Impact of advancement of otitis media with effusion on vestibular organ condition in children
e | 11 lug 2022
Article Category: Original Study
Pubblicato online: 11 lug 2022
Pagine: 300 - 306
Ricevuto: 26 gen 2022
Accettato: 20 apr 2022
DOI: https://doi.org/10.2478/ahem-2022-0041
Parole chiave
© 2022 Katarzyna Pazdro-Zastawny et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Otitis media with effusion (OME) is one of the most common otorhinolaryngological disorders in childhood. It develops as a result of impaired Eustachian tube function. It is characterized by the absence of symptoms of acute infection, with an intact tympanic membrane, with the accumulation of fluid in the middle ear (ME) [1, 2]. An accumulation of fluid leads to progressive hearing loss, most often of the conductive type, which is the disease’s main symptom. Prolonged dysfunction of the Eustachian tube and excessive negative pressure in the ME may lead to atrophic changes in the tympanic membrane and the development of retraction pockets. The untreated disease may cause tympanosclerosis and cholesteatoma.
Due to its complex etiopathogenesis and progressive nature, OME is a significant social problem. The disease can lead to a delay in speech development, cognitive impairment, and emotional and social development disturbances. OME is considered the most common cause of hearing loss in children [3, 4]. In the early stages of the disease, ME anomalies are usually reversible. In some cases, the disease coexists with sensorineural hearing loss [5]. There are reports about the negative impact of the ME effusion on the inner ear condition [6, 7, 8, 9]. However, the exact etiopathology of balance disorders in the course of OME remains unclear. Some authors emphasize the negative impact of hydrostatic pressure changes in the ME, which are transmitted through the round window, and subsequently lead to secondary changes in the inner ear fluids [8, 10, 11]. Some authors postulate that the semi-permeability of the circular window membrane allows ionic flow, which, through the perilymph, may cause a change in the chemical composition of the endolymph. The subsequent changes in the flow within the kinocilia and stereocilia ion channels determine not only the deviations within the equilibrium organ but also may influence the formation of the receiver component of hearing loss [12]. Some authors also claim that balance disorders in children with OME directly result from frequent episodes of acute otitis media [13, 14]. The presence of vestibular disorders may significantly impact disease control and change the assessment of disease severity. This research should help in making specific therapeutic decisions and monitoring the development of the disease and its possible complications.
This study aimed to investigate the vestibular organ condition in children with OME and whether the presence of possible vestibular disturbances depends on the advancement of OME.
53 children (20 girls and 33 boys) aged between 4 and 14 years (mean age: 8 years; SD: 2.5 years) were referred because of bilateral OME and treated with ME drainage, who had not had any previous ear or adenoid surgery. The screening protocol required that all children initially undergo tympanometry; those with bilateral type B tympanogram then progressed to pure-tone audiometry and otoscopy by a consultant otolaryngologist. Selection criteria were persistent bilateral OME after failed watchful waiting of three months or more, with a hearing level in the better ear of 25–30 dBHL or worse, averaged at 0.5 kHz, 1 kHz, 2 kHz, and 4 kHz (or an equivalent dBA where dBHL was not available), and with bilateral type B tympanometry. Exclusion criteria: children with lower birth weight (< 2,500 g); a history of neonatal asphyxia; congenital malformations of the ear (external, middle, or inner); temporal bone fracture; neurological diseases or any other serious illness; a history of meningitis; and a history of vestibulotoxic or ototoxic drugs, the inability to perform full otoneurological diagnostics in a child.
The control group, matched for age and gender in relation to the experimental group, consisted of 29 healthy individuals (13 girls and 16 boys) aged 4–17 years (average age: 10 years; SD: 3.8 years), scheduled for a tonsillectomy operation in the Wroclaw Medical University Otorhinolaryngology Department. The inclusion criteria for this group were: being healthy; absence of a history of vestibular, auditory, body imbalance and/or headache symptoms; and absence of symptoms or signs of neurological diseases and other conditions.
The participants were submitted to an evaluation consisting of anamnesis, otorhinolaryngological evaluation, static posturography, and electronystagmography (ENG). The anamnesis was performed through a detailed interview by applying a guided questionnaire on the patients’ clinical history with particular attention paid to the current disease and the presence of vestibular and balance disorders. Parents and children were asked about frequent falls; difficulty riding a bicycle, climbing or descending stairs; a tendency to bump into objects or misjudge distances; vertigo, dizziness, tinnitus, or disequilibrium; unexplained clumsiness, delayed gross motor development, or recurrent headache.
