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Electronystagmography finding in children with peripheral and central vestibular disorders
International Journal of Pediatric Otorhinolaryngology (2006) 70, 13—18
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Electronystagmography finding in children with peripheral and central vestibular disorders Angelo Salami, Massimo Dellepiane, Renzo Mora *, Giuseppe Taborelli, Barbara Jankowska ENT Department, University of Genoa, Genoa, Italy Received 24 February 2005; accepted 3 May 2005
KEYWORDS Central vertigo; Children; Electronystagmography; Peripheral vertigo
Summary Objective: Dizziness and imbalance are uncommon in children, but often alarming for their families: a detailed interview and otoneurological examination are important for reaching a specific diagnosis and treatment. Children with vestibular disorders are thought to be difficult to examine: vestibular tests (caloric test, roto-acceleratory test, electronystagmography, opto-kinetic nystagmus, cranio-corpography and posturography) are used less frequently for children than in adult patients. The aim of the study was to determine whether the results of electronystagmography testing improve an emergency physician’s diagnosis of dizziness in children. Methods: Patients were selected on the basis of the following inclusion criteria: aged between 2 and 12 years and affected with vertiginous symptoms. All patients underwent the following instrumental examinations: blood tests, audiological screening, electronystagmography of spontaneous nystagmus or provoked by vestibular and optical stimulation and electroencephalogram. Results: The results underlines an high incidence of central vertigo (83%): 52% of the children presented a prevailing unidirectional nystagmus at labyrinth stimulation and 48% of the children an asymmetry in the response of nystagmus at optical kinetic stimulation with quality alteration of shocks. Conclusions: Electronystagmography can register and evaluate the qualitative and quantitative characteristics of the nystagmic response and allow to distinguish between central or peripheric vertigo: different degrees and various combinations of the abnormal responses shown in optokinetic central test were the most characteristic of electronystagmography in patients with vestibular central vertigo. # 2005 Elsevier Ireland Ltd. All rights reserved.
1. Introduction * Corresponding author. Tel.: +39 01035 37631; fax: +39 01035 37684. E-mail address: [email protected] (R. Mora).
Dizziness and imbalance are uncommon in children, but often alarming for their families causing an extensive, often unnecessary evaluation: we should
0165-5876/$ — see front matter # 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2005.05.001
14
remember that vertigo is rather an abstract concept for a small child, who is unable to distinguish between vertigo and a feeling of fear [1,2]. The evaluation of vertigo in children requires a careful anamnesis together with an evaluation of clinical signs and diagnostics tests: audiometry, tympanometry and electronystagmography (ENG) are the most helpful diagnostic tests [1—3]. Sensation of balance is the result of appropriate information that comes from vestibular, ocular and proprioceptive sensory receptors and is properly integrated within the cerebellum and brain stem: it is often difficult to identify its etiopathogenesis [3]. Vertigo in children can be caused by many disorders: in several reviews peripheral causes are stated to be more common than central causes. The differential diagnosis of vertigo in children is extensive: otitis media and middle ear effusion could be the most common causes of vertigo in children, but there are some problems in detecting the other causes for vertigo because they are one of most frequent diseases of childhood. In children with normal eardrums, who not show otitis media or middle ear effusion, vertigo is most commonly caused by migraine and benign paroxysmal vertigo of childhood (BPVC): these findings show to be very different from those with adult vertigo [1—4]. Central causes of vertigo typically affect older population groups because of the associated risk factors of vascular causes of vertigo: children are more commonly affected by migraine, posttraumatic vertigo (cerebral concussion) and cerebellar tumors [5]. Considering that vestibular tests are used less frequently for children than in adult patients, the aim of the study was to determine the efficacy of ENG testing in the diagnosis of dizziness in children.
2. Methods In this study were enrolled 23 patients selected on the basis of the following inclusion criteria: aged between 2 and 12 years and affected with vertiginous symptoms. The patients were divided into two groups (group A and group B). Group A was formed by 19 children, 10 males and 9 females, aged between 2 and 12 years (mean age 7 years) and affected with central vertigo (six posttraumatic, two meningitic, three toxic, four migrainous and four psychogenic vertigo). All the children that presented a posttraumatic vertigo had experienced an occipital trauma during the month prior to the study. The children with migrainous vertigo showed an ‘‘equivalent migraine sundrome’’ caused
