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,

Mycotoxins are low molecular weight non-volatile compounds
secreted by some fungi (moulds) species. They are toxic and stable
secondary metabolites, that confer competitive survival advan-
tages against other organisms (Arias et al., 2018; Mayer et al.,
2008; Miller, 1994). To date, 300 to 400 mycotoxins have been
identified; however, about 30 are of relevant concern for human
health. The major mycotoxin classes of concern are produced
mainly by Aspergillus, Penicillium and Fusarium mould genera
(Bünger et al., 2004; CAST, 2003; Sorenson, 1999). Other usually
occurring toxigenic moulds include species of Alternaria, Pae-
cilomyces, Rhizopus, Trichoderma and Trichothecium (Sorenson,
1999).
Mould growth is necessary for mycotoxin production, however,
a correlation does not necessarily exist between occurrence of
mycotoxigenic mould species and the presence of mycotoxins
(Engelhart et al., 2002; Mayer et al., 2008). Temperature, water
activity (aw), substrate composition, pH, oxygen, are among the
⇑ Corresponding author.
E-mail address: olivier.schlosser@suez.com (O. Schlosser).
2016).
The main exposure route for mycotoxins is oral intake of con-
taminated food (Degen, 2011; Fromme et al., 2016; Mayer et al.,
2008). Ingestion of mycotoxins may result in a variety of health
outcomes, including carcinogenic, immunosuppressive and toxic
effects, and these are mostly known from veterinary practice and
animal studies with oral intake (Bennett and Klich, 2003; Mayer
et al., 2008; Peraica et al., 1999). Mycotoxins that are of major con-
cern in agriculture have a substantial impact on human and animal
health in some developing countries (CAST, 2003; Wild and Gong,
2010) and are subject to extensive regulatory monitoring in most
western countries (Brera et al., 2016; Fromme et al., 2016;
Peraica et al., 1999).
In addition to intake of contaminated food, some people can be
exposed to mycotoxins in occupational settings or in water-
damaged buildings, due to the growth of mycotoxigenic mould
species on materials and products (Mayer, 2016; Täubel and
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
that potentially carries them or has been directly contaminated by
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-
ins at the workplace can be inhaled or achieve skin contact and
thus be responsible for exposure that adds to the burden due to
the dietary background exposure (Mayer et al., 2008; Degen,
2011). Moreover, there is evidence that inhalation of some myco-
toxins may be more harmful than oral exposure (Degen, 2011;
Gustarowska et al., 2014; Mayer et al., 2008; Viegas et al., 2018a)
and be involved in the aetiology of lung disease due to the inhala-
tion of organic dust (Bünger et al., 2004).
Occupational exposure to airborne mycotoxins have mainly
been reported in studies dedicated to settings related to animal
husbandry, dairy and grain farming, or feed and food processing
(reviewed in: Brochard and Le Bâcle, 2010; Degen, 2011; Viegas
et al, 2018a). Most waste treatment systems provide conditions
of moisture and decomposition of organic matter that favour the
growth of fungi, and are thus considered critical with regard to
workers’ exposure to airborne fungi (Dutkiewicz, 1997;
Palmisano and Barlaz, 1996; Schlosser et al., 2012, 2015; Viegas
et al., 2015a, 2017). However, relatively few studies concerning
exposure to mycotoxins in this field have been published
(Bünger et al., 2004; Degen et al., 2003; Déportes et al., 1997;
Fischer et al., 1998, 1999, 2000a, 2000b, 2000c; Gerbl-Rieger
et al., 1999; Gutarowska et al., 2014; Mayer et al., 2012; Thiben,
2007; Viegas et al., 2015b, 2017). Moreover, almost all studies
reported qualitative data of mycotoxin identification, and quanti-
tative results of mycotoxin concentration in the air are quite lim-
ited. The need for more sensitive detection techniques was
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.
The first goal of this study was to estimate the level of occupa-
tional exposure to mycotoxins in the waste management field, and
notably in sectors where the biodegradable fraction of waste is
either subject to a recycling or energy recovery process or present
as residual organic matter in household segregated dry solid waste.
This project aimed to focus on mycotoxins that are particularly rel-
evant to occupational health in the waste management field. Four
mycotoxins, aflatoxine B1, gliotoxin, ochratoxin A and sterigmato-
cystin, were selected for analysis in air samples, using highly sen-
sitive new liquid chromatography-mass spectrometry
technologies. An additional goal was to assess the related health
risk for workers, and to evaluate whether the prevention measures
already in place against dust and bioaerosols in these occupational
settings were effective against these mycotoxins.
