otitis media with effusion case study

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StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024 Jan-.

StatPearls [Internet].

Otitis media with effusion.

Frederick T. Searight ; Rahulkumar Singh ; Diana C. Peterson .

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Last Update: May 20, 2023 .

• Continuing Education Activity

Otitis media with effusion (OME) is a condition in which there is fluid in the middle ear but no signs of acute infection. As fluid builds up in the middle ear and Eustachian tube, it places pressure on the tympanic membrane. The pressure prevents the tympanic membrane from vibrating properly, decreases sound conduction, and therefore results in decreased hearing. This activity reviews the pathophysiology and presentation of otitis media with effusion and highlights the role of the interprofessional team in its management.

• Describe the risk factors for otitis media with effusion.
• Explain the presentation of a patient with otitis media with effusion.
• Summarize the treatment options for otitis media with effusion.
• Review the importance of improving care coordination among interprofessional team members to improve outcomes for patients affected with otitis media with effusion.
• Introduction

Otitis media with effusion (OME) is a condition in which there is fluid in the middle ear but no signs of acute infection. As fluid builds up in the middle ear and Eustachian tube, it places pressure on the tympanic membrane. The pressure prevents the tympanic membrane from vibrating properly, decreases sound conduction, and therefore results in a decrease in patient hearing. Chronic OME is defined as OME that persists for 3 or more months on examination or tympanometry, although some clinicians recommend reserving the term ‘chronic otitis media’ for patients in which the tympanic membrane has perforated. [1]

Risk factors for OME include passive smoking, bottle feeding, daycare nursery, and atopy.  [2]  Both children and adults can develop OME. However, the etiology of these populations is different. The Eustachian tube is positioned more horizontally in younger children. As the child develops into an adult, the tube elongates and angles caudally. Therefore, OME is more common in children, and the position of the head at this age can influence the development of OME.  [3]  Children with development anomalies including the palate, palate muscles, decreased muscle tone for palate muscles, or bone development variations are at increased risk of development of OME, e.g., cleft palate, Down Syndrome.  [4]  Beyond these anatomical variations, patients with Downs syndrome can have mucociliary function disorders that increase the risk of developing OME.  [2] [5]

• Epidemiology

OME is one of the most frequent infectious diseases in children and is the most common cause of acquired hearing loss in childhood.  [6]  The disease commonly affects children between the ages of 1 and 6.  There is a higher prevalence at the age of 2, which drops after the age of 5. OME is more prevalent during the winter months, corresponding to higher patient rates of upper respiratory infections. 

• Pathophysiology

After an acute otitis media in children, fluid builds up in the middle ear, inhibiting vibration of the tympanic membrane and subsequent transmission of sound into the inner ear. With this deficit, children may have a decreased ability to communicate in noisy environments. The child may show signs of inattention or decreased academic performance.

In patients with large adenoids, the adenoids can obstruct the Eustachian tube resulting in a poorly ventilated middle ear. This type of blockage may result in OME. Because the adenoids are a lymphatic structure, it is possible that they can transmit bacteria into the Eustachian tube and allow the growth of biofilms. Such bacterial growth can cause inflammation that would also facilitate blockage and fluid build-up within the middle ear.

• Histopathology

The first line of defense in the middle ear is thought to be the mucociliary defense system in the Eustachian tube. Immunoglobulins produced by the mucosa contribute to this defense system. Due to the significant elevation of these immunoglobulins in effusions, these defense systems may be overactive in OME.  [7]

• Toxicokinetics

Otitis may also be caused by inflammation driven by viruses or allergies. While allergy is a significant risk factor for otitis media, clinical practice guidelines (2004) concluded that there was little evidence to support specific management strategies for allergy-induced OME. However, it is logical to conclude that aggressive treatment of allergic rhinitis may assist patients that develop OME in conjunction with allergies. [8]

• History and Physical

Hearing loss, although not always present, is the most common complaint in OME patients. Patients or parents of patients may complain of communication difficulties, withdrawal, and lack of attention. During an exam, a clinician may notice impaired speech and language development. Otalgia and earache can be intermittent in these patients. In many instances, they will have the symptom of aural fullness or a sensation that the ear is popping. In adults, OME is more often unilateral. Adult patients may report tinnitus and the sensation of a foreign body in the external auditory canal. In either children or adults, OME commonly occurs concurrently with upper respiratory infections. Therefore, it is good to ask patients about prior or recurrent ear infections, nasal obstruction, and upper respiratory tract infections.

During a physical examination, signs of OME include opacification of the tympanic membrane and loss of the light reflex. There may also be a retraction of the tympanic membrane with decreased mobility. If gross retraction of the tympanic membrane is observed, intervention may be required to prevent the formation of a retraction pocket, such as modified cartilage augmentation tympanoplasty. [9] [1]

Age appropriate audiometry and tympanometry should be tested in patients with otitis media with effusion. A ‘flat’ tympanogram will support a diagnosis of otitis media with effusion.  [10] Hearing can be tested in infants with the use of auditory brainstem responses (ABR). This exam tests the electrical activity of the brainstem to acoustic stimuli. The test detects both the frequency range and sound intensity levels in which the patient’s brain responds. Patients do not need to be able to speak and do not even need to be awake to perform the test. Therefore, it is ideal for children from birth to 5 years of age.  [11]

With older children and adults, although ABR testing can still be performed, it is more common to do a classic audiology exam. This exam consists of playing sounds to the patient’s left and right ears at different tones and intensities. Patients are requested to raise either the right or left hand when they hear a sound in the right or left ears, respectively. Results will identify the frequency range and normal hearing levels of the patient.

Individuals with normal hearing can detect lower frequencies at a lower decibel (i.e., intensity) than higher frequencies, meaning that a normal individual needs a sound to be louder to perceive high frequencies than lower frequencies. During an audiology exam, the range of frequencies that an individual can perceive is plotted on an audiograph. The decibel (dB) range of individuals with OME is decreased in the audiograph. 

Hearing loss levels (reduction in hearing thresholds from normal levels):

• Slight impairment: 26-40 dB
• Moderate impairment: 41-60 dB
• Severe impairment: 61-80 dB
• Severe hearing loss: 71-90 dB
• Profound impairment, including deafness: 81 dB or higher. [12]
• Treatment / Management

Otitis media with effusion generally resolves spontaneously with watchful waiting. However, if it is persistent, myringotomy with tympanostomy tube insertion is considered an effective treatment. [13]  In this treatment, a ventilation tube allows for air entry into the middle ear, preventing the re-accumulation of fluid. After this procedure, many patients do not need additional therapy due to the growth and development of the Eustachian tube angle, which will allow for drainage. The most common complication is the development of persistent otorrhea. Otorrhea is seen in nearly 1 in 6 (16%) of children within 4 weeks of surgery, and in 26% of children during the entire period, the tube is in place.

Adenoidectomy is currently utilized in cases of OME that involve enlarged adenoids and is an important addition to management in patients with OME.  [14]

Childhood hearing loss can affect language development. [15]  Therefore hearing aids may be considered a non-invasive option to treat OME. [16]

Clinician decisions for the correct interventional treatment of OME for a specific patient include a variety of factors.

• Comorbidities of the patient
• The severity of hearing loss
• OME presence unilaterally or bilaterally
• Effusion duration
• Age of patient

Social factors

• Cost to patient
• Patient’s likelihood of adherence to treatment
• Familial assistance with treatment

A patient-focused approach should be adopted when assessing hearing disability. How the child is coping socially and at school is more important than the results of audiometry investigations. [17] [18] [19]  Although most OME patients will warrant a conservative management approach as opposed to more invasive interventions, all physical and social factors should be examined to provide a patient-centered treatment plan that optimizes outcomes for the patient. [20] [21] [22]

• Differential Diagnosis

OME needs to be distinguished from acute otitis media  [23] , and in adults, OME can be caused by a nasopharyngeal carcinoma infiltrating the Eustachian tube.  [24]

• Surgical Oncology

Although patients with OME may show no signs or symptoms except for the loss of hearing associated with OME, 5.7% of patients develop the OME due to an obstruction caused by a nasopharyngeal carcinoma. Examination of the nasopharynx, as well as the external acoustic meatus, is suggested with OME patients. If abnormalities are observed within the nasopharynx, a biopsy of the postnasal space is suggested.  [25]

• Radiation Oncology

In patients with nasopharyngeal carcinoma, OME can be induced by radiation treatments. This type of OME may persist over several months.  [26]  More research is needed to determine the risks of developing OME post-radiotherapy and how irradiation dosages may influence this complication.  [27]

• Pertinent Studies and Ongoing Trials

Several different therapies have been tried to find effective treatment options for OME. The use of oral steroids in children has shown some benefits. However, it is unknown whether these benefits are clinically significant. [28]  Otic drops have also been utilized to maintain tympanostomy tube patency. These trials showed no statistical differences in the occlusion rate between patients that received the drug therapy and control (no drug) conditions. [29]

• Treatment Planning

OME is most commonly caused by either viral or allergy-related factors, not bacterial infection. Therefore, the use of antibiotics is not recommended. Also, corticoids for the treatment of allergies have not been significantly proven to impact the outcomes of OME in patients. For these reasons, antibiotics and corticoids are not recommended to treat OME. The best practice for OME patients is watchful waiting for three months as a first-line measure. In cases where OME persists, a specialist referral may be made to assess for surgical treatment options. [30]

• Toxicity and Adverse Effect Management

Ototopical drops can be ototoxic if they enter the middle ear and reach the inner ear. [31]  However, ototopical drops are not routinely used to treat OME.

• Medical Oncology

Radiotherapy after nasopharyngeal carcinoma can produce various complications. The most common complication is xerostomia (i.e., dry mouth caused by a lack of saliva). In some cases, a persistent OME may develop, facilitating the need for additional therapy or surgical intervention. [31]

Most cases of OME resolve on their own. In persistent cases, the condition impedes a patient's ability to hear. Therefore, communication and socialization can be affected. In young children, hearing deficits can cause learning problems or delayed language development. The impact of OME on these factors has not been fully studied. [32]  Unusual complications of OME include dizziness, behavioral disorders, and clumsiness. [33]

• Complications

Long-term changes of the middle ear and tympanic membrane may occur with persistent OME, resulting in permanent hearing loss. Ventilation tubes are used to try and prevent these long-term complications. However, even in treated patients, complications such as tympanosclerosis may occur.   [34]

• Postoperative and Rehabilitation Care

Alongside medical and surgical treatment of OME, Eustachian tube rehabilitation may also be useful in management. Rehabilitation of the Eustachian tube can include muscle strengthening exercises for the tensor veli palatini and levator veli palatini muscles via auto-insufflation, breathing exercises, and education for the improvement of nasal hygiene. [35]

• Consultations

Contact with a wide range of medical professionals, including audiologists and otolaryngologists, is important in OME to ensure holistic care for these patients.

