Allergic Bronchopulmonary Aspergillosis (ABPA)

Epidemiology

  • History: ABPA was first described by Hinson in England in 1952 (Thorax, 1952) [MEDLINE]
  • Prevalence: ABPA is the most common cause of pulmonary eosinophilia in temperate climates (and probably the most common cause worldwide)
  • Age: ABPA is more common in adults than children
  • Sex: males are more commonly affected than females in only some reports
  • Season: some reports suggest more ABPA episodes in fall and winter (when Aspergillus spore counts are known to be high)
    • Intensity of Exposure: in a Chicago study, 80% of exacerbations occurred when mold counts were at their peaks

Diseases Associated with Allergic Bronchopulmonary Aspergillosis

  • Asthma (see Asthma, [[Asthma]])
    • ABPA Occurs in 1-5% (Some Studies Suggest Up to 28%) of Persistent Asthmatics
    • ABPA Occurs in 5-10% of Chronically Steroid-Dependent Asthmatics
    • Most Atopic Patients Have a History of Asthma Dating Back to Childhood, But Some Cases Do Not Manifest Asthma Until Years After the Diagnosis of ABPA
  • Chronic Granulomatous Disease (see Chronic Granulomatous Disease, [[Chronic Granulomatous Disease]])
    • Epidemiology: ABPA rarely occurs in patients with CGD
  • Cystic Fibrosis (CF) (see Cystic Fibrosis, [[Cystic Fibrosis]])
    • ABPA Occurs in 2-9% of Cystic Fibrosis Patients
  • Hyper IgE-Recurrent Infection Syndrome (Job’s Syndrome, Buckley-Job Syndrome) (see Hyper IgE-Recurrent Infection Syndrome, [[Hyper IgE-Recurrent Infection Syndrome]])
    • Epidemiology: ABPA rarely occurs in these patients
  • Lung Transplant (see Lung Transplant, [[Lung Transplant]])
    • Epidemiology: ABPA rarely occurs in lung transplant patients

Microbiology

Organisms Associated with Allergic Bronchopulmonary Mycosis (Crit Rev Microbiol, 2014) [MEDLINE]

  • Aspergillus Fumigatus (see Aspergillus, [[Aspergillus]]): most common etiology
    • Other Aspergillus Species (see Aspergillus, [[Aspergillus]])
      • Aspergillus Niger
      • Aspergillus Oryzae: associated with exposure in a soy sauce factory
      • Aspergillus Ochraceus
  • Candida Albicans (see Candida, [[Candida]])
    • Epidemiology: second most common etiologic organism (accounts for 60% of non-Aspergillus cases)
  • Bipolaris: accounts for 13% of of non-Aspergillus cases
  • Schizophyllum Commune: accounts for 11% of non-Aspergillus cases
  • Curvularia: accounts for 8% of non-Aspergillus cases
  • Scedosporium (Pseudallescheria Boydii) (see Scedosporiosis, [[Scedosporiosis]]): accounts for 3% of non-Aspergillus cases
  • Alternaria Alternata: rare non-Aspergillus etiology
  • Candida Glabrata: rare non-Aspergillus etiology
  • Cladosporium Cladosporioides: rare non-Aspergillus etiology
  • Fusarium Vasinfectum: rare non-Aspergillus etiology
  • Helminthosporium: rare non-Aspergillus etiology
  • Penicillium Species: rare non-Aspergillus etiology
  • Rhizopus Oryzae: rare non-Aspergillus etiology
  • Saccharomyces Cerevisiae: rare non-Aspergillus etiology
  • Stemphylium Languinosum: rare non-Aspergillus etiology
  • Trichosporon Beigelii: rare non-Aspergillus etiology

Physiology

Pathogenesis is Unclear

  • Exposure of Atopic Patients to Fungal Spores Results in IgE and IgG Responses
    • In Contrast, Healthy Patients are Able to Effectively Eliminate Fungal Spores from the Airways
  • T-Cells Play an Important Role

Pathologic Findings

  • Bronchocentric Granulomatosis
  • Eosinophilic Pneumonia: although this may occasionally be found, this is not a major feature of ABPA
  • Histologic Features of Asthma
  • Mucoid Impaction of Bronchi
    • Presence of Septated Hyphae with Acute Dichotomous Branching in the Mucous-Filled Bronchial Lumen
    • Absence of Fungal Invasion of the Mucosal Wall

Diagnosis

Complete Blood Count (CBC) (see Complete Blood Count, [[Complete Blood Count]])

