Marine Pollution Bulletin 160 (2020) 111633

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Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul

Abundance, composition, and potential intake of microplastics in canned T

fish
Razegheh Akhbarizadeha,b, Sina Dobaradarana,c,d, , Iraj Nabipourb, Saeed Tajbakhshb,
⁎

Amir Hossein Darabie, Jörg Spitzf

a
Systems Environmental Health and Energy Research Center, The Persian Gulf Biomedical Sciences Research Institute, Bushehr University of Medical Sciences, Bushehr,
Iran
b
The Persian Gulf Marine Biotechnology Research Center, The Persian Gulf Biomedical Sciences Research Institute, Bushehr University of Medical Sciences, Bushehr, Iran
c
Department of Environmental Health Engineering, Faculty of Health and Nutrition, Bushehr University of Medical Sciences, Bushehr, Iran
d
Instrumental Analytical Chemistry and Centre for Water and Environmental Research (ZWU), Faculty of Chemistry, University of Duisburg-Essen, Essen, Germany
e
The Persian Gulf Tropical Medicine Research Center, The Persian Gulf Biomedical Sciences Research Institute, Bushehr University of Medical Sciences, Bushehr, Iran
f
Akademie für Menschliche Medizin GmbH, Krauskopfallee 27, 65388 Schlangenbad, Germany

ARTICLE INFO ABSTRACT

Keywords: The existence of microplastics (MPs) in canned fish (tuna and mackerel) samples was investigated and their
Microplastics composition, possible sources and potential intake were assessed. Light and fluorescence microscopy were used
Canned fish for the quantification of potential MPs. Furthermore, micro-Raman microscopy, and scanning electron micro­
Food safety scopy coupled with an energy dispersive X-ray were used to identify the polymer types and composition of MPs.
Chemical composition
The results showed that 80% of samples had at least one plastic particle and fibers were the most abundant
Human intake
shapes of MPs. Moreover, polyethylene terephthalate (32.8%) was the most common polymer type in canned fish
samples. The fish, food additives, and contact materials during the cleaning and canning process are possible
sources of MPs. Human intake estimation of MPs showed the possibility of plastics absorption by humans who
consume canned fish several times/week. Hence, the results of this study showed the importance of MPs'
guidelines for food safety and hygiene.

1. Introduction Plastic pollution is one of the newest identified contaminants of

Canning is one of the most widely used ways of fish preserving
(Horner, 1997; Vafaei et al., 2018). About 19 million tons of the total
world fishery production (167.2 million tons) are preserved by canning
(FAO, 2014). The most important fish species canned are tuna, an­
chovies, bonito, sardines, and mackerels (ElShehawy and Farag, 2019).
During the canning process, the fish flesh is kept in sealed cans with
edible oils, vegetables, salt, and brine and subjected to sterilization
(Caponio et al., 2011; ElShehawy and Farag, 2019). Although canning
manufacturing may affect the quality of the lipids and protein in the
final product (Aubourg et al., 1997; Sadok and Selmi, 2007), canned
fish is still a good source of protein, vitamins, minerals and long-chain
omega-3 polyunsaturated fatty acids (ω3-PUFAs) (Bell et al., 2019;
Maqbool et al., 2011). However, the presence of pollutants (i.e. heavy
metals and plastics) raises concerns regarding the safety and hygiene of
canned seafood. Contaminated seafood and its products such as canned
fish can possibly impact on human health.
emerging concern due to their high production, and low degradability
(Rainieri and Barranco, 2019; Toussaint et al., 2019). It is estimated
that from 8.3 billion metric tons of produced plastic, 4.9 billion metric
tons of them were released in the environment or deposited in landfills
(Geyer et al., 2017). Microplastics (MPs) are usually considered as
particles with less than 5 mm in length (Arthur et al., 2009; Wright
et al., 2013). They result from the direct release of micro-sized plastic
debris which are intentionally produced in that size range (primary
MPs) and/or from the fragmentation/degradation of larger plastic
particles due to the bio-photochemical weathering in the environment
or during use (secondary MPs) (Bessa et al., 2018; Hartmann et al.,
2019; Wright et al., 2013). It is proven that MPs are ubiquitous in the
environment and they were found in outdoor and indoor air, drinking
water, soil and sediments, freshwater and seawater, and aquatic and
terrestrial organisms (Alimba and Faggio, 2019; Auta et al., 2017; Avio
et al., 2017; Duis and Coors, 2016; Kaya et al., 2018; Rochman et al.,
2015; Vandermeersch et al., 2015; Wright et al., 2013). However, their

⁎
Corresponding author at: Systems Environmental Health and Energy Research Center, Boostan 19 Alley, Imam Khomeini Street, Bushehr 7514763448, Iran.
E-mail address: s.dobaradaran@bpums.ac.ir (S. Dobaradaran).

https://doi.org/10.1016/j.marpolbul.2020.111633
Received 26 May 2020; Received in revised form 29 August 2020; Accepted 29 August 2020
Available online 14 September 2020
0025-326X/ © 2020 Elsevier Ltd. All rights reserved.
R. Akhbarizadeh, et al. Marine Pollution Bulletin 160 (2020) 111633