2. Material and methods
2.1. Selection of targeted mycotoxins
Main producing mould species and related toxic properties of
the four selected mycotoxins aflatoxine B1, gliotoxin, ochratoxin
A and sterigmatocystin are indicated in Table 1. This selection
was based on the following criteria: (i) the documented presence
in the air in waste management facilities of the mould species that
potentially produce these mycotoxins (Bünger et al., 2004;
Déportes et al., 1997; Degois et al., 2017; Fischer et al., 2000a;
Gutarowska et al., 2014; Madsen et al., 2019; Mbareche et al.,
2017, 2018; Schlosser et al., 2009; Skora et al., 2017; Tolvanen
et al., 2006; Viegas et al., 2015a; Wéry, 2014) and/or data on the
detection of these mycotoxins in air (Gerbl-Rieger et al., 1999;
Thiben, 2007) or in settled dust (Mayer et al., 2012); (ii) results
of biomonitoring studies, which demonstrated aflatoxine B1
(Viegas et a., 2015b) or ochratoxin A (Degen et al., 2003) biomark-
ers in composting or sorting plant workers; (iii) regarding glio-
toxin, the high prevalence of Aspergillus fumigatus within the
Table 1
Main producing mould species of the four selected mycotoxins and related toxic
properties.
Mycotoxins Main producing mould species Main toxic properties
Aflatoxin B1 Aspergillus flavus, A. parasiticus Hepatotoxic
Carcinogenic Group 1
IARC*
Genotoxic
Immunosuppressive
Gliotoxin A. fumigatus, A. niger, Cytotoxic
A. terreus, A. flavus Genotoxic
Immunosuppressive
Ochratoxin A A. ochraceus, A. niger, Penicillium Nephrotoxic
verrucosum Carcinogenic group
2B IARC*
Genotoxic
Teratogenic
Immunotoxic
Sterigmatocystin A. versicolor, A. nidulans, Carcinogenic group
A. flavus, A. parasiticus, 2B IARC*
Chaetomium spp. Immunotoxic
Genotoxic
*: IARC classification of carcinogens:
– Group 1: the agent is carcinogenic to humans. This category applies whenever
there is sufficient evidence of carcinogenicity in humans.
– 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
Group:  Limited evidence of carcinogenicity in humans,  Sufficient evidence of
carcinogenicity in experimental animals,  Strong evidence that the agent exhibits
key characteristics of carcinogens.
https://monographs.iarc.fr/wp-content/uploads/2019/07/Preamble-2019.pdf
mycoflora in waste management facilities (Bünger et al., 2004;
Fischer et al., 1998, 2000a; Gutarowska et al., 2014); and (iiii) the
potential severity of related health outcomes due to long-term
exposure, and especially carcinogenic, mutagenic and immunosup-
pressive effects (Arias et al., 2018; EFSA, 2013; IARC, 2012a; Mayer
et al., 2008; Ostry et al., 2017; Viegas et al., 2018a).
2.2. Selected sites
Five sites in France were selected for this study. Two sites are
mechanical–biological treatment (MBT) facilities (sites A and B),
two are large-scale industrial composting plants (sites C and D),
and one is a materials recovery facility (MRF) (site E).
The MBT facility A is a household waste methane fermentation
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
on the material size fraction. The MBT facility B is a compost pro-
duction plant, which receives household residual waste and
biodegradable waste from the agri-food industry, the mass distri-
bution and the collective catering in the region. For both facilities,
all processes are located indoor, except the aerobic pre-
fermentation tubes.
Sites C and D are both sewage sludge composting plants. Sludge
is mixed with crushed pallets and wood, and green waste. At the
site C, all process phases are located indoor, except compost stor-
age, whilst the site D is a totally enclosed facility. Aerobic decom-
position takes place in open boxes at the site C and in tunnels at
the site D, with negative and positive aeration, respectively. At
both sites, the process air is treated by an acid scrubbing tower
and the ambient air is dispersed by the wind after aerodynamic
propulsion.
The site E is a newly restructured MRF that has implemented
the extension for sorting instructions. These instructions mean that
households can segregate for separate collection all plastic packag-
ing, including pots such as yoghurt or cream pots, polyester trays
such as those used for meat or cheese, and plastic film, which is
 O. Schlosser et al. / Waste Management 105 (2020) 395–404
commonly used to shrink-wrap bottles, cover food trays or wrap
newspapers and magazines (Schlosser et al. 2015). In addition to
the mechanical sorting lines, the MRF is equipped with 8 sorting
lines where papers, cardboards, films and plastic packaging are
picked off by hand.
A more detailed description of the sites is provided in Supple-
mentary material in the online edition (Appendix A).
2.3. Sampling strategy
At each site, two air sampling campaigns were carried out, one
in the warm season (from April to September) and one in the cold
season (from October to March), with the exception of site E where
the two sampling campaigns were carried out in the cold season.
Stationary sampling (the sampler fixed on a tripod) and task-
based personal sampling (the sampler located in the breathing
zone of the worker) were carried out at each of the sites. During
the sampling periods, the operating conditions were normal.
As recommended by INRS (2018), the determination of myco-
toxins concentration in air was carried out by collecting dust with
a CIP 10 sampler (Tecora, France) equipped with the inhalable frac-
tion selector (the first version in our study), which is described in
other studies (Görner et al., 2006; Nieguitsila et al., 2011; Schlosser
et al., 2012). Briefly, this sampler uses the rotative cup technique
with rotation maintaining a flow rate of 10 L min-1. The cup of
the sampler was equipped with a porous polyurethane foam filter
(PUF). After sampling, the rotating cup containing the PUF was
removed from the sampler, closed by the cover and stored at
4 °C before analysis. The physical collection efficiency (i.e., the abil-
ity of the sampler to capture particles) of CIP-10 equipped with the
inhalable fraction selector is estimated to be 50% for particles with
an aerodynamic diameter of 1.8 mm and more than 95% for parti-
cles exceeding 2.8 mm (Görner et al., 2006). Calibration of the CIP
10 samplers was verified in the field by measuring the rotational
speed of the cup using an optical tachymeter (Tecora).
