Long-Term Impact of Recurrent Acute Otitis Media on Balance and Vestibular Function in Children
Abstract
:1. Introduction
2. Materials and Methods
2.1. Setting
2.2. Participants
- -
- Age of 8 years;
- -
- Documented history of rAOM, defined as at least four episodes of AOM within a single year;
- -
- No episodes of otitis media (OME, AOM, or CSOM) in the 12 months prior to this study.
- -
- Any congenital malformations or diseases affecting the outer, middle, or inner ear;
- -
- History of ear surgery, including myringoplasty, tympanoplasty, exploratory tympanotomy, stapedectomy, myringotomy, and tympanostomy tube placement;
- -
- Congenital cytomegalovirus infection;
- -
- Genetic syndromes or mutations known to be associated with HL;
- -
- Clinical evidence of otitis media (OME, AOM, or CSOM) at the time of this study;
- -
- Recent head trauma, exposure to loud noises, or use of ototoxic drugs;
- -
- Any systemic diseases;
- -
- Any neurological disorders;
- -
- Any musculoskeletal disorders;
- -
- Any ocular or visual disorders.
2.3. Clinical Assessments
- -
- Detailed medical history: a thorough medical history was taken, focusing on the total number of AOM episodes, age at first diagnosis of AOM, and previous presence of otorrhea.
- -
- Otomicroscopy: this allowed for detailed visualization of the external auditory canal and TM, helping to exclude any external or middle ear pathologies.
- -
- Pure-tone audiometry (125 Hz to 8000 Hz): air and bone conduction audiometry was conducted using the Piano clinical audiometer by Inventis (Padua, Italy) to assess the presence of conductive, sensorineural, or mixed HL.
- -
- Tympanometry: this was performed using the Clarinet clinical tympanometer by Inventis (Padua, Italy) to assess the mobility of the TM.
- -
- Spontaneous nystagmus assessment: This was undertaken using GIMA Frenzel glasses with fixed, biconvex lenses of 18.0 diopters (Gessate, Italy). These lenses eliminate visual fixation, enabling clear observation of eye movements.
- -
- Static posturography: This was conducted using the SVeP (Standard Vestibology Platform) by Politecnica (Modena, Italy), a professional stabilometric system used for postural analysis. The platform is a stable force plate (50 cm × 50 cm × 7 cm, 12 kg) with three strain-gauge force transducers arranged in an equilateral triangle (400 mm). Tests were performed with a fixed visual target at a distance of 1.20 m at eye level in a quiet room. Children stood barefoot on the platform with their arms by their sides, following strict foot placement instructions.
- Eyes open (EO): firm surface with eyes open, utilizing all sensory inputs;
- Eyes closed (EC): firm surface with eyes closed, removing visual input;
- PAD EO: foam pads with eyes open, reducing somatosensory input;
- PAD EC: foam pads with eyes closed, removing visual input and reducing somatosensory input.
