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Allergic Bronchopulmonary Aspergillosis

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Allergic Bronchopulmonary Aspergillosis Allergic Bronchopulmonary Aspergillosis Karen Patterson1 and Mary E. Strek1 1Department of Medicine, Section of Pulmonary and Critical Care Medicine, The University of Chicago, Chicago, Illinois Allergic bronchopulmonary aspergillosis (ABPA) is a complex clinical type of pulmonary disease that may develop in response to entity that results from an allergic immune response to Aspergillus aspergillus exposure (6) (Table 1). ABPA, one of the many fumigatus, most often occurring in a patient with asthma or cystic forms of aspergillus disease, results from a hyperreactive im- fibrosis. Sensitization to aspergillus in the allergic host leads to mune response to A. fumigatus without tissue invasion. activation of T helper 2 lymphocytes, which play a key role in ABPA occurs almost exclusively in patients with asthma or recruiting eosinophils and other inflammatory mediators. ABPA is CF who have concomitant atopy. The precise incidence of defined by a constellation of clinical, laboratory, and radiographic ABPA in patients with asthma and CF is not known but it is criteria that include active asthma, serum eosinophilia, an elevated not high. Approximately 2% of patients with asthma and 1 to total IgE level, fleeting pulmonary parenchymal opacities, bronchi- 15% of patients with CF develop ABPA (2, 4). Although the ectasis, and evidence for sensitization to Aspergillus fumigatus by incidence of ABPA has been shown to increase in some areas of skin testing. Specific diagnostic criteria exist and have evolved over the world during months when total mold counts are high, the past several decades. Staging can be helpful to distinguish active disease from remission or end-stage bronchiectasis with ABPA occurs year round, and the incidence has not been progressive destruction of lung parenchyma and loss of lung definitively shown to correlate with total ambient aspergillus function. Early recognition allows treatment with corticosteroids, spore counts (1, 7). There is no gender predilection noted. which are effective but may be required indefinitely. There is some evidence to support the use of newer antifungal azoles as cortico- steroid-sparing agents. Patients must be followed closely for re- PATHOPHYSIOLOGY current disease. ABPA should be considered in all patients with The pathophysiology of ABPA is complex. In an allergic host, asthma or cystic fibrosis, but especially in those with difficult to the persistence of A. fumigatus in the lung leads to T lympho- control disease. cyte activation, cytokine, and immunoglobulin (Ig) release and Keywords: allergic bronchopulmonary aspergillosis; ABPA; asthma; inflammatory cell recruitment. Local inflammation results in cystic fibrosis; aspergillus mucus production, airway hyperreactivity, and ultimately bron- chiectasis. Allergic bronchopulmonary aspergillosis (ABPA) is an indolent A viscous mucus layer in the airway, combined with dys- and potentially progressive disease resulting from a hypersensi- functional clearance in the case of CF, may disrupt the natural tivity response to persistent Aspergillus fumagatus in the airways. process of effective spore removal (2, 8). Aspergillus proteolytic Advances have been made in our understanding of the role of products may also interfere with airway clearance by damage to the allergic response in the pathophysiology of this disease (1, 2). and disruption of the epithelial cell barrier (4, 9). Once resident, ABPA occurs most commonly in patients with asthma or cystic aspergillus germinates and proliferates, and antigen burdens can fibrosis (CF), especially those with coexisting atopy (3, 4). become high. Dendritic cells are local antigen-presenting cells Patients present with symptoms that may be attributed to their that process spore and mycelia antigens. This processing leads underlying disease; therefore, considering ABPA in these patient to the release of specific cytokines by antigen-presenting cells populations is important. Therapy is directed at mitigating the and to antigen presentation to T lymphocytes (10). In the allergic inflammatory response (5). Early diagnosis and treatment normal host, the response to antigen presentation is activation has been thought to prevent disease progression, parenchymal of nonallergic T helper (Th)1 and allergic (Th2) lymphocytes damage, and loss of lung function. In this review we highlight (10, 11). The Th1 response is marked by macrophage and salient clinical features and the current understanding of the neutrophil cytotoxic action as well as IgG and IgA antibody pathophysiology of ABPA and review treatment options. production, which may protect against aspergillus infection (12). A frank defect in the Th1 cytotoxic pathway is not