Visual vertigo in children: Adaptation and validation of the visual vertigo analogue scale to European Portuguese

Abstract

BACKGROUND:

Visual vertigo occurs after vestibular and non-vestibular pathology and can be present in children and adolescents. It can be assessed by “the Visual Vertigo Analogue Scale” (VVAS), a questionnaire with a Portuguese version for adults.

OBJECTIVES:

To perform the adaptation to pediatric age and validation of VVAS in European Portuguese.

METHODS:

This prospective study involved the pediatric adaptation of the Portuguese VVAS, according to recognized guidelines. It was then completed by 30 healthy controls and 18 children with vestibulopathy. Patient caregivers also completed the Dizziness Handicap Inventory - Patient Caregivers (DHI-PC) to further explore the link between questionnaires. Groups were compared for severity of visual vertigo and VVAS test-retest reliability was tested.

RESULTS:

The VVAS score was significantly higher in vestibular group (p < 0.001). No statistically significant differences were found between VVAS initial and re-test scores (p = 0.33). VVAS severity scores showed a positive correlation with DHI-PC (r = 0.598, p = 0.009).

CONCLUSION:

The present Pediatric adaptation of VVAS in European Portuguese shows good psychometric properties for the assessment of visual vertigo. A positive correlation with the DHI-PC was showed, establishing the potential use of both questionnaires in the evaluation of vertigo children.

Keywords

Visual vertigo visual analog scale child validity reliability

1 Introduction

Vertigo and imbalance are uncommon complaints in pediatric patients and have been described in around 5.6% of children in the United States [8]. However, the percentage of children with vestibular symptoms, such as dizziness, vertigo or instability, is thought to be higher than that reported in the literature. This is due to the fact that health professionals are not very aware of the issue, as well as the non-specific presentation in some children, who may have more than one diagnosis contributing to their symptoms, and the complexity in history taking from children and caregivers [8 , 22].

In the literature, around 70% of dizziness and vertigo cases in childhood are due to benign paroxysmal vertigo of childhood, vestibular migraine (VM), viral infection, head trauma and otitis media [12 , 23]. Migraine-related syndromes, Benign Paroxysmal Vertigo of Childhood and VM, are the most common cause of this symptomatology [7 , 12]. Recently, the term “Benign Paroxysmal Vertigo of Childhood” has been replaced by the term “recurrent vertigo of childhood” according to the Bàràny society [3].

Visual vertigo (VV) or Visually induced Dizziness (VID) is a complex symptom that is included as a subtype of ‘Persistent Postural-Perceptual Dizziness (PPPD) but can occur in isolation, in various situations such as after acute vestibular pathology, peripheral or central (head trauma, vestibular neuritis, vestibular migraine) [6, 16]. It is often one of the most damaging characteristics, especially in the modern world with the ever-increasing intensity of visual stimulation [17]. Patients report instability or dizziness in visually rich environments (e.g. walking down a supermarket aisle or riding in a car) and with exposure to moving or static objects with complex patterns (e.g. watching passing traffic, striped curtains or a crowd of people) [6, 18].

Recently, a study was published on PPPD in children, which found a prevalence of 7.3% in the pediatric and adolescent population that had not previously been described in the medical literature [21]. There are no systematic reviews on functional vertigo in childhood and adolescence [9, 10]. There is some studies revealing that visually induced symptoms are common in children with a vestibular disorder, migraine, and/or concussion [16] and it has been argued that these patients should receive specific rehabilitation regardless of what gives rise to this symptoms’ constellation [4].

Assessing children with vertigo can be extremely challenging and the use of scales and questionnaires can help in the anamnesis of these patients [9 , 12]. In order to assess the impact of vestibular symptoms on the child’s life, an adaptation of the Dizziness Handicap Inventory (DHI) was published in 2015, creating the Dizziness Handicap Inventory - Patient Caregivers. This questionnaire can be answered by the caregivers of children aged 5 to 12 years old, who provide the clinical history and play an important role in determining the balance deficit. This instrument can be used as the first step in assessing the impact that “balance disorders” have on a child’s daily life, as well as monitor the response to treatment [12]. The DHI-PC has been translated and culturally adapted for use in Portugal [13].