The evaluation of the vestibulospinal through static posturography test was performed with a Posturographer PE 62 Model 04 (Neurocom, Luxembourg). It consists of an IBM microcomputer (IBM Corp., Armonk, USA) with additional converters, a static posturographic 40 × 40 cm platform with pressure sensors recording deflections in the range of ±10 cm (0.05 mm accuracy), and a visual stimulator connected to a TV screen. In each case, a set of 3 tests was performed in order to evaluate static balance. The static posturography test consisted of an integrated plate that measures postural sway in three sensory conditions. Test 1 was performed standing with eyes open (EO); test 2 was performed standing on the platform with eyes closed (EC), and; test 3 was feedback test (FT): eyes open, feet on the platform, subject observing a moving point of light, which reflects the current position of the center of gravity, and making slight movements of the body to self-correct current body position. Three trials, lasting 30s each, were performed for each condition. In addition, the field of developed area (FDA; the area described by the center of mass [mm2]) and the average sway velocity (ASV [mm/s]) were analyzed.
A two-channel Hortmann electronystagmograph linked with a multimedia projector, standard software, and the Alwar swing chair was used for ENG. The ENG examination included calibration and registration of:
possible spontaneous nystagmus with open/closed eyes, positional nystagmus with eyes closed in 4 positions: supine, on the right side, on the left side, nystagmus in Rose position; after performing Hallpike maneuvers to the right and left, the assessment of positional nystagmus was based on the classification proposed by Nylen: I: nystagmus changing direction with a change of head position; II: nystagmus showing a constant direction of the fast phase regardless of the head position; III: irregular nystagmus, manifested by significant variability in both the direction and magnitude of the amplitude and frequencies, sometimes alternating in the same head position; tracking pendulum test (a moving point of light displayed on the screen with a frequency of 0.4 Hz and an amplitude of 30°, alternately clockwise and counterclockwise, was observed by the subject; the speed of the light point was 24°/s. the recording of continuous eye movements was 30 s; the obtained record was assessed qualitatively as correct in the case of a smooth tracking curve or as incorrect). the rotary test was carried out with the use of a swing chair: the response from both labyrinths was obtained after rhythmically repeating sinusoidal stimuli, alternately towards the right and left; symmetry of response was assessed by comparing the number of nystagmus deflections in individual half-periods.
The examination was performed before surgery and one month after ME drainage.
The study group was divided into two subgroups according to the advancement of the disease. The advancement of OME, based on the clinical picture, was assessed in accordance with the following criteria [15]: the first stage of advancement (I): the presence of small otomicroscopic lesions, in some cases with fluid translucency and limited mobility of the tympanic membrane, and conductive hearing loss with a cochlear reserve not exceeding 25 dB; the second stage of advancement (II): cases with more severe pathological changes, including the presence of retraction pockets in the flaccid part and a tense eardrum, as well as with local atrophy and cochlear reserve exceeding 25–30 dB and/or the coexistence of the SNHL.
Statistical analysis was performed using the Statistica software version 13.0 (StatSoft, Inc., USA). Student’s t-test was used to compare the average values of parameters before and after drainage. For all analyses, the statistical significance was set at p values less than .05.
The study group was divided into two subgroups according to the advancement of the disease: a subgroup with the 1st stage (I): of advancement (24 children) and a subgroup with the 2nd stage (II) of the advancement (29 children).
The assessment of the vestibular organ condition during the posturographic examination revealed the presence of disturbances in the study group, both before and after ME drainage. After drainage, the assessed parameters improved, however, they remained elevated compared to the control group. Before and after ME drainage, higher stabilogram parameters were shown in most tests compared to the control group, both for the field of developed area (FDA) and average velocity sway (AVS). Before drainage, significant differences (p <0.001) were demonstrated for all FDA tests and AVS for EO and eyes closed EC. After drainage, these values were statistically significant for the FDA (EO and EC) and AVS (EC and FT). The parameters of the stabilograms were analyzed in the study group with advancement stage I before and after ME drainage. Lower stabilogram parameters after drainage have been demonstrated in most tests for both the FDA and AVS. Statistically significant differences (p <0.05) occurred for FDA in tests at EC and FT and for FDA at EC (Figs. 1 and 2). Posturographic parameters in the subgroup with II stage advancement before and after drainage showed lower values of the stabilograms after ventilation drainage, statistically significant only in the O-O test for FDA (Fig. 3). A bigger improvement in the parameters was shown in the posturographic examination after ventilation drainage in the subgroup with stage I than in the subgroup with stage II advancement. Posturographic parameters were analyzed between stage I and stage II subgroups. Both before and after drainage in group I with stage II advancement, almost all mean values of stabilogram parameters were higher than in group I with stage I. These values were statistically significant (p <0.05) before drainage for FDA at EO and EC and AVS at EO. After drainage, only FDA at EC and FT were significant (Fig. 4, 5, 6).
