Food hypersensitivity in primary school children in Taiwan: relationship with asthma

Abstract

Primary objective. A review of the literature suggested that food allergen intolerance was closely related to inhaled allergen hypersensitivity. Our aim was to determine whether food allergen sensitivity is a marker for increased asthma incidence in children. Methods and procedures. Food allergen sensitivity was evaluated in six- to eight-year-old primary school students (n=1010) using the Phadia ImmunoCAP, Phadiatop Infant and radioallergosorbent tests. Allergy history was obtained by telephone interview. Main outcomes and results. Males were more sensitive than females to food allergens. The most prevalent food allergies were scallop, abalone, lobster, pork, casein, alpha-lactalbumin and garlic. There was gender difference in fruit allergen sensitivity. Of the children who had doctor-diagnosed history of food hypersensitivity, 21.6% had asthma, 65.4% had allergic rhinitis, 16.7% had atopic dermatitis and 1.7% had urticaria.Conclusion. Food allergen hypersensitivity may be an important marker of inhaled allergen-induced respiratory allergy in later childhood.

Keywords:

• food hypersensitivity
• allergy
• asthma
• children
• allergens

Introduction

Food allergy (FA) may present with a variety of respiratory tract symptoms that generally involve IgE antibody-mediated responses. Exposure is typically through ingestion, but in some cases, inhalation of airborne food particles may trigger these reactions (James, 2003). Asthma may develop in about 5% of individuals who suffer from FA, and current asthma may be triggered by foods in among 6–8% of children and 2% of adults (Ozol & Mete, 2008). In a review of the literature, self-reported FA is an independent risk factor for potentially fatal childhood asthma, and asthmatic children or adolescents with FA are a target population for more aggressive asthma management (Vogel, Katz, Lopez, & Lang, 2008). Food allergy more often occurs in children with asthma and concomitant skin and gastrointestinal (GI) disorders than in those with only asthma. The diagnosis of possible concomitant FA should be considered in children with asthma (Krogulska, Wasowska-Krolikowska, & Trezezwinska, 2007). Furthermore, children with asthma and who are allergic to food present with some particular features, such as atopic dermatitis (AD) and a related significantly elevated total serum IgE level. Alternatively, FA may occur in patients who are sensitive to many allergens, including food (Businco, Falconieri, Giampietro, & Beilioni, 1995). Moreover, it has been shown that sensitisation to food allergens early in life is a risk factor for sensitisation to inhalant allergens and respiratory symptoms later on, especially in chronic rhinitis (Baena-Cagnani & Teijeiro, 2001; Heiner, 1984). Wang, Visness, and Sampson (2005) proposed that children sensitised to foods had higher rates of asthma hospitalisation and required more steroid medications than did control groups. Sensitisation to foods also correlated with sensitisation to more indoor and outdoor aeroallergens. (Wang et al., 2005). Therefore, we carried out this study to determine whether food allergen sensitivity is a marker for asthma incidence.

Methods

Previous studies have suggested that high concentrations of food-specific IgE antibodies are predictive of food-induced clinical symptoms (Sampson & Ho, 1997). In the current study, 1010 six- to eight-year-old (637 males and 373 females) grade 1 and grade 2 primary school children were enrolled. A Phadia ImmunoCAP system (Phadia AB, Sweden), Phadiatop Infant and radioallergosorbent test (RAST) were used to detect IgE antibodies to allergens in 54 kinds of food in the regular diet in Taiwan. Each participant was screened by telephone interview for doctor-diagnosed allergic rhinitis, asthma, AD and self-reported food allergy.

The Statistical Package for the Social Sciences (SPSS™ version 12 for Windows™, SPSS, Inc., Chicago, IL, USA) computer software was used for statistical analysis. A p value <0.05 was considered statistically significant.

