Application of the Video Head Impulse Test in the diagnostics of the balance system in children

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Application of the Video Head Impulse Test in the diagnostics of the balance system in children Zastosowanie testu VHIT w diagnostyce układu równowagi u dzieci Pepaś Renata 1, Pyda-Dulewicz Agata 2, Śmiechura Małgorzata 1, Konopka Wiesław 1,2 1 Department of Otolaryngology Institute of Polish Mother Health Centre in Lodz 2 Teaching Department of Pediatrics, Medical University of Lodz Article history: Received: 17.03.2015 Accepted: 17.04.2015 Published: 30.06.2015 ABSTRACT: KEY WORDS: Introduction. VHIT (Video Head Impulse Test) is one of the new methods of testing the balance system. This test is used in the diagnostics of peripheral damage to the balance system with the use of the vestibulo-ocular reflex. The vestibulo-ocular reflex is the eye movement in the opposite direction to the direction of head rotation. It is observed in newborns, normalizes until 2 months of age, and matures within the first two years of life. The VHIT test allows to determine the site of a canal injury within the vestibular system. Material and method. The study included 28 patients aged from 5 to 18 years, including 9 children with vertigo and 19 healthy children. All patients underwent VHIT with the registration of the vestibulo-ocular reflex and ocular lag factor (gain) evaluation. Moreover, a full videonystagmography test was conducted in patients with dizziness. Results. In the group of healthy children, normal results of gain were observed in 16 patients. In the group of children with vertigo, we diagnosed damage of the peripheral part of the balance system in 2 children on the basis of the VNG test. VNG test results in these patients coincide with the results of the VHIT test for individual lateral semicircular canals. We observed vertigo without an injury within the peripheral parts of the balance organ in 7 children. In 4 patients in that group we observed abnormal VHIT test results. Conclusions. The VHIT test enables to perform a rapid and non-invasive screening analysis of the vestibulo-ocular reflex, and to detect damage to the individual semicircular canals. The VHIT test can complement the diagnostics of vertigo in the clinical setting, as well as be an option for children who do not tolerate standard VNG testing. labyrinth, cerebellum, vestibular-cochlear nerve, nystagmus, dizziness STRESZCZENIE: Wstęp. Jedną z nowych metod badania układu równowagi jest VHIT (Video Head Impulse Test). Jest używany w diagnostyce obwodowego uszkodzenia układu równowagi i wykorzystuje odruch przedsionkowo-oczny, który polega na ruchu gałek ocznych w przeciwnym kierunku do kierunku obracania głowy. Odruch przedsionkowo- -oczny u noworodków jest słaby, normalizuje się do 2. miesiąca życia i dojrzewa w ciągu pierwszych 2 lat życia. Test VHIT pozwala na określenie miejsca uszkodzenia kanałowego w obrębie narządu przedsionkowego. Materiał i metoda. Badaniem objęto 28 osób w wieku od 5 do 18 lat, w tym dziewięcioro dzieci z zawrotami głowy i 19 dzieci zdrowych. U badanych przeprowadzono szczegółowy wywiad, badanie laryngologiczne i otoneurologiczne, a także diagnostykę audiologiczną. U wszystkich badanych wykonano badanie VHIT z rejestracją odruchu przedsionkowo-ocznego i oceną współczynnika nadążania (gain). W grupie osób z zawrotami głowy dodatkowo przeprowadzono badanie wideonystagmograficzne. Wyniki.W grupie dzieci zdrowych prawidłowe wyniki współczynnika nadążania (gain) stwierdzono u 16 pacjentów. 6 DOI: 10.5604/20845308.1150794 WWW.OTORHINOLARYNGOLOGYPL.COM

W grupie dzieci z zawrotami głowy na podstawie pełnego badania VNG u dwóch pacjentów rozpoznano uszkodzenie obwodowej części układu równowagi. Wyniki testu VNG u tych pacjentów pokrywały się z wynikami badania VHIT dla poszczególnych kanałów półkolistych bocznych. U siedmiorga dzieci z zawrotami głowy nie stwierdzono uszkodzenia obwodowej części układu równowagi. U czterech pacjentów w tej grupie zaobserwowano nieprawidłowe wyniki testu VHIT. Wnioski. Test VHIT pozwala w sposób szybki i nieinwazyjny przeprowadzić przesiewową analizę odruchu przedsionkowo-ocznego i wykryć uszkodzenie na poziomie poszczególnych kanałów półkolistych. Test VHIT może stanowić uzupełnienie diagnostyki zawrotów głowy w warunkach klinicznych, a także być rozwiązaniem dla dzieci, które źle znoszą standardowe testy VNG. SŁOWA KLUCZOWE: błędnik, móżdżek, nerw przedsionkowo-ślimakowy, oczopląs, zawroty głowy INTRODUCTION Vertigo may be observed in diseases of various aetiology, severity and frequency [1]. It is a symptom of numerous