ARTICLE IN PRESS

Int. J. Hyg. Environ. Health 212 (2009) 18–20

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Childhood hypersensitivity pneumonitis associated with fungal

contamination of indoor hydroponics

Steffen Engelharta,�, Ernst Rietschelb, Martin Exnera, Lars Langeb

aInstitut fur Hygiene und Offentliche Gesundheit, Universitat Bonn, Sigmund-Freud-Straße 25, 53105 Bonn, GermanybKlinik und Poliklinik fur Allgemeine Kinderheilkunde, Universitat Koln, Germany

Received 27 April 2007; received in revised form 8 January 2008; accepted 16 January 2008

Abstract

Childhood hypersensitivity pneumonitis (HP) is often associated with exposure to antigens in the homeenvironment. We describe a case of HP associated with indoor hydroponics in a 14-year-old girl. Water samplesfrom hydroponics revealed Aureobasidium pullulans as the dominant fungal micro-organism (104CFU/ml). Thediagnosis is supported by the existence of serum precipitating antibodies against A. pullulans, lymphocytic alveolitis onbronchoalveolar lavage (BAL) fluid, a corresponding reaction on a lung biopsy, and the sustained absence of clinicalsymptoms following the removal of hydroponics from the home. We conclude that hydroponics should be consideredas potential sources of fungal contaminants when checking for indoor health complaints.r 2008 Elsevier GmbH. All rights reserved.

Keywords: Hypersensitivity pneumonitis; Fungi; Indoor hydroponics; Potting soil; Aureobasidium pullulans

Case report

A 14-year-old girl was admitted to hospital havingexperienced coughing for 10 weeks and increasingdyspnoea on exertion. These symptoms prevailed overthe whole time period without any marked accentuationregarding any particular location or other externalfactors. There were no other allergic or respiratorydiseases in the medical history. The environmentalhistory revealed no contacts to pets or birds; the familyhad lived in the same house for several years, withoutany obvious mould exposure. No ultrasonic humidifiershad been used. In the living room three hydroponicplants (two Yucca elephantipes and one other unspeci-fied palm tree) were grown in three large pots. The

e front matter r 2008 Elsevier GmbH. All rights reserved.

eh.2008.01.001

ing author. Tel.: +228 287 14434; fax: +228 287 14645.

ess: steffen.engelhart@ukb.uni-bonn.de (S. Engelhart).

plants did not suffer from obvious diseases. The plantpots were exclusively filled with extended clay pebbles,tap water and hydroponic nutrient solutions, withoutany supplemental materials (e.g., soil, sand, gravel,perlite, vermiculite, or rock wool).

At the time of hospital admission, the physicalexamination revealed no obvious respiratory distressexcept bilateral inspiratory crackles. The haemoglobinlevel amounted to 15.9 g/dl, and white blood cell count,serum chemistry, and capillary blood gas analysis allranged within the reference values. The chest roentgen-ogram presented bilateral micronodular infiltrates.

Pulmonary function tests used to evaluate the subjectwere carried out according to published ATS/ERSguidelines. Pulmonary function tests performed on theday following admission revealed a vital capacity of57%, FEV1 of 55%, and diffusion capacity for carbonmonoxide (TLCO) of 38% of the adjusted reference

ARTICLE IN PRESSS. Engelhart et al. / Int. J. Hyg. Environ. Health 212 (2009) 18–20 19

values, respectively. An exercise test had to be discon-tinued after 5min due to a decrease in transcutaneousoxygen saturation from 95% to 79%.

Bronchoalveolar lavage (BAL) was performed in thelingula bronchus (5� 20ml of saline, recovery rate55%). The BAL fluid yielded a proportion of 78%lymphocytes with a CD4/CD8-ratio of 0.6. Lung biopsy(via thoracoscopy) and histological analysis showed aninfiltration of alveolar spaces and interstitium withlymphocytes and foamy macrophages consistent with adiagnosis of HP.

Water samples from the hydroponics were drawn bythe family members using sterile 100ml vessels. Samplealiquots (undiluted; 1:10; 1:100; 1:1000; 3� 100 ml each)were plated onto malt extract agar (25 1C) and DG 18agar (25 and 37 1C). The number of colony formingunits (CFU) was counted after 48 h (at 37 1C) and after5–10 days (at 25 1C) and fungal CFUs were differen-tiated to species level by light microscopy according tostandard methods and keys (De Hoog et al., 2000;Samson et al., 1995). The samples revealed Aureobasi-

dium pullulans as the dominant fungal micro-organism(104CFU/ml) and other fungi at lower concentrations,i.e., Fusarium spp., Trichoderma viride, Acremonium spp.,

Penicillium corylophilum, Aspergillus versicolor.Screening for precipitating antibodies in the patient’s

serum was performed by a specialized laboratory(J. Sennekamp, Bonn). The investigation was based onthe usual solid phase peroxidase IgG ELISA using NuncMaxisorb Microplates according to Tijssen (1985) incombination with commercially available antigen pre-parations (detailed description in Sennekamp, 2004).Precipitating antibodies could be detected againstA. pullulans, as well as other antigens (strong reactionsagainst A. pullulans, pigeon, budgerigar; weak reactionsagainst Aspergillus versicolor, Aspergillus fumigatus,

Penicillium brevicompactum). The history and an inspec-tion of the home and school environments revealed nocontacts with birds.