2.4. Statistical Analysis
3. Results
4. Discussion
Limitations and Future Prospects
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Sinno, S.; Dumas, G.; Mallinson, A.; Najem, F.; Abouchacra, K.S.; Nashner, L.; Perrin, P. Changes in the Sensory Weighting Strategies in Balance Control Throughout Maturation in Children. J. Am. Acad. Audiol. 2021, 32, 122–136. [Google Scholar] [CrossRef] [PubMed]
- Tran, H.T.; Li, Y.C.; Lin, H.Y.; Lee, S.D.; Wang, P.J. Sensory Processing Impairments in Children with Developmental Coordination Disorder. Children 2022, 9, 1443. [Google Scholar] [CrossRef] [PubMed]
- Janky, K.L.; Rodriguez, A.I. Quantitative Vestibular Function Testing in the Pediatric Population. Semin. Hear. 2018, 39, 257–274. [Google Scholar] [CrossRef] [PubMed]
- Aldè, M.; Fancello, V.; Di Mauro, P.; Canelli, R.; Zaouche, S.; Falanga, C. Audiological and Vestibular Follow-Up for Children with Congenital Cytomegalovirus Infection: From Current Limitations to Future Directions. Children 2024, 11, 1211. [Google Scholar] [CrossRef]
- Wiener-Vacher, S.R.; Quarez, J.; Priol, A.L. Epidemiology of Vestibular Impairments in a Pediatric Population. Semin. Hear. 2018, 39, 229–242. [Google Scholar] [CrossRef]
- Brodsky, J.R.; Cusick, B.A.; Zhou, G. Evaluation and management of vestibular migraine in children: Experience from a pediatric vestibular clinic. Eur. J. Paediatr. Neurol. 2016, 20, 85–92. [Google Scholar] [CrossRef]
- Aldè, M.; Zanetti, D.; Ambrosetti, U.; Monaco, E.; Gasbarre, A.M.; Pignataro, L.; Cantarella, G.; Barozzi, S. Unilateral Sensorineural Hearing Loss in Children: Etiology, Audiological Characteristics, and Treatment. Children 2024, 11, 324. [Google Scholar] [CrossRef]
- Pinninti, S.G.; Britt, W.J.; Boppana, S.B. Auditory and Vestibular Involvement in Congenital Cytomegalovirus Infection. Pathogens. 2024, 13, 1019. [Google Scholar] [CrossRef]
- Rücklová, K.; von Kalle, T.; Koitschev, A.; Gekeler, K.; Scheltdorf, M.; Heinkele, A.; Blankenburg, F.; Kötter, I.; Hospach, A. Paediatric Cogan’s syndrome—Review of literature, case report and practical approach to diagnosis and management. Pediatr. Rheumatol. Online J. 2023, 21, 54. [Google Scholar] [CrossRef]
- Golz, A.; Westerman, S.T.; Gilbert, L.M.; Joachims, H.Z.; Netzer, A. Effect of middle ear effusion on the vestibular labyrinth. J. Laryngol. Otol. 1991, 105, 987–989. [Google Scholar] [CrossRef]
- Monsanto, R.D.C.; Kasemodel, A.L.P.; Tomaz, A.; Paparella, M.M.; Penido, N.O. Current evidence of peripheral vestibular symptoms secondary to otitis media. Ann. Med. 2018, 50, 391–401. [Google Scholar] [CrossRef] [PubMed]
- Schilder, A.G.M.; Chonmaitree, T.; Cripps, A.W.; Rosenfeld, R.M.; Casselbrant, M.L.; Haggard, M.P.; Venekamp, R.P. Otitis media. Nat. Rev. Dis. Primers. 2016, 2, 16063. [Google Scholar] [CrossRef] [PubMed]
- Rosenfeld, R.M.; Shin, J.J.; Schwartz, S.R.; Coggins, R.; Gagnon, L.; Hackell, J.M.; Hoelting, D.; Hunter, L.L.; Kummer, A.W.; Payne, S.C.; et al. Clinical Practice Guideline: Otitis Media with Effusion (Update). Otolaryngol. Head Neck Surg. 2016, 154 (Suppl. S1), S1–S41. [Google Scholar] [CrossRef] [PubMed]
- Aldè, M.; Marchisio, P.; Folino, F.; Ambrosetti, U.; Di Berardino, F.; Barozzi, S.; Zanetti, D.; Pignataro, L.; Cantarella, G. Otitis Media With Effusion After the COVID-19 Pandemic: Return to the Past and New Lessons. Otolaryngol. Head Neck Surg. 2024, 171, 724–730. [Google Scholar] [CrossRef] [PubMed]
- Chiappini, E.; Ciarcià, M.; Bortone, B.; Doria, M.; Becherucci, P.; Marseglia, G.L.; Motisi, M.A.; de Martino, M.; Galli, L.; Licari, A.; et al. Updated Guidelines for the Management of Acute Otitis Media in Children by the Italian Society of Pediatrics: Diagnosis. Pediatr. Infect. Dis. J. 2019, 38 (Suppl. S12), S3–S9. [Google Scholar] [CrossRef]
- Granath, A. Recurrent Acute Otitis Media: What Are the Options for Treatment and Prevention? Curr. Otorhinolaryngol. Rep. 2017, 5, 93–100. [Google Scholar] [CrossRef]
- Bhutta, M.F.; Leach, A.J.; Brennan-Jones, C.G. Chronic suppurative otitis media. Lancet 2024, 403, 2339–2348. [Google Scholar] [CrossRef]
- Madana, J.; Yolmo, D.; Kalaiarasi, R.; Gopalakrishnan, S.; Sujatha, S. Microbiological profile with antibiotic sensitivity pattern of cholesteatomatous chronic suppurative otitis media among children. Int. J. Pediatr. Otorhinolaryngol. 2011, 75, 1104–1108. [Google Scholar] [CrossRef]
- Kennedy, K.L.; Singh, A.K. Middle Ear Cholesteatoma. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2024. Available online: https://www.ncbi.nlm.nih.gov/books/NBK448108/ (accessed on 10 November 2024).
