Keywords

1 Introduction

Garbage is of high economic and ecologic worth. In Germany, garbage is collected separately and sorted (e.g. metals, sales packaging, glass, paper, electronic devices, and chemicals) for recycling. The ‘green dot’ DSD-company handles predominantly used sales packaging, e.g. from households. Despite high standards of environmental protection as well as protective measures for the workforce, the risk of exposure to bioaerosols remains. Neumann et al. (2002) detected 102–104 colony forming units (CFU) of molds per 1 m3 air at workplaces of garbage workers and up to 107 CFU/m3 during filling processes of garbage. In compost facilities, up to 105 CFU of molds per m3 were detected (Peersons et al. 2010).

Garbage workers may suffer from asthma due to various causes (e.g., bioaerosols, dust, or volatile organic compounds), but the literature shows no evidence of increased risk of allergic asthma in compost workers (Bünger et al. 2000; Schlosser et al. 2009; van Kampen et al. 2012) and only moderate evidence of increased risk of occupational asthma (OA) in garbage workers (Kuijer et al. 2010). Also, only a few cases of hypersensitivity pneumonitis (HP) have been described in compost workers (Bünger et al. 2007; Weber et al. 1993; Vincken and Roels 1984; Schlosser et al. 2009). The aim of this study was to appraise cases of garbage workers with respiratory diseases who were examined due to suspected occupational disease in the outpatient clinic of our institute (IPA) since 2002.

2 Methods

The study was performed in conformity with the Declaration of Helsinki of the World Medical Association and the protocol was approved by a local Ethics Committee.

Medical examinations were reconstructed based on the files of the accident insurance. The subjects were asked by an occupational physician for work-related symptoms, exposures to bioaerosols at their workplaces, atopic diseases, and smoking habits. They underwent a physical examination, extensive lung function testing (spirometry, body plethysmography and methacholine testing), and analysis of routine blood parameters. In cases 2–4, total IgE, and specific IgE and specific IgG antibodies to various molds and environmental allergens were measured by ImmunoCAP (Phadia, Freiburg, Germany). According to the manufacturer’s recommendations a specific IgE concentration of ≥0.35 kU/L (≥CAP-class 1) was considered positive. Specific IgG antibodies were measured with ImmunoCAP (Phadia); elevated IgG concentrations were assumed if the manufacturer’s cut-offs were exceeded. Skin prick tests (SPT) were performed with extracts of environmental allergens and molds and actinomycetes from various manufacturers (Bencard, Munich; HAL, Duesseldorf, Germany). Radiological examination included chest X-rays or a computed tomography (CT) of the thorax. Specific inhalation challenges (details see case descriptions) and measurements of exhaled nitric oxide (eNO; NIOX Flex; serial measurements: NIOX MINO; Aerocine, Solna, Sweden) were performed in accord with ATS/ERS recommendations.

3 Results

3.1 Compost Plants

3.1.1 Case 1

A 53-year-old male Caucasian smoker (20 cigarettes per day) worked in a composting plant from 1991 to 1996. He filled garbage chambers and evacuated them after a 7 days decomposing process. He used respiratory protection irregularly. Since 1993, the man experienced dyspnea on exertion, sometimes cough and phlegm. Physical examination demonstrated inspiratory crackles. X-rays of the thorax showed ‘spotted interstitial markings’ in both lungs. A diagnosis was not provided at that time. Two years later the symptoms persisted. Vital capacity of 65 % predicted was found, blood gas content was normal. IgG antibodies to Saccharopolyspora rectivirgula (38 kU/L; manufacturer’s cut-off 25 kU/L), Thermoactinomyces vulgaris (59 kU/L; manufacturer’s cut-off 25 U/mL) and Candida (74 kU/L; manufacturer’s cut-off 25 kU/L) were positive, whereas no IgG antibodies to Aspergillus fumigatus and Mucor spp. were found. Repeated X-rays of the thorax revealed a progression of the interstitial markings. A diagnosis of HP was made and the patient was advised to quit his job.

