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Food Packaging and Shelf Life
journal homepage: www.elsevier.com/locate/fpsl
Microplastic contamination of packaged meat: Occurrence and associated
risks
Mikaël Kedzierski
a,
*, Benjamin Lechat
a
, Olivier Sire
b
, Gwénaël Le Maguer
c
, Véronique Le Tilly
b
,
Stéphane Bruzaud
a
a
IRDL UMR CNRS 6027, Université Bretagne Sud, 56100 Lorient, France
b
IRDL UMR CNRS 6027, Université Bretagne Sud, 56000 Vannes, France
c
Coordinator of the Archipel Institute, Université Bretagne Sud, 56100 Lorient, France
ARTICLE INFO
Keywords:
Microplastics
Extruded polystyrene
Fibres
Packaging
Contaminant
Human alimentation
ABSTRACT
Food trays are often made from extruded polystyrene (XPS), and quantities of millimetre-sized particles of this
material are trapped between the meat they contain and the sealing film. The purpose of this study is to identify
the chemical nature of these particles and quantify them. Furthermore, the quantification of synthetic or organic
fibres was also carried out. The results show that XPS microplastics (MP-XPS) contaminate food products at a
level ranging from 4.0 to 18.7 MP-XPS/kg of packaged meat. Analysis shows that these microplastics are likely to
come from the XPS trays. These particles are difficult to remove by mere rinsing and are probably cooked before
being consumed. However, at this stage, it is not clear from the scientific literature whether there is a potential
risk to humans associated with the ingestion of MP-XPS. In addition to these MP-XPS, it should also be pointed
out that fibres can also contaminate meat.
1. Introduction
Between 1950 and 2015, 7800 million tons of plastic were pro-
duced, half of which between 2002 and 2015 Geyer, Jambeck, & Law,
2017). The physical properties of plastic materials make them essential
in industrialized societies. In Europe, the packaging, construction, and
automotive sectors account for nearly 70 % of the demand for plastic,
with nearly 40 % for packaging alone (PlasticsEurope, 2018). In the
food sector, the use of plastic packaging helps in the storage, transport,
protection, and preservation of products while reducing their waste
(Lange & Wyser, 2003;Mathlouthi, 2013;Piringer & Baner, 2008;
PlasticsEurope, 2012). Because some plastics such as expanded poly-
styrene (EPS) or extruded polystyrene (XPS) provide a good protection
barrier from oxygen, water vapour, and microorganisms, they facilitate
the preservation of food products at a desired temperature; hence, they
are widely used in food packaging. However, it has been recently re-
ported that packaging may release plastic particles and subsequently
contaminate our food with plastic fragments (Oßmann et al., 2018;
Schymanski, Goldbeck, Humpf, & Fürst, 2018;Winkler et al., 2019).
The presence of small plastic particles in the natural environment
has been known since the early 1970s (Buchanan, 1971), but it is only
in the early 2010s that their presence in food was reported (Barboza,
Dick Vethaak, Lavorante, Lundebye, & Guilhermino, 2018). Among
these, microplastics, namely plastic particles smaller than 5 mm in size
(GESAMP, 2019), were found. In 2013, a study carried out on honey
and sugar coming from different countries revealed contamination by
fibres and fragments (Liebezeit & Liebezeit, 2013). Although no che-
mical analysis was performed to assess the chemical nature of these
particles, a connection was established between the morphology of
these fragments and the plastic bags used by beekeepers to supply sugar
to bees. In 2014, the identification of microplastics in mussels (Mytilus
edulis) grown for human consumption suggests that humans ingest these
particles (Van Cauwenberghe & Janssen, 2014). To date, several studies
have reported the presence of plastic particles in seafood and fish for
human consumption (Azevedo-Santos et al., 2019;Barboza & Gimenez,
2015). Microplastics have also been observed in salt (Gündoğdu, 2018;
Iñiguez, Conesa, & Fullana, 2017;Karami et al., 2017;Yang et al.,
2015), in beers (Kosuth, Mason, & Wattenberg, 2018;Liebezeit &
Liebezeit, 2014), and in water bottles (Mason, Welch, & Neratko, 2018).
These microplastics, generally smaller than 100 μm, probably come
partly from the packaging and/or bottling process (Mason et al., 2018).
A large-scale study of tap water showed that 81 % of the water sampled
was contaminated mainly by fibres of which an unknown part is of
synthetic origin (Kosuth et al., 2018). Fibres can be defined as particles
https://doi.org/10.1016/j.fpsl.2020.100489
Received 30 October 2019; Received in revised form 6 February 2020; Accepted 11 February 2020
⁎
Corresponding author.
E-mail address: mikael.kedzierski@univ-ubs.fr (M. Kedzierski).
Food Packaging and Shelf Life 24 (2020) 100489
2214-2894/ © 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/BY-NC-ND/4.0/).
T
of equal thickness along their entire length, the difference between
artificial and natural fibres being based on the presence or absence of
visible cellular or organic structures (Hidalgo-Ruz, Gutow, Thompson,
& Thiel, 2012). For the purposes of this publication, no distinction will
be made between artificial and natural fibres. The origin of the fibres
observed in food is not always clear, but airborne contamination is
often thought of. The atmosphere is an important vector of micro-
plastics, as shown by the atmospheric deposition of synthetic fibres in
Paris (Boucher & Friot, 2017;Dris, Gasperi, Saad, Mirande, & Tassin,
2016). These fibres are also omnipresent in our indoor environment to
the point of posing a significant risk of contamination of samples
(Dehaut, Hermabessiere, & Duflos, 2019). It is commonly accepted that
synthetic textiles are the main source of these fibres (Boucher & Friot,
2017;Prata, 2018).
This study is part of the OceanWise project, a European project
supported by the European funding program INTERREG Atlantic Area.