The Visual Vertigo Analogue Scale (VVAS) was developed to assess visual vertigo, as a quick method of quantifying VV and monitoring the response to treatment. The VVAS has been shown to be valid and reliable in adults, but not in children [5, 6]. Our aim was to adapt this scale for pediatrics, to assess children aged between 8 to 17 years old, using the translation and adaptation already carried out for use in Portuguese adults [1], as well as to work towards its validation allowing its use in Portuguese speaking children.

2 Material and methods

Written informed consent was obtained from all children and their parents before participating in the study in accordance with WMA Declaration of Helsinki - Ethical Principles for Medical Research Involving Human Subjects. Ethical approval was obtained from the Centro Hospitalar Universitàrio Lisboa Central Research Ethics Committee, Lisbon, Portugal. This work was developed between 2021 and 2023.

2.1 Pediatric adaptation of the VVAS

This prospective study involved the pediatric adaptation of the Visual Vertigo Analogue Scale (VVAS). The adaptation process was carried out based on the steps recommended by Beaton et al. [2] The methodological sequence used was as follows: semantic and vocabulary adaptation, discussion in focus groups, back-translation into English and validation by the team responsible for the original instrument. Formal consent was obtained, via email, from the team that developed the original version of the instrument for its translation and application.

In the first phase, changes were made to the vocabulary to make it easier for the children to understand, some of which were suggested by the original author of the VVAS, using the translation and adaptation already carried out for use in Portuguese adults [1]. Three focus groups were held to assess the preservation of the construct and the correct understanding of phrases and expressions. For the focus groups we had the participation of children’s caregivers attending the vertigo clinic, children aged between 8 and 17 years old attending the vertigo clinic and teachers teaching at the institution’s school. The role of the teachers in our institution is to support learning activities when children are admitted in the hospital for longer periods of time. Eight children and 16 caregivers took part in the focus groups, as well as four teachers of our institution’s school. Half of the children were female, aged between 8 and 15 years old, with an average age of 12 years old. Exclusion criteria were parents/caregivers and children who didn’t understand Portuguese, children with developmental delays or with neurological or orthopaedic limitations.

The team responsible for the adaptation reached a consensus, taking into account the changes discussed in the focus groups, with the aim of achieving semantic, idiomatic, experiential and conceptual equivalence that would guarantee an adequate cultural adaptation. This resulted in the pre-final consensus version of the pediatric VVAS, in Portuguese.

For the pediatric adaptation of the VVAS, after discussion in focus groups, 4 items (Items 3, 4, 8 and 9) were changed and a question was added regarding vestibular symptoms while playing video games or watching videos on a mobile phone (Table 1). This pre-final version was back-translated into its original language by two independent bilingual translators, who had not seen the original version, and who had no medical training and whose first language was the original language used in the questionnaire. The two back-translations were sent to the team responsible for the original instrument (Elizabeth Dannenbaum) for review and formal approval. A final consensus version of the pediatric VVAS emerged from the two translations (Fig. 1).

Table 1
Pediatric adaptation after discussion in focus groups

Items Translation for adults Translation adapted for children

Instructions Indique a intensidade de vertigem/ tontura ou desequilìbrio que sente nas situações que se seguem, marcando de acordo com a escala indicada. Indica a força de tontura ou desequilìbrio que sentes nas seguintes situações. Assinala na escala abaixo.

