Ceramics International 43 (2017) 907–914

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Ceramics International
journal homepage: www.elsevier.com/locate/ceramint

Review article

Zinc oxide nanoparticles: Biological synthesis and biomedical applications

a,b c,d,⁎
crossmark
Hamed Mirzaei , Majid Darroudi
a
Neurogenic Inflammation Research Centre, Mashhad University of Medical Sciences, Mashhad 9177948564, Iran
b
Department of Medical Biotechnology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
c
Nuclear Medicine Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
d
Department of Modern Sciences and Technologies, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

A R T I C L E I N F O A BS T RAC T

Keywords: Nanotechnology is termed as a result of the synthesis, characterization, exploration, and application of nano-
Zinc oxide nanoparticles sized materials in the event of science and technology. In recent years, zinc oxide nanoparticles (ZnO-NPs) as an
Green synthesis important ceramic materials are utilized in completely different industrial sectors such as medication, cosmetic
Eco-friendly materials and concrete, opposed microorganism, textile and automotive industries. Many chemical and physical
Biomedical
methods were applied for preparing of ZnO-NPs but biological methods as “green” routes in different
substrates (e.g., microorganisms, enzymes, bacteria, and plant extracts) are potentially steered as eco-friendly
alternatives in comparison with chemical and/or physical techniques. At the present, ZnO-NPs are being
investigated as associates of antibacterial agents in each microscale and nanoscale formulation. The ZnO-NPs
are widely wont to treat a range of different skin conditions and have anticancer properties. In addition, ZnO-
NPs have emerged as a suitable tool in drug delivery and sensing horizon. In this review, we summarize the
green and biological synthesis methods of ZnO-NPs and investigation of their biomedical applications.

1. Introduction synthetic methods. ZnO is nontoxic and compatible with human skin
by creating an acceptable additive for textiles and surfaces that are in
The field of nanotechnology is one of the every foremost active contact with flesh. In comparison to bulk, the rising extent of nanoscale
analysis areas in fashionable materials science [1,2]. Nanoparticles ZnO has the potential to enhance the potency of fabric operation. As a
exhibit new or improved properties which are supported with specific vital semiconductor with tremendous scientific and technological
characteristics such as size, distribution and morphology. There are interest, ZnO has an outsized exciton-binding energy (60 meV) [11]
spectacular developments in the field of nanotechnology within the and on the spot wide gap (3.37 eV) that could be the most well-liked
recent past years, with various developed methodologies to synthesize multitasking metal and chemical compound which contains an en-
nanoparticles with specific form and size which are counted for specific ormous list of enticing properties. As a result of its distinctive optical
needs. New applications of nanoparticles and nanomaterials are and electrical properties [12], it is considered to be a possible material
increasing rapidly; while operating with nanomaterials has allowed a in optoelectronic applications to operate in the visible and close to
much better understanding of biology [3,4]. As a consequence, there’s ultraviolet spectral regions. ZnO-NPs are widely utilized in several
the potential of providing novel ways regarding the treatment of industrial areas such as UV light-emitting devices [13,14], ethanol gas
diseases that were antecedently tough to focus on due to size restric- sensors [15,16], photo-catalysts [17,18], pharmaceutical, and cosmetic
tions. For medical specialty applications, the synthesis of bio-functional industries [19]. Properties including non-toxic, self-cleansing [20],
nanoparticles is extremely vital, and it has recently caught the attention compatible with skin, antimicrobial, and dermatologic associate de-
of diverse analysis teams, creating a perpetually evolving space [5–8]. greed are employed as UV-blocker in sunscreens and lots of medical
The growing demands for environmental friendly nanoparticles, re- specialty applications [21]. ZnO seems to powerfully resist microorgan-
searchers have utilization inexperienced strategies for the synthesis of isms, while several reports show sizeable antibacterial drug activities of
varied metal oxide nanoparticles for pharmaceutical applications CaO, MgO and ZnO [22] that is attributed to the generation of Reactive
[9,10]. Oxygen Species (ROS) on the surface of these oxides. In spite of those
Zinc oxide (ZnO) exists within the earth crust as a mineral zincite; deserves, ZnO is bio-safe, biocompatible with distinctive abilities such
while most of it that is used commercially is produced through as structure-dependent, electrical and thermal transport properties,