• Deterrence and Patient Education

To avoid the potential of ventilation tube complications, many doctors and parents prefer non-invasive therapies, e.g., hearing aid usage. Reassurance and explanation of the ‘watchful waiting’ approach is an important part of management for patients who do not have speech, language, or developmental problems and for those in whom audiometry shows normal hearing. If ‘watchful waiting” is utilized, the patient should be watched closely for changes in symptoms or signs of increased pressure on the tympanic membrane, as rupture would induce a poor prognosis for future hearing in these patients.

Parents of children with recurrent OME should be informed and educated about the anatomy of the middle ear. Clinicians should identify the family activities of the child in relation to the head position (e.g., breastfeeding, sleeping patterns). Manipulation of the head position during these activities may allow for optimal drainage and assist the child in the prevention of subsequent episodes of OME in the future. 

• Enhancing Healthcare Team Outcomes

Management goals of OME include: eliminating middle ear fluid, improving hearing, and preventing future episodes. In all cases, communication between health care providers, nurse practitioners, patients, and patients' families will assist clinicians to identify optimal treatment plans for patients with OME. 

Children in whom ‘watchful waiting’ is the adopted strategy should be reassessed every 3-6 months until there is a resolution of the effusion or intervention is required. Also, families should be informed about signs and symptoms indicative of progressed pathology. In these instances, subsequent conversations about alterations to the treatment plan may be needed. The outcome for most children is good.

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Acute Otitis Media Contributed by Wikimedia Commons, B. Welleschik (CC by 2.0) https://creativecommons.org/licenses/by/2.0/

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Disclosure: Frederick Searight declares no relevant financial relationships with ineligible companies.

Disclosure: Rahulkumar Singh declares no relevant financial relationships with ineligible companies.

Disclosure: Diana Peterson declares no relevant financial relationships with ineligible companies.

This book is distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) ( http://creativecommons.org/licenses/by-nc-nd/4.0/ ), which permits others to distribute the work, provided that the article is not altered or used commercially. You are not required to obtain permission to distribute this article, provided that you credit the author and journal.

• Cite this Page Searight FT, Singh R, Peterson DC. Otitis Media With Effusion. [Updated 2023 May 20]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024 Jan-.

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• Clinical Practice Guideline: Tympanostomy Tubes in Children (Update). [Otolaryngol Head Neck Surg. 2022] Clinical Practice Guideline: Tympanostomy Tubes in Children (Update). Rosenfeld RM, Tunkel DE, Schwartz SR, Anne S, Bishop CE, Chelius DC, Hackell J, Hunter LL, Keppel KL, Kim AH, et al. Otolaryngol Head Neck Surg. 2022 Feb; 166(1_suppl):S1-S55.
• Clinical Practice Guideline: Otitis Media with Effusion (Update). [Otolaryngol Head Neck Surg. 2016] Clinical Practice Guideline: Otitis Media with Effusion (Update). Rosenfeld RM, Shin JJ, Schwartz SR, Coggins R, Gagnon L, Hackell JM, Hoelting D, Hunter LL, Kummer AW, Payne SC, et al. Otolaryngol Head Neck Surg. 2016 Feb; 154(1 Suppl):S1-S41.
• Clinical practice guideline: Tympanostomy tubes in children. [Otolaryngol Head Neck Surg. 2013] Clinical practice guideline: Tympanostomy tubes in children. Rosenfeld RM, Schwartz SR, Pynnonen MA, Tunkel DE, Hussey HM, Fichera JS, Grimes AM, Hackell JM, Harrison MF, Haskell H, et al. Otolaryngol Head Neck Surg. 2013 Jul; 149(1 Suppl):S1-35.
• Review Grommets (ventilation tubes) for hearing loss associated with otitis media with effusion in children. [Cochrane Database Syst Rev. 2005] Review Grommets (ventilation tubes) for hearing loss associated with otitis media with effusion in children. Lous J, Burton MJ, Felding JU, Ovesen T, Rovers MM, Williamson I. Cochrane Database Syst Rev. 2005 Jan 25; (1):CD001801. Epub 2005 Jan 25.
• Review Otitis media with effusion. [Pediatrics. 2004] Review Otitis media with effusion. American Academy of Family Physicians, American Academy of Otolaryngology-Head and Neck Surgery, American Academy of Pediatrics Subcommittee on Otitis Media With Effusion. Pediatrics. 2004 May; 113(5):1412-29.

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2:  Acute Otitis Media

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Patient presentation.

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Chief Complaint

“Increased irritability and right ear pain.”

History of Present Illness

JL is a 22-month-old female who presents to her primary care provider (PCP) with a 2-day history of rhinorrhea and a 1-day history of increased irritability, fever (to 101.5°F per Mom), and right-ear tugging. Mom denies that JL has had any nausea, vomiting, or diarrhea.

Past Medical History

Full-term birth via spontaneous vaginal delivery. Hospitalized at 9 months of age for respiratory syncytial virus–associated bronchiolitis. Two episodes of acute otitis media (AOM), with last episode about 6 months earlier.

Surgical History

Social history.

Lives with mother, father, and her 5-year-old brother who attends kindergarten. JL attends daycare 2 d/wk, and stays at home with maternal grandmother 3 d/wk.

No known drug allergies

Immunizations

Home medications.

Vitamin D drops 600 IU/d

Physical Examination

Vital signs (while crying).

Temp 100.7°F, P 140 bpm, RR 35, BP 100/57 mm Hg, Ht 81 cm, Wt 23.7 kg

Fussy, but consolable by Mom; well-appearing

Normocephalic, atraumatic, moist mucous membranes, normal conjunctiva, clear rhinorrhea, moderate bulging and erythema of right tympanic membrane with middle-ear effusion

Good air movement throughout, clear breath sounds bilaterally

Cardiovascular

Normal rate and rhythm, no murmur, rub or gallop

Soft, non-distended, non-tender, active bowel sounds

Genitourinary

Normal female genitalia, no dysuria or hematuria

Alert and appropriate for age

Extremities

1. Which of the following clinical criteria is not part of the diagnostic evaluation or staging of acute otitis media (AOM) for this patient?

A. Rhinorrhea

D. Contour of the tympanic membrane

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INTRODUCTION

In general, OME is a spontaneously resolving condition, and watchful observation is the preferred strategy, except for children with hearing impairment, developmental delay, or specific conditions (such as cleft palate) in whom OME is often persistent and needs to be addressed. The management of OME will be reviewed here. The clinical features and diagnosis of OME and the clinical features, diagnosis, treatment, and prevention of AOM are discussed separately:

● (See "Otitis media with effusion (serous otitis media) in children: Clinical features and diagnosis" .)

● (See "Acute otitis media in children: Epidemiology, microbiology, and complications" .)

● (See "Acute otitis media in children: Clinical manifestations and diagnosis" .)

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Risk factors for persistent otitis media with effusion in children: a case-control study.

Author information, affiliations, orcids linked to this article.

• Kim SH | 0000-0002-1694-9435
• Song CI | 0000-0002-2705-4100
• Kim YJ | 0000-0002-2832-036X
• Choi JH | 0000-0003-3284-9407
• Lee JY | 0000-0003-4172-2766

Yeungnam University Journal of Medicine , 30 Jun 2018 , 35(1): 70-75 https://doi.org/10.12701/yujm.2018.35.1.70   PMID: 31620573  PMCID: PMC6784671

Abstract 

Free full text , risk factors for persistent otitis media with effusion in children: a case-control study, ju yeon lee.

1 Department of Pediatrics, Jeju National University Hospital, Jeju, Korea

Se-Hyung Kim

2 Department of Otorhinolaryngology, Jeju National University School of Medicine, Jeju, Korea

Chan Il Song

Young ree kim.

3 Department of Laboratory Medicine, Jeju National University School of Medicine, Jeju, Korea

Yoon-Joo Kim

4 Department of Pediatrics, Jeju National University School of Medicine, Jeju, Korea

Jae Hong Choi

Otitis media with effusion (OME) is defined as middle ear effusion without acute signs of infection. OME usually resolves spontaneously; however, persistent OME may require the insertion of a ventilation tube. This study investigated risk factors for persistent OME in children who undergo ventilation tube insertion.

Children who were admitted to undergo ventilation tube insertion at Jeju National University Hospital between August 2015 and July 2016 were enrolled as the case group. Healthy children without persistent OME from August 2016 to July 2017 were enrolled as the control group. Baseline characteristics and predisposing factor data were collected using an interview questionnaire. Middle ear fluids were collected from the case group.

A total of 31 patients underwent ventilation tube insertion. The mean age of the case group was 4.53 years, with a male-to-female ratio of 21:10. Twenty-nine (93.5%) children attended a daycare center, and 21 (67.7%) had experience with bottle feeding. Fifteen (48.4%) children in the case group and 3 (9.7%) in the control group first attended a daycare center at <1 year of age (odds ratio=9.96; 95% confidence interval=2.44-39.70; p =0.001). No bacteria were found in middle ear fluid collected from the 31 operated children. Nasopharyngeal bacterial colonization was found in 13 (41.9%) and 17 (54.8%) children in the case and control groups, respectively.

Earlier attendance at a daycare center was the only predisposing factor for ventilation tube insertion in our study. The aseptic nature of middle ear fluids found in children with OME highlights the efficacy of antimicrobial use.

• INTRODUCTION

Otitis media with effusion (OME) is characterized by a nonpurulent effusion from the middle ear without symptoms such as otalgia or fever. OME is believed to follow an episode of acute otitis media or abnormal Eustachian tube function. Individuals with OME usually exhibit no specific symptoms; the disease is self-limited within approximately 3 months without specific treatment [ 1 ]; however, it does recur in 30-40% of cases [ 2 ].

Some birth cohorts have reported that >90% children experience at least one episode of OME before 4 years of age [ 2 , 3 ]. OME is the most common cause of acquired hearing impairment in children; permanent hearing loss related to otitis media has a prevalence of 2-35 per 10,000. Although symptoms are not severe, the highest incidence of OME occurs during a highly important period of language skill development. Thereafter, periodic hearing tests are essential to preserving hearing ability in OME patients [ 4 ].