In 1997, 1 year after quitting the job, the patient still suffered from dyspnea on exertion, but had no cough. Physical examination showed weak inspiratory crackles, but spirometry, body plethysmography and CO diffusion capacitance as well as chest X-rays were in normal range. Methacholine testing was negative. SPT with common environmental allergens and intradermal tests with molds indicated a weak reaction with Fusarium culmorum, but specific IgE or enhanced specific IgG antibodies concentration to Saccharopolyspora rectivirgula, Thermoactinomyces vulgaris, Thermopolyspora polyspora, and Aspergillus fumigatus were not detectable. In a workplace-simulating challenge with biocompost in the laboratory lasting 30 min the patient showed no reaction. CT or bronchoscopy were not performed. A final diagnosis of HP was corroborated.

3.1.2 Case 2

A 41-year-old Pakistani was a never-smoker. Until his immigration to Germany in 1992 he worked in an office. In 1997 he started to work as a biological waste sorter in a composting plant; occasionally he worked as a cleaner in the same factory. Paper masks were used regularly. Since 1994 the patient suffered from upper airways infections. Fever and fatigue were manifest after working hours in 2000, whereas during weekends and holidays the complaints diminished. Since 2001 he suffered from chronic sinusitis. X-rays showed swelling of the mucous membranes of sinuses, but the thorax was normal. SPT with environmental allergens and molds gave no reactions. Spirometry revealed a reduction of FEV1/VC of 69 %. However, this test appeared qualitatively insufficient and ignored the ATS criteria. Dyspnea on exertion, flu-like symptoms, fever and shivering developed in 2003. Antiobstructive medication was used on demand since then. In 2005 he quit his job and became unemployed.

In 2006 the patient was examined at the IPA. He was symptom-free and without medication. Physical examination, laboratory investigations, and CT were normal. X-rays of the nasal sinuses showed a swelling of mucous membranes. Spirometry was normal, but methacholine testing revealed bronchial hyperresponsiveness. CO diffusion capacity and blood gases were normal. Skin prick tests were positive with Aspergillus fumigatus, Penicillium expansum and Penicillium chrysogenum, but not with environmental allergens from various manufacturers. Elevated specific IgE antibody to Aspergillus fumigatus (62 mgA/L; cut-off 39 concentrations to Aspergillus fumigatus (11 kU/L) and enhanced specific IgG antibody concentrations mgA/L) and Penicillium chrysogenum (47 mgA/L; cut-off 27 mgA/L) were detected. Total IgE was 637 kU/L. A final diagnosis of HP was made, but a concomitant OA could not be excluded.

3.2 DSD-Plants

3.2.1 Case 3

A 33-year-old, never smoking Tamil worked as a garbage sorter of packaging material in a DSD company from 1998 to 2004. Respiratory protection (FFP2 masks) was changed every day. In 1989, the patient got a replacement of his mitral valve. Since 2001 he developed fever, joint pain, cough with dark expectoration, and dyspnea on exertion. Symptoms occurred occasionally in the evenings after work days and diminished during vacations.

In 2004, symptoms increased and the patient lost body weight (10 kg in 3 months). Medical examination showed an absolute arrhythmia, but no rales in the lungs on auscultation. X-rays of the thorax presented diffuse ground-glass opacities in both lungs and CT showed patchy infiltrates, ill-defined centrilobular nodules and air trapping (Fig. 42.1). An increased number of lymphocytes was found in bronchoalveolar lavage (BAL), but no quantitative analysis was performed. A diagnosis of HP was made and the patient was advised to quit his job.

Fig. 42.1
figure 00421

X-rays of the patient (Case 3) in July 2001 (top left), January, 2005 (top right), November 2004 (bottom left), and January 2006 (bottom right). In July 2001, a normal picture of lungs with a synthetic mitral valve can be seen. Four years later, the lungs show diffuse ground-glass opacities, and in the CT patchy infiltrates, ill-defined centrilobular nodules, and air trapping. One year after exposure cessation in January 2006, the CT of the lungs is normal again

Full size image

In 2006, about 1 year after exposure cessation, the patient complained of mild dyspnea on exertion, but was otherwise symptom-free. Physical examination of the lung was normal, arrhythmia absoluta was corroborated by electrocardiography. SPT with common environmental allergens and molds were negative, as were specific IgE antibodies. IgG antibodies concentrations to Aspergillus fumigatus (39 mgA/L, manufacturers cut off: 39 mgA/L) were normal and minimally elevated to Penicillium chrysogenum (41 mgA/L, manufacturers cut off: 27 mgA/L). Spirometry and methacholine testing were normal, but CO diffusion capacity was slightly reduced (70 % predicted). Exercise testing showed normal blood gases. X-rays and CT of the lungs were normal (Fig. 42.1). A final diagnosis of HP was made.

