Comp Rev Food Sci Food Safe - 2021 - Omerovi - Antimicrobial Nanoparticles and Biodegradable Polymer Composites For Active

Received: 20 August 2020 Revised: 25 January 2021 Accepted: 1 February 2021
DOI: 10.1111/1541-4337.12727
COMPREH ENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY
Antimicrobial nanoparticles and biodegradable polymer

composites for active food packaging applications
Nejra Omerović1 Mila Djisalov1 Kristina Živojević1

Minja Mladenović1 Jovana Vunduk2,3 Ivanka Milenković2
Nikola Ž. Knežević1 Ivana Gadjanski1 Jasmina Vidić4
1 BioSense Institute, University of Novi
Sad, Novi Sad, Serbia Abstract

2 Ekofungi Ltd., Belgrade, Serbia The food industry faces numerous challenges to assure provision of tasty and
3Faculty of Agriculture, Institute of Food convenient food that possesses extended shelf life and shows long-term high-
Technology and Biochemistry, University quality preservation. Research and development of antimicrobial materials for
of Belgrade, Belgrade, Serbia
4
food applications have provided active antibacterial packaging technologies that
Micalis Institute, INRAE,
AgroParisTech, Université Paris-Saclay, are able to meet these challenges. Furthermore, consumers expect and demand
Jouy en Josas, France sustainable packaging materials that would reduce environmental problems
associated with plastic waste. In this review, we discuss antimicrobial compos-
Correspondence
Ivana Gadjanski, BioSense Institute, Uni- ite materials for active food packaging applications that combine highly effi-
versity of Novi Sad, Dr Zorana Djindjica 1, cient antibacterial nanoparticles (i.e., metal, metal oxide, mesoporous silica
21000 Novi Sad, Serbia.
Email: [email protected]
and graphene-based nanomaterials) with biodegradable and environmentally
Jasmina Vidic, Micalis Institute, INRAE, friendly green polymers (i.e., gelatin, alginate, cellulose, and chitosan) obtained
AgroParisTech, Université Paris-Saclay, from plants, bacteria, and animals. In addition, innovative syntheses and pro-
78350 Jouy en Josas, France.
Email: [email protected] cessing techniques used to obtain active and safe packaging are showcased.
Implementation of such green active packaging can significantly reduce the risk
Nejra Omerović and Mila Djisalov con-
of foodborne pathogen outbreaks, improve food safety and quality, and minimize
tributed equally to this study.
product losses, while reducing waste and maintaining sustainability.
KEYWORDS
food safety, foodborne pathogens, nanocomposites, nanofillers, shelf life
1 INTRODUCTION
Foodborne diseases are a global public health concern,

Abbreviations: BNP, biodegradable natural polymers; CEO, cinnamon with a burden of 600 million cases per year of illnesses
essential oil; CNT, carbon nanotube; EFSA, European Food Safety
caused by contaminated food and a yearly average of
Agency; FDA, Food and Drug Administration; GO, graphene oxide;
GRAS, generally recognized as safe; MSN, mesoporous silica 420,000 fatalities (WHO, 2015). In the European region,
nanoparticles; MRSA, methicillin-resistant Staphylococcus aureus; the impact of foodborne diseases results each year in 23
MWCNTs, multiwalled carbon nanotubes; NP, nanoparticles; PBS, million people falling ill from unsafe food, leading to 5000
polybutylene succinate; PCL, poly(ε-caprolactone); PFAS, perfluoroalkyl deaths worldwide. Symptoms vary from mild discomfort
substances; PGA, poly(glycolic acid); PHB, poly(hydroxybutyrate);
due to vomiting, fever, and diarrhea, to life-threatening dis-
PHBV, poly(3-hydroxybutyrate-co-3-hydroxyvalerate); PLA, poly(lactic
acid); PLGA, poly(lactide-co-glycolide); PVA, polyvinil alcohol; rGO,
eases. In addition, outbreaks of foodborne diseases also
reduced graphene oxide; ROS, reactive oxygen species; UV, ultraviolet have serious economic implications as they often involve
2428 © 2021 Institute of Food Technologists

R wileyonlinelibrary.com/journal/crf3 Compr Rev Food Sci Food Saf. 2021;20:2428–2454.
NANOCOMPOSITES FOR ACTIVE FOOD PACKAGING. . . 2429
product recalls, damage credibility, and reputation of food food industry for their intrinsic antibacterial activity. The
brands. antimicrobial nanomaterials applied in active packaging
Food packaging is essential in maintaining the safety keep the food safe from harmful and spoilage-causing
and quality of products, from processing and manufac- bacteria (Figure 1), thus enabling longer-term freshness
turing to handling and storage, until the products reach during storage and higher convenience for consumers
the consumers. For a long time, petroleum-based plastic (Hoseinnejad et al., 2018; R. Sharma et al., 2020). Further-
materials (such as polyethylene terephthalate, polypropy- more, the incorporation of active antimicrobial NPs into
lene, and polystyrene) have been used for food packaging the packaging material makes it lighter, stronger and less
to protect the contents from contamination and spoilage permeable to oxygen.
and to facilitate transport and storage (Piergiovanni & Active packaging based on hybrid nano-biocomposites
Limbo, 2016). However, plastic materials cannot fully pro- protects the food, increases its shelf life, and reduces
tect the food from the environment and, thus, cannot com- the use of traditional plastics. This review provides an
pletely ensure product quality and safety. Importantly, syn- overview of the most recent studies on the development
thetic non-biodegradable plastics have led to serious eco- of nanomaterial-enabled active packaging for food with a
logical problems due to environmental pollution by micro- particular focus on nanofillers with antimicrobial activity
and nanoplastic debris, triggering the development of new and different types of biodegradable polymers. Addition-
biodegradable and less toxic biomaterials as alternatives. ally, the mode of antibacterial action, cytotoxicity, and leg-
In addition, novel active nanomaterial-based agents are islation for the safety of nanomaterials for active packaging
being incorporated into the packaging to further improve are discussed.
