







































_____________________________________________________________________________________________________ 
 
*Corresponding author: E-mail: celso@alergoimuno.med.br; 
 
Cite as: Olivier, Celso Eduardo, Daiana Guedes Pinto, Ana Paula Monezzi Teixeira, Cibele Silva Miguel, Jhéssica Letícia 
Santos Santana, Regiane Patussi Santos Lima, Nicole Sartoreto Rocha, and Raquel Acácia Pereira Gonçalves Santos. 2025. 
“Endotyping Cellular and Humoral Cross-Reactivity Against Chicken Meat and Egg Yolk in Non-IgE-Mediated Food Protein-
Induced Gastrointestinal Allergies”. Asian Journal of Immunology 8 (1):207-21. https://doi.org/10.9734/aji/2025/v8i1172. 

 
 

Asian Journal of Immunology 
 
Volume 8, Issue 1, Page 207-221, 2025; Article no.AJI.141585 
 

 
 

 

 

Endotyping Cellular and Humoral  
Cross-Reactivity Against Chicken Meat  

and Egg Yolk in Non-IgE-Mediated 
Food Protein-Induced Gastrointestinal 

Allergies 
 

Celso Eduardo Olivier a*, Daiana Guedes Pinto a,  
Ana Paula Monezzi Teixeira a, Cibele Silva Miguel a, 

Jhéssica Letícia Santos Santana b,  
Regiane Patussi Santos Lima c,  Nicole Sartoreto Rocha d 

and Raquel Acácia Pereira Gonçalves Santos a 
 

a Instituto Alergoimuno de Americana, Brazil. 
b Instituto de Ensino e Pesquisa do Hospital de Amor de Barretos, Brazil. 

c Biomega Medicina Diagnóstica, São Paulo, Brazil. 
d Faculdade de Americana, São Paulo, Brazil. 

 
Authors’ contributions  

 
This work was carried out in collaboration among all authors. All authors read and approved the final 

manuscript. 
 

Article Information 
 

DOI: https://doi.org/10.9734/aji/2025/v8i1172  
 

Open Peer Review History: 
This journal follows the Advanced Open Peer Review policy. Identity of the Reviewers, Editor(s) and additional Reviewers,  

peer review comments, different versions of the manuscript, comments of the editors, etc are available here: 
https://pr.sdiarticle5.com/review-history/141585  

 
 

Received: 25/07/2025 
Published: 09/08/2025 

 

Original Research Article 

https://doi.org/10.9734/aji/2025/v8i1172
https://pr.sdiarticle5.com/review-history/141585


 
 
 
 

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208 

 

ABSTRACT 
 

Background: Non-IgE-mediated food protein-induced gastrointestinal allergies (FPI-GIAs) are 
poorly understood, although IgE-mediated hypersensitivities have been extensively described. 
Patients with poultry meat allergy may present several phenotypes regarding clinical presentations 
and a wide range of symptom severity, suggesting the existence of several endotypes underlying 
their diseases.  
Aim: To evaluate the potential of the Tube Titration of Precipitins (TTP) and the Leukocyte 
Adherence Inhibition Test (LAIT) to discriminate cellular and humoral immunoreactivity against 
chicken meat extract and chicken egg yolk extract in patients with non–IgE-mediated 
gastrointestinal food protein-induced allergic phenotypes. 
Study Design: We examined retrospectively the medical charts of two cohorts of patients clinically 
diagnosed with non–IgE-mediated gastrointestinal food protein-induced allergic phenotypes related 
to consumption of chicken meat and/or chicken egg yolk, who were investigated with the help of 
TTP or LAIT. 
Methodology: The TTP and LAIT's registered results against chicken meat and chicken egg yolk 
extracts were distributed in ranges through a cascade distribution chart to outline the variability of 
the results within the cohorts. The Pearson correlation test was used to evaluate the correlation 
between the results obtained simultaneously with both food allergens. 
Results: The LAIT for the chicken meat extract and egg yolk extract showed a wide distribution 
range of results. The TTP for the chicken meat and egg yolk extracts showed a distribution 
concentrated on the higher dilutions. The Pearson correlation test showed a non-significant positive 
correlation between LAIT for egg yolk and LAIT for chicken meat extract; r(98) = 0.156, p = 0.121. 
The Pearson correlation test showed a non-significant positive correlation between TTP for the egg 
yolk extract and TTP for the chicken meat extract; r(98) = 0.181, p = 0.072. 
Conclusion: Our preliminary results support that the TTP and LAIT performed with chicken meat 
and egg yolk extracts may discriminate diverse humoral and cellular immunoreactivity degrees in 
patients suffering from food protein-induced gastrointestinal allergies. Despite no statistically 
significant quantitative correlation between the results, these findings may improve dietary 
guidelines for impacted individuals and contribute to creating diagnostic biomarkers. 
 

