Acta Oto-Laryngologica

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Eustachian tube evaluation in patients with obstructive sleep apnea syndrome Giuseppe Magliulo, Marco de Vincentiis, Giannicola Iannella, Andrea Ciofalo, Alessandra Manno, Benedetta Pasquariello, Diletta Angeletti, Annalisa Pace, Giampiero Gulotta & Antonella Polimeni To cite this article: Giuseppe Magliulo, Marco de Vincentiis, Giannicola Iannella, Andrea Ciofalo, Alessandra Manno, Benedetta Pasquariello, Diletta Angeletti, Annalisa Pace, Giampiero Gulotta & Antonella Polimeni (2017): Eustachian tube evaluation in patients with obstructive sleep apnea syndrome, Acta Oto-Laryngologica, DOI: 10.1080/00016489.2017.1385846 To link to this article: http://dx.doi.org/10.1080/00016489.2017.1385846

Published online: 09 Oct 2017.

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Date: 13 October 2017, At: 05:49

ACTA OTO-LARYNGOLOGICA, 2017 https://doi.org/10.1080/00016489.2017.1385846

RESEARCH ARTICLE

Eustachian tube evaluation in patients with obstructive sleep apnea syndrome Giuseppe Magliuloa , Marco de Vincentiisa, Giannicola Iannellaa, Andrea Ciofaloa, Alessandra Mannoa, Benedetta Pasquarielloa, Diletta Angelettia, Annalisa Pacea, Giampiero Gulottaa and Antonella Polimenib

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a ‘Organi di Senso’ Department, Sapienza University of Rome, Rome, Italy; bDepartment of Oral and Maxillo Facial Sciences, Sapienza University of Rome, Rome, Italy

ABSTRACT

ARTICLE HISTORY

Objectives: Investigate the presence of Eustachian Tube Dysfunction (ETD) in Obstructive sleep apnea (OSA) patients. Correlate the ET function and the severity of the sleep apnea syndrome. Correlate nasal resistance and nasal mucociliary clearance with the onset of ETD in these patients. Materials and methods: Forty patients affected by OSA were enrolled in our clinical prospective study. Thirty patients were also investigated as a control group. All of the analyzed subjects underwent ENT examination, anterior rhinomanometry and test for mucociliary transport time. To evaluate Eustachian tube function the Eustachian tube score-7 (ETS-7) were employed. Results: Twenty percent of the patients with a diagnosis of OSA had a diagnosis of ETD (ETS-7  7) with a statistical difference with control group (p ¼ .03). No differences regarding ETD in OSA subgroups were found. Conclusion: This study showed that ET blockage or delayed openings were found in most adult patients with OSA when evaluated by a sensible score as the ETS-7. Our data suggest that an evaluation of the Eustachian tube function should be performed in patients suffering from obstructive sleep apnea syndrome.

Received 3 August 2017 Revised 7 September 2017 Accepted 17 September 2017

Introduction The obstructive sleep apnea (OSA) is a clinical entity characterized by recurring episodes of apnea and/or hypopnea during sleep, due to a total or partial collapse of the upper airway [1,2]. The OSA is characterized by night snoring with excessive daytime sleepiness and is common associated with reduced quality of life, cardiovascular diseases, increased healthcare utilization, motor vehicle accidents and decrease of cognitive performance [1,2]. Pressure differences between the middle ear and the external auditory canal (EAC) are normally equalized by the Eustachian tube (ET), which connects the middle ear to the back of the throat on each side. The ET is usually closed, but opens to allow equalization of the middle ear pressure (MEP) [3,4]. During sleep, MEP could undergo pressure variations due to modification of ET physiology [3,4]. Compromised Eustachian tube function is commonly called Eustachian Tube Dysfunction (ETD). Clinical manifestations of ETD are aural fullness, otalgia and/or hearing loss or could be a ‘latent’ condition, as recently reported by some studies on Eustachian tube function [3–6]. In our clinical practice, we observed many OSA patients who came to our center for sleep apnea disorders reported the above ETD symptoms. Sometimes in these patients, a clinical diagnosis of ETD, otitis media with effusions and/or tympanic retraction pockets was made. To the best of our knowledge, no study has specifically investigated this aspect in OSA patients to date, despite, it is CONTACT Giuseppe Magliulo

