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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 20  |  Issue : 1  |  Page : 113-120

Role of food allergy in otitis media with effusion


1 Department of Medicine & Surgery, Faculty of Medicine, Alexandria University, Kafr El Shiekh, Egypt
2 Department of Otorhinolaryngology, Faculty of Medicine for Girls, Al Azhar University, Cairo, Egypt

Date of Submission26-Aug-2021
Date of Decision26-Oct-2021
Date of Acceptance30-Oct-2021
Date of Web Publication4-Mar-2022

Correspondence Address:
BSc Wessam A Fouad
Department of Medicine & Surgery, Faculty of Medicine, Alexandria University, Kafr El Shiekh, 11517
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/azmj.azmj_99_21

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  Abstract 


Background and aim The role of food allergy (FA) in chronic otitis media with effusion (OME) is argumentative. New proof from cellular biology and immunology clarifies the essentials of allergic responses and permits exact diagnosis more than before for allergies and inflammatory disease. We aimed to detect the occurrence of FA in patients with chronic OME.
Patients and methods This a prospective, cohort randomized controlled study that was conducted at Al Azhar University Hospital, Otorhinolaryngology Department, on 40 patients divided into two groups: patient group included 20 patients with OME, and control group included 20 patients without any medical problems about FA or OME. The prevalence of FA was detected by skin prick test and assessment of serum immunoglobulin E and eosinophil count.
Results There were highly statistically significant correlations between increase in the total serum immunoglobulin E and eosinophil count and developing OME (P<0.00); however, there were no statistically significant correlations between age and developing OME (P<0.396).
Conclusion The possibility of association and the contribution of FA should be kept in mind in OME cases.

Keywords: food allergy, otitis media with effusion, serum immunoglobulin E, skin prick test


How to cite this article:
Fouad WA, Makhemaer SM, Mohamed HE, Awwad AA. Role of food allergy in otitis media with effusion. Al-Azhar Assiut Med J 2022;20:113-20

How to cite this URL:
Fouad WA, Makhemaer SM, Mohamed HE, Awwad AA. Role of food allergy in otitis media with effusion. Al-Azhar Assiut Med J [serial online] 2022 [cited 2022 Jun 29];20:113-20. Available from: http://www.azmj.eg.net/text.asp?2022/20/1/113/339083




  Introduction Top


Otitis media with effusion (OME) is a widespread chronic childhood inflammatory disorder [1]. Conductive hearing losses caused by OME can potentially affect speech and language development [2]. The disorder is diagnosed by tympanometric abnormalities [3]. The causal contributors to OME are still controversial. Patients with OME have an increased prevalence of atopy including asthma, eczema, and food allergy (FA) [1],[3].

FA is an unusual response toward food allergens by the immune response [4]. The most frequently detected foods causing allergies in children are cow’s milk, eggs, peanuts, fish, wheat, walnuts, soybeans, and shellfish. However, children with immunoglobulin E (IgE)-nondependent FA improve within 3 years in 80% of cases [5]. Diagnosis of patients with FA was based on patient history, skin prick test, specific serum IgE, food diet elimination, and subsequent oral food challenges [6]. The oral food challenge is an important test for the diagnosis of FA [7].

In allergic individuals, on subsequent exposure to the allergenic food, stimulation of mast cell and basophil leads to discharge of mediators, leukotrienes, and cytokines, which contribute toward allergic reactions [8].

Tanaka et al. [9], confirmed the role of IgE-mediated hypersensitivity in the occurrence of OME among patients with allergic rhinitis. OME and allergic rhinitis due to food allergy typically caused by typically caused by dairy products, can usually develop in children 2 years of age [10].

A role for FA in chronic OME is controversial. In some infants, OME resulting from having IgG, having IgG complexes with antigens to food, especially proteins of cow milk, may develop OME [11]. We aimed in this study to find the occurrence of FA in patients with chronic OME.


  Patients and methods Top


Ethical consideration

Approval of this study was obtained from the ethical committee of the Faculty of Medicine of Al Azhar University (approval number: 202108955). Written consent was obtained from children’s parents before study.

Study design

This was a prospective, cohort randomized controlled study.