the ability of eco-friendly biopolymer films to protect food
products from light, moisture, oxygen and other environ-
mental factors that cause food degradation. 2 BIODEGRADABLE POLYMERS
Active packaging ensures the quality and safety of the
food product through the interaction between the pack- Nondegradable plastic persists in the environment and
aging film, foodstuffs, and internal and external environ- may interfere with the homeostasis of the ecosystems and
ments (Realini & Marcos, 2014). The technology refers exert toxic effects on human and animal health. Plastics are
to the incorporation of active compounds into packaging estimated to make up about 10% of global waste with about
film. The antibacterial active packaging is a version of 70% of marine litter objects being single-use plastic prod-
active packaging that contains antimicrobial agents that ucts like straws or food and drink containers (Barnes, Gal-
can interact with the headspace and packaged food with gani, Thompson, & Barlaz, 2009), and are even predicted
the aim to prevent bacterial contamination. The European to dramatically increase over the next decade, if the cur-
Regulation (EC) No. 450/2009 defines active packaging rent trends continue (Harrison et al., 2018). Due to the very
as systems that “deliberately incorporate components that slow degradation, the conventional petroleum-based poly-
would release or absorb substances into or from the pack- mers entering the environment undergo mechanical frag-
aged food or the environment surrounding the food” and mentation and become micro- and nanoplastics of <5 mm
intelligent packaging as “Intelligent food contact materi- and <100 nm size range, respectively. The microplastics-
als, which monitor the condition of packaged food or the associated microbial biofilms (so-called “plastisphere”) are
surrounding environment, for instance, by providing infor- a particular concern because the plastisphere microorgan-
mation on the freshness of the food” (European Commis- isms can serve as transport systems for pathogens and can
sion, 2009). In this way, antibacterial packaging functions change the particle buoyancy as well as the degradation
by releasing the active agents onto the foodstuff or into rate of the plastic polymers, affecting the general distri-
the surrounding atmosphere and inhibits the growth phase bution and fate of the plastic pollutants (Oberbeckmann
of microorganisms present on the surface of the packaged et al., 2015).
food (Drago et al., 2020). Furthermore, the improved stor- The genotoxicity and cytotoxicity of such small plas-
age conditions may extend food shelf life and freshness and tic particles have been documented in fish and mussels
preserve food quality and safety. (Oliveira et al., 2019) and concerns about their detrimental
The unique properties of nanostructures and nanoma- effects on human health have been raised (da Costa et al.,
terials, such as their small size, high surface-to-volume 2016; Fadare et al., 2020; Revel et al., 2018), urging the sci-
ratio, and quantum effects, make them suitable for diverse entific and policy making communities to harness all the
applications in the food industry. In particular, metal and available resources in order to further investigate and ulti-
metal oxide nanoparticles (NPs; such as Ag, ZnO, Cu/CuO, mately diminish the negative effects of plastics on human
TiO2 , and MgO NPs), mesoporous particles, graphene, health and the environment (Stojkovic et al., 2020). More-
and carbon dots have attracted remarkable interest in the over, some additives, such as bisphenol A (Cooper, Kendig,
2430 NANOCOMPOSITES FOR ACTIVE FOOD PACKAGING. . .
FIGURE 1 Active packaging fundamentals: composition of nanoparticle–biopolymer composites and their beneficial effects in food
preservation
& Belcher, 2011), polybrominated diphenyl ethers, phtha- ical oxidation are not effective for PFOA and PFOS removal
lates, or perfluoroalkyl substances (PFAS), which have (Vecitis et al., 2010).
been used for a long time in the food industry as moisture To diminish the use of PFAS and other compounds that
and oil penetration barriers can be classified as carcino- prove to be difficult to remediate, a number of new tech-
genic or endocrine disrupting (Llorca, Schirinzi, Martínez, nologies have been explored aiming to develop novel more
Barceló, & Farré, 2018; Thurber & Curtzwiler, 2020). There sustainable food packaging materials that are, in the same
was particular attention on the sulfonate and carboxy- time, able to meet company’s and consumer’s expecta-
late PFAS forms such as perfluorooctane sulfonate (PFOS) tions. To endorse a common circular economy vision in
and perfluorooctanoic acid (PFOA; Kucharzyk et al., 2017). which by 2025 all plastic packaging will be reusable, recy-
Both PFOA and PFOS have high chemical and thermal clable, or compostable, more than 500 businesses, govern-
stability rendering them very difficult to remove from the ments, and other organizations have signed the New Plas-
environment (Rahman et al., 2014). Many conventional tics Economy Global Commitment (Global Commitment,
methods of remediation, such as air stripping, thermal 2020). Already more than 170 countries have banned six
treatment, soil vapor extraction, and hydroxyl-based chem- single-use plastic items including food containers, straws,
plastic grocery bags, and six-pack rings that are hard to addition, the incorporation of quaternary ammonium salts
recycle and often found in the environment. Naturally into the backbone of PCL led toward efficient contact-
sourced biopolymers are the first choice when attempting killing activity against Escherichia coli and Bacillus sub-
to achieve a less toxic and more sustainable food packag- tilis, with enhanced degradability (Bakhshi & Agarwal,
ing because of their biocompatibility, biodegradability, and 2017). Polyvinyl alcohol (PVA) film shows an advantage
nontoxicity (Popović et al., 2018; Spasojević et al., 2019). compared to other synthetic polymers because it can
Biodegradable natural polymers (BNP) are biopolymers be reusable. Another example is kraft paper that is an
derived from biomass and other agro-resources. They are a extensively used material for food packaging due to its
chemically diverse category, comprising polysaccharides, biodegradability and safety. However, it can lose its proper-
proteins of animal or plant origin, lipids, and polyesters ties upon absorbing water when it becomes a good support
from microbial sources. Examples of different BNP cat- for the growth of microorganisms.
