Photodiagnosis and Photodynamic Therapy 19 (2017) 67–72

Contents lists available at ScienceDirect

Photodiagnosis and Photodynamic Therapy

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

Review Article

Safety issues associated with the use of nanoparticles in human body MARK
a,c a b
Mian Muhammad Sufian , Jabar Zaman Khan Khattak , Shahzad Yousaf ,
⁎
Muhammad Suleman Ranac,
a
Department of Bioinformatics and Biotechnology, International Islamic University, Islamabad, Pakistan
b
Department of Bio-Sciences COMSATS Institute of Information Technology, Islamabad, Pakistan
c
Department of Virology, National Institute of Health, Park Road, Chak Shahzad, Islamabad, Pakistan

A R T I C L E I N F O A B S T R A C T

Keywords: Nanotechnology has transformed the world by the introduction of a distinctive class of materials and products in
Nanotechnology a wide array of fields. It has contributed to the production of innovative materials and devices. Having unique
Safety advantages and domestic along with industrial applications, however, has raised the issue of safety for con-
Human body sumers, producers and environment. Having a comparative smaller dimension and other exclusive properties,
Toxicity, Photodynamic Therapy
nanoparticles have the ability to harm human body by interacting through various mechanisms. Here, we en-
deavoured to review and discuss the characteristics of nanoparticles relevant to their toxicity, conceivable ex-
posure routes of nanoparticles to human body like skin contact, inhalation, and ingestion, and the basic ap-
proaches which can aid to control human exposures to toxic nanoparticles have been discussed.

1. Introduction
The 1959s classical talk entitled “There is a plenty of room at the
bottom” by Richard Feynman at American Physical Society (APS)
meeting lead to the genesis of a revolutionary technology, which en-
compasses manipulation of matter at the atomic and molecular level.
Since then nanotechnology has remained an extensively researched
scientific domain and keeps on flourishing in a continuous manner [1].
Present-day nanotechnology has emerged as one of the most innovative
and impactful scientific field. Recent decade have witnessed a re-
markable progress in the use of nanoparticles (NPs), with an approxi-
mately 1814 nano based products in the market [2]. Realizing the fact,
the President Obama’s 2017 Budget provides $1.4 billion to National
Nanotechnology Initiative (NNI), with a gross total of approximately
$24 billion since its foundation in 2001 [3]. Besides this revolutionary
brighter side, there also exists a darker side of the picture, “the perils of
nanotechnology”. Increased industrial usage and commercialization of
nano based items have increased the occupational and consumer based
risks and hazards. The proper knowledge and awareness of these par-
ticular nanoparticles associated health hazards is crucial to make this
cutting-edge technology more beneficial and safe [4].
The prefix “NANO” refers to a mathematical term 10−9 which is
“one billionth” of something. The term nanoparticles is therefore, used
to describe the nano scale particles exhibiting extremely small size with
very exclusive physio-chemical behaviour due their large surface to
volume ratio, and unique size dependent properties [5]. The current
applications of NPs include fields of biotechnology [6], bio sensing and
security [7], diagnostics and therapeutics [8,9], food microbiological
safety [10] and waste water management [11]. Furthermore, nano-
technology exhibits boundless and ever growing list of industrial ap-
plications encompassing areas of paint, agriculture, food and beverages,
construction, textile, energy electronics, optics, and cosmetics [12].
Research institutes around the world are fervently working on the ex-
ploration and development of new exciting applications in the field of
nanotechnology and the visionary industrialists and governments are
generously funding the research projects, realizing the importance and
impact of this future technology [13]. However, scientists and en-
vironmental activists have questioned about the potential risks and
hazards associated with the use of nanomaterials. There is a grave de-
ficiency of comprehensive studies addressing the human health and
environmental impacts of nanoparticles.
One of the most impactful applications of NPs is nanomedicine
which emerged as a promising playground for material scientists and
chemists. A wide array of specialized NPs are being applied successfully
and several other types are under their development stages [14]. Given
the unique magnetic and optical features, the nanoparticles are now
extensively being researched and show a potential to be used in un-
conventional therapeutic approaches for cancer. One such approach is
photodynamic therapy (PDT) which involves use of photosensitizing
agents followed by irradiation at photosensitizer-specific wavelengths,

⁎
Corresponding author.
E-mail address: ranavirologist@gmail.com (M.S. Rana).

http://dx.doi.org/10.1016/j.pdpdt.2017.05.012
Received 5 January 2017; Received in revised form 14 April 2017; Accepted 18 May 2017
Available online 24 May 2017
1572-1000/ © 2017 Elsevier B.V. All rights reserved.

