Environmental Pollution 252 (2019) 1246e1256

Contents lists available at ScienceDirect

Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Partitioning of chemical contaminants to microplastics: Sorption

mechanisms, environmental distribution and effects on toxicity and
bioaccumulation☆
Paula S. Tourinho a, *, Vladimír Ko

cí a, Susana Loureiro b, Cornelis A.M. van Gestel c
a
Department of Environmental Chemistry, Faculty of Environmental Technology, University of Chemistry and Technology Prague, Prague, Czech Republic
b
Department of Biology & CESAM, University of Aveiro, Aveiro, Portugal
c
Department of Ecological Science, Faculty of Science, Vrije Universiteit, Amsterdam, the Netherlands

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

Article history: There is an increasing awareness of the threats posed by the worldwide presence of microplastics (MPs)
Received 17 December 2018 in the environment. Due to their high persistence, MPs will accumulate in the environment and their
Received in revised form quantities tend to increase with time. MPs end up in environments where often also chemical con-
24 May 2019
taminants are present. Since the early 2000s, the number of studies on the sorption of chemicals to
Accepted 8 June 2019
Available online 11 June 2019
plastic particles has exponentially increased. The objective of this study was to critically review the
literature to identify the most important factors affecting the sorption of chemical contaminants to MPs.
These factors include the physicochemical properties of both the MPs and the chemical contaminants as
Keywords:
Sorption
well as environmental characteristics. A limited number of studies on soil together with an increased
Mass balance model notion of the importance of this compartment as a final sink for MPs was observed. Therefore, we
Mixture toxicity assessed the distribution of model chemicals (two PCBs and phenanthrene) in the soil compartment in
Bioavailability the presence of MPs using a mass balance model. The results showed a high variation among chemicals
and microplastic types. Overall, a higher partitioning to MPs of chemical contaminants in soil is expected
in comparison to aquatic environments. As sorption to a large extent determines bioavailability, the
effects of combined exposure to chemicals and MPs on the toxicity and bioaccumulation in biota are
discussed. Finally, some considerations regarding sorption and toxicity studies using MPs are given.
© 2019 Elsevier Ltd. All rights reserved.

1. Introduction approximately 6300 Mt of plastic waste has been generated glob-

ally (Geyer et al., 2017). Only about 20% of this waste was recycled
Nowadays, one of the greatest concerns regarding environ- or incinerated, while 80% is either accumulated in landfills or
mental contamination is the presence of plastics in diverse eco- released to natural environments (Geyer et al., 2017).
systems (Eriksen et al., 2014). Plastics are versatile, low-cost Regarding the plastic waste disposed in the environment,
materials that can be used in a wide number of applications and recently special attention has been drawn to microplastics (MPs).
products. ‘Plastic’ is a generic term used for both natural and syn- MPs are defined as plastic particles with sizes ranging from 1 mm to
thetic polymers. However, synthetic materials account for >90% of 5 mm (Thompson et al., 2004). They can be divided into primary
the plastics produced, such as polyethylene (PE), polypropylene and secondary microplastics (Arthur et al., 2009). Primary MPs are
(PP), polyvinyl chloride (PVC), polyethylene terephthalate (PET) produced and discharged to the environment in the micro or milli-
and polystyrene (PS) (Andrady & Neal, 2009). Moreover, these scale size (such as the beads used in cosmetics). Secondary MPs are
materials are highly persistent, being the most abundant anthro- the result of the breakdown of larger plastic fragments after being
pogenic waste. Until the year 2015, it is estimated that introduced into the environment (Arthur et al., 2009), normally
caused by UV radiation and physical abrasion.
For many years, most studies were conducted mainly on marine
☆
This paper has been recommended for acceptance by Maria Cristina Fossi. environments, reporting alarming quantities of microplastics. For
* Corresponding author. University of Chemistry and Technology Prague, instance, estimations on the total amount of MPs present in oceans
Technicka 5, 160 00, Prague, Czech Republic.
range from 15 to 51 trillion particles (van Sebille et al., 2015). The
E-mail address: dasilvap@vscht.cz (P.S. Tourinho).

https://doi.org/10.1016/j.envpol.2019.06.030
0269-7491/© 2019 Elsevier Ltd. All rights reserved.
 P.S. Tourinho et al. / Environmental Pollution 252 (2019) 1246e1256 1247