egories used as packaging materials are presented in To improve the flexibility and extensibility and even
Table 1. moisture-sensitivity of the packaging film, plasticizers
The most commonly used BNP for producing packag- are mixed with degradable polymers, such as glycerol,
ing are proteins and polysaccharides and their derivatives polyethylene glycol, sorbitol, propylene glycol, ethylene
because they are widely available and can polymerize into glycol, lipids (Haq et al., 2014). Lipids can improve the film
brittle and rigid materials. Casting method is the most fre- barrier properties to the water vapor. In such packaging
quently used method for the preparation of films based on films, lipids may form a protective emulsion layer or may
polysaccharides and proteins. It includes two main steps: be in a separate layer within a multilayered composite film
dissolution or dispersion of biopolymers in suitable sol- (Chiumarelli & Hubinger, 2014). However, the plasticizers
vents, and evaporation of solution under ambient con- can exert certain negative effects such as modification of
ditions or in a controlled relative humidity environment the food aroma or increased oxygen permeability of the
(L.-F. Wang et al., 2016). Some other conventional meth- films.
ods that include extrusion, compression, and injection
molding of biopolymers are performed as dry processes.
Although these methods require precisely defined parame- 3 NANOFILLERS
ters (pressure, temperature, shear impact) and more equip-
ment compared to the casting method, they can be easily Rapid developments in the nanotechnology field in the
adapted for industrial implementation (Park et al., 2014). past several years are expected to bring significant ben-
Polysaccharide- and protein-based films show good bar- efits to the food and food-related industries through the
rier properties to gases, low- to medium-relative humid- whole food chain, including packaging, transportation,
ity, moderate mechanical properties, but are poor barriers storage, and delivery. The European Commission’s defi-
against water vapor due to their hydrophilic nature. The nition for identifying nanomaterial states that a material
major limiting factor for direct application of BNP-based is to be considered a nanomaterial if half or more of the
films in food packaging systems is their high sensitivity to total number of particles in a material have one or more of
moisture. their external dimensions between 1 and 100 nm (Löves-
Biodegradable synthetic polymers exert an array of tam et al., 2010). Biopolymer–nanocomposites display
physicochemical and mechanical characteristics that ren- decreased gas and moisture permeability and increased
der them suitable for packaging applications. Biodegra- mechanical strength in comparison to the pure polymers
dation of these synthetic materials is typically achieved or microscopic composites. Nanofillers can be classified
through their slow chemical hydrolysis in an aqueous into: nanoplatelets, nanofibers, and NPs, having one, two,
environment that can be improved by enzymatic catal- or three nanoscale dimensions, respectively. Nanofillers
ysis (Zhong et al., 2020). Poly(α-hydroxyester)s, such as may also provide antibacterial activity. Figure 2 illustrates
poly(glycolic acid) (PGA), poly(lactic acid) (PLA), and some antibacterial mechanisms of nanomaterials used in
their co-polymers poly(lactide-co-glycolide) (PLGA), are the development of active packaging. Some recent works
being extensively reported for antimicrobial packaging employing different nanofillers are summarized in Table 2.
applications (Biswal et al., 2020; Holman et al., 2018; Lyu Nanofillers may be used in two different concepts of con-
et al., 2019; Radusin et al., 2019; Rao et al., 2016). Poly- ceiving food packaging. When integrated into active pack-
meric nanocapsules based on poly(ε-caprolactone) (PCL) aging, nanofillers act on the headspace or directly on food
were also reported for encapsulation of Thymus capita- to increase the shelf-life. However, within the intelligent
tus and Origanum vulgare essential oils, showing higher packaging nanofillers do not have any action on food, but
activity against foodborne pathogens than that of the cor- monitor the condition of the packaged product and share
responding pure essential oils (Granata et al., 2018). In the information. The packaging that combines intelligent
2432
TA B L E 1 Natural and synthetic biopolymers used to produce film for food packaging
Biopolymer Source for production Properties References
Natural biopolymers—Carbohydrates
Starch Corn, potato, wheat, cassava, rice Widely available and inexpensive polysaccharide, compatible with (Chakravartula et al., 2020)
antioxidants and antimicrobial agents, good film-forming and
gas barrier properties, hydrophilic behavior, low water vapor
barrier, poor mechanical properties
Cellulose Agricultural waste (corn stalks, The most abundant natural polymer; tasteless and odorless, highly (Hassan et al., 2018; C. Wu et al.,
rice straw, sugarcane bagasse), crystalline, fibrous and insoluble, thermally and chemically 2019)
woody plants stable, inherent antimicrobial properties
Chitosan Alkaline deacetylation of chitin; Good film-forming ability with moderate mechanical strength, (Akhter et al., 2019;
exoskeletons of crustaceans inherent antimicrobial activity, compatible with many other Chakravartula et al., 2020;
(crab, shrimp, crawfish) biopolymers, high water sensitivity (solubility issue), low barrier Fernandez-Saiz, 2011)
properties
Alginate Brown seaweeds of Phaephyceae Ability to react with di-valent and trivalent cations, gel and (de Oliveira Filho et al., 2019;
class film-forming ability Hassan et al., 2018; Munteanu
& Vasile, 2020)
Agar Red seaweeds of Rhodophyceae Ability to form strong gels and gums, films are transparent, (Mostafavi & Zaeim, 2020)
class (Gelidium sp. and heat-sealable, biologically inert, brittle, thermally unstable,
Gracilaria sp.) water sensitive (high water vapor permeability)
Carrageenan Chondrus crispus and other Water-soluble, forms pseudoplastic gels, κ-carrageenan has the (Roy et al., 2019)
species of red seaweeds best film-forming ability
Natural biopolymers—Proteins
Soy protein Soybeans, soy flakes Insoluble in water, soluble in acid or alkaline medium, flexible (Emiroğlu et al., 2010; Z. Yu,
films with remarkable gas barrier properties, acidic films display Dhital, et al., 2019)
better antimicrobial activity but weaker mechanical properties
than films prepared in alkaline medium
Zein Corn protein—major coproduct Good film-forming properties, god barrier properties, high (Spasojević et al., 2019;
of oil and bioethanol industries compatibility with biopreservatives, ability to form blends with Yemenicioğlu, 2016)
lipids and fatty acids, insolubility in water, brittleness, problems
with mass production
(Continues)
NANOCOMPOSITES FOR ACTIVE FOOD PACKAGING. . .
