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Review of Bioaccumulation, Biomagnification, and Biotransformation of

Engineered Nanomaterials

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Environmental Chemistry Letters
https://doi.org/10.1007/s10311-019-00947-0

REVIEW

Engineered nanomaterials in the environment: bioaccumulation,

biomagnification and biotransformation
Md. Nizam Uddin1 · Fenil Desai1 · Eylem Asmatulu1

Received: 19 October 2019 / Accepted: 5 November 2019

© Springer Nature Switzerland AG 2020

Abstract
Engineered nanomaterial manufacturing and usage have been increasing in commercial products. There were 1814 nanotech-
nological consumer products available in the market in March 2015. Nanomaterials can accumulate, transform and increase
in concentrations in biological systems. Nanomaterials offer many benefits over traditional materials, yet their small size
also increases their toxicity. Bioaccumulation of nanomaterials begins with nanoparticle accumulation in the organism, then
biomagnification follows in the predatory organism. Biotransformation is the last stage, whereby the chemical concentration
of toxins in the organism exceeds that in the environment. Here, we review the interaction of nanomaterials with biological
substances. It has been observed that the effects of nanomaterials begin at the bottom of the food chain and move all the
way through the human body. We have summarized the mechanisms of interaction between engineered nanomaterials and
the environment.

Keywords Bioaccumulation · Biomagnification · Bioconcentration · Nanoparticles · Toxicity · Microorganisms · Silver ·

Gold · Quantum dots · Carbon nanotube · Titanium

Introduction treat diseases in humans, animals, and aquatic organisms.

Engineered nanomaterials have proven their value and
The rapid development and expansion of nanotechnology novel approaches, especially for biomedical applications
industries have ultimately led to the mass production of (Seraz et al. 2017). However, the long-term effect of these
a wide variety of engineered nanomaterials. These novel nanomaterials is still unknown. That leads to inevitably
engineered nanomaterials exhibit extraordinary perfor- increase the possibility of release into the environment
mance in mechanical, electric, electronic, thermal, and and exposure to ecosystems or even humans. Their inten-
optical applications due to their unique properties, which sive commercial application and production raise concerns
traditional or bulk counterpart materials cannot begin to about their ecotoxicological effects. Therefore, engineered
match (Peng et al. 2017; Kumar et al. 2019; Uddin et al. nanomaterials exposure assessment is crucial because the
2018, 2019). The nanomaterials are used in consumer environmental effects of it are very little known. In recent
products, industries, and the remediation of pollutants, years, several studies addressing the fate, toxicity, risk,
and these are the primary sources of their direct distri- and safety assessment of the nanomaterials in the envi-
bution into the environment. The nanomaterials can be ronment and their effect on living organisms have been
released into different environments during their various carried out. Various interactions of engineered nanoma-
life stages, including production, manufacturing, transpor- terials include dissolution, agglomeration, sedimentation,
tation, customer use, waste treatment plant, disposal, and or chemical transformations as well as uptake and transfer
landfilling. One of the main applications of engineered into the food chain (Núñez and de la Rosa-Álvarez 2018).
nanomaterials and nanotechnology is to diagnose and To study the inherent properties of engineered nanomateri-
als and how they influence bioaccumulation, biomagnifi-
* Eylem Asmatulu cation, and biotransformation is a key issue in the current
e.asmatulu@wichita.edu environment. Typically, bioaccumulation is defined as
the increase in the concentration of contaminants or toxic
1
Department of Mechanical Engineering, Wichita State chemicals in aquatic organisms following uptake from the
University, 1845 Fairmount St, Wichita, KS 67260, USA