3.2.2 Case 4

A 36-year old Caucasian smoker (10–20 cigarettes per day) worked as a driver in a DSD garbage plant from 1996 to 2002. In 2002 he started his work as a garbage sorter of packaging material. Since 2010 he worked again as a driver. Respiratory protection was never used. The patient was healthy without any allergic diseases until 2000 when he noticed rhinitis, later cough and dyspnea during work and post-shift. There was no history of fever. His otolaryngologist recorded multiple sensitizations to common environmental allergens by SPT and specific IgE concentrations to Alternaria tenuis (0.6 kU/L), rye grass (1.8 kU/L) and timothy grass (1.8 kU/L). Symptoms aggravated during the following years with improvement during vacations.

In 2010, the patient was referred to a pneumologist. Airway resistance was 0.34 kPa*s/L (<0.30). Specific IgG to Trichophyton spp. was slightly elevated (56 mgA/L; cut-off >30 mgA/L). FEV1 was 70 % predicted and FEV1/VC was 68 %. CO diffusion capacity was normal. CT of the thorax was normal. A diagnosis of asthma was made and antiobstructive medication was prescribed. Another examination performed by an otolaryngologist showed elevated specific IgE concentrations to Aspergillus fumigatus (26.9 kU/L), Alternaria alternata (5.2 kU/L), Dermatophagoides pteronyssinus (1.1 kU/L), Dermatophagoides farinae (1 kU/L), and timothy grass pollen (3.1 kU/L).

The patient was examined in May of 2011 without prior exposure cessation. He suffered from dry cough and variable work-related shortness of breath. Physical examination was normal. SPT were positive with Alternaria alternata (5 mm wheal diameter), Aspergillus fumigatus (4 mm), and small wheal diameters were recorded with house dust mites, grass pollen and ribwort. Total IgE was 166 kU/L. Specific IgE antibodies to mold mixture (5 kU/L), Aspergillus fumigatus (7 kU/L), Alternaria alternata (2 kU/L), and to various mites and grass pollen were detected. X-rays of the thorax were normal. Spirometry showed a mild obstructive pattern (FEV1 78 % predicted). Methacholine testing demonstrated bronchial hyperresponsiveness with a PD20FEV1 of 76 μg methacholine. Monitoring of daily FEV1 and eNO showed a decrease of eNO and an increase of FEV1 after cessation of exposure on June 3, 2011 (Fig. 42.2). The patient reported a decrease of his symptoms, but mild cough and expectoration persisted until reassessment on July 6, 2011. On this day, a specific inhalation challenge was performed.

Fig. 42.2
figure 00422

Serial measurement of FEV1 and eNO. Grey areas: working days, white areas: leisure time. After starting work, eNO increases and FEV1 decreases, whereas in leisure time eNO decreases and FEV1 increases

Full size image

The inhalative challenge was performed with an Aspergillus fumigatus extract from Allergopharma (Reinbek, Germany) and was carried out with a DeVilbiss 646 nebulizer and an APSpro dosimeter (Jäger, Höchberg, Germany) in quadrupling concentrations from 8 to 128 ng protein/mL (cumulative dose of 15 ng protein). Briefly, each dose was administered in ten consecutive slow inspirations from functional residual to near total lung capacity, while the nebulizer was actuated over 0.6 s. Inspiratory airflow was maintained close to 1 L*s−1 by observation of a visual scale. The time interval between consecutive steps was 15 min. The nebulizer was actuated 0.5 s after the start of inspiration to ensure a significant airflow upon nebulization. The response was evaluated by spirometry and body plethysmography (Masterlab, Jäger, Höchberg). Follow-up lung function measurements were carried out after 10, 20, 30 min, and then hourly from 1 to 5 h and after 24 h. The patient showed a significant increase of airway resistance from 0.35 to 0.83 kPa*s*L−1 and a decrease of FEV1 from 3,170 to 2,450 mL (22 % from baseline; Fig. 42.3). This was accompanied by shortness of breath. Symptoms and lung function gradually returned to baseline without medication.