pathological entities ranging from mild disorders to severe diseases whose early diagnosis may play a significant role for the patient s further life. It is also very frequently an expression of functional disorders that do not have a somatic background. Vertigo is a pathology that affects not only adults but also children. Vestibular disorders, which are observed in young patients as the basic symptoms, are not observed frequently and it is difficult to classify them [2,3]. It is estimated that they affect 20-30% of the adult population, and 8-18% of the paediatric population [4]. Epidemiological studies conducted on a large group of children (2165) indicated that vertigo was observed in 14% of the children [5]. It is important to determine whether vertigo is central or peripheral in nature, and whether there are other symptoms that could suggest systemic diseases or functional disorders [6]. The nervous system matures at the age of 4-5 years, and only then can all tests, which are used for adults, be applied to children (static-dynamic tests Romberg s test, Romberg-Foy s and Unterberger s test, cerebellar tests diadochokinesis, the finger-to-nose test and past-pointing test) [7, 8]. Electronystagmography (ENG) or videonystagmography (VNG) are the most common diagnostic tests and enable the diagnostics of vertigo or balance disorders by registering nystagmus - an important diagnostic symptom. They do not provide responses to all questions, and that is why they cannot be the only examination, on the basis of which the diagnosis is made. VHIT (Video Head Impulse Test) is a method used for the assessment of the balance organ. It utilises the vestibulo-ocular reflex (VOR), evoked in the Halmagyi and Curthoys test. VHIT enables to determine the exact location of a canal injury within the vestibular organ [9]. MATERIAL AND METHOD A total of 28 patients were included in the study: 18 girls and 10 boys aged 5-18 (mean value for age 12.62 +/- 4.36 years), including 9 children with vertigo and 19 healthy children. Diagnostics included a detailed interview, laryngological and otoneurological examination with the evaluation of spontaneous nystagmus, static and dynamic tests. Audiological diagnostics performed in the patients included pure tone audiometry and impedance audiometry. VHIT was performed with the registration of the vestibulo- -ocular reflex and the evaluation of gain. Excitability symmetry was determined using the Halmagyi and Curthoys test in the study group. Computer analysis of VHIT was possible thanks to the camera mounted inside the goggles that registered the vestibulo-ocular reflex. The reflex was evoked passively. When evaluating the semicircular lateral canals, the patient s head was moved horizontally, at first to the right, and then to the left side, and, when evaluating the anterior and posterior semicircular canals, the head was turned vertically by 30 degrees. The eyesight of the patient was fixed on the point located frontally 1 m from the patient. In order to achieve correct results, it was necessary to move the patient s head by 20 degrees, 20 times. The researchers tried to keep movement acceleration at 1000-2500 degrees/s. Quantitative test analysis was based on the determination of the mean value of gain, i.e. an indicator of the correctness of head movement reproduction by the movement of the eyeballs. The perfect value of this coefficient is 1. The authors of VHIT suggest that results lower than 1 are usually achieved by healthy people (within the range of 0.8-0.9) but the result depends on the individual sensitivity of vestibular afference and on the anatomical arrangement of the semicircular canals. In the group of 9 patients with vertigo, videonystagmography was also performed, including the evaluation of spontaneous POLSKI PRZEGLĄD OTORYNOLARYNGOLOGICZNY, TOM 4, NR 2 (2015), s. 6-11 7

nystagmus, eye movement tests (pendulum-swing test, saccades, optokinesis), and postural tests according to Nylen. Moreover, the Fitzgerald-Hallpike caloric test was performed in the patients with the assessment of canal paresis (CP) and directional preponderance (DP). RESULTS No pathology in laryngological or otoneurological examinations was observed in any of the patients. The results of hearing tests were within normal values. In the healthy children group (without balance disorders in history) normal values of gain were observed in 16 patients. A symmetrical decrease in the response from the lateral semicircular canals was observed in one person. Weaker response from the right posterior lateral semicircular canal was observed in two subjects with normal VNG values. Full