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Vol.:(0123456789)
 Environmental Chemistry Letters

ambient environmental medium (Wang 2016). Increased for a Sustainable World (http://www.sprin​ger.com/serie​
concentration of these toxic chemical in the food chain is s/11480​).
known as biomagnification. Biotransformation is a bioac-
tivation process which could produce reactive metabolites
that are more toxic. Exposure pathways and bioaccumulation
For aquatic organisms, the different sources of uptake of engineered nanomaterials
are water (waterborne uptake) and/or food particles (food-
borne uptake). However, in ecotoxicological studies, bio- Information about how the engineered nanomaterials can
accumulation and bioavailability are considered jointly. affect nature and how they accumulate in the human body
It would be impossible to study bioaccumulation without and the environment is relatively unknown. Various stake-
considering bioavailability, and vice versa. Thus, both are holders are increasingly interested in the potential toxicity
considered herein along with the use of bioaccumulation and other risks associated with nanomaterials throughout the
in biomonitoring. The rate of engineered nanomaterials different stages of a product’s life cycle (e.g., development,
uptake and adverse effects, especially, rely on the routes production, use, and disposal). The uptake of nanomateri-
of exposure as well as internalization in the cell and organ- als by living organisms may have cumulative toxic effects,
ism (Gupta et al. 2017). As shown in Fig. 1, there are which organisms may counteract by either their storage or
three main types of uptake, based on the exposure route: excretion in a benign form. The engineered nanomaterials
bioconcentration, bioaccumulation, and biomagnification. could affect plant health and the food supply. Furthermore,
From all three, biomagnification is the most dangerous to environmental conditions may also impact toxicity, as was
the environment and human health. demonstrated with marine phytoplankton, the primary pro-
This review aims to provide an overview of the princi- ducers that support ocean food webs and are integral to the
ples and effects of various engineered nanomaterials due global carbon cycle. Persistent hydrophobic chemicals may
to bioaccumulation, magnification, and transformation accumulate in aquatic organisms through different mech-
to mammalian cells and a wide range of organisms from anisms: via the direct uptake from water by gills or skin
single-cell organisms, such as bacteria to more complex (bioconcentration), the uptake of suspended particles (inges-
organisms, including plants, fishes, etc. This article is an tion), and the consumption of contaminated food (biomag-
abridged version of the chapter by Uddin MN., Desai F., nification). Even without detectable acute or chronic effects
and Asmatulu, E. (2019) [Bioaccumulation, Biomagni- in standard ecotoxicity tests, bioaccumulation should be
fication, and Biotransformation of Nanomaterials, In V. regarded as a hazard criterion. The implication of various
Kumar, P. Guleria, S. Ranjan, N. Dasgupta, and E. Licht- nanomaterials with the environment, ecosystem, and human
fouse, Nanotoxicology and Nanoecotoxicology,] that will being is presented here.
be published in the book series Environmental Chemistry
Gold nanoparticles

Gold nanoparticles, due to their consistency and synthe-

sis, firmness, and properties of integrating with molecules
such as peptides and proteins, are especially useful for bio-
medical applications. Lasagna-Reeves et al. (2010) experi-
mented with using gold nanoparticles in drug delivery,
diagnosis, and treatment, and found that it is essential to
characterize the bioaccumulation and toxicity associated
with repeated administration of these molecules. Tissues
were stained with hematoxylin/eosin as indicated in mate-
rials to assess for potential effects of gold nanoparticles
treatment on the organ morphology and cellular damage.
In all organs studied, there was a significant increase in
gold levels after treatment, which was proportional to the
dose administered. However, gold levels in the blood did
not increase in proportion to the dose, indicating that gold
nanoparticles are mostly taken up and accumulated by tis-
Fig. 1  Direct and indirect exposure paths of engineered nanomateri-
sues. However, even assuming that no blood was removed
als in aquatic organisms to predator species from aqueous suspension from the organs, an estimation shows that from the quan-
and diet (prey) (Gupta et al. 2017). ENP engineered nanoparticles tity obtained in tissues, the contribution of blood was less

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Environmental Chemistry Letters

