspicion of vestibular problems). As a consequence, it is hoped that children with undetected vestibular deficits (because of a possible false negative result on the vestibular screening) will be noticed by caregivers or the child's family and find their way to vestibular testing and appropriate therapy after all. 4. Conclusion Although hearing-impaired children have a higher risk of vestibular deficits, which can influence the child's motor, cognitive and psychosocial development, vestibular assessment of very young hearing-impaired children in clinical practice is still uncommon. The VIS-Flanders project aims to minimize the impact of vestibular dysfunctions on a child's development by implementing a standard vestibular screening protocol at the age of six months for all congenitally hearing-impaired children in Flanders. By providing widespread access to this basic vestibular screening, this pioneer work will increase awareness and lead to early identification of vestibular deficits in hearing-impaired infants and subsequent referral for motor assessment and rehabilitation. As such, the project aims to set an example for other regions worldwide. VIS-Flanders website https://vis-flanders.be/en/ (accessed 26/02/2019). Conflicts of interest There are no conflicts of interest to disclose for all authors. Funding source This work was supported by funding from the Research Foundation – Flanders (FWO TBM project T000917N). Acknowledgments The authors would like to thank the agency ‘Child & Family’, the ‘Federation of Centers for Ambulatory Rehabilitation’, the parent organization ‘VLOK-CI’, the ENT departments of the twenty-five reference 200
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