Site of study

This study was conducted at the otorhinolaryngology Department of Al-Zahraa Hospital, Al Azhar University, Egypt.

Patients

The study was performed on 40 patients who were recruited by convenient random sampling and were divided into two different groups: (a) patient group included 20 children with OME, comprising 12 (60.0%) males and eight (40.0%) females. Their age ranged from 4 to 10 years, with a mean age of 7.65±2.368 years. (b) The control group included 20 children without any medical problems concerning FA or OME, comprising 13 (65.0%) males and seven (35.0%) females. Their age ranged from 4 to 12 years, with a mean age of 7.15±1.089 years. All patients were evaluated by full history, otolaryngologic examinations, tympanometry, FA by means of skin prick testing, specific IgE tests, blood eosinophil counts, and food challenge test. Patients with perforated ear drums, patients with oral immunotherapy to any type of FA, and patients treated for allergy were excluded from the study.


  Methods Top


Workup

  1. Full history taking and clinical examination were done for symptoms and signs of OME, allergy, adenoid hypertrophy, previous VT insertion, adenoidectomy, and nasal or sinus surgery.
  2. Tympanometry (for all) was done using an ICLEAR tympanometer CHR-MI100 Guangdong, China, and audiometry (for 10 patients aged 9 years old) was done using a Madsen 2 channel pure tone and speech audiometer model OB822 (GN Otometrics Company, Bloomington, USA; Minnesota, Hennepin) [12],[13].
  3. Blood sampling:
    1. Intravenous blood was collected from patients and centrifuged at 2500 rpm for 10 min.
    2. Serum samples were kept at −19°C until examination.
    3. Total IgE was confirmed in serum samples in duplicate with a commercially existing enzyme-linked immunoassay kit.
    4. Eosinophils were valued on the smears prepared from 1 cc of the patients’ blood samples, transmitted to oxalate, and stained with eosin by Romanowsky stain.
  4. Radiological examination: plain radiograph in nasopharynx lateral view with mouth opened was done to check the adenoid size.
  5. Skin prick test: the test site is first cleaned and disinfected. The forearm is then marked using a water-soluble skin marker. Histamine and normal saline serve as positive and negative controls, respectively. Allergen extracts from some types of food such as milk, eggs, fish, shellfish, nuts, peanuts, wheat, and soybeans were applied on the inner forearm. A drop of each allergen is then placed corresponding to a number on the grid. Then a sterile needle (lancet) is used to prick in the middle of each drop of allergen using light pressure [14].


Skin prick testing results [15].



According to the results, patients were separated into two groups.

Group 1: patients negative for FA by both skin prick test and specific-IgE in the patient’s serum. They were observed without treatment for 2 months with follow-up with clinical assessment and tympanometry at 4-week and 8-week intervals.

Group 2: patients positive for FA by either or both of skin prick test and specific-IgE in the patient’s serum. The patients proved to be allergic to certain types of food were subjected to elimination of this food item for 2 months and then followed up with clinical assessment and tympanometry at 4-week and 8-week intervals. Another blood sample is taken (clotted) for measuring specific IgE after elimination. The patients were challenged to the same food item to which they proved to be allergic for, followed by clinical and tympanometric follow-up after 4 weeks to detect deterioration or to recollection of effusion fluid clinically and by tympanometry.

Sample size

It was calculated by a Rao-soft sample calculator, using a 5% margin of error, confidence level of 95%, response distribution of 80%, and according to flow at the hospital. They were chosen by a systemic random sample technique.

Statistical analysis

IBM’s SPSS statistics (Statistical Package for the Social Sciences) for Windows (version 25, 2017) (IBM Corp. Released 2017. IBM SPSS Statistics for windows,version 25.0. Armonk, NY: IBM Corp.) was used. Shapiro–Wilk test was operated to assess the normality of the data distribution.

All tests were accomplished with 95% confidence interval. P value less than 0.05 was reflected statistically significant. Charts were created using SPSS chart builder and Microsoft Excel for Windows 2019.


