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Allergic Bronchopulmonary Candidiasis

1984; Elsevier BV; Volume: 85; Issue: 5 Linguagem: Inglês

10.1378/chest.85.5.699

1931-3543

Kazuo Akiyama, David A. Mathison, Jeffrey B. Riker, Paul A. Greenberger, Roy Patterson,

Asthma and respiratory diseases

A patient had an illness consistent with allergic bronchopulmonary candidiasis. She had asthma, fleeting pulmonary infiltrate, immediate skin reactivity and precipitating antibody against Candida albicans, elevated total serum IgE concentration, elevated IgE and IgG antibody activity against C albicans, and two positive sputum cultures for C albicans. Serial serologic studies showed a significant decrease of serum IgE levels and IgE antibody activity after corticosteroid treatment. A patient had an illness consistent with allergic bronchopulmonary candidiasis. She had asthma, fleeting pulmonary infiltrate, immediate skin reactivity and precipitating antibody against Candida albicans, elevated total serum IgE concentration, elevated IgE and IgG antibody activity against C albicans, and two positive sputum cultures for C albicans. Serial serologic studies showed a significant decrease of serum IgE levels and IgE antibody activity after corticosteroid treatment. Allergic bronchopulmonary aspergillosis (ABPA) which was first described in Great Britain in 1952,1Hinson KFW Moon AJ Plummer NS Bronchopulmonary aspergillosis.Thorax. 1952; 7: 317-333Crossref PubMed Google Scholar has become increasingly recognized in the United States. The disease is characterized by asthma, peripheral blood eosinophilia, immediate and occasional late skin reactivity to Aspergillus antigen, fleeting pulmonary infiltrates, occasional expectoration of brown plugs containing abundant hyphae of Aspergillus, central bronchiectasis, and precipitating antibodies against Aspergillus antigen. Subsequently, strikingly elevated total serum IgE levels were found,2Patterson R Fink JN Pruzansky JJ Reed C Roberts M Slavin R et al.Serum immunoglobulin levels in pulmonary allergic aspergillosis and certain other lung diseases, with special reference to immunoglobulin E.Am J Med. 1973; 54: 16-22Abstract Full Text PDF PubMed Scopus (82) Google Scholar and this has become one of the primary criteria for the diagnosis of ABPA.3Rosenberg M Patterson R Mintzer R Cooper BJ Roberts M Harris KE Clinical and immunological criteria for the diagnosis of allergic bronchopulmonary aspergillosis.Ann Intern Med. 1977; 86: 405-414Crossref PubMed Scopus (625) Google Scholar Rosenberg et al,4Rosenberg M Patterson R Roberts M Wang J The assessment of immunologic and clinical changes occurring during corticosteroid therapy for allergic bronchopulmonary aspergillosis.Am J Med. 1978; 64: 599-606Abstract Full Text PDF PubMed Scopus (103) Google Scholar by using solid phase polystyrene tube radioimmunoassay, showed that IgE and IgG antibodies against Aspergillus antigen were increased in most patients with ABPA and reflected disease activity as evidenced by roentgenographic and clinical exacerbations. Serologic measurements of IgE and IgG antibodies against Aspergillus fumigatus are considered to be of diagnostic value in all the stages of ABPA.5Wang JLF Patterson R Rosenberg M Roberts M Cooper BJ Serum IgE and IgG antibody against Aspergillus fumigatus as a diagnostic aid in allergic bronchopulmonary aspergillosis.Am Rev Resp Dis. 1978; 117: 917-927PubMed Google Scholar, 6Patterson R Greenberger PA Radin RC Roberts M Allergic bronchopulmonary aspergillosis: staging as an aid to management.Ann Intern Med. 1982; 96: 286-291Crossref PubMed Scopus (260) Google Scholar Recently, other organisms which may on occasion produce clinical presentations to similar ABPA have been reported,7Dolan CT Weed LA Dines DE Bronchopulmonary helminthosporiosis.Am J Clin Pathol. 1970; 53: 235-242Crossref PubMed Scopus (31) Google Scholar, 8Gordon DS Hunter RG O’Reilly RJ Conway BP Pseudomonas aeruginosa allergy and humoral antibody mediated hypersensitivity pneumonia.Am Rev Respir Dis. 1973; 108: 127-131PubMed Google Scholar, 9Benatar SR Kroenert DB Elder JL Frondist JH Allergic bronchopulmonary stemphyliosis.Thorax. 1980; 35: 515-518Crossref PubMed Scopus (33) Google Scholar, 10McAller R Kroenert DB Elder JL Frondist JH Allergic bronchopulmonary disease caused by Curvularia lunata and Drechislera hawaiiensis.Thorax. 1981; 36: 338-344Crossref PubMed Scopus (78) Google Scholar, 11Hendrick DJ Ellithrope DB Lyon F Hattier P Salvaggio JE Allergic bronchopulmonary helminthosporiosis.Am Rev Respir Dis. 1982; 126: 935-938PubMed Google Scholar including Candida albicans.12Pepys J Faux JA Longbottom JL McCarthy DS Hargreave FE Candida albicans precipitins in respiratory disease in man.J Allerg. 