⁎
Corresponding author at: Nuclear Medicine Research Center, Mashhad University of Medical Sciences, Mashhad, Iran.
E-mail addresses: [email protected], [email protected] (M. Darroudi).

http://dx.doi.org/10.1016/j.ceramint.2016.10.051
Received 26 June 2016; Received in revised form 6 September 2016; Accepted 8 October 2016
Available online 10 October 2016
0272-8842/ © 2016 Elsevier Ltd and Techna Group S.r.l. All rights reserved.
H. Mirzaei, M. Darroudi Ceramics International 43 (2017) 907–914

that might vary according to the particle size, shape, morphology, in completely different industrial sectors including drugs, cosmetic
orientation and ratio [23,24]. One of main applications of ZnO-NPs is materials and concrete, opposed microorganism, textile and automo-
the utilization of them as an effective drug delivery system [3,4]. tive industries [52]. The ZnO-NPs is currently being investigated as an
Recently, various reports have used ZnO-NPs as drug delivery system associate degree of antibacterial drug agents in each microscale and
in various diseases. It has been showed that these nanoparticles could nanoscale formulations. Results have indicated that ZnO-NPs show
target some drug to various cells and tissues [3]. In addition, sensing antibacterial effects that are apparently larger than its microparticles
and imaging are one of important fields in tracking and monitoring [53].
patients. ZnO-NPs could be used as a suitable bio-imaging tool. Here, To synthesize ZnO-NPs, the utilization of environmentally benign
we highlighted significant aspects of ZnO-NPs green synthesis and materials such as natural materials and biopolymers [9,54], plant leaf
various their biomedical applications [4]. extract [55–57], bacteria [58], fungi [59,60], and algae [61] offers
varied advantages of eco-friendliness and compatibility for pharma-
2. Green synthesis of ZnO nanoparticles ceutical and different medicinal applications, whereas noxious chemi-
cals aren’t used for the synthesis protocol. The use of plant extracts in
Chemical and physical synthesis strategies are pricey and require in synthesis methodology has drawn attention as a straightforward and
depth labor and time. Moreover, giant quantities of secondary waste viable difference to chemical and physical strategies. The “green” route
are generated, ensuing from the addition of chemical agents for for nanoparticles synthesis has become interesting as a result of eco-
precipitation and reduction within the processes. Chemical synthesis friendliness, economic prospects, practicable and wide selection of
strategies that are typical such as chemical precipitation result in the applications in nanomedicine, chemical change drugs, nanooptoelec-
presence of some poisonous chemical species which are adsorbate on tronics, etc. [62]. It is a replacement and rising space of analysis within
the surface that will have adverse effects in medical applications [1,25]. the scientific world, whereas day by day developments are noted in
There are reactions that need heat and/or air mass to initiate, whereas warranting a bright future for this particular field. Biosynthetic and
some others need inert atmosphere protection, and/or utilization surrounding-friendly technology to synthesize flower shaped ZnO-NPs
poisonous matters similar to H2S, poisonous model and stabilizer, are believed to be non-toxic, bio-safe, and biocompatible which are
and bimetallic precursors [26]. Chemicals which are used for nano- used as drug carriers, cosmetics, and fillings in medical materials [63].
particles synthesis and stabilization are poisonous and result in non- To be noted, most of the commercially used ZnO-NPs are produced
ecofriendly byproducts [27]. Several physical and chemical procedures synthetically that have various advantages, in comparison to silver