A total of 111 air samples were collected, comprising 52 station-
ary samples and 59 task-based personal samples. Work tasks con-
sisted of maintenance activities, cleaning tasks, monitoring rounds
and operational tasks including loader driving and manual sorting.
Sampling times ranged between 62 and 452 min for stationary
samples (median = 172 min), and from 51 to 296 min for personal
samples (median = 180 min). The first sampling campaign, at the
site C, was used to improve the analytical method and these mea-
surement data (N = 17) were not included in the final results.
Indoor temperature and relative humidity measurements were
taken at midday using Kimo-HD200Ò thermo-hygrometer (Kimo,
Montpon, France).
2.4. Sample analysis
The mass of suspended particulate matter collected in the CIP
10 foam was measured by gravimetric analysis using a balance
with 0.1 mg readability (Mettler Toledo AT200, Switzerland). The
mass measurement was corrected for variations in hygrometry.
The four selected mycotoxins were analysed quantitatively
applying ultra-performance liquid chromatography coupled with
high resolution mass spectrometry (UPLC-Q-Orbitrap HRMS).
Detailed information on mycotoxins analysis is provided in Supple-
mentary material in the online edition (Appendix B and Table S1).
Briefly, mycotoxins were recovered from the PUF by extraction
with methanol and capsules of the PUF were rinsed to recover all
particles of dust. Internal standards solutions were spiked directly
on the PUF before extraction. Chromatographic separation was
performed on a BEH C18 column (2.1 mm  10 mm, 1.7 mm) and
pre-column (WatersÒ) using a Dionex Ultimate 3000 ultrahigh-
performance liquid chromatography system (Thermo Fisher Scien-
397
tificTM). Mass spectrometry detection was carried out on a Q-
Exactive mass spectrometer (Thermo Fisher ScientificTM) operated
in positive electro-spray ionization (ESI (+)) mode. The calibration
curves were developed for each analyte in a mixture of water/
methanol (80/20, v/v) by spiking increasing concentrations of ref-
erence standards. The analytes were identified by matching the
retention times and accurate masses of product ions. The instru-
mental limit of quantification was 0.1 ng mL
1 for aflatoxin B1,
gliotoxin and sterigmatocytin and 0.2 ng mL
1 for ochratoxin A.
Mycotoxin concentration in air was expressed as ng m
3.
2.5. Health risk assessment
To date, no regulatory limits have been set for occupational
exposure to airborne mycotoxins. However, indirect methods of
risk assessment may be applied with which the level of exposure
to the airborne mycotoxin can be compared to benchmark values.
In a first step, we looked for health-based guidelines that were
available. The guideline can be either a Tolerable Daily Intake (TDI)
allowed for food or potency estimates for human cancer. The TDI
characterizes the total amount of the mycotoxin than can be
ingested daily over the lifetime without appreciable health risks
(Fromme et al., 2016). The TDI is expressed in ng per kg body
weight per day. The provisional tolerable weekly intake (PTWI)
of 100 ng per kg of body weight per week proposed by JECFA
(2007) for ochratoxin A and the equivalent TDI of 14 ng kg bw
1
per day were adopted. Cancer potency estimates were used for
aflatoxin B1, which is a genotoxic non-threshold carcinogen
(JECFA, 2017). The potency value is 0.01 liver cancers per
year/100,000 population per ng kg bw
1 per day for individuals
non infected by hepatitis B virus (HBsAg-) and 0.3 liver cancers
per year/100,000 population per ng of aflatoxins kg bw
1 per day
for individuals infected by hepatitis B virus (HBsAg+) (JECFA,
1999, 2017). Regarding ochratoxin A, the risk assessment method
consisted in directly comparing the dose of inhaled mycotoxin
per day with the TDI allowed for food (Halstensen et al., 2004;
Mayer et al., 2007, 2008, 2012; Tangni and Pussemier, 2007). With
regards to aflatoxin B1, the method consisted in estimating the risk
of liver cancer associated with the inhaled daily dose.
The inhaled daily dose of mycotoxin was calculated as follows:
Di ¼ C  Q r  t  k=bw
where: Di = inhaled daily dose (in ng per kg bw per day), C = time-
weighted average concentration of mycotoxin in air (in ng m
3),
Qr = respiratory flow rate (in m3 min
1), t = duration of exposure
per day (in min d
1), k = proportion of working days per year
(0.625, without unit), bw = body weight (60 kg).