Item 1) Caminhar num corredor de supermercado Caminhar no corredor da escola

Item 2) Ser passageiro num carro Andar de carro

Item 3) Estar sob luzes fluorescentes Estar sob luzes fluorescentes / forte

Item 4) Observar trânsito intenso num cruzamento Ver os carros a passar na estrada

Item 5) Caminhar num centro comercial Caminhar no recreio da escola

Item 8) Caminhar sobre um chão com padrões Caminhar sobre um chão com desenhos / padrões

Item 9) Ver um filme de ação na TV Ver um filme de ação/aventura na TV

Item 10) Added Non existent Jogar videojogos ou ver vìdeos no telemòvel

Items	Translation for adults	Translation adapted for children
Instructions	Indique a intensidade de vertigem/ tontura ou desequilìbrio que sente nas situações que se seguem, marcando de acordo com a escala indicada.	Indica a força de tontura ou desequilìbrio que sentes nas seguintes situações. Assinala na escala abaixo.
Item 1)	Caminhar num corredor de supermercado	Caminhar no corredor da escola
Item 2)	Ser passageiro num carro	Andar de carro
Item 3)	Estar sob luzes fluorescentes	Estar sob luzes fluorescentes / forte
Item 4)	Observar trânsito intenso num cruzamento	Ver os carros a passar na estrada
Item 5)	Caminhar num centro comercial	Caminhar no recreio da escola
Item 8)	Caminhar sobre um chão com padrões	Caminhar sobre um chão com desenhos / padrões
Item 9)	Ver um filme de ação na TV	Ver um filme de ação/aventura na TV
Item 10) Added	Non existent	Jogar videojogos ou ver vìdeos no telemòvel

Fig. 1

Visual vertigo analog scale Pediatric adaptation in European Portuguese.

2.2 Validation of VVAS in European Portuguese

To evaluate if the pediatric adaptation in Portuguese maintains the psychometric properties of the original version, two groups were recruited.

The case group included pediatric patients (8–17 years old) followed at the outpatient Equilibrium Clinic of various Portuguese institutions who had more than 3 episodes of vestibular symptoms: dizziness and/or vertigo and/or instability, in the year 2023. The children were diagnosed by one experienced Otolaryngologist based in a structured interview, physical examination, and complementary exams as necessary. Exclusion criteria for the case group were children who didn’t understand Portuguese.

For the control group, pediatric patients without vestibular symptoms from the general ENT consultation were recruited, and children with recurrent headache, migraine, medication acting on the central nervous system, ophthalmic/orthopedic pathology, developmental delay, otitis media with chronic effusion and hypoacusis were excluded.

The VVAS was tested in 18 children with vestibular symptoms and 30 healthy subjects. The patient group consisted of 78% (14/18) females, with a mean age of 14 (2.5) years old. The control group sample was matched for age and sex, with a mean age of 13 (2.9) years old, where 67% (20/30) were female.

Both groups answered the VVAS pediatric version and the DHI-PC through an online survey on the Qualtrics.^XM platform. Additionally, they answered a brief behavioral screening questionnaire (SDQ: Strengths and Difficulties Questionnaire, European Portuguese version of SDQ informant, to be filled in by caregivers or professors).

All patients and their parents/caregivers consented to take part in the study. They were asked to answer the survey a second time, at a time interval of more than 4 days, to test-retest reliability estimations. The participants in the study did not have any help from the assistant and the answers were reviewed for completeness.

2.3 Measurement questionnaires

2.3.1 Pediatric version of Portuguese VVAS

The Pediatric version of Portuguese VVAS consists of ten visual analog scales which subjects were asked to rate. Each scale pertained to a specific visual vertigo provoking situation. The subjects should mark on a 10-cm line to indicate the amount of dizziness provoked by each situation, between two anchors, with zero (0) representing no dizziness and ten (10) representing an extreme dizziness or activity avoided due to dizziness. The distance from the zero anchor to the subject’s marking was measured to the nearest 0.5 centimeter. Items that were not applicable to the participant’s daily life were not completed. If the subject answered with a whole number, that was the one that was considered. To summarize the ten items, two final scores were calculated: VVAS positive and VV severity. The subjects were classified as VVAS positive if two or more items were rated above zero on the analogue scale. The VV severity score was calculated as an average based on the mean scores of items: VV Severity = (sum of rated analogue scale items/number of answered items)×10. Thus, a VV severity score of 0 indicated that the subject would not experience Visual Vertigo, whereas a score of 90–100 would indicate severe visual vertigo [1, 6].

