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Published in final edited form as: J Allergy Clin Immunol Pract. 2024 Apr 24;12(8):2111–2117. doi: 10.1016/j.jaip.2024.04.032

Food Matrix Composition Affects the Allergenicity of Baked Egg Products

Elise G Liu 1, Joey Tan 1, Julia Shook Munoz 2, Veronika Shabanova 3, Stephanie C Eisenbarth 4, Stephanie Leeds 2,*
PMCID: PMC11580806  NIHMSID: NIHMS1998645  PMID: 38670261

Abstract

Background:

Egg allergy is common and caused by sensitization to ovomucoid and/or ovalbumin. Many egg-allergic patients are able to tolerate eggs baked into other foods, such as muffins. While heating egg extensively reduces allergens, the effect of other food ingredients on allergenicity of eggs, or the “matrix effect,” is less well studied.

Objective:

We aimed to define how food matrices impact the matrix effect in egg allergenicity.

Methods:

ELISA was used to quantify ovalbumin and ovomucoid in extracts from various baked egg products: plain baked egg without a matrix, and muffins baked using either wheat flour, rice flour, or a wheat flour/banana puree mix. Allergen-specific IgE blocking ELISAs were performed using the egg product extracts on egg-allergic patient sera to determine whether the amount of extracted egg protein in each extract correlated with how well the extracts could bind patients’ egg IgE.

Results:

Baking eggs in any muffin matrix led to an increase in the amount of extractable ovalbumin and a decrease in the amount of extractable ovomucoid compared to plain baked egg. Compared to wheat muffins, rice muffins had more extractable ovalbumin and wheat/banana muffins had more extractable ovalbumin and ovomucoid. The egg allergens in the extracts were able to block egg allergic patients’ egg IgE.

Conclusions:

Food matrices affect egg allergen availability. Patients and families should be advised that substitutions in baked egg muffin recipes can affect the amount of egg allergens in foods and potentially affect the risk of food allergic reaction.

Keywords: Matrix effect, egg allergy, ovomucoid, ovalbumin, egg IgE, baked egg, muffin

Introduction

Egg allergy is a common form of food allergy, affecting around 1.3% of children under 5 years of age in the United States (1). Egg allergy is common in young children from other countries as well, with reported prevalence ranging from 1.2–2.7% in European countries (2, 3). Egg allergy is caused by the production of egg-specific immunoglobulin E (IgE), particularly to the main egg allergens ovomucoid (Gal d 1) and ovalbumin (Gal d 2), which are found in the egg white (4). Egg allergy is more common in younger children, as a significant portion of egg-allergic individuals outgrow their allergy by school age (5). Notably, the development of tolerance often happens in a stepwise manner, with an initial tolerance of baked egg followed by an eventual tolerance to minimally cooked egg (6).

Clinical practice has moved towards offering baked egg oral challenges to egg-allergic patients with history and testing suggestive of improved likelihood of tolerance (7). This often correlates with patients who have decreasing egg white IgE serum testing and/or skin prick testing, as well as a waning or absent sensitization to linear epitopes on egg allergen, particularly ovomucoid (8). Consumption of baked egg products seems to accelerate the development of tolerance to egg, and it has been associated with reduced IgE responses to egg allergens (7). The rationale behind initial challenge to baked egg is typically related to denaturation of conformational epitopes of egg allergens, particularly ovalbumin, during the baking process. Prior studies have demonstrated that heating at high temperatures can function to denature these conformational epitopes through thermal processing (9), but it has been postulated that a “matrix effect” may also be a factor in the ability of egg-allergic individuals to introduce baked egg successfully (10).

The matrix effect can be defined as the interplay between proteins, fats, and carbohydrates within a food, and the impact this may have on allergenicity of allergens within that food (10). We previously published a case report of a patient who tolerated baked egg muffins made with wheat flour, but had a systemic reaction requiring epinephrine after ingestion of a baked egg muffin that substituted banana puree for flour (11). While some literature is available, robust research examining the translational impact of the matrix effect on allergenicity in allergic individuals is lacking (12–15). However, there is more literature examining food allergen detection within matrices in vitro. One study found that in additional to thermal processing, cooking allergens within food matrices made it more difficult to detect allergen DNA by polymerase chain reaction amplification, and hypothesized that fat, carbohydrates, and other plant metabolites might be affecting availability of the allergen DNA (16). Other studies have looked at allergen protein detection within matrices through various analytical methods, including enzyme-linked immunosorbent assay (ELISA) kits and mass spectrometry (MS) (17, 18). These studies describe the importance of thermal processing, but also point towards the contribution of matrix composition in the changes in the physical and chemical properties of proteins which may affect detectability.