than 6%, 2%, 3%, 1%, and 7.5%, for the values reported in to the organism, and titanium dioxide nanoparticles may
brain, kidney, liver, spleen, and lung, respectively. Con- bioaccumulate through trophic transfer.
sidering the relatively constant levels of gold in the blood
after gold nanoparticles administration at different doses, Silver nanoparticles
the increased accumulation of gold in the brain suggests
non-saturable uptake of gold nanoparticles across the Silver nanoparticles are metal-based and mostly used in
blood–brain barrier. This is important for utilizing these industrial applications. Investigation of the effects of silver
nanoparticles for potential treatment and diagnosis of neu- nanoparticles on caudal fin regeneration in zebrafish (Yeo
rodegenerative disorders. Besides, gold nanoparticles of and Pak 2008) revealed that silver nanoparticles were able
the size 12.5 nm could accumulate in the kidney, liver, to penetrate fish organelles, including the mitochondria and
and spleen. Also, it can pass through a filtration barrier nucleus, in addition to blood vessels. Total silver levels in
because of its small size. In the context of a single trophic intestinal tissues of the zebrafish increased during silver
level, the localization of nanoparticles greatly affects their nanoparticle exposure. Levels of silver nanoparticles were
potential for bioaccumulation (Xing et al. 2016; Kahlon highest in the gills and liver of perch and Japanese medaka
et al. 2018). The pharmacokinetic, bioavailability, bioac- and were primarily adsorbed and accumulated. Coating
cumulation, clearance, and toxicity of nanoparticles are of silver nanoparticles can influence their behavior and
likely dependent on the particle composition, size, and transport at biological interfaces, such as fish gill epithe-
surface characteristics. These properties may be altered to lia; polyvinylpyrrolidone (PVP)-coated silver nanoparticles
reach the most appropriate balance for different applica- primarily passed over the multilayered gill multicellular
tions. One factor regulating the pharmacological proper- epithelium, whereas citrate-coated Ag nanoparticles tended
ties of nanoparticles may be the electrostatic state of the to be absorbed into individual cells (Thio et al. 2012). The
particle (Judy et al. 2012). extent to which the aquatic environment may alter the chemi-
cal properties of silver nanoparticles should also be taken
into consideration when studying the bioaccumulation of
Titanium dioxide nanoparticles nanoparticles.

Titanium dioxide nanoparticles are mainly used in indus- Cerium oxide nanoparticles
trial and household applications, and their use is increas-
ing rapidly. The uptake and accumulation of nanoparticles Cerium oxide nanoparticles have become one of the most
by living organisms may have cumulative toxic effects; popular nanomaterials in the past several years and are
however, organisms may counteract these effects either currently being utilized in various fields as catalysts, cell
by storage or excretion of the nanoparticles in a benign electrolytes, semiconductors, antioxidants, coatings, and
form (Shi et al. 2013). Concentrations of titanium dioxide polishing chemicals (Khan et al. 2011). Cerium oxide
nanoparticles in organisms depend on their toxicokinetics, nanoparticles are more toxic than bulk cerium oxide and
and organisms may be exposed to nanoparticles through may induce cell death, oxidative stress, and DNA damage
multiple pathways. Nanoparticles with a polycationic or (Arnold et al. 2013; Pulido-Reyes et al. 2015; Zhang et al.
anionic surface may bind to mucoproteins because mucus 2016). Zhao et al. (2017) constructed a freshwater ecosystem
can chelate cations. In fish, large materials can enter the and studied the distribution, bioaccumulation, biomagnifica-
tissues via endocytosis across the gut, and diffusion of tion, and impacts of cerium oxide nanoparticles via long-
lipophilic nanoparticles through the cell membrane can- term exposure. Their results demonstrated that cerium was
not be ruled out. The epidermis is protected by mucous; absorbed and accumulated by the tested biota and diluted in
thus, nanoparticles may not easily penetrate the skin of the constructed food web, as manifested by a negative rela-
fish due to a lack of metal transporters in skin cells com- tionship between trophic levels and lipid-normalized cerium
pared to gills (Hartmann et al. 2012; Schütz et al. 2012). concentrations. Cerium oxide nanoparticles induced obvi-
In humans, titanium dioxide nanoparticles collaborate with ous morphological abnormalities in aquatic hydrophytes due
plasma proteins, coagulation variables, and platelets. Fur- to their unique chemical or physical properties, potentially
thermore, anatase-form titanium dioxide nanoparticles can causing an irreversible disturbance in the sustainability of
penetrate red blood cells; this type of cellular uptake likely the aquatic system.
involves processes other than phagocytosis and endocyto-
sis because erythrocytes do not have phagocytic receptors. Carbon nanoparticles
Direct uptake via the skin is a possible route of exposure in
soil organisms. The exposure routes and bioaccumulation Carbon nanomaterials, such as quantum dots, fullerene, car-
patterns of titanium dioxide nanoparticles vary according bon nanotubes, and graphene, have attracted great research