Results

The Phadiatop Infant screening test for mixed food allergens showed milk, egg and meat mix (11.6%), fruit mix (10.25%) and nut mix (6.48%) (Table 1). Interestingly, a high percentage of males than females were sensitive overall. The most prevalent hypersensitivity was to sea food allergen, especially scallop, abalone and lobster. The next most prevalent hypersensitivity was to casein and alpha-lactalbumin, followed by garlic (Table 2a, b). Among the meat allergens, pork was the most common sensitising allergen (7.92%) (Table 3). Interestingly, a larger proportion of males than females were hypersensitive to some fruit allergens including cherry, strawberry, pear, lemon, plum and mango, while a larger proportion of females than males were sensitive to other fruit allergens (Table 4). Less than 1% of subjects were hypersensitive to cereals, nuts and vegetables. Finally, the common food allergens in the diet including scallop, abalone, lobster, oyster, alfa-lactalbumin, casein, pork and octopus which showed moderate probability of food allergen reaction by RAST testing (above class 2, specific-IgE 0.7 and 5 ku/L) were the most hyperallergenic foods (Table 5).

Table 1. Incidence of reactions of mixed food allergens among school children.

	Nut mix 1	Milk and Egg and Meat mix 10	Starch mix 12	Cereal mix 3	Vegetable mix 14	Fruit mix 16	Fruit mix 30	Fruit mix 31
Positive no. (male)	44	78	27	31	21	42	63	20
Positive%	4.36	7.72	2.67	3.07	2.08	4.16	6.24%	1.98%
Positive no. (female)	26	41	17	23	17	28	46	11
Positive%	2.57	4.06	1.68	2.28	1.68	2.27	4.55%	1.09%
Notes: Nut mix 1 includes peanut, hazel nut, Brazil nut, almond and coconut.
Milk and egg and meat mix 10 includes pork, beef, egg yolk, chicken and turkey meat.
Starch mix 12 includes rye, rice, potato, mushroom and pumpkin.
Cereal mix 3 includes wheat, oat, maize, sesame seed and buckwheat.
Vegetable mix 14 includes tomato, spinach, cabbage and paprika.
Fruit mix 16 includes strawberry, pear, lemon and pineapple.
Fruit mix 30 includes kiwi, mango, banana, avocado and papaya.
Fruit mix 31 includes apple, pear, peach, cherry and plum.

Table 2. Prevalence of common food allergens in school children.

A	Clam	Squid	Oyster	Scallop	Abalone	Lobster	Garlic	Cacao	Goat milk	Cheese, cheddar type	Onion
Positive no. (male)	34	17	66	156	162	125	74	3	61	38	10
Positive%	3.37	1.68	6.53	15.45	16.04	12.38	7.33	0.30	6.04	3.76	0.99
Positive no. (female)	14	6	34	95	91	50	43	0	47	25	6
Positive%	1.39	0.59	3.37	9.41	9.01	4.95	4.26	0	4.65	2.48	0.59
B	Celery	Pistachio	Litchi	Melon	Bamboo shoot	Pacific squid	Octopus	Grape	Casein	alpha- lactalbumin	beta-lactoglobulin
Positive no. (male)	11	14	23	14	9	47	48	4	80	90	38
Positive%	1.09	1.39	2.28	1.39	0.89	4.65	4.75	0.00	7.92	8.9*1	3.76
Positive no. (female)	7	8	11	10	3	22	28	3	54	56	30
Positive%	0.69	0.79	1.09	0.99	0.30	2.18	2.77	0.30	5.35	5.54	2.97
Note: *Scallop, abalone, lobster, casein, alpha-lactoalbumin.

Table 3. Prevalence of meat allergens in the diets of school children.

	Pork	Beef	Egg yolk	Chicken	Turkey meat
Positive no. (male)	52	5	9	10	5
Positive%	5.15	0.50	0.89	0.99	0.50
Positive no. (female)	28	4	13	5	0
Positive%	2.77	0.40	1.29	0.50	0.00

Table 4. Prevalence of fruit allergens in the diets of school children.

	Strawberry	Pear	Lemon	Pineapple	Kiwi	Mango	Banana	Avocado	Papaya	Apple	Peach	Cherry	Plum
Positive no. (male)	7	5	7	22	27	5	23	16	13	0	5	9	6
Positive%	0.69	0.50	0.69	2.18	2.67	0.50	2.28	1.58	1.29	0.00	0.50	0.89	0.59
Positive no. (female)	6	6	6	18	26	3	26	15	14	0	4	5	4
Positive%	0.59	0.59	0.59	1.78	2.57	0.30	2.57	1.49	1.39	0.00	0.40	0.50	0.40

Table 5. Severity of the common food allergenic reaction in school children.