- Ungar, O.J.; Cavel, O.; Wasserzug, O.; Oron, Y.; Locketz, G.D.; Handzel, O. Iatrogenic cholesteatoma originating from a misplaced tympanomeatal flap during tympanoplasty: A series of five patients. Eur. Arch. Otorhinolaryngol. 2020, 277, 3295–3299. [Google Scholar] [CrossRef]
- Barozzi, S.; Socci, M.; Soi, D.; Di Berardino, F.; Fabio, G.; Forti, S.; Gasbarre, A.M.; Brambilla, D.; Cesarani, A. Reliability of postural control measures in children and young adolescents. Eur. Arch. Otorhinolaryngol. 2014, 271, 2069–2077. [Google Scholar] [CrossRef]
- Bastani, P.B.; Rieiro, H.; Badihian, S.; Otero-Millan, J.; Farrell, N.; Parker, M.; Newman-Toker, D.; Zhu, Y.; Tehrani, A.S. Quantifying Induced Nystagmus Using a Smartphone Eye Tracking Application (EyePhone). J. Am. Heart Assoc. 2024, 13, e030927. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Villalba, R.; Caballero-Borrego, M. Normative values for the video Head Impulse Test in children without otoneurologic symptoms and their evolution across childhood by gender. Eur. Arch. Otorhinolaryngol. 2023, 280, 4037–4043. [Google Scholar] [CrossRef] [PubMed]
- Cömert, E.; Şencan, Z.; Koçak, F.M.; Şimşek, G.; Muluk, N.B. Clinical evaluation of the vestibular impairment using video head impulse test In children with acute otitis media. Int. J. Pediatr. Otorhinolaryngol. 2021, 141, 110568. [Google Scholar] [CrossRef] [PubMed]
- Aarhus, L.; Tambs, K.; Hoffman, H.J.; Engdahl, B. Childhood otitis media is associated with dizziness in adulthood: The HUNT cohort study. Eur. Arch. Otorhinolaryngol. 2016, 273, 2047–2054. [Google Scholar] [CrossRef]
- Monsanto, R.D.C.; Kasemodel, A.L.P.; Tomaz, A.; Elias, T.G.A.; Paparella, M.M.; Penido, N.O. Evaluation of vestibular symptoms and postural balance control in patients with chronic otitis media. J. Vestib. Res. 2020, 30, 35–45. [Google Scholar] [CrossRef]
- Abdelmotaleb, H.; Sobhy, O.; Bassiouny, M.; Elsherif, M. Evaluation of postural stability and vestibulo-ocular reflex in adults with chronic suppurative otitis media. Eur. Arch. Otorhinolaryngol. 2023, 280, 897–905. [Google Scholar] [CrossRef]
- Monsanto, R.d.C.; Erdil, M.; Pauna, H.F.; Kwon, G.; Schachern, P.A.; Tsuprun, V.; Paparella, M.M.; Cureoglu, S. Pathologic Changes of the Peripheral Vestibular System Secondary to Chronic Otitis Media. Otolaryngol. Head Neck Surg. 2016, 155, 494–500. [Google Scholar] [CrossRef]
- Monsanto, R.D.C.; Schachern, P.; Paparella, M.M.; Cureoglu, S.; Penido, N.O. Progression of changes in the sensorial elements of the cochlear and peripheral vestibular systems: The otitis media continuum. Hear. Res. 2017, 351, 2–10. [Google Scholar] [CrossRef]
- Chang, C.W.; Cheng, P.W.; Young, Y.H. Inner ear deficits after chronic otitis media. Eur. Arch. Otorhinolaryngol. 2014, 271, 2165–2170. [Google Scholar] [CrossRef]