 
Keywords: Endotype; hypersensitivity; chicken meat; food protein-induced enterocolitis syndrome; 

leukocyte adherence inhibition test; Non–IgE-mediated immunoreactivity; poultry meat; 
precipitins. 

 

ABBREVIATIONS 
 
FA : Food Allergies 
FPI-GIA : Food Protein-Induced Gastrointestinal Allergies 
LAI : Leukocyte Adherence Inhibition 
LAIT : Leukocyte Adherence Inhibition Test 
LMIT : Leukocyte Migration Inhibition Test 
TTP : Tube Titration of Precipitins 
 

1. INTRODUCTION  
 

Food protein-induced gastrointestinal allergies 
(FPI-GIA) and Food Allergies (FA) are yet a 
conundrum for physicians, gastroenterologists, 
nutritionists, allergists, but mainly for patients 
who suffer from these conditions (Olivier 2013). 
 

IgE-dependent mechanisms may produce FPI-
GIA; however, most cases are produced by 
hypersensitivities endotypes not mediated by IgE 
(Heine 2015, Khan 2016, Ahmed et al. 2021). 

Non-IgE-mediated FPI-GIA are associated with a 
large spectrum of phenotypic conditions, 
clinically classified by the predominant anatomic 
localization of the symptoms (such as food 
protein-induced proctocolitis, food protein-
induced enterocolitis, food protein-induced 
enteropathy, eosinophilic esophagitis, 
eosinophilic gastroenteritis, food protein-induced 
gastro-esophageal reflux disease, celiac disease, 
multiple food protein intolerance of infancy, food 
protein-induced gastrointestinal motility 
disorders), as well as some “functional” 



 
 
 
 

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conditions, such as infantile colic, which food 
proteins may also induce (Groetch et al. 2025, 
Huang & White 2025). These so-called food 
protein-induced allergic syndromes may manifest 
through exchangeable, heterogeneous, and 
recurrent symptoms with mild, moderate, or 
severe presentations, posing diagnostic and 
therapeutic dilemmas (Heine 2004). 
 
Self-reported allergy to poultry meat is not a very 
common complaint in clinical practice (Sloan & 
Powers 1986). However, when researched, the 
incidence of diagnosis of hypersensitivity to 
chicken meat (Gallus domesticus) may be 
surprising. Sampson reported an incidence of 
16,8% of positive skin prick tests to chicken meat 
among children with atopic dermatitis due to FA 
(Sampson & McCaskill, 1985).  
 
The first report of chicken meat allergy was 
described in 1982 as a non–IgE-mediated 
enteropathy in a child who proved to be allergic 
to chicken meat and cow’s milk through 
provocation tests monitored by jejunal biopsies 
demonstrating severe villous atrophy after 
ingestion of chicken meat (Vitoria et al. 1982). It 
took fourteen years for the subsequent 
description of a non–IgE-mediated Eosinophilic 
Gastroenteritis to be documented after a chicken 
meat provocation test monitored by intestinal 
biopsies (Vandenplas et al. 1994). Food protein-
induced enterocolitis syndrome is a non-IgE-
mediated FPI-GIA that may present with 
symptoms such as flatulence, bloating, cramps, 
postprandial discomfort, vomiting, and diarrhea, 
due to chronic exposure to an offending food, or 
general symptoms, such as failure to thrive, while 
avoiding an offending food. (Agyemang & 
Nowak-Wegrzyn 2019). Initially described by 
pediatricians and attributed to liquid foods, such 
as cow’s milk and liquid infant soy formulas, it 
was becoming apparent that solid foods 
(including poultry meat) could also be 
responsible for food protein-induced enterocolitis 
syndrome (Nowak-Wegrzyn et al. 2003). 
 