	Oyster	Scallop	Abalone	Lobster	Octopus	Casein	Alpha-lactalbumin	Beta-lactoglobulin	Pork	Sesame seed	Pineapple	Kiwi	Banana
Above class 1* Positive%	10.25	25.68	25.32	17.08	7.42	13.19	14.13	6.36	7.89	2.00	3.42	4.71	4.71
Above class 2* Positive%	6.71	19.55	19.20	10.84	4.95	4.95	6.48	2.59	6.24	1.41	1.30	3.18	1.65
RAST class	Range IU/ml	Level of specific lgE antibody
6	>Std 100	Very high
5	Std 100–50	Very high
4	Std 50–17.5	Very high
3	Std 17.5–3.5	High
2	Std 3.5–0.7	Moderate
1	Std 0.7–0.35	Low
0	<Std 0.35	Absent or undetectable
*Significant of class

Discussion

The burden of allergic diseases, especially asthma, is high. In non-atopic healthy individuals, tolerance to allergens appears to be induced by allergen-specific regulatory T-cells. Food tolerance induction might be an important target for allergic diseases prevention (von Hertzen et al., 2009). A subset of food-allergic patients respond to food allergens by developing GI tract symptoms and asthmatic reaction. CD4+ T cells from mesenteric lymph nodes from mice with allergen-induced immediate-type hypersensitivity reactions in the gut have been shown to carry the experimental asthma phenotype (Ozdemir et al., 2007). Food allergen intolerance is, thus, a possible cause of allergic inflammation and thereby respiratory allergy. Elimination of the underlying cause – food allergen intolerance – may also eliminate respiratory hyperreactivity.

Food allergy has variety of clinical presentations, including IgE and non-IgE food allergy, as well as mixed IgE and non-IgE disorders. Also, eosinophilic diseases of the GI tract with occasional IgE-type sensitisation are increasingly recognised (Eigenmann et al., 2008). Leading allergens in foodstuffs are glycoproteins having molecular weights between 10,000 and 60,000 (Richter, 2005). In addition, these glycoproteins usually retain their allergenicity after heating and/or proteolysis (Ebo & stevens, 2001). The symptoms of IgE-mediated allergy usually manifest within a few minutes to two hours after ingestion of the offending food and take the form of tingling and itching, tissue swelling in the mouth, hoarseness, asthma, GI complaints, acute urticaria or even anaphylactic shock (Richter, 2005). Milk, soy, egg, wheat and peanut allergies are the most common allergies in children, whereas peanut, tree nut, fish, shell fish allergies and allergies to fruits and vegetables are the most common ones in adults. Because the majority of patients outgrow their allergies to milk, soy, egg and wheat, and some also to peanut, therefore, patients should be periodically reassessed (Ramesh, 2008). Morisset et al. (2003) reported that respiratory symptoms were observed in 12%, 20%, 10% and 42% of egg, peanut, milk and sesame allergies, respectively. The study by Vogel et al. (2008) showed that 13% of patients who died of childhood asthma had at least one food allergy, with egg, peanut, fish/shellfish, milk and tree nut accounting for 78.6% of all food allergies (Vogel et al., 2008). The study also pointed out that self-reported food allergy is an independent risk factor for potentially fatal childhood asthma. Coexisting asthma is a significant problem, as food reactions tend to be more severe when they involve the lungs. Moreover, patients with allergies to more than one food have increased asthma hospitalisations, emergency department visits and use of oral steroids (Berns et al., 2007).

In conclusion, children with asthma and a history of AD and/or elevated total serum IgE levels should be carefully assessed for FA, and asthmatic children or adolescents with food allergy are a target population of more aggressive asthma management. In addition, self-reported allergy to foods was associated with a worse outcome. Food allergen hypersensitivity, especially to multiple food allergens, may signal that the avoidance of offending foods should be part of a total asthma control program in some cases.

Acknowledgements

The authors gratefully thank the Affiliate of Phadia Diagnostics Taiwan for assistance in the technology of the detection of allergen-specific IgE antibodies.