TA B L E 1 (Continued)
Biopolymer Source for production Properties References
Wheat gluten Wheat flour Hydrophobic nature, insoluble in water, can be dissolved in (Kurek et al., 2014)
aqueous solutions of high or low pH at low ionic strength, Films
are clear with shiny surface and show good resistance to water
Gelatin Partial hydrolysis of collagen; pig Good gas barrier property, light absorption, high moisture (Kadam et al., 2015; S. Shankar
skin, bovine hide, pork and sensitivity, low mechanical strength, low process ability et al., 2016)
cattle bones, fish skin
NANOCOMPOSITES FOR ACTIVE FOOD PACKAGING. . .
Collagen Pork and cattle bone, pig skin, The most exploited raw material for biopolymer packaging, flexible (Popović et al., 2018)
fish skin polymer with complex structure, films display excellent oxygen
barrier at 0% RH, barrier decreases with increase of RH
Whey protein Milk—coproduct of cheese Transparent, odorless, and tasteless films with high moisture (del Carmen Beristain-Bauza
production (remain after the sensitivity (water solubility) and good barrier properties to et al., 2017)
coagulation of caseinate) oxygen and lipids
Casein Skim milk Films obtained from aqueous solutions, opaque films with (Ponce et al., 2016)
excellent sensory properties, high water vapor permeability
Chemically synthesized biopolymers
PLA Large availability, high transparency, processability and rate of (Radusin et al., 2019; Requena
composability, brittleness and low thermal and gas barrier et al., 2018)
properties
PCL Hydrophobic and semicrystalline polyester, films display low (Ahmed et al., 2019)
tensile strength and high elongation at break
PBS High processability, low mechanical strength, and microbial (Petchwattana et al., 2016)
corrosion
PVA Excellent physical and optical properties, excellent film-forming, (de Oliveira et al., 2020;
emulsifying, and adhesive properties, low barrier performance, Jayakumar et al., 2019; Qin
low biodegradation rate, high production costs et al., 2020)
Note: Studies presented are from the past 10 years.
2433
FIGURE 2 Various antibacterial mechanisms of nanoparticles used as inforcers in food packaging
and active components is smart packaging (Drago et al., hyperproduction of one or several ROS can be induced by
2020; Vanderroost et al., 2014). different NPs. For instance, CaO and MgO NPs generate
superoxide radicals, ZnO NPs mainly generate hydrogen
peroxide, whereas CuO NPs can produce all those ROS.
3.1 Metal and metal oxide NPs as The formation of hydrogen peroxide and hydroxyl radicals
antibacterial nanofillers occurs with Ag NPs (Dakal et al., 2016; Durán et al., 2016).
Increased ROS production leads to oxidative stress, impair-
Metal and metal-oxide NPs exhibit different antibacterial ment of biomolecules and membrane integrity, enzyme
efficiencies toward Gram-positive and Gram-negative bac- inhibition, and nucleic acid damage. ROS can also form
teria, and may even have different effects on the bac- holes within the bacterial membrane, causing the contents
terial strains within the same Gram-positive or Gram- of the cell to leak (Gold et al., 2018).
negative group (Auger et al., 2018; Cavassin et al., 2015;
Zanet et al., 2019). This effect originates probably from
the presence of various membrane components in differ- 3.1.1 Silver NP-biopolymers
ent bacteria that are the first barrier and the first target
for NPs. For instance, lipoproteins and phospholipids are Ag NPs are the most commonly used nanofiller to endow
found on the surface of Gram-negative bacteria, while the the composite films with antimicrobial properties (Shiv
surface of Gram-positive bacteria contains abundant pores Shankar & Rhim, 2015; Suppakul et al., 2003). The US Food
and is of a much higher negative surface charge (Sánchez- and Drug Administration (FDA) authorized direct addi-
López et al., 2020; L. Wang et al., 2017). Reactive oxy- tion of Ag salts up to 17 µg/kg as a disinfectant in bottled
gen species (ROS)-induced oxidative stress is one of the water (Duncan, 2011). The antibacterial effect of Ag NPs
most prominent mechanisms associated with the antimi- is achieved through the adhesion of Ag NPs to the bac-
crobial action of metal- and metal oxide NPs. Four types terial membrane and/or penetration inside bacterial cells.
of ROS are mostly produced: superoxide radical, hydrox- Ag NPs may interact with membrane lipids or with DNA
ide radical, hydrogen peroxide, and singlet oxygen. The and proteins inside the cells (Yun’an Qing et al., 2018). Ag
TA B L E 2 Examples of active packaging containing nanofillers

Composites Antimicrobial activity
Nanoparticle Biopolymer toward: Application References
Ag Nanostructured starch S. aureus, E. coli, and C. Active food packaging (Abreu et al., 2015)
albicans
Ag PVA S. aureus and E. coli Active food packaging (Sarwar et al., 2018)
Ag Chitosan E. coli, S. aureus, A. niger, Active food packaging for (Wu et al., 2018)
and P. citrinum litchi fruits
Ag Cellulose nanofibrils E. coli and L. Active food packaging (Z. Yu, Wang, et al.,
monocytogenes 2019)
Ag Agar E. coli and L. UV-screening and active (Shiv Shankar &
monocytogenes food packaging Rhim, 2015)
Ag PVA S. Typhimurium and S. Active food packaging for (Mathew et al.,
aureus chicken meat 2019)
Ag Carrageenan E. coli and L. Active food packaging (Roy et al., 2019)
monocytogenes
Ag Chitosan E. coli, Salmonella, S. Active and intelligent food (Qin et al., 2019)
aureus, and L. packaging
monocytogenes
Au cellulose/keratin S. aureus (MRSA) and Active food packaging (Tran et al., 2018)
Enterococcus (VRE)
Au PVA E. coli Active food packaging for (Chowdhury et al.,
banana 2020)
Au–Ag Cellulose E. coli Active food packaging (Tsai et al., 2017)
Ag–Cu Agar L. monocytogenes and S. UV-screening and active (Arfat, Ahmed, &
Typhimurium food packaging Jacob, 2017)
Ag–Cu Fish skin gelatin L. monocytogenes and S. UV-screening and active (Arfat et al., 2017)
Typhimurium food packaging
Ag-Cu PLA S. Typhimurium, L. UV-screening and active (Ahmed et al., 2018)
monocytogenes, and C. food packaging for
jejuni chicken meat
Se–Ag Gelatin/furcellaran E. coli, S. aureus, and S. Active food packaging for (Jamróz et al., 2019)
aureus kiwi fruits
CuS Agar E. coli and L. Active food packaging (Roy & Rhim, 2020)
monocytogenes
S Chitosan E. coli and L. Active food packaging (Shiv Shankar &
monocytogenes Rhim, 2018)
Nanocellulose Chitosan S. aureus, E. coli, and S. Active food packaging for (Dehnad et al.,
enteritidis ground meat 2014)
Nanocellulose Bagasse paper B. cereus, E. coli, P. Paper-based active food (El-Samahy et al.,
aeruginosa, S. packaging 2017)
Typhimurium, and S.