are used to synthesize huge quantities of nanoparticles in an exceed- nanoparticles, such as lower value and white appearance [64]. Various
ingly and comparatively short period of time [28–36]. Among the most types of plants and bio-templated media which are used to synthesize
generally used approaches for preparing of ZnO-NPs, solution-based ZnO-NPs are shown in Figs. 1–3 respectively.
routes are very wide and simple such as chemical precipitation [37,38], Using plant extract is one of the ways for inexperienced synthesis of
sol-gel [25,39], solvothermal [40], hydrothermal [41,42], and etc. ZnO-NPs. Sangeetha et al.., used aloe barbadensis miller leaf extract
Chemical strategies result in the presence of some noxious chemicals for ZnO-NPs synthesis through chemical and biological methods.
that are absorbable on the surface and have adverse effects in medical Extremely stable and spherical ZnO-NPs are created by utilization zinc
application. Increasing awareness towards inexperienced chemistry nitrate and Aloe vera leaf extract. More than 95% conversion to
associate in nursing different biological processes has light-emitting nanoparticles has been achieved with Aloe vera leaf broth concentra-
diode to the event of an eco-friendly approach for the synthesis of tion greater than 25%. The SEM and TEM analysis show that ZnO-NPs
nanoparticles. ready were poly-dispersed and therefore, the average size has been
Green synthesis of nanoparticles makes use of environmental ranged from 25 to 40 nm. The obtained nanoparticles are found to be
friendly, non-toxic and safe reagents. Khorsand Zak et al.., used gelatin preponderantly spherical and thus the particle size may be controlled
as a stabilizing agent to synthesize ZnO-NPs via a modified sol–gel by variable concentrations of leaf broth solution [65]. Table 1 demon-
route. Long-chain gelatin compounds were used to terminate the strates different green media for preparing of ZnO-NPs.
expansion of ZnO-NPs and to also stabilize them. The ZnO-NPs which
were calcined at completely different temperatures exhibited a hex-
agonal (Wurtzite) structure with sizes from 30 to 60 nm. The influence 3. Biomedical applications of ZnO-NPs
of oxidization temperature on the morphology of ZnO-NPs was
additionally investigated. Their results indicated that gelatin is a Significant interest has arisen in the research of NPs during the last
remarkable material which will be used as a stabilizer within the sol–
gel technique to prepare little ZnO-NPs [43]. Biological (green)
methods for the synthesis of nanoparticles utilization microorganisms,
enzymes, and plants or plant extracts are steered as potential eco-
friendly alternatives to chemical and physical methods. Many biological
systems as well as bacterium, fungi and yeast are employed in the
synthesis of nanoparticles [43–46]. Synthesis of nanoparticles utiliza-
tion microorganisms involves elaborated methods of maintaining cell
cultures, living thing synthesis and multiple steps of purification [47].
During these regard utilization “green” strategies in the synthesis of
ZnO-NPs flower shaped has progressively become a subject of interest,
since standard chemical strategies are costly and require the employ-
ment of chemical/organic solvents as reducing agents [9,40,48].
Among the candidates for fabrication of medical alcohol bio-sensors,
ZnO-NPs are considered a suitable choice [49,50] since it has
deodorizing and medicinal drug properties and square measure
utilization in food packaging. Several ZnO-NPs as products are utilized
to treat skin conditions in powder such as barrier creams to treat diaper
rashes, mineral cream, anti-dandruff shampoos, antiseptic ointments
and medical bandages [7,51]. In recent years, ZnO-NPs are put to use Fig. 1. Different bio-templated media for preparing of ZnO-NPs.