number of studies on MPs in freshwater, freshwater sediment and may also be used as a synonym for absorption in some fields (Endo
soil compartments is increasing, though it is still much lower than & Koelmans, 2016). To avoid misleading interpretations, the terms
the number of marine studies. These compartments are suggested ‘partitioning’, ‘sorption’, and ‘ab/adsorption’ will be used
to be a very important sink of MPs. It is estimated that per year up throughout this review as defined below.
to 0.9 million metric tons of MPs are retained in the continental Sorption is the process of mass transfer of a chemical from a
environments, while up to 0.11 million metric tons reach the oceans liquid (or gaseous) phase to a solid phase. Environmental media can
(Horton et al., 2017). be very complex in their composition, having many phases for the
With the high accumulation in the environment, MPs are not distribution of chemical contaminants. For example, aquatic phases
only potential contaminants but they can also act as an extra have suspended sediments, dissolved and particulate organic
compartment for the partitioning of chemicals. The partitioning matter, while soils and sediments also have dissolved organic
and sorption between compartments is extremely important as it matter and the porewater. Based on the definition given by Endo &
determines the fate and the bioavailability of chemical compounds. Koelmans (2016), we will use partitioning to refer to scenarios
The chemical, also named sorbate, is distributed depending on its involving other phases of the media (e.g., bridging effect involving
affinity for the sorbent phases. Therefore, the distribution of humic acids). And sorption will be used when the process is clearly
chemical contaminants in the environment depends directly on restricted to transfer between the liquid phase and MPs (as the
their physicochemical properties and on environmental factors. solid phase). Sorption includes the attachment to surfaces
Even though the first reports on contaminant sorption to plastic (adsorption) and the assimilation into the bulk of a matrix (ab-
particles dated back to the 1970s and 1980s (Mato et al., 2001, and sorption). The detachment from the solid phase is named desorp-
references cited therein), only in the early 2000s this subject star- tion. Both absorption and adsorption can happen concurrently and
ted to be investigated more intensively (Mato et al., 2001; Endo it can be difficult to discriminate one process from the other (Endo
et al., 2005). These studies observed high concentrations of et al., 2008; Da˛ browski, 2001). For this reason, we have chosen to
chemical contaminants on MPs collected in marine environments, use the term sorption, regardless of the original term used by the
indicating that sorption to MPs was likely to be a relevant issue. authors of the cited studies.
Consequently, partitioning studies under laboratory conditions The partitioning of chemicals between two phases is a dynamic
were found necessary to understand the sorption of chemical process and a state of equilibrium is reached when the concen-
contaminants to microplastics. The number of studies in this field is trations in both phases are constant. At equilibrium, isotherm
exponentially increasing. A search on the Web of Science database equations can be applied in order to obtain equilibrium constants
for “microplastics sorption” produced 91 results, with more than (Tables SIe1). These are empirical equations, and many authors
half of the papers being published only between 2018 and 2019 have successfully used isotherms to determine the sorption of
(Figure SI-1). With the increasing number of studies on the sorption different chemicals to MPs.
of chemicals to MPs, this paper aims at critically reviewing the In a linear isotherm model, the sorption distribution coefficient
literature to gather information on the relevant mechanisms and (Kd) is the ratio between the concentration in the solid phase (i.e.,
factors driving the sorption process. Even though MPs can also amount of chemical per unit mass of MP) and the equilibrium
release additives, like plasticizers, to the environment, this review concentration in the liquid phase. The relationship between solid
will focus only on the sorption/desorption of chemical contami- and liquid phases however, might not be linear, which asks for the
nants (aside from the additives) from the environment to MPs. use of non-linear sorption isotherms. A number of theories have
First, a brief summary of the theory of sorption isotherms and been developed since the first studies on sorption processes
sorption kinetic models will be presented, followed by an overview (Da˛ browski, 2001), but two non-linear isotherms are mostly used.
of the mechanisms responsible for the affinity between MPs and The Freundlich isotherm, which has been widely applied for
chemicals, and the possible influencing factors. Since a few studies chemical sorption to MPs, describes the sorption to heterogeneous
have been conducted in the field, the differences between labora- surfaces. In this model, the occupancy of high energy sites occurs,
tory and field data will also be discussed. followed by the occupancy of low energy sites (Guo et al., 2018).
Throughout the review process, it was evident that studies Alternatively, the Langmuir isotherm has been applied, for
conducted on soil are lacking. In order to fill this gap, we used a considering homogenous surfaces in which the sorbate will have
mass balance model to determine the importance of MPs as a one-layer (monolayer) coverage and with a finite number of sorp-
compartment for chemical distribution in soils. Two PCB congeners tion sites. Extensions of the Langmuir model (Extended Langmuir
and phenanthrene were used as model chemicals and results are isotherm and Interaction Factor Model) can be used for assessing
compared with those obtained for other environmental the sorption of two sorbates simultaneously, as used by Bakir et al.
compartments. (2012) to study the sorption of phenanthrene and DDT to PVC (see
In addition, we review the toxicity outcomes of combined ex- Bakir et al. (2012) for the equations).
posures to MPs and chemical contaminants. Although a number of It is also possible to determine Kd values taking into account
studies used biomarkers (Browne et al., 2013; O'Donovan et al., other phases, such as dissolved organic matter as done by
2018; Brandts et al., 2018; Batel et al., 2016) or assessed neuro- Seidensticker et al. (2017). These authors used a linear isotherm
and genotoxicity (O'Donovan et al., 2018; Zhang et al., 2019b), this that includes the partitioning coefficient between organic matter
review will focus more on the studies that allow relating toxicity to and liquid phase (KDOM) and the concentration of dissolved organic
the sorption to MPs and help understanding its importance for the matter. This approach should be encouraged as unifying different
bioavailability of chemical compounds. Finally, we will discuss equilibrium constants to a single equation can produce more real-
some considerations to be taken into account when performing istic values than using separate equations.
sorption and toxicity experiments with MPs. In addition to the equilibrium partitioning coefficients, it is also
important to understand the rate of the sorption process, by using
2. Sorption isotherms and sorption kinetics empirical kinetics equations (Tables SIe1). Kinetic models are good
for evaluating the sorption efficiency, understanding rate-limiting
The terms ‘partitioning’ and ‘sorption’ are often used as syno- steps, and identifying sorption mechanisms (Febrianto et al.,
nyms to describe the transfer of chemicals between phases. Even 2009). The most commonly applied kinetic models are first order