The ultimate treatment goal for OME is to mitigate hearing loss. American guidelines recommend that physicians manage children with OME who are not at risk with watchful waiting for 3 months from the date of effusion onset without antimicrobial treatment [ 4 , 5 ]. However, the guidelines also recommend that clinicians offer ventilation tube insertion to children with documented hearing difficulties, structural abnormalities of the tympanic membrane or middle ear, increased risk for speech and/or language difficulties, and/or reduced quality of life in cases of OME lasting ≥3 months [ 5 ].

Predisposing factors for persistent OME that require ventilation tube insertion include: attendance at a day care center, familial history of otitis media, low socio-economic status, tobacco smoke exposure and adenoid hypertrophy [ 6 , 7 ]. Allergic tendency or biofilm formation of nasal colonizing bacteria is suspected to contribute to the pathogenesis of persistent OME [ 8 - 10 ]. Recurrent otitis media is known to be another risk factor for persistent OME. Although the pathogenesis of recurrent otitis media is multifactorial, the invasion of nasopharyngeal colonizing bacteria is believed to be related [ 11 , 12 ]. The most frequent pathogens colonizing the nasopharynx include Streptococcus pneumoniae, Haemophilus influenzae , and Moraxella catarrhalis .

In Korea, the clinical guidelines for pediatric otitis media has been updated [ 13 ]. This domestic guideline recommends the appropriate use of antimicrobials, an indication for ventilation tube insertion, and the importance of hearing tests during treatment for OME, which were not different from other guidelines [ 4 , 13 ]. However, long-term antimicrobial use (>3 months) for the treatment of OME was usually found in the clinical field.

A previous domestic study investigating OME reported risk factors for children undergoing recurrent ventilation tube insertion or ventilation tube insertion for children with craniofacial abnormalities [ 14 ]. We investigated the risk factors for persistent OME in children according to need for middle ear ventilation. Our aim was to determine the relationship between the colonization of bacteria in the nasopharynx and middle ear effusion.

• MATERIALS AND METHODS

1. Study subjects and design

The present investigation was a prospective case-control study. Children <12 years of age, who were admitted for ventilation tube insertion at Jeju National University Hospital (JNUH) between August 2015 and July 2016, were enrolled as the case group. All participants were enrolled when they were definitively diagnosed with OME by two otolaryngologists. The children were scheduled to undergo middle ear ventilation for persistent OME 3 months after diagnosis, despite previous antimicrobial use. Patients with immunodeficiency disorders or craniofacial abnormalities, such as cleft palate and/or cleft lip, were excluded. However, patients who previously underwent ventilation tube insertion were included.

A group of age- and sex-matched subjects representing the controls was chosen from a group of healthy children without persistent OME, who visited the JNUH between August 2016 and July 2017. Apart from no history of persistent OME, subjects with recurrent acute otitis media were excluded. The present study was approved by the Institutional Review Board of Jeju National University Hospital (IRB No. 2015-05-006). Informed written consent was obtained from all participants before enrollment.

2. Data and specimen collection

Baseline characteristics and predisposing factors for the case and control groups were collected using a questionnaire interview. Investigated factors included: age, sex, familial member, pattern of daycare center attendance, recent history of antimicrobial use, history of breastfeedin, exposure to tobacco smoke in the house and vaccination history. Daycare center attendance was defined as attendance at a daycare center for at least 6 months, or younger subjects who attended a daycare center when enrolled in the study. Breastfeeding was defined in children who were breastfed for at least 2 months, and was distinguished from bottle feeding. History of pneumococcal conjugate and H. influenzae type b vaccination was also examined.

3. Statistical analysis

Statistical analysis was performed using R software version 3.4.3 (R Foundation for Statistical Computing, Vienna, Austria). The relationship between the investigated risk factors and middle ear ventilation tube insertion was analyzed using the chi-square test. Multivariate logistic regression analysis was performed, and the data are expressed as odds ratio (OR) and 95% confidence interval (CI). All tests were two tailed, and p <0.05 was considered to be statistically significant.

A total of 31 patients (21 male, 10 female) underwent ventilation tube insertion. The mean age of the case group was 4.53 years (median age, 4.20 years [range, 0.95-12.00 years]); the mean age of the control group was 4.06 years (median age, 3.88 years [range, 0.74-12.22 years]). In the case group, 26 patients underwent bilateral ventilation tube insertion, and 11 underwent unilateral insertion. There were no complications after the operation. Before the operation, hearing tests, such as tympanometry or pure tone audiometry, were performed in 20 (64.5%) patients. All of them had hearing loss; more specifically, 18 (90%) had 20-40 dB hearing loss, and 2 had <20 dB hearing loss. We determined ventilation tube insertion after counselling in 11 patients who did not undergo a hearing test because the parents complained of middle ear effusion >3 months.

In the case group, 29 (93.5%) children attended a daycare center, which was more than in the control group (n=23); this difference was not statistically significant (OR=5.04; 95% CI=0.98-26.09; p =0.084) ( Table 1 ). However, the number of subjects <1 year of age who attended a daycare center was 15 (48.4%) in the case group, which was significantly more than the number of children in the control group (n=3 [48.4%]); this difference was statistically significant (OR=9.96; 95% CI=2.44-39.70; p =0.001) ( Fig. 1 ). There were more breastfed children in the control group (n=22) than in the case group (n=19) ( p =0.592), and more bottle-fed children in the case group (n=21) than in the control group (n=18) ( p =0.599). However, these feeding habits had no statistically significant influence on ventilation tube insertion for OME ( Table 1 ). Exposure to household tobacco smoke appeared to have no significant effect on persistent OME. Regardless of whether subjects had siblings, there were no differences in the prevalence of persistent OME. In the case group, there were no siblings who underwent ventilation tube insertion.

Odds ratio of patient characteristics who underwent ventilation tube insertion. DCC, daycare center; Hib, Haemophilus influenzae type b; PCV, pneumococcal conjugate vaccine.

General characteristics of otitis media in the case and control groups

OR, odds ratio; CI, confidence interval; Hib, Haemophilus influenzae type b; PCV, pneumococcal conjugate vaccine.

Eighteen (58.1%) children in the case group and 16 (51.6%) in the control group were taking antibiotics for persistent OME. Contrary to expectations, no bacteria were isolated from middle ear effusions collected from those who underwent ventilation tube insertion. The positive nasopharyngeal carriage rate was 41.9%(13/31) in the case group: S. pneumoniae (n=6); H. influenzae (n=2); and M. catarrhalis (n=6). In the control group, the nasopharyngeal carriage rate was 54.8%(17/31): S. pneumoniae (n=6); H. influenzae (n=7); and M. catarrhalis (n=5) ( Table 2 ).

Microbiological status of otitis media in the case and control groups

Values are presented as number (%).

This investigation was a prospective study aimed at determining risk factors for ventilation tube insertion for persistent OME that did not spontaneously improve in children. Another goal of this study was to identify the relationship between nasopharyngeal colonizing bacteria and persistent middle ear effusion. Two otolaryngologists with experience in ventilation tube insertion in the middle ear were involved in this study. Indications for ventilation tube insertion were significant hearing loss due to persistent middle ear effusion, and persistent OME >3 months, which was refractory to spontaneous improvement despite of the use of antibiotics.

OME may occur after an upper respiratory tract infection due to poor Eustachian tube function or as a result of recurrent acute otitis media. A major risk factor for developing OME is age because of its direct correlation with the angulation of the Eustachian tube. Other factors reported to increase the risk for developing OME include daycare center attendance, exposure to tobacco smoke, low socio-economic status, shorter duration of breastfeeding, adenoid hypertrophy, and recurrent otitis media [ 6 , 7 , 15 , 16 ].

In our study, children <1 year of age, who attended a daycare center, was the only statistically significant risk factor ( Fig 1 ). Usually, younger children had more respiratory tract infections than adults because of their immature immune system. In addition, daycare center attendance enhances close contact with other children in confined spaces. In the present study, however, daycare attendance regardless of age had no clinically significant association with persistent OME. We speculate that the difference is the diluted result because of high attendance rates at daycare centers in both the case and control groups (52/62 [83.9%]). We did not use data for recurrent otitis media as a risk factor for persistent OME. The recall ability of the patients’ parents regarding the number of episodes or treatment of otitis media was uncertain. Attendance at a daycare center, however, was easy to recall, and this factor was believed to be related to recurrent otitis media. We used this particular questionnaire for our investigation based on previous studies [ 17 , 18 ].

Exposure to household tobacco smoke and breastfeeding were not significant factors for persistent OME. We had no method to quantitatively evaluate the level of smoke exposure or breastfeeding. There was no relationship between bottle feeding and persistent OME. We speculate that this can be explained by the fact that most of our participants combined breast and bottle feeding.

Experts have recommended the use of pneumatic otoscopy or tympanometry to assess OME with hearing loss [ 4 ]. Furthermore, the first-line treatment choice to manage persistent OME in individuals not at risk is watchful waiting for 3 months from the date of effusion onset. This recommendation was applied to children with hearing loss <20 dB. Ventilation tube insertion is the definitive treatment for removing middle ear effusions and an effective method to prevent conductive hearing loss caused by middle ear effusion. Operative methods, such as ventilation tube insertion, are especially recommended when structural damage to the tympanic membrane, tympanosclerosis, cholesteatoma, symptoms of otalgia or vertigo, and hearing loss >40 dB, are found [ 4 , 19 ].

Previous studies have reported that bacterial prevalence in middle ear effusions is 20-50%, although the population was diagnosed as acute otitis media or OME [ 20 - 23 ]. We assumed that some bacteria could be expected to be found in middle ear effusions, and the pathogen could have a relationship with nasopharyngeal colonizing bacteria. However, no bacteria were isolated from any of the 31 middle ear effusion samples collected. This may be explained by the indication for ventilation tube insertion that was applied to the study population, which was different from other studies. Regardless of antimicrobial use in the recent 2 months, the sterile nature of middle ear effusions support no need for antibiotics to treat persistent OME. The American clinical guidelines also made strong recommendations against using systemic antibiotics for treatment OME in children [ 4 ].

Recently, molecular genetic techniques, such as polymerase chain reaction (PCR), have replaced conventional culture methods. Using these recently developed techniques, detection rates of causative pathogens have increased. This methodology has been applied to middle ear fluid specimens [ 24 , 25 ]. However, we could not perform a PCR assay due to a storage problem. In addition, considering the over-detection of inactive bacteria in PCR assays, we focused on living bacteria isolated using conventional culture methods.