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M.M. Sufian et al.
generate reactive oxygen species (ROS) that lead to the apoptosis and
cell death [15]. Several types of nanoparticles are currently being used
as carriers for photosensitizers including metallic, ceramic, inorganic
oxide and biodegradable polymer-based nanomaterials [16,17]. How-
ever, the photosensitizers with extreme hydrophobicity require carrier
systems. Nano particles with their exceptionally unique properties not
merely serve as effective carrier systems for photosensitizers but also
carry non-photoactive cytotoxic drugs (combinational therapy) to en-
hance the effectiveness of PDT [18]. Another such innovative approach
is Nanoparticle based Self-lighting photodynamic therapy which in-
volves use of water-soluble scintillation nanoparticles that can serve as
effective photodynamic agents in PDT [19,20]. Nano and PDT joint
venture is proving to be promising approach to fight deep tumors. For a
detailed understanding of the rapid advancements in nano-based PDT
modalities opted to counteract various tumors and other chronic dis-
eases, the readers are referred to review articles published in
[16,17,21–23]. Naturally the use of NPs as drug carriers and in diag-
nostics may pose severe toxic and harmful effects to human body [24].
The capacity of Nanoparticles to generate reactive oxygen species
(ROS), Triggering inflammation and induction of apoptosis can be the
crucial cellular effects of nanomaterials [25,26]. Furthermore, nano-
particles can also alter gene expression by acting as epigenetic mod-
ulators [27]. Better understanding of the nano-particle interactions and
their effects on biological systems is essential for the developing a
consumer friendly and safe nanotechnology.
The hazards based on particular properties, routes of exposure,
potential toxic effects and prevention are briefly reviewed. Before
proceeding further, it is worth mentioning the classification of NPs on
the basis of their composition and structure four types: (1) Inorganic
NPs which include all metal and metal oxide NPs; (2) Organic NPs
which include polymeric and biologically compatible NPs; (3) Carbon-
based NPs include carbon nanotubes, graphene, carbon nanofibers,
carbon black, carbon Nano foams, carbon rods; (4) Organic–inorganic
hybrid NPs.
2. Toxicological basis of nanoparticles
Appropriate awareness of factors and properties of NPs is of utmost
importance to predict any kind of toxicological side effects of nano-
particles in the human body. The interactions of NPs with human body
and environment, directly or indirectly affect the potential outcomes of
the use of NPs. The application of NPs as drug delivery systems re-
present a most attractive and obvious application of NPs in human
body. Distribution of NPs and their clearance from the body depends on
their nature and properties [28]. Let us briefly navigate the toxic
properties of NPs.
2.1. Size
Nanoparticles exhibit an exceptionally increased surface to volume
ratio due to their ultra-small size. This property provides these particles
with a more prompt reactive approach and hence, toxicity.
Furthermore, these nano-sized particles have comparatively higher and
efficient penetrative potential in human and plant tissues than ordinary
particles [29]. Penetration levels of NPs, across different barriers of
cells are mostly size dependent. Decreased size exponentially increases
surface area resulting in higher levels of oxidation and DNA damaging
capabilities [30]. NPs with a size of 35 nm or less are assumed to pe-
netrate and cross the blood–brain barrier, and particles with size <
40 nm or more have a potential to enter nuclei of cells while those with
size up to 100 nm can cross cell membrane [31]. Increased Nano sized
penetrative potential is associated with higher toxicity by inducing
oxidative stress, genomic and mitochondrial DNA damage and apop-
tosis [32]. Silver nanoparticles (AgNPs), for example, were observed to
induce size-dependent cytotoxicity in human lungs cells due to sub-
stantial release of Ag in cellular medium [33]. Similarly gold
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Photodiagnosis and Photodynamic Therapy 19 (2017) 67–72
nanoparticles (AuNPs), exhibited acute and chronic toxicity based on
their size [34]. Some other examples of size-dependent toxicity of NPs
include cellular interaction studies which indicated that AgNPs also
showed cytotoxicity to human lung cells at size of 10 nm which was
