Waste Management 105 (2020) 395–404

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Waste Management
journal homepage: www.elsevier.com/locate/wasman

Airborne mycotoxins in waste recycling and recovery facilities:

Occupational exposure and health risk assessment
Olivier Schlosser ⇑, Samuel Robert, Naike Noyon
SUEZ, CIRSEE, 38 rue du Président Wilson, 78230 Le Pecq, France

a r t i c l e i n f o a b s t r a c t

Article history: Mycotoxins are metabolites secreted by certain types of moulds, and some of them can be harmful to
Received 27 November 2019 health. The objective of this study was to estimate the level of exposure to airborne aflatoxin B1, ochra-
Revised 7 January 2020 toxin A, gliotoxin and sterigmatocystin in waste recycling and recovery facilities. An additional goal was
Accepted 23 February 2020
to assess the related health risks for workers. Targeted mycotoxins were analysed quantitatively in 94 air
samples collected in five sites using ultra-performance liquid chromatography coupled with high resolu-
tion mass spectrometry. The level of exposure to mycotoxin during working day scenarios was compared
Keywords:
to benchmark values, either health-based guidelines when available or the concentration of no toxicolog-
Mycotoxin
Fungi
ical concern (CoNTC) when not. Eleven per cent of samples showed quantifiable measurement results.
Bioaerosols Aflatoxin B1 and sterigmatocystin were quantified at the mechanical separation area in mechanical–bi-
Waste management facilities ological treatment (MBT) facilities and in the materials recovery facility (MRF), but not in composting
Health risks plants and composting units in MBT facilities. The levels of exposure were all below 1 ng m
3. This is
the first time exposure to sterigmatocystin in waste management facilities is reported and quantified.
Ochratoxin A and gliotoxin were not quantified in any of the air samples. Health risk assessment
approaches did not suggest a significant threat to workers’ health. These data do not suggest the need
for specific prevention measures in addition to those against other airborne biological agents.
Ó 2020 Elsevier Ltd. All rights reserved.

1. Introduction factors that influence mycotoxin secretion (CAST, 2003; Mayer,

2016).
Mycotoxins are low molecular weight non-volatile compounds The main exposure route for mycotoxins is oral intake of con-
secreted by some fungi (moulds) species. They are toxic and stable taminated food (Degen, 2011; Fromme et al., 2016; Mayer et al.,
secondary metabolites, that confer competitive survival advan- 2008). Ingestion of mycotoxins may result in a variety of health
tages against other organisms (Arias et al., 2018; Mayer et al., outcomes, including carcinogenic, immunosuppressive and toxic
2008; Miller, 1994). To date, 300 to 400 mycotoxins have been effects, and these are mostly known from veterinary practice and
identified; however, about 30 are of relevant concern for human animal studies with oral intake (Bennett and Klich, 2003; Mayer
health. The major mycotoxin classes of concern are produced et al., 2008; Peraica et al., 1999). Mycotoxins that are of major con-
mainly by Aspergillus, Penicillium and Fusarium mould genera cern in agriculture have a substantial impact on human and animal
(Bünger et al., 2004; CAST, 2003; Sorenson, 1999). Other usually health in some developing countries (CAST, 2003; Wild and Gong,
occurring toxigenic moulds include species of Alternaria, Pae- 2010) and are subject to extensive regulatory monitoring in most
cilomyces, Rhizopus, Trichoderma and Trichothecium (Sorenson, western countries (Brera et al., 2016; Fromme et al., 2016;
1999). Peraica et al., 1999).
Mould growth is necessary for mycotoxin production, however, In addition to intake of contaminated food, some people can be
a correlation does not necessarily exist between occurrence of exposed to mycotoxins in occupational settings or in water-
mycotoxigenic mould species and the presence of mycotoxins damaged buildings, due to the growth of mycotoxigenic mould
(Engelhart et al., 2002; Mayer et al., 2008). Temperature, water species on materials and products (Mayer, 2016; Täubel and
activity (aw), substrate composition, pH, oxygen, are among the Hyvärinen, 2016). The routes of exposure are then inhalation and
dermal contact. Mycotoxins can be present in airborne particles,
such as fungal spores, fragments of spores and hyphae, and in dust
⇑ Corresponding author. that potentially carries them or has been directly contaminated by
E-mail address: [email protected] (O. Schlosser). mycotoxins excreted by the fungi (Fischer et al., 2000b; Fischer and

https://doi.org/10.1016/j.wasman.2020.02.031
0956-053X/Ó 2020 Elsevier Ltd. All rights reserved.
396 O. Schlosser et al. / Waste Management 105 (2020) 395–404