We initiated oral treatment with 2mg/kg bodyweight/d prednisolone and advised the family to removethe hydroponics from their home. Four weeks later thesteroid dose was tapered and after an additional eightweeks stopped altogether. Clinical condition and lungfunction tests slowly improved. Six months later thelung function parameters, including an exercise test,presented within the age-adjusted reference values andhave remained so without any treatment for more thantwo years.

Discussion

In this report we describe a case of childhood HPassociated with fungal contamination of hydroponics.

Although once believed to be an adult disease because ofits frequent association with occupational settings, HPexists in the paediatric population and often goesunrecognized (Venkatesh and Wild, 2005). In mostreported paediatric cases, hypersensitivity pneumonitisresults from exposure to avian antigens, but it has alsobeen seen with exposure to moulds and some otherantigens (Fan, 2002). Possible mould sources include,for example, extensive exposure to an unventilatedbasement shower (Hogan et al., 1996); fungal growthin older wooden homes stimulated by the warm, moistsummers in the central and southern parts of Japan(Iyori et al., 1991; Ando et al., 1995); exposure to moistor mouldy hay or grains (Bureau et al., 1979;Thorshauge et al., 1989); exposure to organic compostin a play area (Aebischer et al., 2002), or mouldcontamination of home humidifiers (Miller et al., 1976;Suda et al., 1995; Patterson et al., 1998). It must beassumed, however, that any antigen that can cause HPin adults can also cause the disease in susceptiblechildren exposed to it.

In this case report, the diagnosis of HP relied uponthe typical clinical symptoms and signs developed in anappropriate setting for childhood HP, demonstratingfine nodular and reticular densities on chest radio-graphs, serum precipitating antibodies against offendingantigens with proven exposure to this antigen, alymphocytic alveolitis on BAL, and a correspondingreaction on the lung biopsy, thus fulfilling the majordiagnostic criteria of HP (Knutsen et al., 2006; Lacasseet al., 2003; Schwartz and Patterson, 1983; Terho, 1986;Richerson et al., 1989; Schuyler and Cormier, 1997).Childhood HP is often associated with exposure toantigens in the home environment and the mostsignificant diagnostic tool is a detailed environmentalexposure history and inspection (Knutsen et al., 2006;Venkatesh and Wild, 2005).

Based upon a thorough investigation, hydroponicscontaminated with A. pullulans (and other fungi) wereidentified as the most probable source of the HP in thiscase report. This hypothesis is supported by the findingof precipitating antibodies against A. pullulans and bythe fact that the patient was symptom-free following theremoval of the hydroponics from the home, this beingthe only environmental intervention. Although precipi-tating antibodies against avian antigens could also bedetected, their clinical relevance seems unlikely as aproper evaluation of the domestic and school environ-ments found no exposure to birds or bird antigens.Precipitating antibodies to avian antigens are found in1–3% of non-exposed and 30–50% of exposed indivi-duals without evidence of HP (Fan, 2002; Lacasse et al.,2003; Sennekamp, 2004). To our knowledge, this is thefirst report of hydroponics being a source of fungalcontamination and associated allergic complaints in anindoor environment. In contrast, potting compost is well

ARTICLE IN PRESSS. Engelhart et al. / Int. J. Hyg. Environ. Health 212 (2009) 18–2020

known as a matrix favouring fungal growth, and hasbeen associated with allergic diseases (Velcovski andGraubner, 1981; Burge et al., 1982) as well asopportunistic infections in immunocompromised people(Summerbell et al., 1989; Lass-Florl et al., 2000).

A. pullulans is an ubiquitous and cosmopolitansaprophyte and has repeatedly been described as acause of HP in industrial settings (Woodard et al., 1988),as well as in the home (Velcovski and Graubner, 1981;Torok et al., 1981). Available data indicate that its mainhabitat is aerial plant parts. Additionally, A. pullulans

has frequently been isolated in different soils (exclusivelyin the surface layers) and liquids (fresh water, marinesediments, seawater, sewage, and other liquid wastematerials). The temperature range for growth is 2–35 1C,the optimum being 25 1C. A. pullulans has an unusuallyhigh resistance to both UV and X-rays (Domsch et al.,1980).

In summary, we conclude that hydroponics should beconsidered as a potential source of fungal contaminantswhen checking for indoor health complaints. Futureresearch should focus on fungal ecology and releasemechanisms, as well as on the proper maintenance ofhydroponics.

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