origin is not usually described, unless the primary origin of MPs can be vacuum filtration using Schleicher & Schüll (S&S) quantitative filter
established convincingly (Hartmann et al., 2019). paper, grade 593 (pore size 5 μm and 5 cm diameter), by vacuum pump
Since the intake of MPs through the food chain could impact on (Rocker-800 oil-free, Germany) connected to a magnetic filter funnel
human health, the possible accumulation of MPs in fish flesh and the (Pall Co., USA). Then, the residue was washed by using deionized water
edible parts of other aquatic organisms such as prawns, bivalves, and to remove the remaining KOH. It should be noted that, more than one
crabs could become a food safety issue (Akhbarizadeh et al., 2019; filter paper was used for some samples due to the presence of oils,
Toussaint et al., 2019). Although the presence of MPs in the edible parts herbs, and fish bones. Filter papers were air-dried (at 25 °C and for
of the aquatic organisms are investigated in recent studies 2 days) prior to microscopic investigations and other analyses.
(Akhbarizadeh et al., 2018, 2019; Karami et al., 2017b; Li et al., 2018;
Su et al., 2019), the occurrence of MPs in processed seafood products 2.2. Quality control (QC)/quality assurance (QA)
such as canned fish was rarely checked. To the best of our knowledge,
only Karami et al. (2018) considered the presence of meso- and mi­ To prevent contamination by MPs, nitrile gloves and a cotton la­
croplastics in 20 brands of canned sardines and sprats. According to boratory coat were worn during all the steps of the analytical proce­
their results, 20% of samples contained 1–3 plastics particle. However, dures. Moreover, the room of the laboratory didn't have any window
to date, there is no study on the presence of MPs' particle in canned tuna and the door was closed during all the steps. All work surfaces were
and mackerel fish. Hence, the aims of this study were: 1) investigate the cleaned with ethanol 70% (Zakarya Co, Iran) before and during the
presence of MPs in the popular brands of canned tuna and mackerel fish steps to prevent airborne plastics and cross contamination. All cans
available in the Persian market, and their characteristics such as color, were washed with tap water and rinsed with pure distilled water prior
size, type, morphology, and chemical composition, 2) determine the to opening. In addition, to avoid the possible contamination during the
possible correlations between the added ingredients (i.e. salt, oil types, opening of the cans and during the analysis, easy open cans were
etc.) and MPs' content of canned fish, and 3) assess the human intake of purchased and they were opened in the clean cabinet of the laboratory.
MPs through canned tuna fish consumption. The samples were immediately covered with clean white sheets of
paper in all the steps. All liquids and solutions (i.e. ethanol, distilled
water, and KOH solution) were filtered through 2.5 μm Whatman filter
2. Materials and methods paper. Furthermore, during all the steps, clean devices were used to
collect and store the samples. Five blanks with no fish flesh were run
2.1. Sampling, sample preparation, and analysis parallel to the samples during the sample preparation and digestion
procedure in each batch, and they were then checked for possible
In total, fifty canned fish (tuna and mackerel) samples from 7 contamination. For more assurance, in each batch, a control glass petri
popular brands were purchased from Iranian hypermarkets. Fish species dish with deionized filtered water was left in the clean cabinet of the
were longtail tuna (Thunnus tonggol), yellowfin tuna (Thunnus alba­ laboratory in which all steps were done to capture any possible airborne
cares), and mackerel fish (Scombermorus commerson) (Featherstone, contamination they were then checked for possible plastic pollution.
2016). Table 1 represents the brands and number of sampled canned
fish and their characteristics (i.e. the oil types, fish species, and salt 2.3. Microplastics' quantification and identification
concentration). Various brands with different types of canned contents
were investigated for their MPs' content. As shown in Table 1, four 2.3.1. Optical analysis
different types of canned fish were sampled from brand A. Brands B and A KRÜSS binocular microscope (A. KRÜSS optronic, Germany) with
F preserved the fish in soybean oil and the rest of the samples were used up to 400× magnification was used as the primary tool for optical
fish in sunflower oil. Fish species in all samples (except Brand E) were analysis and enumeration of extracted particles. For plastics quantifi­
tuna fish. cation, particles were assessed visually and classified according to their
The extraction of plastic particles from canned fish was done ac­ known physicochemical characteristics including opacity, hardness,
cording to the modified version of the method suggested by Karami color, structure, and specific elasticity (Bellas et al., 2016; Hidalgo-Ruz
et al., 2017b. To be specific, 20 g of homogenized fish flesh from each et al., 2012). However, in some cases, it was necessary to test the object
canned was weighted using a four-digit microbalance (100 μg; Sartorius with a hot probe, for confidence. The longest part of each identified
Secura 225D-1S, Germany), placed in a cleaned beaker and immersed in plastic particle was measured by probe diameter and noted. According
50 ml of 10% (w/v) potassium hydroxide (KOH-Merck, Germany). The to the literature, the identified MPs were classified into 3 morphotypes
beakers were incubated at 40 °C in an oven (drying oven BF55E, FG, including fragments, fibers, and films (Hartmann et al., 2019). Neither
Iran) for 24 h (until the absolute digestion of fish flesh was complete). organic or cellular structure should be noticeable on plastic particles,
After the incubation time, the liquid in beakers were subjected to and fibers must be uniformly thick along their entire length (Hidalgo-
Ruz et al., 2012).
Table 1
Characteristics of sampled canned fish.
2.3.2. Fluorescence analysis
Brands n Descriptions Fish species After optical analysis, a Nikon 80i epifluorescence microscope
(Tokyo, Japan) equipped with a DS-5Mc-L1 digital camera was used to
Type of liquid Liquid Salt/herb content
quantify the fluorescence plastic particles. The fluorescence microscopy
percent
was used for additional confirmation of potential MPs especially for
Brand A 5 Sunflower oil 18.5% oil 1.5% salt Longtail tuna screening of smaller particles which were possibly overlooked by op­
Brand A 5 Olive oil 18.5% oil 1.35% salt Longtail tuna tical microscopy. The magnified fluorescence images (up to ×400)
Brand A 5 Sunflower oil 18% oil 1.5% salt-0.5% Longtail tuna
under ultraviolet light can be recorded allowing particles down to a few
herbs
Brand A 5 Brine water 28% water 2% salt Longtail tuna micrometers to be detected (Tiwari et al., 2019). Associated uncertainty
Brand B 5 Soybean oil 18% oil 1.35% salt Yellowfin tuna with fluorescence technique is mostly related to the interference of
Brand C 5 Sunflower oil 18% oil 1.35% salt Yellowfin tuna other materials with MPs (Dehghani et al., 2017). However, using Nile
Brand D 5 Sunflower oil 18% oil 1.5% salt Longtail tuna Red (NR) staining can improve the identification of MPs in this method
Brand E 5 Sunflower oil 18% oil 1.5% salt Mackerel fish
and also rules out most non-plastic items such as lipid, chitin, and wood
Brand F 5 Soybean oil 18% oil 1.35% salt Yellowfin tuna
Brand G 5 Soybean oil 18% oil 1.4% salt Yellowfin tuna (Erni-Cassola et al., 2017; Kaya et al., 2018; Maes et al., 2017). Hence,
all filter papers were soaked in NR solution and then checked by