  Results Top


Regarding demographic characteristics of the 40 children enrolled in this study, there were no statistically significant differences between the two groups for age and sex (P=0.396 and 0.744, respectively). This is shown in [Table 1].
Table 1 Demographic characteristics of both groups

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On comparing the two groups, there were no statistically significant differences regarding history of allergy or family history for allergy (P=0.548 and 0.311, respectively). However, there was a statistically significant difference between both groups regarding history of adenoidectomy and history of tonsillectomy (P=0.072, 0.072, and 0.035, respectively). The data are summarized in [Table 2].
Table 2 History of allergy, ventilation tubes, adenoidectomy, and tonsillectomy in both groups

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On comparing IgE and eosinophil count of both groups, there were highly statistically significant differences (P≤0.001), as shown in [Table 3].
Table 3 Total serum immunoglobulin E and eosinophil count in the studied groups

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On comparing FA in both groups, there were highly statistically significant differences (P≤0.001). The prevalence of FA in the studied groups is summarized in [Table 4].
Table 4 Occurrence of food allergy in the studied groups

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There was a highly statistically significant correlation total serum IgE and eosinophil count and developing OME (P<0.00); however, there were no statistically significant correlation between age and developing OME (P<0.396), as shown in [Table 5].
Table 5 Correlation between age, total serum immunoglobulin E, and eosinophil count with developing otitis media with effusion

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OME occurred two times more in patients with history of allergy (odds ratio=2). [Table 6] shows the odds ratio regarding sex, history of allergy, family history of allergy, history of ventilation tube, history of adenoidectomy, and history of tonsillectomy.
Table 6 Odds ratio of developing otitis media with effusion with effusion in the presence of food allergy

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OME occurred five times more in patients with FA. Nuts, shellfish, and peanuts recorded higher odds ratios (4.00, 3.500, and 3.00) respectively. [Table 7] shows the odds ratio in presence of FA.
Table 7 Odds ratio of developing otitis media with effusion with effusion in the presence of food allergy

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Comparison between before and 1 month after elimination of allergen from diet in the patient group with FA showed a highly statistically significant improvement of total serum IgE (P<0.001) and tympanometry (P<0.014), as shown in [Table 8].
Table 8 Immunoglobulin E and presence of effusion fluid 1 month after elimination of allergen from diet in the study group

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On comparing total serum IgE and presence of effusion 1 month after food challenge test, we found a highly statistically significant recurrence of elevation of total serum IgE (P<0.001) and OME (P<0.014), as shown in [Table 9].
Table 9 Immunoglobulin E and presence of effusion fluid 1 month after food challenge test in the study group

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  Discussion Top


OME is a usual disorder, with an estimated prevalence of 10−17% from 2 to 4 years and 3−4% from 6 to 8 years. By the age of 4 years, 90% of children are estimated to have experienced OME at least once [16].

FA is a type of adverse food reaction that refers to immunologically mediated reactions [17],[18].

Multiple studies hypothesized that the middle ear itself can be a target organ of allergic disease and that other mechanisms are relevant in OME pathogenesis besides local and mechanical processes [16],[19],[20]. Allergic mediators such as IgE, activated mast cells, tryptase, or myeloperoxidase have been noticed and analyzed in the middle ear of patients with OME [20]. Other studies investigated not only middle ear secretions but also mucosal levels of the same allergic inflammation markers, also considering additional parameters such as eosinophil counts, Th2-type cytokines, and their messenger RNA [16],[21].

The allergic process may also induce delivery of inflammatory mediators to middle ear microcirculation, besides local changes in blood flow and gas exchange. It has hence been suggested that immune complexes involving food allergens, especially with dairy products, may play a relevant role in promoting OME and that it can be a unique mechanism for FA-elicited OME [22].

Despite such pathophysiological research and the theoretical association between OME and FA, literature reporting clinical investigation data is not as comprehensive as expected [16].

This study was conducted at Al Azhar University Hospitals aiming to detect the prevalence of FA in patients with chronic OME. We conducted a study on 40 subjects who were divided into two groups: the patient group included 20 cases diagnosed with otitis media, and the control group included the residual 20 healthy controls.

No significant difference was detected between the two groups concerning age (P=0.396) and sex (P=0.744) ([Table 1]).