though only ‘partitioning’ refers to a process involving any phase, it (or Lagergren equation) and second order models, which assume
1248 P.S. Tourinho et al. / Environmental Pollution 252 (2019) 1246e1256

that the sorbate interacts with one and two types of adsorption antibiotics (Li et al., 2018) and 17b-Estradiol (Liu et al., 2019).
sites (i.e., one-site or two-site occupancy adsorption), respectively Similarly, lower sorption of non-polar organic contaminants to PA
(Rudzinski & Plazinski, 2006). It is also possible to add the was observed in comparison to PE, PVC and PS (Hüffer & Hofmann,
desorption rate (K-1) in the first-order equation, as in Turner & 2016), while lower sorption of phenanthrene to nylon than to PE
Holmes (2015) and Müller et al. (2018). was attributed to hydrophilic functional groups in nylon (Wang
Beside the first and second order kinetics equations, which are et al., 2018).
controlled by the reactions occurring on the surface, the intra- Electrostatic interactions, on the other hand, are caused by the
particle diffusion equation corresponds to a diffusion-controlled attraction of oppositely charged molecules or repulsion of similarly
process (Simonin, 2016). This model has also been used in kinetic charged molecules. In general, MP surfaces can become negatively
studies on MPs. It assumes that sorption to the external surface and charged due to the pH of point of zero charge (pHpzc) being lower
diffusion to interior pores occur in a multiple step process than most environmental pHs (Li et al., 2018; Xu et al., 2018b;
(Markandeya & Kisku, 2015). Also, for spherical pellets, the diffu- Zhang et al., 2018a). As a result, the negative net charges on the MP
sion model based on Fick's second law can be applied surface (such as PE, PP, PS and PVC) are likely to attract positively
(Karapanagioti et al., 2010; Fries & Zarfl, 2012), which considers the charged species (Guo et al., 2018; Wang et al., 2015; Xu et al., 2018a;
radius of the pellet. Razanajatovo et al., 2018). For chemicals existing mainly in the
The interpretation of the results is crucial in sorption studies. So anionic form, however, the repulsion by the MP surface is likely to
firstly, the assumptions of each model should not be ignored. For reduce the sorption (Xu et al., 2018a; Razanajatovo et al., 2018; Wu
example, using the isotherm equations mentioned in the Sup- et al., 2019). Therefore, whether attraction or electrostatic repulsion
porting Information, equilibrium must be reached. For non- occur depends on media pH, pHpzc of the polymer and the acid
equilibrium conditions, the apparent distribution coefficient (Kda) dissociation constant (pKa) of the chemical contaminant
should be used (Grathwohl, 1998). Secondly, to decide the best (Razanajatovo et al., 2018).
fitting model, many studies compared R2 values of linearized
Freundlich and Langmuir equations (Li et al., 2018; Liu et al., 2018; 3.2. Other mechanisms
Wang & Wang, 2018b; Zhan et al., 2016; Wu et al., 2019). Since
these equations have different number of parameters, such com- Hydrogen bonds are specific weak electrostatic interactions,
parison however, is not appropriate. One option is to conduct the involving hydrogen ion Hþ, and can affect the sorption of polymers
extra sum of squares F-test, if models are nested (i.e., one model when proton donor and proton acceptor groups are involved. Li
containing all the parameters in the other model) (Motulsky & et al. (2018) found that polyamide (PA) had a greater sorption ca-
Ransnas, 1987). This is the case for the first order and reversible pacity for a group of antibiotics than did PVC, PE, PS and PP. This
first order models. For non-nested models, the Akaike's Informa- was attributed to the hydrogen bond caused by the proton donor
tion Criterion (AIC) can be used (Motulsky & Christopoulos, 2004). characteristic of the amide group in PA.
For instance, Hüffer & Hofmann (2016) applied AIC and root mean Other interactions also promote the sorption of chemicals onto
square error (RMSE) when comparing isotherm models of organic MPs, including van der Waals and pi-pi interactions. van der Waals
compounds to different MP materials. When comparing the line- forces are weak interactions occurring between molecules not
arized versions of kinetics equations, comparisons should be made involving covalent or ionic bonding, while pi-pi interactions are
with original scales and not transformed scales (i.e., linear version attraction forces between aromatic molecules. Thus, aliphatic
of kinetic equations) (Simonin, 2016). As pointed out by Tran et al. polymers, such as PE and PVC, undergo van der Waals interactions,
(2017), the linear version of the kinetic equations will also produce while aromatic polymers, such as PS, can undergo pi-pi interactions
higher R2 values in comparison to the original, nonlinear equations. (Hüffer & Hofmann, 2016; Müller et al., 2018; Hüffer et al., 2018). As
This can mislead the results, if R2 of the linear version is used and a pi-pi interactions are stronger, the Kf value was one order of
lower R2 of the original equations is ignored. The same can be magnitude higher for the sorption of aromatic chemicals to PS than
applied to isotherms. Wang & Wang (2018a) observed a high R2 for to PE, PA and PVC (Hüffer & Hofmann, 2016).
the linearized Freundlich equation (R2 ¼ 0.96), even though the
data did not yield a good fit to the Freundlich model. 4. Influence factors on chemical contaminant sorption to
MPs
3. Mechanisms of the sorption of chemicals to microplastics
4.1. MP and chemical contaminant characteristics
3.1. Hydrophobic and electrostatic forces
Several key factors have been found to affect the sorption of
The sorption process is intrinsically related to the physio- chemicals to MPs, including the characteristics of both MPs and
chemical properties of both the sorbate and the sorbent. There- sorbates as well as the properties of the medium. For MPs, the type
fore, the mechanism depends on the interactions between sorbate of material determines the interactions that occur on the MP sur-
and sorbent, which can be dominated by a specific interaction or face (as discussed above), and sorption capacity can vary by several
even be a contribution of different interactions. orders of magnitude among materials (Teuten et al., 2007;
Hydrophobic and electrostatic interactions are the predominant Brennecke et al., 2016; Velzeboer et al., 2014; Hüffer & Hofmann,
mechanisms for the sorption of many chemical contaminants 2016). However, the type of MP material should not be the only
(Mato et al., 2001; Xu et al., 2018b; Wang et al., 2015; Guo et al., characteristic to be taken into account, as other characteristics have
2018; Llorca et al., 2018; Wu et al., 2019). Hydrophobic in- been found to interfere with the sorption process.
teractions relate to the attraction of non-polar (or slightly polar) Among the most relevant characteristics studied are MP size and
molecules to the non-polar MP surface, and are considered to be shape. It should be highlighted, however, that size and shape may
one of the main mechanisms governing the sorption of hydro- affect adsorption, but are less important in the absorption process,
phobic organic chemicals to MPs (Wang et al., 2015; Du et al., 2014; as absorption does not depend on the availability of sorption sites
Mato et al., 2001; Hüffer & Hofmann, 2016; Liu et al., 2018). More on the surface. In the adsorption process, as a general rule, particles
hydrophilic MPs, such as polyamides (PA), however, seem to have presenting a higher area-to-volume ratio are expected to have a
higher sorption affinity for hydrophilic organic compounds, such as higher adsorption capacity, such as the smaller sized particles (Liu
 P.S. Tourinho et al. / Environmental Pollution 252 (2019) 1246e1256 1249