2.3.2 Dizziness Handicap Inventory - Patient Caregivers

The DHI-PC is a 21-item questionnaire that asks the patients caregivers to rate their perception of their child disability arising from dizziness. A score of 4-points is assigned to a “yes” response, 2-points to “sometimes”, and 0-points to “no” response. Thus, the total score ranges from 0 (no perceived disability) to 84 (maximum perceived disability). Scores can fluctuate from normal (less than 16 points), mild handicap (16–26 points), moderate handicap (26–43 points) or severe handicap (>43 points) [12].

2.3.3 Strengths and Difficulties Questionnaire

The Strengths and Difficulties Questionnaire (SDQ), include five subscales: emotional, conduct, hyperactivity/inattention, peer relationship problems, and prosocial behavior. Subscale scores range between 0 and 10; total score is the sum of the first four scales (range 0–40).

2.4 Statistical analysis

Data analysis was performed using Statistical Product and Service Solutions (SPSS) software version 25.0 (IBM Corp. Released 2017. IBM SPSS Statistics for Windows, Version 25.0. Armonk, NY: IBM Corp.). The total score of the VVAS in the patient group and the control group were compared (Mann-Whitney test). ROC (Receiver operating characteristic) curve assessed discriminative capacity. Test-retest reliability was determined by comparing initial and second survey total scores using mixed-effects regression models and Bland-Altman methods. The relationship between questionnaires was explored (Spearman‘s correlation coefficient). A level of significance α= 0.05 was considered.

3 Results

3.1 VVAS characteristics

The sample was classified as VVAS positive if two or more items were classified above zero. The VVAS was positive in 17 patients (94.4%) and in 13 (43.3%) healthy controls. The proportion of patients in the VVAS positive group was higher than the proportion in the VVAS negative group (56.7% vs. 5.6%; p < 0.001 from the Chi-square test).

3.2 External reliability

For test-retest reliability estimations, 35 (72.9%) participants (15 patients and 20 healthy controls) repeated the VVAS (repeated after 4 to 22 days, mean of 9.2 days). No statistically significant differences were found between the results of the initial score of the VVAS and the final score (p = 0.332) (Fig. 2).

Fig. 2

Bland-Altman graph for initial versus final scores of VVAS.

3.3 VV severity between controls and the patient group

Total scores of VVAS were compared between the groups. Visual vertigo scores were significantly different between control and patients groups, respectively (6.0 (7.4) vs. 35.7 (22.5), p < 0.001). Moreover, ROC (Receiver operating characteristic) analysis demonstrated that the VVAS could discriminate between the two groups. The optimal cut-off score was 15 (out of 100) with a sensitivity of 83% and specificity of 86%. The area under the curve (with 95% confidence intervals) was 0.897 (0.795–0.999).

3.4 Correlation between the VVAS and DHI-PC

Spearman correlation analysis carried out between VV severity and total DHI-PC scores for the vestibulopathy patients revealed a positive correlation (r = 0.598, p = 0.009).

3.5 Strength and Difficulties Questionnaire

In the control group, the average SDQ scores were 7.1 (5.0) out of 40 and in the children with vestibular symptoms it was 15.5 (6.8) out of 40. In the group with vestibular symptoms, there was no correlation between the VVAS or DHI-PC scores and the total scores on the SDQ questionnaire.

4 Discussion

We aimed to perform the adaptation to pediatric age and validation of VVAS in European Portuguese, in order to obtain an instrument to evaluate visually induced dizziness in Portuguese children.