Likewise, a recent study by Sharifian et al. [23] and Hardani et al. [20], reported no significant difference between cases and controls regarding the same parameters (P>0.05). Teele [24], also reported no significant relationship between age and the incidence of OM. Both of the previous studies confirmed our findings. Conversely, Walker et al. [25], reported that the mean age of the cases was significantly younger than the controls (P=0.04). This confirmed our findings regarding the higher prevalence of male sex in both groups, together with the absence of any significant difference between the studied groups regarding that parameter. Another study by Wijayanti et al. [26], also negated the presence of any significant difference between cases and controls regarding the same parameter (P>0.05). However, boys have a lower prevalence compared with our study, as they represented 48.8 and 50% of subjects in the two groups, respectively.

Generally, there was no significant difference between cases and controls regarding general characteristics, which should nullify any bias that may have skewed the results in favor of one group than the other one.

In our study, there was no significant difference between the two groups regarding previous history of allergy (P=0.548) ([Table 2]).

It was reported by 10 and 5% of subjects in the cases and control groups, respectively.

Likewise, Wijayanti et al. [26], reported no significant difference between the two groups (P=1). On the contrary, Usonis et al. [27], stated that child care and history of allergy are linked to the incidence of otitis media. Daud & Rahman [28], through their meta-analysis, concluded that family history of allergy did not play a strong role for OME (P=0.5245 with odds ratio=1.13), which confirms our findings.

In our study, no significant difference was detected between cases and controls regarding history of previous adenoidectomy (P=0.072). Family history of allergy did not show any significant difference between cases and controls (P=0.311). Previous tonsillectomy operation showed a significant increase in cases (20%) compared with controls (0%). Statistical analysis revealed a P value of 0.035 ([Table 2]).

In line with our findings, Corey et al. [29], reported that adenoidectomy was performed in 10 (11%) of 89 otitis media cases versus no subjects in the control group (0%), with no significant difference between the two groups (P>0.05). In contrast to previous findings, the study by Juntti et al. [30], reported a significant increase in previous adenoidectomy rates in OM cases compared with controls (41 vs. 23%, respectively; P=0.004).

Regarding IgE levels in our study, it showed a significant elevation in cases compared with controls (P<0.001). The IgE-mediated allergy has long been considered a contributing factor in about one-third of patients with OME based on clinical notes and skin testing [31]. Blood eosinophil count showed a significant elevation in OM cases compared with controls (P<0.001) ([Table 3]).

The current research is in agreement with Passali et al. [32], who found a relation between allergic rhinitis and the development of OME. Hurst [33], postulated that OME is considered frequently to be an IgE-mediated, late-phase allergic disease. The significant incidence of atopy associated with OME has suggested a role of allergy in the pathogenesis of OME.

A study conducted by El-Sharnoby et al. [34], confirmed our findings, as IgE was significantly elevated in OME cases compared with controls (P<0.001). In addition, Gomaa et al. [35], also reported a significant difference between the two groups (P<0.05).

Other authors [36],[37] confirmed the previous findings; however, they did not include a control group. They reported that eosinophil counts in peripheral blood (%) were higher than the normal range in most of the patients (mean=11.4%).

In the current study, there was a significant increase in the prevalence of FA in patients with OM (P<0.001) ([Table 4]).

Pathophysiology of OME in allergic cases is based on many mechanisms: one of them is based on congestion of the nasal mucosa induced by FA, and the other is the damage of mucosal lining of middle ear [28],[31].

In a study by Lecks [38], FA was present in 50% of 82 cases diagnosed with OME. Nsouli et al. [39], described one of the highest FA prevalence rates (∼78%) in a group of 104 children with OME. Döner et al. [40], analyzed a group of 22 patients with recurrent OME after adenoidectomy and ventilation tube placement, where 31.8% were positive for FA. The study by Aydoğan et al. [41], directly focusing on the role of FA in OME showed that 44.6% of 25 patients with OME had FA (as opposed to 18% in the control group).

When it comes to every food type in our study, although allergy to milk showed a slight increase in cases compared with controls (10 vs. 0%, respectively), no significant difference was detected on statistical analysis (P=0.147) ([Table 4]).