Dott, 2003; Mayer, 2016; Sorenson et al., 1999). Airborne mycotox- Table 1
ins at the workplace can be inhaled or achieve skin contact and Main producing mould species of the four selected mycotoxins and related toxic
properties.
thus be responsible for exposure that adds to the burden due to
the dietary background exposure (Mayer et al., 2008; Degen, Mycotoxins Main producing mould species Main toxic properties
2011). Moreover, there is evidence that inhalation of some myco- Aflatoxin B1 Aspergillus flavus, A. parasiticus Hepatotoxic
toxins may be more harmful than oral exposure (Degen, 2011; Carcinogenic Group 1
Gustarowska et al., 2014; Mayer et al., 2008; Viegas et al., 2018a) IARC*
Genotoxic
and be involved in the aetiology of lung disease due to the inhala- Immunosuppressive
tion of organic dust (Bünger et al., 2004). Gliotoxin A. fumigatus, A. niger, Cytotoxic
Occupational exposure to airborne mycotoxins have mainly A. terreus, A. flavus Genotoxic
been reported in studies dedicated to settings related to animal Immunosuppressive
Ochratoxin A A. ochraceus, A. niger, Penicillium Nephrotoxic
husbandry, dairy and grain farming, or feed and food processing
verrucosum Carcinogenic group
(reviewed in: Brochard and Le Bâcle, 2010; Degen, 2011; Viegas 2B IARC*
et al, 2018a). Most waste treatment systems provide conditions Genotoxic
of moisture and decomposition of organic matter that favour the Teratogenic
growth of fungi, and are thus considered critical with regard to Immunotoxic
Sterigmatocystin A. versicolor, A. nidulans, Carcinogenic group
workers’ exposure to airborne fungi (Dutkiewicz, 1997;
A. flavus, A. parasiticus, 2B IARC*
Palmisano and Barlaz, 1996; Schlosser et al., 2012, 2015; Viegas Chaetomium spp. Immunotoxic
et al., 2015a, 2017). However, relatively few studies concerning Genotoxic
exposure to mycotoxins in this field have been published
*: IARC classification of carcinogens:
(Bünger et al., 2004; Degen et al., 2003; Déportes et al., 1997; – Group 1: the agent is carcinogenic to humans. This category applies whenever
Fischer et al., 1998, 1999, 2000a, 2000b, 2000c; Gerbl-Rieger there is sufficient evidence of carcinogenicity in humans.
et al., 1999; Gutarowska et al., 2014; Mayer et al., 2012; Thiben, – Group 2B: the agent is possibly carcinogenic to humans. This category generally
applies when only one of the following evaluations has been made by the Working
2007; Viegas et al., 2015b, 2017). Moreover, almost all studies
Group:  Limited evidence of carcinogenicity in humans,  Sufficient evidence of
reported qualitative data of mycotoxin identification, and quanti- carcinogenicity in experimental animals,  Strong evidence that the agent exhibits
tative results of mycotoxin concentration in the air are quite lim- key characteristics of carcinogens.
ited. The need for more sensitive detection techniques was https://monographs.iarc.fr/wp-content/uploads/2019/07/Preamble-2019.pdf
stressed in several articles one or two decades ago (Degen, 2011;
Fischer et al., 2000b, 2000c; Halstensen et al., 2004; Mayer et al.,
2008, 2012) and may explain this lack of information. mycoflora in waste management facilities (Bünger et al., 2004;
The first goal of this study was to estimate the level of occupa- Fischer et al., 1998, 2000a; Gutarowska et al., 2014); and (iiii) the
tional exposure to mycotoxins in the waste management field, and potential severity of related health outcomes due to long-term
notably in sectors where the biodegradable fraction of waste is exposure, and especially carcinogenic, mutagenic and immunosup-
either subject to a recycling or energy recovery process or present pressive effects (Arias et al., 2018; EFSA, 2013; IARC, 2012a; Mayer
as residual organic matter in household segregated dry solid waste. et al., 2008; Ostry et al., 2017; Viegas et al., 2018a).
This project aimed to focus on mycotoxins that are particularly rel-
evant to occupational health in the waste management field. Four 2.2. Selected sites
mycotoxins, aflatoxine B1, gliotoxin, ochratoxin A and sterigmato-
cystin, were selected for analysis in air samples, using highly sen- Five sites in France were selected for this study. Two sites are
sitive new liquid chromatography-mass spectrometry mechanical–biological treatment (MBT) facilities (sites A and B),
technologies. An additional goal was to assess the related health two are large-scale industrial composting plants (sites C and D),
risk for workers, and to evaluate whether the prevention measures and one is a materials recovery facility (MRF) (site E).
already in place against dust and bioaerosols in these occupational The MBT facility A is a household waste methane fermentation
settings were effective against these mycotoxins. and compost production plant that treats residual household waste
and household source-separated biowaste with two process lines.
Digestate is either composted and refined, or stabilized, depending
2. Material and methods on the material size fraction. The MBT facility B is a compost pro-
duction plant, which receives household residual waste and
2.1. Selection of targeted mycotoxins biodegradable waste from the agri-food industry, the mass distri-
bution and the collective catering in the region. For both facilities,
Main producing mould species and related toxic properties of all processes are located indoor, except the aerobic pre-
the four selected mycotoxins aflatoxine B1, gliotoxin, ochratoxin fermentation tubes.
A and sterigmatocystin are indicated in Table 1. This selection Sites C and D are both sewage sludge composting plants. Sludge
was based on the following criteria: (i) the documented presence is mixed with crushed pallets and wood, and green waste. At the
in the air in waste management facilities of the mould species that site C, all process phases are located indoor, except compost stor-
potentially produce these mycotoxins (Bünger et al., 2004; age, whilst the site D is a totally enclosed facility. Aerobic decom-
Déportes et al., 1997; Degois et al., 2017; Fischer et al., 2000a; position takes place in open boxes at the site C and in tunnels at
Gutarowska et al., 2014; Madsen et al., 2019; Mbareche et al., the site D, with negative and positive aeration, respectively. At
2017, 2018; Schlosser et al., 2009; Skora et al., 2017; Tolvanen both sites, the process air is treated by an acid scrubbing tower
et al., 2006; Viegas et al., 2015a; Wéry, 2014) and/or data on the and the ambient air is dispersed by the wind after aerodynamic
detection of these mycotoxins in air (Gerbl-Rieger et al., 1999; propulsion.
Thiben, 2007) or in settled dust (Mayer et al., 2012); (ii) results The site E is a newly restructured MRF that has implemented
of biomonitoring studies, which demonstrated aflatoxine B1 the extension for sorting instructions. These instructions mean that
(Viegas et a., 2015b) or ochratoxin A (Degen et al., 2003) biomark- households can segregate for separate collection all plastic packag-
ers in composting or sorting plant workers; (iii) regarding glio- ing, including pots such as yoghurt or cream pots, polyester trays
toxin, the high prevalence of Aspergillus fumigatus within the such as those used for meat or cheese, and plastic film, which is
 O. Schlosser et al. / Waste Management 105 (2020) 395–404 397