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 Environmental Chemistry Letters

interest in the past decades (Uddin et al. 2014; Bhuyan et al. release occurs and gets collected in water sources, such as
2015, 2016; LeCroy et al. 2016; Yay et al. 2018). Their wastewater treatment plants and aquatic environments. It
unique structures and fantastic properties make carbon nano- has been assessed that 69,200 and 189,200 metric tons of
materials suitable for biomedical applications. In particular, nanoparticles are released every year universally into water
carbon nanomaterials have been found to have great poten- sources and landfills, respectively. As nanomaterials are
tial in theranostics, including bioimaging, diagnosis, drug released into the natural environment, they go through vari-
delivery, gene therapy, photothermal therapy, etc. (Luo et al. ous stages and cooperate with chemical, biological, physical,
2014; Son et al. 2016). The accumulation and toxicity of car- and ecological elements that may inhibit their performance
bon nanoparticles in mice were investigated, where a carbon and transport in ecological networks where the danger starts
nanoparticle suspension injection was trapped in nature in (Gupta et al. 2017). Herein, the biological magnification of
many cases, and no apparent toxicity was observed. Carbon different nanomaterials is described as follows:
nanoparticle suspension injection accumulated dramatically
in the liver and spleen after intravenous injection, but minor Quantum dots
contamination was noticed in the lungs (Xie et al. 2017).
According to Stern et al. (2012), a wide range of metal-
Zinc oxide nanoparticles lic nanoparticles are associated with bacteria. For example,
cerium oxide nanoparticles can be absorbed by Escheri-
Zinc oxide nanoparticles are typical metal oxide nanopar- chia coli or can activate sludge, and CdSe quantum dots
ticles broadly used in a range of products including sun- can get into a cell of Pseudomonas aeruginosa to affect
screens, cosmetics, paint, paper, plastics, ceramics, and the body function. Werlin et al. (2011) studied bare CdSe
building materials because of their high stability, anti-cor- quantum dots that accumulated in specific bacteria called
rosion, and photocatalytic properties (Osmond and McCall Pseudomonas aeruginosa, which were biomagnified in
2010). The toxicity of nano-ZnO (96 h LC50, 4.9 mg L−1) the Tetrahymena thermophila protozoa by consumption.
to zebrafish was much higher than that of titanium diox- The concentration of cadmium in protozoa as a predator is
ide nanoparticles (96 h LC50, 124.5 mg L−1) (Xiong et al. higher than in its bacterial prey. Because protozoa do not
2011). Hao et al. (2013) concluded that nano-ZnO exhibited undergo lysis, they largely consume quantum dots to stay
much higher bioaccumulation and oxidative effects and more available at higher trophic levels. The detected biomagnifica-
severe histopathological changes to the test fish than bulk- tion from bacterial prey is considerably high since they are
ZnO after a 30-day sub-acute exposure. at the center of the food chain.

Silver nanoparticles
Biological magnification of engineered
nanomaterials Toxicity of the bioaccumulation and biomagnification of
silver nanoparticles is another area of study that has been
Biological magnification begins with processes that include examined in the model food chain (Yoo-iam et al. 2014). In
specific substances such as heavy metals and pesticides mix- this study, the toxicity effect of silver nanoparticles ­(Ag+
ing with a body of water (e.g., river, lake, and ocean), mov- and ­Ag0) on Chlorella sp., Chironomus spp., Moina mac-
ing into the food chain as water microorganisms that can be rocopa, and Barbonymus gonionotus was examined. Based
prey for fish, and traveling through the human body. Even- on the test results, toxicity order on all four organisms was
tually, the substances are progressively gathered in tissues ­Ag+ > Ag nanoparticles. They found that the highest ­Ag+
or inner organs as they progress through the food chain, for bioaccumulation factor was 101.84 L g−1 in Chlorella sp,
example, the use of the insecticide dichlorodiphenyltrichlo- and the least bioaccumulation factor of Ag nanoparticles
roethane for insect control and it has a high toxicity level. was 1.89 L g−1 in B. gonionotus, because the food chain
The steadiness of dichlorodiphenyltrichloroethane in nature transfer of Ag nanoparticles happened only from Chlorella
and its bioaccumulation and biomagnification have severely sp. to M. macrocopa, and there was no sign of biomagnifi-
impacted numerous organisms. This insecticide has been cation from food sources to consumers in a basic tropical
associated with the occurrence of cancer, premature birth, food chain (Yoo-iam et al. 2014). The authors’ findings
infertility, and diabetes. It has more broadly been connected indicate that the biomagnification of heavy metals did not
to the populace decay of bird species on the natural way occur at a higher trophic level. For biomagnification to
of life; for example, the peregrine falcon and bald eagle be considered at the trophic level, trace metal concentra-
may be linked to dichlorodiphenyltrichloroethane toxicity tion should appear in at least two trophic levels. A lower
where the eggshell thickness has diminished (Olenick 2013). concentration of heavy metal in the animal body indicates
Besides, nanoproducts go into waste disposal areas where a lower level of heavy metal in the water body/source.