[email protected]

ß 2017 Acta Oto-Laryngologica AB (Ltd)

KEYWORDS

Obstructive sleep apnea; Eustachian tube dysfunction; mucociliary transport time; anterior rhinomanometry

well known that several OSA patients suffer from oro-nasal pathological conditions and other comorbidities such as nasal obstruction, chronic rhinosinusitis and gastroesophageal reflux [7,8] that are also considered among the pathogenetic factors of an ETD [9,10]. On the strength of these observations, we decided to investigate ET function in patients suffering from sleep apnea. The purpose of the study was (a) to investigate an eventual ETD in OSA patients; (b) to evaluate whether there were any differences in ET function according to the severity of the sleep apnea disorder; and (c) to identify any possible correlation between nasal resistance and nasal mucociliary clearance with the onset of ETD in these patients. To achieve these objectives, the ETS-7-score [11] was employed to evaluate the ETD.

Materials and methods Patients affected by OSA were enrolled in our prospective clinical observational study at the ‘Organi di Senso’ Department of the ‘Sapienza’ University in Rome. Subjects of the study were consecutively selected between patients comes to our department with suspect of OSA syndrome. Patients underwent surgery to the middle ear, the nose, the oropharynx and/or other surgical procedures to the OSA treatment were excluded from the study.

Via Gregorio VII n.80, Rome, Italy

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No patients of the study were undergoing treatment with a CPAP device at home. All patients reflecting above characteristics underwent polysomnography (PSG) for the diagnosis of the OSA. The parameters, sleep stage scores and event scores were evaluated in accordance with the AASM Manual for the Scoring of Sleep and Associated Events [1]. According to American Academy of Sleep Medicine (AASM) the diagnosis and classification of OSA patients were performed on the basis of the apnea þ hypopnea index (AHI) index. Patients were classified into normal (AHI was 1) indicating restricted Eustachian tube function. No opening (R negative or not measurable) indicates complete obstruction of the Eustachian tube [5,6,11–13]. ETS-7 score calculation The parameters adopted for the calculation of the ETS-7 [5,6,11] are shown in Table 1. ETS-7 ranges from a minimum of 0 to a maximum of 14 points. The Toynbee maneuver is performed by pinching the nostrils during swallowing. By doing this, it is possible to equalize middle ear pressure giving the perception of a crackling sound during swallowing. Toynbee’s clicking sound is rated with 0 points when the answer is ‘never’, 1 point for ‘sometimes’ and 2 points for ‘always’. The same assessment is adopted to the perception of a crackling during the Valsalva maneuver. The patients’ specifications are supposed to relate to a period of at least the 2 months prior to examination [5,6,11]. Regarding TMM results at 30, 40 and 50 mbar, an immediate opening of the ET (R < 1) is given 2 points, a delayed opening (R > 1) 1 point and no opening (negative or not measurable R) 0 points. The results of tympanometry are divided according to Jerger’s classification [5,6,11]: a type A curve is given 2 points, type C 1 point and type B 0 points. The answers to the objective Valsalva aspect are given 2 points for ‘immediately positive’, 1 point for ‘only minimal and slow movement of the tympanic membrane’ and 0 points for ‘negative evaluation’. ETS-7 evaluation was considered separately for each of the ears examined. The ETS-7 outcome corresponds to a diagnosis of chronic ETD in cases with a score 7, a sensitivity of73% and a specificity of 60% [11]. Rhinomanometry Nasal resistance using anterior rhinomanometry was evaluated in both OSA patients and the control group. It has been reported in the literature that the mean total resistance in normal subjects ranges between 0.10 and 0.40 Pa/cm3/s [14], with a mean of 0.23 Pa/cm3/s. For this reason, a total nasal airway resistance >0.3 Pa/cm3/s has been considered pathological. Mucociliary transport time Mucociliary transport times were evaluated in order to investigate any possible deficits of nasal mucociliary

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clearance responsible for stagnation of secretions and incorrect function of the tubal orifice function. Mucociliary transport time was evaluated in each patient by means of the saccharin test which is a very simple, quick, non-invasive and reproducible method. A quantity of 2.5 mg of granulated saccharin was placed 1 cm posterior and inferior to the head of the inferior turbinate, while the patient was in the sitting position with the head bent forward. The patients were instructed to swallow every 30 s and not to sniff, sneeze, or wipe their noses until they tasted the saccharin. The time from placement to the perception of the sweet taste was recorded as the nasal mucociliary clearance time (NMCT) [15]. The same test was performed in the OSA patients and the study group. This research study was performed in accordance with the principles of the Declaration of Helsinki and approved by the local Ethics Committee of the University ‘Sapienza’ of Rome. Informed consent was obtained from all patients included in the study.