1968; 41: 305-318Abstract Full Text PDF PubMed Scopus (66) Google Scholar, 13Voisin C Tonnel AB Jacob M Thermol P Malin P Lahoutte C Infiltrates pulmonaires avec grane eosinophillie sanguine associes a une candidose bronchique.Rev Fr Allergie Immunol Clin. 1976; 16: 279-281Google Scholar, 14Sandu RS Mehta SK Khan ZU Singh MM Role of Aspergillus and Candida species in allergic bronchopulmonary mycoses.Scand J Respir Dis. 1979; 60: 235-242PubMed Google Scholar However, serologic studies have been limited to precipitins with the exception of hemagglutination studies and total serum IgE measurement as reported in the paper by Voisin et al.13Voisin C Tonnel AB Jacob M Thermol P Malin P Lahoutte C Infiltrates pulmonaires avec grane eosinophillie sanguine associes a une candidose bronchique.Rev Fr Allergie Immunol Clin. 1976; 16: 279-281Google Scholar This report describes a patient with an illness consistent with allergic bronchopulmonary candidiasis (ABPC) which was diagnosed by the aid of measurement of serum antibody against C albicans and showed a decrease of total serum IgE and IgE against C albicans during prednisone therapy. The IgE content of serum samples was determined by doubleantibody radioimmunoassay and expressed as nanograms per milliliter. 15Gleich GJ Averbeck AK Swedlund HA Measurement of IgE in normal and allergic serum by radioimmunoassay.J Lab Clin Med. 1971; 77: 690-698PubMed Google Scholar The C albicans antigen was obtained from Hollister-Stier Laboratories. Precipitins against C albicans were demonstrated by the double diffusion technique of Ouchterlony.16Crowle AJ Immunodiffusion. Academic Press, New York1961: 1-310Google Scholar The polystyrene tube radioimmunoassay technique which was used to demonstrate IgE and IgG antibodies against A fumigatus has been described previously.17Patterson R Roberts M IgE and IgG antibodies against Aspergillus fumigatus in sera of patients with bronchopulmonary allergic aspergillosis.Int Arch Allergy Appl Immunol. 1974; 46: 150-160Crossref PubMed Google Scholar This technique was used to evaluate IgE and IgG antibodies against C albicans. In this study, the polystyrene tubes were coated with the C albicans antigen (40 mg/ml). Results were compared with serum from a nonatopic subject who had no precipitins to C albicans. A 54-year old white woman had a flu-like upper respiratory illness that was followed by development of corticosteroid dependent asthma in 1971. The lowest possible prednisone dose over the next ten years was 5 mg every other day in addition to bronchodilators. She often had copious production of stringy, thick white mucus over the past decade. Sputum cultures in April and May 1981 grew C albicans. In October 1981, hospitalization was required for status asthmaticus. Her chest roentgenogram revealed marked hyperinflation. Serum IgE value was 1,320 ng/ml. From February to May 1982, asthma was managed with albuterol and beclomethasone by inhalation. She was hospitalized for status asthmaticus in September 1982. She had taken 40 mg of prednisone daily for a week prior to admission. Chest roentgenogram again revealed hyperinflation without evidence for bronchiectasis. Intradermal skin test was performed using common inhalant allergens. She showed negative reactions to these antigens except C albicans (10 mm of immediate wheal reaction with 1:200 w/v). Serum IgE level during her hospitalization was markedly elevated at 5,178 ng/ml. She was receiving troleandomycin, 250 mg twice daily, and methylprednisolone, 40 mg daily when in November 1982, a left lower lobe infiltrate was observed. This infiltrate was considered consistent with atelectasis from a mucus plug in left lower lobe with distal obstruction and marked volume loss. Sputum cultures did not yield Candida species. Corticosteroids were continued and within one week, the atelectasis had improved markedly. Because this patient demonstrated positive immediate skin reactivity to C albicans, elevated total serum IgE, precipitins to C albicans antigen, and positive sputum culture of C albicans, it was suggested that this woman might have an illness consistent with ABPC. Further serologic examinations were performed. The serum at time of hospitalization (October 1982) was analyzed for antibodies against species of Aspergillus. There were no precipitins against A fumigatus, A nidulans, A terreus, A glaucus, or A niger. The IgE and IgG antibody activity against A fumigatus using a radioimmunoassay17Patterson R Roberts M IgE and IgG antibodies against Aspergillus fumigatus in sera of patients with bronchopulmonary allergic aspergillosis.Int Arch Allergy Appl Immunol. 