aureus
CuO Agar, alginate, L. monocytogenes and E. UV-screening and active (Shiv Shankar et al.,
carrageenan, chitosan, coli (O157:H7) food packaging 2017)
and CMC
ZnO Ethyl cellulose/gelatin E. coli and S. aureus Active food packaging (Yuyu Liu et al.,
nanofibers 2018)
ZnO Corn starch, E. coli Green-based active food (Ni et al., 2018)
Guanidine-based packaging
starch
ZnO Soy protein isolate A. niger Active food packaging (J. Wu et al., 2019)
(Continues)
TA B L E 2 (Continued)
Composites Antimicrobial activity
Nanoparticle Biopolymer toward: Application References
TiO2 Wheat gluten and S. cerevisiae, E. coli, and S. Active food packaging (El-Wakil et al.,
cellulose nanocrystals aureus 2015)
TiO2 Whey protein isolate Pseudomonas spp., Active food packaging for (Sani et al., 2017)
/cellulose nanofiber Enterobacteriaceae, meat preservation
lactic bacteria, S. aureus,
L. monocytogenes, and
E. coli
TiO2 Zein/sodium alginate S. aureus and E. coli Active packaging for meat, (Amjadi et al., 2020)
cheese, nuts, cereal
ZnO PBS E. coli and S. aureus Active food packaging (Petchwattana
et al., 2016)
ZnO Polylactide/polyethylene S. aureus and E. coli Active food packaging for (Ahmed et al., 2019)
glycol/ eggs
polycaprolactone
MgO PLA E. coli UV-screening and active (Swaroop & Shukla,
food packaging 2018)
Zn-MgO Alginate L. monocytogenes Active food packaging for (Vizzini et al., 2020)
smoked salmon meat
TiO2 Chitosan/PVA S. aureus, P. aeruginosa, E. Active food packaging for (Youssef et al., 2015)
coli (O157:H7), and soft white cheese
Candida albicans
Carbon dots Bacterial nanocellulose L. monocytogenes and E. UV-screening and (Kousheh et al.,
coli forgery-proof packaging 2020)
Iron-oxide Chitosan hydrogel MRSA, S. aureus, E. coli, Biomedical and active (Konwar et al.,
coated GO and C. albicans food packaging 2016)
applications
MWCNTs Chitosan/PLA E. coli, S. aureus, B. Active food packaging for (Yaowen Liu et al.,
cinerea, and Rhizopus fruit and vegetable 2019)
SiO2 (silica) Chitosan E. coli, S. Typhimurium, S. Active food packaging (Bi et al., 2020)
aureus, L.
monocytogenes
MSN (SBA-15) Chitosan S. aureus, E. coli Active food packaging (C. Wu et al., 2019)
MSN Potato starch Mucor sp., Mucor Active food packaging for (Zhang et al., 2019)
circinelloides mushrooms
MSN and Bitter vetch proteins Micrococcus luteus Active food packaging (Fernandez-Bats
amino-MSN et al., 2018)
SiO2 and SiO2 Polyhydroxy E. coli (O157:H7) and S. Active food packaging and (Lin et al., 2018)
-HDTMS/SPH butyrate/poly-ɛ- aureus biomedical materials
caprolactone
MSN (MCM-41) PHBV S. aureus and E. coli Interlayers or coatings for (Melendez-
active food packaging Rodriguez et al.,
2019)
Note: Studies presented are from the past 10 years.
NPs were also shown to downregulate the expression of generate a high concentration of ROS and interact with
antioxidant enzymes such as glutathione, superoxide dis- bacterial proteins from the respiratory chain causing cell
mutase, and catalase depriving the bacterial cell of defense death (Long et al., 2017). Unfortunately, Ag NPs may also
against oxidative stress (Yuan et al., 2017). Another mode kill human cells as shown in vitro (Carrola et al., 2016;
of action involves the release of highly toxic silver ions that Jiang et al., 2018; Kim & Shin, 2014; L. Li et al., 2018; Sabella
bind protein sulfhydryl groups or intercalate within the et al., 2014). In active packaging, Ag NPs are immobilized
DNA chain. Moreover, Ag+ -ions released by Ag NPs can into polymeric materials, which allows controlled release
of Ag+ -ions suppressing in this way their cytotoxicity. The factor in reducing the water vapor permeability, oxygen
migration of silver from the packaging film to food may transmission rate, solubility, swelling of the films, and in
occur through the detachment of Ag NPs from the com- increasing the film’s antimicrobial activity against E. coli,
posites or the oxidative dissolution of silver ions. It was S. aureus, Aspergillus niger, and Penicillium citrinum. The
shown that the highest level of silver migrating from var- film enabled to extend the shelf life of litchi fruit from 4
ious nanocomposites into food simulants occurred with to 7 days. Melanin, as a reducing agent, enables green syn-
acidic food (Echegoyen & Nerín, 2013). Moreover, food thesis and capping of Ag NPs within the carrageenan film
heating, and especially microwave heating, induces migra- (Roy et al., 2019). In addition, melanin, as a well-known
tion of toxic Ag/Ag+ from the packaging film to the food- ultraviolet (UV)-blocking agent, enhanced the UV-barrier
stuff. Cushen et al. (2014) developed a model of Ag NPs property of the films. Finally, carrageenan/Ag NPs packag-
migration from food packaging. Using modeling to predict ing film notably reduced the growth of E. coli and L. mono-
the level of migration of Ag NPs is highly beneficial to the cytogenes.