Results In 18 (45%) patients, a diagnosis of severe OSA was made with a mean AHI value of 41.5; 14 patients had a diagnosis of moderate OSA with an AHI of 22.1 and 8 patients a diagnosis of mild OSA with a mean AHI value of 9.7. Six (15%) patients of the study group reported chronic aural fullness, otalgia or other symptoms compatible with ETD. In two of these cases the otoscopic examination revealed a TM retraction. Of these patients, four were severe OSA and two moderate OSA. Another severe OSA patient showed a TM retraction without clinical symptoms (Table 2). Only one patient of the control group presented aural fullness and TM retraction. No statistical differences between OSA patients and the control group regarding clinical symptoms of ETD (aural fullness, otalgia or other ETD symptoms) were found (p ¼ .2). No patients of the study had rhinopharyngeal or tubal orifice pathologies visible at endoscopy. Besides, none of the patients showed a tympanic membrane aspect of otitis media with effusion (OME). Only two patients showed a type C tympanogram according to Jerger’s classification, compatible with a possible diagnosis of ETD. Analyzing the results of the ETS-7 score emerged that of patients with OSA 8 (20%) cases had an ETS-7  7 with a diagnosis of ETD (3 right side, 3 left side and 2 bilateral). In all OSA patients with clinical episodes of aural fullness and/or otoscopic TM retraction, the diagnosis of ETD was confirmed by the ETS-7 calculation. Only one patients of the control group showed an unilateral ETS7 value 7. This patient was the same one who reported aural fullness on the same side and showed retraction of TM. A difference between OSA patients and the

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Table 2. Characteristics of the study and control group; ETD and nasal obstruction distribution in OSAS patients and control group.

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Number of patients Patients reported aural fullness, otalgia or other symptoms of ETD Tympanic membrane retraction Rhinopharyngeal or tubal orifice pathologies ETS-7  7 Rhinomanometry

Control group (number of patients)

OSAS group (number of patients)

Mild OSAS (number of patients)

Moderate OSAS (number of patients)

Severe OSAS (number of patients)

30 1 (3.3%)

40 6 (15%)

8 (20%) 0

14 (35%) 2 (14.2%)

18 (45%) 4 (22.2%)

1 (3.3%) 0 1 (3.3%) 6 (20%)

3 (7.5%) 0 8 (20%) 29 (72%)

0 – 0 6 (75%)

1(7.1%) – 2 (14.2%) 10 (71%)

2(11.1%) – 6 (33.3%) 13 (72.2%)

control group regarding the incidence of ETD estimated by ETS7 was present (p ¼ .03). Regarding the OSA patients with ETS 7, six patients (33.3%) had a severe OSA whereas two patients (14.2%) had a moderate OSA. Interesting to note was that no patient with mild OSA showed an ETS-7  7 and a diagnosis of ETD. Despite the fact that an increased number of patients with ETD was present in the group of severe OSA in comparison to patients with moderate and mild OSA, no statistical difference regarding ETD incidence was observed between these three groups (p > .05 in each case). The mean value of ETS-7 in the entire study group was 10.1 (Standard Deviation ¼ 2.40; Hi ¼ 14.0 Low ¼ 4.00). The control group showed a mean value of 12.4 (Standard Deviation ¼ 1.81; Hi ¼ 14.0 Low ¼ 5.00). The difference between the two groups was statistically different with a p value of .002. Rhinomanometry Twenty-nine patients (72%) had pathological bilateral values of nasal airway resistance at the rhinomanometry examination. No differences in rhinomanometry results emerged for the different subclasses of OSA patients. In the control group, six patients (20%) showed pathological values. The difference between pathological rhinomanometry results in the two groups of patients was statistically significant (p ¼ .0001). Mucociliary transport time The mean value of NMCT in OSA patients was 13.8 min (Hi 20 min Low ¼ 9 min). Differently, in the control group a lower NMCT mean value (Hi 15 min Low ¼ 5 min) of 9.4 min was estimated. A statistical difference between the two groups was present (p ¼ .0001) (Figure 2). ETS-7, rhinomanometry and mucociliary transport time All OSA patients with an ETS-7  7 reported a pathological rhinomanometry. There was no difference between patients with and without ETD regarding rhinomanometry results (p ¼ .08). The average mucociliary transport time of patients with ETD was greater than the mean value of the remaining OSA patients (15.1 min versus 12.5 min). A statistical difference between these two groups emerged (p ¼ .04) (Table 3).