- Tomaz, A.; Monsanto, R.D.C.; Cusin, F.S.; Kasemodel, A.L.P.; Penido, N.O. Evaluation of the vestibulo-ocular reflex in patients with chronic otitis media. Braz. J. Otorhinolaryngol. 2022, 88, 675–682. [Google Scholar] [CrossRef]
- Xiao, Q.; Zhang, Y.; Lv, J.; Yang, J.; Zhang, Q. Case Report: Suppurative Labyrinthitis Induced by Chronic Suppurative Otitis Media. Front. Neurol. 2022, 13, 892045. [Google Scholar] [CrossRef] [PubMed]
- Kishan Siddapur, G.; Gangwar, N.; Coimbatore Balakrishnan, M.; Murugesan, V. Clinical Study of Labyrinthine Fistula in Cholesteatomatous Chronic Otitis Media: A Tertiary Care Hospital-Based Retrospective Study in a South Indian Population. Cureus. 2023, 15, e42413. [Google Scholar] [CrossRef] [PubMed]
- Yao, Q.; Li, Z.; Xu, M.; Jiang, Y.; Wang, J.; Wang, H.; Yu, D.; Yin, S. The Spectrum of Vestibular Disorders Presenting With Acute Continuous Vertigo. Front. Neurosci. 2022, 16, 933520. [Google Scholar] [CrossRef] [PubMed]
- Tailor, B.V.; Phillips, J.S.; Nunney, I.; Yung, M.W.; Doruk, C.; Kara, H.; Kong, T.; Quaranta, N.; Peñaranda, A.; Bernardeschi, D.; et al. Presentation of dizziness in individuals with chronic otitis media: Data from the multinational collaborative COMQ-12 study. Eur. Arch. Otorhinolaryngol. 2022, 279, 2857–2863. [Google Scholar] [CrossRef]
- Rehagen, S.K.; Valente, M.; Lieu, J.E.C. Vestibular Screening in Pediatric Patients with Otitis Media. J. Am. Acad. Audiol. 2020, 31, 209–216. [Google Scholar] [CrossRef]
- Saliba, I.; Dagher, C.; El-Zir, E.; Yammine, F.G. A Pilot Study to Assess the Vestibular Apparatus Function with Videonystagmography During Chronic Otitis Media with Effusion. Curr. Pediatr. Rev. 2015, 11, 135–140. [Google Scholar] [CrossRef]
- Rosenfeld, R.M.; Tunkel, D.E.; Schwartz, S.R.; Anne, S.; Bishop, C.E.; Chelius, D.C.; Hackell, J.; Hunter, L.L.; Keppel, K.L.; Kim, A.H.; et al. Clinical Practice Guideline: Tympanostomy Tubes in Children (Update). Otolaryngol. Head Neck Surg. 2022, 166 (Suppl. S1), S1–S55. [Google Scholar] [CrossRef]
- Bista, R.; Datta, R.; Nilakantan, A.; Gupta, A.; Singh, A. Vestibular Dysfunction in Children Suffering from Otitis Media with Effusion: Does Grommet Help? An Observational Study Using Computerized Static Posturography. Indian J Otolaryngol. Head Neck Surg. 2019, 71, 537–541. [Google Scholar] [CrossRef]
- Cohen, M.S.; Mandel, E.M.; Furman, J.M.; Sparto, P.J.; Casselbrant, M.L. Tympanostomy tube placement and vestibular function in children. Otolaryngol. Head Neck Surg. 2011, 145, 666–672. [Google Scholar] [CrossRef]
- Kaplan, B.; Altın, B.; Akyol, M.U.; Aksoy, S. Evaluation of Balance with Computerized Dynamic Posturography in Children with Otitis Media. Laryngoscope 2024, 134, 4126–4133. [Google Scholar] [CrossRef]