commonly used to shrink-wrap bottles, cover food trays or wrap tificTM). Mass spectrometry detection was carried out on a Q-
newspapers and magazines (Schlosser et al. 2015). In addition to Exactive mass spectrometer (Thermo Fisher ScientificTM) operated
the mechanical sorting lines, the MRF is equipped with 8 sorting in positive electro-spray ionization (ESI (+)) mode. The calibration
lines where papers, cardboards, films and plastic packaging are curves were developed for each analyte in a mixture of water/
picked off by hand. methanol (80/20, v/v) by spiking increasing concentrations of ref-
A more detailed description of the sites is provided in Supple- erence standards. The analytes were identified by matching the
mentary material in the online edition (Appendix A). retention times and accurate masses of product ions. The instru-
mental limit of quantification was 0.1 ng mL
1 for aflatoxin B1,
2.3. Sampling strategy gliotoxin and sterigmatocytin and 0.2 ng mL
1 for ochratoxin A.
Mycotoxin concentration in air was expressed as ng m
3.
At each site, two air sampling campaigns were carried out, one
in the warm season (from April to September) and one in the cold 2.5. Health risk assessment
season (from October to March), with the exception of site E where
the two sampling campaigns were carried out in the cold season. To date, no regulatory limits have been set for occupational
Stationary sampling (the sampler fixed on a tripod) and task- exposure to airborne mycotoxins. However, indirect methods of
based personal sampling (the sampler located in the breathing risk assessment may be applied with which the level of exposure
zone of the worker) were carried out at each of the sites. During to the airborne mycotoxin can be compared to benchmark values.
the sampling periods, the operating conditions were normal. In a first step, we looked for health-based guidelines that were
As recommended by INRS (2018), the determination of myco- available. The guideline can be either a Tolerable Daily Intake (TDI)
toxins concentration in air was carried out by collecting dust with allowed for food or potency estimates for human cancer. The TDI
a CIP 10 sampler (Tecora, France) equipped with the inhalable frac- characterizes the total amount of the mycotoxin than can be
tion selector (the first version in our study), which is described in ingested daily over the lifetime without appreciable health risks
other studies (Görner et al., 2006; Nieguitsila et al., 2011; Schlosser (Fromme et al., 2016). The TDI is expressed in ng per kg body
et al., 2012). Briefly, this sampler uses the rotative cup technique weight per day. The provisional tolerable weekly intake (PTWI)
with rotation maintaining a flow rate of 10 L min-1. The cup of of 100 ng per kg of body weight per week proposed by JECFA
the sampler was equipped with a porous polyurethane foam filter (2007) for ochratoxin A and the equivalent TDI of 14 ng kg bw
1
(PUF). After sampling, the rotating cup containing the PUF was per day were adopted. Cancer potency estimates were used for
removed from the sampler, closed by the cover and stored at aflatoxin B1, which is a genotoxic non-threshold carcinogen
4 °C before analysis. The physical collection efficiency (i.e., the abil- (JECFA, 2017). The potency value is 0.01 liver cancers per
ity of the sampler to capture particles) of CIP-10 equipped with the year/100,000 population per ng kg bw
1 per day for individuals
inhalable fraction selector is estimated to be 50% for particles with non infected by hepatitis B virus (HBsAg-) and 0.3 liver cancers
an aerodynamic diameter of 1.8 mm and more than 95% for parti- per year/100,000 population per ng of aflatoxins kg bw
1 per day
cles exceeding 2.8 mm (Görner et al., 2006). Calibration of the CIP for individuals infected by hepatitis B virus (HBsAg+) (JECFA,
10 samplers was verified in the field by measuring the rotational 1999, 2017). Regarding ochratoxin A, the risk assessment method
speed of the cup using an optical tachymeter (Tecora). consisted in directly comparing the dose of inhaled mycotoxin
A total of 111 air samples were collected, comprising 52 station- per day with the TDI allowed for food (Halstensen et al., 2004;
ary samples and 59 task-based personal samples. Work tasks con- Mayer et al., 2007, 2008, 2012; Tangni and Pussemier, 2007). With
sisted of maintenance activities, cleaning tasks, monitoring rounds regards to aflatoxin B1, the method consisted in estimating the risk
and operational tasks including loader driving and manual sorting. of liver cancer associated with the inhaled daily dose.
Sampling times ranged between 62 and 452 min for stationary The inhaled daily dose of mycotoxin was calculated as follows:
samples (median = 172 min), and from 51 to 296 min for personal
Di ¼ C  Q r  t  k=bw
samples (median = 180 min). The first sampling campaign, at the
site C, was used to improve the analytical method and these mea- where: Di = inhaled daily dose (in ng per kg bw per day), C = time-
surement data (N = 17) were not included in the final results. weighted average concentration of mycotoxin in air (in ng m
3),
Indoor temperature and relative humidity measurements were Qr = respiratory flow rate (in m3 min
1), t = duration of exposure
taken at midday using Kimo-HD200Ò thermo-hygrometer (Kimo, per day (in min d
1), k = proportion of working days per year
Montpon, France). (0.625, without unit), bw = body weight (60 kg).
Four different scenarios were constructed based on the tasks
2.4. Sample analysis that make up the work day, the work task-related concentration
of mycotoxin in air, and two levels of respiratory flow rate, 18 L
The mass of suspended particulate matter collected in the CIP min
1 and 27 L min
1 for light workload and moderate workload
10 foam was measured by gravimetric analysis using a balance task, respectively, according to Horwat and Meyer (1998) and the
with 0.1 mg readability (Mettler Toledo AT200, Switzerland). The workload level classification from ISO 8986:1987 standard
mass measurement was corrected for variations in hygrometry. (1987). Two additional scenarios included the wearing of a filtering
The four selected mycotoxins were analysed quantitatively face piece respirator FFP3 during cleaning tasks. According to INRS,
applying ultra-performance liquid chromatography coupled with the assigned protection factor of FFP3 was estimated at 10
high resolution mass spectrometry (UPLC-Q-Orbitrap HRMS). (Guimon, 2019). For each scenario, the estimated inhaled daily
Detailed information on mycotoxins analysis is provided in Supple- dose was compared to the TDI or was used to calculate the attribu-
mentary material in the online edition (Appendix B and Table S1). table risk of liver cancer. In addition, in order to assess health risk
Briefly, mycotoxins were recovered from the PUF by extraction associated to both occupational and dietary exposure to the myco-
with methanol and capsules of the PUF were rinsed to recover all toxin, the daily intake from food was also taken into account
particles of dust. Internal standards solutions were spiked directly (Degen, 2011). Data of dietary exposure to mycotoxins in France
on the PUF before extraction. Chromatographic separation was were provided by the second French total diet study (Sirot et al.,
performed on a BEH C18 column (2.1 mm  10 mm, 1.7 mm) and 2013). In the upperbound approach where the measurement
pre-column (WatersÒ) using a Dionex Ultimate 3000 ultrahigh- results below the limit of quantification (LOQ) were replaced with
performance liquid chromatography system (Thermo Fisher Scien- the LOQ, the mean and the 95th centile French adult exposure to
398 O. Schlosser et al. / Waste Management 105 (2020) 395–404