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Fig. 2. Some of plants used for the synthesis of ZnO-NPs; Cassia auriculata (a), Parthenium hysterophorous (b), Aloe vera (c), Acalypha indica (d), Calotropis gigantean (e) and Abrus
precatorius (f).

decade, regarding biomedical applications in particular [66]. The very important for biomedical applications and recently it has drawn
integration of nanotechnology into medical science has opened new the attention of numerous research groups that constantly evolve this
possibilities and allowed a better understanding of molecular biology. field [68]. Currently, there is a vast extent of materials and chemical
As a consequence, there is the potential of providing novel methods for synthesis techniques that are being investigated for biomedical appli-
the treatment of diseases which were difficult to target before due to cations as we mentioned several medical approaches of ZnO-NPs in
size restrictions [67]. The synthesis of biofunctional nanoparticles is this review. Zinc is a natural component and a part of nature's inherent,

Fig. 3. Schematic of green synthesis of ZnO-NPs.

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H. Mirzaei, M. Darroudi Ceramics International 43 (2017) 907–914

Table 1 ing particle dose, treatment time and synthesis methodology. In

Green materials for preparing of ZnO-NPs. addition, its clearly incontestable that the particle size variation and
surface area to volume ratio of green ZnO-NPs are the cause of vital
Green substrates Name References
higher antimicrobial activity which this info results obtained. It is
Polymer Gelatin [43] recommended that inexperienced ZnO-NPs has the potential to be used
Starch [9] effectively in agricultural and food safety applications and also address
future medical issues [65].
Plant Calotropis gigantean [20,79]
Abrus precatorius [80]
Aloe barbadensis [77] 3.2. Antimicrobial Potential of ZnO-NPs
Cassia auriculata [81,82]
Acalypha indica [83,84] ZnO is being investigated as an associate degree medicament agent
Parthenium hysterophorus [85]
in each microscale and nanoscale formulations. Results have indicated
Camellia sinensis [86]
Calotropis procera [79] that ZnO-NPs has shown medicament activity that was apparently
Musa balbisiana [87] larger than small particles; although the precise mechanisms of
Citrus paradise [88] medicament action haven’t been clearly comprehended, yet it’s been
Medicago sativa [89]
prompt that most of the causes regarding cell swelling are the rule of
Algae Marine macroalgae [90] ROS that generate on the surface of particles, zinc ion release,
Caulerpa peltata [71] membrane dysfunction, and nanoparticles acquisition area unit. High
Hypnea Valencia [71] temperature treatment of ZnO-NPs incorporates an important impact
Sargassum myriocystum [71] on their medicament activity, while treatment at the next temperature
Sargassum muticum [90]
results in a lower activity. The mechanisms of medicament activity of
Bacteria Aeromonas hydrophila [91] ZnO-NPs aren’t well understood and although it is projected that the
Lactobacillus sporogen [92] generation of oxide can be the main issue of this activity, yet it is
Enterococcus faecalis [93] indicated that the binding of the particles on microorganism surface,
Bacillus cereus [94]
owing to the electricity forces, can be a mechanism study regarding the
Fungi Aspergillus fumigates [95,96]
medicament behavior of ZnO-NPs which can be done by employing a
Aspergillus aeneus [95] chemiluminescence and oxygen electrode analysis. Metal nanoparticles
Fusarium spp [97] area unit are extremely ionic and may be ready with extraordinarily
high surface areas, along with uncommon crystal and morphologies
that possess varied edge/corner and different reactive surface sites.
which fulfills important metabolic functions in humans, animals and ZnO-NPs area unit is being studied in unison with medical procedure
plants. Exposure to natural background levels of zinc in the biosphere ablation regimens. In addition to higher thermal impact on neoplasm
is essential for all living organisms. Zinc oxide is recognized as a ablation, nanoparticles will deliver antineoplastic medical specialty that
valuable nutritional additive and is widely used in cosmetic, pharma- illustrates a synergistic antineoplastic impact in the presence of
ceutical and medical applications. Although it is generally recognized warmth and may even be imaged to attain preciseness in medical
as being safe, yet inhaling of zinc oxide dust and fumes must be aid. Several studies indicated that the molecular mechanism involved
avoided. Regulations are in place to control potential exposure in ablation of tumor mediated nanoparticles would further help
scenarios [69]. Fig. 3 illustrates a schema of ZnO-NPs green synthesis engineer nanoparticles of suitable composition and properties to
and their applications. synergize the ablation property [74–76].