A. Salami et al.
by vasomotor phenomena in the vertebro-basilar systems and characterised by a migraine attack which follows vertigo [6] (Table 1). All the patients of group A presented these symptoms: vertigo, neurovegetative symptoms, intense headache and decrease of postural control (in no case a conscience loss has been noticed). Only seven children presented a spontaneous nystagmus (Table 1). Group B was formed by 4 children, 3 males and 1 female, aged between 3 and 11 years (mean age 5 years) with peripheral vertigo (two viral, one BPVC and one neoplastic vertigo). All these children were affected by intense vertigo crisis and marked neurovegetative symptomatology (nausea, vomit, sweating, abdominal pain etc.): such crises were lasting few minutes and were separated by long remission periods of variable time length. Only one child with viral vertigo presented a spontaneous nystagmus (Table 2). After a careful and detailed anamnesis, all patients underwent the following examinations: complete audiological screening (liminal tonal audiometry, tympanometry, otoacoustic emission and otoacoustic products of distortion); ENG (with thermal labyrinth stimulation, rotatory vestibular stimulation and optokinetic stimulation); electroencephalogram (EEG); pediatric, neurological, neuropsychiatric and to evaluation by an oculist. The child with neoplastic vertigo has not been submitted to the thermal labyrinth stimulation, this child had been previously submitted to petro mastoid evidement. No preparation was necessary for the ENG recording: the children, head blocked, sat on a ‘‘Tonnies rotatory chair Pro model’’ which was placed in the middle of a rotatory cylindrical chamber (2 m in diameter and 1.9 m in height). The rotatory cylinder was lighted from above by a 100 W bulb and was driven by a direct current engine which turned it clockwise and counterclockwise up to 2008/s, maximum speed, with preset acceleration ranging from 18 to 28/s. and its internal area was covered with thirty-two black vertical contrast. Ocular movements was recorded according to the usual method by means of a ‘‘Tonnies electronystagmograph’’ with eight channels: the electrodes were placed to the side, above and below each eye (a ‘‘ground’’ electrode was attached to the forehead). All the subjects underwent to thermal test according to the Fitzgerald-Hallpike method, rotatory vestibular stimulation by stop test from a constant angular velocity of 908/s (be in sense time that anticlockwise) and to ‘‘stare type’’, optokinetic stimulation with a cylinder rotation velocity of 308 for 60 s (be in sense time that anticlockwise):
Central vertigo n
Ny
Thermal labyrinth stimulation Hyporeflexia
Post traumatic 6 Meningitic 2 Toxic 3 Migrainous 4 Psychosomatic 4 Total 19
Rotatory vestibular stimulation
Optokinetic stimulation Asymmetry
I
Prevailing Hyporeflexia Normo-reflexia Hypereflexia Symmetry unidiretional II Monolateral Bilateral Monolateral Bilateral Ny Monolateral Bilateral Monolateral Bilateral
1 0 1 0 0 2
1 1 1 0 0 3
5 1 1 3 1 11
0 0 0 0 0 0
Hypereflexia
3 0 0 0 2 5
0 0 0 0 0 0
0 0 0 1 1 2
3 2 3 3 1 12
1 1 2 0 0 4
3 1 0 0 3 7
1 0 0 0 0 1
1 0 1 0 0 2
0 0 0 4 1 5
1 1 2 1 3 8
ENG finding in children with peripheral and central vertigo
Table 1 Results after the three instrumental stimulations (thermal, rotatory and optokinetic) in the group A (n: number of patients affected by vertigo; Ny I-II: number of patients with spontaneous nystagmus of I and II grade; nono: monolateral; bil: bilateral)
Table 2 Results after the three instrumental stimulations (thermal, rotatory and optokinetic) in the group B (n: number of patients affected by vertigo; Ny I—II: number of patients with spontaneous nystagmus of I and II grade; nono: monolateral; bil: bilateral) Peripheral vertigo n
Ny
Thermal labyrinth stimulation Hyporeflexia
BPVC Viral Neoplastic Total
1 2 1 4
Rotatory vestibular stimulation
Hypereflexia
I
II
Monolateral
Bilateral
Monolateral
Bilateral
Prevailing unidiretional Ny
0 1 0 1
0 0 0 0
0 0 0 0
1 1 0 2
0 0 — 0
0 1 — 1
0 0 0 0
Hyporeflexia
Normo-reflexia
Monolateral
Bilateral
0 0 0 0
1 1 1 3
0 0 0 0
Optokinetic stimulation Hypereflexia Monolateral
Bilateral
0 1 0 1
0 0 0 0
Symmetry
Asymmetry
1 2 1 4
0 0 0 0
15
16
the optokinetic reflex was tested by measuring optokinetic nystagmus slow and fast phases velocity during rotation of the subject in light. Vestibular tests (thermal test and rotatory stimulation) were executed one or two days after optokinetic stimulation and between each stimulation there was a fifteen minutes interval.