- Gawron, W.; Pośpiech, L.; Orendorz-Fraczkowska, K. An evaluation of postural stability and the effects of middle-ear drainage on vestibulo-spinal reflexes of children with chronic otitis media with effusion. Int. J. Pediatr. Otorhinolaryngol. 2004, 68, 1175–1179. [Google Scholar] [CrossRef] [PubMed]
- Pazdro-Zastawny, K.; Pośpiech, L.; Zatoński, T. Long-term evaluation of the effect of middle ear effusion on the vestibular system in children. Int. J. Pediatr. Otorhinolaryngol. 2018, 109, 13–16. [Google Scholar] [CrossRef]
- Sabir, O.A.; Johnson, E.G.; Hafiz, A.E.; Nelson, R.N.; Hudlikar, M.; Sheth, I.; Daher, N.S. Chronic Effects of Pediatric Ear Infections on Postural Stability. Int. J. Pediatr. 2021, 2021, 6688991. [Google Scholar] [CrossRef] [PubMed]
- Casselbrant, M.L.; Villardo, R.J.; Mandel, E.M. Balance and otitis media with effusion. Int. J. Audiol. 2008, 47, 584–589. [Google Scholar] [CrossRef]
- Kim, H.Y. Vertigo due to Eustachian Tube Dysfunction. Arch. Otorhinolaryngol. Head Neck Surgery 2017, 1, 5. [Google Scholar] [CrossRef]
- Carlborg, B.I.; Konrádsson, K.S.; Carlborg, A.H.; Farmer, J.C., Jr.; Densert, O. Pressure transfer between the perilymph and the cerebrospinal fluid compartments in cats. Am. J. Otol. 1992, 13, 41–48. [Google Scholar] [CrossRef]
- Suzuki, M.; Kitano, H.; Yazawa, Y.; Kitajima, K. Involvement of round and oval windows in the vestibular response to pressure changes in the middle ear of guinea pigs. Acta Otolaryngol. 1998, 118, 712–716. [Google Scholar] [CrossRef]
- Francescon, D.; Jamal, Z.; Cooper, J.S. Alternobaric Vertigo. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2024. Available online: https://www.ncbi.nlm.nih.gov/books/NBK482211/ (accessed on 10 November 2024).
- Golz, A.; Netzer, A.; Angel-Yeger, B.; Westerman, S.T.; Gilbert, L.M.; Joachims, H.Z. Effects of middle ear effusion on the vestibular system in children. Otolaryngol. Head Neck Surg. 1998, 119, 695–699. [Google Scholar] [CrossRef]
- Kaya, S.; Tsuprun, V.; Hızlı, Ö.; Schachern, P.A.; Paparella, M.M.; Cureoglu, S. Cochlear changes in serous labyrinthitis associated with silent otitis media: A human temporal bone study. Am. J. Otolaryngol. 2016, 37, 83–88. [Google Scholar] [CrossRef]
- Casselbrant, M.L.; Furman, J.M.; Mandel, E.M.; Fall, P.A.; Kurs-Lasky, M.; Rockette, H.E. Past history of otitis media and balance in four-year-old children. Laryngoscope 2000, 110, 773–778. [Google Scholar] [CrossRef]
Variables | N (%) |
---|---|
Sex | |
Male | 25 (45.5) |
Female | 30 (54.5) |
Number of episodes of acute otitis media | |
4–8 | 24 (43.6) |
>8 | 31 (56.4) |
Age at first diagnosis of acute otitis media | |
<1 year old | 23 (41.8) |
>1 year old | 32 (58.2) |
Otorrhea | |
No | 26 (47.3) |
Yes | 29 (52.7) |
TOTAL | 55 (100.0) |
Healthy (n = 38) [21] (SX, mm2) | History of Recurrent Otitis Media (n = 55) (SX, mm2) | p-Value | |