2
R. Akhbarizadeh, et al.
fluorescence microscope. A NR solution was prepared by adding
0.005 g of NR powder in 25 ml acetone. NR is a lipophilic dye that has
been used as a promised tool for fluorescently labeling of MPs
(Dobaradaran et al., 2018; Toussaint et al., 2019) and has been suc­
cessfully applied for the rapid detection and quantification of small MPs
in environmental samples (Erni-Cassola et al., 2017; Maes et al., 2017).
The excitation/emission for fluorescent analysis was 460/525 nm.
2.3.3. Micro-Raman analysis
Since the accurate diagnosis of plastics is not feasible with only
visual methods, the third step of Micro-Raman analysis was used in the
identification of the MPs to confirm the previous analyses and to
identify the chemical composition of the plastics. This method is widely
used for the identification and quantification of MPs in environmental
samples (Allen et al., 2019; Erni-Cassola et al., 2017; Käppler et al.,
2016; Lenz et al., 2015; Song et al., 2015). It should be noted that due
to the possible interference of the NR fluorescence with the Raman
signals, the particles were bleached for two min before analysis
(Halstead et al., 2018). The polymer types of the identified plastic
particles were inspected by a Confocal Raman Spectroscopy (Horiba
LabRam HR Evolution, Japan) coupled with an Olympus microscope.
The spectra ranged between 400 and 1800/cm. The spectrometer was
adjusted with 600 grooves (lines)/mm grating and equipped with a
single-mode 785 nm laser with 10–100 mW output power. Moreover,
the samples were inspected under ×50 magnification and the in­
tegration times ranged from 20 to 25 s. Moreover, the confocal hole
ranged from 200 to 300 μm, the slit was set to 100 μm, and the accu­
mulations were 5 for all analyzed particles. In order to enhance the
spectrum quality and reduce the noise, baseline correction and noise
removal were carried out. Using to the method described by Erni-
Cassola et al. (2017), the size of small particles was checked by the scale
bar and square root of the area measured in micro-Raman analysis for
each particle. Finally, the corrected spectra were checked and com­
pared with the spectral libraries (reference database from Bio-Rad's
KnownItAll® ID Expert software) to identify their type. MPs were
identified with a high certainty level (more than 85%) of the most
appropriate match based on the correspondence of peak positions.
2.3.4. SEM-EDX analysis
In the fourth and last step of the MPs analysis, a scanning electron
microscope (SEM) combined with an energy dispersive X-ray (EDX)
unit was applied to check the surface morphology of identified MP
particles and their chemical composition. The instrument was a
TESCAN-VEGA3 (TESCAN, Czech Republic) coupled with an EDX
spectrometer. MPs were transferred onto an adhesive and conductive
carbon tape and a nanometric gold layer was used on the surface of the
particles by a Q150R-ES instrument (Quorum Technologies, England)
to prevent the sample's charging. The SEM-EDX analysis is generally
used to investigate the morphology and the elemental composition of
previously identified polymers. The electron accelerating voltage of
SEM was 10 and 20 kV in a backscatter mode. Also, images were mainly
obtained by secondary electrons to gain the best possible resolution.
2.4. Statistical analysis
The XLSTAT software (2016) and Microsoft Excel 2016 were used
for the statistical analysis. In order to identify if parametric or non-
parametric tests were the appropriate the descriptive statistics, and the
Shapiro-Wilk test was conducted on the data. Due to the lack of data
normality, non-parametric tests (Kruskal Wallis test or the Mann-
Whitney U test) were applied to determine the significance of differ­
ences in MPs numbers, size, shapes, colors, and fish species among the
different brands of the analyzed canned fish. A linear regression ana­
lysis was used to determine the relationship between the plastics and
the salt content of the different canned samples. Statistical significance
was accepted at p < 0.05.
3
Marine Pollution Bulletin 160 (2020) 111633
2.5. Human intake of microplastics
There are many questions regarding the human health risks posed
by plastic particles (Dehaut et al., 2019). Hence the estimation of
human exposure to MPs through seafood consumption is important. In
this study, two approaches were used to estimate the human exposure
to MPs through canned fish consumption. The first one was according
to data from Iranian Fisheries Organization Statistical Yearbook
(IFOSY) regarding the rate of canned fish consumption per capita for
Iranian people (4.94 g/person/day) for adults (IFOSY, 2015). The
second one was based on the published serving sizes of foods by the
Food and Drug Administration (FDA): 85 g (1 serving) for adults (FDA,
2016). The human exposure to plastics was calculated using the mean
number of MPs in canned fish. The mean intake (MI) was calculated
using the following equation:
MI = IR × C
where IR is the canned fish consumption rate (g/meal) or (g/day/ca­
pita) and C is the MPs number (items/g) (Akhbarizadeh et al., 2019;
Barboza et al., 2020).
3. Results and discussions
3.1. Microplastics in canned fish
Three blue ribbon-shaped fibers were found in the control petri
dishes and procedural blanks. Hence, similar fibers were excluded from
the potential MPs list in the first stage (visual quantification). Out of the
50 investigated canned tuna and mackerel fish from seven popular
brands, 40 (80%) had potential MPs in their fish flesh after visual in­
vestigation. After visual quantification, all filters were subjected to
fluorescence analysis using NR to rule out non-plastic particles. In the
third stage, micro Raman analysis was used to confirm the detected MPs
from previous analysis and also distinguish the polymer types.
After excluding the verified non-plastic particles, 128 MPs were
identified in the 50 canned fish samples. In detail, among the 165
collected particles from the canned fish samples, 34 particles were ruled
out after optical (physiochemical parameters) and fluorenes analysis.
Then, μ-Raman analysis was used and 128 items were verified as MPs
(77.6% of the total particles were true MPs). As shown in Table 2,
Yellowfin tuna fish in soybean oil (brand F) had the lowest (mean
0.05 ± 0.01 items/g muscle), and longtail tuna fish in brine water
(brand A) had the highest (mean 0.22 ± 0.02 items/g muscle) plastics
abundance. Unfortunately, to date, there is no much similar research to
compare the obtained results, and the only research on plastic content
of canned sardine and sprats, was Karami et al. (2018) in which 9 meso-
and microplastics were identified in 4 out of 20 samples (Karami et al.,
2018). The possible reasons for difference between the results of pre­
sent study and the mentioned study might be due to the species di­
versity and/or pore size of the used filters. The digested fish flesh was
filtered through a 149 μm-filter membrane in the Karami et al. (2018)
study while, a 5 μm-filter was used in the present study. The importance
of the use of filters with sufficient pore size to prevent wastage of
smaller MPs particles was previously mentioned in the literature (Al-
Salem et al., 2020; Cai et al., 2020; Dehaut et al., 2019; Toussaint et al.,
2019; Walkinshaw et al., 2020). The larger pore size of the filter
membrane might have caused an underestimation of the number of MPs
with a smaller size in samples (Cai et al., 2020; Toussaint et al., 2019).
Accordingly, as the pore size or bead diameter decreases, the number of
plastic items found increases.
There were no statistically significant differences among samples
with different fish species, samples with various oil content (type and
percent), and samples with distinct herbs' content (Kruskal Wallis test,
p > 0.05). This statement is shown in Fig. S1 and the possible reason
could be the low number of samples in each group. Hence, further
studies with higher numbers of samples/various herbs and oil content
R. Akhbarizadeh, et al. Marine Pollution Bulletin 160 (2020) 111633

