Interaction of fungal spores with the lungs: Distribution and retention of inhaled puffball (Calvatia excipuliformis) spores

Abstract

Background: The biologic responses to inhaled airborne fungal spores, which are well-known allergen carriers, would be better understood if we had an insight into their pattern of distribution and interaction with lung structures. Objectives: To investigate the retention characteristics of inhaled basidiospores, which often represent the major portion of the spore load in air-sampling surveys and to analyze their regional distribution within and interaction with the lungs. Methods: Intubated and anesthetized Syrian Golden hamsters inhaled aerosols of puffball (Calvatia excipuliformis ) spores, with an aerodynamic diameter of 3.1 μm, either by spontaneous breathing (group A, n = 3) or by continuous negative-pressure ventilation (group B, n = 4). Lungs were fixed by intravascular perfusion of fixative solution within 29 minutes of the initial inhalation, and tissue samples were then processed for light and electron microscopy. Results: Stereological (fractionator) analysis of lung tissue revealed that the greatest number of spores was deposited within the alveoli (67.2% in group A and 89.8% in group B). The intrapulmonary conducting airways retained an intermediate proportion (32.3% in group A and 10.0% in group B), whereas the extrapulmonary mainstem bronchi and trachea held the lowest proportion (0.5% or less). Deposited spores were lodged within the aqueous lining layer and in close proximity to the epithelial cells. Within the intrapulmonary conducting airways, 22.3% of the spores in group A and 9.0% of those in group B had been engulfed by macrophages. Conclusion: This study demonstrates that inhaled 3-μm-diameter basidiospores become distributed over a large surface area. It also reveals that such particles are displaced by surfactant (surface forces) into the aqueous lining layer of airways and alveoli, thereby facilitating subsequent phagocytosis by macrophages. This interaction of spores with lung structures may be important for the development of respiratory allergies induced by airborne fungal allergens. (J Allergy Clin Immunol 2000;106:92-100.)