independent of surface functionalization [33]. In another study,
Rainbow trout fish was exposed to commercially available AgNPs of
different sizes (10, 35, 600–1600 nm) in order to determine their out-
comes. The results showed a higher concentration of small sized
(10 nm) particles accumulated in gill and liver tissues [35]. A different
study revealed faster cellular uptake of carboxylic acid-functionalized
polystyrene beads (PBs) of 20 nm size compared to 200 nm [36]. Cel-
lular uptake, interaction mechanism, and intercellular stability are
dependent on NP size but still a definite correlation cannot be estab-
lished based on accessible studies. In a brief way, it can be supposed
that small size particles are more prone to cellular internalization and
display more toxicity than the larger ones [37].
2.2. Shape
Shape of NPs also plays a part in their toxic effects. A study by
Nangia and Sureshkumar [38] showed that shape and charge on NPs
can accelerate the translocation through cell membranes up to 60 or-
ders of magnitude. AgNPs with varying shapes are reported to affect the
cells in a diverse way [39]. Keeping size and surface area same for one
type of NPs helps in evaluating their shape affecting toxicity. ZnO NPs
in shape of nanorods bring more toxic to human lung epithelium cells
(A549) compared to spherical ZnO NPs [40].
2.3. Kinesis
NPs are compact units capable of moving in the way gases and li-
quids move. Accessing any toxic effects of NPs to human body, a clear
consideration of their kinesis is necessary. NPs easily diffuse into the
animal and plant cells due to their extraordinary small size and in-
creased mobility. Size of NPs is inversely related to the diffusion ca-
pacity. Kinesis is also one important factor which facilitates accumu-
lation of NPs by getting them close to each other [29]. Kinesis refers to
process of absorption of NPs, their distribution in the body, metabolism
and finally the elimination [41]. On entering the biological system the
plasma proteins bind to the surface of the NPs and form a nanoparticle
protein complex. This nanoparticle protein complex further influences
the biological response of the body. The protein binding is among the
key factors that are responsible for bio-distribution of NPs throughout
body [42]. Similarly, inside the biological system the NPs can behave
differently than ordinary particles as the charge, size and shape of the
NPs vary among diverse particle types. All these properties are re-
sponsible for the fate of NPs inside biological systems, ultimately af-
fecting the process of kinesis and toxic effects. The term nanotox-
icodynamics is used to confer the interactions of NPs with biological
matrices [43]. Moreover, studies have shown that NPs can cross various
biological barriers. The study by Fu et al. [44] investigated the kinesis
and toxic effects of Silver nanoparticles sized 110 nm via different ex-
posure routes. Orally administered silver nanoparticles were found to
be absorbed through intestine and found in the liver of the mice. While
intravenously administered were found to be present in both spleen and
liver. A low absorption rate was observed and finally the excretion of
NPs was mainly through urine and faeces following different exposure
routes. Additionally, inflammation at the injection site was also evi-
dent. Similarly Choi et al. [45] demonstrated that NPs with diameter
less than 34 nm and with a non-cationic surface charge can efficiently
translocate to mediastinal lymph nodes from the lungs while NPs with
less than 6 nm were found to be more rapidly translocated from lungs to
lymph nodes, than to the blood stream and finally cleared by the kid-
neys.
M.M. Sufian et al.
2.4. Nature
Nature of NPs also plays an important role in determining the
toxicity. Nanoparticles possess a diverse nature with phases of both
solute and separate particle based properties. Nanoparticles with
smaller size have an increased surface/volume ratio (S/V) compared to
NPs with greater size. A 10 nm particle contain an approximate of
35–40% of atoms localized at this area while a particle with a size of
30 nm have less than 20% of atoms localized. The higher S/V ratio
provides these particles with a specific and strong surface reactivity.
Additionally, NPs are also found to denature proteins by adsorbing and
altering their structure [46]. Particulate composition [47], direct re-
lease of ions after dissolution [48], catalytic properties [49], and redox
potential [50,51] are the possible mechanisms associated with the