Figure 2. Difference between OSA patients and control group regarding Mucociliary transport time. Statistical difference between the two groups was present (p ¼ .0001).

Discussion According to our clinical practice, some OSA patients could present several otologic conditions (otitis media with effusions, tympanic membrane retraction and/or symptoms) compatible with Eustachian tube dysfunction. However, to date, no study evaluating ETD in adult OSA patients has been reported. Only Robison et al. [16], in a retrospective study, evaluated the incidence of ETD in infants with obstructive sleep apnea. They used the PSG to diagnose the OSA, while the presence of ETD was inferred from the performance of myringotomy with tympanostomy tube placement (MT). A prevalence of ETD was estimated in 31.9% of these young patients with OSA, significantly above the expected 4–5% for this age group in the general pediatric population [16]. However, no specific tests for evaluating Eustachian tube function were performed in the above-mentioned study and all patients who underwent tympanostomy tube placement were considered to be affected by ETD. There are many methods for evaluating ET function, including tympanometry, Valsalva maneuver, Toynbee maneuver, endoscopy, otoscopy, radiological imaging, acoustic

ACTA OTO-LARYNGOLOGICA

Table 3. Evaluation of OSAS patients according to ETS, rhinomanometry results and mucociliary transport time.

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Pathological Normal Mucociliary rhinomanometry rhinomanometry p transport time (min) p ETS-7  7 8 patients (20%)

8

0

ETS-7  7 32 patients (80%)

21

11

.08

14.1

.1

13.5

testing and various other non-metric tests that are employed clinically. However, accurate evaluation tools for ET function are scarce [4–6,11]. Recently, tubomanometry (TMM) has been introduced into clinical practice as a specific test for the evaluation of ETD. It is a relatively simple instrumental examination that allows the assessment of ET and provides reliable information about the dynamic capacity of ET patency [5,6,11–13]. It has been considered by several authors to be a routine diagnostic tool for chronic obstructive Eustachian tube dysfunction [11,12]. Moreover, since it allows direct assessment of ET opening, TMM has been used to evaluate ET opening in adult patients with OME and it has become increasingly popular, particularly for routine assessment before and after ET balloon dilation [5,6,11–13]. Ockermann et al. [12] used the TMM developed a score for ET function evaluation that they called the Eustachian Tube Score (ETS). The ETS comprises three TMM measurements and two subjective patient assessments concerning the feasibility of Valsalva’s and Toynbee’s clinical symptoms. Subsequently, in a retrospective clinical study, Schr€ oder et al. [11] extended the classic ETS scale formulated by Ockermann et al. [12] to include the results of tympanometry and objective Valsalva. Hence, they proposed the new ETS-7 that employs multiple parameters to obtain a more precise evaluation of the Eustachian tube function. Recent studies adopted this score to analyze the function of the ET in different patients and/or pathologies [5,6]. The ETS-7 score was used in this study to evaluate the prevalence of ETD in OSA patients, with interesting results emerged. Twenty percent of the patients with a diagnosis of OSA had an ETS-7  7 with a diagnosis of ETD. Besides, OSA patients showed an higher incidence of ETD in comparison to the control group (3.3% of these patients reported ETD), consisting of adult patients without sleep apnea syndrome. Similar characteristics regarding sex incidence and average age were present between study and control group, excluded these aspects as possible selection bias in the method enrollment of OSA patients and control group. These aspects would seem to corroborate our findings. Only two patients of the OSA group showed a type C tympanogram according to Jerger’s classification (tympanometric result indicative of a possible diagnosis of ETD). These data confirmed, as also recently claimed by many authors, that the ETS-7 score has a diagnostic value much more reliable in the diagnosis of ETD if compared with clinical and tympanometric evaluation alone [5,11]. Although no statistical differences regarding ETD emerged between