et al., 2018; Velzeboer et al., 2014; Zhan et al., 2016; Wang et al., isotherm: glassy polymers present non-linear isotherms with
2018) and particles with irregular shapes (Brennecke et al., 2016). higher competition for the sorption sites, while rubbery polymers
For instance, the equilibrium concentration (Qe) of PCBs increased show linear sorption isotherms with lower competition (Bakir et al.,
from ~60 to 210 mg/g with decreasing PP sheet size from 5 to 2012; Endo & Koelmans, 2016).
0.18 mm (Zhan et al., 2016). The larger Brunauere-Emmette-Teller However, as mentioned above for MP size and shape, crystal-
(BET) surface area of high density polyethylene (HDPE) (6.9 m2/g) linity alone may not always explain the differences in sorption
also resulted in a higher sorption capacity for pyrene compared among MPs. The Kd of FOSA, for instance, was not correlated to
with PS (2.3 m2/g) and PVC (1.8 m2/g) (Wang & Wang, 2018a). crystallinity of PE, PS and PVC, and other polymer characteristics
Llorca et al. (2018) concluded that MP size affected the sorption were found to be more important (Wang et al., 2015). Also Li et al.
process. They used PS and PE MPs with particle sizes of 10 and (2018) found that the degree of crystallinity of five different poly-
3e16 mm, respectively. The overlap of particle sizes however, makes mers (e.g., PE, PP, PA, PS and PVC) failed to explain their sorption
it difficult to believe that any difference in particle size could be capacity for antibiotics.
responsible for the difference in sorption. The characteristics of the sorbate are also equally important in
Nevertheless, MP area effect can be overruled by other charac- defining its sorption to MPs, affecting both the equilibrium time
teristics or if absorption is involved, making its influence negligible (Zhan et al., 2016) and sorption capacity (Zhan et al., 2016;
(Hüffer & Hofmann, 2016; Xu et al., 2018b). Xu et al. (2018b) found a Velzeboer et al., 2014). For organic chemicals, hydrophobicity and
higher sorption capacity of tetracycline for PS than PE, even though molecular weight may help explaining the sorption. Due to the
PE had a higher surface area (0.23 m2/g) and smaller size (150 mm) hydrophobic nature of the MP surface, sorption coefficients for
compared with PS (0.05 m2/g, <280 mm). This result was attributed organic chemicals may be correlated to their octanol-water parti-
to the pi-pi interactions between tetracycline and PS. Similarly, tion coefficient (Kow) (Llorca et al., 2018; Wu et al., 2016;
particle size and surface area could not explain the differences in Beckingham & Ghosh, 2017; Li et al., 2018; Zuo et al., 2019). When
sorption of organic chemicals to PA, PE, PS, and PVC MPs due to the diffusion is the rate-limiting process, the molecular weight how-
greater influence of hydrophobic interactions (Hüffer & Hofmann, ever, becomes more important than Kow as diffusion is hampered
2016). Moreover, the size of pores in the MPs will be crucial, as by the increase of molecular size (Fries & Zarfl, 2012). Similarly, for
small pores enable the interaction of the sorbate with the sorbent hydrophilic chemicals, molecular size (i.e., carbon-chain length)
surface, leading to the formation of monolayer adsorption, while can be more important than hydrophobic interactions (Llorca et al.,
larger pores allow mono- and multilayer formation (Da˛ browski, 2018). When evaluating sorption of 19 polar and non-polar chem-
2001). Li et al. (2018) found that PA had a greater sorption capac- icals on PS and PE MPs using a pH-dependent partitioning coeffi-
ity for antibiotics than PVC, PE, PS and PP, which was partially cient, Seidensticker et al. (2018) observed that overall neutral
attributed to surface pores observed by SEM images (together with species had a stronger sorption in comparison to charged species.
the formation of hydrogen bonds). Nevertheless, thye authors However, some charged compounds can also have strong hydro-
should be cautious when speculating on the influence of pore size. phobic interactions with MPs, such as nonylphenol and diazinon.
Wang et al. (2015) concluded that benzene rings of the PS structure In the case of metals, chemical speciation can be a good
decreased the free volume between atoms of polymer chains by approach for predicting their sorption to MPs. Sorption of metals
steric effects, and no sorption of perfluorooctanesulfonate (PFOS) can be driven by the formation of free cation species and organo-
could be detected. This explanation is, however, contradicted by the metallic complexes in the medium. Free cations are likely to react
fact that perfluorooctanesulfonamide (FOSA), which has the same with charged regions of negative MP surfaces which can be created
chain length and similar molecular weight, did sorb to PS MPs, and by the adsorption of organic molecules (Ashton et al., 2010; Holmes
therefore steric hindrance could not explain these results. et al., 2014, 2012) or due to the presence of plastic additives (Ashton
Another major characteristic affecting sorption is the degree of et al., 2010). Organo-metallic complexes, on the other hand, can
crystallinity of the polymers, which is related to the arrangement of interact with the neutral areas of MP surfaces due to hydrophobic
the principal carbon chain. A higher degree of crystallinity indicates interactions (Holmes et al., 2012).
that the polymeric chain is more ordered, while more disordered
chains result in a greater proportion of amorphous regions. Due to 4.2. Medium characteristics
the size and complexity, the polymer chains are often semi-
crystalline, interposing crystalline and amorphous regions. Medium proprieties may also influence sorption by altering MP
In the crystalline region, a high energy is necessary for surface charge and the speciation of chemicals. This is especially
absorbing chemicals, while in amorphous regions the atoms can true when electrostatic interactions are involved, as pH, ionic
move more freely favoring chemical absorption (Callister, 2001). strength and salinity can considerably affect the electrostatic in-
The amorphous region will present different states depending on teractions, or when surface processes are predominant. For
the temperature. This is known as glass transition temperature (Tg). instance, NaCl and CaCl2 levels did not affect the hydrophobic
At environmental temperatures below Tg, the amorphous region sorption of FOSA to PE, but it did affect the sorption of PFOS, indi-
will be in the rubbery state, and above Tg in the glass state. This is cating a predominance of electrostatic interactions in the latter case
important because in the rubbery state the carbon chain can move, and therefore a greater influence of the ionic chemical composition
while in the glassy state movement is restricted (Endo & Koelmans, of the media (Wang et al., 2015).
2016). Therefore, the higher sorption of chemicals is observed in The effect of pH is rather complex, and a non-linear relationship
rubbery polymers (Wu et al., 2016; Guo et al., 2012; Rochman et al., with sorption is commonly observed. The sorption of tylosin to PVC
2013b). Pyrene sorption was higher to PE than to PS and PVC, which and PS increased with increasing pH up to pH 7.1, due to the elec-
was related to surface area, but also because PE is a semi-crystalline trostatic interactions of the positively charged tylosin with the
polymer, while PS and PVC are glassy polymers with large crys- negative surface charge on the polymers (Guo et al., 2018). For
talline regions (Wang & Wang, 2018a). In accordance with Bakir pH > 7.1, it was expected that sorption would keep increasing as the
et al. (2012), Seidensticker et al. (2018) and Zuo et al. (2019), the polymers become more negatively charged, however, sorption
main sorption mechanism for rubbery polymers is partitioning, decreased. The authors believe that electrostatic forces decreased
while for glassy polymers both partitioning and pore-filling are at higher pH due to a decrease of the cation species of tylosin and
involved. These characteristics can be observed from the sorption the subsequent prevalence of hydrophobic forces. The sorption of
1250 P.S. Tourinho et al. / Environmental Pollution 252 (2019) 1246e1256