---|---|---|---|
Test | |||
Eyes open (EO) | 364.3 ± 201.2 | 557.9 ± 153.2 | <0.001 * |
Eyes closed (EC) | 564.4 ± 337.7 | 792.1 ± 275.0 | <0.001 * |
Pad EO | 445.4 ± 314.6 | 751.2 ± 235.7 | <0.001 * |
Pad EC | 602.9 ± 442.0 | 1032.4 ± 309.7 | <0.001 * |
Sex | Number of Episodes of Acute Otitis Media | Age at First Diagnosis of Acute Otitis Media | Otorrhea | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Test | Male | Female | p-Value | 4–8 | >8 | p-Value | <1 Year | >1 Year | p-Value | No | Yes | p-Value |
Eyes open (EO) | 591.3 ± 144.0 | 530.0 ± 157.4 | 0.14 | 505.0 ± 125.1 | 598.8 ± 162.1 | 0.02 * | 589.0 ± 159.9 | 535.5 ± 144.4 | 0.2 | 544.6 ± 170.8 | 569.8± 137.4 | 0.55 |
Eyes closed (EC) | 849.7 ± 315.2 | 744.1 ± 231.0 | 0.16 | 703.6 ± 170.6 | 860.6 ± 320.4 | 0.03 * | 811.4 ± 239.1 | 778.2 ± 301.1 | 0.66 | 791.3 ± 333.0 | 792.8 ± 216.3 | 0.98 |
Pad EO | 805.6 ± 234.3 | 705.8 ± 231.0 | 0.12 | 651.0 ± 153.0 | 828.7 ± 260.5 | 0.005 * | 803.4 ± 236.7 | 713.7 ± 231.4 | 0.16 | 733.8 ± 262.1 | 766.8 ± 212.8 | 0.61 |
Pad EC | 1107.9 ± 338.5 | 969.5 ± 273.5 | 0.1 | 899.9 ± 202.2 | 1134.9 ± 341.2 | 0.004 * | 1079.5 ± 252.7 | 998.5 ± 344.9 | 0.35 | 995.0 ± 357.0 | 1065.9 ± 262.2 | 0.40 |
Semicircular Canals | Vestibular Hypofunction, N (%) |
---|---|
Right Lateral (RL) | 0 (0.0) |
Left Lateral (LL) | 3 (5.5) |
Right Anterior (RA) | 8 (14.5) |
Left Posterior (LP) | 4 (7.3) |
Left Anterior (LA) | 2 (3.6) |
Right Posterior (RP) | 2 (3.6) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Aldè, M.; Bosi, P.; Muck, S.; Mayr, T.; Di Mauro, P.; Berto, V.; Aleandri, B.G.; Folino, F.; Barozzi, S.; Zanetti, D.; et al. Long-Term Impact of Recurrent Acute Otitis Media on Balance and Vestibular Function in Children. Brain Sci. 2024, 14, 1246. https://doi.org/10.3390/brainsci14121246
Aldè M, Bosi P, Muck S, Mayr T, Di Mauro P, Berto V, Aleandri BG, Folino F, Barozzi S, Zanetti D, et al. Long-Term Impact of Recurrent Acute Otitis Media on Balance and Vestibular Function in Children. Brain Sciences. 2024; 14(12):1246. https://doi.org/10.3390/brainsci14121246
Chicago/Turabian StyleAldè, Mirko, Pietro Bosi, Stefanie Muck, Thomas Mayr, Paola Di Mauro, Valentina Berto, Beatrice Gaia Aleandri, Francesco Folino, Stefania Barozzi, Diego Zanetti, and et al. 2024. "Long-Term Impact of Recurrent Acute Otitis Media on Balance and Vestibular Function in Children" Brain Sciences 14, no. 12: 1246. https://doi.org/10.3390/brainsci14121246
APA StyleAldè, M., Bosi, P., Muck, S., Mayr, T., Di Mauro, P., Berto, V., Aleandri, B. G., Folino, F., Barozzi, S., Zanetti, D., & Marchisio, P. (2024). Long-Term Impact of Recurrent Acute Otitis Media on Balance and Vestibular Function in Children. Brain Sciences, 14(12), 1246. https://doi.org/10.3390/brainsci14121246