Patients with poultry meat FA may present 
several phenotypes regarding clinical severity 
and features, suggesting the existence of several 
endotypes underlying clinical symptoms 
(Wanniang et al. 2022). As with any FA, the 
endotypes behind poultry allergy are primarily 
classified as IgE-mediated and non–IgE-
mediated. Chicken meat allergy has complex 
sensitization profiles with nine major established 
allergens and twenty-five proposed candidates 
(Guiddir et al. 2024). The major chicken meat 

allergen identified by a proteomics-based 
approach is a myosin light chain protein 
designated Gal d 7 (shared by several poultry 
species), containing the majority of IgE-binding 
epitopes, characterized by remarkable thermal 
stability, refolding capacity, and resistance to 
salivary and gastrointestinal enzymes (Klug et al. 
2020). Poultry species develop common 
allergens, making usual cross-reactivity between 
chicken meat and turkey meat, as well as with 
other species (Cahen et al. 1998). 
 
Allergic reactions following the administration of 
hen’s egg yolk-based vaccines (such as for 
yellow-fever and typhus) have been described 
since the forties (Rubin 1946). Allergic symptoms 
related to ingestion of hen’s egg yolk have been 
reported since the 1950s, mainly in children, 
including regurgitation, eczema, and respiratory 
symptoms (Todd et al. 1957). 
 
Allergy to chicken meat can also develop as a 
cross-sensitivity against hen egg proteins (bird-
egg syndrome) (Hemmer et al. 2016). Bird-egg 
syndrome is a peculiar IgE-mediated cross-
hypersensitivity to egg-yolk alpha-livetin (chicken 
serum albumin or Gal d 5), also associated with 
inhaling birds’ feathers and dander (Mandallaz et 
al. 1988, Szépfalusi et al. 1994). Three chicken 
meat allergens: parvalbumin (Gal d 8), enolase 
(Gal d 9), and aldolase (Gal d 10) are also 
present in fish and are responsible for a cross-
reactive hypersensitivity condition called the 
“fish–chicken syndrome” (Kuehn et al. 2016). 
 
Usually, patients present reactions to multiple 
foods, an issue reinforced by the few laboratory 
tests which can suggest the possibility of non-
IgE-mediated hypersensitivities (Katz & Goldberg 
2014). Some facilities employ the Lymphocyte 
Stimulation Test for diagnosing hen’s egg yolk–
induced enterocolitis syndrome (Kajita et al. 
2023).  
 
Humoral immunoreactivity against food allergens 
and aeroallergens had been classically evaluated 
by Precipitins (Augustin 1953, Augustin et al. 
1960, Cunningham-Rundles et al. 1978, 
Ferguson and Carswell 1972, Heiner et al. 1962). 
We also routinely employ the Tube Research of 
Precipitins (TTP) in our facilities as a triage to 
evaluate humoral non–IgE-mediated 
immunoreactivity against suspected allergens 
before performing more exhaustive in vivo 
provocation tests (Olivier et al. 2023b, Olivier et 
al. 2021e, Olivier et al. 2021d, Olivier et al. 
2024e, Olivier et al. 2024c).  



 
 
 
 

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The Leukocyte Adherence Inhibition Test (LAIT) 
and its similar assay, the Leukocyte Migration 
Inhibition Test (LMIT), have classically been 
used to differentiate non–IgE-mediated 
immunoreactivity against microorganisms and 
aeroallergens (Fink et al. 1987, Kallen and 
Nilsson 1979, Kuratsuji 1981, Thomson 1982). 
The LAIT and the LMIT have also classically 
been used to differentiate non-IgE-mediated 
immunoreactivity against food allergens 
(Allardyce & Shearman 1975, George & 
Vaughan 1962, Ashkenazi et al. 1980, Butler et 
al. 1981, Papageorgiou et al. 1983). Non–IgE-
mediated cellular immunoreactivity against food 
allergens had also been reported by our group 
with the help of the LAIT (Olivier et al. 2022b, 
Olivier et al. 2022a, Olivier et al. 2022c, Olivier et 
al. 2023a). 
 