industry because it could reduce time and costs usually In the polymer industry, enormous efforts have been
associated with the migration studies. made to produce environmentally friendly materials for
The addition of Ag NPs may also improve the mechan- food packaging. Biodegradability of PVA-based nanocom-
ical properties of packaging films. Abreu et al. (2015) posites can be improved through the green synthesis
applied a solution casting method to prepare nanos- method using a natural extract as a plasticizer. Mathew
tructured starch films containing organically modified et al. (2019) applied ginger extract having a reductant activ-
nanoclay and Ag NPs. They demonstrated that Ag NPs ity to improve the plasticity of PVA and to partake in
improved the clay dispersion, contributing to higher the in situ synthesis of Ag NPs. This nanocomposite was
homogeneity of films and improving their mechanical degraded entirely under simulated environmental condi-
properties. The presence of Ag NPs reduced water vapor tions after 100 days. In addition, the mechanical strength of
and oxygen permeability, providing excellent barrier prop- the prepared films was greatly enhanced, suggesting high
erties. Moreover, the nanocomposite showed antimicrobial compatibility between the nanofillers and PVA. The pre-
activity against Staphylococcus aureus, E. coli, and Candida pared films show superior inhibition on S. Typhimurium
albicans. A composite film prepared of cellulose nanofib- and S. aureus growth. Qin et al. (2019) developed a chi-
rils impregnated with Ag NPs through casting and evapo- tosan bio-nanocomposite with potential for use in active
rating at room temperature showed strong inhibition effec- food packaging. Multifunctionality was enabled via incor-
tiveness against E. coli and Listeria monocytogenes and no poration of Ag NPs, acting as antimicrobial agents, and
significant cytotoxicity to human epithelial cell or colon anthocyanin-rich purple corn extract, functioning as an
cell lines (Z. Yu et al., 2019). Similarly, PVA packaging film antioxidant and pH indicator (Figure 3). Silver NPs, pro-
reinforced with nanocellulose and starch-capped Ag NPs duced through the green synthesis, and oxygen groups of
showed no cytotoxic effect on the hepatocyte function (Sar- chitosan interact through coordination providing a strong
war et al., 2018). The authors suggested that starch served synergic effect that decreased UV-vis light transmission,
as a protective layer that prevented the undesired release water vapor permeability, and the moisture content of the
of silver ions from capped NPs. Besides contributing to film. Improvement of tensile strength was ascribed to the
antimicrobial properties of films that efficiently inhibited reduction of the mobility of polymer chains and flexibility
the growth of E. coli and S. aureus, Ag NPs in a PVA film of the matrix, caused by Ag NPs embedding into the chi-
enhanced its thermal stability and mechanical properties, tosan films. Films showed color changes at pH 3 to 10 due
such as breaking stress and elongation at break. Moreover, to the structural transformations of anthocyanin, the phe-
the PVA/AgNPs film had low water vapor permeability and nomenon that could be utilized for food freshness moni-
high moisture retention due to glycerol hydroxyl groups’ toring (Qin et al., 2019).
affinity toward water molecules (Sarwar et al., 2018). Ag NPs are also used in combination with other NPs to
A green synthesis method is generally used for preparing further improve packaging film characteristics. The syner-
Ag NPs for food packaging applications. Wu et al. (2018) gism was observed between selenium and silver NPs where
synthesized laponite-immobilized silver NPs by reactive selenium NPs enhance water resistance and antimicrobial
template grain growth method using quaternized chitosan activity, while Ag NPs improve the mechanical properties
as a green reducing agent and stabilizer. Prepared Ag NPs of furcellaran/gelatin films (Jamróz et al., 2018, 2019).
and laponite improved chitosan films for the wrapping Such films were tested for the preservation of kiwi fruit.
of litchi fruits, by increasing the film density, improv- The addition of Se-AgNPs into furcellaran/gelatin matrix
ing its mechanical properties and making it more uni- resulted in denser and more compact films, which were
form and homogenous. The tripartite interactions between less soluble in water. The kiwi fruits had shelf life
NPs, chitosan, and laponite were proposed as a crucial prolongation of 2 days when protected with
F I G U R E 3 Active packaging obtained by incorporation of silver nanoparticles and purple corn extract (PCE) into chitosan films
improved the physical properties of chitosan films and increased antioxidant and antimicrobial properties
Note: Illustration adapted from Qin et al. (2019).
furcellaran/gelatin/Se-AgNPs film, which was attributed Au NP is a promising enhancer because of its safety and
to the antimicrobial effectiveness of incorporated NPs. the simple method of post-deposition onto the cellulose
paper. Au NPs may also enhance the silver coating of a
cellulose film (Tsai et al., 2017). Excellent antibacterial
3.1.2 Gold NP-biopolymers activity of the silver coated cellulose paper was enhanced
by Au NPs against E. coli (Tsai et al., 2017). An in vitro
An antibacterial packaging incorporating gold NPs was size-dependent cytotoxicity study suggested that Au NPs
also elaborated. In contrast to most antibacterial nanoma- of a diameter ≥ 15 nm can be considered harmless, while
terials that generate cytotoxic ROS, the gold NPs kill the smaller ones may cause mammalian cell necrosis (Yah,
bacterial cells via ROS-independent mechanisms. Further- 2013).
