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Clinical implications of cross-reactive foodallergens

As a consequence of the general increase in allergic sensitization, the prevalence of hypersensitivityreactions to multiple foods that share homologous proteins has become a significant clinical problem .A variety of these allergens conserved among plants (eg, profilin and lipid transfer proteins) andanimals (eg, tropomyosin and caseins) have been characterized . Although studies with molecularbiologic techniques have elucidated the nature of these ubiquitous allergens , clinical studies havelagged behind . The physician is called on to determine the risk of reaction to related foods amonglegumes, tree nuts, fish, shellfish, cereal grains, mammalian and avian food products, and a variety of other plant-derived foods that may share proteins with pollens, latex, and each other. Clinicalevaluations require a careful history, laboratory evaluation, and in some cases oral food challenges. Thepitfalls in the evaluation of food allergy unreliable histories and limitations in laboratory assessment

primarily caused by false-positive skin prick test responses/RAST results are magnified when dealingwith cross-reactive proteins. This review focuses on the clinical data regarding cross-reacting foodallergens with the goal of providing a background for improved risk assessment and a framework onwhich to approach these difficult clinical questions. (J Allergy Clin Immunol 2001;108:881-90.)

Food allergen sensitization in inner-citychildren with asthma- The Journal of Allergyand Clinical Immunology Volume 115, Issue 5 , Pages 1076-1080, May2005Background

Asthma continues to be an increasing cause of morbidity in the pediatric population, andstudies have shown an association between food sensitivity and asthma.

Objective

We investigated the degree of food allergen sensitization in inner-city patients with asthma.
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Methods

Five hundred four random serum samples from the National Cooperative Inner City AsthmaStudy were evaluated for specific IgE (UniCap) to 6 common food allergens (egg, milk, soy,

peanut, wheat, and fish). Statistical analyses were performed to determine food sensitization

prevalence and its association with asthma morbidity.

Results

Forty-five percent of patients had evidence of sensitization (food- specific IgE 0.35 kU/L) to atleast 1 food. Nineteen percent had IgE levels at 50% positive predictive value for clinicalreactivity to at least 1 food, with 4% of patients having levels >95% positive predictive value for food allergy. Children sensitized to foods had higher rates of asthma hospitalization ( P < .01)and required more steroid medications ( P = .025). Sensitization to foods also correlated withsensitization to more indoor and outdoor aeroallergens ( P < .001).

Conclusion

Food allergen sensitization is highly prevalent in the inner-city population with asthma, and it isassociated with increased asthma healthcare and medication use. Therefore, food allergensensitivity may be a marker for increased asthma severity.

Key words: Asthma , food allergy , sensitization , IgE, inner-city children

Abbreviation used: NCICAS , National Cooperative Inner City Asthma Study

Asthma is a highly prevalent disease and a significant cause of morbidity and mortality in the pediatric population, especially in the inner city .1 Approximately 12% of children in the UnitedStates had a diagnosis of asthma in 2002 .2 Studies have shown an association between foodsensitivity and the development and exacerbation of asthma. In fact, it is estimated that 4% to 8%of patients with asthma have coexistent food allergy .3 Although the true prevalence of asthmacaused by food allergy is unknown, it is estimated that food-induced respiratory symptoms occur in approximately 2% to 29% of children with asthma 4, 5, 6, 7 on the basis of respiratorysymptoms observed during food challenges.

A case-controlled study by Roberts et a l3 showed that food allergy is also an independent risk

factor for life-threatening asthma. Of the 19 ventilated children in the study, 52.6% hadsensitization to a food allergen, compared with only 13.2% of controls who were evaluated in theemergency department for milder exacerbations.