3. Results For the analysis of the results we have considered nystagmus slow phase after the three instrumental stimulations (thermal, rotatory and optokinetic). In the group A 12 children presented a prevailing unidirectional nystagmus after thermal labyrinth stimulation: these patients were affected by posttraumatic (n = 3), meningitic (n = 2), toxic (n = 3), migrainous (n = 3) and psychogenic vertigo (n = 1) (Table 1). After the rotatory vestibular stimulation 11 children presented vestibular hyporeflexia (7 bilateral and 4 monolateral), 7 vestibular hypereflexia (5 bilateral and 2 monolateral) and one child normoreflexia (Table 1). In the same group (group A), 11 children showed an asymmetry in the response of nystagmus with a quality alteration of shocks (of their morphology) after optokinetic stimulation: five of these presented a posttraumatic vertigo, three a migrainous vertigo, one a meningitic vertigo, one a psychogenic vertigo and one a toxic vertigo (Table 1). This asymmetry was revealed by a low amplitude and a significantly impaired slow-phase velocity (SPV) of nystagmus: the impaired SPV was of the right optokinetic pattern in six patients (three of these affected by posttraumatic, two migrainous and one meningitic vertigo) and of the left optokinetic pattern in five patients (two with a posttraumatic vertigo, one a migrainos vertigo, one a psycosomatic vertigo and one a toxic vertigo) (Table 1). EEG showed changes of cortical electrical activity in two patients (a cortex increase in the relative theta activity in the centrotemporal region and a decrease of centroparietal beta activity): these patients were affected by meningitic vertigo and presented an impaired slow-phase velocity of nystagmus. In the group B EEG did not show any changes of cortical electrical activity. In the same group by group B, after thermal labyrinth stimulation the ENG showed a bilateral vestibular hyporeflexia in two patients and a bilateral vestibular hypereflexia in one child; after the rotatory vestibular stimulation three children pre-
A. Salami et al.
sented bilateral vestibular hyporeflexia and one child monolateral vestibular hypereflexia, no patients presented ENG abnormalities after optokinetic stimulation: in all the children there was no asymmetry between the SPV of nystagmus (Table 2). The audiological screening has highlighted cochlear alterations in three cases: a bilateral sensorineural hearing lost in the two children with viral vertigo and a monolateral transmissive hypoacusia in the child with neoplastic vertigo.
4. Discussion Vestibular evaluation in the pediatric population has in the past taken several forms: for the most part, the pediatric vestibular evaluation has been more subjective than objective. One of the primary reasons for this has been the obvious difficulties encountered in trying to conduct a standard adult procedure on a pediatric patient [7]. Our experience has shown that children tolerate ENG testing easily and the discomfort is minimal. Sensation of balance is the result of appropriate information that comes from vestibular, ocular and proprioceptive sensory receptors and is properly integrated within the cerebellum and brain stem: it is often difficult to identify its etiopathogenesis: ENG can perform an analysis of these systems by itself or in conjunction with others tests data [3]. The history usually provides the key information for distinguishing between peripheral and central causes of vertigo. The duration of attacks is most helpful in distinguishing between central and peripheral causes: vertigo associated with vertebrobasilar insufficiency typically lasts minutes, whereas peripheral inner ear causes of recurrent vertigo typically last hours [8]. Vertigo, instability, dizziness, or equilibrium disorders are not usually considered as consequences of ophthalmologic problems: ocular disorders can be responsible for these symptoms in children [9]. The visual system is not mature at birth and continues to develop during infancy; during this period various abnormalities can appear and become symptomatic (vergence insufficiency, latent strabismus with binocular vision and anisometropia). Failures in binocular vision or in convergence can be responsible for inadequate gaze stabilization during movement and double or blurry vision during fixation, which could generate a sensation of imbalance and dizziness [10]. Child complaining of vertigo or dizziness but with normal clinical somatic neurologic and vestibular examinations should have a complete ophthalmologic examination before additional, more costly,
ENG finding in children with peripheral and central vertigo
17
Fig. 1 Asymmetry of the nystagmus response in a patient with post-traumatic vertigo, after optokinetic stimulation (A: left cylinder rotation; B: right cylinder rotation).