tetracycline to PE, PP and PS peaked at pH 6 and was dominated by As mentioned above, organic matter (OM) can react with metals
hydrophobic forces, however, at higher or lower pH values, sorption and therefore play an important role in the sorption of metals and
was rather dominated by electrostatic interactions (Xu et al., metallic species to MPs. Generally, neutral organo-metallic com-
2018b). Indeed, pH effect is dependent on the chemical specia- plexes are formed, with higher hydrophobicity compared to the
tion. Sorption of the antibiotic oxytetracycline to weathered PS free ions, and thus favoring the sorption to hydrophobic MPs
foam peaked at pH 5 due to the greater proportion of its cationic (Holmes et al., 2012). However, it is also possible that OM decreases
form in the solution (Zhang et al., 2018a). In this case, electrostatic the free ion concentration in the medium, resulting in lower
repulsion to the negatively charged MP surface decreased and sorption. This should probably be treated on a case-by-case basis,
sorption was enhanced. It indicates that sorption mechanism was with particular metals and/or OM composition and concentration
regulated by the electrostatic forces, and when it was minimal at giving different outcomes.
pH 5, H-bonding between sorbate and sorbent was the predomi- For organic chemicals, the presence of OM is likely to decrease
nant mechanism. the sorption to MPs, as small and dissolved OM (DOM) can also bind
The relationship between pH and ionic strength and its effects the chemicals and compete with MPs (Xu et al., 2018b; Llorca et al.,
on the sorption of atrazine and 4-(2,4-dichlorophenoxy) butyric 2018; Zuo et al., 2019). In accordance with Wu et al. (2016), the
acid (DB) in soils has been presented in Hüffer et al. (2019). At pH 3, higher affinity of non-polar chemicals to organic matter will result
DB is mostly in nonionic form (pKa of 4.95) and Kd values were not in a decreased sorption to MPs, while less influence of DOM will be
influenced by the presence of Ca2þ. However, at pH 7, the bridging observed for polar chemicals. On the other hand, cationic or zwit-
effects of Ca2þ is more evident, and Kd increased with increasing terionic species can bind to MPs bridged by deprotonated (OH)
CaCl2 levels, since DB is fully deprotonated and PE and soil particles humic acids, as shown for the sorption of oxytetracycline to PS
are negatively charged. Atrazine, on the other hand, has a small foam MPs (Zhang et al., 2018a). In this study, cationic species of
proportion (5%) of cations at pH 3, but is neutral at pH 7. Therefore, oxytetracycline bound to deprotonated sites of humic acid via H-
at pH 3 a decrease in Kd was observed with increasing ionic bonding and cation exchange. The presence of DOM was also found
strength, as Ca2þ competes with the cations for the sorption sites to be less significant when absorption is the dominant process
on PE surface. At pH 7, Kd did not change with increasing Ca2þ (Velzeboer et al., 2014), as it has greater effects on the processes
levels, once atrazine is neutral and no competition occurs (Hüffer occurring on the surface, or when the MPs are nonporous, as no
et al., 2019). pore blockage by OM occurs (Liu et al., 2019).
For metals, the pH influence is metal-dependent (Holmes et al.,
2014; Turner & Holmes, 2015). For metals producing cationic spe- 5. Comparison between field and laboratory studies
cies (e.g. Cd2þ, Co2þ, Ni2þ, Pb2þ), higher sorption capacities were
observed with increasing pH, as there is a decline in the relative Most sorption studies with MPs are conducted in the laboratory
abundance of free ions (Holmes et al., 2014; Turner & Holmes, under controlled conditions. In the field, environmental conditions
2015). For Cr, sorption decreased with increasing pH, suggesting can vary considerably, such as sorbate concentration, temperature
that Cr speciation produced negative forms like HCrO4- and CrO2- 4 and medium composition. In addition, MP degradation, biofilm
(Holmes et al., 2014; Turner & Holmes, 2015). For other metals, such formation, and the presence and possible competition of sorbates
as Cu and Hg, MP sorption showed no clear relation to pH which can also affect the processes and rates of the sorption of chemicals
was attributed to the low free ion concentration and the sorption of to MPs. Interestingly, several studies have been successful in fitting
organic complexes with neutral charge (Holmes et al., 2014). sorption isotherms and kinetics equations to samples collected
When comparing fresh and seawater, sorption of perfluoroalkyl from the field (Rochman et al., 2013a, 2014; Ashton et al., 2010;
substances to PE, PS and polystyrene carboxylate (PS-COOH) Wang et al., 2018). This is an indication that, even though not all
decreased with increasing pH and found to be lower in seawater assumptions are fulfilled, the current models are able to predict the
(Llorca et al., 2018). Even though the presence of bivalent cations sorption of chemicals to MPs also under field conditions.
could result in a bridging effect (e.g., negatively charged MP and One main difference between lab and field experiments is the
sorbate bridged by Ca2þ and Mg2þ), the pH effect was predominant equilibration time (Rochman et al., 2014; Zhan et al., 2016; Holmes
and generally sorption to MPs decreased in seawater in comparison et al., 2012). Equilibrium is reached much faster under lab condi-
to freshwater. The mechanisms for decreasing sorption with tions, and for the same sorbate equilibrium can be reached within
increasing the salinity include the competition between ions for hours or days in the lab, while it takes several months in the
sorption sites (Liu et al., 2018; Zhang et al., 2018a) and electrostatic environment (Zhan et al., 2016; Rochman et al., 2014). Possible
forces (Li et al., 2018). The latter can be caused by the production of explanations include the lower sorbate concentrations in the
negative species of a sorbate with increasing salinity, which causes environment (Rochman et al., 2014) and the constant agitation
electrostatic repulsion to the negative MP surface (Li et al., 2018). usually applied in lab experiments (Zhan et al., 2016).
Nevertheless, salinity may also increase sorption depending on the Once in the environment, the aging or weathering of MPs can
chemical contaminant and even MP properties. Besides the lead to several modifications of the MP surface. For example, MPs
bridging effect mentioned above, the salting out effect can increase can be covered by fouling material which is composed of organic
sorption to MPs by decreasing the solubility of the chemical matter and biological material (i.e., biofilm). Fouling material can
contaminant (Wu et al., 2016; Liu et al., 2019). change the density of MPs (Bakir, 2014b) or even act as an addi-
Bakir et al. (2014b) and Zuo et al. (2019) found conflicting results tional sorbent (Endo et al., 2005).
when studying pH effects on phenanthrene sorption to MPs with Aged and weathered MPs undergo degradation, including
different degree of crystallinity. Zuo et al. (2019) found that phen- photo-degradation, biodegradation, thermo-degradation and hy-
anthrene sorption was more affected by salinity when the MPs drolysis (Andrady, 2011). Aging and weathering can result in a
were in the rubbery state (PE) than in the glass state (PS), while higher sorption capacity by increasing surface area (Mato et al.,
Bakir et al. (2014b) observed no effect of pH on phenanthrene 2001; Zhang et al., 2018a) and pore area of the aged MPs (Zhang
sorption to PE and PVC (glassy). Taking into consideration the et al., 2018a). Photo-oxidation, the predominant degradation pro-
discussion in the previous section, pH would be expected to have a cess of polymers (Feldman, 2002), results in the formation of
low influence on the sorption to MPs in a rubbery state, as ab- carbonyl groups, which increase the polarity of the surface.
sorption is the main mechanism. Therefore, photo-oxidation can increase the sorption of polar
 P.S. Tourinho et al. / Environmental Pollution 252 (2019) 1246e1256 1251