Because there appears to be a link between food sensitization and asthma, and the true prevalence of food allergy in the population with asthma is unknown, we undertook this study todetermine the prevalence of food allergen sensitization in an inner-city asthma population and toassess its association with asthma symptoms and healthcare utilization.
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Back to Article Outline

Methods

Five hundred four random serum samples from the National Cooperative Inner City Asthma

Study (NCICAS) were obtained. The NCICAS study included children 4 to 9 years old withasthma who were recruited from emergency departments and clinics in inner-city areas in theUnited States .8, 9 Baseline assessments included demographics, health history, access to care,environmental factors, and asthma symptoms. Information regarding medications and healthcareutilization was recorded on the basis of 3-month recall. Data was not obtained regarding foodallergy diagnoses or reactions. This information was collected at baseline and at 3-month intervalassessments for 12 months. Skin prick testing to 13 indoor and outdoor environmental allergenswas performed during enrollment in the NCICAS study.

The serum samples were evaluated for specific IgE (UniCap system; Pharmacia Diagnostics,Uppsala, Sweden) to the 6 most common food allergens: egg, milk, soy, peanut, wheat, and

fish .10

On the basis of the specific IgE levels to individual foods, the subjects were divided into 4groups. Group 1 had food-specific IgE levels that had >95% predictive value for food allergy ,11 group 2 was considered to have possible food allergy (food specific IgE 0.7 kU/L), group 3 hadany sensitization to foods (food specific IgE 0.35 kU/L), and group 4 had no evidence of I gE-mediated food allergy (food specific IgE < 0.35 kU/L).

Comparisons between food sensitization and morbidity measures were made by analysis of variance of mean outcomes, and a P value < .05 was considered significant.


Results

Characteristics of the NCICAS participants

Five hundred four samples were tested for specific IgE to 6 food allergens. Both the sensitizedgroup (groups 1-3) and the nonsensitized group (group 4) had an age range of 4 to 9 years andmedian age of 6 years. There was a similar sex distribution in both groups (62.4% male subjectsin the sensitized group and 63.9% male subjects in the nonsensitized group). The racedistribution was also similar in the sensitized and nonsensitized groups with 12% Hispanic, 82%

black, and the remaining indicating white or other. Sensitization to foods significantly correlatedwith more indoor and outdoor aeroallergen sensitization ( P < .001). Sensitization to soy, wheat,

or peanut had significant correlations with sensitization to the highest number of aeroallergens,with strongest correlations with molds and outdoor allergens (Table I ). Indeed, studies havedemonstrated cross-reactivity between peanut and wheat with grass pollen proteins .12, 13 Egg,milk, or fish sensitization correlated with the least number of aeroallergen sensitization.

Table I. Correlation of food sensitization with environmental allergen sensitization

Egg Milk Soy Wheat Peanut Fish
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Dermatophagoides pteronyssinus

.465 (0.034)

.586(0.026)

.030 (0.102) .022 (0.022) .003 (0.137) .011(0.120)

Dermatophagoides farinae .882(0.007)

.255(0.053)

.023 (0.107) .018 (0.111) .008 (0.125) .007(0.126)

Cat .691 (0.019) .408(0.039)

.003 (0.139) .033 (0.100) .061 (0.088) .533 (0.09)

Dog .013 (0.117) .0001(0.139)

.011 (0.120) .019 (0.110) .0006(0.159)

.808(0.011)

Rat .0002

(0.174)

.008

(0.125)


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Numbers indicate P values, with Pearson correlation coefficients in parentheses. Boldfacingindicates significant P value ( 0.35 kU/L).Four percent of patients had food- specific IgE levels that had a 95% positive predictive valuefor food allergy and were categorized in group 1. Twenty-six percent of the children had

probable food allergy (group 2), and 14% were sensitized to foods but were unlikely to bereactive (group 3). Fifty-five percent of the children enrolled were not sensitized to any of the 6foods (group 4). The breakdown of sensitization in groups 1 to 3 based on specific food IgElevels is shown in Table II .

