http://informahealthcare.com/mcb ISSN: 1040-841X (print), 1549-7828 (electronic) Crit Rev Microbiol, Early Online: 1–19 ! 2012 Informa Healthcare USA, Inc. DOI: 10.3109/1040841X.2012.754401 REVIEW ARTICLE Allergic bronchopulmonary mycosis due to fungi other than Aspergillus: a global overview Anuradha Chowdhary1, Kshitij Agarwal2, Shallu Kathuria1, Shailendra Nath Gaur2, Harbans Singh Randhawa1, and Jacques F. Meis3,4 1Department of Medical Mycology, and 2Department of Pulmonary Medicine, University of Delhi, Vallabhbhai Patel Chest Institute, Delhi, India, 3Department of Medical Microbiology and Infectious Diseases, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands, and 4Department of Medical Microbiology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands Abstract Keywords Allergic bronchopulmonary mycosis (ABPM) is a hypersensitivity-mediated disease of world- Allergic bronchopulmonary mycosis, Candida wide distribution. We reviewed 143 reported global cases of ABPM due to fungi other than albicans, India, moulds, yeasts aspergilli. The commonest etiologic agent was Candida albicans, reported in 60% of the cases, followed by Bipolaris species (13%), Schizophyllum commune (11%), Curvularia species (8%), History Pseudallescheria boydii species complex (3%) and rarely, Alternaria alternata, Fusarium vasinfectum, Penicillium species, Cladosporium cladosporioides, Stemphylium languinosum, Received 5 October 2012 Rhizopus oryzae, C. glabrata, Saccharomyces cerevisiae and Trichosporon beigelii. India accounted Revised 21 November 2012 for about 47% of the globally reported cases of ABPM, attributed predominantly to C. albicans, Accepted 27 November 2012 followed by Japan (16%) where S. commune predominates, and the remaining one-third from Published online 5 February 2013 the USA, Australia and Europe. Notably, bronchial asthma was present in only 32% of ABPM cases whereas its association with development of allergic bronchopulmonary aspergillosis (ABPA) is known to be much more frequent. The cases reviewed herein revealed a median IgE value threefold higher than that of ABPA, suggesting that the etiologic agents of ABPM incite a stronger immunological response than that by aspergilli in ABPA. ABPM is currently underdiagnosed, warranting comprehensive basic and clinical studies in order to elucidate For personal use only. its epidemiology and to devise a more effective therapy. Introduction candidiasis, helminthosporiosis, curvulariosis, penicilliosis, mucormycosis, Schizophyllum, Bipolaris, Alternaria, Allergic bronchopulmonary mycosis (ABPM) is a hypersen- Curvularia, Cladosporium, Stemphylium and Penicillium sitivity-mediated disease of the lower airways caused by etc. Additionally, the references not listed in PubMed but environmental fungi, the most common being Aspergillus cited in published articles were included. Altogether 159 fumigatus. The other etiologic agents include Candida cases of ABPM were compiled. Of these, 143 cases published albicans, Schizophyllum commune, species of Alternaria, in English have been analyzed in detail. Bipolaris, Cladosporium, Curvularia, Fusarium, Penicillium, Pseudallescheria, Rhizopus, Saccharomyces, Stemphylium Historical and Trichosporon. The disease was first recognized by 2013 Hinson et al. (1952) in the UK who described it in asthmatics Historically, the association of molds with allergic respiratory Critical Reviews in Microbiology Downloaded from informahealthcare.com by The University of Manchester on 02/22/13 with recurrent pulmonary infiltrates, peripheral blood eosi- disorders spans over three centuries. The first case linking nophilia and sputum culture positive for A. fumigatus. While molds to an exacerbation of asthma appeared in 1698; the allergic bronchopulmonary aspergillosis (ABPA) has been patient had experienced an ‘‘asthmatic attack’’ when he came extensively studied worldwide, there is paucity of information into contact with fermenting wine (Floyer, 1698). Further on ABPM due to other fungi. This review aims to provide an observations supporting the allergenic role of molds and their update on the work done globally on ABPM, excluding association with asthma accumulated over the nineteenth and ABPA. As stated above, numerous fungi have been implicated twentieth centuries. A definitive evidence of fungi causing in the etiology of ABPM. Our literature search done through asthma was first brought out in 1924 by Cadham (Cadham, PubMed covered the period up to July 2012; the search words 1924) who showed that Puccinia graminis, a plant pathogenic used were allergic, bronchopulmonary, mycosis, mycoses, fungus, incited asthma. Later in the same decade, Alternaria (Hopkins et al., 1930), Aspergillus (Bernton, 1930) and Trichophyton (Ramirez, 1930) were incriminated in the Address for correspondence: Anuradha Chowdhary MD, PhD, Depart- ment of Medical Mycology, Vallabhbhai Patel Chest Institute, University causation of asthma. The triad of asthma, pulmonary of Delhi, Delhi, India. E-mail: [email protected] infiltrates and eosinophilia was linked to Aspergillus species 2 A. Chowdhary et al. Crit Rev Microbiol, Early Online: 1–19 and the term allergic bronchopulmonary aspergillosis was 1988; Ogawa et al., 2004; Ogawa et al., 2012; Patterson et al., coined in 1952 by Hinson, Moon and Plummer from the UK 1982b; Sahn & Lakshminarayan, 1973; Tajima et al., 2000; (Hinson et al., 1952). The pioneering work on ABPA done in Tomita et al., 1996; Travis et al., 1991) as well as ABPA the UK led to the recognition of this disease as an important (Agarwal et al., 2009a; Amin & Mahmood, 2008; Berkin mycosis with a worldwide distribution. Subsequently, in the et al., 1982; Bondue et al., 2005; Glancy et al., 1981; Gupta 1970s series of well-documented ABPA cases, some of whom et al., 2012; Hinson et al., 1952; Hoshino et al., 1999; Koh had been masquerading as pulmonary tuberculosis not et al., 2007; Shah et al., 2004; Yoshida et al., 1992) have been responding to anti-tubercular therapy were reported from diagnosed in non-asthmatics. Likewise, false positive and the V. P. Chest Institute, Delhi, India (Khan et al., 1976; Khan negative results for serum precipitins are not uncommon in & Sandhu, 1978; Pamra et al., 1972; Radha & Viswanathan, ABPM cases (Chowdhary et al., 2012; Darke et al., 1976; 1978; Sandhu et al., 1972; Sandhu et al., 1978; Sandhu et al., Longbottom & Pepys, 1964; Vlahakis & Aksamit, 2001; 1979; Subramanian & Viswanathan, 1972). For further Zacharisen & Fink, 2005). The presence of serum precipitins information pertaining to ABPA, reference may be made to against an antigen should be taken as indicative of a previous several reviews (Agarwal, 2009; Agarwal et al., 2009b; exposure to it and not necessarily a sign of active disease Agarwal et al., 2012; Burnie, 1995; Hogan & Denning, 2011; (Darke et al., 1976). Knutsen & Slavin, 2011; Mahdavinia & Grammer, 2012; The country-wise distribution and the fungi implicated in a Patterson & Strek, 2010; Shah, 2008; Tillie-Leblond & total of 159 cases of ABPM are shown in Table 2 and depicted Tonnel, 2005). The role of molds other than Aspergillus, and in Figures 1 and 2. It is noteworthy that only 16 of 143 ABPM of yeasts, as etiologic agents of ABPM came to light much cases (11%) analyzed and summarized in Tables 3–5 fulfilled later as described below. the Rosenberg–Patterson criteria. The data pertaining to individual diagnostic parameters were as follows: total IgE Diagnostic criteria reported in 81.1% (116/143) cases, increase in eosinophil ABPM is a complex disease that is diagnosed by a count in 47% (67/143), culture of fungus in 46.8% (67/143), combination of clinical, mycoserologic and radiological type I skin test in 38.5% (55/143), precipitins in 30% (43/143) features. The most commonly accepted criteria are those and fungus-specific IgE/IgG antibodies in 27% (39/143). proposed by Rosenberg et al. (1977) and Patterson et al. Asthma which figured prominently in the discussion was (1986) as listed in Table 1. Subsequently, the minimal present in only 32% of the cases (Table 6). Actually, a essential diagnostic criteria were proposed (Greenberger, majority of the published cases lacked data on all the 2002; Schwartz & Greenberger, 1991; Stevens et al., 2003). diagnostic parameters. Consequently, their diagnosis as This simplified version excluded eosinophilia and demonstra- ABPM would be better regarded as probable and not tion of precipitating antibodies as diagnostic criteria. The unequivocally proven. Table 6 provides a synopsis of clinical exclusion of precipitating antibodies was done on the ground and laboratory diagnostic profiles of 143 reported ABPM For personal use only. that they are prone to be false negative in patients receiving cases. The highest positivity of 94.5% (52/55 cases) was corticosteroid therapy or during remission of the disease. found for type I skin hypersensitivity to the etiologic fungus, However, controversy regarding the essential diagnostic followed by eosinophilia in 92.5% (62/67 cases), precipitating criteria continues due to lack of their specificity. For example, antibody in 90.7% (39/43), fungal isolation in 89.6% (60/67), although asthma is an important diagnostic criterion, many increased serum total IgE in 86.2% (100/116), pulmonary cases of ABPM (Chowdhary et al., 2012; Gendry et al., 2006; infiltrates in 66.2% (43/65) and central bronchiectasis in Glancy et al., 1981; Halloran, 1983; Hamilton et al., 2006; 32.3% (21/65). Hendrick et al., 1982;