VNG was performed in the group of children with vertigo. The children were classified into the following groups on the basis of its results: Patients with damage to the peripheral part of the vestibular balance organ (2 children) Patients without damage to the peripheral part of the vestibular balance organ (7 children) In the first group features of canal paresis were observed without directional preponderance, with normal results of the eye movement test and postural test. A compensation injury to the peripheral part of the organ of balance was observed in one child on the right side, in another on the left side. The results of VNG in those patients coincided with VHIT for particular lateral semicircular canals. In the second group, spontaneous nystagmus was not observed in VNG in any of the patients. The results of eye movement tests, positional tests, and caloric tests in this group were within normal values. VHIT showed the following results in this group: In two patients, a symmetrical decrease in the values of gain was observed. The values were below normal limits for both lateral semicircular canals. In two people, a decrease in the gain value was observed for lateral semicircular canals on the right side (Tab. I and II). Tab. I. Mean values for gain for each semicircular canal in the healthy children group DISCUSSION LATERAL L LATERAL R LA RP LP RA gain mean value 0.90 0.89 1.11 1.06 1.03 0.96 Standard deviation 0.21 0.26 0.26 0.33 0.35 0.39 Tab. II. Mean values for gain for each semicircular canal in the group of children with vertigo. LATERAL L LATERAL R LA RP LP RA gain mean value 0.60 0.75 0.91 1.12 1.23 1.12 Standard deviation 0.,33 0.19 0.36 0.26 0.19 0.2 Numerous different tests and measurements, which require specialist knowledge and experience or medical equipment, are used in contemporary clinical practice. The observation of nystagmus, both spontaneous and induced, deserves particular attention in otoneurological diagnostics. Constant advancement in the already-existing techniques used for its observation significantly decreases the testing time and enables to provide a more precise diagnosis. Recording nystagmus and its parameters, such as free-phase angular velocity or frequency, is possible thanks to the use of videonystagmography. Nowadays, VNG constitutes one of the basic methods in otoneurological diagnostics [10]. The development of VNG dates back to the 1990 s and started in 1991 when dr. Eric Ulmer, developed the first prototypes of videonystagmographs in cooperation with Philippe Guilemant. This method is based on the registration of eye movement with the use of a very sensitive (<1 Lux) infrared camera. The records of eye-pupil movement can be achieved, and they can be analysed later using specialist software. This method is not devoid of disadvantages, especially in diagnostics of paediatric patients, even though it is more modern. During VNG it is essential to keep a homogenous image of the pupil, with maximum black colour intensity and high contrast (blinking, lachrymation). The young children s fear of total, enforced darkness should be taken into account when performing records with fixation exclusion. Relatively long duration of the test is an important disadvantage and often constitutes a big problem, as young patients are frequently impatient. The full set of tests included in VNG lasts approximately 1 hour [11]. 8 WWW.OTORHINOLARYNGOLOGYPL.COM

VHIT (Videonystagmography Head Impulse Test) is another examination used for the assessment of the balance system. It is a valuable test and it used for the diagnostics of peripheral injury to the balance organ and utilises the vestibulo-ocular reflex (VOR) evoked in the Halmagyi and Curthoys test [12]. The vestibulo-ocular reflex is a phenomenon in which the contralateral movement of the eyeball accompanies the movement of the head. Its role is the stabilisation of the picture on the retina. Its latency time is very short (approximately 15 ms), thanks to which the picture on the retina is stable even if the movements of the head are very fast. Information concerning the movement of the head comes from the vestibular organ. Receptors that receive the information concerning rotational movement are located within the ampullary crests of the semicircular canals, and for linear movement within the otolith organ of the saccule (for vertical movement) and utricle (horizontal movement). VOR provides compensation eyeball movements for the head movement in all planes. According to the Ewald s first law, eyeball movements, which compensate angular acceleration of the head, develop due to excitation generated