OceanWise aims to jointly develop a set of long-term measures to re-
duce the impact of expanded and extruded polystyrene (EPS/XPS)
products in the North-East Atlantic Ocean. Some economic activities,
which generate EPS/XPS waste, are particularly investigated in the
OceanWise project: the fishing industry (fisheries, aquaculture, sea-
food), the food industry (supermarket chains, distribution of vegetables,
fish, meat, fruit), consumer goods, outdoor festivals, and tourism. In
this context, several observations of more or less free sub-millimetre
particles inside food packaging with an XPS bottom containing meat
were made during a preliminary study for the OceanWise project tests.
These microparticles have the same colour as the XPS food packaging
that contained them. Faced with these elements, it was therefore
decided to verify the following hypotheses: Are these particles micro-
plastics of extruded polystyrene (MP-XPS)? What is the estimated mass
of MP-XPS per mass of meat? How many fibres are present on the
surface and inside the food packaging? In an attempt to determine the
origin of the particles and fibres as well as the timing of the deposition,
the distribution of MP-XPS was studied inside and outside the tray.
Thus, this preliminary study, limited to the case of France, seeks to
answer these questions and identify some elements of discussion re-
garding the possible origins of these particles, as well as the possible
consequences of ingesting them for human health.
2. Materials and methods
2.1. Sample collection and preparation
This study focuses on meat products (chicken) packed in extruded
polystyrene trays (230 × 140 × 20 mm). The mass of the pieces of meat
was determined by reading the mass displayed on the label on the
plastic packaging. Samples of meat from brands B, C, D had a roughly
equivalent mass (on average close to 250 g), while brand A meat
samples were slightly larger in mass (about 315 g) (Table 1). Products
from four different brands (named A, B, C, and D) were purchased in a
local supermarket (n = 3 by brand). No special conditions were taken
to transport (in few minutes) them to the laboratory.
It is necessary to take into consideration all the surfaces of the
packaging in order to describe the state of contamination of the tray
and obtain information on the sources of this contamination. Thus, the
outside of the packaging (i.e. tray and plastic film) was first rinsed with
distilled water. This rinsing water was then analysed to determine the
amounts of particles and fibres on the outside of the packaging. In order
to avoid generating MP-XPS when tearing offthe plastic film sealing the
trays, the tray openings were made with a scalpel. Then, after opening,
the meat was rinsed thoroughly until the thin layer of fat covering the
surface of the samples was completely collected. Finally, the inside of
the tray and plastic film were rinsed with distilled water. The rinsing
water was then vacuum filtered (Buchner JIPO, 62 mm) on a glass
microfiber filter (pore diameter: 0.8 μm, diameter 55 mm, Fisherbrand
MF300). This step allows the fat layer to be vacuumed with the water,
while the particles remain trapped on the surface of the filter. In order
to limit external contamination by fibres, rinsing the packaging and
meat and filtering were carried out under a funnel hood. The operators
conducting the experiments wore a cotton grown and nitrile gloves to
avoid contamination by fibres from their clothing. The glassware used
was systematically rinsed at least three times with distilled water and
one last time with ethanol. After the filtration step, the filters were
stored in glass petri dishes also in order to limit contamination by the
fibres present in the ambient environment.
2.2. Isolation, visual characterization, and identification of microplastics
A dissection microscope (30X magnification) was used to count fi-
bres and potential MP-XPS. All fibres were counted, but their chemical
nature was not identified. The spectra of all recovered fragments were
acquired using an Attenuated Total Reflection Fourier Transform
Infrared microspectrometer (ATR-FTIR Lumos, Bruker). All spectra
were recorded in the absorbance mode in the 4,000−600 cm
−1
region
with 4 cm
−1
resolution and 16 scans. The spectra were acquired and
compared to reference spectra of polystyrene.
The maximum and minimum Feret diameters of the particles were
measured using the camera of the Lumos microscope associated with
the OPUS software. These diameters were then used to estimate the
volume of the particles. For this calculation, the shape of the particle
was approximated to a spheroid, with the two smallest axes considered
as equal.
2.3. Estimated per capita consumption of microplastics and statistical
analysis
Since the microplastics were too light to be weighted by a precision
balance (readability: 0.1 mg), the mass of the particles was calculated
according to two density hypotheses. The low hypothesis corresponds
to the density of extruded polystyrene (40 kg.m
−3
), whereas the high
hypothesis corresponds to that of polystyrene (1040 kg.m
−3
)
(Kedzierski, Le Tilly, César, Sire, & Bruzaud, 2017). The per capita
consumption of MP-XPS was calculated using the weight of the meat
samples and the average meat consumption rate of a French person
(Tavoularis & Sauvage, 2018). The following equation was used:
N
t
=N
MP
/m*m
t
(1)
Where, N
t
is the number of microplastics per person and per day,
N
MP
is the number of microplastics per tray, m is the mass of meat in the
tray, and m
t
is the mass of meat consumed per unit of time and per
person (135 g/d/person).
The equality of group averages was then measured using the Excel
Student and the Fisher tests.
3. Results
3.1. Particles
The characteristics of the microparticles were the same as those of
the XPS tray: presence of vacuoles, identical colour, and identical
chemical nature. There is therefore no doubt that they came from the
Table 1
Sample characteristics.
Brand Colour of the tray Meat Mass of meat (g)
A Black White chicken breast 315 ± 15
B Yellow Turkey escalope 239 ± 47
C Yellow Turkey escalope 254 ± 36
D Yellow Turkey escalope 240 ± 47
M. Kedzierski, et al. Food Packaging and Shelf Life 24 (2020) 100489
2
tray. FTIR spectra and the microscopic observations of the collected
particles showed the presence of MP-XPS microparticles inside the
packaging as well as on its outer surface. It should also be noted that
some MP-XPS were found between the meat and the plastic seal (Fig. 1).