The contribution of nasopharyngeal colonizing bacteria to otitis media has been established, and the bacterial pathogens had been studied [ 26 , 27 ]. In our study, there was no difference in antimicrobial use during a recent 2-month period between the case and control groups. However, nasopharyngeal colonization rates in the control group (54.8%) were greater than those in the case group (41.9%). This result suggests that other factors, in addition to nasopharyngeal colonizing bacteria, contribute to persistent OME. We cannot draw definitive conclusions because some patients in the control group visited our hospital complaining of respiratory symptoms.

This study had some limitations, the first of which were the relatively small sample size and its single-center design. Other predisposing factors, such as adenoid hypertrophy and allergic disorders, could not be investigated. If patients who spontaneously improved after the diagnosis of OME were investigated, risk factors for ventilation tube insertion could be more defined. Despite these limitations, this study should prompt clinicians to prospectively investigate risk factors for ventilation tube insertion in patients with OME disease only. Additionally, during the study period, we applied strict indications for ventilation tube insertion while considering the guidelines. We were able to confirm the principle of test hearing loss watching for spontaneous improvement. The sterile middle ear fluid found in children with OME children support the efficacy of antimicrobial use. Earlier attendance at a daycare center was the only statistically significant risk factor and, therefore, should prompt careful consideration before a decision is made to send a child to a daycare center. Future studies investigating OME should further examine the relationship between ventilation tube insertion and antimicrobial use. Furthermore, we believe that molecular-based methods investigating middle ear effusion and nasopharyngeal aspirates are promising research areas to pursue.

• Acknowledgments

This work was supported by a research grant from Jeju National University Hospital in 2015.

No potential conflict of interest relevant to this article was reported.

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Determinants of chronic otitis media with effusion in preschool children: a case–control study

• Rebecca E. Walker 1 ,
• Jim Bartley 2 ,
• David Flint 2 ,
• John M. D. Thompson 1 &
• Edwin A. Mitchell 1  

BMC Pediatrics volume  17 , Article number:  4 ( 2017 ) Cite this article

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Chronic otitis media with effusion (COME) is a prevalent upper airway infection resulting in hearing loss. The aim of this research was to determine risk factors for COME in preschool children.

A case–control design was conducted in Auckland, New Zealand from May 2011 until November 2013. The cases were children aged 3 and 4 years referred for tympanostomy tube placement due to a diagnosis of COME ( n  = 178). The controls were a random sample of healthy children aged 3 and 4 years from primary care practices ( n  = 209). The children’s guardians completed an interviewer-administered questionnaire that covered topics including socio-demographic information, pregnancy and birth, infant feeding practices, home environment, and respiratory health. In addition, skin prick tests for atopy were performed. Odds ratios (OR) estimating the risk of COME independently associated with the exposures were calculated using a logistic regression model.

Children with COME frequently had nasal obstruction (OR: 4.38 [95% CI: 2.37–8.28]), always snored (OR: 3.64 [95% CI: 1.51–9.15]) or often snored (OR: 2.45 [95% CI: 1.04–5.96]), spent more hours per week in daycare (OR per hour/week: 1.03 [95% CI: 1.00–1.05]), had frequent colds (OR: 2.67 [95% CI: 1.59–4.53]), had siblings who had undergone tympanostomy tube placement (OR: 2.68 [95% CI: 1.22–6.02]), underwent long labour (OR: 2.59 [95% CI: 1.03–6.79]), and had early introduction of cow’s milk (OR: 1.76 [95% CI: 1.05–2.97]). Asian ethnicity (OR: 0.20 [95% CI: 0.07–0.53]) and having older siblings (OR: 0.54 [95% CI: 0.31–0.93]) were inversely associated with COME.

COME in preschool children was associated with pathogen exposure, respiratory infection, and nasal obstruction. Strategies to prevent pathogen transmission warrant investigation. The novel findings of long labour and early cow’s milk introduction require replication in future studies.

Peer Review reports

Otitis media with effusion (OME) is a childhood condition where fluid gathers behind the tympanic membrane. OME is a common reason for doctors’ visits, antibiotic use and surgery [ 1 ]. Chronic otitis media with effusion (COME), defined as effusion lasting 3 or more months, causes hearing loss that may lead to learning delays and behavioural problems [ 2 ].

COME is caused by bacteria and viruses entering the middle ear from the upper respiratory tract, leading to a chronic inflammatory response. COME chronicity may be explained by the formation of biofilms in the middle ear [ 3 ]. Biofilms are sessile communities of microorganisms that can evade the host’s immune system and are often resistant to antibiotic treatment [ 1 ]. Risk factors associated with COME include young age, ethnicity, family history, breastfeeding practices, exposure to other children, and upper respiratory infection (URI) [ 4 ]. Acute otitis media (AOM) and OME often follow each other, and can be viewed as aspects of a disease continuum.

While many risk factors for COME have been reported, there is a lack of recent research in which a wide range of potential determinants and confounders are considered together. The aim of the study was to examine a comprehensive array of variables, including prenatal and perinatal factors for which research is lacking [ 4 ], to identify risk factors that are independently associated with COME.

Study design

A case–control study of children aged 3 and 4 years was conducted, to compare children with COME to healthy children.

Recruitment and data collection were conducted between May 2011 and November 2013. Subjects were assessed in interview rooms at Waitakere Hospital or North Shore Hospital, in the Waitemata District Health Board (WDHB) catchment area in Auckland. WDHB is the largest of 20 district health boards in New Zealand (NZ), with a population of approximately 560,000 people, and the third most affluent. Its population consists of 10% Maori, 7% Pacific Island, and 19% Asian people, with the remaining 64% being European or Other ethnicities [ 5 ]. Children in NZ have free hospital care and primary care practice visits.

Participants

Cases were children aged 3 or 4 years referred for tympanostomy tube placement (TTP) at Waitakere Hospital, who had a recent medical history of COME and/or signs of COME confirmed by an otorhinolaryngologist during surgery.

Controls were selected at random from children enrolled in primary care practices in proportion to the number and sex of children those practices had referred to Waitakere Hospital for TTP in 2010. This approach was designed to recruit controls from the same population that cases were referred from, to mitigate against selection bias. Eligible controls were aged 3 or 4 years, had no medical history of TTP, no episodes of OME lasting longer than one month in the past year, and never had OME lasting longer than three months.

Cases and controls were excluded if they had craniofacial abnormalities including Down syndrome or cleft palate, or immunodeficiency, as risk factors for COME in children with these conditions may not be generalizable.

An interviewer administered a questionnaire to obtain information regarding socio-demographic factors, pregnancy, feeding practices, allergy, nasal symptoms, and childcare environment. The interviewer was blind to whether the participant was a case or control. Recall misclassification and bias was mitigated by using a standardized questionnaire including validated questions where available.

Respondents could provide multiple ethnicities, which were coded as a single ethnicity using the “prioritized output” method from the NZ Ministry of Health ethnicity data protocol [ 6 ]. The ethnicity categories were Maori, Pacific Island, Asian, European, and Other. European and Other ethnicity were grouped into a single European/Other category for analysis due to the small number of subjects of Other ethnicity. Residential address was used to assign NZ Deprivation Index (NZDep) ratings. NZDep is a validated proxy measure of socio-economic status (SES) ranging from 1 (least deprived) to 10 (most deprived) [ 7 ]. Crowding was assessed by number of people per bedroom. Long labour was defined as total length of labour (stage 1 and 2) lasting for 21 h or longer in first-born children or otherwise lasting 14 or more hours. These cutoffs were based on the top 5 th percentile of labour length in our control subjects. Mode of delivery was categorized as unassisted (normal vaginal delivery), elective Caesarean section, emergency Caesarean section, or forceps/vacuum delivery. Reflux in infancy was defined as bringing up milk and crying in pain after feeding. Colic in infancy was defined as prolonged crying, reddened face, tight body, and bringing up knees. Time of first exposure to cow’s milk (not including formula or foods containing cow’s milk) was dichotomized around the median time in the controls, which was 13 months. Allergic symptoms were assessed using questions from the ISAAC questionnaire ( http://isaac.auckland.ac.nz ). Allergic rhinoconjunctivitis was defined as sneezing, or a runny, or blocked nose, combined with itchy-watery eyes, in the absence of a cold or flu.

The child’s height and weight were measured, their temperature taken using an ear thermometer, pneumatic otoscopy and tympanometry were performed, and skin prick tests for house dust mite, cat pelt, dog, mold, birch tree and grass mix were administered following the Australasian Society of Clinical Immunology and Allergy protocol [ 8 ].

Other factors analyzed included maternal age, smoking during pregnancy, induced labour, small for gestational age (bottom 10% of birth weight adjusted for gestational age, parity, sex, and ethnicity) [ 9 ], season of birth, pacifier use, age of solid food introduction, maternal and child supplement use, and body mass index (BMI) Z-score (adjusted for age and sex) [ 10 ].

Statistical methods

To detect an odds ratio of 2 at the 5% level and 80% power, assuming an exposure frequency of at least 20% in the controls, a sample size of 173 cases and 173 controls is required.

Statistical analysis was conducted using JMP 12, SAS Institute Inc., Cary, NC, 1989–2015. Categorical variables were analyzed using a chi-squared test and continuous variables were analyzed using a Student t -test. Variables with a P value ≤ .1 were entered into a logistic regression model. Age in months, the child’s sex, and NZDep were retained in the model as potential confounders. The model was reduced by excluding the least significant variable with P  > .05, in a stepwise manner until all variables in the model remained significant at the 5% level. This was done to maximize sample size, due to missing data for some variables. Sensitivity analyses were conducted by adding each removed variable back into the final model to ensure that they remained non-significant and did not impact the variables in the model.

Of 259 potential cases identified, 18 were excluded due to surgery being cancelled or postponed, 35 due to not having COME, and 6 due to Down syndrome, cranial-facial abnormalities, or immunodeficiency. Of 200 cases confirmed eligible, 178 (89%) were enrolled. Of 517 potential controls identified, 27 were no longer in the study area, 47 were no longer in the age range, and 5 had Down syndrome, cranial-facial abnormalities or immunodeficiencies. A history of COME was found in 66 potential controls, 44 had TTP, 16 could not be contacted, and we were advised not to contact 9 subjects by their primary care practices. Of 303 controls confirmed eligible, 209 (69%) were enrolled (Fig.  1 ).

Recruitment stages and participation

The mean age of the cases was 47.8 months [standard deviation (SD) = 6.79], significantly younger than the controls who had a mean age of 49.3 months [SD = 6.67] ( P  = .04). Of the cases, 62% were male compared to 58% of controls ( P  = .42). Mean NZDep in the cases was 5.5 [SD = 2.66], higher (i.e. more deprived) than the controls who had a mean of 4.8 [SD = 2.65] ( P  = .01).