aflatoxin B1 from food were estimated at 0.22 and 0.39 ng kg bw
1 matocystin were both quantified. Gliotoxin and ochratoxin A were
per day, respectively. Assumption was made that bioavailability by not quantified in any of the samples. None of these four targeted
respiratory route was similar to that by ingestion. mycotoxins were quantified in sludge composting plants or at
For gliotoxin and sterigmatocystin, no health-based guideline the composting unit in the MBT facilities.
has been established (CAST, 2003; EFSA, 2013). The method we Aflatoxin B1 and sterigmatocystin were quantified in both sta-
used is based on the Threshold of Toxicological Concern (TTC) con- tionary and personal air samples. In stationary samples, aflatoxin
cept, introduced by the U.S. Food and Drug Administration in 1995 B1 and sterigmatocystin were quantified at the mechanical separa-
for substances for which no chemical-specific toxicity data is avail- tion area, in both MBT facilities and the MRF. Concentration of afla-
able (FDA, 1995). The TTCs are based on known structure-activity toxin B1 was 0.06 ng m
3, and concentration of sterigmatocystin
relationship. The concentration of no toxicological concern ranged between 0.01 and 0.32 ng m
3. Regarding personal sam-
(CoNTC) was derived for application to inhaled chemical sub- pling, aflatoxin B1 and sterigmatocystin were quantified during
stances, and the lifetime average CoNTC value was established at cleaning tasks and manual sorting. None of the 14 samples col-
30 ng m
3 (Drew and Frangos, 2007). With this approach, which lected during front-end loader driving showed quantifiable mea-
has already been applied to mycotoxin inhalation (Hardin et al., surement. The level of exposure to aflatoxin B1 was 0.98 ng m
3
2009), the time-weighted average concentration of mycotoxin during compressed-air cleaning at the mechanical separation area
was thus directly compared to the CoNTC. at the site B, and 0.10 ng m
3 during manual sorting of newspapers
and magazines at the site E. The level of exposure to sterigmato-
3. Results cystin at the MRF (site E) ranged between 0.06 and 0.1 ng m
3 dur-
ing manual sorting (newspapers and magazines, cartons) and
3.1. Indoor air parameters monitoring round, and reached 0.92 ng m
3 during a cleaning task.
Sterigmatocystin concentration was not significantly correlated to
The midday indoor temperature ranged from 6.0 to 16.0 °C dur- inhalable dust (Spearman test, rs = 0.190, P = 0.665). Due to only 3
ing the cold season sampling campaigns, and from 25.0 to 30.0 °C measurement results above the LOQ, this correlation could not be
during the warm season ones. The midday indoor relative humid- estimated for aflatoxin B1.
ity ranged between 21% and 72% during the cold season sampling
campaigns, and between 45% and 72% during the warm season 3.4. Health risk assessment
campaigns.
3.4.1. Risk of liver cancer due to inhaled aflatoxin B1
3.2. Inhalable dust The highest concentration of aflatoxin B1 (0.98 ng m
3) was
measured at the MBT site B during compressed-air cleaning of
Overall, the mass of sampled dust ranged from <0.1 mg to the equipment at the mechanical separation area (Table 3). This
74.6 mg, with a median value of 2.7 mg (Table 2). In stationary concentration was used for inhaled dose calculation. Otherwise,
samples, median dust concentration ranged between 1.0 and exposure to aflatoxin B1 was estimated at 0.1 ng m
3, which was
7.4 mg m
3 depending on the site, and the 95th centile was consistent with both other quantified measurements and the
27.3 mg m
3. Highest concentrations were measured at the LOQ. The description of the 6 working day scenarios (S1-S6) is
mechanical sorting area in MBT facilities, at the screening area in shown in Table 4. These scenarios differ according to duration
sludge composting plants, and at the process area (i.e., mechanical and frequency of the compressed-air cleaning task, the workload-
separation and optical separation area) in the MRF. In work task- related respiratory flow rate, and depending on whether or not a
based personal samples, median dust concentration ranged respiratory protective equipment (a filtering face piece FFP3) was
between 0.4 and 2.5 mg m
3 depending on the site. However, vari- worn during the compressed-air cleaning task. In the worst-case
ability in dust exposure was large, and the highest level reached scenarios (S1 and S4), the daily mean exposure to aflatoxin B1
51.2 mg m
3. The 95th centile was 30.3 mg m
3, and the highest was estimated at the highest measured concentration of aflatoxin
exposure levels (>5 mg m
3) were all measured during ground B1, that is 0.98 ng m
3. In scenarios close to actual operating con-
and equipment cleaning tasks, whatever the site. ditions, the equipment was cleaned with compressed air 3 h a day
once every two weeks (S2, S3, S5 and S6), and the level of exposure
3.3. Mycotoxins to aflatoxin B1 for the remaining time was considered equal to the
highest value of LOQ, that is 0.1 ng m
3. Depending on the scenar-
Of the 94 samples, 10 (11%) showed quantifiable measurement io, the estimated mean dose of inhaled aflatoxin B1 ranges
results (Table 3). Quantified mycotoxins were aflatoxin B1 (in 3 between 0.009 and 0.132 ng kg bw
1 per day (Table 4).
samples) and sterigmatocystin (in 8 samples), in both MBT facili- Based on the potency value of 0.01 liver cancers per
ties and the MRF. In one sample at the MRF, aflatoxin B1 and sterig- year/100,000 population per ng of aflatoxin B1 kg bw
1 per day

Table 2
Mass of sampled dust and concentration in air. Median (Min-Max).