Considering the available evidence, baked egg challenges are recommended to be performed with egg cooked into a food matrix, most commonly with muffins (19). In particular, a muffin recipe published by Mount Sinai is frequently used to perform these baked egg challenges (6). While the recipe specifies that a certain ratio of egg to wheat flour should be used, real-world considerations such as other food allergies or dietary preferences, may lead to ingredient substitutions in the muffin recipe that can have clinical consequences on allergenicity (11). The present study sought to investigate the matrix effect on egg allergenicity using various baked egg recipes. We aimed to understand the effect of the food matrix on the extractability of major egg allergens in various forms of baked egg, as well as to evaluate IgE reactivity to these baked egg products using egg-allergic patient sera.

Methods

Baked egg product recipes

Four formulations of baked egg were used for this study: plain baked egg, baked egg in a muffin made using the Mount Sinai recipe (6) with wheat flour, or with wheat flour substituted with rice flour or a wheat flour and banana puree mixture. Rice flour was studied as an alternative to wheat flour because it is the most common gluten-free option that is commercially available. Whole eggs were blended to create a homogenized source of egg that was used for all the recipes. These homogenized eggs were weighed on a food scale and divided into equal 100-gram aliquots (equivalent to two large eggs). Baked egg was prepared either with no added ingredients, or when compared side-by-side to muffins, baked egg without matrix was prepared with the addition of water equivalent to the amount of wet ingredients in the muffin recipes to achieve similar cubic volume and minimize differential heating. For the rice matrix muffin, white rice flour was substituted for wheat flour 1:1. For the wheat/banana matrix muffin, half the volume of wheat flour was replaced with an equivalent volume of pureed banana. All baked egg products were cooked at 350°F for 30 minutes. Ingredients were obtained from a local supermarket and cooked in a domestic kitchen by one of the researchers in the study, to best mimic the conditions families would use in preparation for individual oral food challenges. All baked egg products were prepared by the same person in the same kitchen for consistency.

Baked egg product extractions

The total baked weight of each batch of muffins was obtained. Multiple representative wedges of muffin or baked egg weighing 1/50th of the total batch weight, corresponding to the amount of product containing 2 grams of whole egg, were obtained. These slices were then added to 15 mL of phosphate buffered saline (PBS) with 2% Tween and chopped with a razor for 1 minute, to mimic the process of mastication. The resulting suspensions were incubated at 37°C for 30 minutes. The muffin suspensions were then centrifuged at 2800 g for 15 minutes. The resulting aqueous supernatant containing free food allergens was collected from each sample and stored at −20°C for use in future assays.

Quantification of egg allergens

An ovalbumin assay from a previously published protocol was adapted to quantify ovalbumin in muffin and baked egg extracts (20). Briefly, 96-well ELISA plates (Thermo Fisher Scientific) were coated with 1 μg/mL mouse anti-chicken ovalbumin capture antibody (TOSGAA1, BioLegend) in PBS at 4°C overnight. Plates were blocked with 1% bovine serum albumin (BSA) in PBS with 0.05% Tween for 1 hour at 37°C. Muffin, heated ovalbumin (Sigma Aldrich), or heated ovomucoid (Sigma Aldrich) samples were loaded and serially diluted in 1% BSA in PBS/Tween to yield at least 4 biologic replicates. Samples were incubated for 1.5 hours at 37°C. Sample plates were then incubated with 10 μg/mL mouse anti-chicken ovalbumin detection antibody (F2–3.58. Bio X Cell) in 1% BSA in PBS/Tween for 1 hour at 37°C. Plates were then incubated with a 1:5000 dilution of goat anti-mouse IgG1 conjugated to horseradish peroxidase (HRP) (Southern Biotech) in 1% BSA in PBS/Tween for 1 hour at 37°C to detect the OVA detection antibody. Plates were then developed using tetramethylbenzidine (TMB) substrate solution (Invitrogen) and stopped with 0.5 N hydrochloric acid. Plates were read on a spectrophotometer plate reader (Molecular Devices) and analyzed using SoftMax Pro and Microsoft Excel.

Sandwich ELISA-based ovomucoid detection kits from Indoor Biotechnologies (EPC-GD1–5) were used to quantify ovomucoid in muffin and baked egg extracts. These plates were read on a spectrophotometer plate reader (Molecular Devices) and analyzed using SoftMax Pro and Microsoft Excel.