On the contrary, Juntti et al. [30], have reported that children with cow’s milk allergy in infancy, even when properly treated, experience recurrent OM. In their study, a higher proportion of children with cow milk allergy, who had acquired respiratory atopy, had recurrent OM (27 vs. 12%, P=0.009).

Our findings revealed no significant difference between cases and controls regarding allergy to eggs (P=1), which was detected in 5% of subjects in both groups ([Table 4]).

Daud and Rahman [28], confirmed our findings, as there was no significant difference between the two groups regarding the same parameter (P=0.244), although it was detected in 4.8% of cases versus no controls.

In the current study, there was no significant difference between cases and controls regarding the presence of peanut allergy (P=0.292). It was reported in 15 and 5% of subjects in cases and control groups, respectively ([Table 4]).

Similarly, Daud and Rahman [28] also negated any significant difference between cases and controls regarding peanut allergy (P>0.95), as it was present in 3.2% of the included subjects in both groups.

In our study, allergy to wheat did not constitute a significant difference between the two groups (P=0.311). It was detected in 5% of cases compared with no controls ([Table 4]).

In agreement with the previous findings, Daud and Rahman [28], reported that wheat allergy was detected with no significant difference between the two groups (P=0.365).

Regarding the remaining tested food materials in the current study (fish, shellfish, nuts, and soybeans), there was no significant difference between cases and controls (P>0.05) ([Table 4]). To the best of our knowledge, there is a paucity of studies handling the role of these specific food materials in the pathogenesis of OME [16],[42]. However, we tested these materials as they were reported among the commonest food types causing FA.

In this study, there were highly statistically significant correlations between total serum IgE and eosinophil count and developing OME (P<0.00). However, there were no statistically significant correlations between age and developing OME (P<0.396) ([Table 5]). OME occurred two times more in patients with history of allergy (odds ratio=2) ([Table 6]). OME occurred five times more in patients with FA. Nuts, shellfish, and peanuts recorded higher odds ratios (4.00, 3.500, and 3.00, respectively) ([Table 6]).In our study, elimination of allergen led to a significant decrease in IgE level (from 274.07 down to 212.4; P<0.001). Moreover, the prevalence of effusion showed a significant decrease from being detected in all cases down to only 60% 1 month after allergen elimination (P=0.014). Re effusion and increase in IgE was detected after food challenge test ([Table 8] and [Table 9]).{Table 8}{Table 9}

The previous findings indicate two facts: the first one is that FA plays a crucial role in the pathogenesis of OME, and second, elimination of the causative allergen and decrease of recurrent exposure will have a significant positive effect on decreasing disease recurrence rates. Therefore, all otorhinolaryngologists should keep FA in mind when evaluating children with OME, identify the causative agent if present, and strictly advise the parents to keep their children away from the incriminating food materials.

In a study conducted by Lecks [38], more than 80% of the included cases diagnosed with OME improved with allergy treatment (inhalant allergen immunotherapy combined with elimination of food allergens). Although not reporting the relative prevalence rates of OME and FA, Viscomi [43], described OME improvement with elimination diet. Ruokonen et al. [44], advocated the role of elimination diets in OME treatment, when in association with FA. A widely cited article by Nsouli et al. [39], included 104 children with OME, who were randomly selected from among patients with OME and valued for FA through skin prick testing, specific IgE testing, and food challenge. The authors showed a significant OME improvement with elimination diet and OME recurrence after subsequent challenge. Bernstein [22], and Lanphear et al. [45], performed many clinical studies to clarify that treatment of allergy improves the condition of otitis media in the cases of OM with evidences of allergy. All of the previous reports confirmed our findings.

Limitations

First of all, it is a single center study. Moreover, the included sample size was relatively small. Hence, more studies including more studies from different ENT centers should be conducted in the near future.

Recommendations

Further studies on more patients, longer follow-up, and multicenter experience are all necessary to accurately figure out the prevalence of FA in patients with chronic OME.


  Conclusion Top


OME and FA are common disorders that may significantly affect patients’ development and well-being. Incidence of FA, in particular, appears to be rising in recent years. The possibility of association and the contribution of FA should be considered in OME cases.

Acknowledgements

The authors express the deepest appreciation for immunology & clinical pathology department at Alzhraa hospital for their support, which facilitated the completion of this work.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]



 

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