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Environmental Chemistry Letters

Also, animals located in higher trophic levels might be Gold nanoparticles

more competent in removing heavy metals than organisms
located in lower trophic levels. The antioxidant enzyme Most nanomaterial-containing consumer products com-
system in infected animals could also be in charge of the plete their service life and end up in waste streams. Many
end of oxidative stress within the beginning time of the classes of nanomaterials accumulate in the sludge obtained
body’s protective system (Thio et al., 2012; De La Torre- from wastewater treatment and finally in soil resulting in
Roche et al. 2013). land applications as bio-solids. In order to evaluate the
impact of nanoparticles on terrestrial ecosystems, model
organisms Nicotiana tabacum L. cv Xanthi and Manduca
Titanium dioxide nanoparticles sexta (tobacco hornworms) were chosen to examine plant
uptake and the potential trophic movement for 5-, 10-, and
Kubo-Irie et al. (2016) studied biomagnification of 15-nm-diameter gold nanoparticles. The outcome indicated
titanium dioxide nanoparticles in the terrestrial food a trophic movement and biomagnification of gold nanoparti-
chain. The oviposited eggs of the swallowtail butter- cles from a first producer to a first user through mean factors
fly (Atrophaneura alcinous) were hatched on the leaves of 6.2, 11.6, and 9.6 for the 5-, 10-, and 15-nm treatments,
of the Aristolochia debilis, and the rootstock and hairs respectively. This outcome is essential for nanotechnology-
were dipped in a suspension prepared with the ratio of related risks, involving the potential for human exposure
10 μg mL−1 titanium dioxide nanoparticles in a 100 mL (Judy et al. 2011).
bottle. X-ray analytical microscopy was used to confirm
the existence of titanium dioxide nanoparticles in the veins
of the Aristolochia debilis. First instar hatchlings benefited Biotransformation of engineered
from the leaves to shed into second instar hatchlings. Also, nanomaterials
transmission electron microscopy results show that the lit-
tle agglomerates of titanium dioxide nanoparticles under Understanding the biotransformation (biochemical modifica-
150 nm in diameter were distinguished in the vascular tis- tion by living organisms) of nanomaterials and their cyto-
sue of the subjected plant, the midgut, and the excreta of toxicity and potential environmental health issues involving
the hatchlings. As a result of this study, titanium dioxide their applications is inevitable. Knowing the interactions
nanoparticles were transferred from the plant to the lar- of nanomaterials with their environment is essential to
vae and distributed throughout the environment by larval assess their exposure, hazards, and risks. The development
excreta (Kubo-Irie et al. 2016). The higher accumulation and usage of nanomedicines in the medical sector validate
of titanium dioxide nanoparticles affects the ingestion rate the assessment of the fate of nanomaterials in vivo. Some
and causes greater biomagnification. Zhu et al. (2010) con- acute effects of nanomaterials have been described, but their
ducted a toxicity assessment to understand the potential transformation by the biological environment is little inves-
ecotoxicity of nanoscale titanium dioxide (nTiO2) to the tigated and therefore gaining a research interest these days.
aquatic organism Daphnia magna. They performed a com- Nanoparticles can enter the human body through inhalation,
prehensive study by modifying acute (72 h) and chronic ingestion, and dermal penetration from contaminated envi-
(21 days) toxicity tests along with nTiO 2 accumulation ronments and food (Sanchez et al. 2012). The interaction
analysis. As a result, nTiO2 applied minimal toxicity to of nanomaterials with the biological environment, such as
Daphnia within 48-h exposure time and caused high toxic- biological fluids, membranes, cell components, proteins,
ity when the exposure time was longer, such as 72 h. From and DNA, remodels their structure, surface properties,
this perspective, exposure duration might be the contrib- biotransformation, enzymatic attack, toxicity, degradation,
uting factor in NP-mediated toxicity. Furthermore, upon particle distribution, fate, and bio-assimilation throughout
chronic exposure to nTiO 2 for 21 d, Daphnia exhibited the organism (Fig. 2) (Kolosnjaj-Tabi et al. 2016). This, in
critical growth delay as well as mortality, and reproduc- turn, leads to the transport of nanomaterials in physiological
tive defects. Captivatingly, an essential amount of nTiO2 media, cellular internalization, and potential toxicity (Loeve
was observed in Daphnia. Conversely, Daphnia showed et al. 2013). Although nanomaterials have a lengthy tenac-
difficulty in eliminating nTiO 2 from its body with the ity within the body, their transformation or transportation
increased bioconcentration factor values. A high level of through kinetic processes is an ultimately slower processes,
bioaccumulation may interfere with food intake and even- which can evoke chronic inflammatory reactions. Hence,
tually distress the growth and reproduction of individuals the life cycle of nanomaterials within the body from initial
as well as the population, thereby posing risks to aquatic exposure to complete elimination is a critical issue. Some-
ecosystems (Zhu et al. 2010). times reactive, rapidly degradable nanomaterials are desired,
whereas for persistence nanomaterials, remain inactive in the