To evaluate the potential of the LAIT and TTP to 
endotyping non–IgE-mediated cellular and 
humoral immunoreactivity against egg yolk and 
chicken meat, we retrospectively compiled the 
electronic medical charts of patients diagnosed 
primarily with gastrointestinal food allergies 
(associated or not with other extra-intestinal 
allergic phenotypes) related to non–IgE-mediated 
hypersensitivity, who were investigated for 
immunoreactivity by one of these two assays. 
 
The present study is a proof-of-concept that 
hypothesizes that LAIT and the TTP may 
demonstrate a correlation between cellular 
and/or humoral immunoreactivity between egg 
yolk and chicken meat proteins in patients 
suffering from non–IgE-mediated FPI-GIA. 

 

2. MATERIALS AND METHODS  
 

2.1 Subjects 
 
After receiving Institutional Review Board 
approval from the Instituto Alergoimuno de 
Americana (Brazil; 05/2025), we reviewed the 
electronic chart of 10.600 outpatients who 
attended our facility from January 2018 to 
January 2025.  
 
A cohort of 100 consecutive outside patients 
(TTP cohort) had been submitted to TTP with 
chicken meat extract and egg yolk extract for 
presenting non–IgE-mediated FPI-GIA. This 
cohort counted 35 males; mean age 43.6 years; 
SD 22 years; range 5 to 94 years; median 42.5 
years; modes = 46 (appeared four times); 
geometric mean = 36.5 years.  
 

A cohort of 100 consecutive outside patients 
(LAIT cohort) had been simultaneously submitted 
to LAIT with chicken meat extract and egg yolk 
extract for presenting non–IgE-mediated FPI-
GIA. This cohort counted 35 males; mean age 34 
years; SD 24.7 years; range 1 to 100 years; 
median 31 years; modes = 5 years (appeared six 
times); geometric mean = 22.3 years.  
 

This study did not include patients under 
biological and/or systemic anti-inflammatory 
therapy. These procedures were offered to 
patients with clinical suspicion of chicken meat 
hypersensitivity who demonstrated a non-
reactive or inconclusive skin test against chicken 
meat (Olivier et al. 2013). 
 

2.2 Extracts 
 

2.2.1 Chicken meat extract 
 

Chicken meat (300g of breast) acquired from the 
local market (half cooked and half uncooked) 
was crushed, homogenized, and then left for 48 
hours in a Coca-based extractor solution 
(propylparaben 0.5g, methylparaben 1g, sorbitol 
30g, NaCl 5g, NaHCO3 2.5g, 1,000mL H2O)  at 4 
°C for protein extraction before centrifugation 
and separation of the water-soluble fraction from 
solid particles and oily fraction (Coca, 1922). The 
protein quantification of the allergen extracts was 
done according to Bradford’s protein-dye binding 
methodology (Bradford 1976). The solution was 
diluted in antigen dilution solution (NaCl 10g; 
KH2PO4 0.72g; Na3PO4 2.86g; methylparaben 
1g; propylparaben 0.5g; glycerin 400mL; H2O 
600mL) to an estimated protein concentration of 
1 mg/mL and stored at 4 °C in amber opaque 
glass vials. The chicken meat extract solution 
was used to perform allergic skin tests, TTP, and 
LAIT. All relevant and mandatory laboratory 
health and safety measures have been complied 
with during the experiments.  
 

2.2.2 Egg yolk extract 
 

Three cooked egg yolks and three uncooked egg 
yolks were prepared similarly with the chicken 
meat extract. 
 

2.3 LAIT: Ex vivo Investigation: 
Leukocyte Adherence Inhibition Test 

 
2.3.1 LAIT: Procedure for allergen ex vivo 

challenges 
 

We performed the LAIT as previously described 
(Olivier et al. 2012, Olivier et al. 2014, Olivier et 



 
 
 
 

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al. 2021a, Olivier et al. 2021b, Olivier et al. 
2021c).  
 