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severe, moderate and mild OSA patients, it should be noted that a greater number of severe patients with OSA have a diagnosis of ETD. Theoretically, the number and duration of the apnea crises may be directly related to the modification of the pressure in the nasopharynx and the incorrect opening of the Eustachian tube. However, definitive results regarding this aspect cannot be provided in this preliminary study. Only an extensive study with more cases will be able to clarify this important aspect. Which factors could predispose OSA patients to an Eustachian tube dysfunction? Usually the etiology of ETD is attributed to structural as well as functional entities and includes nasal obstruction, chronic sinusitis, allergic rhinitis, adenoid hyper-trophy, tobacco smoking, reflux, cleft palate, radiation therapy, reduced mastoid air cell system and exposure to nitrous oxide [3–5,12]. The relationship between the middle ear, the nasopharynx and the nasal cavity has been investigated in many studies [4,9,10]. To this regard, some authors affirmed that an incorrect middle ear ventilation is due to an inadequate air passage through the nasal cavity and the nasopharynx [4,9,10]. Therefore, a blocked nose is considered to be one of the main factors that could predispose to a Eustachian tube dysfunction by many authors [4,9,10]. Finally, it should be considered that any factor causing an inflammation of the rhinopharynx mucous may also cause phlogosis and/or swelling of the Eustachian tube orifice mucosa that, consequently, might not be opened promptly and sufficiently. Lazo-Saenz et al. [17] demonstrated that ET function in children has a stronger correlation with inflammatory nasal pathologies. In a subsequent study, Bakhshaee et al. [9] reported that subjective symptoms of ETD such as hearing loss and aural fullness, flat tympanogram and disturbed Toynbee and Valsalva tests, were significantly higher among the population of patients who suffered from chronic rhino-sinusitis. Patients with obstructive sleep apnea often showed severe nasal obstruction, chronic sinusitis and/or a deficit of nasal mucociliary clearance with nasopharyngeal stagnation of secretions [7,8,16,18]. Twenty-nine (72%) patients of the study group had pathological bilateral values of nasal airway resistance at the rhinomanometry examination. The difference between the incidence of pathological rhinomanometry in OSA patients and the control group was statistically significant (p ¼ .0001). Despite the fact that all OSA patients with an ETS-7  7 reported a pathological rhinomanometry, there was no difference in the group of study between patients with and without ETD regarding rhinomanometry results (p ¼ .08). These data could indicate that nasal obstruction is more frequent in patients suffering from sleep apnea: however, this condition might not be the only factor related to the onset of ETD in OSA patients. The mean value of NMCT in OSA patients was higher than in the control group (13.8 min versus 9 .4 min) and the average mucociliary transport time of OSA patients with ETD was greater than the mean value of the NMCT in the remaining OSA patients without ETD. Such differences

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could be indicate that a deficit in mucociliary clearance due to inflammation of the rhinopharynx and ET orifice mucous is more frequent in case of ETD. In our opinion, in patients with obstructive sleep apnea syndrome, several factors (nasal obstruction, increase in upstream airflow resistance, inflammation of the rhinopharynx and ET orifice mucous) could responsible for ET collapse, hindering its correct opening to exchange air with the middle ear.

[2]

Conclusion

[6]

In conclusion, our data showed that ET blockage or delayed opening are present in different adult patients with OSA when evaluated by a sensitive scoring system such as the ETS-7. This study suggests that an evaluation of the Eustachian tube function should be performed in patients suffering from obstructive sleep apnea syndrome.

Disclosure statement

[3]

[4]

[5]

[7]

[8]

[9]

[10]

The authors declare that they have no conflict of interest. [11]

Ethical approval All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and/ or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors. Write informed consent was obtained from all individual participants included in the study.

[12]

ORCID

[15]

Giuseppe Magliulo

http://orcid.org/0000-0003-3052-1969

[13]

[14]

[16]

[17]

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Eustachian tube evaluation in patients with obstructive sleep apnea syndrome.

Investigate the presence of Eustachian Tube Dysfunction (ETD) in Obstructive sleep apnea (OSA) patients. Correlate the ET function and the severity of...
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