Table 2
Number of total cans, number of cans with microplastics (MPs), frequency of occurrence (%), total number of identified MPs, and abundance (mean ± standard
deviation) of total MPs in canned fish samples with different contents.
Brands and content Number of total Number of cans Frequency of Number of identified MP items/cans MP items/g (Mean ± SD)
cans with MPs occurrence (%) MPs (Mean ± SD)

Brand A-in sunflower oil 5 4 80 15 3.00 ± 0.37 0.15 ± 0.02

Brand B-in soybean oil 5 4 80 13 2.60 ± 0.34 0.13 ± 0.02
Brand C-in sunflower oil 5 4 80 12 2.40 ± 0.32 0.12 ± 0.02
Brand D-in sunflower oil 5 5 100 11 2.20 ± 0.25 0.11 ± 0.01
Brand E-in sunflower oil 5 5 100 15 3.00 ± 0.51 0.15 ± 0.03
Brand A-in olive oil 5 3 60 9 1.80 ± 0.27 0.09 ± 0.01
Brand F-in soybean oil 5 2 40 5 1.00 ± 0.12 0.05 ± 0.01
Brand A-in sunflower oil+ 5 4 80 16 3.20 ± 0.42 0.16 ± 0.02
herbs
Brand G-in soybean oil 5 5 100 10 2.00 ± 0.32 0.10 ± 0.02
Brand A-in brine water 5 4 80 22 4.40 ± 0.47 0.22 ± 0.02
Total 50 40 80 128 25.60 ± 0.87 1.28 ± 0.04

2.5 abundant of the detected MPs in canned tuna and mackerel fish samples
were fibrous. Specifically, 54, 38 and 8% of the identified MPs (after
2 y = 3.5895x + 1.0157 micro-Raman analysis) in canned fish were fibers, fragments, and films,
R² = 0.6973 respectively. Previous studies also reported fibers as the most common
MPs in fish samples (Barboza et al., 2020; Bessa et al., 2018; Guven
Salt content (%)