chemicals (Holmes et al., 2012), while decreasing the sorption of Qt ¼ CwVw þ CwMsKd þ CwMdocKdoc þ CwMbKbio þ CwMplKpl
non-polar chemicals (Hüffer et al., 2018). However, no clear relation
was observed between carbonyl index and the sorption of PCBs where Cw is the concentration in porewater (mg/L) and Vw the
(Endo et al., 2005), aromatic hydrocarbons (Müller et al., 2018; volume of porewater (L), Ms, Mdoc, Mb and Mpl are the masses, in kg,
Hüffer et al., 2018) and ethers (Müller et al., 2018) to MPs. Aging of soil, dissolved organic carbon, biota (in terms of lipid) and
seems to have little influence when absorption is involved, as microplastics, respectively. Kd, Kdoc, Kbio and Kpl are the partitioning
changes in the surface are not likely to affect absorption (Müller coefficients compartment-porewater for soil, DOC, biota, and
et al., 2018). Hüffer et al. (2018) found a decrease in sorption to microplastics in L/kg. Kbio in fact is the bioconcentration factor
UV-aged PS for polar and non-polar organic chemicals, because the (BCF) expressed on a lipid basis, so given as L/kg lipid.
oxidation of the aged surface of PS powder favored the reaction The mass of a chemical in compartment i can be calculated by
with water by hydrogen bonds and the formation of clusters of dividing the amount in that compartment i (MiKi) by the total
water molecules, together with a non-significant increase in sur- amount, cancelling out Cw. To get the total amount of the chemical
face area. Still, non-polar chemicals had higher distribution co- in microplastics, the equation can be rewritten to read:
efficients than had polar ones, indicating the importance of
hydrophobic interactions. Qtpl ¼ MplKpl / (Vw þ MsKd þ MdocKdoc þ MbKbio þ MplKpl)
Beside the aging of MPs, the co-existence of chemical contam-
inants in the environment may also affect sorption if the compe- The following assumptions were made: (1) the air compartment
tition for sorption sites occurs. Even though many studies tested a was not included; (2) the microplastic compartment was consid-
mixture of chemicals (Turner & Holmes, 2015; Velzeboer et al., ered to consist of only one material (e.g., polyethylene, polyvinyl
2014; Fries & Zarfl, 2012; Beckingham & Ghosh, 2017), to our chloride or polypropylene); (3) partitioning processes were
knowledge only the work by Bakir et al. (2012) has evaluated considered to be linear in all cases and at equilibrium; (4) Kd values
sorption in single and combined exposures of two chemicals (DDT for sediment were chosen due to the lack of data for soil and in
and phenanthrene). The sorption of DDT to both PVC and PE order to use Kd and Kpl values from the same study.
powders (200e250 mm) was higher and independent of phenan- The parameters used in the model can be found in Tables SIe2.
threne presence, while the competition to binding sites limited The mass of microplastics (Mpl) was defined as the microplastic
phenanthrene sorption to PVC but not to PE (Bakir et al., 2012). amount entering agricultural lands from biosolids. According to Ng
Therefore, the competition between sorbates in the field can also et al. (2018), in Europe a lifetime input between 2.3 and 15.8 ton/ha
result in lower sorption capacity in comparison to lab studies, of microplastics end up in the top 100 mm layer of agricultural soils
which it is likely to be dependent on sorbate and MP properties. from biosolids. We used these values of Mpl for best and worst case
scenarios, respectively.
6. Partitioning of chemicals in soil in the presence of MPs A single biosolid application in Europe can give a dose of 0.63
ton MP/ha/y. Considering an area of 1 ha (or 10,000 m2) and
A large number of studies have investigated the presence and 100 mm topsoil, this dose ends up in a soil volume of 1000 m3. With
effects of microplastics in the aquatic compartment, especially in an average soil density of 1400 kg/m3, this corresponds with a mass
the marine environment. However, sediment and soil are also of soil (Ms) of 1.4  106 kg. The volume of porewater (Vw) was
important sinks for MPs. In sediments, few studies have been calculated as 25% of soil dry weight, corresponding to 350,000 L. In
conducted to assess the quantities and interactions of MPs by using this volume of porewater, with an average dissolved organic carbon
passive samplers (Velzeboer et al., 2014), by performing MP filtra- level of 33 mg/L (De Troyer et al., 2014), the total mass of DOC
tion from sediment and subsequent analysis (Teuten et al., 2007), or (Mdoc) is 11.55 kg. For the biota compartment, the mass was
by mass balance modeling (Kleinteich et al., 2018). To our knowl- expressed as the lipid concentration in soil, assuming that living
edge, no studies on the sorption of chemicals to MPs have been organisms make up 10% of the soil organic matter and that their
performed yet in soil. lipid content is 1% of their body mass (Jager, 1998).
Nevertheless, increasing awareness of soils as a final destination For PCBs, the partitioning coefficients to sediment and micro-
for microplastics is observed. The amount of plastic waste retained plastic were taken from Velzeboer et al. (2014). To verify the dis-
in the continent is estimated to be 4 to 23 times higher than the tribution of different congeners, the PCBs with the highest and
amount released to the oceans (Horton et al., 2017). One important lowest microplastic-water coefficients (Kpl) from this study were
route of MPs (and many other contaminants) to soils is the appli- used: PCB 169 and PCB 44 with a log Kpl of 7.31 and 4.68, respec-
cation of biosolids. It has been estimated that up to 430,000 tons of tively. The Kdoc was estimated from the equation logKdoc ¼ 0.72
microplastics can end up in agricultural lands in Europe, through logKow þ 0.87 (from Karickhoff et al. (1979) in Evans (1988)), and
the application of biosolids (Nizzetto et al., 2016). Thus, the PCB uptake in earthworms was estimated using the equation pre-
assessment of MP interactions with other chemicals in biosolids sented in Jager (1998): BCF ¼ 0.93 Kow - 3.01.
and soils and its consequences for chemical bioavailability in soil For phenanthrene, the Kpl for polyethylene (PE), polyvinyl
are urgently needed. chloride (PVC) and polypropylene (PP) were taken from Teuten
With the increasing input of microplastics in soils, it is impor- et al. (2007), with values of 38100, 1650 and 2190 L/kg, respec-
tant to consider the possibility of microplastics to bind chemicals tively. The Kd of 135 L/kg for phenanthrene (Phe) in sediment was
compared to other compartments of the soil. Previously, a mass taken from the same study. The log Kdoc for Phe was 4.70 L/kg (Mott,
balance model has been used to assess the importance of MPs in the 2002), log BCF in earthworms was 3.9 L/kg (Jager et al., 2000).
distribution of hydrophobic organic chemicals between compart- Fig. 1 shows the distribution of PCBs and Phe in the different
ments in the marine environment (Koelmans et al., 2016) and in compartments. The major amount of the chemicals was found to be
freshwater sediments (Kleinteich et al., 2018). Here, we use a mass bound to the soil compartment. For PCBs, microplastics are the
balance model for estimating the partitioning of PCBs and phen- second compartment with the highest proportions in both best and
anthrene (Phe) in soil in the presence of microplastics. Using worst case scenarios, with 2% of the PCBs being sorbed to micro-
porewater, soil, dissolved organic carbon, biota and plastic as the plastics in the latter one. For Phe, the distribution varied greatly
environmental compartments, the distribution of the total amount among the different scenarios, and was mainly dependent on MP
(in mg) of a chemical in soil (Qt) can be described as: composition. In the worst case scenario, up to 23% of Phe was
1252 P.S. Tourinho et al. / Environmental Pollution 252 (2019) 1246e1256