Variables with P values over .1 univariably that were not analyzed further were: induced labour, small for gestational age, season of birth, pacifier use, age of solid food introduction, maternal and child supplement use, positive skin prick test, eczema, BMI, and crowding.

Upright bottle-feeding was excluded from further analysis because children with COME are recommended to be bottle-fed upright in NZ [ 11 ]. Age at first episode of AOM and age of first starting antibiotics were excluded because AOM is part of the same disease continuum as COME and antibiotics are frequently prescribed for children with OM.

Variables with P values ≤ .1 univariably (Table  1 ) were analyzed using logistic regression. Those with P values over .05 in the stepwise model that were not entered into the final model were: maternal smoking during pregnancy, mode of delivery, breastfeeding duration, formula feeding, colic, reflux, parental smoking, childhood use of vitamin C, mouth breathing, full vaccination, probiotic use, wheezing, allergic rhinoconjunctivitis, runny nose, and maternal history of OM.

In the final multivariable model (Table  2 ), Asian ethnicity was inversely associated with COME as compared to European/Other ethnicity (OR: 0.20 [95% CI: 0.07–0.53]). Deprivation was not associated. Long labour (OR: 2.59 [95% CI: 1.03–6.79]), starting cow’s milk before 13 months of age (OR: 1.76 [95% CI: 1.05–2.97]), and having a blocked nose (always or often, OR: 4.38 [95% CI: 2.37–8.28]) were significant risk factors. Snoring was associated with COME when compared to never snoring (always, OR: 3.64 [95% CI: 1.51–9.15]) or often (OR: 2.45 [95% CI: 1.04–5.96]) Four or more colds in the last 12 months (OR: 2.67 [95% CI: 1.59–4.53]), siblings with a history of TTP (OR: 2.68 [95% CI: 1.22–6.02]), and number of hours per week at daycare (OR per hour: 1.03 [95% CI: 1.00–1.05]) were all risk factors, and having older siblings was inversely associated (OR: 0.54 [95% CI: 0.31–0.93]).

To address the many inter-related factors associated with COME, we included a comprehensive set of variables in our regression analysis. In addition to well known risk factors such as frequent URI, daycare attendance, and sibling history of TTP, we also identified some respiratory risk factors that were independently associated with COME, notably nasal obstruction and snoring. Prenatal and perinatal events also appear to impact the risk of COME in preschoolers, including long labour and early introduction of cow’s milk.

URI is a frequently observed risk factor [ 4 , 12 ]. In animal models, bacteria in the nose are more likely to ascend to the middle ear if respiratory viruses are also present [ 13 ]. Our finding regarding URI may reflect viruses acting as a compounding risk factor through polymicrobial interactions with bacteria in the nose and nasopharynx.

Daycare attendance exposes children to infection that can lead to COME [ 12 ]. Children congregating at daycare increases the transfer of viruses, and the transmission of bacteria that may survive in a biofilm state in mucous secretions on toys and other surfaces [ 14 ]. Sibling TTP being a risk factor may reflect shared family environment including parental healthcare practices, awareness of COME, or exposure to the same pathogens. It may also indicate familial predisposition, which is a risk factor supported by a number of twin studies [ 15 ], however a history of maternal OM was not significant in the multivariable analysis.

Reports as to whether atopy and allergic rhinitis are risk factors for OME are mixed [ 4 ]. We did not find atopic diseases to be risk factors for COME. The discrepancy among studies could be explained by blocked nose or URI acting as confounders, as these conditions are associated with both allergic conditions and COME. We used a validated questionnaire for rhinoconjunctivitis, eczema and asthma, which may have improved our specificity in identifying allergic diseases.

Frequent nasal obstruction in the last 12 months was reported in 53% of cases compared to 14% of controls, while frequent snoring in the last 3 months was found in 64% of cases versus 30% of controls. Nasal obstruction has been considered to be related to COME only via its associations with allergy and URI [ 16 ], however there is also evidence to support our finding that nasal obstruction and snoring can be associated with OM independently of allergy and colds [ 17 – 19 ]. Our observation that nasal obstruction was associated with COME independently of rhinitis, atopy, and URI raises the question of what other mechanism could be underlying this relationship. Given the importance of bacterial biofilms in the middle ear in causing COME [ 3 ], a possible explanation is that biofilms in the nose and nasopharynx act as a common factor for both chronic nasal obstruction and COME. In animal models biofilms can spread from the nose to the middle ear, leading to COME [ 13 ]. Nasal biofilms are associated with increased nasal resistance, a measure of nasal obstruction [ 20 ]. The otopathogen non-typable Haemophilus influenza requires anaerobic conditions to form biofilms [ 21 ], and may therefore be aided by nasal congestion. Although direct evidence that nasal and nasopharyngeal biofilms connect nasal obstruction to COME is lacking, adenoid hypertrophy in particular is a risk factor for nasal obstruction, snoring, and COME, with the preferred explanation being that adenoids can act as a reservoir for otopathogens [ 22 , 23 ].

In addition to respiratory factors, we made several findings regarding socio-demographic factors, perinatal factors and feeding practices. Maori and Pacific Island children in NZ are more likely to fail preschool hearing tests [ 24 ]. The prevalence of OME in 2 year old Pacific Island children has been measured at 25.4%, however chronicity and other ethnicities were not studied, and subjects were recruited from a less affluent area of Auckland [ 18 ]. We did not observe Maori or Pacific Island ethnicities to be risk factors for COME. If a correlation exists, it may be concealed by these families being less likely to attend primary care practices for COME, as our subjects are limited to those referred for surgery.

Asian ethnicity was inversely associated with COME. It is also inversely correlated with a diagnosis of AOM in the US [ 25 ]. A longitudinal study could determine whether this reflects a lower likelihood of referral/attendance for TTP surgery, genetic propensity, or cultural differences such as diet, housing, or hygiene practices.

Low SES is sometimes linked to OM [ 4 ]. In NZ, deprivation is associated with infectious diseases [ 26 ], surgical interventions for OM [ 27 ], and infection with the otopathogen Staphylococcus aureus [ 28 ]. However, we did not find deprivation to be associated with COME. Crowding and tobacco smoke exposure were also not identified as risk factors, in contrast to some previous studies [ 29 , 30 ]. It appears that the presence of COME is better predicted by other potentially related factors in our subjects.

Having older siblings was inversely correlated with COME. Previous research has found this to be a risk factor that declines with age, no longer being associated by 3 years of age [ 12 ]. Exposure to commensal bacteria from older siblings may help to protect children from infections and allergic manifestations [ 31 ].

Long labour was associated with COME. Prolongation of labour is the most common cause of maternal fever during labour, and is also associated with instrument use, emergency Caesarean section deliveries, and admission to neonatal care units [ 32 – 34 ]. In cases of maternal fever, prophylactic antibiotics are often administered to mother and newborn, which may affect the infant’s microbiome and thereby decrease their resistance to colonization with pathogens [ 31 , 34 ].

Longer duration of breastfeeding is sometimes reported as a protective factor against OM, and early introduction of infant formula or cow’s milk is sometimes found to be a risk factor [ 35 ]. The introduction of cow’s milk before 13 months of age was a risk factor for COME. Cow’s milk is not recommended until after 12 months of age, because its composition is significantly different to breast milk and infant formula, and its use can lead to iron deficiency [ 36 , 37 ]. Another consideration is cow’s milk protein allergy, which is associated with TTP [ 38 ]. We did not find infant formula to be a risk factor, even though it usually contains cow’s milk. This could be due to the differences in its content, or the use of hypoallergenic and dairy-free varieties. Infant consumption of cow’s milk also supports a different microbiome composition [ 39 ], which could promote pathogen colonization leading to COME.

A recent systematic review concluded that children with COME have a high prevalence of reflux, and suggested that aspiration of pepsin into the airways may result in an inflammatory response in the middle ear cavity [ 40 ]. Frequent reflux and colic were not significant in our final model and may only be related to COME via other risk factors.

Study limitations need to be considered. The cases were referred for surgery, so they may not represent all preschool children with COME. Retrospective case–control designs have a potential for selection bias and recall bias. Selection bias was mitigated by recruiting controls from practices that had recently referred preschoolers for surgery and by having a high participation rate. Differential recall bias was mitigated with the use of a standardized questionnaire using validated questions where available. While NZDep is a useful indicator of deprivation, it reflects data from a small area of houses rather than specific households. A major strength of the study is that an otorhinolaryngologist confirmed disease presence at surgery, which is preferable to relying on medical history or tympanometry alone. Furthermore, a comprehensive range of risk factors were explored and the sample size was relatively large, allowing us to have confidence in these findings.

Our results support well-established risk factors for COME relating to exposure to infection, specifically URI, daycare attendance, and sibling TTP.

There is growing interest in how respiratory microbiota may support the immune system against conditions such as COME. More investigation is required to confirm whether our results regarding older siblings, prolonged labour (with associated antibiotic use), and the timing of cow’s milk introduction reflect effects on the commensal microbiota.

We postulate that biofilms in the nose and nasopharynx link nasal obstruction, snoring, and COME. The child’s nose or nasopharynx is first colonized by otopathogenic bacteria that form biofilms. The resulting chronic inflammation may cause nasal obstruction and snoring, but fails to fully suppress the biofilm infection. The otopathogens pass up the Eustachian tube to the middle ear, a risk that is compounded by viral infection, and form biofilms again in the middle ear. This may produce chronic inflammation in the middle ear, i.e. COME. Research on the association between bacterial biofilms in the nose and nasopharynx, nasal obstruction, and COME is required to test this hypothesis.

Abbreviations

Acute otitis media

Body mass index

Chronic otitis media with effusion

The International Study of Asthma and Allergy in Children

New Zealand

New Zealand Deprivation Index

Otitis media

• Otitis media with effusion

Standard deviation

Tympanostomy tube placement

Upper respiratory infection

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Acknowledgments

We would like to thank Ann Paddy, DHSc, who administered the questionnaires and performed part of the physical examinations for the children involved in the study. Peter Reed, DPhil, helped with the statistical analysis. We would like to acknowledge the staff at Waitakere and North Shore Hospital, Bede Saldanha and Denise Burdett for going above and beyond reception support, and especially ear nurse specialist Barbara Middleton. Finally, a thank you to the families and their general practitioners whose help and support made the study possible. Edwin Mitchell and John Thompson were supported by Cure Kids.

The Oticon Foundation, Starship Foundation, Brian Johns Fellowship Trust, Deafness Research Foundation, and Cure Kids.

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Data is available on request from the author.