Fig. 42.3
figure 00423

Specific inhalation test with Aspergillus fumigatus. After cumulative exposure of 15 ng, FEV1 decreased >20 % and sRt increased >2.0 kPa*s. eNO showed no change in 24 h

Full size image

After complete exposure cessation in June of 2011, the patient had a follow-up examination in 2012. He suffered from dyspnea on exertion and cough, but reported an important improvement of his symptoms. He inhaled topical steroids daily and short-acting beta agonists about twice per week. Physical examination showed wheezing after forced expiration. SPT reactions remained unchanged. Whereas sensitizations to environmental allergens and Alternaria alternata (1.94 kU/L) were unchanged, the concentration of specific IgE to Aspergillus fumigatus dropped from 6.5 to 1.8 kU/L. Spirometry showed a mild obstructive pattern (FEV1 75 % predicted). Bronchial hyperresponsiveness had improved slightly (PD20FEV1 of 147 μg methacholine). A final diagnosis of OA was made.

4 Discussion

Although garbage workers are exposed to high concentrations of airborne microbial organisms, epidemiologic data about health effects on the airways or lungs remain rare. This is also the case for allergic respiratory diseases. Very few cases with HP have been reported in garbage workers in the literature and to our knowledge no cases of allergic OA due to molds. Recently, it has been reported from Finland that molds from moisture damaged buildings are frequent causes of OA in contrast to Canada where such cases have not been found (Piipari and Keskinen 2005). These discrepancies suggest that diagnostic differences between both countries may exist.

Some diagnostic difficulties can be demonstrated in the four cases described in the present article. Prior diagnoses of OA (Cases 2 and 4) or HP (Cases 1 and 3) were made by the patients’ pneumologists. Three out of the four cases (Cases 1–3) had already quit their jobs since at least a year and were more or less symptom-free without lung function impairment. Thus, a complete diagnostic work-up including collection and analysis of BAL fluid or challenge tests was not considered due to ethical reasons. The final diagnoses of HP (Cases 1–3) were based on previous HP typical symptoms, the demonstration of enhanced mold- or actinomycetes-specific IgG antibody concentrations and improvement of symptoms after exposure cessation. In Case 3 we had additional information from CT and BAL. A diagnosis of OA in Case 2 could be excluded as the patient presented signs of both OA and HP. He also presented both specific IgE and IgG antibodies against Aspergillus fumigatus. The development of specific IgE and IgG antibodies to the same antigen is unusual. Rydjord et al. (2007) described an association between high mold exposure and the development of IgG antibodies to molds, whereas IgE antibodies were seen more often in low exposure scenarios and in susceptible subjects. IgG and IgE antibodies in that study were found to be correlated inversely. We found only a few case descriptions of combined asthma and hypersensitivity pneumonitis due to mold exposure in the literature. O’Brien et al. (1978) described a case with IgE and IgG antibodies to Merulis lacrymalis and diagnosed both asthma and HP. A similar combined diagnosis of asthma and HP due to Bjerkandarea adusta was described by Katayama et al. (2008). Only 4 case had not quit his job at the time of our examination and reported recent work related symptoms. Thus we considered performing the challenge testing in this case.

Although the diagnoses of HP in the presented cases may be questioned if stringent diagnostic criteria are applied, we consider the likelihood of a false positive diagnosis as low, as HP in garbage workers have been described (in less detail) also by others (Weber et al. 1993; Vincken and Roels 1984; Schlosser et al. 2009). Work related symptoms and a favorable course after exposure cessation, together with specific IgG antibodies, point to occupational reasons. HP has an overall good prognosis if symptomatic exposure duration is minimized. This is often the case in occupational HP because workers relate symptoms to work and quit their jobs. The primary examination of subjects with HP is often inconclusive and the diagnostic work-up for compensation has to find a compromise between the need for a valid diagnosis and the risk of invasive diagnostic tools in nearly asymptomatic subjects. Thus it is recommended that physicians involved in the primary diagnostic procedure should use the full spectrum of diagnostic tools (Sennekamp et al. 2007), including computed tomography of the thorax and BAL, which demonstrate high diagnostic specificity.