Fig. 1. Best (left) and worst (right) case scenarios for the distribution of PCBs and phenanthrene (Phe) in the compartments soil, dissolved fractions (pore water and dissolved
organic carbon), biota and microplastics. For PCBs, the partitioning coefficient for polyethylene was used, while for phenanthrene partitioning coefficients for polyethylene (Phe-PE),
polyvinyl chloride (Phe-PVC) and polypropylene (Phe-PP) were used.

bound to PE microplastics, which was caused by the high Kpl for PE exposure of soil organisms should be considered.
(38100 L/kg) in comparison to a low Kd for soil (135 L/kg). Also in
this scenario, the proportion of Phe bound to PVC and PP was small 7. Implications for toxicity and bioaccumulation
at 1.3 and 1.7%, respectively. In the best case scenario, the amount of
Phe bound to the microplastic compartment decreased to 4% for PE 7.1. MP effects on chemical contaminant toxicity
and to ~0.2% for PVC and PP.
The amount of chemical found in the other compartments, The sorption of chemicals to MPs may become a threat to biota
biota, water and DOM, showed little difference between the when ingestion occurs. Animals collected from aquatic environ-
different scenarios or types of microplastic. For both PCBs, negli- ments found to ingest MPs include copepods (Desforges et al.,
gible amounts were detected in these compartments in all cases, 2015), polychaetes (Gusma ~o et al., 2016), and even mussel (van
while for Phe up to 0.2% were observed in water and DOM. The Cauwenberghe and Janssen, 2014) and fish species (Rochman
proportion of Phe in the biota compartment was more significant, et al., 2015) used for human consumption. In soils, it has been
ranging from 4.2 to 5.5%. shown that earthworms (Huerta Lwanga et al., 2016; Rodriguez-
We are aware that different results may be obtained in real soils. Seijo et al., 2017) and mealworms (Wu et al., 2018) can ingested
For example, assuming that all plastics will constitute of PE leads to MPs. Therefore, it is important to determine the role of MPs in the
an overestimation of the partitioning of Phe to the MP compart- toxicity of chemical contaminants. In Tables SI-3, SI-4 and SI-5, an
ment, since PE presented much higher Kd values in comparison to overview is given of toxicity studies conducted in marine water,
PP and PVC (Teuten et al., 2007). Moreover, a linear sorption may freshwater and sediment/soil, respectively.
overestimate the partitioning to solid phases, as it considers that A good approach is to test both the single and combined effects
absorption is the dominant process. However, if the sorption pro- and compare the outcomes. For instance, the EC50 for the immo-
cess is non-linear, it can be restricted to the availability of the bilization of Daphnia magna of bisphenol in the presence of PA
sorption sites on the microplastic surface. (5.5 mg/L) did not significantly differ from bisphenol alone (6.5 mg/
When modeling the mass balance of PCB 169 in the ocean, L) (Rehse et al., 2018). Therefore, PA was a negligible source of
Koelmans et al. (2016) found that only 0.0002% is likely to parti- bisphenol. Also, no significant difference was found between the
tioning to microplastics, while the majority (98%) is likely to be in EC50s for D. magna immobility of phenanthrene alone (0.47 mg/L)
the water compartment. As pointed out by these authors, the and in the presence of irregular PE MPs (0.14 mg/L) (Frydkjær et al.,
product of MiKi determines the importance of the compartment i. 2017). An increase in the EC50 for cefalexin effects on Pomato-
The mass of water in the ocean was 13 orders of magnitude higher schistus microps predatory performance was observed upon com-
than microplastic mass (Koelmans et al., 2016). Thus, the propor- bined exposure with PE spheres (5.2 mg/L) compared with single
tion bound to microplastics was much lower, even though a higher exposure (3.8 mg/L), but the overlap of 95% confidence intervals
partitioning coefficient Kpl was used. indicated a lack of significance (Fonte et al., 2016). Similarly, the
The mass of microplastics used in the present study was only 3 EC10, EC20 and EC50 of copper for growth inhibition in the algae
to 4 orders of magnitude lower than the mass of soil. This may Tetraselmis chuii did not differ from the corresponding ECx when
explain the higher fraction of chemical binding to MPs in soil in exposed with PE microspheres (Davarpanah & Guilhermino, 2015).
comparison to the aquatic compartment (Gouin et al., 2011; And the presence of PS did not affect the toxicity of the pesticides
Koelmans et al., 2016). Here, the MPs accounted for 0.1% of the total dimethoate and deltamethrin, regarding mortality and immobili-
amount of soil in the worst case scenario, which is in the range zation of D. magna (Horton et al., 2018). Altogether, these results
(0.03e6%) of microplastics found in an industrial area in Australia indicate that PA, PS and PE MPs did not affect the toxicity of the
(Fuller & Gautam, 2016). Our results are in agreement with mentioned chemicals to aquatic organisms.
Kleinteich et al. (2018), who also used a mass balance model to For other chemicals, MP presence may decrease contaminant
assess the distribution of phenanthrene and anthracene in fresh- toxicity. Due to the strong sorption of glyphosate to PS-NH2
water sediment in the presence of MPs. They found that more than nanospheres, an antagonistic effect on growth of the algae Micro-
80% of the chemicals were in sediment, with around 15% bound to cystis aeruginosa was observed by Zhang et al. (2018b). Phenan-
MPs and only 1% partitioned to the water phase. threne and 17a-ethinylestradiol sorption to PVC decreased their
Although Kpl probably was overestimated (as commented bioavailability to zebrafish as well, as indicated by gene expression
above), it is suggested that larger quantities of chemicals may be (Sleight et al., 2017). On the other hand, an increase in the toxicity of
bound to microplastics in the terrestrial compartment in compar- chemical contaminants when exposed with MPs can occur,
ison to marine environments (Koelmans et al., 2016; Gouin et al., depending on the endpoint analyzed or treatment method (Brandts
2011). Therefore, microplastics should be looked at as a signifi- et al., 2018; Ranieri et al., 2018; Zhang et al. 2019a; Kim et al., 2017;
cant sink of chemicals in the soil compartment, and its potential Ma et al., 2016; Kleinteich et al., 2018). For this reason, a summary
consequences (i.e., bioaccumulation and biomagnification) for the of the effects of MP on the analyzed endpoints (i.e., increasing,
 P.S. Tourinho et al. / Environmental Pollution 252 (2019) 1246e1256 1253

decreasing or no change in the chemical contaminant toxicity) is (Fig. 2B), the presence of MPs does not affect bioaccumulation,
presented in Tables SI-3, SI-4 and SI-5. being similar to the single exposure to the chemical (Fig. 2A). This
As surface properties of MPs may affect sorption, Kim et al. can be related to: (1) a low affinity between chemical and MPs
(2017) evaluated the effects of PS and PS-COOH on nickel toxicity leading to a low sorption capacity; (2) a low MP uptake by the or-
to D. magna. PS and Ni showed slight antagonistic effects, and PS- ganism; or (3) the fraction accumulated from MPs is negligible
COOH and Ni showed synergistic effects. The higher effect of the compared with uptake from other routes of exposure. In an
functionalized surface was not related to sorption, as similar experiment with zebrafish (Danio rerio), the lack of an effect of MPs
sorption levels were observed for both MPs. It could be related to on Ag bioaccumulation was explained from the insufficient time for
the higher toxicity of PS-COOH itself, as in the single MP experi- Ag sorption to MPs and to the tendency of MPs to float on the
ments the EC50 for PS-COOH (25 mg/L) was significantly lower surface (Khan et al., 2015). So, we can conclude that both low
than that for PS (42 mg/L) (Kim et al., 2017). Due to COOH func- sorption levels and low MP uptake could be the reason for such
tionalization, nano-PS was suspended in water as hydrogen bonds result. Fluoranthene bioaccumulation in mussels (Mytilus spp.) was
are formed with water molecules (Velzeboer et al., 2014), which also not affected by MPs, since proportionally smaller amounts of
could have enhanced the toxicity of PS-COOH to D. magna in fluoranthene from MPs were taken up in comparison with uptake
comparison to PS. from water and food (Paul-Pont et al., 2016). The distribution and
In the sorption studies discussed in the previous sections, MP bioavailability of the chemical, therefore, would be the same with
size may have a great effect on sorption capacity. By comparing or without the MPs.
micro and nanoplastics of different sizes, Ma et al. (2016) found that In the following scenario (Fig. 2C), MPs act as a sink for the
a smaller particle (50 nm) and phenanthrene combination had chemical contaminant and decrease its bioaccumulation. Sorption
additive effects on D. magna and also increased the bio- of the chemical to MPs is relevant, but somehow the sorbed fraction
accumulation of phenanthrene by-products. For bigger particles is less available. This can be due to a strong sorption to MPs as was
(10 mm), no difference with single phenanthrene toxicity was observed for the bioaccumulation of PDBEs in amphipods (Chua
observed. The authors attributed this finding to the lower adsorp- et al., 2014) and bifenthrin in Chironomus tepperi (Ziajahromi
tion of phenanthrene to 10 mm MP, as the sorption experiment et al., 2019) exposed to PE MPs. Similarly, the pre-incubation of
found a higher Freundlich Kf for the 50 nm MP. This is a solid piece the chemical with MPs prior the exposure may decrease bioavail-
of work, as it performed batch sorption experiments to support the ability due to a strong sorption and low desorption during the
toxicity findings. exposure. This has been found for fluoranthene (Magara et al.,
2018) and Ag (Khan et al., 2015) pre-sorbed to PE MPs, decreasing
the bioaccumulation in mussels and zebrafish, respectively. Also, a
7.2. MP effects on chemical contaminant bioaccumulation
low desorption from the MPs in the organism's gut can lead to this
result (Paul-Pont et al., 2016). Therefore, the gut conditions are also
Chemical characteristics can also affect the sorption to MPs and
of major importance regarding desorption of chemicals from MPs,
consequently their uptake and toxicity. PCB congeners were found
and potential chemical accumulation by the organisms. A decrease
to have different bioaccumulation patterns in Arenicola marina
in bioaccumulation, giving final results such as presented in Fig. 2C,
depending on MP concentration, which was related to congener
could also be obtained with the ingestion of “clean” MPs. As shown
hydrophobicity (Besseling et al., 2013). Also, the uptake of higher
in Mohamed Nor & Koelmans (2019), PCBs were transferred from
brominated PBDEs by the marine amphipod Allorchestes compressa
contaminated food to clean PE MPs in a simulated gut condition.
was favored in the presence of MPs (Chua et al., 2014). The authors
In soils, a decrease in hydrophobic organic contaminant (HOC)
indicated the lower solubility and higher Kow of these compounds
bioaccumulation in the presence of PE and PS MPs (1% w/w) was
as crucial factors for determining their sorption to MPs. This result
observed in the earthworm Eisenia fetida (Wang et al., 2019). This
is in agreement with the findings from sorption experiments,
result was attributed to the decrease in free HOC concentration in
which pointed at factors such as Kow-related hydrophobic forces.
porewater due to the sorption of HOC to the MPs. However, no
However, MPs have been found to not affect Paul-Pont et al. (2016);
effect of MPs on HOC bioaccumulation was found in two situations.
Devriese et al. (2017); Khan et al. (2015) or even decrease (Khan
The first was found in earthworms exposed to low MP concentra-
et al., 2015; Sleight et al., 2017; Chua et al., 2014; Magara et al.,
tion (0.1% w/w), which showed no difference from controls (i.e.,
2018) the bioavailability of chemicals.
worms exposed only to HOC in soil). Also, no effects of MPs (from
In Fig. 2, possible scenarios for the effects of MPs on the uptake/
0.1 to 10% w/w) was observed in the bioaccumulation of phenan-
bioaccumulation of chemicals are presented. In the first scenario
threne. Phenanthrene was the least hydrophobic compound, with
lowest Koc and Kpl, and also can be rapidly transformed by the
earthworms (Wang et al., 2019). These results are in agreement
with the findings from the previous section (Partitioning of
chemicals in soil in the presence of MPs), showing the importance
of MP concentration and partitioning coefficients of the
contaminants.
The final scenario (Fig. 2D) shows the MPs acting as a vector for
bioaccumulation. In this case, high sorption levels combined with
MP uptake and chemical desorption in the gut result in increased
bioaccumulation. A fast desorption rate of organic compounds is
expected under gut conditions (Bakir et al., 2014a; Coffin et al.,
2019; Mohamed Nor & Koelmans et al., 2015). Therefore, this sce-
nario is very likely if higher sorption of the contaminant to MPs
Fig. 2. Three possible scenarios of a chemical contaminant bioaccumulation (number together with high MP ingestion rate occur. By increasing MP
of ) due to microplastic (; MP) ingestion in comparison to a single exposure
(Fig. 2A). The microplastics may not affect the bioaccumulation (Fig. 2B). However, it
concentration from 1 mg/L to 50 mg/L, a higher amount of ven-
can also be a sink of the chemical, decreasing bioaccumulation (Fig. 2C) or act as a lafaxine was found in the liver of the pond fish Misgurnus anguil-
vector and increase the bioaccumulation (Fig. 2D). licaudatus, which may be a consequence of incidental MP uptake by
1254 P.S. Tourinho et al. / Environmental Pollution 252 (2019) 1246e1256