Site Activity Type of sampling N Mass of sampled dust (mg) Dust concentration in air (mg m
3)
A MBT Stationary 12 2.9 (0.6–25.8) 1.5 (0.3–8.4)
Personal 9 2.4 (0.3–9.8) 1.5 (0.1–3.4)
B MBT Stationary 10 2.5 (0.7–3.2) 1.5 (0.6–3.0)
Personal 11 2.0 (<0.1–59.4) 1.1 (<0.1–35.8)
C Sludge composting Stationary 4 11.3 (3.5–39.5) 7.4 (1.2–28.8)
Personal 5 0.8 (0.5–1.7) 0.4 (0.4–1.3)
D Sludge composting Stationary 11 6.1 (2.4–74.7) 5.2 (2.0–39.0)
Personal 10 3.8 (0.7–36.9) 2.5 (0.4–51.2)
E MRF Stationary 7 3.3 (<0.1–4.1) 1.0 (<0.1–4.5)
Personal 15 2.8 (0.8–29.4) 1.2 (0.6–28.0)

N: number of samples; MBT: mechanical and biological treatment; MRF: materials recovery facility.
 O. Schlosser et al. / Waste Management 105 (2020) 395–404 399

Table 3
Proportion of mycotoxin measurements above the limit of quantification and concentration in air of quantified mycotoxin.

Site (activity) Aflatoxin B1 Gliotoxin Ochratoxin A Sterigmatocystin

a
A (MBT) 0/21 0/21 0/21 1/21
(LOQ = 0.09 ng m
3) (LOQ = 0.09 ng m
3) (LOQ = 0.09 ng m
3) 0.01 ng m
3
B (MBT) 2/21 0/21 0/21 0/21
0.98 and 0.06 ng m
3 (LOQ = 0.04 ng m
3) (LOQ = 0.05 ng m
3) (LOQ = 0.03 ng m
3)
C (sludge composting) 0/9 0/9 0/9 1/9
(LOQ = 0.07 ng m
3) (LOQ = 0.01 ng m
3) (LOQ = 0.03 ng m
3) (LOQ = 0.03 ng m
3)
D (sludge composting) 0/21 0/21 0/21 1/21
(LOQ = 0.08 ng m
3) (LOQ = 0.04 ng m
3) (LOQ = 0.08 ng m
3) (LOQ = 0.04 ng m
3)
E (MRF) 1/22 0/22 0/22 7/22
0.10 ng m
3 (LOQ = 0.1 ng m
3) (LOQ = 0.1 ng m
3) 0.12 (0.06–0.92 ng m
3)b

In bold: measurements quantified.

a
: number of measurements above the LOQ/total number of samples; b: median (min–max).

Table 4
Description of working day scenarios and estimated inhaled dose of aflatoxin B1 per day.

Working day AFB1 concentration in air (ng m
3) Respiratory flow rate Duration and frequency of Dose of inhaled AFB1 (ng kg
scenario (L min
1) compressed-air cleaning bw
1 per day)
S1 0.98 during compressed-air cleaning task 18 All day long, every day 0,088
S2 0.98 during compressed-air cleaning task and 0.1 18 3 h a day once every 2 weeks 0,012
otherwise
S3 0.98 during compressed-air cleaning task with 18 3 h a day once every 2 weeks 0,009
FFP3* and 0.1 otherwise
S4 0.98 during compressed-air cleaning task 27 All day long, every day 0,132
S5 0.98 during compressed-air cleaning task and 0.1 27 3 h a day once every 2 weeks 0,018
otherwise
S6 0.98 during compressed-air cleaning task with 27 3 h a day once every 2 weeks 0,013
FFP3* and 0.1 otherwise

AFB1: aflatoxin B1; FFP3: Filtering face piece respirator class 3.

*
: according to INRS, the assigned protection factor of FFP3 is 10 (Guimon, 2019).

for individuals non infected by hepatitis B virus, the estimated risk doses combined (Dc). In scenarios close to actual operating condi-
of liver cancer due to inhaled aflatoxin B1 at the workplace ranges tions (S2, S3, S5 and S6), the contribution of the inhaled dose did
between 9.0  10
10 (S3) and 1.3  10
8 (S4) per year (Table S2 in not exceed 7.7%. Based on the upperbound approach of left-
Supplementary material in the online edition). Based on a 30-times censored data management and the 95th centile of dietary expo-
higher potency value of liver cancer for individuals infected by sure assumption, the estimated risk of liver cancer per year due
hepatitis B virus, the estimated risk ranges between 2.7  10
8 to ingested and inhaled combined exposure to aflatoxin B1 ranges
(S3) and 4.0  10
7 (S4) per year. Considering a 1.6% prevalence between 4.0  10
8 (scenario S3) and 4.9  10
8 (scenario S4) for
rate of hepatitis B virus infection in the WHO European Region individuals not infected by hepatitis B virus (Table S3 in Supple-
(World Health Organization, 2019), the population-based esti- mentary material in the online edition). This range is 1.2  10
6–
mated risk of liver cancer due to inhaled aflatoxin B1 at the work- 1.5  10
6 for individuals infected by hepatitis B virus, and
place ranges between 1.3  10
9 (S3) and 1.9  10
8 (S4) per year. 5.8  10
8 to –7.2  10
8 assuming a 1.6% prevalence rate of hep-
Assuming an unchanged pattern of exposure to inhaled aflatoxin atitis B virus infection in the general population.
B1 at the workplace, the 40-yr occupational lifetime estimated risk
of liver cancer due to inhaled aflatoxin ranges between 5.3  10
8 3.4.2. Comparison of ochratoxin A inhaled dose with the tolerable daily
(S3) and 7.7  10
7 (S4). intake
Adding the daily intake from food to the inhaled dose provides A TDI of 14 ng kg bw
1 per day derived from the JECFA PTWI of
the daily aflatoxin B1 exposure results indicated in Table 5. In the 100 ng kg bw
1 per week was used for the interpretation of ochra-
worst-case scenarios (S1 and S4), the inhaled dose of aflatoxin at toxin A measurement results. In our series of measurements, the
the workplace contributed up to 41% of the inhaled and ingested results were all below the LOQ, and the highest LOQ value was

Table 5
Estimation of the inhaled and ingested aflatoxin B1 doses combined (Dc) and ratio between inhaled dose and Dc.