Allergen-specific IgE blocking ELISAs

96-well ELISA plates (Thermo Fisher Scientific) were coated with either 20 μg/mL ovomucoid (Sigma-Aldrich) or ovalbumin (Sigma-Aldrich) in carbonate buffer overnight at 4°C. Plates were blocked with 1% BSA in PBS/Tween for 1 hour at 37°C. Pooled muffin extracts were incubated with serum from egg allergic patients, with a 1:10 final dilution of serum, for 15 minutes at room temperature. Samples were then loaded onto blocked plates and incubated for 2 hours at 37°C. Allergen-specific IgE bound to the plates was then detected by incubating with goat anti-human IgE-HRP (Southern Biotech) at a 1:4000 dilution in 1% BSA in PBS/Tween for 1 hour at 37°C. Plates were then developed using TMB and read, as above.

Patient serum samples

Serum samples and clinical data were collected from four pediatric egg-allergic patients seen at the Yale Pediatric Allergy and Immunology Clinic (New Haven, CT). Sex was self- or caregiver-reported and gathered from chart review. Serum collection was approved by the Yale University Institutional Review Board (HIC Protocol Number 2000028137). Informed consent was obtained from legal guardians, and assent was obtained from child participants. All methods were performed in accordance with relevant guidelines and regulations.

Data analysis

Data in the text are presented as means with standard deviations (SD). Between-group comparisons of ELISA data were conducted at the two-sided alpha of 0.05 and were performed using Student’s t-test or analysis of variance (ANOVA), with post-hoc analysis conducted using Tukey’s multiple comparison test. ELISA dilution curves were analyzed with area under the curve (AUC) comparisons. All statistical analyses were performed using GraphPad Prism.

Results

Baking reduces the amount of detectable major egg allergens

First, the study aimed to confirm the effect of heating on the amount of extractable allergen in baked egg without a muffin matrix, representing available free egg allergen that could be solubilized and lead to systemic reactions in allergic patients. Baking egg alone at 350°F for 30 minutes resulted in a reduction in both extractable ovalbumin (Figure 1A) and ovomucoid (Figure 1B), although there was a greater reduction in free ovalbumin concentrations compared to ovomucoid concentrations. Ovalbumin concentration in extracts was reduced from a mean of 67,960 to 35 μg/mL (a 1,942-fold reduction) while ovomucoid concentration was reduced from a mean of 720 to 10 μg/mL (a 72-fold reduction) after baking. In baked egg, allergen availability could be affected either by heat denaturation or by heat aggregation of the egg proteins leading to lower amounts of extractable free protein. To better understand the effect of heating alone on ovalbumin and ovomucoid, we heated dilute solutions of purified ovalbumin and ovomucoid to various temperatures between 30°C and 100°C. We found that heating these individual solutions led to lower amount of detectable ovalbumin and ovomucoid (Figure 1C). Consistent with previous reporting (20), 50% of ovalbumin was denatured at 70°C. Detectable ovomucoid was also reduced by heating, though it appeared to be more resistant to denaturation than ovalbumin. Of note, both ovalbumin and ovomucoid continued to be denatured between 90°C and 100°C, the temperature many muffins are cooked to, so alterations to the final internal temperature of muffins may affect the amount of detectable ovalbumin and ovomucoid.

Figure 1: Baking reduces the amount of detectable major egg antigens.

Figure 1:

Open in a new tab

Measurement of the amount of extractable ovalbumin (A) and ovomucoid (B) in raw egg (n=10) and baked egg (n=4). (C) The amount of ovalbumin and ovomucoid in a pooled heated solution of ovalbumin or ovomucoid, as a percentage of the amount detectable in unheated solutions of each, expressed as a graph (left) and a table (right). p-values are displayed, **** denotes p<0.0001.

The matrix effect impacts ovalbumin and ovomucoid differently

Next, the effect of a food matrix on the amount of extractable free egg allergens in the four experimental baked egg product formulations was examined. In order to control for the effect of heating, as opposed to the matrix effect, on detectable ovalbumin and ovomucoid, we added an amount of water equivalent to the amount of wet ingredients in the muffin recipes to the baked egg alone. The ovalbumin concentration in extracts from baked egg alone (mean=19 μg/mL, SD=6 μg/mL) was lower than the ovalbumin concentrations in all of the muffin extracts (Figure 2A). Though the difference in ovalbumin concentration was less pronounced between the muffin extracts, muffins made using wheat had less extractable ovalbumin (mean=209 μg/mL, SD=56 μg/mL) than those made using rice (mean=349 μg/mL, SD=80 μg/mL) or wheat/banana mix (mean=357 μg/mL, SD=156 μg/mL).