the fish with increasing MP concentration (Qu et al., 2018). remains to be understood. The influence of MP and chemical
It should be emphasized, however, that most studies reviewed properties on sorption has been investigated in more detail, while
here did not observe an increased bioaccumulation of chemicals in the influence of medium characteristics and effects of MP aging
the presence of MPs. This is in agreement with the findings of need to be further addressed.
Koelmans et al. (2016) who concluded that the role of MPs as a Sorption studies are important as they can identify the chem-
route of uptake for organic contaminants by marine organisms is icals with higher affinity to MPs under different environmental
negligible in comparison to other routes, such as the dietary route. conditions. Overall, hydrophobic compounds are attracted by hy-
Moreover, more complex and realistic media can weaken the ef- drophobic forces to the neutral areas on the MP surface, while
fects of MPs on bioaccumulation, as shown by Ziajahromi et al. hydrophilic or charged compounds are attracted to the negative
(2019): In synthetic water, MP presence decreased the toxicity of areas on the MP surface with electrostatic interactions and media
bifenthrin in Chironomus tepperi, while the organic fraction in river characteristics being most important. It should also be kept in mind
water mitigated any influence of MPs. that laboratory studies are likely to result in shorter times to reach
The influence of MPs on chemical uptake and elimination rates equilibrium in comparison to field studies, and that aging and
seems to be important indeed as delayed effects might be observed. biofilm formation on the MP surface can lead to increased sorption.
The combined exposure of pyrene and PE MPs resulted in a delayed Sorption studies were also essential for the mass balance model.
mortality of the fish P. microps (Oliveira et al., 2013). The median The sorption capacities could be used for estimating the distribu-
lethal time (LT50) for pyrene changed from ~30 h in the single tion of chemicals in an environment containing a significant
exposure to ~40 h in the presence of PE spheres (Oliveira et al., quantity of MPs. In contrast to marine environments, where low
2013). At the end of an experiment, the organisms might still quantities of chemicals are partitioned to MPs, much higher
contain MPs inside the gut, and it is possible that further effects amounts were found in soils. Therefore, more studies on MPs in the
may be observed during depuration. Higher histopathological soil compartment should be conducted, aiming to assess chemical
damage and higher fluoranthene concentration in the digestive partitioning and toxicity.
glands was found in the mussel Mytilus spp. when exposed to The toxicity outcomes agree to some extent with the sorption
fluoranthene in the presence of PS MPs in comparison to fluo- data. However, a higher sorption to MPs does not always lead to
ranthene single exposure after 7 days of depuration (Paul-Pont higher toxicity or bioaccumulation of a contaminant. Even though
et al., 2016). Prior to the depuration (i.e., at the end of the experi- MPs may not act as a vector for bioaccumulation, there is some
ment), fluoranthene single was found to be more toxic than its indication that they are likely to affect the kinetics of uptake and
mixture with PS (Paul-Pont et al., 2016). More studies are needed to depuration of chemical contaminants in organisms, as well as the
better understand the possible effects of MPs on the toxicody- mechanisms of toxicity at the molecular and physiological level.
namics of chemical contaminants.
As pointed out by Phuong et al. (2016), MPs with irregular Conflicts of interest
shapes (fragments and fibres) are the most abundant microplastics
in the environment, yet microspheres and beads are the most used The authors declare that they have no conflict of interest.
in toxicity tests on marine organisms. Similarly, most MPs used are
microspheres (see Tables SI-3 to SI-5). It is understandable that Acknowledgments
these particles can be purchased and their spherical shapes facili-
tate the detection in the samples or inside the organisms, however, This work was supported by the European Structural and In-
it has been shown that shape can affect the results of sorption vestment Funds, OP RDE-funded project ‘CHEMFELLS4UCTP’ (No.
studies. Therefore, the use of irregular shapes should be encour- CZ.02.2.69/0.0/0.0/17_050/0008485).
aged in order to obtain a more realistic view on the topic.
Regarding toxicity studies, a full dose-response study should be
Appendix A. Supplementary data
conducted to address the effects of MPs on organisms when
possible (van Gestel & Selonen, 2018). And in the case of testing a
Supplementary data to this article can be found online at
co-exposure of MPs and chemical contaminants, the experiment
https://doi.org/10.1016/j.envpol.2019.06.030.
should be design to allow some kind of comparison between single
and combined toxicities. For example, Zhang et al. (2019a) evalu-
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