Working day scenario Inhaled and ingested doses combined (Dc) Ratio between inhaled dose and Dc (%)
(ng kg bw
1 per day)
ma 95Pb ma 95Pb
S1 0.288 0.458 31 19
S2 0.229 0.399 5.2 3.0
S3 0.227 0.397 4.0 2.3
S4 0.322 0.492 41 27
S5 0.234 0.404 7.7 4.5
S6 0.230 0.400 5.7 3.3
a
: calculation considering the mean of the daily exposure from food in the French adult population (Sirot et al., 2013)
b
: calculation considering the 95th centile of the daily exposure from food in the French adult population (Sirot et al., 2013).
400 O. Schlosser et al. / Waste Management 105 (2020) 395–404

0.1 ng m
3. Substituting exposure for LOQ, the mean inhaled dose crepancy observed (CAST, 2003; Mayer, 2016; Vaamonde et al.,
over the working life was estimated at 0.013 ng kg bw
1 per day in 2006), however, these factors were not explored in this study.
the worst-case scenario (S4). In the second French total diet study, As far as we know, it is the first time sterigmatocystin was
the estimated mean and 95th centile of the daily intake of ochra- detected (and quantified) in air samples in waste management
toxin A by the adult population were 1.92 and 3.23 ng kg bw
1 facilities. Sterigmatocystin is a mycotoxin that is produced by more
per day, respectively (Sirot et al., 2013). These doses are well below than 50 fungal species, of which A. versicolor is the most common
the TDI, and the estimated inhaled dose of ochratoxin A at the source (EFSA, 2013). Sterigmatocystin shares its biosynthetic path-
workplace did not exceed 0.7% of the average daily intake from way with aflatoxins; however, A. versicolor and A. nidulans are
food. unable to transform sterigmatocystin into aflatoxin B1, so that sub-
strates colonized by these fungi may contain high amounts of
sterigmatocystin (EFSA, 2013; Viegas et al., 2018b). Numerous
3.4.3. Comparison of gliotoxin and sterigmatocystin measurement studies reported identification of sterigmatocystin-producing
data with the CoNTC Aspergillus species in waste or air samples in the waste industry
In these series of measurements, no concentration reached the (Bünger et al., 2004; Déportes et al., 1997, Fischer et al., 2000a,
CoNTC value (30 ng m
3) (Table 3). The highest measurement 2000b, 2000c; Madsen et al., 2019; Viegas et al., 2017; Wéry,
value was 33 times lower than the CoNTC. 2014), and sterigmatocystin was detected in extracts of pure cul-
tures of moulds that were cultivated from municipal solid waste
compost samples (Déportes et al., 1997) or from air sampled in
4. Discussion composting facilities (Fischer et al., 1998, 2000a, 2000b). However,
though produced by most fungal strains, sterigmatocystin was not
4.1. Mycotoxin measurement results detected in extracts from spore suspensions (Fischer et al., 2000a,
2000b), and some authors stressed that sterigmatocystin was thus
One of the main results of this study is the quantification of afla- unlikely to occur in bioaerosols in composting plants (Fischer et al.,
toxin B1 and sterigmatocystin in the air at the mechanical separa- 2000b). In our study, sterigmatocystin was not quantified in air
tion area in MBT facilities and in the MRF. These mycotoxins were samples in composting plants and composting units of MBT facili-
quantified in both stationary and personal air samples. To our ties, and these results support the hypothesis mentioned above. On
knowledge, this study is the first one in which personal sampling the other hand, we quantified sterigmatocystin in 32% of samples
in waste management facilities was carried out. These results sug- collected at the MRF, and notably in personal samples (5 out of 7
gest workers can be exposed to aflatoxin B1 and/or sterigmato- samples). Sterigmatocystin was also quantified in one sample in
cystin in MBT facilities and MRFs. On the other hand, aflatoxin one of the MBT facilities, at the mechanical separation area. These
B1 and sterigmatocystin were not quantified in any of air samples results are innovative, and they are consistent with the findings of
collected in the sludge composting plants and at the composting Mayer et al. (2012), who detected sterigmatocystin in settled dust
units in the MBT facilities, that is to say concentration, if not zero, samples taken on the ground of equipment surface at municipal
was below 0.08 ng m
3 and 0.04 ng m
3, respectively. waste and waste papers recovery facilities. Differences in sterigma-
A few limited studies suggest workers in waste management tocystin measurement results between MBT and MRF on one side,
facilities may be exposed to airborne aflatoxin B1. These studies and composting plants on the other, may be partly explained by
reported either biomonitoring data or air sampling measurement differences in temperature and water activity between the materi-
results. Viegas et al. (2015b) quantified aflatoxin B1 biomarker in als depending on the waste treatment system, as emphasized
the serum of workers in waste sorting or composting units, whilst above for aflatoxin.
it was below the limit of detection in the serum of all controls. Afla- For both aflatoxin B1 and sterigmatocystin, the highest myco-
toxin B1 has been detected in the air in composting plants (Gerbl- toxin level was associated with the highest level of inhalable dust,
Rieger, 1999, cited by Mayer et al., 2008, and by Brochard and Le which occurred during cleaning tasks (0.98 ng m
3/35.8 mg m
3,
Bâcle, 2010; Thiben, 2007) and concentrations were below and 0.92 ng m
3/28.0 mg m
3, respectively). However, regarding
1 ng m
3. In our study, aflatoxin B1 measurement data support sterigmatocystin, for which association with dust could be esti-
the hypothesis of very low exposure, if any, to aflatoxin B1 in com- mated, no significant correlation was found. A lack of correlation
posting facilities/units, and this finding does not conflict with pub- with dust has been reported in other studies, regarding metabo-
lished data indicated above. For comparison purpose, in studies lites specific for A. fumigatus (Fischer et al.,1999) or ochratoxin A
conducted in the grain industry, the reported concentrations of (Iavicoli et al., 2002). These data suggest a heterogeneous distribu-
aflatoxin B1 in the air frequently reached several tens or hundreds tion of mycotoxins in airborne dust and do not support the hypoth-
of ng m
3 (reviewed in Brochard and Le Bâcle, 2010, and Fromme esis that inhalable dust may be used as a marker of exposure to
et al., 2016). mycotoxins.
The discrepancy between the measurement results in MBT Another key result of this study is the absence of quantifiable
facilities and MRF on one side and in composting plants/units on measures of ochratoxin A and gliotoxin. Ochratoxin A was not
the other side can be partly explained by temperature differences quantified in any of the air samples we collected, that is to say con-
between the materials being processed depending on the waste centrations, if not zero, were all below 0.1 ng m
3. Under temper-
treatment system. A. flavus can grow at temperatures up to ate climatic conditions, ochratoxin A is mainly produced by P.
48 °C, but its optimum growth temperature is 37 °C (Hedayati verrucosum (Mayer et al., 2008) and A. ochraceus, A. carbonarius
et al., 2007). Consequently, during composting, high temperatures and A. niger are other producing fungal species (IARC, 2012b).
substantially decrease A. flavus populations and aflatoxin produc- Among these fungal species, A. niger is the one most frequently
tion (Déportes, 1997; Fischer et al., 1998). That makes difference reported in reviewed studies (Bünger et al., 2004; Fischer et al.,
with operation conditions at the mechanical separation area in 2000a, 2000b; Viegas et al., 2017), and A. ochraceus was detected
MBT facility and in MRFs, where aerobic decomposition of organic in a few works (Gutarowska et al., 2014; Göttlich et al., 1994, cited
matter is not as important and material does not reach a temper- by Bünger et al., 2004). None of the studies in this review indicated
ature as high as in the composting process. Differences in compo- the identification of P. verrucosum in the mycoflora examined.
sition and water activity of materials being processed and in Results of ochratoxin A measurement in the air have been reported
storage and retention time may be other explanations for the dis- in studies on grain handling, grain harvesting, coffee, cacao or
 O. Schlosser et al. / Waste Management 105 (2020) 395–404 401