toxicity of NPs. Different NPs have varying effects on similar tissues.
Many studies favour this phenomenon, for example, AgNPs were found
more toxic than CeO2 NPs for a wide variety of toxicity measures and
parameters carried out in animal and cell models [52]. The difference in
the sizes of the particles can be one potential factor, as the AgNPs used
in this study were of larger size than CeO2. One another important
factor regarding this difference in toxicity could be variable interspecies
susceptibility potential and differences in the nature of cell and animal
model. This study proved the toxicity of AgNPs to be higher for aquatic
invertebrate species. In an another study AgNPs were found to induce
higher toxicity to transparent embryos of zebrafish compared to gold
NPs at similar size range and concentrations [53]. This significantly
different toxic potential, with the AgNPs being more toxic than gold
NPs signifies the importance of nature, chemistry and physiochemical
properties of the nanoparticles.
2.5. Stability
Stability of NPs in biological systems is primarily dependent on
nature, size and concentration of NPs. Apart from their own special
characteristics, environment within the biological systems like a human
body affects the stability of NPs. For example most of the organic and
inorganic NPs become soluble in pH prevalent in human body. In case
of metals and metal oxide NPs, concentration of metal ions increases
within the cells resulting in high stress within the cells. Solubility of NPs
in an environment is basic parameter to their stability and toxicity. In
case of insoluble NPs such as ceria, zirconia, and titinia, studies showed
reduced cell activity and DNA quantity [54].
2.6. Medium and storage time
Medium in which NPs are produced or kept in, is also critical in
determining their toxicity. Size of NPs can differ in varying ionic
strengths consequently resulting in variable toxicity. Kittler et al. [48]
studies citrate and poly-vinylpyrrolidone stabilized AgNPs for dissolu-
tion in water by dialysis at 5, 25, and 37 °C for up to 125 days. A very
slow ionic dissolution rate was observed for a time period of several
days with no or very little particle diameter change. The aged silver
particles with slow dissolution were further tested for toxicity measures
in comparison with freshly prepare AgNPs and showed a significantly
higher toxicity. Similarly in another study. Citrate capped AgNPs ex-
hibited media-dependent toxicity against (Oncorhynchus mykiss) gill,
RTgill-W1 cell line. Three diverse exposure media naming L15/ex, L15/
ex w/o Cl and d-L15/ex were studied. d-L15/ex is low ionic strength
medium is potentially excellent media to study effects of NPs to gill
cells [55].
3. Hazards and mechanisms of NPs entry to human body
The Nanotechnology has emerged as the main stream technological
innovation of the current century. Consequently, the higher production
rates also pose risk of potential release of these nano structured
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Photodiagnosis and Photodynamic Therapy 19 (2017) 67–72
materials in the environment and resultant harmful effects on eco-
system. With this increased industrial usage has also increased occu-
pational exposure [56]. Typically occupational hazards occur to pro-
ducers and workers (including engineers, researchers, and technicians)
during the research-scale manufacturing and processing. These hazards
mostly results raw material handling while performing chemical reac-
tions through the equipment [57]. Classification of NPs, packaging,
storage, transportation and waste treatments is other possible hazards.
The next level hazards are associated to the consumers that are exposed
to such nanomaterial during usage and application, which may un-
knowingly lead to harmful and toxic effects [58]. Interaction of NPs to
human body can occur via: (1) penetration through skin nodes; (2)
Inhalation; and (3) Ingestion. Extent of NPs exposure is also important
in determining the toxicity of NPs. Any substance, whether small heavy
metals or organic macromolecules is toxic to living systems above a
certain level. Current studies explaining the mechanism of NPs diffusion
into human system, uptake by cells and tissues, how they are dis-
tributed and possible health hazards are insufficient and are being re-
searched throughout the world. Main routes of NPs exposure to human
body are penetration through skin, ingestion through food materials
and inhalation through respiration. The up taken NPs penetrate to other