1.5
1 as the main tools in the fishery (Barboza et al., 2020; Neves et al., 2015;
0.5
0 Hence, finding of a large number of fibers in the gills, gastrointestinal
0 0.05 0.1 0.15 0.2
MPs (items/g)
Fig. 1. Relationship between the average level of microplastics in each brand
and its salt content.
are needed to verify their impacts on plastics content. The possible
correlation between MPs and the salt content of different canned
samples was investigated using correlation analysis and Kruskal-Wallis
test (Fig. 1). The results demonstrated that a statistically significant
positive correlation (p < 0.05) existed between MPs and the salt
content of samples. Hence, salt could be considered as a possible source
of MPs in canned fish. Salt is already reported as a potential source of
MPs in previous studies (Iñiguez et al., 2017; Karami et al., 2017a;
Kosuth et al., 2018; Yang et al., 2015). In addition, the used fish and
contact materials during cleaning and canning process are other pos­
sible sources. The uptake of MPs by fish could have happened both
directly from the surrounding environment and indirectly from their
food (Barboza et al., 2020; Ding et al., 2018; Lusher et al., 2013). The
presence of MPs in edible parts of fish has been previously reported
(Abbasi et al., 2018; Akhbarizadeh et al., 2018, 2019; Akoueson et al.,
2020; Barboza et al., 2020; Karami et al., 2017b). However, the re­
ported values for edible parts were significantly lower than for the di­
gestive tracts and gills in previous studies. In addition, the laboratory
contamination and atmospheric deposition may affect the MPs' level of
the fish flesh (Akoueson et al., 2020). Besides the mentioned sources,
the plastic particles in canned fish could also have originated from the
fish gutting in the canning factory (MPs in gastrointestinal tracts) and
from the canning process (Garrido Gamarro et al., 2020; Karami et al.,
2018).
3.2. Microplastics' physical characteristics
MPs with an extensive diversity of shape, color, and size were de­
tected in most of the studied samples (Table 2 and Fig. 2). The most
et al., 2017; Koongolla et al., 2020; Lusher et al., 2013; Neves et al.,
2015). It should be considered that fishing nets and ropes are still used
Welden and Cowie, 2017) and their breakdown can make microfibers
(Welden and Cowie, 2017). Moreover, synthetic microfibers are very
common in cloths, and atmospheric fiber shedding has been detected
almost everywhere (Bessa et al., 2018; Napper and Thompson, 2016).
0.25 tracts, and muscle of fish is not surprising. Fig. 3 illustrates some col­
lected MPs in canned tuna and mackerel fish samples and their fluor­
escent images by using NR. Color of detected MPs in canned fish was as
follows: black (61%) > blue (17%) > green (12%) > red
(7%) > transparent (3%). That the majority of the MPs in marine
organisms are black has been already reported in the literature
(Akhbarizadeh et al., 2019; Lusher et al., 2013; Murphy et al., 2017).
The color diversity of the collected MPs reflects the various sources of
the MPs (Bellas et al., 2016).
The length of investigated fragments and films in the studied sam­
ples ranged from ⁓10 to ⁓1100 μm and ⁓70 to ⁓1000 μm, respec­
tively. Moreover, fibers ranged in length from ⁓100 to ⁓8000 μm
(Fig. 2). In the case of fibers, if two dimensions are in the range of
micrometer, it would be sufficient to qualify the item as a MP
(Hartmann et al., 2019). The most predominant size of identified fibers,
fragments, and films were in the range of 1–5 mm (n = 35), 10–50 μm
(n = 20), and 100–500 μm (n = 7), respectively. The size of the meso-
and microplastics reported in canned sardine and sprats was between
190 and 3800 μm (Karami et al., 2018). As previously mentioned, they
used a 149 μm-filter membrane while a 5 μm-filter was used in the
present study. Hence, their identified MPs were lower in number and
larger in size compared with the results of the present study. As the
larger pore size of the filter membrane might have caused a reduction in
the number of MPs with a smaller size found in samples (Cai et al.,
2020; Toussaint et al., 2019), an emphasis on the use of filters with
sufficient pore size to prevent wastage of smaller microplastic particles
has been previously mentioned in the literature (Al-Salem et al., 2020;
Cai et al., 2020; Dehaut et al., 2019; Toussaint et al., 2019; Walkinshaw
et al., 2020). Hence, as the pore size or bead diameter decreases, the
minimum size of the found plastic particles decreases.
The detected MPs in the studied canned fish may come from the
preparing and packaging process (canneries) or translocation of MP
items into fish flesh (Karami et al., 2018). The canning of fish is a
multiple process and divided into a number of steps. From the time of
capture, until it is supplies to the market as canned fish, raw fish is

4
R. Akhbarizadeh, et al. Marine Pollution Bulletin 160 (2020) 111633

a Brand A-in brine water

Brand G- in soybean oil
Brand A-in sunflower oil+herbs
Brand F-in soybean oil
Brand A-in olive oil
Brand E-in sunflower oil
Brand D-in sunflower oil
Brand C-in sunflower oil
Brand B-in soybean oil
Brand A-in sunflower oil
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%

<50 50-100 100-500 500-1000 1000-5000 >5000

b Brand A-in brine water

Brand G- in soybean oil
Brand A-in sunflower oil+herbs
Brand F-in soybean oil
Brand A-in olive oil
Brand E-in sunflower oil
Brand D-in sunflower oil
Brand C-in sunflower oil
Brand B-in soybean oil
Brand A-in sunflower oil
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%

Black White/Transparent Red Blue Green/yellow

c Brand A-in brine water

Brand G- in soybean oil
Brand A-in sunflower oil+herbs
Brand F-in soybean oil
Brand A-in olive oil
Brand E-in sunflower oil
Brand D-in sunflower oil
Brand C-in sunflower oil
Brand B-in soybean oil
Brand A-in sunflower oil
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%

Fiber Frag Film

Fig. 2. Size distribution (a), color (b) and shapes (c) of identified microplastics in the studied canned fish samples. (For interpretation of the references to color in this
figure legend, the reader is referred to the web version of this article.)

submitted to a variety of cleaning and canning steps. After the fish is
caught, the time to transfer fish to the cannery should be as short as
possible. However, chilling and freezing are sometimes essential for
holding the raw fish before the canning process. In the factory, the
washing and dressing of fish is the first step in the canning process. The
three general types of washing for fish are soaking or tank washing,
washing by agitation, and spray washing. However, tank washing may
act as a source of contamination for fish. After washing, the viscera are
removed and careless cleaning may result in the inclusion of waste (i.e.
blood, parts of tissues, and MPs) in the canned products. Precooking is
done in steam for at least 8 h for large fish. Then, fish are allowed to air
cool, often overnight (Featherstone, 2016). Hence, fish may subject to
environmental contamination (i.e. airborne plastic particles). If it has
not been already done so, the tail, head, fins, and the skin are removed
and the edible portions are picked and then transferred to filling areas
(Featherstone, 2016). Filling of cans may be accomplished either by
filling machines or hand (Warne, 1988). Using hand filling method is
very common in many countries and leads to more contamination in­
cluding plastic particles, metal fragments and other debris. In the next
step, dry salt, water, oil, and other food additives such as herbs are
added to the filled cans (Featherstone, 2016). Each of these food ad­
ditives can be a source of MPs contamination in the final products.
Finally, thermal treatment (cooking and sterilization) are employed for
reducing moisture and to inactivate endogenous enzyme and micro­
organism's activity (Aubourg, 2001). The cans are then sealed.
Large predators such as tuna and mackerel may ingest different size
of MPs. Large pieces are easily removed as a result of continued in­
gestion and excretion, while, the tiny ingested plastic debris may be