The MP-XPS particles stuck on the surface of the meat were difficult to
recover during the rinsing phase. A thorough rinsing was necessary
each time to recover the particles, usually also by removing the layer of
fat from the surface of the meat. The average size of MP-XPS, measured
along the main axis, was comprised between 300 and 450 μm. On the
secondary axis, the average size of MP-XPS varied between 130 and
250 μm. The variability in particle size was quite high within the
packaging of the same brand. The colour of the MP-XPS was generally
the same as that of the XPS tray. The morphology of the particles was
variable. Some seemed to belong to porosity walls, others were more or
less compressed blocks of XPS. Thus, we used the density of XPS (40 kg/
m
3
and polystyrene 1040 kg/m
3
) to calculate the total mass of MP-XPS
per sample (Kedzierski, Le Tilly, Cesar, Sire, & Bruzaud, 2017).
The average quantities of MP-XPS observed on the external surface
of the food packaging varied, depending on the brands, between
1.1 ± 1.9 and 10.8 ± 6.0 MP-XPS/kg of packaged meat (Fig. 2).
Variations were large for the packaging samples of the same brand. The
amounts of MP-XPS recovered inside the packaging were on average
higher than those found outside for brands A and B whereas the op-
posite was observed for brand C. The average quantities of MP-XPS
observed on the internal surface of food packaging varied, depending
on the brands, between 4.0 ± 4.5 and 18.7 ± 8.3 MP-XPS/kg of
packaged meat. The amounts recovered inside and outside were similar
for brand D. Due to the large variability between samples of the same
brand, there was no statistically significant difference between the
quantities of MP-XPS inside and outside the packaging. For all the
brands under investigation, the number of MP-XPS was generally below
20. Although the amounts of MP-XPS found on the surface of packaging
A were on average lower than those of other brands, there was also no
statistically significant difference from one brand to another. Similarly,
although the quantities of particles found inside tray B were on average
much higher than those observed in the other trays, no statistical dif-
ferences were clearly identified. However, the p-values were very close
to 0.05. There is therefore a weak statistical presumption that brand B
meat is more contaminated than other brands.
The masses of MP-XPS were calculated per meat mass according to
the two extreme particle densities 40 and 1040 kg/m
3
)(Table 2). In the
first case, the masses of MP-XPS present on the outer surface of the
packaging ranged from 5 μg/kg of packaged meat (brand A) to 93 μg/kg
(brand B). Within the packaging, the masses of MP-XPS varied between
2μg/kg (brand D) and 402 μg/kg (brand B). In the second case, the
masses of MP-XPS present on the outer surface of the packages varied
between 0.14 mg/kg of packaged meat (brand A) and 2.4 mg/kg (brand
B). Inside the packaging, the masses of MP-XPS varied between 54 μg/
kg (brand D) and 10.5 mg/kg (brand B).
Based on the average French daily consumption of meat, the mass of
XPS observed inside the packaging and potentially ingested per day and
per year was calculated (Table 3). If the particle density was 40 kg/m
3
(low hypothesis), the average mass of XPS ingested per day could range
from 0.1 μg/d (brand D) to 54 μg/d (brand B). Per year, this would vary
between 0.04 mg/y (brand D) and 19.7 mg/y (brand B). For a particle
density of 1,040 kg/m
3
(high hypothesis), the average mass of XPS in-
gested per day could vary between 7 μg/d (brand D) and 1.4 mg/d
(brand B). Per year, this could range from 2.6 mg/y (brand D) to
511 mg/y (brand B).
3.2. Fibres
On average, the number of fibres observed on the surface of the food
packaging was between 134 fibres/kg (brand C) and 221 fibres/kg
(brand B) (Fig. 3). For most of the brands tested, the number of fibres
inside the packaging was between 18 fibres/kg (brand D) and 164 fi-
bres/kg (brand B). For brands A, C, and D, the quantities of fibres were
therefore higher outside than inside. In the case of brand D, the
amounts of fibres were about 11 times lower on the inside of the
package than on the outside. For brands A and C, the amounts were
Fig. 1. MP-XPS observed with a dissecting microscope (the Photoshop software
was used to improve the image brightness). The observed particle was trapped
between the sealing film and the meat. In this example, the particle was black
because the tray itself was that colour. In the yellow trays, the particles were
yellow. In this example, the particle contrasts with the colour of the meat,
making it very easy to observed. The structure of the particle corresponds, for
the thinnest parts, to the walls of the porosity of the XPS, and for the thickest
part, to a fragment of XPS. Therefore, the density of these MP-XPS varies ex-
tensively, as noted above (For interpretation of the references to colour in this
figure legend, the reader is referred to the web version of this article).
Fig. 2. Number of MP-XPS per kilogram of meat observed at the surface of and
inside the food packaging for the different brands.
Table 2
Mass of MP-XPS per kilogram of meat for the different brands estimated from
each density hypothesis.
Brand Hypothesis 1: 40 kg/m3 mass of
MP-XPS in mg/kg
Hypothesis 2: 1040 kg/m3
mass of MP-XPS in mg/kg
A Outside 0.005 ± 0.009 0.14 ± 0.24
Inside 0.09 ± 0.12 2.2 ± 3.1
B Outside 0.09 ± 0.16 2.4 ± 4.2
Inside 0.4 ± 0.5 10.5 ± 13.7
C Outside 0.02 ± 0.03 0.5 ± 0.8
Inside 0.2 ± 0.2 4.5 ± 4.5
D Outside 0.05 ± 0.08 1.2 ± 2.0
Inside 0.002 ± 0.001 0.05 ± 0.03
M. Kedzierski, et al. Food Packaging and Shelf Life 24 (2020) 100489
3
between 2 and 5 times lower. However, this was not true for brand B,
where the number of fibres inside and outside of the packaging was
quite similar. Thus, the differences between the amounts observed in-
side and outside the packaging were significant for brands A, C, and D.