investigations: this should lead to better screening and more appropriate care of ocular disorders in children and avoid unnecessary magnetic resonance imaging [9]. On the other hand, disorders of balance are much more frequent but the factors involved are numerous and the role of the vestibular system is often debatable: as a matter of fact, there are many kinds of nystagmus which are not related to any changes in the vestibular system, but which are rather more part of the overal changes of conjugated eye movements [11]. Seen in this light, ENG by exploring the different kinds of conjugated eye movement, can help decisively in the diagnosis: ENG can record and evaluate the qualitative and quantitative characteristics of the nystagmic response and allow to distinguish between central or peripheral vertigo. Central or peripheral nystagmus can usually be distinguished by other features in the history or on clinical examination: the presence of a spontaneous nystagmus with fixation indicates a probable central lesion while the presence of a spontaneous nystagmus without fixation a probable peripheric lesion, positional nystagmus is indicative of a central lesion if it has no latency and it is present only when the head is in a particular position, peripheral vestibular lesions usually lead to a mixed horizontal-torsional or vertical-torsional nystagmus, a pure vertical or pure torsional nystagmus is always caused by a central lesion [12,13]. By ENG it is possible to record and study the nystagmus, either spontaneous or provoked. Spontaneous nystagmus can be observed in the different position of the glance with open eyes, or eliminating the fixation in the dark or with close eyes. Provoked nystagmus is analysed by caloric stimulation, rotatory stimulation and the study of the flash-inducednystagmus [13]. Diagnosis of central neurological disturbances is submitted to four conditions: specific criteria selection, complete oculomotor and vestibular testing,
graduated conclusions in function of the acquired data and not only an etiological but a functional or topographical diagnosis. Central vestibular syndromes lead also to labyrinthine weakness or nystagmus directional preponderance but, first at all, to specific criteria who are: saccadic, pursuit and horizontal optokinetic abnormalities, central spontaneous or positional nystagmus, failure of fixation suppression, hyperreflexia, perverted nystagmus, slowing of the nystagmus fast phases, slowing-down of the nystagmus slow phases, asymmetry of the nystagmus, vertical optokinetic deficits and retraction nystagmus [14] (Fig. 1). According with other authors, in central vertigo ENG recordings showed typical asymmetry of the optokinetic pattern. This asymmetry was revealed by a low amplitude and a significantly impaired slow-phase nystagmus velocity of the optokinetic pattern [15,16]. In the patients affected by post-traumatic vertigo, the vestibular and optokinetic abnormalities indicate that as an occipital trauma can lead to an haemorrhage of the frontal and temporal area near the cortical projection of the vestibular pathway [17]. In patients with meningitic vertigo, the prevailing unidirectional nystagmus and the asymmetry in the response of nystagmus with a quality alteration of the shocks (after thermal and optokinetic stimulations) underline the possibility of central nervous system modification caused by the neurotrophism of meningococcus bacteria: this neurotrophism can lead to peripheral and central nervous system alterations [18,19]. In the patients with toxic vertigo, the prevailing unidirectional nystagmus justify an alteration in the vestibular nuclei complex and in reticular formation by the action of the drugs, while the asymmetry in the optokinetic response remarks the correlations between the spontaneus and optokinetic nystagmus.
18
The presence of the same ENG abnormalities in the patients with headache shows that the vestibular pathways are also affected in these patients, even when there are no vestibular signs [20]. These modifications can be due to a transitory ischemia of the internal carotid and/or vertebrobasilar systems [21]. The effects of attention levels upon the intensity of the nystagmus, explain our data in the patients with psychogenic vertigo [22]. Peripheral vestibular disturbances lead to labyrinthine paresis or paralysis, sometimes to vestibular hypereflexia. The optical kinetic response is often normal. Thes cochlear alterations highlighted the neurotrophism of the viruses and the surgical complications of the previous petro mastoid evidement [23]. It is evident that vertigo in children is still an unclear problem and it can represent migraine attacks, manifestation of psychologic and somatic problems and serious organic disorders: it is evident that the collaboration between different specialists is needed. The diagnostic techniques are not easily applicable because of the poor cooperation of the patient and radiographic examinations (CT, MRI) effected as a first diagnostic step are unlikely to reveal a specific cause for dizziness [24]. The minimal discomfort and the specificity to determinate a topographic diagnosis of the disease highlight the importance of ENG in children affected by vestibular disorders.
References [1] S. Ravid, R. Bienkowski, L. Eviatar, A simplified diagnostic approach to dizziness in children, Pediatr. Neurol. 29 (2003) 317—320. [2] A. Golz, B. Angel-Yeger, S. Parush, Evaluation of balance disturbances in children with middle ear effusion, Int. J. Pediatr. Otorhinolaringol. 43 (1998) 21—26. [3] R. Probst, Dizziness from a neuro-otological viewpoint, Ther. Umsch. 52 (1995) 724—731. [4] Y.H. Choung, K. Park, S.K. Moon, C.H. Kim, S.J. Ryu, Various causes and clinical characteristics in vertigo in children with normal eardrums, Int. J. Pediatr. Otorhinolaryngol. 67 (2003) 889—894. [5] A. Uneri, D. Turkdogan, Evaluation of vestibular functions in children with vertigo attacks, Arch. Dis. Child. 88 (2003) 510—511.