Authors’ contributions

REW designed the study, conducted all data collection, data analysis and interpretation, drafted the initial manuscript, and approved the final manuscript as submitted. JB assisted in the study design, supervised the data analysis and interpretation, reviewed and revised the manuscript, and approved the final manuscript as submitted. DF assisted in the study design, was involved in data collection, and approved the final manuscript as submitted. JMDT assisted in the study design, was involved in the data analysis, and approved the final manuscript as submitted. EAM designed the study, supervised the data analysis and interpretation, reviewed and revised the manuscript, and approved the final manuscript as submitted.

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The authors declare that they have no competing interests.

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Ethical approval and consent to participate

The parents or legal guardians were informed of the nature of the study and provided written consent. The study was approved by the Northern X Regional Ethics Committee (reference NTX/11/EXP/027).

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Walker, R.E., Bartley, J., Flint, D. et al. Determinants of chronic otitis media with effusion in preschool children: a case–control study. BMC Pediatr 17 , 4 (2017). https://doi.org/10.1186/s12887-016-0767-7

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Neutrophil Extracellular Trap Formation and Deoxyribonuclease I Activity in Patients with Otitis Media with Antineutrophil Cytoplasmic Antibody-Associated Vasculitis

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Shinya Morita , Yuji Nakamaru , Atsushi Fukuda , Keishi Fujiwara , Masanobu Suzuki , Kimiko Hoshino , Aya Honma , Akira Nakazono , Akihiro Homma; Neutrophil Extracellular Trap Formation and Deoxyribonuclease I Activity in Patients with Otitis Media with Antineutrophil Cytoplasmic Antibody-Associated Vasculitis. Int Arch Allergy Immunol 2024; https://doi.org/10.1159/000537927

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Introduction: No previous studies have evaluated the levels of neutrophil extracellular trap (NET) remnants or the importance of deoxyribonuclease (DNase) I activity based on the disease activity of otitis media with antineutrophil cytoplasmic antibody-associated vasculitis (OMAAV). The aim of this study was to explore the formation of NETs in the middle ear of patients with OMAAV during the onset and remission phases of the disease, with a particular focus on the relationships between the quantifiable levels of NET remnants and DNase I activity. Methods: OMAAV patients were eligible for inclusion. Patients with otitis media with effusion (OME) were examined as controls. The levels of cell-free deoxyribonucleic acid (DNA), citrullinated-histone H3 (cit-H3)-DNA complex, and myeloperoxidase (MPO)-DNA complex were quantified using an enzyme-linked immunosorbent assay. DNase I activity was measured using a fluorometric method. Results: The quantifiable levels of cell-free DNA, cit-H3-DNA complex, and MPO-DNA complex in the middle ear lavage of patients with OMAAV at onset were significantly higher than those in patients with OMAAV at remission and in patients with OME. DNase I activity in the patients with OMAAV at onset was significantly lower than those in patients with OMAAV at remission and OME and was negatively correlated with the level of MPO-DNA complex. Conclusions: This study suggests that NET remnants and DNase I activity may be potentially useful biomarkers for the diagnosis and disease activity of OMAAV.

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Research Article

Nasal microbial composition and chronic otitis media with effusion: A case-control study

Contributed equally to this work with: Rebecca E. Walker, Carlos A. Camargo Jr., Edwin A. Mitchell

Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Validation, Visualization, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Affiliation Department of Paediatrics: Child and Youth Health, The University of Auckland, Auckland, New Zealand

Roles Conceptualization, Data curation, Investigation, Methodology, Resources, Software, Writing – review & editing

¶ ‡ These authors also contributed equally to this work.

Affiliation Centre for Longitudinal Research–He Ara ki Mua, Department of Population Health, The University of Auckland, Auckland, New Zealand

Roles Conceptualization, Formal analysis, Methodology, Supervision, Writing – review & editing

Affiliation Department of Emergency Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, United States of America

Roles Conceptualization, Formal analysis, Methodology, Resources, Supervision, Writing – review & editing

Affiliation Division of Otolaryngology-Head and Neck Surgery, Counties-Manukau District Health Board, Manukau SuperClinic, Manukau City, Auckland, New Zealand

Roles Conceptualization, Methodology, Supervision, Writing – review & editing

Roles Conceptualization, Formal analysis, Methodology, Supervision, Validation, Writing – review & editing

Roles Conceptualization, Formal analysis, Funding acquisition, Methodology, Resources, Supervision, Writing – review & editing

• Rebecca E. Walker, 
• Caroline G. Walker, 
• Carlos A. Camargo Jr., 
• Jim Bartley, 
• David Flint, 
• John M. D. Thompson, 
• Edwin A. Mitchell

• Published: February 22, 2019
• https://doi.org/10.1371/journal.pone.0212473
• Reader Comments

Chronic otitis media with effusion (COME) in children can cause prolonged hearing loss, which is associated with an increased risk of learning delays and behavioural problems. Dispersal of bacterial pathogens from the nasal passages to the middle ear is implicated in COME. We sought to determine whether there is an association between nasal microbial composition and COME in children.

A case-control study of children aged 3 and 4 years was conducted. Cases undergoing placement of tympanostomy tubes for COME were compared to healthy controls. Nasal swabs were collected and a questionnaire was administered. The V1-3 region of the 16S rRNA gene was amplified, and sequenced on the Illumina MiSeq.

73 children with COME had a lower Shannon diversity index than 105 healthy controls (1.62 [.80] versus 1.88 [.84], respectively; P = .046). The nasal microbiota of cases and controls differed in composition using Bray-Curtis dissimilarity (p = 0.002). Children with COME had a higher abundance of otopathogens and lower abundance of commensals including alpha haemolytic Streptococci and Lactococcus . Cluster analysis revealed 4 distinct nasal microbial profiles. Profiles that were Corynebacterium -dominated (aOR 4.18 [95%CI, 1.68–10.39], Streptococcus -dominated (aOR 3.12 [95%CI, 1.08–9.06], or Moraxella -dominated (aOR 4.70 [95%CI, 1.73–12.80] were associated with COME, compared to a more mixed microbial profile when controlling for age, ethnicity, and recent antibiotics use.

Conclusions

Children with COME have a less diverse nasal microbial composition with a higher abundance of pathogens, compared to healthy children who have a more mixed bacterial profile with a higher abundance of commensals. Further research is required to determine how nasal microbiota may relate to the pathogenesis or maintenance of COME, and whether modification of the nasal microbiota can prevent or treat children at risk of COME.

Citation: Walker RE, Walker CG, Camargo CA Jr, Bartley J, Flint D, Thompson JMD, et al. (2019) Nasal microbial composition and chronic otitis media with effusion: A case-control study. PLoS ONE 14(2): e0212473. https://doi.org/10.1371/journal.pone.0212473

Editor: Brenda A. Wilson, University of Illinois at Urbana-Champaign, UNITED STATES

Received: August 29, 2018; Accepted: February 4, 2019; Published: February 22, 2019

Copyright: © 2019 Walker et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: The dataset is available in the SRA repository https://www.ncbi.nlm.nih.gov/bioproject/PRJNA414455/ .

Funding: This work was supported by: REW -The Oticon Foundation (Grant no. 3701863) http://www.oticon.org.nz/ ; REW -CRC Starship Foundation (Grant No. 18071300) https://www.starship.org.nz/ ; REW -Brian Johns Fellowship Trust (Grant no. 4711); EAM -Deafness Research Foundation (Grant no. 2013/08) https://www.nfd.org.nz/ . The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Chronic otitis media with effusion (COME) is diagnosed when fluid gathers behind the tympanic membrane for three months or longer [ 1 ]. The hearing loss associated with COME may impact language acquisition, and increase the risk of learning delays and behavioural problems [ 2 ].

COME has historically been regarded as a sterile inflammatory condition, as pathogens were seldom cultured from effusion in the middle ear (ME). However, with the advent of culture-independent methods, otopathogens have been found in COME as often as in the closely-related condition acute otitis media (AOM) [ 3 , 4 ]. This discrepancy in findings may be explained by bacteria that are less likely to be detected by culture because they are residing in a biofilm state [ 5 ]. The key otopathogens are non-typeable Haemophilus influenzae , Streptococcus pneumoniae , Moraxella catarrhalis , and to a lesser extent Staphylococcus aureus [ 3 ].

While pathogenic bacterial biofilms residing in the ME may be involved in the maintenance of chronic effusion [ 6 ], it is unknown whether the nasal microbiota are also involved. The composition of both commensals and potential pathogens in the nasal microbiota may affect the risk of pathogens spreading to the ME. Commensal bacteria provide resistance against pathogen overgrowth by competing for nutrients and epithelial cell binding sites, producing antimicrobials, disrupting bacterial biofilms, and inducing the host’s immune system [ 7 , 8 ].

Low bacterial diversity in a niche is often a marker of disease [ 9 ] and is associated with AOM [ 10 ]. Higher abundances of Haemophilus , Moraxella , and Neisseria in the nose have also been found to be associated with AOM [ 11 ]. Conversely, lower abundances of Staphylococcus , Corynebacterium , Propionibacterium , Streptococcus (usually not S . pneumoniae ) and Lactococcus have been found in children with AOM [ 10 , 11 ].

There are no published data on associations between nasal microbiota compositions and COME using cluster analysis. Nasal microbiota compositions characterized by Moraxella , Streptococcus , or Haemophilus have been reported to be associated with upper respiratory infection (URI) [ 12 ] asthma [ 13 ], AOM [ 12 ], pneumonia, or bronchiolitis [ 14 , 15 ]. Protective compositions may also be emerging, with those dominated by Staphylococcus , Sphingobium , Corynebacterium , or Dolosigranulum associated with reduced risk of AOM [ 12 ] and asthma [ 16 ].

We investigated whether nasal microbial composition is associated with COME. Commensal bacteria in the nasal passages may protect against otopathogen overgrowth, or ongoing otopathogen overgrowth in the nasal passages may maintain persistence of effusion in the ME. We hypothesized that COME would be associated with a less diverse nasal microbiome; higher relative abundance of the otopathogens H . influenzae , S . pneumoniae , and M . catarrhalis ; and lower relative abundance of the commensals S . epidermidis , Corynebacterium , Propionibacterium , Dolosigranulum , Lactococcus , Lactobacillus , and the alpha haemolytic Streptococci (AHS) spp.