  • Peripheral Eosinophilia (see Peripheral Eosinophilia, [[Peripheral Eosinophilia]])
    • Elevated: >500/mm3 (Often >1000/mm3)
    • Peripheral Eosinophilia May Decrease Following Glucocorticoid Administration
    • Peripheral Eosinophilia >2000/mm3: should raise the consideration of other diagnoses, such as Churg-Strauss syndrome and hypereosinophilic syndromes

Aspergillus Skin Testing

  • Positive
    • Positive Immediate Skin Test Reactivity to Aspergillus Fumigatus is Present in 20-30% of All Asthmatics (Chest, 2000) [MEDLINE]: this subset of asthmatics has been termed “Severe Asthma with Fungal Sensitization” (SAFS) (see Asthma, [[Asthma]])
      • These Asthmatics May Respond to Itraconazole Therapy (FAST Trial) (Am J Respir Crit Care Med, 2009) [MEDLINE]

Serum Immunoglobulin E (IgE) (see Serum Immunoglobulin E, [[Serum Immunoglobulin E]])

  • Elevated: >1000 IU/mL (International Society for Human and Animal Mycology, ISHAM) (Clin Exp Allergy, 2013) [MEDLINE]
    • Generally Higher in ABPA than in Asthma
    • May Be as High as 25k IU/mL
    • Serum IgE May Decrease (But Does Not Usually Normalize) Following Glucocorticoid Administration
  • Recommendations (Infectious Diseases Society of America 2016 Aspergillosis Diagnosis and Treatment Guidelines) (Clin Infect Dis, 2016) [MEDLINE]
    • Total Serum IgE and Aspergillus-Specific IgE are Recommended for Diagnosis and Screening (Strong Recommendation, High-Quality Evidence)

Aspergillus-Specific Immunoglobulin E (IgE)

  • Elevated: >0.35 kU/L (International Society for Human and Animal Mycology, ISHAM) (Clin Exp Allergy, 2013) [MEDLINE]
  • Recommendations (Infectious Diseases Society of America 2016 Aspergillosis Diagnosis and Treatment Guidelines) (Clin Infect Dis, 2016) [MEDLINE]
    • Total Serum IgE and Aspergillus-Specific IgE are Recommended for Diagnosis and Screening (Strong Recommendation, High-Quality Evidence)

Serum Immunoglobulin G (IgG) (see Serum Immunoglobulin G, [[Serum Immunoglobulin G]])

  • Elevated: non-specific

Aspergillus Serum Precipitins

  • Precipitating Aspergillus Antibodies: useful diagnostically, but not useful for follow-up or monitoring
    • Newer Assays Can Detect Specific IgG Antibodies Against Aspergillus Antigens

Pulmonary Function Tests (PFT’s) (see Pulmonary Function Tests, [[Pulmonary Function Tests]])

  • Obstruction
  • Gas Trapping: increased RV/TLC ratio
  • Positive Bronchodilator Response: present in <50% of cases

Bronchoscopy (see Bronchoscopy, [[Bronchoscopy]])

  • May Be Necessary in Some Cases for Diagnostic Purposes or to Clear Mucous Plugging of Airways

Sputum Culture (see Sputum Culture, [[Sputum Culture]])

  • Gross Findings
    • Bronchial Casts
    • Pellets
    • Plugs
    • Thick Lumps
  • Microscopic Features
    • Charcot-Leyden Crystals
    • Curschmann’s Spirals
    • Eosinophils
  • Microbiologic Features
    • Aspergillus Can Be Grown from Sputum of Approximately 66% of ABPA Patients: although hyphae may not be seen by microscopy

Chest X-Ray (CXR) (see see Chest X-Ray, [[Chest X-Ray]])

  • Indications
    • May Be Used as Initial Radiologic Evaluation: however, CXR is not sensitive enough to detect the presence or extent of bronchiectasis in ABPA
      • CXR is Normal in 50% of ABPA Cases (World J Radiol, 2012) [MEDLINE]
  • Findings
    • Atelectasis (see Atelectasis, [[Atelectasis]]): due to mucoid impaction
    • Consolidation
    • Fleeting Pulmonary Opacities: usually involving the upper lobes preferentially
    • Findings Suggestive of Bronchiectasis
      • Gloved Finger Shadows (Branched Tubular Densities 2-3 cm Long and 5-8 mm Wide That Extend From the Hilum): due to intrabronchial exudates with bronchial wall thickening
      • Parallel Lines: due to ectatic bronchi
      • Peri-Hilar Opacities (Mimicking Hilar Lymphadenopathy): due to mucous plugging
      • Ring Shadows: due to bronchial wall thickening or saccular bronchiectasis
      • Toothpaste Shadows: due to mucoid impaction 2nd-4th order bronchi
      • Tram Track Opacities: due to thickened walls of non-dilated bronchi