more, the antibacterial action of Au NPs was shown to
largely depend on particle size, functionalization, and the
bacterial strain to which they are applied (Ortiz-Benítez 3.1.3 Copper and copper oxide NPs
et al., 2019). Nano-gold particles either bind to the bacterial
membrane and change its potential or internalize into the Copper oxide NPs (CuO NPs) were demonstrated to rein-
cells where they decrease adenosine triphosphate levels or force mechanical (such as tensile strength and elastic mod-
inhibit tRNA binding to the ribosome (Cui et al., 2012). ulus) and antibacterial properties of carbohydrate poly-
In contact with E. coli and S. aureus, Au NPs were shown mers. The effect of CuO NPs addition to carbohydrate
to damage bacterial membrane (Badwaik et al., 2012; Rai biopolymers was tested using agar, alginate, carrageenan,
et al., 2010). chitosan, and carboxymethyl cellulose (Shiv Shankar et al.,
When PVA films were cross-linked with glyoxal and 2017). All obtained CuO NP–composite films showed
reinforced with Au NPs as nanofillers, the composites had homogeneous, uniform, compact, and smooth surface
improved hydrophobicity, mechanical and barrier proper- structure except the agar/CuO NP—nanocomposite film
ties (Chowdhury et al., 2020). Intermolecular cross-linking that exhibited agglomerates and clusters of CuO NPs.
contributed towards formation of a packed pores structure Only agar/CuO nanocomposite films did not show antimi-
that decreased water vapor transmission rate and increased crobial activity indicating that the available surface area
water and thermal stability of the film. The nanocompos- of the NPs was low. Interestingly, incorporation of Cu
ite showed effective antimicrobial activity against E. coli NPs into the agar polymer, did not significantly improve
because Au NPs created holes in the cell walls and inac- the mechanical properties nor the thickness of the
tivated bacterial enzymes through blocking of their thiol films.
groups. The material demonstrated superior capability for CuNPs in active packaging were also used in combi-
the preservation of wrapped organic bananas compared to nation with AgNPs to obtain the synergic effect of two
PVA film cross-linked with glutaraldehyde and graphene metals. Ahmed et al. (2018) prepared a PLA nanocompos-
oxide (GO; Figure 4). ite loaded with bimetal Ag-CuNPs and cinnamon essential
F I G U R E 4 The structure of PVA-based composite films containing gold nanoparticles (AuNPs), glutaraldehyde (GA) as a cross linking
agent and graphene oxide (GO), representation of their antimicrobial mechanisms and application for extending shelf life of fruits.
Illustration adapted from (Chowdhury et al., 2020).
oil (CEO) through the compression molding process. The were all shown to be dependent on the concentration of
obtained Ag-CuNPs/PLA films had improved barrier prop- NPs.
erties, a decreased light transmittance, modified morphol- Cu/CuO NPs in active films inhibit bacterial growth by
ogy, and thermal stability compared to the pure PLA films. producing highly toxic ROS or releasing Cu2+ -ions. Cu NPs
Storage tests demonstrated that such films became more accumulate on the bacterial membrane, decrease trans-
rigid over time due to the evaporation of the CEO. The membrane electrochemical potential, and disrupt bacterial
antimicrobial effectiveness of films was confirmed against cell wall (Din et al., 2017). The ruptured bacterial mem-
Salmonella Typhimurium, L. monocytogenes, and Campy- brane facilitates entry of the NPs into the cell, but also
lobacter jejuni in chicken meat as a model food system, induces leakage of the cell content into the extracellu-
during 21 days of refrigeration. The antimicrobial activity lar space. Released Cu2+ -ions induce ROS-induced oxida-
decreases after 150 days of storage at 4 ◦ C, because of the tive stress, which produces oxidative damage to DNA and
loss of the CEO component that restricts the release of NPs. proteins. In addition, Cu2+ can interact directly with the
The bimetallic Ag-Cu NPs incorporated into agar-based bacterial proteins and denature them. Cu2+ is estimated
film via a solution casting method and plasticized with to interact with sulfhydryl groups that are necessary for
glycerol showed also a high antimicrobial activity (Arfat the activity of many essential enzymes, like phosphatases
et al., 2017). The thickness of the film, its tensile strength, and kinases (Makvandi, Wang, et al., 2020). Similar toxic
thermal stability, oxygen-barrier, and light transmittance mechanisms of Cu/CuO NPs toward human cells were
also shown (Katsumiti et al., 2018). Practical applications isolate/cellulose nanofiber nanocomposite with TiO2 NPs
of Cu/CuO NP-biopolymer composites strongly depend and rosemary essential oil demonstrated antimicrobial
on the stabilization of NPs within films that control the activity against Pseudomonas spp., Enterobacteriaceae, S.
release of Cu2+ -ions thus preventing cytotoxicity to human aureus, L. monocytogenes, E. coli, and lactic bacteria, in
cells. inoculated lamb meat (Sani et al., 2017). The shelf-life of
meat samples packed with this biodegradable film was
extended up to 6 days compared to controls. Besides ensur-
3.1.4 Titanium dioxide NPs ing the microbial quality of food, the TiO2 -biopolymer
composite preserved the sensory quality of the meat
TiO2 particles are commonly used as a food additive to samples.
provide a whitening effect that makes the foodstuffs look Recently, novel zein/sodium/TiO2 NPs-alginate nano-
brighter and more appealing (Ropers et al., 2017). In food biocomposite fibers for food packaging applications were
packaging, TiO2 NPs are used for their wide range of obtained using the electrospinning technique (Amjadi
antimicrobial properties (Makvandi, Gu, et al., 2020; Stan- et al., 2020). Even though the pure zein polymer is flexible,
kic et al., 2016). Until recently, TiO2 NPs were consid- tough, compressible, hydrophobic, and safe, it has weak
ered as safe. However, the European Food Safety Agency mechanical properties. Carbohydrates were added to rein-
(EFSA) revealed some concerns due to the ability of TiO2 force the mechanical properties of zein fibers while sodium
NPs to alter the intestinal barrier, which pushed some EU alginate facilitated its electrospinning and the addition of
countries to ban TiO2 NPs in food (Boutillier et al., 2020). TiO2 NPs improved mechanical and thermal properties as
Numerous reports confirmed the toxic effects of TiO2 NPs well as gas and water barrier properties and provided high
on human cells (Acar et al., 2015; Coccini et al., 2015; antibacterial activity. The antibacterial activity against S.