Study design and setting

As previously reported, a case-control study of children aged 3 and 4 years was conducted in Auckland, New Zealand, to compare children with COME to healthy children [ 17 ]. Briefly, recruitment and data collection were conducted between May 2012 and November 2013. Cases were referred for tympanostomy tube placement (TTP), and had a recent medical history of COME and/or signs of COME confirmed by an otorhinolaryngologist during surgery. Controls were selected at random from children enrolled in primary care practices that had referred children for TTP in the previous year. Controls had no medical history of TTP, no episodes of otitis media with effusion (OME) lasting longer than one month in the past year, and never had OME lasting longer than three months. Cases and controls were excluded if they had craniofacial abnormalities or immunodeficiency.

The parent or legal guardian was informed about the study and provided written consent. The study was approved by the Northern X Regional Ethics Committee (reference NTX/11/EXP/027)

Specimen collection

A sterile paediatric FLOQ swab (Copan, California, USA) moistened with sterile saline was inserted into subjects’ anterior nares. The swab was rotated in each nostril three times and placed into a 2ml tube of sterile STGG medium (skim milk, oxoid tryptone soya broth, glucose, and glycerol). Samples were stored at -80°C.

DNA extraction, PCR, library preparation, sequencing, and bioinformatics

DNA was extracted from nasal samples and negative controls using the Qiagen Allprep kit (Qiagen, California, USA). We had 3 negative controls consisting of STGG broth and a swab exposed to the air, STGG broth only, and reagents only. The 16S ribosomal gene was PCR amplified using primers 27F and 534R to target the V1-3 region. Sequencing libraries were generated using the Nextera XT Index kit (Illumina Inc., San Diego. CA, USA) and amplicons sequenced on the Illumina MiSeq. USEARCH 64 (version 7) analysis pipeline was used. For operational taxonomic unit (OTU) assignment the UPARSE algorithm [ 18 ] was followed using a de novo picking approach with OTUs assignment clustered at 97% sequence similarity. Full details of the sample preparation, sequencing and nasal microbiota analysis are provided in Appendix A in S1 File .

Statistical analysis was carried out in R version 3.3.3 ( www.r-project.org/ ) using the Phyloseq [ 19 ], vegan [ 20 ], DESeq2 [ 21 ], and cluster packages [ 22 ].

Downstream analysis

OTUs were filtered to remove contaminants (see Appendix A in S1 File ). OTUs with a total read number less than .005% of total reads and samples containing less than 1000 reads were removed. Additional species-level identification was achieved by aligning representative sequences using the Basic Local Alignment Search Tool (BLAST). Due to the limitations of classification using the 16S rRNA gene, these species identifications are not definitive.

Subject characteristics

Statistical analysis was conducted using JMP 13, SAS Institute Inc., Cary, NC, 1989–2016. Categorical variables were analyzed using a chi-squared test and continuous variables were analyzed using a Student t-test. A P < .05 was considered statistically significant.

Diversity analysis

Alpha diversity was calculated with absolute numbers using the Shannon diversity index in the R vegan package. Beta diversity was assessed with the Bray-Curtis dissimilarity measure. Permutation multivariate analysis of variance (PERMANOVA) using distance matrices was used to assess differences and significance was tested using ADONIS.

Differential abundance

DESeq2 package from R was used for differential abundance analysis with Benjamini-Hochberg adjustment to control for multiple testing. We adjusted for age, ethnicity and antibiotic usage in the past month. A two-tailed P < .05 was considered statistically significant.

OTU presence

For OTUs that were differentially abundant, presence of any reads was compared between cases and controls in JMP 13 using a Chi-square test with Benjamini-Hochberg adjustment, and a two-tailed P < .05 test for statistical significance.

Cluster profiling

OTUs were collapsed at the genus level. To assess nasal microbiota profiles, we partitioned using a medoid clustering approach (PAM) and the Bray-Curtis dissimilarity metric. Number of clusters was selected using the gap statistic [ 23 ]. Using JMP 13, cluster was entered into a multivariable logistic regression model along with age, ethnicity, and antibiotics in the last month, which were identified as potential confounding variables. A two-tailed P < .05 test was considered statistically significant.

Study population

Of 190 subjects who provided nasal samples, 12 were excluded due to having fewer than 1000 reads in total. The subjects whose samples were included did not differ from those whose samples were excluded, in terms of the subject characteristics listed in S1 Table .

As shown in Table 1 , the mean age of the cases was younger than controls, there were more children of Asian ethnicity in the control group than in the case group, and the cases were younger than the controls when they were first given antibiotics. There was no difference between cases and controls for sex, season seen, method of delivery, being fully vaccinated, antibiotic exposure in the last month, attendance at daycare, or having older siblings.

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https://doi.org/10.1371/journal.pone.0212473.t001

Microbiota analysis

A total of 3,606,750 sequences were assembled from pair-end reads across all samples. After filtering and chimera removal, 3,428,213 sequences were assembled into 300 OTUs. The median number of sequences per sample was 21,255 in cases (range 1,011–80,297) and 9,562 in controls (range 1,100–82,013).

OTU9 was classified in Greengenes as Alloiococcus , however the representative sequence matched Dolosigranulum pigrum in BLAST. This is a known misclassification in the Greengenes database. The representative sequence for OTU1 matched Corynebacterium pseudodiptheriticum using BLAST. OTU1 made up 97% of all reads of genus Corynebacterium .

Core microbiome

The core nasal microbiome, defined as those OTUs present in over 80% of all samples, consisted of 16 taxa including Corynebacterium , Moraxella , Streptococcus , unknown Bacilli ( Staphylococcus ), Alloiococcus/Dolosigranulum pigrum , and Neisseria ; see S2 Table .

Shannon diversity index was lower in children with COME than in healthy controls (mean = 1.62 [.80] versus mean = 1.88 [.84] respectively; P = .046); see Fig 1 . Shannon diversity index was also measured using only subjects with the most frequently observed ethnicity (European) due to the strong inverse correlation between COME and Asian ethnicity. In this sensitivity analysis Shannon diversity was also lower in children with COME than in the healthy controls; see Appendix B in S1 File . We also found a significant difference in the microbial composition of children with COME and healthy controls (Bray-Curtis dissimilarity, unadjusted R2 = 0.02, P < .002); see S1 Fig .

Diversity calculated using absolute abundance. Controls have higher alpha diversity than cases ( P < .046).

https://doi.org/10.1371/journal.pone.0212473.g001

OTUs that were more common in children with COME were OTU3 ( Streptococcus) , OTU4 ( Moraxella) , and OTU6 ( H . influenzae) ( Fig 2 ). Examining their representative sequences on BLAST, OTU3 matched S . pneumoniae ( but also S . mitis at 99%), and OTU4 matched M . catarrhalis ( but also M . caprae at 99%).

Calculated using R package DESeq2. Log2 fold change from 105 healthy controls to 73 children with chronic otitis media with effusion, controlling for age, ethnicity and recent antibiotic usage.

https://doi.org/10.1371/journal.pone.0212473.g002

All three OTUs that had greater abundance in the cases were also found to be present in a majority of the control samples (see S3 Table ). OTU6 ( H . influenzae) was found in 68% of the cases and 52% of the controls, OTU3 ( Streptococcus ) was found in 99% of the cases and 100% of the controls and OTU4 ( Moraxella ) was found in 92% of the cases and 85% of the controls. No significant differences were observed between detection of these OTUs in cases compared to controls.

Taxa more common in the healthy controls were three Streptococcus OTUs of uncertain species, Streptococcus infantis , Propionibacterium acnes , Lactococcus sp., Neisseria sp., Lautropa sp., Capnocytophaga sp., and two Oxalobacteraceae OTUs.

Cluster profiles

Nasal microbiota clustered into 4 distinct profiles consisting of a Corynebacterium -dominated cluster (40% of case subjects were in this cluster, and 27% of control subjects), S treptococcus -dominated cluster (cases: 19%, controls: 15%), Moraxella -dominated cluster (cases: 27%, controls: 19%), and a mixed profile cluster (cases: 14%, controls: 39%); see Fig 3 . Cluster was not associated with age, ethnicity, or antibiotics in the last month in univariable analyses. In an unadjusted analysis, Corynebacterium -dominated (OR 4.25 [95%CI, 1.84–10.47]), Streptococcus -dominated (OR 3.59 [95%CI, 1.34–9.98]), and Moraxella -dominated (OR 4.10 [95%CI, 1.64–10.72]) profiles were associated with COME, compared to the more mixed microbial profile. When controlling for potential confounders (age, ethnicity, and antibiotics in the last month), the Corynebacterium -dominated (aOR 4.18 [95%CI, 1.68–10.39], Streptococcus -dominated (aOR 3.12 [95%CI, 1.08–9.06]), and Moraxella -dominated (aOR 4.70 [95%CI, 1.73–12.80]) profiles remained associated with COME compared to the mixed profile.

Profiles were partitioned using a medoid clustering approach (PAM) and the Bray-Curtis dissimilarity metric, based on absolute abundance. Four cluster profiles are indicated: Corynebacterium -dominated profile with prominent Moraxella and Streptococcus (1), Streptococcus -dominated profile (2), mixed profile (3), and Moraxella -dominated profile (4). A heatmap of the 25 most abundant genera is displayed adjacent.

https://doi.org/10.1371/journal.pone.0212473.g003

Our findings that the nasal microbiota of children with COME had lower diversity, higher relative abundance of otopathogens, and a lower relative abundance of commensal bacteria–compared with healthy controls–indicates that the nasal microbiota may be important in initiating or maintaining COME.

Nasal and nasopharyngeal diversity have not previously been examined in OME or COME. Two studies have found low diversity to be associated with AOM [ 10 , 24 ], two have found no association [ 11 , 12 ], and one found that children with AOM had higher diversity [ 25 ]. The association observed between COME and low nasal diversity may reflect well-balanced microbiota exhibiting a higher resilience to infection, however the causal direction of such relationships has not been fully established [ 9 ]. It could equally signify that a bacterial infection that led to COME has also caused an overgrowth of pathogenic bacteria in the nose, which would result in lower alpha diversity by reducing the evenness of bacterial abundance.

A high load of pathogenic bacteria in the nasal passages may increase the risk of movement of those bacteria up the ET to the ME. S . pneumoniae , non-typeable H . influenzae and M . catarrhalis are the three main bacterial pathogens that have been identified in relation to COME [ 26 ], and are commonly detected in the ME effusion of children with COME [ 3 ]. Specific strains of these otopathogens are shared between the nasopharynx and the ME in individuals [ 27 ]. In some animal models, injection of bacteria into the nose results in ME carriage of those bacteria. [ 28 ] Polymicrobial infection further increases the risk of spread to the ME, as shown by nasal challenges using co-infection with multiple bacteria or respiratory viruses [ 29 , 30 ].