High-Resolution Chest CT (HRCT) (see High-Resolution Chest Computed Tomography, [[High-Resolution Chest Computed Tomography]])

  • Indications
    • HRCT is the Imaging Procedure of Choice to Diagnose Bronchiectasis in ABPA
      • Sensitivity for Bronchiectasis: 96-98%
      • Specificity for Bronchiectasis: 93-98%
  • Findings
    • Normal: 37% of cases had normal HRCT in recent studies (Current Probl Diagn Radiol, 2016) [MEDLINE]
    • Atelectasis (see Atelectasis, [[Atelectasis]])
    • Bronchiectasis (see Bronchiectasis, [[Bronchiectasis]]): common
      • Central Bronchiectasis with Bronchial Wall Thickening is Classically Present with Upper Lobe Predominance: however, peripheral bronchiectasis may also be seen
    • Consolidation: may be seen in some cases
      • However, HRCT Studies Suggest that Most Consolidations Identified on CXR are Actually Mucous-Filled Bronchi (Current Probl Diagn Radiol, 2016) [MEDLINE]
    • Ground-Glass Infiltrates: may be seen in some cases
    • Mosaic Perfusion/Air Trapping: may be seen in some cases
    • Mucoid Impaction (see Mucoid Impaction, [[Mucoid Impaction]]): common
      • Mucoid Impaction May Be Hypodense or Hyperdense (Denser Than Paraspinal Skeletal Muscle)
        • Hyperdense Mucoid Impaction Occurs in 18-28% of Cases
        • When Present, the Hyperdensity Has Been Attributed to the Presence of Calcium Salts, Metals, or Desiccated Mucous
      • High Attenuation Mucoid Impaction on HRCT (>100 Hounsfield Units) was Correlated with Significantly Higher Values of Serum IgE, Specific IgE, and Number of Bronchial Segments Affected (Current Probl Diagn Radiol, 2016) [MEDLINE]
    • Tree-in-Bud Opacities (see Tree-in-Bud Sign, [[Tree-in-Bud Sign]]): may be seen

Bronchogram

  • No Longer Performed: due to invasive nature and risk of adverse effects

Clinical Diagnostic Criteria for Allergic Bronchopulmonary Aspergillosis (ABPA) (International Society for Human and Animal Mycology, ISHAM) (Clin Exp Allergy, 2013) [MEDLINE]

Predisposing Criteria (One Must Be Present)

Obligatory Criteria (Both Must Be Present)

  • Positive Aspergillus Skin Test or Detectable Aspergillus Fumigatus-Specific IgE
    • Aspergillus Skin Prick Test: >3mm wheel 10 min after skin prick (usually with negative reaction to other allergens)
    • Aspergillus Intradermal Skin Test
    • ISHAM Definition of Elevation of Aspergillus Fumigatus-Specific IgE: >0.35 kU/L
  • Elevated Serum IgE
    • ISHAM Definition of Elevation of Serum IgE: >1000 IU/mL
      • May Be <1000 IU/mL, if Patient Meets All Other Criteria

Other Criteria (At Least Two Must Be Present)

  • Precipitating Serum Antibodies to Aspergillus Fumigatus or Elevated Serum Aspergillus IgG by Immunoassay
  • Radiographic Pulmonary Opacities Consistent with the Diagnosis of ABPA
  • Peripheral Eosinophilia (Eosinophil Count >500 cells/μL) in Corticosteroid-Naive Patient: may be historical

Clinical Diagnosis in Patients with Cystic Fibrosis (CF) (see Cystic Fibrosis, [[Cystic Fibrosis]]) (Cystic Fibrosis Foundation Consensus Conference Guidelines) (Clin Infect Dis, 2003) [MEDLINE]

  • Maintain High Clinical Suspicion for ABPA in CF Patients >6 y/o: especially in those with clinical deterioration
  • Measure Total Serum IgE Annually
    • *If Serum IgE 200-500 IU/mL, Repeat the Measurement if Clinical Suspicion is High and Consider Other Evaluation (Chest X-Ray, Aspergillus Precipitins, Aspergillus Fumigatus-Specific IgE, Aspergillus Skin Test, etc)
    • If Serum IgE >500 IU/mL, Evaluate with Aspergillus Fumigatus-Specific IgE and Aspergillus Skin Test