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 Environmental Chemistry Letters

Fig. 2  Nanoparticle life cycle after administration into veins

organism. However, unexpected biological reactions with intestinal) upon their in vitro digestion (Guarnieri et al.
nanomaterials produce by-products that saturate lysosomal 2018). It is observed that graphene oxide and few-layer gra-
compartments and perturb degradative and autophagic path- phene exhibit typical D and G bands, and few-layer graphene
ways that are essential for cells to degrade proteins (Stern also exhibits D’ and 2D bands. However, physiological
et al. 2012). Herein, the biotransformation of different nano- juices exhibit two bands at 1450 and 2900 cm−1, which are
materials and toxicity of pristine and bio-transformed nano- attributed to the bending and stretching vibrational modes
materials and other health-related issues are discussed. of –CH2 or –CH3, respectively. Apparently, a change in
defects was observed as the graphene oxide/few-layer gra-
Graphene‑related materials phene passes through the simulated digestive tract. Another
study was carried out to investigate in vivo biotransforma-
Through inhalation, skin contact, or ingestion, graphene- tion of graphene oxide in two simulated lung fluids: Gam-
related materials can enter the human body; consequently, ble’s solution and artificial lysosomal fluid (Qi et al. 2018).
many in vitro and in vivo research studies have been car- The results show that graphene oxide significantly alters its
ried out to assess their potential risk to humans (Ema et al. physiochemical properties, morphology, and functionality
2017). Once these materials enter the biological system, in two simulated lung fluids. The sheet-like graphene oxide
their physical–chemical properties may alter depending on was reduced to randomly wrinkled and stacked sheets, in
the biological environment, such as temperature, pH, con- comparison with Gamble’s graphene oxide and artificial
centration, salts, and many other factors. Recent studies have lysosomal fluid–graphene oxide. Also, after biotransfor-
shown that graphene-related materials may be degraded by mation, Gamble’s graphene oxide and artificial lysosomal
oxidase enzymes, such as horseradish peroxidase and human fluid–graphene oxide had increased functionalities compared
myeloperoxidase, both of which usually exist in physiologi- to pristine graphene oxide. The physicochemical proper-
cal fluids (Gebel et al. 2014). One recent study was car- ties of the bio-transformed graphene oxide are depicted in
ried out to investigate the biotransformation, cytotoxicity, Table 1. In addition, graphene oxide sheets are transformed
and inflammatory response of graphene oxide/few-layer by the blood plasma. However, little information is known
graphene in the gastrointestinal tract (salivary, gastric, and about the effect of nanomaterial biotransformation in blood