organs through respiratory and blood circulation systems [59].
3.1. Penetration through skin
The increased use of nanostructured based cosmetics increased the
exposure of NPs to skin and ultimately penetration into the blood cir-
culation, raising serious safety and health concerns [29]. As a con-
sequence of this boom in the use of NPs in cosmeceutical like ZnO has
resulted in the serious deliberate exposure. Unintended exposure to
human skin occurs through manufacture, burn, and removal of used
NPs. NPs can penetrate through skin cells, (transcellular pathway) and
through hair follicles (follicular penetration pathway) [60]. Human
skin is an effective barrier towards NPs and other toxic chemicals;
nevertheless, the existence of hair follicles and sweat glands makes this
barrier susceptible by facilitating the diffusion of small-sized NPs [61].
Titanium dioxide nanoparticles (TiO2), a class of the most widely used
nanoparticles are thought to indirectly damage the skin. Rapid dis-
tribution, poor elimination, and increased tissue accumulation are the
key factors responsible for increased cellular toxicity. The wide use of
nano particles especially TiO2 NPs is consequently posing serious ne-
gative developmental effects along with other health risks [62]. The
topical application of NPs in treating wounds and skin damage favours
smooth penetration [61]. Antimicrobial properties of AgNPs offer ex-
citing medical applications especially in the field of cosmeceuticals
[63]. The exaggerated use of NPs in cosmeceuticals have increased
health concerns keeping in view their discrete toxic nature [64]. Others
sources of unintentional human exposure involve vehicle emissions
[65], ultrafine particles generation during welding fumes emissions
[66], emission from incineration of community waste [67], emissions
from coal [68], natural gas and oil production units [69]. Once NPs
enter the skin, they can show their various toxic implications like in-
creased oxidative insult, DNA damage, inhibition of mitochondrial ac-
tivity and the initiation of apoptosis [70]. NPs in murine and human
cell line studies have shown marked irritation and inflammation fol-
lowing a dose dependent exposure [71].
3.2. Inhalation
Inhalation of NPs result in their penetration into lungs and inter-
action with the epithelium layer present there. The resulting in-
flammation can finally take NPs to lymph nodes [72]. The inhalation of
NPs and their effect on lungs depend on: (1) quantity of nanoparticles;
(2) amount and rate of deposition in lungs; (3) structural properties of
NPs; (4) efficacy of clearance mechanisms [73]. Several studies have
reported the adverse effects of NPs on alveolar macrophages and also a
M.M. Sufian et al.
predisposition to the lung cancer [74,75]. TiO2 nanoparticles in murine
model inhalational studies have shown to cause vasodilation impair-
ment in coronary arterioles [76]. Nanoparticle inhalation is thought to
adversely affect the asthmatic symptoms by inducing a prompt in-
flammatory response. Carvalho et al. [77] observed a robust increase in
eosinophilic response in mice lungs when exposed to carbon based
nanoparticles.
3.3. Ingestion
The global environmental changes have adopting alternative stra-
tegies to counter food shortages. The use of Nanoparticles in agriculture
and food industry has gained immense attention in the recent decade
[78]. The nanoparticles in the food sector are used to develop products
with newer taste and texture features, to enhance nutrient absorption
capacity, to improve packaging of food products. Moreover, a diverse
class of food related products such as food ingredients, supplements,
additives are already being synthesized and used in some countries
[79]. Apart from these beneficial aspects the extensive uses of NPs in
food industry have raised serious safety concerns. Ingestion of NPs is
one of the principal exposure route to human body [70]. NPs directly or
indirectly used in food products and drugs are ingested orally and get
absorbed through digestive system [80] from where they move in
lymphatic cell tissues [61]. These ingested NPs dependent upon their
nature are either excreted if unstable or accumulated by physical or
chemical changes resulting in blockage of gastrointestinal tract leading
to death [81]. Gerloff et al. [82] investigated the cytotoxic effects of
various types of NPs being used as food additives (TiO2 and SiO2), NPs
in food packaging (ZnO and MgO) and carbon black on human in-