Clinical Manifestations

General Comments

  • ABPA May Be Asymptomatic in Some Cases

Otolaryngologic Manifestations

Allergic Fungal Rhinosinusitis (see Chronic Rhinosinusitis, [[Chronic Rhinosinusitis]])

  • Epidemiology: allergic fungal rhinosinusitis may occur coexistent with ABPA in small percentage of cases
  • Clinical: allergic fungal rhinosinusitis is a distinct type of chronic rhinosinusitis

Pulmonary Manifestations

Asthma-Like Presentation with Recurrent Exacerbation (see Asthma, [[Asthma]])

  • Epidemiology: characteristic clinical presentation
  • Clinical: typically with recurrent exacerbation
    • Bronchospasm/Wheezing (see Obstructive Lung Disease, [[Obstructive Lung Disease]]): variably present
    • Chest Pain (see Chest Pain, [[Chest Pain]])
    • Cough (see Cough, [[Cough]])
    • Expectoration of Bronchial Casts: occurs in 66% of cases
    • Mucopurulent/Bloody Sputum: occurs in some cases
    • Dyspnea (see Dyspnea, [[Dyspnea]])

Atelectasis (see Atelectasis, [[Atelectasis]])

  • Epidemiology: may occur in some cases
  • Clinical
    • Right Middle Lobe Syndrome

Pneumonia-Like Presentation (see Pneumonia, [[Pneumonia]])

  • Epidemiology: may occur in some cases
  • Clinical
    • Chest Pain (see Chest Pain, [[Chest Pain]])
    • Cough (see Cough, [[Cough]])
    • Expectoration of Bronchial Casts: occurs in 66% of cases
    • Mucopurulent/Bloody Sputum (see Hemoptysis, [[Hemoptysis]]): occurs in some cases
    • Dyspnea (see Dyspnea, [[Dyspnea]])

Lung Nodule/Mass (see Lung Nodule or Mass, [[Lung Nodule or Mass]])

  • Epidemiology: may occur in some cases
  • Physiology

Pulmonary Fibrosis

  • Epidemiology: may occur in advanced cases
  • Physiology: recurrent inflammation

Other Manifestations

  • Fever (see Fever, [[Fever]])
    • Epidemiology: occurs in 10% of cases
  • Malaise
  • Night Sweats

Complications

  • Aspergilloma (see Aspergillus, [[Aspergillus]])
    • Epidemiology
      • Rare Complication of ABPA (Ann Allergy Asthma Immunol, 2006) [MEDLINE]
  • Chronic Pulmonary Aspergillosis (see Aspergillus, [[Aspergillus]])
    • Epidemiology
      • Rare Complication of ABPA (Respir Med, 2015) [MEDLINE]
  • Invasive Pulmonary Aspergillosis (see Aspergillus, [[Aspergillus]])
    • Epidemiology
      • Rare Complication of ABPA (Mycopathologia, 2015) [MEDLINE]
      • May Occur During Itraconazole Therapy: may be due to immunosuppressive effects of corticosteroids

Treatment

Acute Allergic Bronchopulmonary Aspergillosis (ABPA)

Systemic Corticosteroids and Azole Antifungals

  • Indications
    • Acute ABPA with Radiographic Opacities (Usually Upper/Middle Lobes and Serum IgE >1000 IU/mL
  • Administration
    • Prednisone (see Prednisone, [[Prednisone]]): 0.5 mg/kg qday x 14 days (although some patients require a higher prednisone dose of 40-60 mg/day for acute asthma exacerbation)
      • Subsequently, Change to Every Other Day Prednisone Dosing
      • Subsequently, Taper Prednisone Off at 3 mo
    • Itraconazole (Sporanox) (see Itraconazole, [[Itraconazole]]): 200 mg TID x 3 days, then 200 mg BID x 16 wks
      • Rationale for Antifungal Component of Therapy: to decrease the corticosteroid dose
      • Alternative: Voriconazole (Vfend) (see Voriconazole, [[Voriconazole]]): 400 mg PO BID x 2 doses, then 200 mg PO BID x 16 wks
        • Voriconazole is Better Absorbed and Has Better Gastrointestinal Tolerance Than Itraconazole
  • Monitoring
    • Serum IgE (Measured Every 1-2 mo): serum IgE generally decreases by 25% after 1 month of treatment and by 60% after 2 months of treatment (Ann Thorac Med, 2014)[MEDLINE]
      • Decrease of 35% is Considered a Good Therapeutic Response: this merits tapering of prednisone
      • Note: Aspergillus-specific IgE is not considered useful for monitoring
  • Clinical Efficacy
    • Corticosteroid Use is Based Largely on Case Series, as No Clinical Trials Have Been Performed (Arch Intern Med, 1986) [MEDLINE] and (Chest, 2006) [MEDLINE
    • Trial of Itraconazole in Corticosteroid-Dependent ABPA (NEJM, 2000) [MEDLINE]
      • Itraconazole (x 16 wks) Increased Clinical Response Over Corticosteroids Alone
    • Trial of Itraconazole in Stable ABPA (J Allergy Clin Immunol, 2003) [MEDLINE]
      • Itraconazole (x 16 wks) Decreased Corticosteroid-Requiring Exacerbations in ABPA
  • Recommendations (Infectious Diseases Society of America 2016 Aspergillosis Diagnosis and Treatment Guidelines) (Clin Infect Dis, 2016) [MEDLINE]
    • ABPA with Bronchiectasis and/or Mucoid Impaction Should Be Treated with Corticosteroids and Itraconazole (with Therapeutic Drug Monitoring) (Weak Recommendation; Low-Quality Evidence)