Four different scenarios were constructed based on the tasks
that make up the work day, the work task-related concentration
of mycotoxin in air, and two levels of respiratory flow rate, 18 L
min
1 and 27 L min
1 for light workload and moderate workload
task, respectively, according to Horwat and Meyer (1998) and the
workload level classification from ISO 8986:1987 standard
(1987). Two additional scenarios included the wearing of a filtering
face piece respirator FFP3 during cleaning tasks. According to INRS,
the assigned protection factor of FFP3 was estimated at 10
(Guimon, 2019). For each scenario, the estimated inhaled daily
dose was compared to the TDI or was used to calculate the attribu-
table risk of liver cancer. In addition, in order to assess health risk
associated to both occupational and dietary exposure to the myco-
toxin, the daily intake from food was also taken into account
(Degen, 2011). Data of dietary exposure to mycotoxins in France
were provided by the second French total diet study (Sirot et al.,
2013). In the upperbound approach where the measurement
results below the limit of quantification (LOQ) were replaced with
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
per day, respectively. Assumption was made that bioavailability by
respiratory route was similar to that by ingestion.
For gliotoxin and sterigmatocystin, no health-based guideline
has been established (CAST, 2003; EFSA, 2013). The method we
used is based on the Threshold of Toxicological Concern (TTC) con-
cept, introduced by the U.S. Food and Drug Administration in 1995
for substances for which no chemical-specific toxicity data is avail-
able (FDA, 1995). The TTCs are based on known structure-activity
relationship. The concentration of no toxicological concern
(CoNTC) was derived for application to inhaled chemical sub-
stances, and the lifetime average CoNTC value was established at
30 ng m
3 (Drew and Frangos, 2007). With this approach, which
has already been applied to mycotoxin inhalation (Hardin et al.,
2009), the time-weighted average concentration of mycotoxin
was thus directly compared to the CoNTC.
3. Results
3.1. Indoor air parameters
The midday indoor temperature ranged from 6.0 to 16.0 °C dur-
ing the cold season sampling campaigns, and from 25.0 to 30.0 °C
during the warm season ones. The midday indoor relative humid-
ity ranged between 21% and 72% during the cold season sampling
campaigns, and between 45% and 72% during the warm season
campaigns.
3.2. Inhalable dust
Overall, the mass of sampled dust ranged from <0.1 mg to
74.6 mg, with a median value of 2.7 mg (Table 2). In stationary
samples, median dust concentration ranged between 1.0 and
7.4 mg m
3 depending on the site, and the 95th centile was
27.3 mg m
3. Highest concentrations were measured at the
mechanical sorting area in MBT facilities, at the screening area in
sludge composting plants, and at the process area (i.e., mechanical
separation and optical separation area) in the MRF. In work task-
based personal samples, median dust concentration ranged
between 0.4 and 2.5 mg m
3 depending on the site. However, vari-
ability in dust exposure was large, and the highest level reached
51.2 mg m
3. The 95th centile was 30.3 mg m
3, and the highest
exposure levels (>5 mg m
3) were all measured during ground
and equipment cleaning tasks, whatever the site.
3.3. Mycotoxins
Of the 94 samples, 10 (11%) showed quantifiable measurement
results (Table 3). Quantified mycotoxins were aflatoxin B1 (in 3
samples) and sterigmatocystin (in 8 samples), in both MBT facili-
ties and the MRF. In one sample at the MRF, aflatoxin B1 and sterig-
Table 2
Mass of sampled dust and concentration in air. Median (Min-Max).
Site Activity Type of sampling
A MBT Stationary
Personal
B MBT Stationary
Personal
C Sludge composting Stationary
Personal
D Sludge composting Stationary
Personal
E MRF Stationary
Personal
N: number of samples; MBT: mechanical and biological treatment; MRF: materials recovery facility.
matocystin were both quantified. Gliotoxin and ochratoxin A were
not quantified in any of the samples. None of these four targeted
mycotoxins were quantified in sludge composting plants or at
the composting unit in the MBT facilities.
Aflatoxin B1 and sterigmatocystin were quantified in both sta-
tionary and personal air samples. In stationary samples, aflatoxin
B1 and sterigmatocystin were quantified at the mechanical separa-
tion area, in both MBT facilities and the MRF. Concentration of afla-
toxin B1 was 0.06 ng m
3, and concentration of sterigmatocystin
ranged between 0.01 and 0.32 ng m
3. Regarding personal sam-
pling, aflatoxin B1 and sterigmatocystin were quantified during
cleaning tasks and manual sorting. None of the 14 samples col-
lected during front-end loader driving showed quantifiable mea-
surement. The level of exposure to aflatoxin B1 was 0.98 ng m
3
during compressed-air cleaning at the mechanical separation area
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-
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
monitoring round, and reached 0.92 ng m
3 during a cleaning task.
Sterigmatocystin concentration was not significantly correlated to
inhalable dust (Spearman test, rs = 0.190, P = 0.665). Due to only 3
measurement results above the LOQ, this correlation could not be
estimated for aflatoxin B1.