3.1. Antibacterial Activity of ZnO-NPs 3.3. Selective killers of proliferating cells

Medicinal drug agents generally divide to organic and inorganic ZnO-NPs induce the death of cancerous cells without having any
materials. At high temperatures/pressures organic medicinal drug cytotoxic impact on normal cells [77,78]. There are many problems
materials square measure are found to be less stable in comparison that need to be resolved before translating ZnO-NPs into medical use,
to inorganic medicinal drug agents [53]. The ZnO-NPs has proven to be as well as the lack of appropriate biocompatible dispersion protocols
a strong medicinal drug agent within the formulation of microscale and and a much better understanding is required for the mechanism of
nanoscale systems for therapeutic applications. Although ZnO-NPs has their selective cytotoxic action [73]. Up to now, there have been few
apparently shown bigger medicinal drug activity than its microparticles studies regarding the cytotoxicity effects of ZnO-NPs on mammalian
but the precise mechanisms of medicinal drug action haven’t been cells and also there is no clear consensus between scientists on the
clearly identified [70]. The ZnO-NPs have germicidal effects on each significance of published results. A study has reported that ZnO-NPs
gram-positive and gram-negative bacterium [71] and also contain have bottom effects on the viability of primary human T cells at
medicinal drug activity against spores that are resistant to high concentrations which have toxic to each gram-negative and gram-
temperature and high pressure. It is evident from the literature that positive microorganism [79]. Different reports have recommended that
the medicinal drug activity of ZnO-NPs depends on extent and these nanoparticles area unit are nontoxic to cultivated human dermal
concentration, whereas the crystalline structure and particle form have fibroblasts; however they exhibit toxicity towards metastatic tumor
very little impact. Therefore the higher concentration and larger the cells [80] and vascular endothelial cells [81] while inducing apoptosis
extent of nanoparticles, the higher will be its medicinal drug activity in neural stem cells. It has been conjointly reported that nanoparticle
[72]. The mechanism of medicinal drug activity of ZnO-NPs continues size can influence cell viability. Jones et al. has discerned in
to not be well understood. Some researchers have suggested in their Staphylococcus aureus that ZnO-NPs that measured eight nm in size
study that the generation of hydrogen peroxide is the main issue of were more toxic than larger zinc oxide particles (50–70 nm) [82].
medicinal drug activity, whereas it is conjointly indicated that the Recently, Hanley et al. has ascertained that there’s an associate degree
binding of particles on the bacterium surface, due to the static forces, inverse relationship between nanoparticle size and toxicity in class
can be another factor [73]. Results have indicated that ZnO-NPs have cells, such as nanoparticle size and reactive oxygen species production
shown antibacterial activity that was apparently greater than micro [83], whereas Deng et al. has demonstrated the toxic effect of ZnO-NPs
particles. The effectiveness of nanoparticles will escalate with increas- on neural stem cells, based on a dose-dependent manner and without

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concerning the size of particles [84]. Table 2

Some drug delivery systems based on the ZnO-NPs.
3.4. Anticancer effects of ZnO-NPs
Materials Drug Cell line References

Cancer nanotechnology is associated in nursing knowledge domain Chitosan/ZnO-NPs DOX – [92]