Figure 2: The matrix effect depends on the components of the food matrix and impacts ovalbumin and ovomucoid differently.

Figure 2:

Open in a new tab

Measurement of the amount of extractable ovalbumin (A) and ovomucoid (B) in baked egg (n=10) or muffins baked with wheat flour (n=20), a 1:1 blend of wheat flour and mashed banana (n=20), or rice flour (n=20). Dotted line on both figures indicates average amount of measured antigen in raw egg. p-values are displayed, **** denotes p<0.0001.

A different pattern was observed with ovomucoid in baked egg products (Figure 2B). Overall, ovomucoid concentrations were higher in extracts from baked egg alone (mean=25 μg/mL, SD=8 μg/mL) than in muffin extracts. Between the muffin extracts, there was less difference in how much free ovomucoid could be extracted, but there was significantly more ovomucoid in extracts from wheat/banana muffins (mean=10 μg/mL, SD=2 μg/mL) compared to wheat muffins (mean= 6 μg/mL, SD=2 μg/mL) or rice muffins (mean=6 μg/mL, SD=1 μg/mL).

The matrix effect reduces the amount of free egg allergen available to bind egg allergic IgE

The ability of the free egg allergens in extracts to bind allergen-specific IgE from egg allergic patients was then examined. Serum from individual egg allergic patients (Figure 3A) was incubated with various dilutions of pooled muffin extracts to allow ovalbumin or ovomucoid IgE from the patient samples to bind to the allergens in the muffin extracts. These incubated samples were then loaded onto ovalbumin- or ovomucoid-coated plates to detect any remaining free, unbound ovalbumin- or ovomucoid-specific IgE. In this assay, if patients’ egg-specific IgE targeted similar epitopes in the muffin extracts as in the egg allergen coating the plates, then the muffin extracts would block binding of the egg-specific IgE to these plates. Indeed, based on the area under the curve analyses, muffin extract was able to block binding of egg-allergic patient IgE to both ovalbumin (Figure 3B) and ovomucoid (Figure 3C). Notably, the wheat/banana muffin extract was able to inhibit ovomucoid IgE binding more than the wheat or rice muffin extracts.

Figure 3: The matrix effect reduces the amount of free egg allergen available to bind egg allergic IgE.

Figure 3:

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(A) Table describing clinical characteristics of egg allergic patients who contributed serum samples. (B) Averaged ovalbumin IgE dilution curves from patient numbers 1, 2, 3, and 4 after incubation with various concentrations of muffin or egg extracts, expressed as percent inhibition compared to unblocked samples. (C) Averaged ovomucoid IgE dilution curves from patient numbers 1, 2, and 4 after incubation with various concentrations of muffin or egg extracts, expressed as percent inhibition compared to unblocked samples. AUCs of each set of ELISA dilution curves were compared by ANOVA, and p-values of post-hoc pairwise comparisons are displayed in a table next to each figure, with * denoting p<0.05 and ** denoting p<0.01.

Discussion

This study examined the effect of baking and food matrices on the amount of extractable egg allergens in various formulations. The study found that there was less detectable ovalbumin and ovomucoid in extracts from baked eggs compared to raw eggs, confirming the previously described effect of heating on egg allergens. While heat denaturation appeared to similarly affect ovalbumin and ovomucoid, the reduction in detectable ovalbumin was greater than the reduction in ovomucoid after baking, which is consistent with previous literature showing that ovalbumin is uniquely susceptible to heat aggregation in addition to denaturation (9).