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[6] P. Vercelletto, J.M. Cler, M. Friol, Vertiges benins de l’enfant, Rev. Otoneuroophtalmol. 51 (1979) 231—238. [7] S.L. Levens, Electronystagmography in normal children, Br. J. Audiol. 22 (1988) 51—56. [8] R.W. Baloh, Differentiating between peripheral and central causes of vertigo, Otolaryngol. Head Neck Surg. 119 (1998) 55—59. [9] M.J. Anoh-Tanon, D. Bremond-Gignac, S.R. Wiener-Vacher, Vertigo is an underestimated symptom of ocular disorders: dizzy children do not always need MRI, Pediatr. Neurol. 23 (2000) 49—53. [10] S.J. Isenberg, Physical and refractive characteristics of the eye at birth and during infancy, in: S.J. Isenberg (Ed.), The Eye in Infancy, Mosby-Year Book, Chicago, 1994, pp. 36—51. [11] R. Haas, Multiple sclerosis and electronystagmography, Wien Med. Wochenschr. 135 (1985) 34—35. [12] M. Fetter, Assessing vestibular function: which tests, when? J. Neurol. 247 (2000) 335—342. [13] A. Salami, M.C. Medicina, M. Dellepiane, R. Mora, G. Guglielmetti, Optokinetic nystagmus and visual-vestibular interaction in subjects with ‘‘whiplash injuries’’, Acta Otorhinolaryngol. Ital. 16 (1996) 91—98. [14] G. Wei, L.S. Yu, C. Liu, G.Q. Li, R. Zhang, S.H. Chen, Electronystagmographic features in some peripheral and central vestibular disorders: application of multiple discriminant analysis of electronystagmographic parameters, ORL J. Otorhinolaryngol. Relat. Spec. 54 (1992) 71—75. [15] K. Kaga, M. Nakamura, N. Furuya, M. Shindo, Analysis of optokinetic nystagmus in patients with lesions on the left unilateral parietal lobe or the entire left hemisphere, Acta Otolaryngol. Suppl. 545 (2001) 166—169. [16] J.H. Allum, M. Ura, F. Honegger, C.R. Pfaltz, Classification of peripheral and central (pontine infarction) vestibular deficits. Selection of a neuro-otological test battery using discriminant analysis, Acta Otolaryngol. 111 (1991) 16—26. [17] H.O. Barber, Positional nystagmus expecially after head injury, Laryngoscope 74 (1964) 891. [18] M.P. Fired, The evaluation of dizziness in children, Laryngoscope 90 (1980) 1548—1560. [19] L. Eviatar, A. Eviatar, Vertigo in children: differential diagnosis and treatment, Pediatrics 59 (1977) 833—838. [20] L.S. Bir, F.N. Ardic, C.O. Kara, O. Akalin, H.S. Pinar, A. Celiker, Migraine patients with or without vertigo: comparison of clinical and electronystagmographic findings, J. Otolaryngol. 32 (2003) 234—238. [21] P. Watson, J.C. Steele, Paroxysmal dysequilibrium in the migraine syndrome of childhood, Arch Otolaryngol. 99 (1974) 177—179. [22] W.E. Collins, Effects of mental set upon vestibular nystagmus, J. Exp. Psychol. 63 (1962) 191. [23] A. Melagrana, V. Tarantino, R. D’Agostino, G. Taborelli, Electronystagmography findings in child unilateral sensorineural hearing loss of probable viral origin, Int. J. Pediatr. Otorhinolaryngol. 42 (1998) 239—246. [24] N. Colledge, S. Lewis, G. Mead, R. Sellar, J. Wardlaw, J. Wilson, Magnetic resonance brain imaging in people with dizziness: a comparison with non-dizzy people, Neurol. Neurosurg. Psychiatry 72 (2002) 587—589.
www.elsevier.com/locate/ijporl
Electronystagmography finding in children with peripheral and central vestibular disorders Angelo Salami, Massimo Dellepiane, Renzo Mora *, Giuseppe Taborelli, Barbara Jankowska ENT Department, University of Genoa, Genoa, Italy Received 24 February 2005; accepted 3 May 2005
KEYWORDS Central vertigo; Children; Electronystagmography; Peripheral vertigo
Summary Objective: Dizziness and imbalance are uncommon in children, but often alarming for their families: a detailed interview and otoneurological examination are important for reaching a specific diagnosis and treatment. Children with vestibular disorders are thought to be difficult to examine: vestibular tests (caloric test, roto-acceleratory test, electronystagmography, opto-kinetic nystagmus, cranio-corpography and posturography) are used less frequently for children than in adult patients. The aim of the study was to determine whether the results of electronystagmography testing improve an emergency physician’s diagnosis of dizziness in children. Methods: Patients were selected on the basis of the following inclusion criteria: aged between 2 and 12 years and affected with vertiginous symptoms. All patients underwent the following instrumental examinations: blood tests, audiological screening, electronystagmography of spontaneous nystagmus or provoked by vestibular and optical stimulation and electroencephalogram. Results: The results underlines an high incidence of central vertigo (83%): 52% of the children presented a prevailing unidirectional nystagmus at labyrinth stimulation and 48% of the children an asymmetry in the response of nystagmus at optical kinetic stimulation with quality alteration of shocks. Conclusions: Electronystagmography can register and evaluate the qualitative and quantitative characteristics of the nystagmic response and allow to distinguish between central or peripheric vertigo: different degrees and various combinations of the abnormal responses shown in optokinetic central test were the most characteristic of electronystagmography in patients with vestibular central vertigo. # 2005 Elsevier Ireland Ltd. All rights reserved.
1. Introduction * Corresponding author. Tel.: +39 01035 37631; fax: +39 01035 37684. E-mail address: [email protected] (R. Mora).