space of analysis in science, engineering, and drugs with broad ZnO@PMAA-co- DNA COS-7 [94]
PDMAEMA-NPs
applications for molecular imaging, molecular identification, and
Mesoporous ZnO DOX – [95]
targeted medical care. The essential explanation is that nanometer- ZnO – cancerous T, [96]
sized particles, such as semiconductor quantum dots and iron chemical activated human T
compound nanocrystals have optical, magnetic, or structural properties ZnO-NPs PPDME T47D [97]
that don’t seem to be on the market from molecules or bulk solids. ZnO-NPs DOX HeLa [98]
ZnO (Tetrapod) – CHO-K1, HeLa, [99]
Once joined with neoplasm targeting ligands like organism antibodies,
Vero, VK2/E6
peptides, or little molecules, these nanoparticles will be wont to target ZnO/PEG-NPs DOX Gram-positive [100]
neoplasm antigens (biomarkers) as neoplasm vasculatures with high microorganisms
affinity and specificity. Within the mesoscopic size vary of 5–100 nm ZnO@Polymer-NPs DOX U251 [101]
ZnO/Au-NPs Camptothecin Hela [102]
diameter, nanoparticles have massive surface areas and practical teams
ZnO@PNIPAM-NPs DOX – [103]
for conjugating to multiple diagnostic (e.g., optical, radio-isotopic, or ZnO/Carboxymethyl Curcumin L929, MA104 [104]
magnetic) and therapeutic (e.g., anticancer) agents. Recent advances Cellulose (CMC)
have had junction rectifier to bio-affinity nanoparticle probes for ZnO-QDs – HepG2 [105]
molecular and cellular imaging, targeted nanoparticle medicine for Curcumin/O-CMCS/n- Curcumin MA 104 [106]
ZnO
cancer medical care, and integrated nano-devices for early cancer
nanocomposites
detection and screening. These developments raise exciting opportu-
nities for personalized medical specialty in genetic and super-molecule
biomarkers area unit that are wont to diagnose and treat cancer in NPs with chitosan to improve the nanomaterial stability. Their results
supported molecular profiles of individual patients [85]. Some studies indicated that this drug delivery system could be used as an effective
have shown that ZnO-NPs are effective on cancer cells. Premanathan system for targeting doxorubicin to cancer cells [92]. One of other main
et al. has examined the toxicity profiles of human PBMCs and HL60 aspects of NPs application is the utilization of them as vehicles for gene
cells on ZnO-NPs and in result, the cellular response seemed to be delivery to different cells especially tumor cells [3]. The using of this
dynamic and thus the final constitution suffered from a myriad of system for gene delivery is association with various advantages. For
competitor or overlapping signals that were present within the micro- example, the expression of plasmid containing gene on NPs surface
environment. The findings were incontestable since cancerous HL60 could ensure safe and efficient gene targeting to the receipt tissues
cells were highly prone to ZnO-NPs mediate toxicity than the conven- [3,4]. Hence, NPs could be suitable tools for targeting genes to various
tional PBMCs with the therapeutic index (i.e. the quantitative relation cells such as tumor cells.
of hepatotoxic dose to effective dose) [73]. The inability of malignant In a study, Nie and colleagues indicated that ZnO tetrapod-like
neoplasm medicine to effectively distinguish between traditional and nanostructures have been synthesized could be used as novel vehicles
remodeled tissues could be a vital clinical interest and one of the best for gene delivery [93]. They showed that silica-coated amino-modified
challenges in therapy [86]. Although several ordinarily used therapy tetrapod-like ZnO nanostructures enable to effectively bind to DNA via
medicine can target the dividing cells apace, several cases suffer from a electrostatic interactions and it could improve transfection efficiency of
comparatively low therapeutic index [87,88]. melanoma cells [93]. In other study, Zhang et al., revealed that
polycation-capped ZnO quantum dots could deliver DNA into COS-7
3.5. Treat a range of different skin conditions cells [94]. In addition, the utilization of this system enable to real-time
imaging of gene delivery [94]. Various studies used different metal
ZnO is widely wont to treat a range of different skin conditions, in oxide NPs as a suitable vehicle for gene delivery and gene silencing
products similar to powder and barrier creams to treat diaper rashes, (Table 2) [3,4]. Although, it is require to do additional studies in this
hemimorphite cream, anti-dandruff shampoos, and antiseptic oint- field.
ments. Also it is conjointly a part in tape (called “zinc chemical
compound tape”) which is employed by athletes as a bandage to stop
soft tissue injuries throughout workouts [89]. ZnO-NPs may be utilized 3.7. Bio-imaging
in ointments, creams, and lotions for protection against sunburn and
different injury to the skin, caused by ultraviolet illumination. It’s the ZnO is also known as one of well semiconductors, which has good
broadest spectrum UVA and UVB reflector that’s approved to be used potential for replacing the traditional Cd-related species used in the
as a sunblock by the bureau, and is completely photo-stable [90]. When biology and optical landscapes [4,107]. Nowadays, different types of
used as associate degree ingredient in sunblock, zinc oxide blocks every ZnO nanostructures such as NPs, nanotubes, nano-rods, and nano-
UV-A (320–400 nm) and UV-B (280–320 nm) rays of ultraviolet rings have been recognized. The utilization of ZnO-NPs as bio-imaging
illumination. ZnO-NPs is also the most different typical physical is interesting for researchers [4,107]. This property could be used in
sunblock, pigment, area unit which is considered to be nonirritating, various levels and has type of biology and medical applications
nonallergenic, and non-comedogenic [91]. (Table 3). For example, the luminescent ZnO-NPs, which also called
ZnO- QDs, could have good photophysical properties [4,107]. It has
3.6. Drug delivery been shown that the surfaces of these NPs could be modified
conveniently. It has been found that ZnO-NPs could be very stable in
Among of various applications of nanotechnology, drug delivery has aqueous solution and their quantum yield (QY) could be enhanced to
been emerged as a powerful tool in treatment of different diseases such about 30% after carefully modification [3,4,107]. ZnO is known as a
as cancer [3,4]. NPs are one of main systems in drug delivery. Some safe matter generally. ZnO has been utilized in sunscreen products, and
studies used ZnO-NPs for drug delivery in various diseases [3,4]. In a in food packaging is used as a food additive. Hence, the luminescent
study, Yuan et al., used of ZnO quantum dots as a drug delivery system properties of ZnO-NPs, could be used in various biological and medical
for targeting doxorubicin to HeLa cells [92]. They encapsulated ZnO- applications [3,4,107].

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