Acute Allergic Bronchopulmonary Aspergillosis (ABPA) in Remission

  • Definition of Remission: normal-mildly increased serum IgE and absence of radiographic findings in a patient who has been off corticosteroids for >6 mo
  • Inhaled Corticosteroids (see Corticosteroids, [[Corticosteroids]]): used to maintain asthma control
  • Monitoring
    • Pulmonary Function Tests (PFT’s) (Annually or In Response to Symptoms) (see Pulmonary Function Tests, [[Pulmonary Function Tests]])
    • Serum IgE (Measured Every 3-6 mo): increase in serum IgE may precede or accompany radiographic changes or peripheral eosinophilia

Acute Allergic Bronchopulmonary Aspergillosis (ABPA) Exacerbation

  • Exacerbations May Be Frequent
    • Exacerbations May Be Asymptomatic, Being Detected Only by Serum IgE and Radiographic Changes
    • Corticosteroids in Doses Adequate to Maintain Control of Asthma May Be Inadequate to Prevent Exacerbations of ABPA: for this reason serum IgE monitoring is useful
  • Agents
    • Omalizumab (Xolair) (see Omalizumab, [[Omalizumab]])
  • Clinical Efficacy
    • Trial of Omalizumab in ABPA with Poorly-Controlled Asthma (J Allergy Clin Immunol Pract, 2015) [MEDLINE]
      • Omalizumab Can Be Used to Treat ABPA, Despite High Serum IgE

Other Interventions

  • Avoidance of Aspergillus Exposure: while avoidance of exposure seems logical, its impact is not clear
  • Allergen Immunotherapy (see Allergen Immunotherapy, [[Allergen Immunotherapy]]): unclear role
  • Bronchoscopy (see Bronchoscopy, [[Bronchoscopy]]): may be required in some cases to clear mucous plugs
  • Inhaled Corticosteroids (see Corticosteroids, [[Corticosteroids]])
    • Inhaled Corticosteroids are Not Believed to Have No Role in the Management of Serologically-Diagnosed ABPA, But May Be Useful as an Adjunct to Treat Asthmatic Symptoms (Intern MED, 2011) [MEDLINE]
  • Nebulized Amphotericin B (see Amphotericin, [[Amphotericin]]): has been reported to be efficacious in childhood cases with associated cystic fibrosis

Treatment of Acute Allergic Bronchopulmonary Aspergillosis (ABPA) in Patients with Cystic Fibrosis (CF) (see Cystic Fibrosis, [[Cystic Fibrosis]])

  • General Approach: treat as per standard therapy above
  • Clinical Efficacy
    • Trial of Itraconazole in ABPA Associated with CF (Chest, 1999) [MEDLINE]
  • Recommendations (Infectious Diseases Society of America 2016 Aspergillosis Diagnosis and Treatment Guidelines) (Clin Infect Dis, 2016) [MEDLINE]
    • In Patients with CF with Frequent Exacerbations and/or Decreasing FEV1, Itraconazole is Suggested (with Therapeutic Drug Monitoring) to Minimize Corticosteroid Use (Weak Recommendation; Low-Quality Evidence): if therapeutic levels of itraconazole cannot be achieved, other azole antifungals should be considered

Prognosis

  • Prognosis of Serologic ABPA with Normal HRCT (Respir Med, 2012) [MEDLINE]: mean follow-up duration was 43.7 +/- 10.1 mo
    • No Patients Developed Central Bronchiectasis

References

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