Shortly, each donor's fresh plasma was divided 
into two parts and used in parallel ex vivo 
challenging tests with the chicken meat extract 
(or the egg yolk extract) and the unchallenged 
plasma (added with antigen dilution solution as a 
control). We collected plasma with high leukocyte 
content (buffy coat) from the heparinized tube 
after one hour of sedimentation at 37 °C. Then, 
we distributed aliquots of 100 μL into Eppendorf 
tubes with (or without) the challenging extract 
and kept them under agitation for 30 minutes 
(200 rpm at 37 °C). 

 

2.3.2 LAIT: Procedure for adherence assay  
  

After incubation, the plasma was allocated into a 
standard Neubauer hemocytometer counting 
chamber with a plain, non-metallic glass surface 
and left to stand for 2 hours at 37 °C in the 
humidified atmosphere of the covered water bath 
to allow leukocytes to adhere to the glass. Next, 
we counted the leukocytes, removed the 
coverslip, and washed the chamber by 
immersion in a beaker with phosphate buffer 
saline (PBS) at 37 °C. Then, we added a drop of 
PBS to the hemocytometer's chamber and 
placed a clean coverslip over it. The remaining 
cells were counted in the same squares as 
previously examined.  

 

2.3.3 LAIT: Procedure for calculation  
 

The percentage of Leukocyte Adherence (LA) of 
each assay was estimated as: (the number of 
leukocytes observed on the hemocytometry 
chamber after washing divided by the number of 
leukocytes observed on the hemocytometry 
chamber before washing) and multiplied by 100 
(%). The Leukocyte Adherence Ratio (LAR) was 
estimated based on the ratio between the LA 
from the antigen-specific challenged plasma and 
the LA from the unchallenged control plasma: 
LAR = LA of the challenged sample divided by 
LA of unchallenged control plasma multiplied by 
100 (%). To further calculate the Leukocyte 
Adherence Inhibition (LAI), we subtracted the 
LAR from 100 (%). We employed the LAI results 
for the cascade distribution chart and the 
statistics calculations; both performed with the 
help of the Microsoft Excel® statistical package. 
 

2.4  TTP: In vitro Investigation: Tube 
Titration of Precipitins 

 

As previously reported, the semi-quantitative 
TTP against the chicken meat extract (or the egg 

yolk extract) was performed in a transparent 
vitreous tube array (Olivier et al. 2024f, Olivier et 
al. 2024d, Olivier et al. 2024b, Olivier et al. 
2024a). Shortly, the patient’s blood was collected 
in a clot-activator collecting tube. After 
separation, the serum was centrifuged at 2,000 
rpm for 10 minutes. Each allergen extract was 
allocated in sets of eleven glass tubes at 
progressively duplicated serum dilutions. The 
progressive dilutions were combined with 
separated aliquots of 15 μL of the allergen 
extract with 250 μL of the patient’s serum, 
progressively diluted into physiological saline 
solution (NaCl 0,9%) in the dilution ratios of 1:1; 
1:2; 1:4; 1:8; 1:16; 1:32; 1:64; 1:128; 1:256; and 
1:512. One tube was a blank control done with 
water and serum to observe occasional 
spontaneous precipitation (Sia Test). After 24 
hours, the tubes were examined, and the titers 
(the highest dilution factor that yields a positive 
reading) were recorded (Williams & Chase 
1971). 
 

3. RESULTS 
 
As a retrospective survey, there was no research 
protocol; therefore, we report the incidental 
immune investigation as registered in the digital 
medical charts.  
 
The TTP for the chicken meat extract showed a 
distribution concentrated on the higher dilutions 
(Fig. 1). There was no negative result. The mean 
was estimated at 1:307; the median was 1:256; 
the standard deviation was estimated at 1:175; 
the mode was 1:512 (appeared 39 times).   
 
The TTP for the egg yolk extract showed a 
distribution concentrated on the higher dilutions 
(Fig. 2). There were two negative results. The 
mean was estimated at 1:335; the median was 
1:256; the standard deviation was estimated at 
1:179; the mode was 1:512 (appeared 48 times).   
 
The Pearson correlation estimates a non-
significant, small positive relationship between 
TTP for the egg yolk extract and TTP for the 
chicken meat extract; r(98) = 0.181, p = 0.072. 
See Fig. 3. 
 