Table II. Specific IgE levels to the most common food allergens

Food Number sensitized ingroups 1-3 (n = 227)

Number of patients with >95%positive predictive level

Median specificIgE (kU/L)

Range of specificIgE (kU/L)

Egg 75 (15%) 10 0.66 0.35-32.3

Milk 115 (23%) 5 0.78 0.35 to >100

Fish 40 (8%) 4 1.20 0.36 to >100

Peanut 85 (17%) 14 1.10 0.35 to >100

Soy 77 (15%) 2 1.10 0.36 to >100

Wheat 118 (23%) 3 0.93 0.36-81.3

Patients with food allergy to egg and peanut had the highest food-specific IgE levels, with 13%of egg-sensitized patients and 16% of peanut-sensitized patients having greater than 95%

positive predictive values. These data suggest that sensitization to these foods may be morehighly correlated with asthma morbidity. Egg and peanut are frequent ingredients in a variety of foods, increasing the chance for inadvertent exposures and reactions in individuals with allergy.

Food sensitization and asthma morbidity

Children with asthma who were sensitized to at least 1 food (groups 1-3) had a higher rate of hospitalization ( P < .01) and required more steroid medications ( P = .025) than nonsensitizedindividuals (Table III ). There was a trend for needing more medications in general in thesensitized group ( P = .06). There was no significant difference in quality of life, healthcareutilization, and medication use when comparing those with specific IgE levels at high positive
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predictive values for food allergy (group 1) with group 4; however, the lack of significance may be caused by small sample numbers in group 1.

Table III. Morbidity differences between food allergen sensitized patients with asthma comparedwith nonsensitized patients with asthma (groups 1-3 vs group 4)

Group Mean SE ANOVA P value

Maximum symptom days 1-3 3.99 0.22 .753

4 3.90 0.20

Wheeze 1-3 3.50 0.19 .535

4 3.34 0.17

Emergency department visits 1-3 0.22 0.03 .243

4 0.18 0.03

Unscheduled visits (emergency department + clinic) 1-3 0.42 0.04 .289

4 0.36 0.04

Hospitalizations 1-3 0.10 0.01 .001

4 0.04 0.01

Number of medications 1-3 1.87 0.09 .060

4 1.65 0.08

Number of steroid medications 1-3 0.40 0.04 .025

4 0.28 0.03

Boldfacing indicates significant P value (


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sensitized to multiple foods. More importantly, sensitization to more than 1 food was associatedwith increased hospitalization for asthma (Table IV ).

Table IV. Sensitization to more than 1 food is associated with increased asthma morbidity

Groups 1-3 (>1

food) Group 4

Groups 1-3 (1

food)

Emergency department visits

0.22 (0.04 ) 0.18(0.03)

0.21 (0.04)

P = .304 P =.446

Unscheduled visits (emergency

department + clinic)

0.44 (0.05) 0.36(0.04)

0.40 (0.06)

P = .446 P =.570

Hospitalizations

0.12 (0.02) 0.04(0.01)

0.07 (0.02)

P =.0003

P =.110

Number of medications

1.92 (0.11) 1.65

(0.08) 1.78 (0.13)

P = .053 P =.398

Number of steroid medications

0.39 (0.05) 0.28(0.03)

0.41 (0.06)

P = .078 P =.067

Numbers indicate mean value, with SE in parentheses. Boldfacing indicates significant P value(


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emergency department visits and hospitalizations and had increased medication use (Table V ).Sensitization to fish was correlated with higher medication use and increased visits to theemergency department or to their clinics.

Table V. Sensitization to specific foods is associated with increased asthma morbidity

Sensitized toegg vs group4 ANOVA P

values

Sensitized tomilk vsgroup 4

ANOVA P values

Sensitized tofish vs group4 ANOVA P

values

Sensitized topeanut vsgroup 4

ANOVA P values

Sensitized tosoy vs group4 ANOVA P

values

Sensitized towheat vsgroup 4

ANOVA P values

Emergencydepartment visits

.270 .564 .015 .177 .027 .208

Unscheduled visits

(emergencydepartment +clinic)

.145 .406 .034 .272 .228 .344

Hospitalizations .002 .090 .178 .0002 .0005 .0002

Number of medications

.510 .457 .008 .017 .011 .081

Number of steroidmedications

.651 .370 .079 .060 .086 .026

Boldfacing indicates significant P value (


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Although 45% of patients in our study were sensitized to at least 1 food, we could not determinethe true prevalence of food allergy in this population, because this would require double-blind

placebo-controlled food challenges. Unfortunately, these food challenges cannot be performed because this was a study performed on anonymous serum samples. In addition, the diagnosis of food allergy was not known in any of these patients. Nevertheless, our random sample included