1974; 46: 150-160Crossref PubMed Google Scholar was not elevated. The total serum IgE was measured, and IgE and IgG antibody activity against C albicans was evaluated in the serum of the patient (October 1982) by using the polystyrene tube radioimmunoassay. The results are shown in Figure 1. Serum IgE level was 5,120 ng/ml at that time. Both IgE and IgG antibody activities against C albicans were elevated compared with nonatopic control serum. Serum IgE antibody activity was 287 percent of control at the dilution of 1:10. Serum IgG antibody activity was 153 percent of control at the dilution of 1:10,000. The same indices were examined in the serum of the patient obtained in January 1983 three months after diagnosis, when prednisone therapy was being continued. A marked decrease of serum IgE level (944 ng/ml) and IgE antibody activity (160 percent of control) was observed while IgG antibody had increased (Fig 1). The diagnosis of ABPA was considered in this patient because of the clinical findings, but serologic evaluation and negative skin tests excluded this disorder. The diagnosis of ABPC was considered because of precipitins against C albicans and elevated serum IgE. The patient described had asthma, positive sputum culture for C albicans, a fleeting pulmonary infiltrate, immediate skin reactivity to C albicans antigen, precipitating antibody against C albicans antigen, an elevated serum IgE concentration, and elevated serum IgE and IgG antibody activity against C albicans. Serial serologic studies showed a significant decrease of serum IgE levels and IgE antibody activity against C albicans after corticosteroid treatment for three months. These immunologic findings are similar to the course in ABPA.4Rosenberg M Patterson R Roberts M Wang J The assessment of immunologic and clinical changes occurring during corticosteroid therapy for allergic bronchopulmonary aspergillosis.Am J Med. 1978; 64: 599-606Abstract Full Text PDF PubMed Scopus (103) Google Scholar The early diagnosis of allergic bronchopulmonary disease is difficult because, with the exception of proximal bronchiectasis, none of the classic findings is specific for this disease. Diagnosis of ABPA has been aided by the fact that total serum IgE level and IgE and IgG antibody activity against A fumigatus were markedly elevated in the serum of patients with ABPA during the acute phase of disease.2Patterson R Fink JN Pruzansky JJ Reed C Roberts M Slavin R et al.Serum immunoglobulin levels in pulmonary allergic aspergillosis and certain other lung diseases, with special reference to immunoglobulin E.Am J Med. 1973; 54: 16-22Abstract Full Text PDF PubMed Scopus (82) Google Scholar, 18Greenberger PA Patterson R Ghory A Arkins JA Walsh T Graves T et al.Late sequelae of allergic bronchopulmonary aspergillosis.J Allerg Clin Immunol. 1980; 66: 327-335Abstract Full Text PDF PubMed Scopus (47) Google Scholar The measurements of IgE and IgG antibody activity against C albicans have proven useful in suggesting ABPC in our patient. Several papers have been published reporting cases of ABPC in the United Kingdom,12Pepys J Faux JA Longbottom JL McCarthy DS Hargreave FE Candida albicans precipitins in respiratory disease in man.J Allerg. 1968; 41: 305-318Abstract Full Text PDF PubMed Scopus (66) Google Scholar France,13Voisin C Tonnel AB Jacob M Thermol P Malin P Lahoutte C Infiltrates pulmonaires avec grane eosinophillie sanguine associes a une candidose bronchique.Rev Fr Allergie Immunol Clin. 1976; 16: 279-281Google Scholar and India.14Sandu RS Mehta SK Khan ZU Singh MM Role of Aspergillus and Candida species in allergic bronchopulmonary mycoses.Scand J Respir Dis. 1979; 60: 235-242PubMed Google Scholar Most of the patients reported in these papers had classic clinical symptoms and findings compatible with ABPC, but inadequate serologic data were reported. The ABPC disorder may be diagnosed more frequently or may occur as isolated cases such as allergic bronchopulmonary helminthosporiosis.7Dolan CT Weed LA Dines DE Bronchopulmonary helminthosporiosis.Am J Clin Pathol. 1970; 53: 235-242Crossref PubMed Scopus (31) Google Scholar, 11Hendrick DJ Ellithrope DB Lyon F Hattier P Salvaggio JE Allergic bronchopulmonary helminthosporiosis.Am Rev Respir Dis. 1982; 126: 935-938PubMed Google Scholar Considering the development of late sequelae of allergic bronchopulmonary disease,6Patterson R Greenberger PA Radin RC Roberts M Allergic bronchopulmonary aspergillosis: staging as an aid to management.Ann Intern Med. 1982; 96: 286-291Crossref PubMed Scopus (260) Google Scholar,86 early diagnosis and precise treatment of disease may be necessary to prevent development of lung destruction in patients with syndromes consistent with ABPC.