The LAIT for the chicken meat extract showed a 
wide distribution range of results. The LAI ranged 
from 0% to 99%. The mean was 48.5%; the 
median was 50.5%; the standard deviation was 
29.8%; the mode was 0% (appeared eleven 
times). The cascade distribution demonstrates a 
wide range of LAI results (see Fig. 4). Some 



 
 
 
 

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patients showed low or moderate 
immunoreactivity during the ex vivo challenge 
test. In contrast, others displayed strong 
immunoreactivity, which could reflect the 
participation of chicken meat allergens in a Non–
IgE-mediated hypersensitivity condition in these 
patients. 
 
The LAIT for the egg yolk extract showed a wide 
distribution range of results. Most results were 
concentrated in the more immunoreactive 
groups. The LAI ranged from 0% to 99%. The 
mean was 50.2%; the median was 51%; the 
standard deviation was 27%; the mode was 0% 

(appeared eight times). The cascade distribution 
demonstrates a wide range of LAI results (see 
Fig. 5). Some patients showed low or moderate 
immunoreactivity during the ex vivo challenge 
test. In contrast, others displayed strong 
immunoreactivity, which could reflect the 
participation of egg yolk allergens in a Non–IgE-
mediated hypersensitivity condition in these 
patients. 
 
The Pearson correlation estimates a non-
significant small positive relationship between 
LAIT for egg yolk and LAIT for chicken meat 
extract; r(98) = 0.156, p = 0.121. See Fig. 6.

 

 
 

Fig. 1. Cascade distribution chart of the tube titration of precipitins (x-axis %) resulting from 
the chicken meat extract against the serum of the TTP cohort of 100 tests/subjects (y-axis) 

 

 
 

Fig. 2. Cascade distribution chart of the tube titration of precipitins (x-axis %) resulting from 
the hen’s egg yolk extract against the serum of the TTP cohort of 100 tests/subjects (y-axis) 



 
 
 
 

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213 

 

 
 
Fig. 3. Dispersion chart of the Tube Titration of Precipitins (TTP) results against hen’s egg yolk 

extract (x-axis), plotted against the TTP results against chicken meat extract (y-axis). The 
tendency line shows a non-significant, small positive relationship between the assays; r(98) = 

0.181, p = 0.072 
 

 
 
Fig. 4. Cascade distribution chart of the range groups of Leukocyte Adherence Inhibition (LAI) 
results (x-axis %) of the ex vivo challenge test against chicken meat extract monitored by the 
Leukocyte Adherence Inhibition Test (LAIT), according to the respective number of outcomes 

over the LAIT cohort with 100 tests/subjects (y-axis) 
 



 
 
 
 

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Fig. 5. Cascade distribution chart of the range groups of Leukocyte Adherence Inhibition (LAI) 
results (x-axis %) of the ex vivo challenge test against hen’s egg yolk extract monitored by the 
Leukocyte Adherence Inhibition Test (LAIT), according to the respective number of outcomes 

over the LAIT cohort with 100 tests/subjects (y-axis) 
 

 
 

Fig. 6. Dispersion chart of the Leukocyte Adherence Inhibition (LAI) results of the ex vivo 
challenge test against hen’s egg yolk extract (x-axis %), plotted against the LAI results of the 

ex vivo challenge test against chicken meat extract (y-axis %). The tendency line shows a non-
significant, small positive relationship between the assays; r(98) = 0.156, p = 0.121 

  

4. DISCUSSION 
 
The semi-quantitative titration of precipitins is a 
pioneering technique to evaluate humoral 
immunoreactivity (Wells 1911, Hunter 1905, 
Olivier et al. 2025b, Olivier et al. 2025a). 
Precipitating antibodies suggest the presence of 

a specific humoral immune response against the 
tested antigens (Gell et al. 1946, Ishizaka et al. 
1959). Before the discovery of IgE, the research 
of precipitins was the leading way to realize in 
vitro diagnosis of immunoreactivity against 
antigenic and allergenic agents (Augustin & 
Hayward 1960). The discovery of IgE and its 



 
 
 
 

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reaginic activity, as well as the concomitant 
development of the Radio-Allergo Sorbent Test 
(RAST) to detect specific IgE antibodies, focused 
the attention of the scientific and medical 
community on this particular antibody class, 
mainly after the incorporation of similar non-
radioactive assays into routine clinical assays 
(Wide 1967, Ishizaka & Ishizaka 1967). 
 