For fibres on the external food packaging, there was no statistical dif-
ference between the brands, nor was there any statistical difference
between brands for the fibres present inside the packaging. This was
due in particular to the variability observed from one sample to another
for the same brand.
4. Discussion
4.1. Contamination of the surface of meat products with microplastics
4.1.1. Sources of MP-XPS
To our knowledge, this study is the first one to draw attention to the
microplastics found on the surface of meat products sealed in their
packaging. This contamination necessarily raises the question of the
origin of the microplastics. The observation of the presence of MP-XPS
inside and outside the tray, as well as between the tray and the meat,
and between the meat and the protective film, leads to the hypothesis
that the deposition of particles starts before the meat was deposited and
lasts at least until the film was closed. It is possible that the packaging
may be contaminated by XPS dust suspended in the air of the produc-
tion buildings. The MP-XPS are easily airborne because of their low size
and mass and because their electrostatic properties make them sticky. It
should also be noted that the presence of microplastics trapped between
the meat and the plastic film that seals the tray implies that MP-XPS are
present, suspended in the air, in the food preparation areas.
4.1.2. Areas for study improvement
Feedback on the protocol proposed within the framework of this
study has generated several propositions for improvement. In parti-
cular, it would be desirable to work on more samples of the same brand.
When the protocol was designed, working on the basis of a triplicate
seemed relevant. However, due to the variability observed from one
sample to another, it appears a posteriori that this number could be
increased. In the case of the study of microplastics ingested by living
organisms, a minimal number of 50 individuals per species is re-
commended to obtain a representative sample (Dehaut et al., 2019).
This recommendation may also be relevant to the study of microplastic
contamination of packaged food.
4.2. Ingesting MP-XPS: a threat to human health?
Regardless of the source of these MP-XPS, it should be noted that
despite the thorough rinsing of the surface of the meat examined,
plastic particles often remained trapped on the meat surface. Thus,
whether the meat is rinsed or not, the MP-XPS are likely to be present
when the food is cooked, and some will be ingested.
4.2.1. Potential impacts of polystyrene microplastics (MP-PS) on human
health
While it has sometimes been argued that certain species fished are
potential microplastic vectors for humans, extraction from the digestive
system (containing microplastics) before consumption greatly reduces
this risk (Alomar & Deudero, 2017;Rummel et al., 2016;Sanchez,
Bender, & Porcher, 2014;Van Cauwenberghe, Claessens,
Vandegehuchte, & Janssen, 2015;Van Cauwenberghe & Janssen, 2014;
Vroom, Halsband, Besseling, & Koelmans, 2016). Another source of
contamination of human food comes from the packaging (Schymanski
et al., 2018). The masses of MP-XPS ingested per day and per person
could reach 1.4 mg based on the results obtained in this study, but there
is no reference or standard for determining whether or not this value is
dangerous to human health. In fact, the potential impact of MPePS
ingestion on human health remains very limited (Wang, Gao, Jin, Li, &
Na, 2019). A study conducted on human epithelial (HeLa) and cerebral
(T98 G) cell lines has shown that PS microspheres (diameter 10 μm)
caused oxidative stress (Schirinzi et al., 2017). On the contrary, MPePS
(1, 4 and 10 μm) do not seem to have an impact on some human im-
mune cells (macrophages) (Stock et al., 2019). In mice exposed to
0.5−50 μm polystyrene particles, disruptions in energy and lipid me-
tabolism, oxidative stress, neurotoxic disorders, and microbiotic dys-
biosis were observed that suggest potential risks to mammalian health
(Deng, Zhang, Lemos, & Ren, 2017;Lu, Wan, Luo, Fu, & Jin, 2018).
However, these results are qualified by a recent study suggesting that,
under certain conditions, oral exposure to microplastic particles does
not pose an acute risk to mammalian health (Stock et al., 2019).
However, several limitations to the transferability of these ha-
zardous effects to the human case must be mentioned. First, the sensi-
tivity to plastics may vary between animal species (Walum, 1998).
Second, it is necessary that the plastic quantities ingested and the ex-
posure duration of the animals be relevant to the quantities actually
observed in their natural environment or, as in this case, in human food
(Bour, Haarr, Keiter, & Hylland, 2018;Lönnstedt & Eklöv, 2016). In
experiments conducted on mouse exposure to MP-PS, the dose tested
was 0.1 mg/d, which is in line with the amounts that could be ingested
by humans (Deng et al., 2017). However, this dose is much higher if we
consider the difference in body weight between a mouse and a human
Table 3
Consumption of MP-XPS per person based on a meat consumption of 135 g/d/person.
Brand MP-XPS density Daily consumption (mg/d) Annual consumption (mg/y)
A Hypothesis 1: 40 kg/m3 0.01 ± 0.02 4.2 ± 6.0
Hypothesis 2: 1040 kg/m3 0.3 ± 0.4 110.1 ± 154.9
B Hypothesis 1: 40 kg/m3 0.5 ± 0.07 19.8 ± 26.0
Hypothesis 2: 1040 kg/m3 1.4 ± 1.9 515.2 ± 675.3
C Hypothesis 1: 40kg/m3 0.02 ± 0.02 8.6 ± 8.4
Hypothesis 2: 1040 kg/m3 0.6 ± 0.6 223.2 ± 219.4
D Hypothesis 1: 40 kg/m3 0.0003 ± 0.0001 0.1 ± 0.05
Hypothesis 2: 1040 kg/m3 0.007 ± 0.003 2.7 ± 1.3
Fig. 3. Amounts of microfibres per kilogram of packaged meat observed on the
surface and inside of the food packaging examined. * Results that show sta-
tistical differences (p-value < 0.05).