spices processing industries and cowsheds (as reviewed by 4.3. Strengths and limitations
Brochard G. and Le Bâcle C., 2010, and by Mayer, 2016); on the
other hand, data in the waste management field are quite limited. The main methodological strengths of our study were the sam-
Gerbl-Rieger (1999, cited by Mayer et al., 2008, and by Brochard pling strategy, which involved three waste management sectors
and Le Bâcle, 2010) reported ochratoxin A concentration between and both stationary and personal air samplings, the use of UPLC-
0.58 and 31 pg m
3 in composting plants. Degen et al. (2003) anal- HRMS for airborne mycotoxins quantitative analysis, which is a
ysed ochratoxin A serum levels in landfill workers, waste sorting highly sensible and specific method that enabled quantification
workers and controls. They concluded that their data pointed to of low mycotoxin concentrations in air, and the interpretation of
an additional uptake of ochratoxin A by inhalation in workers measurement results for health risk assessment purposes. Most
exposed to bioaerosols, however, there was no statistical analysis of these characteristics make this study innovative.
performed and the significance of the observed differences cannot Some methodological points deserve further comments. First,
be stated. Consequently, evidence of exposure to ochratoxin A in the ability of the CIP-10 sampler equipped with the inhalable frac-
waste management facilities is limited, and our results do not con- tion selector to capture small particles, and especially submicronic
flict with the data in the literature. particles, is low, less than 50% (Görner et al., 2006). Some studies
Gliotoxin was selected as a targeted mycotoxin in this study reported that the proportion of mycotoxins was higher in the alve-
because it is mainly produced by A. fumigatus, which is known as olar fraction of grain dusts than in the inhalable one (Gareis and
a quite prevalent fungal species in the organic waste management Meussdoerffer, 2000; Ghosh et al., 1997). Furthermore, it has been
field (Fischer et al., 1998, 1999; Pankhurst et al., 2011; Viegas et al., demonstrated that mycotoxins in indoor air can be carried by par-
2017; Wéry, 2014), and because of its immunosuppressive proper- ticles smaller than spores, such as fungal fragments and other
ties (Arias et al., 2018; Kwon-Chung and Sugui, 2009). In our study, small particulates (Brasel et al., 2005). To our knowledge, no infor-
gliotoxin was not quantified in any of the air samples either, that is mation on size distribution of mycotoxin containing-particles is
to say concentrations, if not zero, were all below 0.1 ng m
3. To the available in the field of waste recycling and recovery. However,
best of our knowledge, no published study relating to the waste the bioaerosol sampler we used may have underestimated the real
management field reported detection of gliotoxin in air samples. concentration of the targeted airborne mycotoxins.
Fischer et al. (2000b, 2000c) detected gliotoxin in pure culture Secondly, the use of the UPLC-HRMS method might suggest that
extracts, but the authors failed to detect it in extracts from spore the analysis of the samples could have involved a higher number of
suspensions. Moreover, in compost extract-based culture media, compounds in a presumptive approach to identifying non-targeted
A. fumigatus did not produce gliotoxin (Gutarowska et al., 2014). mycotoxins. In our study, the analysis focused on four targeted
The possibility of gliotoxin to be present in air should not be ruled mycotoxins. A preliminary objective of this study was to select rel-
out, however, since gliotoxin was detected and quantified in per- evant mycotoxins with regard to the chance of occurrence in the
sonal air samples during the handling of cattle feed ration consti- waste management field and the potential severity of related
tuted by corn silage, oilseed cakes and hay (Lanier et al., 2010). health outcomes due to long-term exposure. On the other hand,
As far as we know, this study is nevertheless the only one that the identification of potential mycotoxins in the waste environ-
reports gliotoxin occurrence in air, and to date there is no strong ment was not an objective of this study, and UPLC-HRMS was
evidence that supports the hypothesis of occupational exposure not used for this purpose. Further studies could quantify other
to gliotoxin in waste management settings, and notably in com- mycotoxins of health concern in air samples and contribute to
posting facilities. This statement is consistent with previous posi- increasing knowledge of potential exposure in the waste manage-
tions (Fischer et al., 1999). ment field.
Then, the health risk assessment approaches assumed that
4.2. Health risk assessment mycotoxins inhaled with dust are absorbed and systematically
available. This hypothesis is strongly supported for aflatoxin B1
The health risk assessment approaches provided results that do (Autrup et al., 1991) and experiments in rats showed that bioavail-
not suggest that exposure to these targeted mycotoxins in waste ability of ochratoxin A after intratracheal administration was very
management facilities is a threat to workers’ health. For all four high (Breithotz-Emanuelson et al., 1995). However, information is
selected mycotoxins, all levels of concentration in air were low not available for most mycotoxins and we assumed a 100% avail-
and did not reach 1 ng m
3 when quantifiable. These levels are ability of airborne mycotoxins as usually applied in a conservative
far below the CoNTC value of 30 ng m
3. Ochratoxin A was not way (Kelman et al., 2004; Mayer et al., 2007).
quantifiable in air samples, and the inhaled daily doses derived Dermal contact could be a frequent route of exposure to myco-
from the highest LOQ in air in this series of analyses were clearly toxins in some occupational settings (Viegas et al., 2018a). How-
lower than the TDI proposed by JECFA (2007). Furthermore, this ever, regarding aflatoxins, it has been reported that, in vitro,
LOQ was also lower than the air quality criterion derived value aflatoxins penetrate very slowly and in small quantities through
for ochratoxin A inhalation proposed by Pirard et al. (2016). This the human epidermis (Brochard and Le Bâcle, 2010). Moreover,
quality criterion is 0.2 ng m
3, and by relating this quality criterion workers in waste management facilities usually wear gloves and
to the time spent at the workplace, the derived value for inhalation long-sleeved clothes that reduce the surface of exposed skin. Along
at the workplace is 0.84 ng m
3. with a gap of knowledge about systemic consequences of dermal
Regarding aflatoxin B1, based on conservative assumptions and exposure to mycotoxins, we therefore did not consider this route
a worst-case scenario approach, the estimated population-based of exposure for health risk assessment. Analysis of biomarkers in
risk of liver cancer due to inhaled aflatoxin did not reach 10
7 biological fluids is the best way to consider all potential routes of
per year. For comparison purposes, the incidence rate of liver can- exposure to mycotoxins and to assess the internal exposure
cer in France in 2018 was estimated in men at 12.5 per 105 person- (Brochard and Le Bâcle, 2010; Degen, 2011; Viegas et al., 2015b),
year (Defossez et al., 2018). however, it was not the purpose of this work.
Our findings are in line with those of previous works, such as Multi-exposure to mycotoxins and potential inter-actions with
that of Degen (2011) who concluded in a review study that with other compounds are other sources of uncertainty for risk assess-
the exception of aflatoxins, inhalation exposure to mycotoxins ment. Although the concentration values in this study were low,
investigated so far in workers in Europe does not appear to add sig- this issue should not be ruled out (Mayer et al., 2008; Tangni and
nificantly to their usually low exposure from dietary intake. Pussemier, 2007). Moreover, it is worth stressing that TDI values,
402 O. Schlosser et al. / Waste Management 105 (2020) 395–404