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Environmental Chemistry Letters

Table 1  Physicochemical properties of pristine and bio-transformed plasma. After 14 days of graphene oxide sheet exposure to
graphene oxide materials (Liu et al. 2018) human blood plasma, the graphene oxide sheets degraded
Graphene oxide Gamble’s Artificial and formed biological corona on them (Wen et al. 2016).
graphene lysosomal Notably, the biotransformation influenced the cytotoxicity
oxide fluid–graphene induced by graphene oxide.
oxide

C (wt%) Magnetic iron oxide nanoparticles

Aromatic rings 24.62 29.04 22.88
Epoxy/hydroxyl 33.38 28.61 26.19 Magnetic iron oxide nanoparticles are favorable inorganic
Carbonyl 6.02 1.92 – nanoparticles for diagnostic and therapeutic applications
Carboxyl 5.69 8.7 25.19 such as magnetic resonance imaging diagnosis. Iron oxide
Total C (wt%) 70.23 68.27 74.98 nanoparticles can reach the liver and the spleen because
Total O (wt%) 29.03 28.27 23.58 of their coating. Also, electron paramagnetic resonance
C/O ratio 2.41 2.43 3.18 discloses the coating-dependent elimination of super-
pH 5.71 6.45 6.51 paramagnetic iron from these organs, which occurs a long
ID/IG 0.61 0.82 0.84 while after injection. Correspondingly, with the desertion
Hydrodynamic 144.3 ± 6.1 345.7 ± 22.9 323.6 ± 15.2 of superparamagnetic iron, magnetic iron oxide nanoparti-
diameter Dh cles dissipated in the liver and spleen, and transformed into
(nm)
nonmagnetic iron (Lartigue et al. 2013). Figure 3 illustrates
Polydispersity 0.27 0.5 0.45
index
the in vivo time-dependent biodistribution and transforma-
tion of magnetic iron oxide nanoparticles. It is expected that

Fig. 3  In vivo biotransformation of magnetic iron oxide nanoparticles in mice using magnetic resonance imaging, ex vivo electron paramagnetic
resonance quantification in organs, and associated transmission electron microscopy observations (Lartigue et al. 2013)

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 Environmental Chemistry Letters

the metabolism that controls iron in the living being can nanotubes by bacteria identified as Trabusiella guamen-
likewise deal with magnetic iron oxide nanoparticles. The sis. The multi-walled carbon nanotubes and bacteria could
morphology and subcellular distribution of magnetic iron interact in order to obtain insight into the biotransformation
oxide nanoparticles have been studied by transmission elec- of their structure. Redox-enzyme activity and cell viabil-
tron microscopy (Fig. 3). After 1 day of injection and later ity testing revealed that multi-walled carbon nanotubes
period, the clusters of magnetic iron oxide nanoparticles are oxidized and bio-transformed through the formation of
within the lysosomes of splenic and hepatic macrophages C=O and –COOH groups on the outer walls of nanotubes.
shortened in the periphery and local degradation of mag- Also, oxygen-containing functional groups on the surface of
netic iron oxide nanoparticles within the lysosomes. Another multi-walled carbon nanotubes increased. The morphologi-
study by Levy et al. (2011) reported the biotransformation of cal study showed that surface roughness and the number of
magnetic iron oxide nanoparticles in vivo over a long period concentric walls of the multi-walled carbon nanotubes were
of time. They used ferromagnetic resonance and inductively also reduced. The biotransformation process is oxidation
coupled plasma to observe magnetic iron oxide nanoparti- and partial catalytic degradation process. The interaction
cles in mice tissue. Results show a reduction in the magneti- between bacteria and multi-walled carbon nanotubes is pre-
zation of the liver or spleen over time after magnetic iron sented in Fig. 4.
oxide nanoparticles are injected. The low-field magnetiza-
tion for field-cooled and zero-field-cooled specimens of liver Silver nanoparticles
and spleen after injection exhibits similar results, revealing
that superparamagnetic nanoparticles transformed to poorly The potential routes of exposure of silver nanoparticles in
magnetic iron species over a three-month time period. humans are inhalation, dermal contact, and oral administra-
tion. In addition, they can gain access to the human body
Carbon nanotubes through coated contact lenses, bone cement, and other
implants, eye drops, nanosilver-coated medical catheters,
Carbon nanotubes are extensively used in biomedical appli- cardiovascular implants, etc. (Ge et al. 2014). These par-
cations such as targeted drug delivery and remediation ticles can enter and gather in different tissues and organs
agents. As a result, public awareness of carbon nanotubes such as the lung, spleen, heart, kidney, ovary, and brain.
in the environment and related issues has gained much Van der Zande et al. (2012) studied the biotransformation of
attention in the research community. Chouhan et al. (2016) silver nanoparticles in vivo. Experimenting with rats, they
investigated the biotransformation of multi-walled carbon found that the amount of free silver ions released in a silver