31% of children with serum specific IgE levels 0.7 kU/L, suggestive of a possible food allergy.Even if half of these patients had clinical reactivity to foods, the prevalence of food allergy inthis group would be much higher than the general population. Furthermore, the median age of our patient population was 6 years, an age at which many children already would have outgrowntheir egg and milk allergies, possibly underestimating the prevalence of food sensitization. Thus,we predict that in general, children with asthma in the inner city are more likely to have foodallergy than the general population, as reported in other series of children with asthma .5, 14, 15

We next determined the effect of food sensitization on asthma severity. Patients with asthmawho had at least 1 food sensitization (groups 1-3) were more likely to be hospitalized andrequired more steroid medications than patients with asthma without food sensitization. There

was also a trend for increased asthma medication use overall ( P

= .060). No significantdifferences were noted between patients with the highest specific IgE levels (group 1) and patients with asthma not sensitized to food (group 4), possibly because of the small sample sizeinvolved (23 patients in group 1). However, patients who were sensitized to more than 1 foodhad significantly more hospitalizations and required more asthma medications than those with asingle food sensitization. We were able to demonstrate a trend suggesting a more significant rolefor fish and soy in increased asthma morbidity (Table IV ). Together, these findings support theconcept that food sensitization is a marker of more severe asthma morbidity.

The exact role of food allergens in the pathophysiology of asthma has not been elucidated,although a link between the 2 has been established. Asthma is the most common respiratorysymptom of food-induced anaphylaxis, but it is rarely an isolated symptom; it usually occurs inassociation with other clinical manifestations such as cutaneous or gastrointestinal symptoms .4 The study by Bock 16 found that nearly half of patients with asthma with positive food challengeshad food-induced wheezing, but only 7% had wheezing as the only symptom. A cohort study of children allergic to peanut observed that 4 out of 46 (9%) died of asthma exacerbation, a higher fatality risk than for any high-risk asthma population, which supports the hypothesis that food isa risk factor for fatal asthma .17 Conversely, asthma has been identified to be a risk factor for fatalor near-fatal food-induced anaphylaxis .18 It is clear that an intimate link exists between asthmaand food allergy. However, our study is the first to demonstrate a correlation between foodsensitization and the severity of symptoms related to asthma on its own.

The prevalence of food sensitization, and likely food allergy, is increased in patients with asthmaand is associated with increased healthcare utilization and medication use. The presence of foodsensitization is thus a helpful marker for increased asthma severity. Although true food allergycould not be tested in our patients, food sensitization is easier to determine, requiring simply aserum sample from the patient. On the basis of our data, caretakers should consider screening

patients with moderate to severe asthma whose disease is not well controlled with standardasthma medications. Future studies may help elucidate the role of specific food sensitizations inasthma morbidity as well as in sensitization to specific environmental allergens. It may also be
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interesting to determine whether specific food avoidance in sensitized individuals would behelpful in selected populations with asthma.


We thank Pharmacia Diagnostics for providing us with the reagents for detection of food specificIgE.


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The National Cooperative Inner-City Asthma Study was supported by grants UOI A1-30751,A1-30752, A1-30756, A1-30772, A1-30773-01, A1-30777, A1-30779, A1-30780, and N01-A1-15105 from the National Institutes of Allergy and Infectious Disease (National Institutes of Health, Bethesda, Md).Disclosure of potential conflict of interest: H. A. Sampson has consultant

arrangements with Seer Pharmaceutical, LLC, and has received grants/research support from the National Institutes of Health and Pharmacia Diagnostics.

PII: S0091-6749(05)00369-6

doi:10.1016/j.jaci.2005.02.014

2005 American Academy of Allergy, Asthma and Immunology. Published by Elsevier Inc. Allrights reserved.
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