M. Kedzierski, et al. Food Packaging and Shelf Life 24 (2020) 100489
4
being. Thus, it is important to note that the polystyrene particles used in
these studies are one to two orders of magnitude smaller than those
observed in the present study. Nevertheless, it cannot be completely
excluded that polystyrene particles from a few micrometres to a few
tens of micrometres in size were not effectively detected and extracted
from the surface of the samples. However, while it is possible that the
total number of microplastics may be underestimated, the very low
mass of these fine particles should not have too much influence on the
total mass values of MP-XPS calculated in this study. However, it should
be noted, that it is essentially on this size range of small microplastics
(less than a few tens of microns) that the discussion on the toxicity of
polystyrene particles is based. Therefore, a better assessment of the
amount of these small microplastics present on the surface of foods
appears to be important to better identify the associated risks. Finally,
the number of studies on the impact of MP-PS on mammals is very low,
which makes it difficult to accurately assess their potential impact on
humans (Rainieri & Barranco, 2019).
4.2.2. Styrene desorption
In addition, for polystyrene, there is a risk of desorption of styrene
monomers during the use phase (Rist, Carney Almroth, Hartmann, &
Karlsson, 2018). Styrene is quickly absorbed by organisms through in-
gestion or inhalation (Bonnard et al., 2016). It is stored in fatty tissues
where it is rapidly metabolized (half-life of about 6 h). After metabo-
lisation, it is mainly eliminated by urine. Styrene therefore does not
accumulate in organisms. In terms of chronic toxicity, in rats, ingestion
of high doses of styrene (1.0 g/kg/d, 5d/week, 28d) causes irritation of
the gastrointestinal tract, which is lethal. This dose corresponds, for a
person weighing 70 kg, to about 50,000 times the maximum daily mass
of MP-XPS potentially ingested per day and per person recorded in our
study (1.4 mg/d). Since a small fraction of styrene is desorbed from MP-
XPS, the doses are actually even lower.
At lower doses, ingestion induces changes in kidney and liver
weight. Styrene is metabolized by cytochrome P450 enzymes to
styrene-7,8-oxide that undergoes hydration or conjugation with glu-
tathione (Shen Li, Ding, & Zheng, 2014). In mice, styrene is involved in
lung tumour development, whereas no data indicate a similar effect in
humans (Cruzan et al., 2018). The derived no-effect level (DNEL) of
styrene is 7.7 μg/kg bw/d (European Chemicals Agency, 2019e), which
represents, in the framework of our study, about 0.4 times the max-
imum daily mass of MP-XPS potentially ingested per day and per person
weighing 70 kg. However, again, the amounts of styrene released from
MP-XPS are most likely much lower. Finally, in humans, styrene ab-
sorption results in memory loss, difficulties in concentration and
learning, brain and liver damage, and cancer (Gibbs & Mulligan, 1997).
More generally, according to a recent study, the toxicity of poly-
styrene packaging can vary greatly from one polystyrene sample to
another (Zimmermann, Dierkes, Ternes, Völker, & Wagner, 2019).
Thus, some PS samples were cytotoxic to the cells used in the AREc32
test at lower concentrations than the other plastics tested. This study
also highlights a toxicity linked to oestrogenic (Yeast Estrogen Screen)
and especially anti-androgenic (Yeast Anti-Androgen Screen) effects for
some samples. This implies that some additives used in the food
packaging have endocrine activity. Due to higher average meat con-
sumption among men than women (Hercberg & Tallec, 2000), there is a
differential exposure to MP-XPS between the sexes. Similarly, in France,
the protein intake reaches its maximum around adolescence (Hercberg
& Tallec, 2000), corresponding with a period of vulnerability to endo-
crine disruptors.
Thus, the ingestion of microplastics could be an additional route of
contamination that would add to the more traditional route of con-
tamination via food. However, this contamination would be several
orders of magnitude lower than that passing through food products
(Rist et al., 2018).
4.2.3. Cooking microplastics
Cooking conditions can vary considerably from one cooking method
to another. Thus, the temperatures reached during cooking may vary
between 100 and 230 °C or much more for open fire grills. When sub-
jected to temperatures between 200 and 300 °C, the molecular weight
of polystyrene decreases due to thermal degradation inducing random
scission of the carbon chain, and disproportionation of the macro-
radicals formed, leading to the release of many degradation products
(McNeill, Zulfiqar, & Kousar, 1990). At 200 °C, the rate of volatile
fragments formed is low, but the amounts of degradation residues may
be significantly higher. At around 300 °C, gaseous styrene is mainly
produced, but so are other compounds such as ethylbenzene, methyl-
benzene (or toluene), benzene, phenylpropene, α-methylstyrene, 1-
methylindene, and naphthalene (McNeill et al., 1990). The toxicity of
these molecules cannot be established for the doses of MP-XPS quan-
tified on the surface of the meat even if an endocrine activity of these
molecules cannot be completely excluded (Zimmermann et al., 2019).
Furthermore, based on the DNEL of styrene (7.7 μg/kg bw/d), low
toxicity leading to irritation cannot be completely ruled out (European
Chemicals Agency, 2019).
4.3. Microfibres: another contaminant
The number of fibres observed inside the trays is of the same order
of magnitude as that observed in previous studies on other food pro-
ducts; as for honey, sugar, or salt, the observed quantities were gen-
erally lower than 1000 fibres per kg of food (Gündoğdu, 2018;Iñiguez
et al., 2017;Karami et al., 2017;Liebezeit & Liebezeit, 2013). If, in the
case of these studies, the origin of the contamination is not always easy
to determine (contamination in the natural environment or during the
manufacturing process of the product), in the case of our study, the
presence of fibres inside the tray implies the presence of these fibres in
the production environment of the food product. In the absence of
analysis of procedural blank, it cannot be totally excluded that a frac-
tion of the fibres observed are derived from airborne contamination.
However, the differences observed, in particular between the inner and
outer surfaces of the trays, are statistically significant. It is highly un-
likely that, under similar study conditions such large variations can be
due to contamination without affecting the variance within the same
brand.