3.4. Health risk assessment
3.4.1. Risk of liver cancer due to inhaled aflatoxin B1
The highest concentration of aflatoxin B1 (0.98 ng m
3) was
measured at the MBT site B during compressed-air cleaning of
the equipment at the mechanical separation area (Table 3). This
concentration was used for inhaled dose calculation. Otherwise,
exposure to aflatoxin B1 was estimated at 0.1 ng m
3, which was
consistent with both other quantified measurements and the
LOQ. The description of the 6 working day scenarios (S1-S6) is
shown in Table 4. These scenarios differ according to duration
and frequency of the compressed-air cleaning task, the workload-
related respiratory flow rate, and depending on whether or not a
respiratory protective equipment (a filtering face piece FFP3) was
worn during the compressed-air cleaning task. In the worst-case
scenarios (S1 and S4), the daily mean exposure to aflatoxin B1
was estimated at the highest measured concentration of aflatoxin
B1, that is 0.98 ng m
3. In scenarios close to actual operating con-
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
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-
io, the estimated mean dose of inhaled aflatoxin B1 ranges
between 0.009 and 0.132 ng kg bw
1 per day (Table 4).
Based on the potency value of 0.01 liver cancers per
year/100,000 population per ng of aflatoxin B1 kg bw
1 per day
N Mass of sampled dust (mg) Dust concentration in air (mg m
3)
12 2.9 (0.6–25.8) 1.5 (0.3–8.4)
9 2.4 (0.3–9.8) 1.5 (0.1–3.4)
10 2.5 (0.7–3.2) 1.5 (0.6–3.0)
11 2.0 (<0.1–59.4) 1.1 (<0.1–35.8)
4 11.3 (3.5–39.5) 7.4 (1.2–28.8)
5 0.8 (0.5–1.7) 0.4 (0.4–1.3)
11 6.1 (2.4–74.7) 5.2 (2.0–39.0)
10 3.8 (0.7–36.9) 2.5 (0.4–51.2)
7 3.3 (<0.1–4.1) 1.0 (<0.1–4.5)
15 2.8 (0.8–29.4) 1.2 (0.6–28.0)
 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
of liver cancer due to inhaled aflatoxin B1 at the workplace ranges
between 9.0  10
10 (S3) and 1.3  10
8 (S4) per year (Table S2 in
Supplementary material in the online edition). Based on a 30-times
higher potency value of liver cancer for individuals infected by
hepatitis B virus, the estimated risk ranges between 2.7  10
8
(S3) and 4.0  10
7 (S4) per year. Considering a 1.6% prevalence
rate of hepatitis B virus infection in the WHO European Region
(World Health Organization, 2019), the population-based esti-
mated risk of liver cancer due to inhaled aflatoxin B1 at the work-
place ranges between 1.3  10
9 (S3) and 1.9  10
8 (S4) per year.
Assuming an unchanged pattern of exposure to inhaled aflatoxin
B1 at the workplace, the 40-yr occupational lifetime estimated risk
of liver cancer due to inhaled aflatoxin ranges between 5.3  10
8
(S3) and 7.7  10
7 (S4).
Adding the daily intake from food to the inhaled dose provides
the daily aflatoxin B1 exposure results indicated in Table 5. In the
worst-case scenarios (S1 and S4), the inhaled dose of aflatoxin at
the workplace contributed up to 41% of the inhaled and ingested
doses combined (Dc). In scenarios close to actual operating condi-
tions (S2, S3, S5 and S6), the contribution of the inhaled dose did
not exceed 7.7%. Based on the upperbound approach of left-
censored data management and the 95th centile of dietary expo-
sure assumption, the estimated risk of liver cancer per year due
to ingested and inhaled combined exposure to aflatoxin B1 ranges
between 4.0  10
8 (scenario S3) and 4.9  10
8 (scenario S4) for
individuals not infected by hepatitis B virus (Table S3 in Supple-
mentary material in the online edition). This range is 1.2  10
6–
1.5  10
6 for individuals infected by hepatitis B virus, and
5.8  10
8 to –7.2  10
8 assuming a 1.6% prevalence rate of hep-
atitis B virus infection in the general population.
3.4.2. Comparison of ochratoxin A inhaled dose with the tolerable daily
intake
A TDI of 14 ng kg bw
1 per day derived from the JECFA PTWI of
100 ng kg bw
1 per week was used for the interpretation of ochra-
toxin A measurement results. In our series of measurements, the
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
over the working life was estimated at 0.013 ng kg bw
1 per day in
the worst-case scenario (S4). In the second French total diet study,
the estimated mean and 95th centile of the daily intake of ochra-
toxin A by the adult population were 1.92 and 3.23 ng kg bw
1
per day, respectively (Sirot et al., 2013). These doses are well below
the TDI, and the estimated inhaled dose of ochratoxin A at the
workplace did not exceed 0.7% of the average daily intake from
food.
3.4.3. Comparison of gliotoxin and sterigmatocystin measurement
data with the CoNTC
In these series of measurements, no concentration reached the
CoNTC value (30 ng m
3) (Table 3). The highest measurement
value was 33 times lower than the CoNTC.
4. Discussion
4.1. Mycotoxin measurement results
One of the main results of this study is the quantification of afla-
toxin B1 and sterigmatocystin in the air at the mechanical separa-
tion area in MBT facilities and in the MRF. These mycotoxins were
quantified in both stationary and personal air samples. To our
knowledge, this study is the first one in which personal sampling
in waste management facilities was carried out. These results sug-
gest workers can be exposed to aflatoxin B1 and/or sterigmato-
cystin in MBT facilities and MRFs. On the other hand, aflatoxin
B1 and sterigmatocystin were not quantified in any of air samples
collected in the sludge composting plants and at the composting
units in the MBT facilities, that is to say concentration, if not zero,
was below 0.08 ng m
3 and 0.04 ng m
3, respectively.