VVAS was developed as a simple and easy to administer assessment tool to specifically evaluate visual vertigo. Visual vertigo scores were significantly different between control and vestibulopathy groups, respectively 6.0 (7.4) vs. 35.7 (22.5), p < 0.001, confirming that the VVAS can effectively discriminate controls from vestibular patients. We added a question to the original VVAS regarding dizziness/instability caused by playing video games or watching videos on a mobile phone. We chose to add this question because studies have indicated an association between increased screen time, headache frequency and dizziness symptoms in children [19, 20]. Time spent on smartphones, tablets, and computers should be considered when asking children about their symptoms and symptom triggers [16].

Normally a child free of vestibular signs and symptoms should report ‘0’ on all items, but we found that 43% of children in the control group were VVAS positive, which means that they scored > 2 items above zero, of which only one scored above 25. Children in the control group were excluded if they had a known vestibular pathology, migraine or headache. However, it is possible that they had undiagnosed vestibular problems. We should also consider that many children and adolescents show symptoms of visual vertigo and seem to be more susceptible to visual vertigo than adults, as they rely more on visual cues for spatial orientation and their ability to integrate multisensory data in situations of sensory conflict is still developing [16]. Many children may be prone to motion-sickness, [10] and therefore may score above 0 on the VVAS. Nonetheless, the proportion of VVAS positive patients was significantly higher than the VVAS negative patients.

This study demonstrated that the VVAS has good test and re-test reliability. We found that the VVAS scores from vestibular and a non-vestibular group were significantly different, further demonstrating specificity of the test. Moreover, ROC area under the curve indicates a test with “good accuracy” in separating those with and without abnormal VV symptom levels.

The positive strong correlation with the DHI-PC that we demonstrate contributes to the validation of this instrument to be used in the vestibulopathy population. Because of language and cultural differences, DHI-PC original version use is limited in non-validated populations. The DHI-PC was previously translated and culturally adapted to use in Portugal and this version was used in the present work [13]. The strong correlation, showed between the VVAS and the DHI-PC, demonstrates the potential use in combination of these two questionnaires in the evaluation of children with vertigo.

Children with vestibular disorder should also be screened for associated psychological symptoms [11, 16]. In the present work we found that mean parent-rated SDQ scores were increased in the patients group when compared to healthy controls, in accordance to previous studies, but we did not find a significant correlation between questionnaires and SDQ in this sample.

Some study limitations were present. Our sample size was exploratory, and relatively small due to the fact that vertigo and imbalance are uncommon complaints in pediatric age and also due to the difficulty in recruiting children interested in taking part. In the present study we did not establish a correlation between the visual vertigo and the final vertigo etiology so we do not know which patients presented with more severe visual vertigo. The time between the test and re-test reliability was not homogeneous but it reflects real life conditions. Participants reported forgetting to complete the questionnaire a second time within the required time period, despite email or telephone reminders, due to their normally busy weekly schedule. Furthermore, when children felt better, as their symptoms fluctuated over time, they did not value participating again. Further studies are needed, namely with a larger sample size and with a more homogeneous time between responses to further prove test–retest reliability. Further research in responsiveness to change over time is also needed to further validate the pediatric VVAS for clinical use.

5 Conclusion

The present Pediatric adaptation of the VVAS in European Portuguese shows good psychometric properties for the assessment of self-perceived and severity of visual vertigo in a small patient group. A positive correlation with the DHI-PC was showed, establishing the potential use of both questionnaires in the evaluation of vertigo children.

Conflict of interest

None.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Footnotes

Acknowledgments

We would like to thank Prof. Ana Luisa Papoila, Senior Lecturer in Medical Statistics and Clinical Trials, NOVA Medical School, for her statistical analysis and results.

We would like to thank Elizabeth Dannenbaum, original author of the VVAS, for her permission, as well as her valuable suggestions, to adapt this scale for pediatrics.

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