Fig. 1
Stabilogram parameters for FDA for subgroup with 1st stage of advancement before and after middle ear drainage
Fig. 2
Stabilogram parameters for AVS for subgroup with 1st stage of advancement before and after middle ear drainage
Fig. 3
Stabilogram parameters for FDA for subgroup with 2nd stage of advancement before and after middle ear drainage
Fig. 4
Stabilogram parameters for FDA for subgroup with 1st and 2nd stage of advancement before middle ear drainage
Fig. 5
Stabilogram parameters for AVS for subgroup with 1st and 2nd stage of advancement before middle ear drainage
Fig. 6
Stabilogram parameters for FDA for subgroup with 1st and 2nd stage of advancement after middle ear drainage
Disturbances in posturography, both before and after drainage, were expressed in the subgroup with stage II more than in the I stage subgroup, especially before drainage.
Due to the lack of cooperation with some children, conducting the ENG in all study groups was impossible. Therefore, the final evaluation records containing numerous artifacts were excluded, which significantly prevented their correct interpretation. ENG records of 26 children were assessed. In the control group, the study was performed on 29 children.
The presence of spontaneous nystagmus with eyes closed was demonstrated before the drainage in 14 children (54%). Spontaneous nystagmus after drainage was found in 7 respondents (27%). In the control group, spontaneous nystagmus occurred in 1 child (3.5%). Positional nystagmus was demonstrated before the ME drainage in 18 children (69%), with a predominance of Nylen III nystagmus. Nylen III positional nystagmus was present in 2 children in the control group (6.8%). After drainage, positional nystagmus was demonstrated in 10 subjects (38.5%). Before drainage, the incorrect recording of the tracking test was found in 7 children (27%). After drainage, no anomalies were found. The control group showed no disturbances in the tracking test. The asymmetry in the rotational chair test before drainage was demonstrated in 4 children (15.4%). After drainage, the record did not show disturbances. In a control group in the control panel, anomalies were not revealed.
Spontaneous nystagmus before ME drainage was present in 3 children at stage I of advancement (11.5%) and 11 in a subgroup with stage II of advancement (42.3%). After drainage, spontaneous nystagmus was detected in 2 children with stage I advancement (7.7%) and 5 with stage II of OME advancement (19.2%). Positional nystagmus occurred both before and after ME drainage. However, after drainage, a lower percentage of positional nystagmus was observed in the study group, regardless of the degree of advancement. Before ME drainage, the presence of positional nystagmus in the subgroup with stage II advancement was found in 6 children (23%) and 12 children from the subgroup with stage II advancement (46%). After drainage, an improvement in the ENG testing was noted. Positional nystagmus in the stage I subgroup was shown in 2 children (7.7%) and in the stage II subgroup in 8 (30.7%). Both before and after drainage, positional nystagmus Nylen III type was present most often. This nystagmus occurred before drainage in 4 children (33.4%) from stage II and in 6 with stage II subgroups (42.8%). Moreover, in the subgroup with stage I, 2 subjects had a different type of positional nystagmus: 1 child had Nylen I (8.3%) and 1 child had Nylen II (8.3%) nystagmus. In the subgroup with stage II, Nylen I positional nystagmus occurred in 1 child (7.2%) and the Nylen II in 5 children (35.7%). After drainage, there was an improvement in the vestibular organ condition in the form of a reduction in the percentage of positional nystagmus. Type III nystagmus occurred in 6 children in total: 3 children (21.4) in the subgroup with stage II. Nylen I and II positional nystagmus was present only in the type III group. It occurred in 6 children in total: 3 children in the stage 1 subgroup (25%) and 3 (21.4) in the stage II subgroup. Nylen I was recorded in 1 (7.2%) and Nylen II in 3 children (21.4%). Incorrect tracking test in the study group before drainage was found in 2 (7.7%) children with stage I advancement and in 5 (19.2%) children with stage II advancement. After ME drainage, no abnormalities were found in these subgroups. The asymmetry of the rotational chair before drainage was demonstrated in 1 child (3.8%) with stage I of the disease and 3 (11.5%) with stage II. After drainage, the ENG record in the analyzed groups was correct.