Dizziness and imbalance are uncommon in children, but often alarming for their families causing an extensive, often unnecessary evaluation: we should
0165-5876/$ — see front matter # 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2005.05.001
14
remember that vertigo is rather an abstract concept for a small child, who is unable to distinguish between vertigo and a feeling of fear [1,2]. The evaluation of vertigo in children requires a careful anamnesis together with an evaluation of clinical signs and diagnostics tests: audiometry, tympanometry and electronystagmography (ENG) are the most helpful diagnostic tests [1—3]. Sensation of balance is the result of appropriate information that comes from vestibular, ocular and proprioceptive sensory receptors and is properly integrated within the cerebellum and brain stem: it is often difficult to identify its etiopathogenesis [3]. Vertigo in children can be caused by many disorders: in several reviews peripheral causes are stated to be more common than central causes. The differential diagnosis of vertigo in children is extensive: otitis media and middle ear effusion could be the most common causes of vertigo in children, but there are some problems in detecting the other causes for vertigo because they are one of most frequent diseases of childhood. In children with normal eardrums, who not show otitis media or middle ear effusion, vertigo is most commonly caused by migraine and benign paroxysmal vertigo of childhood (BPVC): these findings show to be very different from those with adult vertigo [1—4]. Central causes of vertigo typically affect older population groups because of the associated risk factors of vascular causes of vertigo: children are more commonly affected by migraine, posttraumatic vertigo (cerebral concussion) and cerebellar tumors [5]. Considering that vestibular tests are used less frequently for children than in adult patients, the aim of the study was to determine the efficacy of ENG testing in the diagnosis of dizziness in children.
2. Methods In this study were enrolled 23 patients selected on the basis of the following inclusion criteria: aged between 2 and 12 years and affected with vertiginous symptoms. The patients were divided into two groups (group A and group B). Group A was formed by 19 children, 10 males and 9 females, aged between 2 and 12 years (mean age 7 years) and affected with central vertigo (six posttraumatic, two meningitic, three toxic, four migrainous and four psychogenic vertigo). All the children that presented a posttraumatic vertigo had experienced an occipital trauma during the month prior to the study. The children with migrainous vertigo showed an ‘‘equivalent migraine sundrome’’ caused
A. Salami et al.
by vasomotor phenomena in the vertebro-basilar systems and characterised by a migraine attack which follows vertigo [6] (Table 1). All the patients of group A presented these symptoms: vertigo, neurovegetative symptoms, intense headache and decrease of postural control (in no case a conscience loss has been noticed). Only seven children presented a spontaneous nystagmus (Table 1). Group B was formed by 4 children, 3 males and 1 female, aged between 3 and 11 years (mean age 5 years) with peripheral vertigo (two viral, one BPVC and one neoplastic vertigo). All these children were affected by intense vertigo crisis and marked neurovegetative symptomatology (nausea, vomit, sweating, abdominal pain etc.): such crises were lasting few minutes and were separated by long remission periods of variable time length. Only one child with viral vertigo presented a spontaneous nystagmus (Table 2). After a careful and detailed anamnesis, all patients underwent the following examinations: complete audiological screening (liminal tonal audiometry, tympanometry, otoacoustic emission and otoacoustic products of distortion); ENG (with thermal labyrinth stimulation, rotatory vestibular stimulation and optokinetic stimulation); electroencephalogram (EEG); pediatric, neurological, neuropsychiatric and to evaluation by an oculist. The child with neoplastic vertigo has not been submitted to the thermal labyrinth stimulation, this child had been previously submitted to petro mastoid evidement. No preparation was necessary for the ENG recording: the children, head blocked, sat on a ‘‘Tonnies rotatory chair Pro model’’ which was placed in the middle of a rotatory cylindrical chamber (2 m in diameter and 1.9 m in height). The rotatory cylinder was lighted from above by a 100 W bulb and was driven by a direct current engine which turned it clockwise and counterclockwise up to 2008/s, maximum speed, with preset acceleration ranging from 18 to 28/s. and its internal area was covered with thirty-two black vertical contrast. Ocular movements was recorded according to the usual method by means of a ‘‘Tonnies electronystagmograph’’ with eight channels: the electrodes were placed to the side, above and below each eye (a ‘‘ground’’ electrode was attached to the forehead). All the subjects underwent to thermal test according to the Fitzgerald-Hallpike method, rotatory vestibular stimulation by stop test from a constant angular velocity of 908/s (be in sense time that anticlockwise) and to ‘‘stare type’’, optokinetic stimulation with a cylinder rotation velocity of 308 for 60 s (be in sense time that anticlockwise):
Central vertigo n
Ny
Thermal labyrinth stimulation Hyporeflexia
Post traumatic 6 Meningitic 2 Toxic 3 Migrainous 4 Psychosomatic 4 Total 19
Rotatory vestibular stimulation
Optokinetic stimulation Asymmetry
I
Prevailing Hyporeflexia Normo-reflexia Hypereflexia Symmetry unidiretional II Monolateral Bilateral Monolateral Bilateral Ny Monolateral Bilateral Monolateral Bilateral
1 0 1 0 0 2
1 1 1 0 0 3
5 1 1 3 1 11
0 0 0 0 0 0
Hypereflexia
3 0 0 0 2 5
0 0 0 0 0 0
0 0 0 1 1 2
3 2 3 3 1 12
1 1 2 0 0 4
3 1 0 0 3 7
1 0 0 0 0 1
1 0 1 0 0 2
0 0 0 4 1 5
1 1 2 1 3 8
ENG finding in children with peripheral and central vertigo
Table 1 Results after the three instrumental stimulations (thermal, rotatory and optokinetic) in the group A (n: number of patients affected by vertigo; Ny I-II: number of patients with spontaneous nystagmus of I and II grade; nono: monolateral; bil: bilateral)