We found that children with COME had higher nasal levels of H . influenzae , a Streptococcus OTU matching S . pneumoniae (and S . mitis ), and a Moraxella OTU resembling M . catarrhalis (and M . caprae ). Haemophilus has been found to be differentially abundant in children with recurrent AOM [ 25 ]. This correlation may reflect overgrowth of these pathogens initiating or maintaining COME by spreading to the ME. Although these three OTUs had higher differential abundance in the cases than the controls, they were all present in more than half of the controls. These OTUs may therefore be endogenous pathobionts, common microorganisms of children’s noses that may be disrupted and become infectious due to stimuli such URI [ 9 ]. URI often precedes OM, and can disrupt the airway microbiota. Viruses may promote adherence and virulence of otopathogens [ 31 ] by disrupting the airway epithelial barrier [ 32 ], decreasing mucociliary clearance [ 33 ], inducing the host to supply nutrients to pathogenic bacteria [ 34 ], and provoking biofilms to release virulent dispersed bacteria [ 35 ].

We also found that certain commensal bacteria were more common in controls. These included several AHS spp., a Lactococcus sp., and Propionibacterium acnes . AHS have been reported to help prevent otopathogen infection and OM [ 36 ]. Nasal Lactococcus also has higher relative abundance in healthy children than in children with AOM [ 11 ]. Propionibacteria appear to be protective against S . pneumoniae colonization, URI, and OM, and nasal levels are inversely associated with levels of S . pneumoniae and S . aureus [ 11 , 37 , 38 ].

We report the first cluster analysis of nasal bacterial profile in any OM-related condition. Our observation that a mixed nasal profile was inversely associated with COME compared with profiles dominated by Corynebacterium , S treptococcus , or Moraxella has not previously been reported in relation to OM. This finding may indicate that a more mixed profile is protective against infection. Adult profiles tend to be more mixed, more stable, and more resistant to infection that those of children [ 39 ].

The association between COME and a profile dominated by Corynebacterium was unexpected, as this genus has previously been inversely associated with otitis media [ 25 ]. Nearly all reads of Corynebacterium belonged to an OTU classified in BLAST as Corynebacterium pseudodiptheriticum . This species is an opportunistic pathogen [ 40 , 41 ]. However, it was not differentially abundant in our cases. The association may therefore be due to a higher abundance of S treptococcus and Moraxella in the Corynebacterium -dominated cluster than in the mixed cluster, rather than a direct association with Corynebacterium pseudodiptheriticum itself.

Randomized controlled trials of probiotics have demonstrated that bacterial interference can be successful in reducing nasal colonization with otopathogens to treat URIs and OM in children [ 42 ], although not all trials show a protective effect for every condition [ 43 ]. Such studies support the plausibility of certain microbial compositions, such as the mixed bacterial profile that we observed, helping to protect against disease.

The study has potential limitations. Cases and controls differed by ethnicity, however similar results were found in a sensitivity analysis that examined all major findings in the largest single ethnicity, and when including ethnicity in a multivariable analysis. Limitations of 16S rRNA gene sequencing are that it is unable to distinguish between live and dead microbial DNA, and is poorly suited to distinguishing between many bacteria below the genus level, including genera that include both respiratory pathogens and commensals. We did identify the key otopathogen H . influenzae using 16S rRNA sequencing, however future research using whole genome sequencing would enable more precise differentiation between pathogen and commensal species and strains. We did not include analysis of the virome which may have provided additional clarification. Finally, this case-control study could not investigate the causal direction of the association between COME and nasal bacterial composition, therefore we recommend future longitudinal studies.

The spread of pathogenic bacteria from the nasal passages to the ME may be involved in the pathogenesis of COME. Children with COME had a different nasal microbial profile to healthy controls, with lower diversity, higher abundance of pathogens, and lower abundance of commensals. Pathogens were equally likely to be present in the noses of healthy controls as in children with COME, and may therefore be endogenous pathobionts. Higher abundance of these pathobionts may increase the risk of COME, or help to maintain effusion once established. More research is required to determine the order of events leading to COME. If a more diverse and mixed nasal bacterial composition dominated by commensals proves to be protective against the spread of bacteria to the ME, this may present new opportunities to prevent or treat COME by influencing the microbiota of the nasal passages.

Supporting information

Appendix A. Detailed Methods and Appendix B. Detailed Results.

https://doi.org/10.1371/journal.pone.0212473.s001

S1 Table. Comparison of characteristics of participants whose nasal samples were included in the analysis with those that had unusable samples, with Benjamini-Hochberg adjustment.

https://doi.org/10.1371/journal.pone.0212473.s002

S2 Table. The core microbiome of 73 children with chronic otitis media with effusion and 105 healthy controls.

https://doi.org/10.1371/journal.pone.0212473.s003

S3 Table. Presence of differentially abundant operational taxonomic units in 73 samples with chronic otitis media with effusion and 105 healthy controls, with Benjamini-Hochberg adjustment.

https://doi.org/10.1371/journal.pone.0212473.s004

S1 Fig. Non-metric multidimensional scaling (NMDS) ordination plot of Bray–Curtis community dissimilarities of OTUs for children with chronic otitis media with effusion and healthy controls, with variance stabilizing transformation to correct for difference in sequencing depth.

https://doi.org/10.1371/journal.pone.0212473.s005

Acknowledgments

We would like to thank Ann Paddy, DHSc, who administered the questionnaires and performed part of the physical examinations for the children involved in the study. Dr. Rinki Murphy reviewed the manuscript and provided statistical advice. We would like to acknowledge the staff at Waitakere and North Shore Hospital, Bede Saldanha and Denise Burdett for going above and beyond reception support, and especially ear nurse specialist Barbara Middleton. Finally, a thank you to the families and their general practitioners whose help and support made the study possible.

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Intratympanic steroid treatment in otitis media with effusion resistant to conventional therapy in children, hossam eldin mohammed abdelazeem, khaled elhusseiny mohammed khdr, mohammed goda elnems.

Background : Children's hearing impairment is primarily caused by otitis media with effusion (OME). OME may be linked to  developmental delays, thus early and appropriate therapy of OME avoids hearing and speech impairment in children. Treatment is still a contentious topic, though.

Objectives : We aimed to assess the efficacy of Intratympanic (IT) steroids for the management of OME resistant to traditional medical  Therapy.

Patients and methods : The study was conducted on 40 patients who had complaints of hearing loss and bilateral OME that resisted  medical treatment lasting at least three months. Under general anesthesia, we performed myringotomy and ventilation tube (VT) was  inserted bilaterally on each patient Then we injected steroid (.5 ml methylprednisolone 40 mg/mL) into the right middle ear. During the  operation and in follow-up visits, once a week for three weeks in a row.

Results : Resolved OME was 32 (80%) ears with ventilation tube  (VT) alone and 38 (95%) ears with ventilation tube (VT) and steroid injection. This difference was significant (p = 0.043). As regard  postoperative complication, tympanosclerosis was noted in 6 (15%) non-injected ears and one injected ear (2.5%) and the difference was statistically significant (p<0.05). Also, permanent perforation occurred in two (5%) non-injected ears and one (2.5%) injected ears, with  statistically non-significant difference (p =1.000). While Otorrhea occurred in 4 (10%) non-injected ears and 5 (12.5%) injected ears, with  statistically non-significant difference (p =1.000).

Conclusion : IT steroid injections have been shown to be effective in treating OME  resistant to pharmaceutical and surgical interventions, with a little risk of recurrence and surgical side effects. The best well-known  therapeutic method combines IT steroid injection with ventilation tubes. 

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Journal Identifiers

Determinants of chronic otitis media with effusion in preschool children: a case-control study

Affiliations.

• 1 Department of Paediatrics: Child and Youth Health, The University of Auckland, Private Bag 92019, Auckland, 1142, New Zealand. [email protected].
• 2 Division of Otolaryngology-Head and Neck Surgery, Counties-Manukau District Health Board, Manukau SuperClinic™, PO Box 98743, Manukau City, Auckland, 2241, New Zealand.
• 3 Department of Paediatrics: Child and Youth Health, The University of Auckland, Private Bag 92019, Auckland, 1142, New Zealand.
• PMID: 28056905
• PMCID: PMC5217332
• DOI: 10.1186/s12887-016-0767-7

Background: Chronic otitis media with effusion (COME) is a prevalent upper airway infection resulting in hearing loss. The aim of this research was to determine risk factors for COME in preschool children.

Methods: A case-control design was conducted in Auckland, New Zealand from May 2011 until November 2013. The cases were children aged 3 and 4 years referred for tympanostomy tube placement due to a diagnosis of COME (n = 178). The controls were a random sample of healthy children aged 3 and 4 years from primary care practices (n = 209). The children's guardians completed an interviewer-administered questionnaire that covered topics including socio-demographic information, pregnancy and birth, infant feeding practices, home environment, and respiratory health. In addition, skin prick tests for atopy were performed. Odds ratios (OR) estimating the risk of COME independently associated with the exposures were calculated using a logistic regression model.

Results: Children with COME frequently had nasal obstruction (OR: 4.38 [95% CI: 2.37-8.28]), always snored (OR: 3.64 [95% CI: 1.51-9.15]) or often snored (OR: 2.45 [95% CI: 1.04-5.96]), spent more hours per week in daycare (OR per hour/week: 1.03 [95% CI: 1.00-1.05]), had frequent colds (OR: 2.67 [95% CI: 1.59-4.53]), had siblings who had undergone tympanostomy tube placement (OR: 2.68 [95% CI: 1.22-6.02]), underwent long labour (OR: 2.59 [95% CI: 1.03-6.79]), and had early introduction of cow's milk (OR: 1.76 [95% CI: 1.05-2.97]). Asian ethnicity (OR: 0.20 [95% CI: 0.07-0.53]) and having older siblings (OR: 0.54 [95% CI: 0.31-0.93]) were inversely associated with COME.

Conclusion: COME in preschool children was associated with pathogen exposure, respiratory infection, and nasal obstruction. Strategies to prevent pathogen transmission warrant investigation. The novel findings of long labour and early cow's milk introduction require replication in future studies.

Keywords: Biofilms; Cow’s milk; Long labour; Nasal obstruction; Otitis media with effusion; Risk factors; Snoring; Upper respiratory tract infections.

Publication types

• Research Support, Non-U.S. Gov't
• Case-Control Studies
• Child, Preschool
• Logistic Models
• New Zealand / epidemiology
• Otitis Media with Effusion / ethnology
• Otitis Media with Effusion / etiology*
• Retrospective Studies
• Risk Factors