5
R. Akhbarizadeh, et al.
Fig. 3. Some detected microplastics in canned fish samples. The scale bar for a, b, c, d and e represents 1 mm, 30 μm, 500 μm, 50 μm, and 100 μm, respectively.
translocated through the gut wall or through the gills and end up in the
tissues of the various organs including the edible ones (Galloway et al.,
2017; Grigorakis et al., 2017; Triebskorn et al., 2019; Zeytin et al.,
2020). The possible translocation of MPs through the gastrointestinal
tract or through the gills into the other organs (i.e. liver, and muscle)
has been reported in previous studies (Akhbarizadeh et al., 2019; Avio
et al., 2015; Collard et al., 2017; Grigorakis et al., 2017; Kashiwada,
2006; Zeytin et al., 2020). The results of Zeytin et al. (2020) showed
that the entrance of MPs to lymphatic and/or vascular systems through
the gastrointestinal tract is the most likely pathway for translocation of
MPs to the organs. However, size, shape, surface charge, and compo­
sition of MPs and organism's tissue damage, loss of cells, membrane
injuries, and disease might influence the possible translocation of MPs
to the blood/lymph and then muscles of marine organisms (Elizalde-
Velázquez et al., 2020; Powell et al., 2010; Triebskorn et al., 2019;
Zeytin et al., 2020). Upon entrance, endocytosis, phagocytosis, eosi­
nophilic granule cells, and specialized enterocytes namely ‘microfold
cells’ could be involved in the transport of macromolecules, micro­
organisms, and plastic particles into the tissues (Browne et al., 2008;
Carr et al., 2012; Von Moos et al., 2012; Zeytin et al., 2020). Large
particles which are not able to pass through the enterocytes/transcel­
lular uptake, are instead passed between them in a paracellular manner
(Volkheimer, 1975). The paracellular mechanical process (persorption)
which is potentially facilitated by the weakening of gap junctions, is
driven by the kneading of particles through an epithelial layer into the
underlying tissues (Carr et al., 2012; Wright and Kelly, 2017). In ad­
dition, cationic particles are more likely to attach to a cell surface and
be taken up by active transport mechanisms than anionic and neutral
particles (Zhu et al., 2013). An active immune response and a good
excretion of MPs are the probable reasons for the low numbers of MPs
in the fish fillets. The MPs in the blood and stomach of fish could not be
fully washed out from the fillets prior to the canning process. Hence,
the plastic items in fish cans could also come from the blood and sto­
mach of fish in the canning factory or from the contamination during
the canning process (Garrido Gamarro et al., 2020). Those large plastic
6
Marine Pollution Bulletin 160 (2020) 111633
particles (> 150 μm) which are not adsorbed by the intestine (Lusher
et al., 2017) and which are not similar to the MPs collected from the
environment, may possibly have originated from the canning process
(Garrido Gamarro et al., 2020; Karami et al., 2018). The MPs collected
from the environment are mostly eroded with an irregular shape, and
an uneven surface (Acosta-Coley and Olivero-Verbel, 2015; Karbalaei
et al., 2019a). Hence, the surface structure of the identified MPs can be
helpful for identification of the source of plastic contamination in
canned fish.
3.3. Microplastics' type and chemical composition
Raman spectroscopy has some advantages over other techniques for
MPs analysis such as low sample amount requirement, small size
identification (1–100 μm), higher sensitivity, non-destructiveness, eco-
friendliness, and high throughput screening (Araujo et al., 2018;
Oßmann et al., 2018; Pico et al., 2018; Xu et al., 2019). Furthermore,
for small sized MPs (less than 20 μm) the signal to noise ratio of micro-
Raman spectroscopy is lower than micro- Fourier-transform infrared
spectroscopy (Käppler et al., 2015). Hence, out of 131 possible MPs
(after optical and fluorescence analysis), 70 particles were chosen
randomly for analysis using the Confocal Raman Spectrometer. Based
on the results, only 2% of the analyzed particles that were initially
detected as plastics were really composed of natural cellulose, about
80% of them corresponded to six different polymer types, and the
others (⁓18%) belonged to a combination of two plastic types espe­
cially for black fragments and for those items that had two colors (i.e.
green and yellow) (Fig. S2). The most abundant identified plastics were
polyethylene terephthalate (PET, 36.6%), polystyrene (PS, 17.6%), and
polypropylene (PP, 13.5%) followed by combination of PS-PP (10.2%),
a combination of PS-PET (7.9%), nylon (7.1%), polyvinyl chloride
(PVC, 3.9%), and low density polyethylene (LDPE, 3.2%). Previous
studies also reported that PET, PP, and PS are the most commonly
identified polymers in aquatic organism and prepared seafood (Avio
et al., 2015; Collard et al., 2018; Karami et al., 2018; Koongolla et al.,
R. Akhbarizadeh, et al.
2020). In addition, the presence of PET, PVC in canned sardine was also
reported by Karami et al. (2018). According to Karami et al. (2018) the
original size and shape of almost all plastic types (except low density
polyethylene-LDPE), were maintained after the canning process. The
possible reason for the low abundance of LDPE items is their having the
lowest melting point (110 °C) among different plastic types (Karbalaei
et al., 2019b). Hence, they may be deformed and/or melted at the high
pressure and temperature of the canning process (Karami et al., 2018).
The PET type plastics are widely used in the plastic bottles and textile
industry (clothes and blankets with synthetic fibers) (Alomar et al.,
2017; Hidalgo-Ruz et al., 2012; Liu et al., 2019a; Teng et al., 2019) and
their high proportion in canned samples may confirm the hypothesis
that they were directly/indirectly release into the Persian Gulf. PS is
widely used in food packaging materials, textile, fishing gears, and
insulation in industry (Alomar et al., 2017; Pirsaheb et al., 2020; Teng
et al., 2019). In addition, nylons are mainly used in fisheries activities
and fiber manufacturing (Ferreira et al., 2020; Zitouni et al., 2020). PP
has been used in different goods for human daily life including bottle
caps, ropes in the aquaculture industries, tanks, and junks, textiles,
drinking straws, and car fenders (Cho et al., 2019; Li et al., 2016;
Napper and Thompson, 2016; Welden and Cowie, 2017; Zander et al.,
2017). Those particles that showed two types of polymers might have
originated from the recycled or mixed plastics (co-polymers) (Florestan
et al., 1994; Sobhani et al., 2019; Zander et al., 2017). In order to re­
inforce PP and prevent excessive crystallinity of PET during industrial
processing, polymer blending technique by adding rigid and amorphous
polymers such as PS are commonly used (Kolahchi et al., 2015; Li et al.,
2009; Wellen, 2014). PP-PS copolymers are usually immiscible and
used in car dashboards and computer cases (Brostow et al., 2008; Li
et al., 2009). The copolymer of PET-PS is suitable for applications in