Table 2 Results after the three instrumental stimulations (thermal, rotatory and optokinetic) in the group B (n: number of patients affected by vertigo; Ny I—II: number of patients with spontaneous nystagmus of I and II grade; nono: monolateral; bil: bilateral) Peripheral vertigo n
Ny
Thermal labyrinth stimulation Hyporeflexia
BPVC Viral Neoplastic Total
1 2 1 4
Rotatory vestibular stimulation
Hypereflexia
I
II
Monolateral
Bilateral
Monolateral
Bilateral
Prevailing unidiretional Ny
0 1 0 1
0 0 0 0
0 0 0 0
1 1 0 2
0 0 — 0
0 1 — 1
0 0 0 0
Hyporeflexia
Normo-reflexia
Monolateral
Bilateral
0 0 0 0
1 1 1 3
0 0 0 0
Optokinetic stimulation Hypereflexia Monolateral
Bilateral
0 1 0 1
0 0 0 0
Symmetry
Asymmetry
1 2 1 4
0 0 0 0
15
16
the optokinetic reflex was tested by measuring optokinetic nystagmus slow and fast phases velocity during rotation of the subject in light. Vestibular tests (thermal test and rotatory stimulation) were executed one or two days after optokinetic stimulation and between each stimulation there was a fifteen minutes interval.
3. Results For the analysis of the results we have considered nystagmus slow phase after the three instrumental stimulations (thermal, rotatory and optokinetic). In the group A 12 children presented a prevailing unidirectional nystagmus after thermal labyrinth stimulation: these patients were affected by posttraumatic (n = 3), meningitic (n = 2), toxic (n = 3), migrainous (n = 3) and psychogenic vertigo (n = 1) (Table 1). After the rotatory vestibular stimulation 11 children presented vestibular hyporeflexia (7 bilateral and 4 monolateral), 7 vestibular hypereflexia (5 bilateral and 2 monolateral) and one child normoreflexia (Table 1). In the same group (group A), 11 children showed an asymmetry in the response of nystagmus with a quality alteration of shocks (of their morphology) after optokinetic stimulation: five of these presented a posttraumatic vertigo, three a migrainous vertigo, one a meningitic vertigo, one a psychogenic vertigo and one a toxic vertigo (Table 1). This asymmetry was revealed by a low amplitude and a significantly impaired slow-phase velocity (SPV) of nystagmus: the impaired SPV was of the right optokinetic pattern in six patients (three of these affected by posttraumatic, two migrainous and one meningitic vertigo) and of the left optokinetic pattern in five patients (two with a posttraumatic vertigo, one a migrainos vertigo, one a psycosomatic vertigo and one a toxic vertigo) (Table 1). EEG showed changes of cortical electrical activity in two patients (a cortex increase in the relative theta activity in the centrotemporal region and a decrease of centroparietal beta activity): these patients were affected by meningitic vertigo and presented an impaired slow-phase velocity of nystagmus. In the group B EEG did not show any changes of cortical electrical activity. In the same group by group B, after thermal labyrinth stimulation the ENG showed a bilateral vestibular hyporeflexia in two patients and a bilateral vestibular hypereflexia in one child; after the rotatory vestibular stimulation three children pre-
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sented bilateral vestibular hyporeflexia and one child monolateral vestibular hypereflexia, no patients presented ENG abnormalities after optokinetic stimulation: in all the children there was no asymmetry between the SPV of nystagmus (Table 2). The audiological screening has highlighted cochlear alterations in three cases: a bilateral sensorineural hearing lost in the two children with viral vertigo and a monolateral transmissive hypoacusia in the child with neoplastic vertigo.
4. Discussion Vestibular evaluation in the pediatric population has in the past taken several forms: for the most part, the pediatric vestibular evaluation has been more subjective than objective. One of the primary reasons for this has been the obvious difficulties encountered in trying to conduct a standard adult procedure on a pediatric patient [7]. Our experience has shown that children tolerate ENG testing easily and the discomfort is minimal. Sensation of balance is the result of appropriate information that comes from vestibular, ocular and proprioceptive sensory receptors and is properly integrated within the cerebellum and brain stem: it is often difficult to identify its etiopathogenesis: ENG can perform an analysis of these systems by itself or in conjunction with others tests data [3]. The history usually provides the key information for distinguishing between peripheral and central causes of vertigo. The duration of attacks is most helpful in distinguishing between central and peripheral causes: vertigo associated with vertebrobasilar insufficiency typically lasts minutes, whereas peripheral inner ear causes of recurrent vertigo typically last hours [8]. Vertigo, instability, dizziness, or equilibrium disorders are not usually considered as consequences of ophthalmologic problems: ocular disorders can be responsible for these symptoms in children [9]. The visual system is not mature at birth and continues to develop during infancy; during this period various abnormalities can appear and become symptomatic (vergence insufficiency, latent strabismus with binocular vision and anisometropia). Failures in binocular vision or in convergence can be responsible for inadequate gaze stabilization during movement and double or blurry vision during fixation, which could generate a sensation of imbalance and dizziness [10]. Child complaining of vertigo or dizziness but with normal clinical somatic neurologic and vestibular examinations should have a complete ophthalmologic examination before additional, more costly,
ENG finding in children with peripheral and central vertigo
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Fig. 1 Asymmetry of the nystagmus response in a patient with post-traumatic vertigo, after optokinetic stimulation (A: left cylinder rotation; B: right cylinder rotation).