A few limited studies suggest workers in waste management
facilities may be exposed to airborne aflatoxin B1. These studies
reported either biomonitoring data or air sampling measurement
results. Viegas et al. (2015b) quantified aflatoxin B1 biomarker in
the serum of workers in waste sorting or composting units, whilst
it was below the limit of detection in the serum of all controls. Afla-
toxin B1 has been detected in the air in composting plants (Gerbl-
Rieger, 1999, cited by Mayer et al., 2008, and by Brochard and Le
Bâcle, 2010; Thiben, 2007) and concentrations were below
1 ng m
3. In our study, aflatoxin B1 measurement data support
the hypothesis of very low exposure, if any, to aflatoxin B1 in com-
posting facilities/units, and this finding does not conflict with pub-
lished data indicated above. For comparison purpose, in studies
conducted in the grain industry, the reported concentrations of
aflatoxin B1 in the air frequently reached several tens or hundreds
of ng m
3 (reviewed in Brochard and Le Bâcle, 2010, and Fromme
et al., 2016).
The discrepancy between the measurement results in MBT
facilities and MRF on one side and in composting plants/units on
the other side can be partly explained by temperature differences
between the materials being processed depending on the waste
treatment system. A. flavus can grow at temperatures up to
48 °C, but its optimum growth temperature is 37 °C (Hedayati
et al., 2007). Consequently, during composting, high temperatures
substantially decrease A. flavus populations and aflatoxin produc-
tion (Déportes, 1997; Fischer et al., 1998). That makes difference
with operation conditions at the mechanical separation area in
MBT facility and in MRFs, where aerobic decomposition of organic
matter is not as important and material does not reach a temper-
ature as high as in the composting process. Differences in compo-
sition and water activity of materials being processed and in
storage and retention time may be other explanations for the dis-
crepancy observed (CAST, 2003; Mayer, 2016; Vaamonde et al.,
2006), however, these factors were not explored in this study.
As far as we know, it is the first time sterigmatocystin was
detected (and quantified) in air samples in waste management
facilities. Sterigmatocystin is a mycotoxin that is produced by more
than 50 fungal species, of which A. versicolor is the most common
source (EFSA, 2013). Sterigmatocystin shares its biosynthetic path-
way with aflatoxins; however, A. versicolor and A. nidulans are
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
studies reported identification of sterigmatocystin-producing
Aspergillus species in waste or air samples in the waste industry
(Bünger et al., 2004; Déportes et al., 1997, Fischer et al., 2000a,
2000b, 2000c; Madsen et al., 2019; Viegas et al., 2017; Wéry,
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
composting facilities (Fischer et al., 1998, 2000a, 2000b). However,
though produced by most fungal strains, sterigmatocystin was not
detected in extracts from spore suspensions (Fischer et al., 2000a,
2000b), and some authors stressed that sterigmatocystin was thus
unlikely to occur in bioaerosols in composting plants (Fischer et al.,
2000b). In our study, sterigmatocystin was not quantified in air
samples in composting plants and composting units of MBT facili-
ties, and these results support the hypothesis mentioned above. On
the other hand, we quantified sterigmatocystin in 32% of samples
collected at the MRF, and notably in personal samples (5 out of 7
samples). Sterigmatocystin was also quantified in one sample in
one of the MBT facilities, at the mechanical separation area. These
results are innovative, and they are consistent with the findings of
Mayer et al. (2012), who detected sterigmatocystin in settled dust
samples taken on the ground of equipment surface at municipal
waste and waste papers recovery facilities. Differences in sterigma-
tocystin measurement results between MBT and MRF on one side,
and composting plants on the other, may be partly explained by
differences in temperature and water activity between the materi-
als depending on the waste treatment system, as emphasized
above for aflatoxin.
For both aflatoxin B1 and sterigmatocystin, the highest myco-
toxin level was associated with the highest level of inhalable dust,
which occurred during cleaning tasks (0.98 ng m
3/35.8 mg m
3,
and 0.92 ng m
3/28.0 mg m
3, respectively). However, regarding
sterigmatocystin, for which association with dust could be esti-
mated, no significant correlation was found. A lack of correlation
with dust has been reported in other studies, regarding metabo-
lites specific for A. fumigatus (Fischer et al.,1999) or ochratoxin A
(Iavicoli et al., 2002). These data suggest a heterogeneous distribu-
tion of mycotoxins in airborne dust and do not support the hypoth-
esis that inhalable dust may be used as a marker of exposure to
mycotoxins.
Another key result of this study is the absence of quantifiable
measures of ochratoxin A and gliotoxin. Ochratoxin A was not
quantified in any of the air samples we collected, that is to say con-
centrations, if not zero, were all below 0.1 ng m
3. Under temper-
ate climatic conditions, ochratoxin A is mainly produced by P.
verrucosum (Mayer et al., 2008) and A. ochraceus, A. carbonarius
and A. niger are other producing fungal species (IARC, 2012b).