Fig. 4  Scanning electron

microscopy images: a bacteria;
b, c bacteria and multi-walled
carbon nanotube bundles;
and d bacteria wrapped by
multi-walled carbon nanotubes
(Chouhan et al. 2016)

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Environmental Chemistry Letters

nanoparticles suspension is directly related to the silver con- Conclusion and recommendations
tent in the main organs of the rat. Even after 28 days, the rat
blood treated with silver nanoparticles exhibited approxi- The manufacture and use of engineered nanomaterials
mately 7–10 times lower silver content than in the silver have been increasing in both commercial and consumer
nitrate group. Another study on silver nanoparticle-contain- products. Engineered nanomaterials have one-of-a-kind
ing paint additive reported that silver nanoparticles release physical and chemical properties, which make them attrac-
ions and dissolve, crossing the air–blood barrier (Smulders tive materials for a wide range of applications but also
et al. 2015). These particles can enter the blood circulation contribute to their adverse behavior in biological systems
system and be transformed into an ion or precipitate into including the environment and public health. Understand-
other silver-containing matter, thereby being distributed in ing the nanomaterial’s accumulation and magnification
the organs and parts of animal bodies. The possible biotrans- for each species is still in its infancy. Nanoparticles are
formation of silver nanoparticles includes silver sulfide and potential transfer mechanisms for human health as humans
silver chloride by reactions with sulfur and chloride species, sit at the highest point of the food chain, so they could
respectively. be risky if biomagnification proceeded as far up the food
chain possible. Considering all three stages of nanoparticle
Cerium oxide nanoparticles movement in the food chain (bioaccumulation, biomagni-
fication, and bioconcentration), manufacturers are playing
Cerium oxide nanoparticles have the potential to be used a significant role in balancing the nanomaterial concen-
in a therapeutic strategy for cerium neurodegenerative dis- tration. It is very important to develop safe engineered
eases in humans (Kyosseva et al. 2013). The cerium oxide nanoparticles and nano-enabled products so that they can
nanoparticles retained in the hepatic phagolysosomes and benefit human health (e.g., targeted drug delivery and
release secondary plum while in the biotransformation of the imaging), mitigate climate change (e.g., fuel-saving vehi-
mammalian system. Zhang et al. (2012) studied the biotrans- cles), purify water (e.g., nanosized membrane filters and
formation of cerium oxide nanoparticles in cucumber plants. selective sorbents), produce energy (e.g., carbon capturing
They treated cucumber roots with 2000 mg L−1 cerium and solar cells), and be distributed and stored (e.g., long-
oxide nanoparticles. After 21 days of treatment, C ­ ePO4 life batteries, fuel cells, and catalysts for water splitting).
was observed on the epidermis and intercellular spaces of The characteristic of nanomaterials can be tailored to be
cucumber roots. It was also observed that in the biotrans- safer if manufacturers design them carefully. Finding the
formation and particle dissolution process, the reducing balance point between safety and application is essential.
substances (ascorbic acids) and organic acids played a vital
role. The biotransformation process includes cerium oxide
nanoparticles being absorbed on the root surfaces and dis-
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