The chemical nature of these fibres, outside the scope of the pre-
liminary analysis, was not analysed. Thus, it is not possible to specify
whether these fibres are mineral or organic. The impact of the inhala-
tion of man-made mineral fibres is well known; as a function of dif-
ferent parameters such as particle size and composition, they have the
intrinsic potential to induce oxidative stress, inflammation, genotoxi-
city, and carcinogenicity (Greim, 2004).
Similarly, the consequences of the inhalation of man-made organic
fibres is known (Gasperi et al., 2018;Greim, 2004). For example, var-
ious studies conducted on cohorts of textile workers have shown no or a
moderate impact on the respiratory tract (Warheit et al., 2001). The
impact of fibre ingestion is less well documented as this mode of con-
tamination appears, in the air, to be secondary to respiration. Very few
studies report cases of airborne ingestion of these fibres by living beings
(Cook & Olson, 1979;Zhao, Zhu, & Li, 2016). Hence, apart from the
particular case of certain mineral fibres (e.g. asbestos), which has been
well documented for several decades (Davis, 1981), the impact of fibre
ingestion on human health is poorly described in the scientific litera-
ture. Nevertheless, it should also be noted that the average amount of
fibres outside the tray is up to 10 times higher than inside the tray. It
thus appears that the packaging plays a protective role against micro-
fibres.
5. Conclusion
Only few scientific studies report the presence of microplastics that
M. Kedzierski, et al. Food Packaging and Shelf Life 24 (2020) 100489
5
contaminate food. Our study, by assessing the presence of microplastics
on the surface of meat products, extends the state of knowledge on the
contamination of human food by microplastics. These microplastics are
highly adherent to the meat surface and are likely to be eaten by con-
sumers. Although polystyrene trays are made of polystyrene suitable for
food contact, the presence of MP-XPS on the food surface is potentially
problematic due to the toxicity of the microparticles, the potential
desorption of styrene, and the formation of degradation products during
cooking. Nevertheless, given current knowledge on the issue, it should
be noted that the comparison of the amounts of MP-XPS observed in the
trays with the data available in the scientific literature does not enable
us to definitively conclude on the existence or not of potential risks for
humans. However, in view of the tray uses, no doubt should remain
concerning the contamination impacts for human health.
As a consequence, this preliminary investigation should be ex-
panded and further developed along several lines of investigation. First,
it would be relevant to identify the sources of contamination in asso-
ciation with possible distinct packaging processes. This step is necessary
to propose counter measures that could reduce exposition to MP-XPS.
Second, the risks associated with the regular ingestion of MP-XPS
should be clarified. In addition, greater knowledge of the molecules that
can be desorbed by MP-XPS is necessary, especially if they behave as
endocrine disruptors.
CRediT authorship contribution statement
Mikaël Kedzierski: Conceptualization, Methodology, Formal ana-
lysis, Supervision, Writing - original draft, Writing - review & editing.
Benjamin Lechat: Validation, Investigation, Data curation. Olivier
Sire: Methodology, Supervision, Writing - review & editing. Gwénaël
Le Maguer: Project administration, Writing - review & editing.
Véronique Le Tilly: Methodology, Supervision, Writing - review &
editing. Stéphane Bruzaud: Supervision, Funding acquisition, Writing
- review & editing.
Acknowledgement
The authors are grateful to the OceanWise project that made this
publication possible. OceanWise is funded by the European Regional
Development Fund (ERDF) INTERREG Atlantic Area, under Priority
Axis 4: Enhancing biodiversity and the natural and cultural assets.
References
Alomar, C., & Deudero, S. (2017). Evidence of microplastic ingestion in the shark Galeus
melastomus Rafinesque, 1810 in the continental shelf offthe western Mediterranean
Sea. Environmental Pollution, 223, 223–229. https://doi.org/10.1016/j.envpol.2017.
01.015.
Azevedo-Santos, V. M., Gonçalves, G. R. L., Manoel, P. S., Andrade, M. C., Lima, F. P., &
Pelicice, F. M. (2019). Plastic ingestion by fish: A global assessment. Environmental
Pollution, 255, 112994. https://doi.org/10.1016/j.envpol.2019.112994.
Barboza, L. G., & Gimenez, B. C. (2015). Microplastics in the marine environment:
Current trends and future perspectives. Marine Pollution Bulletin, 97(1–2), 5–12.
https://doi.org/10.1016/j.marpolbul.2015.06.008.
Barboza, L. G. A., Dick Vethaak, A., Lavorante, B. R. B. O., Lundebye, A.-K., &
Guilhermino, L. (2018). Marine microplastic debris: An emerging issue for food se-
curity, food safety and human health. Marine Pollution Bulletin, 133, 336–348.
https://doi.org/10.1016/j.marpolbul.2018.05.047.
Boucher, J., & Friot, D. (2017). Primary microplastics in the oceans: A global evaluation of
sources. Primary microplastics in the oceans: A global evaluation of sourceshttps://doi.
org/10.2305/iucn.ch.2017.01.en.
Bour, A., Haarr, A., Keiter, S., & Hylland, K. (2018). Environmentally relevant micro-
plastic exposure affects sediment-dwelling bivalves. Environmental Pollution, 236,
652–660. https://doi.org/10.1016/j.envpol.2018.02.006.
Buchanan, J. B. (1971). Pollution by synthetic fibres. Marine Pollution Bulletin, 2,23.
Cook, P. M., & Olson, G. F. (1979). Ingested mineral fibers: Elimination in human urine.
Science, 204(4389), https://doi.org/10.1126/science.219478 195 LP –198.
Davis, J. M. G. (1981). The biological effects of mineral fibres. The Annals of Occupational
Hygiene, 24(2), 227–234. https://doi.org/10.1093/annhyg/24.2.227.
Dehaut, A., Hermabessiere, L., & Duflos, G. (2019). Current frontiers and recommenda-
tions for the study of microplastics in seafood. TrAC Trends in Analytical Chemistry,
116, 346–359. https://doi.org/10.1016/j.trac.2018.11.011.