When investigating the matrix effect, this study found that baking eggs in muffins, with a food matrix, appeared to increase the amount of extractable ovalbumin as compared to baked egg alone. This finding was interesting, suggesting that the muffin may be “protecting” ovalbumin in some way that the baked egg alone did not. This study also found that baking eggs in muffins, with a food matrix, appeared to decrease the amount of extractable ovomucoid compared to baking eggs in water, with some differences appreciated with variations in ingredient amounts. This finding is consistent with previous reports that have shown that food matrices can inhibit egg protein solubilization. This finding is consistent with the observation that egg allergic children can often tolerate muffins (21), as baked muffins would have less bioavailable ovomucoid. Furthermore, this effect of the food matrix appears to be partially dependent on the ingredients used in the muffin, with wheat and rice flours preventing ovomucoid solubilization better than a wheat flour and mashed banana mix. Wheat gluten is known to form protein networks (22), which may limit protein extraction and affect detection of ovomucoid in different muffin formulations. Similarly, rice flour has been shown to form protein-starch-lipid matrices (23), which could potentially decrease protein extractability. It appears that replacing wheat flour with banana may partially abrogate the matrix effect, which suggests that using the full amount of flour in a recipe may be important for maximizing the matrix effect.

Finally, by utilizing egg-allergic patient sera, this study found that the ovalbumin and ovomucoid detected in extracts was capable of binding ovalbumin and ovomucoid-specific IgE from egg-allergic patients. This supports the translational and clinical relevance of these lab findings.

Though muffins were processed in a way to approximate physiologic processes, this study is limited by the in vitro methods used to obtain data for muffin extracts. First, it is important to note that we extracted proteins from muffin formulations at 37 °C in order to mimic physiologic conditions, even though optimal egg protein recovery may occur at higher temperatures and with different extraction buffers (24, 25). Additionally, we did not measure the inner temperatures of muffins after baking, and therefore cannot report on the effect of differences in final internal temperature between the muffin formulations on allergen detection. However, when processing muffins after baking, we used a representative cross section that contained both outside and inside portions of the muffin in equal proportions across samples, which we hope allowed for consistent sampling of muffins despite variations on internal temperatures. Second, we had access to ELISA technology for this study, but MS may be a superior technology for these experimental conditions. Previous researchers have described challenges in using ELISA kits for reliably quantifying egg in various matrices (25, 26). A multi-allergen MS allows for the use of more stringent extraction conditions for protein solubilization, which allows for more targeted egg peptide detection after digestion procedures (18). While our study adds to the literature on basic and translational aspects of the matrix effect, it would be beneficial to optimize protein extraction conditions and detection methods in future experiments.

Future studies may also determine how baking and food matrices affect in vivo allergy response, such as in sensitized mouse models. This study focused on the effect of certain commonly used flours and substitutes on egg allergen availability. In future work, other ingredients or components of the food matrix, such as fats, proteins, carbohydrates, and water, can be examined separately to determine how each affects egg allergen availability.

Overall, this work demonstrates that the food matrix can affect egg allergen availability and may be important to take into consideration during clinical practice. This suggests that patients and families should be advised that substitutions in baked egg recipes, perhaps for example substituting fruit or vegetable starch for wheat starches, may affect the amount of available egg allergen in foods and thus potentially affect the risk of food allergic reaction.

Highlights Box.

  • What is already known about this topic? Egg allergy is prevalent, and often, egg-allergic patients can tolerate egg baked into other ingredients, or a food matrix. The effect of the composition of the food matrix on egg allergenicity is still not fully understood.

  • What does the article add to our knowledge? Changing the food matrix that egg is cooked in can affect how much egg allergen is extractable from the food. The composition of the food matrix impacts the availability of ovalbumin and ovomucoid differently.

  • How does this study impact current management guidelines? Patients and families should be advised that making ingredient substitutions in baked egg recipes can increase the amount of available egg allergen in foods and thus potentially affect the risk of food allergic reaction.

Acknowledgments

We sincerely appreciate the participation of egg allergic patients and their families in this study.

Funding:

This study was funded by the Hurst Family Research Endowment for Pediatric Food Allergy. In addition, this publication was made possible by a Yale Physician Scientist Development Award and CTSA Grant Number UL1 TR001863 from the National Center for Advancing Translational Science (NCATS), a component of the National Institutes of Health (NIH). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of NIH.

Abbreviations

ANOVA

analysis of variance

AUC

area under the curve

BSA

bovine serum albumin

°C

degrees Celsius

DNA

deoxyribonucleic acid

ELISA

enzyme-linked immunosorbent assay

°F

degrees Fahrenheit

HRP

horseradish peroxidase

IgE

immunoglobulin E

μg

microgram

mL

milliliter

PBS

phosphate buffer saline

SD

standard deviation

TMB

tetramethylbenzidine

Footnotes

Conflict of Interest Disclosure: SL is a paid consultant for Regeneron and Linical, and she also receives funding from Food Allergy Research and Education (FARE). EGL, JT, JSM, VS, and SCE declare no conflicts of interest.

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