asymmetrically in the corresponding semicircular canals. The information from the vestibular organ is transmitted to the vestibular nuclei and it is later transmitted to the oculomotor nuclei and oculomotor muscles. If the rotational movement of the head is constant, eyeballs move smoothly until they reach their maximum amplitude within the socket (slow nystagmus phase). Later, they return to the central location in the component motion (fast nystagmus phase) [13-17]. The vestibulo-ocular reflex is weak in neonates and it normalises until the age of 2 months and matures within the first 2 years of life [18]. The vestibulo-ocular reflex became the basis for numerous research methods that make it possible to direct further detailed otoneurological diagnostics relatively quickly. These methods include: caloric test, head-thrust test, Halmagyi and Curthoys test (H-C, HIC). The basic concept of the Halmagyi test is to perform quick movements of the head in the plane of particular semicircular canals. The examination includes the monitoring of eyeball movements with the patient s eyesight focused on an immobile target, while his/her head is moving vigorously to the left and to the right within the plane of the semicircular canals. Patients with a defective canal cannot follow a fast head rotation and that is why one can observe saccadic catching-up movements after the impulses of the head to the affected side are observed. The use of a video camera in the test and computer analysis of the eyeball movement enables to observe the movements that are invisible with a naked eye [19,20]. The VHIT examination enables quick and non-invasive screening of the vestibulo-ocular reflex. This system seems to be a useful clinical tool for the diagnostics and classification of disorders affecting the peripheral part of the vestibular organ by identifying overt and covert saccades and measuring the vestibulo-ocular reflex (VOR) [21]. According to MacDougal et al. [22], VHIT can increase the specificity of diagnostics in the patients with acute and sudden vertigo at emergency departments. The measurement system is easy to use in the clinical environment and provides objective measurements of the vestibulo-ocular reflex (VOR). Both overt and covert saccades in patients with vestibular organ disorders are detected in this examination. The measurements are performed quickly (approximately 10 minutes) and are non-invasive. Moreover, the automated analytic software generates results immediately. It is possible to identify an ipsilateral vestibulo-ocular reflex disorder in patients with acute vestibular neuritis, even if it is accompanied by spontaneous nystagmus. In the presented material, it was observed that VHIT corresponded with VNG in the group of children with vertigo in cases in which compensated labyrinth excitability was decreased. Nevertheless, abnormal VHIT results and normal VNG results were observed in more than a half of the patients (57%) in the group of subjects in whom no features of peripheral damage to the balance organ were observed. The differences in VHIT and caloric test results acquired in VNG were analysed in a similar manner as in the study by Rambold [23] that comprised 1063 patients. Abnormal results were observed in 13.3% of the patients in both tests, in 4.6% of the patients only the VNG result was abnormal. The author suggests that performing VHIT as the first test, and caloric examination as the second one only in patients with abnormal VHIT results would limit the time required for the diagnostics in most patients affected by vertigo. It does not concern patients with migraine headaches and Meniere s disease, in whom performing the caloric test as the first one seems more effective. Similarly, Bell et al. [24] concluded in their study that VHIT may be a useful addition to vestibular tests but it should not be treated as an alternative. Marzec et al. [19] did not observe any relationship between the values of gain in VHIT and the severity of canal paresis and directional preponderance in the caloric test in their studies. The authors suggest that more attention should be paid in further analyses concerning the VHIT test to the alleged bigger capacity for the correction of the vestibulo-ocular reflex in right-handed people that exhibit directional preponderance to the right side (aspect of vestibular tension at the central level) may influence the gain value [19]. POLSKI PRZEGLĄD OTORYNOLARYNGOLOGICZNY, TOM 4, NR 2 (2015), s. 6-11 9