Deng, Y., Zhang, Y., Lemos, B., & Ren, H. (2017). Tissue accumulation of microplastics in
mice and biomarker responses suggest widespread health risks of exposure. Scientific
Reports, 7(1), 46687. https://doi.org/10.1038/srep46687.
Dris, R., Gasperi, J., Saad, M., Mirande, C., & Tassin, B. (2016). Synthetic fibers in at-
mospheric fallout: A source of microplastics in the environment? Marine Pollution
Bulletin, 104(1–2), 290–293. https://doi.org/10.1016/j.marpolbul.2016.01.006.
European Chemicals Agency (2019). Styrene - brief profile. https://echa.europa.eu/brief-
profile/-/briefprofile/100.002.592.
Gasperi, J., Wright, S. L., Dris, R., Collard, F., Mandin, C., Guerrouache, M., et al. (2018).
Microplastics in air: Are we breathing it in? Current Opinion in Environmental Science &
Health, 1,1–5. https://doi.org/10.1016/j.coesh.2017.10.002.
Geyer, R., Jambeck, J. R., & Law, K. L. (2017). Production, use, and fate of all plastics ever
made. Science Advances, 3(7), e1700782. https://doi.org/10.1126/sciadv.1700782.
Gibbs, B. F., & Mulligan, C. N. (1997). Styrene toxicity: An ecotoxicological assessment.
Ecotoxicology and Environmental Safety, 38(3), 181–194. https://doi.org/10.1006/
eesa.1997.1526.
Greim, H. A. (2004). Research needs to improve risk assessment of fiber toxicity. Mutation
Research/Fundamental and Molecular Mechanisms of Mutagenesis, 553(1), 11–22.
https://doi.org/10.1016/j.mrfmmm.2004.06.013.
Gündoğdu, S. (2018). Contamination of table salts from Turkey with microplastics. Food
Additives & Contaminants Part A, 35(5), 1006–1014. https://doi.org/10.1080/
19440049.2018.1447694.
Hidalgo-Ruz, V., Gutow, L., Thompson, R. C., & Thiel, M. (2012). Microplastics in the
marine environment: A review of the methods used for identification and quantifi-
cation. Environmental Science & Technology, 46(6), 3060–3075. https://doi.org/10.
1021/es2031505.
Iñiguez, M. E., Conesa, J. A., & Fullana, A. (2017). Microplastics in spanish table salt.
Scientific Reports, 7(1), 8620. https://doi.org/10.1038/s41598-017-09128-x.
Karami, A., Golieskardi, A., Keong Choo, C., Larat, V., Galloway, T. S., & Salamatinia, B.
(2017). The presence of microplastics in commercial salts from different countries.
ScientificReports, 7, 46173. https://doi.org/10.1038/srep46173.
Kedzierski, M., Le Tilly, V., Cesar, G., Sire, O., & Bruzaud, S. (2017). Efficient micro-
plastics extraction from sand. A cost effective methodology based on sodium iodide
recycling. Marine Pollution Bulletin, 115(1–2), 120–129. https://doi.org/10.1016/j.
marpolbul.2016.12.002.
Kedzierski, M., Le Tilly, V., César, G., Sire, O., & Bruzaud, S. (2017). Efficient micro-
plastics extraction from sand. A cost effective methodology based on sodium iodide
recycling. Marine Pollution Bulletin, 115(1–2), https://doi.org/10.1016/j.marpolbul.
2016.12.002.
Kosuth, M., Mason, S. A., & Wattenberg, E. V. (2018). Anthropogenic contamination of
tap water, beer, and sea salt. PloS One, 13(4), e0194970. https://doi.org/10.1371/
journal.pone.0194970.
Lange, J., & Wyser, Y. (2003). Recent innovations in barrier technologies for plastic
packaging—A review. Packaging Technology and Science, 16(4), 149–158. https://doi.
org/10.1002/pts.621.
Liebezeit, G., & Liebezeit, E. (2013). Non-pollen particulates in honey and sugar. Food
Additives & Contaminants Part A, 30(12), 2136–2140. https://doi.org/10.1080/
19440049.2013.843025.
Liebezeit, G., & Liebezeit, E. (2014). Synthetic particles as contaminants in German beers.
Food Additives & Contaminants Part A, 31(9), 1574–1578. https://doi.org/10.1080/
19440049.2014.945099.
Lönnstedt, O. M., & Eklöv, P. (2016). Environmentally relevant concentrations of mi-
croplastic particles influence larval fish ecology. Science, 352(6290), https://doi.org/
10.1126/science.aad8828 1213 LP –1216.
Lu, L., Wan, Z., Luo, T., Fu, Z., & Jin, Y. (2018). Polystyrene microplastics induce gut
microbiota dysbiosis and hepatic lipid metabolism disorder in mice. The Science of the
Total Environment, 631–632, 449–458. https://doi.org/10.1016/j.scitotenv.2018.03.
051.
Mason, S. A., Welch, V. G., & Neratko, J. (2018). Synthetic polymer contamination in
bottled water. Frontiers in Chemistry, 6, 407. https://doi.org/10.3389/fchem.2018.
00407.
Mathlouthi, M. (2013). Food packaging and preservation. US: Springer. https://books.
google.fr/books?id=2gHTBwAAQBAJ.
McNeill, I. C., Zulfiqar, M., & Kousar, T. (1990). A detailed investigation of the products of
the thermal degradation of polystyrene. Polymer Degradation and Stability, 28(2),
131–151. https://doi.org/10.1016/0141-3910(90)90002-O.
Oßmann, B. E., Sarau, G., Holtmannspötter, H., Pischetsrieder, M., Christiansen, S. H., &
Dicke, W. (2018). Small-sized microplastics and pigmented particles in bottled mi-
neral water. Water Research, 141, 307–316. https://doi.org/10.1016/j.watres.2018.