Although the serum-free IgE (as detected by 
routine immunoassays) is not held responsible 
for clinical symptoms (as are the tissue-bound 
IgE, responsible for the autocoids released after 
the encounter with the antigen), the research on 
serum-specific IgE constructed a paradigm in the 
physician’s mentality. The research of tissue-
bond IgE, as performed by allergic skin tests, is 
easily performed; however, the demonstration of 
tissue-bond IgE in mucosal sites is a complex 
task, substituted by the research of eosinophils 
and T cells in endoscopic biopsies of patients 
with FA. This technical hindrance did not prevent 
the creation of the “IgE-mediated Local Allergic 
Reaction” concept in food hypersensitive patients 
(Lin et al. 2002). This concept gave further origin 
to the similar concept of “IgE-mediated Local 
Allergic Rhinitis”, which advocates the mucosal 
production of IgE at insufficient concentrations to 
be reflected in the blood immunoassays or the 
skin tests (Rondon et al. 2010). 
 
Usually, the correlation and the distribution of 
simultaneous positive specific-IgE against food 
allergens and inhalant allergens are weak; 
however, when properly investigated, 
polysensitization is more the rule than the 
exception in FPI-GIA (Zhang et al. 2025, 
Čelakovská et al. 2024).  
 
The paradigm of the specific antibody to 
diagnose the etiology of the allergic symptoms 
has led to the “IgE culture” and a pressing pursuit 
to determine the utility of the specific IgG to 
diagnose the non–IgE-mediated hypersensitivity 
conditions (Atwah & Koshak 2024). The use of 
specific IgG against food allergens may be 
contentious and controversial since the IgG may 
sometimes act as a hypersensitivity trigger and 
sometimes as an allergen blocker, depending on 
its subclass, the antigen-antibody proportion, and 
the participation of other immune players 
(Alkhateeb 2020). IgG antibodies can participate 
in type II (antibody-dependent cell-mediated) and 
type III (immune complex disease) Gell and 
Coombs hypersensitivity reactions, which may be 
theoretically reproduced by the LAIT and the TTP 
assays, respectively (Olivier et al. 2021a). 

However, there is a lack of effective and practical 
tools to diagnose gastrointestinal inflammatory 
reactions due to FA in patients with no evidence 
of systemic circulatory IgE (Olivier 2022). 
 
The LAIT is an ex vivo challenge test performed 
with a viable leukocyte buffy coat that can 
theoretically explore most known immune 
pathways, as it allows the interaction of all 
immune-circulating participants with the allergens 
(Olivier et al. 2021a). Several immune pathways 
can produce the final leukocyte adherence 
inhibition (Tong et al. 1979, Halliday 1974). 
 
The present study is a proof-of-concept that 
hypothesizes that LAIT and the TTP may 
differentiate diverse degrees of cellular and 
humoral immunoreactivity against hen’s egg yolk 
and chicken meat allergens among patients 
suffering from non–IgE-mediated FPI-GIA. As the 
tests were performed simultaneously with the 
same venous sample with the two allergens, it 
was possible to calculate a correlation test to 
distinguish some order of cross-reactivity 
between them.  
 
The retrospective compilation of our data showed 
a large distribution of results when we 
ascertained the results of TTP and LAIT to 
explore humoral and cellular immunoreactivity 
against two chicken food allergens. These 
immunoassays did not precisely identify the 
mechanisms responsible for the clinical 
condition. Instead, they provide evidence about 
cellular and humoral immunoreactivity distributed 
into an extensive spectral range that may 
suggest immune tolerance or hypersensitivity. 
 