insulation, composite reinforcement and textiles (Zander et al., 2017).
Elemental composition and surface structure of verified MPs (after
micro-Raman analysis) were investigated using SEM-EDX.
Environmental degradation such as erosion, weathering, temperature,
humidity, and photooxidation can significantly change the surface
structure of MPs (Karbalaei et al., 2019a).The surface of the virgin MPs
is flat and smooth, while the surface of the weathered plastics is irre­
gular and rough with fractures, cracks, notching and many small debris
and fragments (Dong et al., 2020). In the present study, 20 identified
MPs were subjected to SEM- EDX analysis. As shown in Fig. 4, various
fragments and films displayed different shape and surface roughness,
while, identified fibers had a plain surface. One of the preliminary
specifications that can be applied to scan the plastic particles by SEM is
the created face texture by environmental exposure (Wang et al., 2017).
Polymer aging and oxidative/mechanical weathering could be easily
identified by SEM analysis. The irregular and angular shapes of the MPs'
surfaces represent the mechanical and photochemical breakdown of
larger plastic materials (Ding et al., 2019; Wang et al., 2017). In ad­
dition, mechanical weathering can result in surface characteristics such
as gouges and grooves (Zbyszewski et al., 2014). Rough surfaces of MPs
could lead to an enhancement their surface area and thus increase the
surface level of organic and inorganic hydrophilic pollutants (Ding
et al., 2019). The EDX tests indicated that the identified particles were
plastic and showed their chemical composition. The results showed that
all the MPs debris are mainly contained C and O. However, Cl, Si, and S,
together with trace quantities of Ti, Al, and Cu, were present in some
particles. The O/C ratio is a potential indicator of oxidation degree of
MPs (Liu et al., 2019b). The O/C ratio of weathered (oxidized) MPs is
0.1–0.5, while its ratio for virgin MPs is 0.01–0.03 (Dong et al., 2020).
The O/C ratio of the analyzed MPs was in the range of 0.21–0.50, which
indicates that all of them were oxidized MPs. As plastics are composed
of both organic and inorganic forms of certain commonly found ele­
ments, such as carbon, hydrogen, oxygen, silicon, sulfur, and chlorine,
the presence of unusual trace elements may reflect their being either
additives or adsorbents (Karami et al., 2018; Kowalski et al., 2016). Al
and Cu have been shown to be sorbed to marine MPs (Fries et al., 2013;
7
Marine Pollution Bulletin 160 (2020) 111633
Holmes et al., 2014). On the other hand, titanium dioxide (TiO2) is
usually added to different plastic polymers as a filler, non-toxic pig­
ment, and UV blocker (Fries et al., 2013; Karami et al., 2018; Yang
et al., 2004). Dong et al. (2020), found Ti on some PVC and PET par­
ticles. SEM-EDX of reference particles of PVC generated the unique
features of strong chlorine peaks in the EDX spectrum (Fig. 4d and e),
fairly bright backscattered electrons (BSE) frequency, and fairly smooth
and rough surfaces (Tooma et al., 2015; Wang et al., 2017). As can be
seen in Fig. 4, other types of the identified plastic (i.e. PET, PS, and PP)
have no different EDX peak other than a strong carbon peak and a
smaller O peak (Wang et al., 2017).
3.4. Human intake of microplastics
The presence of plastic particles in seafood and their products can
be consider as an emerging risk (a possible threat) for human health
(Akoueson et al., 2020; Galloway, 2015; Smith et al., 2018). Hence,
their introduction into human food should be monitored carefully. The
rate of canned fish consumption per capita for Iranian people was es­
timated 4.94 and 1.53 g/person/day for adults and children, respec­
tively (IFOSY, 2015; Rahmani et al., 2018). It should be noted that this
consumption rate was estimated for tuna fish in sunflower oil. So, the
intake of plastic items through canned tuna fish in sunflower oil was
234 and 72 items/g/year for adults and children, respectively. In an­
other point of view, to examine the potential risks for MPs intake
through canned fish consumption, the canned fish meal size for adults
and children was assumed to be 85 g (1 serving) and 40 g, respectively
(FDA, 2016). Hence, the mean intake of MPs after taking of canned fish
in olive oil, soybean oil, sunflower oil, sunflower oil and herbs, and
brine water were 8, 8, 11, 13, and 19 items/85 g for adults and 4, 4, 5,
6, and 9 items/40 g for children, respectively. Based on the total mean
of plastic particles in canned fish samples (0.13 items/g, n = 50), the
average intake of MPs in four different scenarios (one, two, four, and six
meals/week) of canned fish consumption are presented in Table 3. It is
worth mentioning that the canned fish consumption for the general
population is usually 2 times per week or less. However, eco-tourists
(those who spend one or two weeks in nature) usually consumed more
canned foods, especially canned tuna fish, during their journey. Hence,
6 times a week (almost every day) canned fish consumption was used as
a worst-case scenario for special consumers. According to the calcula­
tions, the intake of MPs for adults ranged from 572 to 3432 particles/
year. This is much higher than the findings of Karami et al. (2018) and
as previously mentioned the probable reason is the higher presence of
particles with a size of smaller than 149 μm in canned fish. However,
the obtained results are comparable with those previously estimated
values for humans' fish consumption in Europe (842 MP items/year),
Portugal (3078 MP items/year), Spain (2576 MP items/year), Italy
(1679 MP items/year), United States (1156 MP items/year), Brazil (518
MP items/year), and Iran (877–3742 MP items/year) (Akhbarizadeh
et al., 2018, 2019; Barboza et al., 2020). Moreover, consumers of
shellfish in United Kingdom, Belgium, Europe, and China might ingest
123, 4620, 11,000, and 10,800 MP items/year, respectively (Catarino
et al., 2018; EFSA, 2016; Van Cauwenberghe and Janssen, 2014).
Hence, where the consumption rate of seafood is high and the en­
vironment is more polluted with plastic particles, the human uptake of
these tiny particles should be more considered. In addition to seafood
products, the presence of MPs items in some types of beverages, food
additives and foods (Akhbarizadeh et al., 2020a; Kim et al., 2018;
Kosuth et al., 2018; Liebezeit and Liebezeit, 2014; Peixoto et al., 2019;
Wiesheu et al., 2016) is also well documented. Therefore, these avail­
able data and numerical calculations raise a question regarding the fate
of the ingested small polymer particles in the human body.
There is still a huge lack of knowledge regarding the accumulation
and toxicological effects of the ingested MPs in human bodies (Barboza
et al., 2018; Toussaint et al., 2019). The presence of MPs in human faces
(Schwabl et al., 2019) indicated that humans can eliminate some of the
R. Akhbarizadeh, et al. Marine Pollution Bulletin 160 (2020) 111633