CONCLUSIONS The VHIT test enables fast and non-invasive screening analysis of the vestibulo-ocular reflex which detects damage to particular pairs of semicircular canals. VHIT is a supplementation of diagnostics concerning the location of damage to the vestibular organ in the clinical environment. Also, it may be a solution for children who are not comfortable with standard VNG tests. References 1. Józefowicz-Korczyńska M., Łukomski M., Pajor A.: Ocena elektronystagmograficzna stanu narządu przedsionkowego u chorych z szumami usznymi i zmianami zwyrodnieniowymi odcinka szyjnego kręgosłupa. Otolaryngol. Pol., 2004, 58, 2, 349-247. 2. Santana Fonseca A., Davidsohn V., Angeleri S.: Correlation between dizziness and impaired glucose metabolism. Rev. Bras. Otorhinolaryngol., 2006, 72, 3, 367-369. 3. Talaska A. E., Schacht J.: Współczesne spojrzenie na uszkodzenia słuchu spowodowane lekami. Otorynolaryngol., 2006, 5, 1, 7-12. 4. Lempert T., Neuhauser H.: Epidemiology of vertigo, migraine and vestibular migraine. J. Neurol. 2009, 256, 333 338. 5. Prusiński A.: Zawroty głowy. PZWL, Warszawa 2001. 6. Pilarska E., Konieczna S., Lemka M.: Zawroty głowy u dzieci klasyfikacja, przyczyny, objawy, diagnostyka. Neurologia Dziecięca, 2012, 21, 42, 53-58. 7. Pierchała K., Janczewski G.: Zawroty głowy. OINPHARMA, Warszawa 2008. 8. Pajor A., Gryczyński M., Łukomski M., Józefowicz-Korczyńska M.: Stan narządu przedsionkowego u chorych z odbiorczym uszkodzeniem słuchu. Otolaryngol. Pol., 2002, 56, 6, 707-712. 9. Mangabeira Albernaz P.L., Zuma E Maia F.C.: The video head impulse test. Acta Otolaryngol. 2014, 134, 12, 1245-50. 10. Pyda-Dulewicz A., Pepaś R., Konopka W.: Trudności w diagnostyce i rehabilitacji zawrotów głowy i zaburzeń układu równowagi u dzieci. Rehabilitacja w praktyce, 2015, 1, 64-69. 11. Pepaś R., Śmiechura M., Konopka W.: Ocena sprawności układu przedsionkowego u dzieci z zaburzeniami równowagi. Otorynolaryngologia, 2014, 13, 1, 36-41. 12. Olszewski J., Pietkiewicz P., Miłoński J., Bielińska M.: Zastosowanie testu VHIT (Videonystagmography Head Impulse Test) w diagnostyce uszkodzeń kanałów półkolistych. Otolaryng. Pol., 2010, 64, 7, 32-35 13. Leigh R.J., Zee D.S.: The neurology of eye movements. Oxford University Press, New York 2006. 14. Wong A.M.F.: Eye movement disorders. Oxford University Press, New York 2008. 15. Krauzlis R..J. Eye movements. W.: Squire L.R. (red.). Fundamental neuroscience. Wyd. 3. Elsevier, Amsterdam 2008, 775 792. 16. Gawron-Koziorowska E., Budrewicz S., Jadanowski K.: Patofizjologia zaburzeń gałkoruchowych w niektórych schorzeniach ośrodkowego układu nerwowego. Pol. Przegl. Neurol. 2009, 5, 117 122. 17. Schweigart G., Mergner T., Evdokimidis I., Morand S., Becker W.: Gaze stabilization by optokinetic reflex (OKR) and vestibulo-ocular reflex (i) during active head rotation in man. Vision Res. 1997, 12, 1643 1652. 18. Fife T.D., Tusa R.J., Furman J.M.: Assessment: Vestibular testing techniques in adults and children. Neurology 2000, 55, 10, 1431-41. 19. Marzec M, Pawlak-Osińska K., Kaźmierczak H.: Znaczenie testu Halmagyi i Curthoysa w standardowej diagnostyce otoneurologicznej chorych z zaburzeniami przedsionkowymi. Otolaryngologia Polska, 2014, 68, 2, 89-93. 20. Halmagyi G.M., Curthoys I.S.: A clinical sign of canal paresis. Arch Neurol 1988, 45, 7, 737 739. 21. Curthoys I.S.: The Interpretation of clinical tests of peripheral vestibular function; Laryngoscope 2012, 122, 1342-1352 22. MacDougall H.G., Weber K.P., McGarvie L.A., Halmagyi G.M., Curthoys I.S.: The video head impulse test - Diagnostic accuracy in peripheral vestibulopathy; Neurology. 2009, 6, 73, 14, 1134 1141. 23. Rambold H.A.: Economic management of vertigo/dizziness disease in a county hospital: video-head-impulse test vs. caloric irrigation.eur. Arch.Otorhinolaryngol. 2014 Jul 31. 24. Bell S.L., Barker F., Heselton H., MacKenzie E., Dewhurst D., Sanderson A.: A study of the relationship between the video head impulse test and air calorics. Eur. Arch.Otorhinolaryngol. 2014 Nov 23. 10 WWW.OTORHINOLARYNGOLOGYPL.COM

Word count: 1749 Tables: 2 Figures: References: 24 Access the article online: DOI: 10.5604/20845308.1150794 Full-text PDF: www.otorhinolaryngologypl.com/fulltxt.php?icid=1150794 Corresponding author: Wiesław Konopka wieslaw.konopka@umed.lodz.pl Copyright 2015 Polish Society of Otorhinolaryngologists Head and Neck Surgeons. Published by Index Copernicus Sp. z o.o. All rights reserved Competing interests: The authors declare that they have no competing interests. Cite this article as: Pepaś R., Pyda-Dulewicz A., Śmiechura M., Konopka W.: Application Video Head Impulse Test in the diagnosis of balance system in children. Pol Otorhino Rev 2015; 4(2): 6-11 POLSKI PRZEGLĄD OTORYNOLARYNGOLOGICZNY, TOM 4, NR 2 (2015), s. 6-11 11