when available, do not account for these multi-exposure and analysis of aflatoxin B1 adducts to serum albumin. Scand. J. Work Environ.
Health 17, 436–440.
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detected 33 mycotoxins and 5 bacterial metabolites in settled dust Stachybotrys chartarum macrocyclic trichothecene mycotoxins on particulates
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Acknowledgments Fischer, G., Schwalbe, R., Ostrowski, R., Dott, W., 1998. Airborne fungi and their
secondary metabolites in working places in a compost facility. Mycoses 41,
383–388.
The authors wish to thank the waste management site man- Fischer, G., Müller, T., Ostrowski, R., Dott, W., 1999. Mycotoxins of Aspergillus
agers and operators for their cooperation during the sampling cam- fumigatus in pure culture and in native bioaerosols from compost facilities.
paigns. They are also grateful to Amélie Guillon for her advice and Chemosphere 38, 1745–1755.
Fischer, G., Müller, T., Schwalbe, R., Ostrowski, R., Dott, W., 2000a. Exposure to
constructive comments on the mycotoxin analysis section. Funding airborne fungi, MVOC and mycotoxins in biowaste-handling facilities. Int. J.
for this project was provided by SUEZ. The authors declare no con- Hyg. Environ. Health 203, 97–104.
flict of interest relating to the material presented in this article. Its Fischer, G., Müller, T., Schwalbe, R., Ostrowski, R., Dott, W., 2000b. Species-specific
profiles of mycotoxins produced in cultures and associated with conidia of
contents, including any opinions and/or conclusions expressed, are
airborne fungi derived from biowaste. Int. J. Hyg. Environ. Health 203, 105–116.
solely those of the authors. Fischer, G., Müller, T., Thißen, R., Schwalbe, R., Ostrowski, R., Dott, W., 2000c.
Mycotoxins of compost-derived airborne fungi in pure culture and in native
bioaerosols from compost facilities. Mycotoxin Res. 16 (Suppl 1), 94–98.
Appendix A. Supplementary material Fischer, G., Dott, W., 2003. Relevance of airborne fungi and their secondary
metabolites for environmental, occupational and indoor hygiene. Arch.
Microbiol. 179, 75–82.
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