Among these fungal species, A. niger is the one most frequently
reported in reviewed studies (Bünger et al., 2004; Fischer et al.,
2000a, 2000b; Viegas et al., 2017), and A. ochraceus was detected
in a few works (Gutarowska et al., 2014; Göttlich et al., 1994, cited
by Bünger et al., 2004). None of the studies in this review indicated
the identification of P. verrucosum in the mycoflora examined.
Results of ochratoxin A measurement in the air have been reported
in studies on grain handling, grain harvesting, coffee, cacao or
 O. Schlosser et al. / Waste Management 105 (2020) 395–404
spices processing industries and cowsheds (as reviewed by
Brochard G. and Le Bâcle C., 2010, and by Mayer, 2016); on the
other hand, data in the waste management field are quite limited.
Gerbl-Rieger (1999, cited by Mayer et al., 2008, and by Brochard
and Le Bâcle, 2010) reported ochratoxin A concentration between
0.58 and 31 pg m
3 in composting plants. Degen et al. (2003) anal-
ysed ochratoxin A serum levels in landfill workers, waste sorting
workers and controls. They concluded that their data pointed to
an additional uptake of ochratoxin A by inhalation in workers
exposed to bioaerosols, however, there was no statistical analysis
performed and the significance of the observed differences cannot
be stated. Consequently, evidence of exposure to ochratoxin A in
waste management facilities is limited, and our results do not con-
flict with the data in the literature.
Gliotoxin was selected as a targeted mycotoxin in this study
because it is mainly produced by A. fumigatus, which is known as
a quite prevalent fungal species in the organic waste management
field (Fischer et al., 1998, 1999; Pankhurst et al., 2011; Viegas et al.,
2017; Wéry, 2014), and because of its immunosuppressive proper-
ties (Arias et al., 2018; Kwon-Chung and Sugui, 2009). In our study,
gliotoxin was not quantified in any of the air samples either, that is
to say concentrations, if not zero, were all below 0.1 ng m
3. To the
best of our knowledge, no published study relating to the waste
management field reported detection of gliotoxin in air samples.
Fischer et al. (2000b, 2000c) detected gliotoxin in pure culture
extracts, but the authors failed to detect it in extracts from spore
suspensions. Moreover, in compost extract-based culture media,
A. fumigatus did not produce gliotoxin (Gutarowska et al., 2014).
The possibility of gliotoxin to be present in air should not be ruled
out, however, since gliotoxin was detected and quantified in per-
sonal air samples during the handling of cattle feed ration consti-
tuted by corn silage, oilseed cakes and hay (Lanier et al., 2010).
As far as we know, this study is nevertheless the only one that
reports gliotoxin occurrence in air, and to date there is no strong
evidence that supports the hypothesis of occupational exposure
to gliotoxin in waste management settings, and notably in com-
posting facilities. This statement is consistent with previous posi-
tions (Fischer et al., 1999).
4.2. Health risk assessment
The health risk assessment approaches provided results that do
not suggest that exposure to these targeted mycotoxins in waste
management facilities is a threat to workers’ health. For all four
selected mycotoxins, all levels of concentration in air were low
and did not reach 1 ng m
3 when quantifiable. These levels are
far below the CoNTC value of 30 ng m
3. Ochratoxin A was not
quantifiable in air samples, and the inhaled daily doses derived
from the highest LOQ in air in this series of analyses were clearly
lower than the TDI proposed by JECFA (2007). Furthermore, this
LOQ was also lower than the air quality criterion derived value
for ochratoxin A inhalation proposed by Pirard et al. (2016). This
quality criterion is 0.2 ng m
3, and by relating this quality criterion
to the time spent at the workplace, the derived value for inhalation
at the workplace is 0.84 ng m
3.
Regarding aflatoxin B1, based on conservative assumptions and
a worst-case scenario approach, the estimated population-based
risk of liver cancer due to inhaled aflatoxin did not reach 10
7
per year. For comparison purposes, the incidence rate of liver can-
cer in France in 2018 was estimated in men at 12.5 per 105 person-
year (Defossez et al., 2018).
Our findings are in line with those of previous works, such as
that of Degen (2011) who concluded in a review study that with
the exception of aflatoxins, inhalation exposure to mycotoxins
investigated so far in workers in Europe does not appear to add sig-
nificantly to their usually low exposure from dietary intake.
401
4.3. Strengths and limitations
The main methodological strengths of our study were the sam-
pling strategy, which involved three waste management sectors
and both stationary and personal air samplings, the use of UPLC-
HRMS for airborne mycotoxins quantitative analysis, which is a
highly sensible and specific method that enabled quantification
of low mycotoxin concentrations in air, and the interpretation of
measurement results for health risk assessment purposes. Most
of these characteristics make this study innovative.