Comparing posturographic parameters between the study group and control group showed, both before and after drainage, higher values of posturographic parameters for the FDA and AVS. There was an improvement 4 weeks after drainage of evaluated parameters, which, however, remained elevated in comparison with the control group. The results of our study suggest that in the period analyzed by the authors, despite the drainage, the function of the vestibular organ improved but was not normal. Similar results were also obtained in the other studies [6, 12, 16, 17]. Casselbrant et al. [6] showed that episodes of OME might affect balance, leaving children clumsier and more accident-prone and possibly impairing motor development. Children with OME were evaluated by moving platform posturography before and after insertion of tympanostomy tubes and were compared to children with no ear disease. The velocity of sway increased with increasing difficulty of test conditions (IVI) for both groups of children. Children with OME had a higher velocity than normal children. For children tested < 30 days after insertion of tympanostomy tubes, the velocity for condition VI was significantly lower than before insertion. The 6 children who had fallen during all trials on condition V or VI were able to stand during these trials after the insertion of tympanostomy tubes. Rehagen et al. state that the incidence of OME in children and the associated vestibular impairments is high, and a screening measure can identify those in need of diagnostic testing. Children with conductive hearing loss due to OME appear to experience more oculomotor abnormalities, consistent with vestibular disturbances, than their peers with normal hearing [18].
The chronic inflammatory process in the ME can lead to irreversible changes in the tympanic membrane in the form of retraction pockets and tympanosclerosis, as well as sensorineural hearing loss [5]. Treatment of the disease is to prevent the development of those complications. The most common lesions observed in the course of OME include retraction pockets involving both the flaccid and tense parts of the tympanic membrane. Their formation is related to the long-term negative pressure within the tympanic cavity. Other causative factors include frequent episodes of acute otitis media and the use of prolonged and multiple drainages. Animal studies revealed that structural changes in the tympanic membrane in the course of OME depend on the type of effusion. Wielinga et al. [19] report that the presence of sterile effusion causes the typical tympanosclerotic lesions, whereas, in experimentally induced acute purulent otitis, fibrosis predominates. This confirms the old view about the relationship between OME and the presence of tympanosclerosis, especially in patients undergoing ME drainage. According to Skarżyński [20], these observations are not entirely reliable because no studies have been conducted to determine whether it is the presence of ME effusion or ME drainage that is responsible for the development of tympanosclerosis. Clinical observations and retrospective studies of children who have undergone drainage in the course of OME indicate a relationship between the duration of the disease, the number of drainages, and the presence of advanced changes in the tympanic membrane, such as tympanosclerosis [21, 22]. Riley et al. [21] showed that tympanosclerotic lesions occurred in 39% of children who were drained multiple times and in 34% of children who were drained once. Tos et al. [23] revealed that ME drainage weakens the natural movement of the tympanic membrane related to sneezing, coughing, or speech, which results in better blood supply and regeneration of the tympanic membrane, and thus has an indirect influence on the occurrence of tympanosclerosis. It is also recognized that the severity of the disease depends on the duration, number of relapses, and appropriate monitoring of the disease course. That is why an early diagnosis and proper qualification for drainage and its optimal maintenance are so important. The high value of constant ENT control in children with OME, especially in younger children and those with permanent changes in the tympanic membrane, which persist despite the treatment, is also stressed.
Our study showed that the stage of OME advancement impacts the function of the vestibular organ. One month after drainage in the subgroup with stage II advancement, greater vestibular disturbances were revealed compared to the results obtained in the subgroup with stage I advancement. Thus, the stage of advancement influences the improvement of the vestibular organ efficiency after ME drainage. The improvement of balance system conditions is more pronounced in children with less advanced disease compared to children with more advanced disease. Over time, its function improves, especially in children with less severe disease. The analysis of the ENG confirmed earlier observations that the stage of clinical advancement affects the severity of vestibular disorders in children with OME. Greater vestibular disorders in the form of the presence of spontaneous nystagmus and position disorders were more frequent in the subgroup with stage II.
The study has not been randomized. The group of patients was relatively small. That was due to the difficulty of performing full otoneurologic assessment in children. Children younger than 3 are not able to perform posturography and ENG because of problems with focusing and anxiety manifested during testing. Otoneurologic evaluation needs to be done with the child’s cooperation with the technician. Therefore, some children were excluded from the study group. Another limitation is the difficulty in collecting any history of dizziness and/or balance problems; for many patients, the concept of vertigo is ambiguous, and the symptoms, due to their elusive nature, are difficult to define. Young children may react to dizziness and/or balance disturbances by crying, excessive sweating, paleness, or a tendency to faint. Other substitute symptoms are headache, nausea, and vomiting, as well as digestive tract dysfunction and heart rhythm disturbances.
The presence of ME effusion affects vestibular organ condition in children with OME.
The degree of vestibular disturbances in OME depends on the clinical advancement of the disease. In more advanced cases, both before and after drainage, vestibular system dysfunction is present both in posturography and electro-nystagmography.
The assessment of the vestibular organ condition is beneficial and should be included in the OME diagnostic and qualification for surgical treatment and is useful in monitoring OME.
In clinically advanced cases, with permanent changes in the tympanic membrane, vestibular organ evaluation should be a routine activity.