05.027.
Piringer, O. G., & Baner, A. L. (2008). Plastic packaging materials for food: Barrier function,
mass transport, quality assurance, and legislation. Wileyhttps://books.google.fr/books?
id=7Uz9XW-VihgC.
PlasticsEurope (2012). Plastic packaging: Born to protect.
PlasticsEurope (2018). Plastics - the Facts 2018.
Prata, J. C. (2018). Airborne microplastics: Consequences to human health? Environmental
Pollution, 234, 115–126. https://doi.org/10.1016/j.envpol.2017.11.043.
Rainieri, S., & Barranco, A. (2019). Microplastics, a food safety issue? Trends in Food
Science & Technology, 84,55–57. https://doi.org/10.1016/j.tifs.2018.12.009.
Rist, S., Carney Almroth, B., Hartmann, N. B., & Karlsson, T. M. (2018). A critical per-
spective on early communications concerning human health aspects of microplastics.
The Science of the Total Environment, 626, 720–726. https://doi.org/10.1016/j.
scitotenv.2018.01.092.
Rummel, C. D., Loder, M. G., Fricke, N. F., Lang, T., Griebeler, E. M., Janke, M., et al.
(2016). Plastic ingestion by pelagic and demersal fish from the North sea and Baltic
sea. Marine Pollution Bulletin, 102(1), 134–141. https://doi.org/10.1016/j.marpolbul.
M. Kedzierski, et al. Food Packaging and Shelf Life 24 (2020) 100489
6
2015.11.043.
Sanchez, W., Bender, C., & Porcher, J.-M. (2014). Wild gudgeons (Gobio gobio) from
French rivers are contaminated by microplastics: Preliminary study and first evi-
dence. Environmental Research, 128,98–100. https://doi.org/10.1016/j.envres.2013.
11.004.
Schirinzi, G. F., Pérez-Pomeda, I., Sanchís, J., Rossini, C., Farré, M., & Barceló, D. (2017).
Cytotoxic effects of commonly used nanomaterials and microplastics on cerebral and
epithelial human cells. Environmental Research, 159, 579–587. https://doi.org/10.
1016/j.envres.2017.08.043.
Schymanski, D., Goldbeck, C., Humpf, H.-U., & Fürst, P. (2018). Analysis of microplastics
in water by micro-Raman spectroscopy: Release of plastic particles from different
packaging into mineral water. Water Research, 129, 154–162. https://doi.org/10.
1016/j.watres.2017.11.011.
Stock, V., Böhmert, L., Lisicki, E., Block, R., Cara-Carmona, J., Pack, L. K., et al. (2019).
Uptake and effects of orally ingested polystyrene microplastic particles in vitro and in
vivo. Archives of Toxicology, 93(7), 1817–1833. https://doi.org/10.1007/s00204-
019-02478-7.
Tavoularis, G., & Sauvage, É. (2018). Les nouvelles générations transforment la consomma-
tion de viande. CREDOC 4.
Van Cauwenberghe, L., & Janssen, C. R. (2014). Microplastics in bivalves cultured for
human consumption. Environmental Pollution, 193,65–70. https://doi.org/10.1016/j.
envpol.2014.06.010.
Van Cauwenberghe, L., Claessens, M., Vandegehuchte, M. B., & Janssen, C. R. (2015).
Microplastics are taken up by mussels (Mytilus edulis) and lugworms (Arenicola
marina) living in natural habitats. Environmental Pollution, 199,10–17. https://doi.
org/10.1016/j.envpol.2015.01.008.
Vroom, R., Halsband, C., Besseling, E., & Koelmans, A. A. (2016). Effects of microplastics on
zooplankton: Microplastic ingestion: The role of taste.
Walum, E. (1998). Acute oral toxicity. Environmental Health Perspectives, 106(suppl 2),
497–503. https://doi.org/10.1289/ehp.98106497.
Wang, W., Gao, H., Jin, S., Li, R., & Na, G. (2019). The ecotoxicological effects of mi-
croplastics on aquatic food web, from primary producer to human: A review.
Ecotoxicology and Environmental Safety, 173, 110–117. https://doi.org/10.1016/j.
ecoenv.2019.01.113.
Warheit, D. B., Hart, G. A., Hesterberg, T. W., Collins, J. J., Dyer, W. M., Swaen, G. M. H.,
et al. (2001). Potential pulmonary effects of man-made organic Fiber (MMOF) dusts.
Critical Reviews in Toxicology, 31(6), 697–736. https://doi.org/10.1080/
20014091111965.
Winkler, A., Santo, N., Ortenzi, M. A., Bolzoni, E., Bacchetta, R., & Tremolada, P. (2019).
Does mechanical stress cause microplastic release from plastic water bottles? Water
Research, 166, 115082. https://doi.org/10.1016/j.watres.2019.115082.
Yang, D., Shi, H., Li, L., Li, J., Jabeen, K., & Kolandhasamy, P. (2015). Microplastic
pollution in table salts from China. Environmental Science & Technology, 49(22),
13622–13627. https://doi.org/10.1021/acs.est.5b03163.
Zhao, S., Zhu, L., & Li, D. (2016). Microscopic anthropogenic litter in terrestrial birds
from Shanghai, China: Not only plastics but also natural fibers. The Science of the Total
Environment, 550, 1110–1115. https://doi.org/10.1016/j.scitotenv.2016.01.112.
Zimmermann, L., Dierkes, G., Ternes, T. A., Völker, C., & Wagner, M. (2019).
Benchmarking the in vitro toxicity and chemical composition of plastic consumer
products. Environmental Science & Technology, 53(19), 11467–11477. https://doi.org/
10.1021/acs.est.9b02293.
M. Kedzierski, et al. Food Packaging and Shelf Life 24 (2020) 100489
7