Fig. 4. SEM-EDX analysis of some identified microplastics in canned fish samples.

Table 3 gastrointestinal tracts' tissues), the indirect harm of pathogenic and

The average intake of microplastics for canned fish consumers. non-pathogenic bacteria, chemicals, and additives of ingested plastics
Canned fish Adults Children
should also be considered (Barboza et al., 2018; Dehaut et al., 2019;
consumption Hermsen et al., 2018; Smith, 2018). Although desorption of the ad­
per week Items/ Items/ Items/year Items/ Items/ Items/year sorbed pollutants such as persistent organic pollutants (POPs), heavy
week month week month metals, and released of additives such as bisphenol-A and phthalates
1 time 11 44 572 5 20 260
may also occur in the human body (Akhbarizadeh et al., 2020b;
2 times 22 88 1144 10 40 520 Hermsen et al., 2018; Wright et al., 2013), the actual risk is a subject of
4 times 44 176 2288 20 80 1040 debate (Dehaut et al., 2019; Koelmans et al., 2016; Rist et al., 2018).
6 times 66 264 3432 30 120 1560 Nevertheless, the intake, absorption, and excretion of MPs depend on
many parameters including sex, age, lifestyle options (physical ac­
tivity), disease, and geographic location (Barboza et al., 2020;
ingested plastic particles. It is thought that more than 90% of the in­
Toussaint et al., 2019). Hence, more scientific investigations are needed
gested micro- and nanoplastics are eliminated through the excretory
to estimate the exact human exposure to MPs through their diet and
system of human's body (Smith et al., 2018; Wright and Kelly, 2017).
consequently their toxicological effects.
However, the intestinal uptake and translocation of ingested plastic
particles across the mammalian gut have been shown to occur (Carr
et al., 2012; Hussain et al., 2001). Obviously, the size, shape, surface 4. Conclusions
chemistry, surface charge, and polymer type of MPs plays an important
role in their retention and clearance rate and also in their effects in the The existence of MPs in canned tuna and mackerel fish samples was
human body (Barboza et al., 2020; Rainieri and Barranco, 2019; Smith, investigated in the present study. To the best of our knowledge, this is
2018). It has been assumed that the absorption and cellular uptake of the first study that checks the presence of MPs in tuna and mackerel
MPs smaller than 150 μm may occur after ingestion (Barboza et al., canned fish. The results demonstrated that 80% of the analyzed samples
2020; EFSA, 2016). In addition, MPs in the range of 0.1–10 μm would had at least one MP. The MPs' content of canned seafood could be in­
be able to penetrate into organs, cross cell membranes, the blood-brain creased in the presence of added ingredients such as salt. However,
barriers and the placenta (Barboza et al., 2018; Browne et al., 2008; further studies are needed to investigate the exact impacts of herbs, oil
EFSA, 2016; Lusher et al., 2017). The results of in vitro studies with types, and other food additives on the MPs content of canned fish.
epithelial and cerebral human cells showed the potential cytotoxic ef­ Moreover, based on the EDX analysis, trace elements (i.e. Ti, Cu, Al)
fects of micro- (10 μm) and nano-plastics (40–250 nm) on human cells were found on MPs that are possibly either additives or adsorbents. The
in terms of oxidative stress (Schirinzi et al., 2017). Beside the physical concomitance of the detected MPs and trace elements revealed the
injuries of MPs (inflammation, cellular necrosis, and lacerations of possible risks posed by long-term consumption of canned fish in human

8
R. Akhbarizadeh, et al.
populations that depend to a great extent on canned seafood. In addi­
tion, the presence of tiny MPs (10–50 μm) in seafood products, such as
canned tuna fish, indicates that more scientific attention should be
given to the possible health risks of the chronic exposure of consumers
to plastic in food. Hence, further study is indicated of MPs as food
pollutants and of their effects on human health in order to identify the
knowledge gaps in this field.
CRediT authorship contribution statement
Razegheh Akhbarizadeh: Sampling, Samples preparation,
Conceptualization, Methodology, Analysis, Writing-original draft and
revision, Software.
Sina Dobaradaran: Supervision, Writing-Review and Editing,
Methodology, Resources, Project administration, Funding acquisition.
Iraj Nabipour: Writing-Review and editing.
Saeed Tajbakhsh: Resources and Analysis.
Amir Hossein Darabi: Writing-Editing.
Jörg Spitz: Writing-Review and Editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ­
ence the work reported in this paper.
Acknowledgement
This research was financially supported by the Bushehr University
of Medical Sciences (grant No. 1286). The authors would also like to
extend their gratitude to the laboratory staff of Systems Environmental
Health and Energy Research Center for their support. We also thank Dr.
Bruce Spittle for helping us in English editing the paper.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.marpolbul.2020.111633.
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