Some methodological points deserve further comments. First,
the ability of the CIP-10 sampler equipped with the inhalable frac-
tion selector to capture small particles, and especially submicronic
particles, is low, less than 50% (Görner et al., 2006). Some studies
reported that the proportion of mycotoxins was higher in the alve-
olar fraction of grain dusts than in the inhalable one (Gareis and
Meussdoerffer, 2000; Ghosh et al., 1997). Furthermore, it has been
demonstrated that mycotoxins in indoor air can be carried by par-
ticles smaller than spores, such as fungal fragments and other
small particulates (Brasel et al., 2005). To our knowledge, no infor-
mation on size distribution of mycotoxin containing-particles is
available in the field of waste recycling and recovery. However,
the bioaerosol sampler we used may have underestimated the real
concentration of the targeted airborne mycotoxins.
Secondly, the use of the UPLC-HRMS method might suggest that
the analysis of the samples could have involved a higher number of
compounds in a presumptive approach to identifying non-targeted
mycotoxins. In our study, the analysis focused on four targeted
mycotoxins. A preliminary objective of this study was to select rel-
evant mycotoxins with regard to the chance of occurrence in the
waste management field and the potential severity of related
health outcomes due to long-term exposure. On the other hand,
the identification of potential mycotoxins in the waste environ-
ment was not an objective of this study, and UPLC-HRMS was
not used for this purpose. Further studies could quantify other
mycotoxins of health concern in air samples and contribute to
increasing knowledge of potential exposure in the waste manage-
ment field.
Then, the health risk assessment approaches assumed that
mycotoxins inhaled with dust are absorbed and systematically
available. This hypothesis is strongly supported for aflatoxin B1
(Autrup et al., 1991) and experiments in rats showed that bioavail-
ability of ochratoxin A after intratracheal administration was very
high (Breithotz-Emanuelson et al., 1995). However, information is
not available for most mycotoxins and we assumed a 100% avail-
ability of airborne mycotoxins as usually applied in a conservative
way (Kelman et al., 2004; Mayer et al., 2007).
Dermal contact could be a frequent route of exposure to myco-
toxins in some occupational settings (Viegas et al., 2018a). How-
ever, regarding aflatoxins, it has been reported that, in vitro,
aflatoxins penetrate very slowly and in small quantities through
the human epidermis (Brochard and Le Bâcle, 2010). Moreover,
workers in waste management facilities usually wear gloves and
long-sleeved clothes that reduce the surface of exposed skin. Along
with a gap of knowledge about systemic consequences of dermal
exposure to mycotoxins, we therefore did not consider this route
of exposure for health risk assessment. Analysis of biomarkers in
biological fluids is the best way to consider all potential routes of
exposure to mycotoxins and to assess the internal exposure
(Brochard and Le Bâcle, 2010; Degen, 2011; Viegas et al., 2015b),
however, it was not the purpose of this work.
Multi-exposure to mycotoxins and potential inter-actions with
other compounds are other sources of uncertainty for risk assess-
ment. Although the concentration values in this study were low,
this issue should not be ruled out (Mayer et al., 2008; Tangni and
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
potential interactions (Mayer, 2016). In a study in waste recycling
plants for municipal waste and waste paper, Mayer et al. (2012)
detected 33 mycotoxins and 5 bacterial metabolites in settled dust
samples. This finding does not mean that all these compounds
were present in the air, however, multi-exposure was most likely.
Available data on the combined effects of mycotoxins are limited
(Mueller et al., 2013; Speijers and Speijers, 2004; Zouaoui et al.,
2016) and further research is needed.
4.4. Potential for health risk management
Our measurement results suggest that workers can be exposed
to aflatoxin B1 and/or sterigmatoscystin in mechanical and biolog-
ical treatment plants and in materials recovery facilities, notably
during cleaning work tasks. However, the levels of exposure were
low, and the results of health risk assessment approaches do not
suggest a significant threat to workers’ health. These data do not
suggest there is a need for specific prevention measures in addition
to those that should be put in place against other airborne biolog-
ical agents and dust (Goyer et al., 2001; Schlosser, 2019; Stagg
et al., 2013). However, as highlighted by IARC (2012b), the interest
of vaccination against hepatitis B virus should be emphasized,
since it would reduce the potency of aflatoxins in vaccinated pop-
ulations and consequently reduce the risk of liver cancer.
5. Conclusion
Decomposition of organic matter and moisture conditions in
most waste management facilities favour the growth of fungi.
Some of these fungi can produce mycotoxins, some of which can
be harmful to health. This study suggests that workers can be
exposed to airborne aflatoxin B1 and sterigmatocystin in mechan-
ical and biological treatment plants and in materials recovery facil-
ities. However, the levels of exposure were low and do not suggest
a significant threat to health. This study focused on four mycotox-
ins of highly relevant health concern. Along with future studies on
the adverse health effects of inhaled mycotoxins, further works
could contribute to increase knowledge on potential exposure to
other mycotoxins in the waste management field.
Acknowledgments
The authors wish to thank the waste management site man-
agers and operators for their cooperation during the sampling cam-
paigns. They are also grateful to Amélie Guillon for her advice and
constructive comments on the mycotoxin analysis section. Funding
for this project was provided by SUEZ. The authors declare no con-
flict of interest relating to the material presented in this article. Its
contents, including any opinions and/or conclusions expressed, are
solely those of the authors.
Appendix A. Supplementary material
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.wasman.2020.02.031.
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