A comparison of the airway response to segmental antigen bronchoprovocation in atopic asthma and allergic rhinitis

doi:10.1067/mai.2003.28

Journal of Allergy and Clinical Immunology

Volume 111, Issue 1, January 2003, Pages 79-86

https://doi.org/10.1067/mai.2003.28 Get rights and content

Abstract

Background: Patients with allergic asthma and those with allergic rhinitis (without asthma) share many immunopathologic features but differ in the presence of lower airway symptoms in response to antigen. Objectives: We sought to compare the airway inflammatory response to antigen in patients with atopic asthma and allergic rhinitis. Methods: Segmental bronchoprovocation with saline or ragweed antigen was performed in 9 patients with atopic asthma and 9 patients with allergic rhinitis without asthma. The antigen dose used in segmental bronchoprovocation was 10% of the dose that caused a 20% decrease in FEV₁ in response to inhalation challenge. Bronchoalveolar lavage (BAL) was performed from the saline- and antigen-challenged segments at 5 minutes and 48 hours after challenge. BAL fluid was analyzed for cell count and differential, distribution of lymphocytes, and concentration of soluble factors (histamine, IL-5, matrix me-talloproteinase 9, tissue inhibitor of metalloproteinase 1, and fibronectin). In addition, BAL cells were cultured ex vivo, and IL-5, IFN-γ, and IL-10 generation was measured. Results: Antigen challenge led to similar patterns of cellular recruitment, mediator levels, and BAL cell cytokine generation in both groups; however, the dose of antigen required to promote comparable responses in the airway was significantly less in patients with asthma. Conclusion: These data suggest that the pattern of acute airway inflammation in response to allergen does not by itself explain antigen-induced lower airway obstruction and asthma symptoms. We speculate that other factors, such as increased airway sensitivity to allergen or preexisting airway injury and remodeling, might explain why patients with asthma and rhinitis differ in their clinical and physiologic response to antigen exposure. (J Allergy Clin Immunol 2003;111:79-86.)

Section snippets

Subjects

Eighteen patients with ragweed allergy, 9 with mild asthma, and 9 with allergic rhinitis without asthma were recruited for the study (Table I). Selection criteria for asthma were in accordance with the American Thoracic Society guidelines⁹ and included a history of asthma and a methacholine PC₂₀ of less than 8.0 mg/mL. Patients with allergic rhinitis had a positive skin prick test response and a history of hay fever to ragweed, no history of asthma, normal pulmonary function, and normal airway

Subject characteristics

Asthmatic subjects (n = 9) had mild intermittent disease with normal spirometry results (FEV₁ >80%) and 12% or greater reversibility to inhaled β-agonist, increased airway hyperresponsiveness to methacholine, or both (Table I). Subjects with allergic rhinitis (n = 9) had normal spirometry results and no airway hyperresponsiveness to methacholine (PC₂₀ >8 mg/mL). The ragweed PD₂₀ was significantly lower among patients with asthma. Even with a lower antigen dose, patients with asthma had a

Discussion

Our findings demonstrate that the airways of patients with allergic rhinitis and asthma have a similar pattern of allergic inflammation in response to antigen provocation but that asthmatic patients are more sensitive (eg, the PD₂₀ was nearly 5-fold less in asthmatic patients compared with that in patients with rhinitis). Yet when the 2 groups were given physiologically equivalent doses of antigen (ie, 10% of the individual's antigen PD₂₀), airway inflammation was comparable. The 2 groups

Acknowledgements

We thank our research nurses, Ann Dodge, Mary Jo Jackson, Andrea Tweedie-Felgus, and Lisa Peronto, for patient recruitment and assistance with bronchoscopies; Raymond Rodriguez, Andy Cardoni, and Sarah Panzer for their technical expertise; and Dr Jacqueline Houtman for assistance with preparation of the manuscript.

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In other words, the upper and the lower airways are considered as a single functional entity that responds to the offending allergen with the same inflammatory processes.2 The concept of united airways is supported by numerous epidemiological surveys showing the frequent coexistence of allergic rhinitis (AR) and allergic asthma (AA) (for review, see Cruz et al3) and by mechanistic studies, showing that when 1 of the 2 districts is stimulated with an allergen, changes in the other district also occur.4,5 Whether a functional connection exists among upper and lower airways and upper digestive tract is unclear.
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^☆: Supported by National Institutes of Health grant RO1 64066, an institutional Specialized Center of Research grant (NIH HL56396), and the American Lung Association of Wisconsin.

^☆☆: Reprint requests: Elizabeth A. Becky Kelly, PhD, Section of Pulmonary and Critical Care Medicine, 600 Highland Ave, CSC K4/928, University of Wisconsin School of Medicine, Madison, WI 53792.

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Asthma, Rhinitis, Other Respiratory DiseasesA comparison of the airway response to segmental antigen bronchoprovocation in atopic asthma and allergic rhinitis☆,☆☆

Abstract

Section snippets

Subjects

Subject characteristics

Discussion

Acknowledgements

J Allergy Clin Immunol

J Allergy Clin Immunol

J Allergy Clin Immunol

J Allergy Clin Immunol

J Biol Chem

Immunobiology of asthma and rhinitis. Pathogenic factors and therapeutic options

Am J Respir Crit Care Med

Inflammatory and mechanical factors of allergen-induced bronchoconstriction in mild asthma and rhinitis

J Appl Physiol

Pulmonary inflammation after segmental ragweed challenge in allergic asthmatic and nonasthmatic subjects

Am J Respir Crit Care Med

Asthma, Rhinitis, Other Respiratory Diseases
A comparison of the airway response to segmental antigen bronchoprovocation in atopic asthma and allergic rhinitis☆,☆☆