This preliminary retrospective survey 
demonstrated extensive results from the TTP 
and the ex vivo challenge test monitored by LAIT 
against hen’s egg yolk and chicken meat 
allergens in two cohorts of non–IgE-mediated 
food allergic patients. TTP and LAIT are 
complementary triage tests used at our facilities 
to select worthwhile antigens to proceed with 
more laborious in vivo provocation tests when 
the specific IgE is undetectable. None of our 
patients presented an exclusive reaction to these 
allergens. Every patient was simultaneously 
tested for several chemical and biological 
allergens, demonstrating positive results for 
some of them. Our results suggest that patients 
suffering from FPI-GIA due to hen’s egg yolk 
allergy may experience additional cross-
immunoreactivity against chicken meat allergens 
and vice-versa. 



 
 
 
 

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5. LIMITATIONS 
   

This study is a retrospective analysis of data 
collected over seven years. There was no 
research protocol, and the subject's data was 
limited to the essentials available on our 
electronic sheets. Therefore, we could not 
establish a cross-comparison between positive 
and negative controls to validate the results. The 
number of subjects is appropriate for preliminary 
analyses; however, future studies must be more 
comprehensive. The lack of a research protocol 
implies the possibility of a bias produced by the 
physician's point of view who indicated the exam 
(Olivier, CE) based on a clinical suspicion led by 
anamnesis, physical examination, results of skin 
tests, and the research of specific IgE. The study 
lost the follow-up of most patients, hampering the 
registration of the relationship between the 
immunoassay results and the patient's clinical 
outcome. Unfortunately, it was also impossible to 
compare the two procedures with paired tests 
because they were taken from distinct groups of 
patients. 

 

6. CONCLUSION 
 
Our preliminary results show that the LAIT and 
TTP may differentiate diverse degrees of 
immunoreactivity against chicken meat and egg 
yolk extracts in patients clinically diagnosed with 
non–IgE-mediated Gastrointestinal Food 
Allergies. LAIT and TTP are inexpensive, can be 
performed with minimum laboratory equipment, 
and can be incorporated into strategies to 
address respiratory and food allergy health 
disparities (Anagnostou et al. 2025). As a 
preliminary report, the propaedeutic meaning of 
the presented results and the possibility of 
interferents must be yet established (Anouar 
2024). More studies focused on the quality-by-
design approach, with prospective larger double-
blind cohorts needed to evaluate the potential 
contribution of LAIT and TTP for endotyping 
cellular and humoral immunoreactivity in patients 
suspected of hypersensitivity against chicken 
allergens (Chiarentin et al. 2023). 

  

7. FUTURE DIRECTIONS AND 
RECOMMENDATIONS FOR CLINICAL 
PRACTICE 

 
The primary intended use of in vitro or ex vivo 
allergen challenge tests is to spare the patients 
from being submitted to unnecessary, 
exhaustive, and dangerous in vivo challenge 

tests. Exploring the humoral and the cellular 
arms of immune systems, the TTP and LAIT 
alone or combined may represent, in the near 
future, a tool for allergists to construct an 
etiologic diagnosis from their patients, as well as 
determine the endotypes (mechanisms) of 
hypersensitivity, in order to choose more 
convenient and personalized therapies for them. 
Adding data provided by TTP and LAIT may also 
contribute to streamlining biomedical research 
and improving tools such as Large Language 
Models, usually used by clinicians as a decision 
support system to enhance diagnostic accuracy 
(Abers & Mathias 2025). 
 

DISCLAIMER (ARTIFICIAL INTELLIGENCE) 
 
Author(s) hereby declare that NO generative AI 
technologies such as Large Language Models 
(ChatGPT, COPILOT, etc) and text-to-image 
generators have been used during writing or 
editing of this manuscript.  
 

ETHICAL APPROVALS 
 
As a retrospective survey of results recorded in 
cognito, consent was given collectively by the 
institution's ethics committee following the 
principles of the Declaration of Helsinki (WMA 
2013). 
 

ACKNOWLEDGEMENTS 
 

The Instituto Alergoimuno de Americana funded 
this work. We want to thank the laboratory 
technicians Alessandra Vieira de Oliveira and 
Luciana Sacilotto Carvalho for their help with the 
exams.  
 

COMPETING INTERESTS 
 

Authors have declared that no competing 

interests exist. 
 

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of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, 
distribution, and reproduction in any medium, provided the original work is properly cited. 

 
 

 

Peer-review history: 
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https://pr.sdiarticle5.com/review-history/141585  

https://pr.sdiarticle5.com/review-history/141585

