Chicken meat allergy in children: Complex sensitization profiles with newly described allergen candidates
Authors: T. Guiddir, H. Sénéchal, M. A. Selva, R. Couderc, I. Swoboda, C. Hilger, A. Kuehn, Y. Chantran, S. Yen‐Nicolaÿ, T. Vrai, G. Ruellou, B. Baudin, P. Poncet, A. Nemni
Journal: Allergy (2024)

Chicken meat allergy (ChMA) has an estimated incidence of 0.6%–5%.1 Symptoms range from mild oral syndrome to systemic reactions. Individual sensitization profiles remain poorly understood. The objective was to exhaustively and individually explore the clinical parameters (Table 1) and the IgE repertoire of five children (P1 to P5, 6–12 years old) with primary ChMA, without egg allergy, in order to compare clinical and IgE sensitization profiles. IgE repertoires were evaluated using multi-allergen chip (ALEX2©), dotline immunoassay on selected purified proteins, allergomic analysis, that is, two-dimensional (2D) gel electrophoresis of cooked chicken breast meat extract followed by IgE immunoblot (Figure 1A; Figure S1) and identification of allergens by liquid chromatography (LC) and mass spectrometry (MS) (see Methods in Data S1). Patients developed ChMA as the result of a break in tolerance. The skin prick test (SPT) and oral food challenge (OFC) were positive using chicken breast meat, poached and grilled. As depicted in 1D and 2D western blots (WB) (Figure 1D; Figure S1), profile complexity was low for P1 and P2, high for P4 and P5, and intermediate for P3. Proteins present in 30 excised gel spots matching 2D IgE-reactivities were identified by LC/MS/MS analysis (Figure S1). Out of 95 different proteins identified, 25 were considered to be the most relevant allergen candidates (Figure 1B) (see explanations in Data S1). Nine proteins corresponded to known allergens. Gal d 3, an allergen of mainly, but not only, egg white, is restricted to P2 and P3 and hemoglobin to P4 and P5. Gal d 7, 9, 10 and triose phosphate isomerase are potential allergens for P2, P3, P4 and P5. Gal d 5, also described in egg and chicken meat, is recognized by P5 only and Gal d tropomyosin by P4 only. Gal d 7 was found for all patients in WB and also in a dot/line immunoassay (Figure 1C), in agreement with its major characteristic.2 IgE reactivity to parvalbumin, not explored in 2D WB because the protein is not present in chicken breast,3 was shown to be recognized by five patients by the dot/line immunoassay. Ten chicken candidate allergens already described as allergens in other animal sources (fish, crustaceans, cattle, worms, mites, and insects) were identified, such as troponin and cofilin-2, candidate allergens for all five patients. Patients P3 and P4 are allergic to other fowl (turkey and duck) and P3 is allergic to tuna fish, likely because of reported IgE cross-reactivities between known allergen families such as parvalbumin or myosin light chain,2-5 but also other uncharacterized allergens. Some of these, mainly muscle proteins, are proposed as candidate allergens. As these proteins are part of large protein complexes, they might be processed together leading to a joint/synergistic Th2 sensitization. The ALEX2© multiplex assay (Table 1) detected reactivities to fish parvalbumin, probably as a consequence of IgE cross-reactivity not systematically related to allergy-induced symptoms. Finally, six additional putative IgE reactive proteins, not reported in animal food allergies, were found and some of them, like ATP synthase, malate dehydrogenase, and phosphoglycerate kinase, include allergens in plants and molds exhibiting more than 50% sequence identity with chicken orthologs. Chicken allergens with potential cross-reactivity with fish or crustacean are mentioned in Figure 1B either because they were reported cross-reactive in literature1, 6 or because they share more than 60% sequence identity (Uniprot Blast and Align). Allergens and patient overlaps are represented in a Venn diagram (Figure S2) and location of candidate allergens is shown on 1D WB (Figure 1D). In conclusion, the allergomic study, performed with the sera from five ChMA children, showed highly diversified sensitization profiles with no correlation with clinical severity evaluated by symptoms, SPT, sIgE, OFC results, and potential cross-reactivities. The 25 candidate allergens pointed out pave the way for the identification of additional clinically relevant allergens as an approach to patient endotyping and stratification. Conceptualization, writing original draft, review and editing: T. Guiddir, A. Nemni; 2D electrophoresis, western blot, protein spotting and data interpretation, writing, review and editing: H. Sénéchal, P. Poncet, M-A. Selva; Data processing, review and editing: R. Couderc, B. Baudin; Production of reagents, review and editing: I. Swoboda, C. Hilger, A. Kuehn; Serum laboratory analysis: Y. Chantran: Supervision of proteomic analysis from experiment design to data interpretation, review and editing: S. Yen-Nicolaÿ; Tryptic digestion, LC/MS analysis and data processing: G. Ruellou and T. Vrai. No funding. A-C. de Ménibus, A. Alsagaff, C. Billard-Larue. The authors declare no conflicts of interest for this article. The data that supports the findings of this study are available in the supplementary material of this article. Data S1. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.