present in BACKGROUND AND EPIDEMIOLOGY ABPA, although it is present in immunocompromised patients who are at risk for invasive disease. Activation of the Th2 Aspergillus is a fungus that is found throughout the world. Its pathway results in specific cytokine and immunoglobulin elab- spores are hardy and ubiquitous, thriving in moist, organic oration that mediate allergic inflammation. Th2 signaling pre- materials. Aspergillus can be cultured from outdoor and indoor dominates in the aspergillus allergic host; the imbalance of the environments and grows optimally at core body temperature Th2 over the Th1 response is thought to drive ABPA (1, 4). (1). Spores are tiny and easily aerosolized and deposit in distal Although the Th2 response predominates in patients with and terminal airways, where they germinate if the airway allergy to aspergillus and in patients with ABPA, the magnitude environment is favorable. Aspergillus is variably pathogenic in of the Th2 immune activation is greatest in ABPA (12). humans. Host characteristics are a major determinant of the Activated Th2 cells release specific cytokines that orches- trate downstream cell signaling and the inflammatory response (11). IL-4 may be especially important. It is linked to B-cell isotype conversion to IgE production, the expression of vascular (Received in original form August 10, 2009; accepted in final form September 8, 2009) cell adhesion molecules on endothelial cells and vascular cell Correspondence and requests for reprints should be addressed to Mary E. Strek, adhesion molecule ligands on eosinophils, and to IgE and IgA M.D., The University of Chicago, Department of Medicine – MC7076, Chicago, Fc receptor expression on eosinophils (7, 12). When bound to IL 60637. E-mail: [email protected] aspergillus antigen, locally produced IgE may activate mast Proc Am Thorac Soc Vol 7. pp 237–244, 2010 DOI: 10.1513/pats.200908-086AL cells. Mast cell chemokines, in concert with IL-5, recruit Internet address: www.atsjournals.org eosinophils. Eosinophils are the most conspicuous immune cells 238 PROCEEDINGS OF THE AMERICAN THORACIC SOCIETY VOL 7 2010 TABLE 1. PULMONARY MANIFESTATIONS OF ASPERGILLUS ABPA in CF Disease Host Patients with CF are at risk for developing ABPA (4). The prevalence of ABPA is increased in patients with CF who are Aspergilloma Cavity from sarcoid, previous TB, male, are adolescent, have lower lung function, have a history of bullae, or bronchiectasis Allergic bronchopulmonary Asthma, cystic fibrosis wheezing or asthma, or have pseudomonas in the sputum. aspergillosis Atopy is present in up to 60% of patients with CF (4). The Chronic necrotizing COPD, previous TB, corticosteroids, DM impaired airway clearance characteristic of CF may contribute aspergillosis directly to ABPA, although other factors likely play a role as Invasive aspergillosis Immunocompromised, especially well (25, 26). neutropenia Hypersensitivity pneumonia Intense or repeated exposure to aspergillus CLINICAL FEATURES Definition of abbreviations: COPD 5 chronic obstructive pulmonary disease; Symptoms DM 5 diabetes mellitus; TB 5 tuberculosis. With the development of ABPA, asthma or CF typically worsens and may manifest with a new or worsening cough or in airway mucosa in patients with ABPA and are thought to be an increase in sputum production or wheezing. Thick mucus a major effector of inflammation (12, 13). Degranulation of production is common; mucus can be remarkably tenacious and activated mast cells and eosinophils results in the release of resistant to suctioning (27). Patients may cough up well-formed, mediators of vasodilation and bronchoconstriction (12). tan to brownish-black mucus plugs. Plugs are composed of de- Activated T and B lymphocytes infiltrate lymphatics and generating eosinophils, desquamated epithelial cells, and mucin release cytokines systemically. Circulating IL-4 is thought to (28). Hemoptysis may occur secondary to airway inflammation drive total IgE production, and total serum IgE levels are and bronchiectasis; however, massive hemoptysis from ABPA increased out of proportion to aspergillus-specific IgE levels (7). alone is not well described in the literature (5, 29). Systemic IgE and IgG antibodies specific for aspergillus circulate system- symptoms of low-grade fever, malaise, and weight loss are ically as well (14). variably part of the clinical spectrum of ABPA (16). These symptoms should trigger an evaluation for ABPA in a patient with asthma or CF. HOST CHARACTERISTICS Susceptibility to ABPA is likely mediated by genetically de- Laboratory Evaluation termined inflammatory responses in atopic patients. Although Total serum IgE levels of at least 1,000 IU/ml are a hallmark of atopy is an inheritable trait, familial occurrence of ABPA, ABPA (2). A. fumigatus–specific IgE levels are also elevated though reported,
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