investigations: this should lead to better screening and more appropriate care of ocular disorders in children and avoid unnecessary magnetic resonance imaging [9]. On the other hand, disorders of balance are much more frequent but the factors involved are numerous and the role of the vestibular system is often debatable: as a matter of fact, there are many kinds of nystagmus which are not related to any changes in the vestibular system, but which are rather more part of the overal changes of conjugated eye movements [11]. Seen in this light, ENG by exploring the different kinds of conjugated eye movement, can help decisively in the diagnosis: ENG can record and evaluate the qualitative and quantitative characteristics of the nystagmic response and allow to distinguish between central or peripheral vertigo. Central or peripheral nystagmus can usually be distinguished by other features in the history or on clinical examination: the presence of a spontaneous nystagmus with fixation indicates a probable central lesion while the presence of a spontaneous nystagmus without fixation a probable peripheric lesion, positional nystagmus is indicative of a central lesion if it has no latency and it is present only when the head is in a particular position, peripheral vestibular lesions usually lead to a mixed horizontal-torsional or vertical-torsional nystagmus, a pure vertical or pure torsional nystagmus is always caused by a central lesion [12,13]. By ENG it is possible to record and study the nystagmus, either spontaneous or provoked. Spontaneous nystagmus can be observed in the different position of the glance with open eyes, or eliminating the fixation in the dark or with close eyes. Provoked nystagmus is analysed by caloric stimulation, rotatory stimulation and the study of the flash-inducednystagmus [13]. Diagnosis of central neurological disturbances is submitted to four conditions: specific criteria selection, complete oculomotor and vestibular testing,
graduated conclusions in function of the acquired data and not only an etiological but a functional or topographical diagnosis. Central vestibular syndromes lead also to labyrinthine weakness or nystagmus directional preponderance but, first at all, to specific criteria who are: saccadic, pursuit and horizontal optokinetic abnormalities, central spontaneous or positional nystagmus, failure of fixation suppression, hyperreflexia, perverted nystagmus, slowing of the nystagmus fast phases, slowing-down of the nystagmus slow phases, asymmetry of the nystagmus, vertical optokinetic deficits and retraction nystagmus [14] (Fig. 1). According with other authors, in central vertigo ENG recordings showed typical asymmetry of the optokinetic pattern. This asymmetry was revealed by a low amplitude and a significantly impaired slow-phase nystagmus velocity of the optokinetic pattern [15,16]. In the patients affected by post-traumatic vertigo, the vestibular and optokinetic abnormalities indicate that as an occipital trauma can lead to an haemorrhage of the frontal and temporal area near the cortical projection of the vestibular pathway [17]. In patients with meningitic vertigo, the prevailing unidirectional nystagmus and the asymmetry in the response of nystagmus with a quality alteration of the shocks (after thermal and optokinetic stimulations) underline the possibility of central nervous system modification caused by the neurotrophism of meningococcus bacteria: this neurotrophism can lead to peripheral and central nervous system alterations [18,19]. In the patients with toxic vertigo, the prevailing unidirectional nystagmus justify an alteration in the vestibular nuclei complex and in reticular formation by the action of the drugs, while the asymmetry in the optokinetic response remarks the correlations between the spontaneus and optokinetic nystagmus.
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The presence of the same ENG abnormalities in the patients with headache shows that the vestibular pathways are also affected in these patients, even when there are no vestibular signs [20]. These modifications can be due to a transitory ischemia of the internal carotid and/or vertebrobasilar systems [21]. The effects of attention levels upon the intensity of the nystagmus, explain our data in the patients with psychogenic vertigo [22]. Peripheral vestibular disturbances lead to labyrinthine paresis or paralysis, sometimes to vestibular hypereflexia. The optical kinetic response is often normal. Thes cochlear alterations highlighted the neurotrophism of the viruses and the surgical complications of the previous petro mastoid evidement [23]. It is evident that vertigo in children is still an unclear problem and it can represent migraine attacks, manifestation of psychologic and somatic problems and serious organic disorders: it is evident that the collaboration between different specialists is needed. The diagnostic techniques are not easily applicable because of the poor cooperation of the patient and radiographic examinations (CT, MRI) effected as a first diagnostic step are unlikely to reveal a specific cause for dizziness [24]. The minimal discomfort and the specificity to determinate a topographic diagnosis of the disease highlight the importance of ENG in children affected by vestibular disorders.
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