testinal Caco-2 cells. All particles were found to be cytotoxic with en-
hance DNA damaging effects. There is a lack in research and knowledge
implicating and assessing toxicity of NPs in food-related materials and
goods that completely link and describe ingestion process [83].
4. Control of exposure to nanoparticles
As we know that the realm of nanotechnology spans the form of
matter that is in the size range of 100 nm or less. This little big science
laid the foundations for a great industrial revolution and continuously
generating innovative classes of materials and state of the art technol-
ogies [84]. Such extensive use of large number and variety of these
nano structured particles has raised questions related to the safety of
producers, consumers, and environment. NPs can be irritants, haptens,
reactive materials, and interactive substances [85]. Murine model stu-
dies have shown metal oxide nanoparticles such as ZnO, CeO2, Al2O3,
TiO2, on inhalation induce significant toxic effects such as acute airway
irritation, DNA damage, pulmonary inflammation and airflow limita-
tion [86,87]. Similarly, the haptenic metal oxide NPs particularly NiO
and CO3O4 were also shown to induce chronic immune-inflammatory
responses via delayed type hypersensitivity mechanisms in rats [88].
Atomic force microscopy showed that NPs can bind to genomic DNA
and hence can compromise DNA replication fidelity [89]. The bio-
physiochemical interactions of NPs with cell membranes, cell orga-
nelles, proteins, and genetic material lead to processes that may result
in either biocompatibility or bio-adversity [90]. Therefore, a proper
knowledge and awareness regarding hazardous nature of NPs and use of
personal protective equipment (PPE) are primary points of considera-
tion. Following nano-safety guidelines [91], good laboratory practices
(GLPs) and international safety protocols can be advantageous in the
risk management [57]. Ventilation system can help to get rid of NPs
that are airborne within the working equipment. Regular cleaning of
work place, walls, equipment, and other accessories is also re-
commended for minimizing exposure extent [92]. Studies suggest that
handling of NPs in glove box helps in preventing exposure to them [59].
In addition to all protective measures, regular medical testing of oc-
cupational workers in inevitable. The testing may include investigating
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Photodiagnosis and Photodynamic Therapy 19 (2017) 67–72
levels of pulmonary and cardiac disease markers, markers for oxidative
stress and inflammation, antioxidant enzymes and markers for acces-
sing genotoxicity [93]. Inhalational exposure can be avoided by
maintaining a proper control of workplace environment [94]. Aerosol
control mechanisms are of utmost importance in reducing NPs gen-
eration. Use of filters in the laboratory can be helpful [95]. Nevertheless
personal safety equipment can hinder or stop inhalation of NPs. Like-
wise, reduction in period where nanoparticles are handled can be
helpful. Such kind of approaches can also be adopted to avoid skin and
ingestion exposure.
5. Conclusion
Because of the unique attributes, NPs are being widely used and are
driving an appealing consumer market. However, compelling evidences
of direct and indirect toxicity of NPs to the human body are also pre-
sent. Generation of reactive oxygen species causing cellular toxicity has
also been reported. Cytotoxicity of NPs has become a concern for re-
searchers. Toxicity of NPs is affected by their inherent properties such
as size, shape, nature, surface chemistry, and charge, medium of
synthesis, storage time, aggregation, stability, mobility, and reactivity.
Skin contact, inhalation, and ingestion are three main routes through
which NPs can enter human body. Environmental conditions play a
vital role in determining toxicity of nanoparticles. Keeping all the ha-
zards posed by NPs, control of exposure to NPs can be attained by
scrutinizing the specificity of engineering equipment and working
place. Use of personal protective equipment (PPE) and regular medical
check-ups may substantially save from risks of exposure. Research in
area of NPs toxicity is much dispersed and different toxicity assays have
been tried and reported for different kind of NPs. Any conclusive re-
marks would be deficient based on available literature. Nevertheless,
standard methods must be established to determine toxicity of all kind
of NPs to human body.
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