Radziwill-Bienkowska et al., 2018). In vivo tests revealed aureus and E. coli was even further enhanced by incor-
that upon inhalation or oral exposure, TiO2 NPs accumu- porating natural pigments, such as betanin. The obtained
late in lungs, digestive tract, liver, heart, spleen, kidneys, nano-biocomposite complex showed good biocompatibil-
and heart (Baranowska-Wójcik et al., 2020; Shukla et al., ity and homogeneous morphology despite its multicompo-
2013; Song et al., 2016). However, nanosized TiO2 is still nent structure. TiO2 improved the properties of the fabri-
among the few approved nanomaterials used by the food cated nanofibers by forming hydrogen bonds with zein and
industry. producing highly regular and compact polymer chains.
The main mechanism of antimicrobial activity of TiO2 Fresh white cheese prepared from buffalo milk is char-
NPs involves ROS production under exposure to UV light acterized by rapid spoilage under aerobic conditions. It
(Makvandi, Wang, et al., 2020). This photocatalytic mech- deteriorates usually in less than 7 days when packed
anism involves: (i) electron–hole pairs production and using traditional petrochemical plastics. To provide pro-
migration to the TiO2 NP surface, (ii) interaction of photo- longed storage and shelf life of buffalo milk cheese
generated holes with adsorbed H2 O/OH– leading to the a chitosan/PVA/TiO2 NPs nanocomposite was elaborated
generation of hydroxyl radicals, (iii) electron binding to (Youssef et al., 2015). Mechanical properties, such as ten-
empty oxygen portions and superoxide formation. sile strength and elongation at break, were significantly
TiO2 NPs incorporated into the wheat gluten-based improved by the addition of TiO2 . This was associated
biopolymer ensured antimicrobial properties of the food with a uniform dispersion of NPs providing stable stress
packaging (El-Wakil et al., 2015). Wheat gluten was cho- distribution and diminishing the formation of stress con-
sen as a plant protein because it is inexpensive and centration centers. In addition, the TiO2 NPs incorporation
shows good film-forming properties. Advanced nanocom- increased the hydrophobicity of the film, improving its pro-
posite film was fabricated by incorporation of glyc- tective effect against moisture during the storage period.
erol, cellulose nanocrystals, and TiO2 NPs to the wheat The chitosan/PVA/TiO2 films exhibited good antibacterial
gluten by casting/evaporation. Obtained films showed activity against S. aureus, Pseudomonas aeruginosa, and E.
enhanced mechanical properties in terms of increased ten- coli, as well as good antifungal properties against C. albi-
sile strength and decrease of elongation at break, and cans, thus enabled prolonged cheese shelf life.
low water vapor permeability and water vapor uptake due
to the increased surface hydrophobicity. The addition of
TiO2 NPs was shown to further prevent water absorp- 3.1.5 Zinc oxide NPs
tion. Kraft paper coated with three layers of this nanocom-
posite excelled at antimicrobial activities against S. cere- ZnO is classified as an essential micronutrient for human
visiae, E. coli, and S. aureus after UVA light irradiation. In and animal health and considered as GRAS (generally rec-
another study, packaging films composed of whey protein ognized as safe) by the FDA. ZnO is used by food industries
as a nutritional supplement and as a food additive due to the pure form. ZnO NPs also decreased water vapor perme-
its white appearance (Auger et al., 2019; Jeon et al., 2020; ability due to the formation of tortuous paths that hinder
Z. L. Wang, 2004). In nanosized form, ZnO is used for food the diffusion of water across the composite films. ZnO NPs,
packaging because its presence in the polymeric matrix together with the clove essential oil, made the biopolymer
provides improved mechanical strength, barrier proper- chains more flexible, yielding the film that contains small
ties, and material stability together with high antibacterial pits. These micropores significantly increased the surface
and antifungal activities. The dynamic role of ZnO NPs in of the film. The authors suggested that such increased
food preservation entails the production of ROS, especially surface facilitated antimicrobial activity. Indeed, the high
hydrogen-peroxide in the presence of light (Auger et al., antimicrobial efficacy of the film was found against S.
2019; Vidic et al., 2013). Their antibacterial efficiency was aureus and E. coli inoculated in scrambled eggs during 21
shown for a broad range of microorganisms such as B. sub- days of storage at 4 ◦ C.
tilis, S. aureus, E. coli, Salmonella, P. aeruginosa, C. jejuni Antimicrobial composites were also synthesized based
(Auger et al., 2019; Stankic et al., 2016; Vidic et al., 2013; on ZnO NPs imbedded into biodegradable polymers like
Zanet et al., 2019). Indeed, a greater sensitivity to H2 O2 polybutylene succinate (PBS) resin (Petchwattana et al.,
was observed in bacteria that were more sensitive to ZnO 2016), or corn starch-based carboxymethyl cellulose (Ni
NPs (d’Água et al., 2018). In contrast, research conducted et al., 2018). Physicochemical tests of the composite con-
on S. aureus indicated the independence of antimicrobial firmed the intermolecular interactions between ZnO and
activity of ZnO NPs from increased production of ROS and starch and their excellent compatibility. Grain boundaries
pointed to an alternative antibacterial mechanism affect- of ZnO form an electrostatic field that triggers water-
ing the energy metabolism of the cell and amino acid repulsion, ensuring a good water vapor barrier and resis-
biosynthesis pathway (Kadiyala et al., 2018). ZnO NPs may tance to solvents upon soaking. The nano-biocomposite
also release cytotoxic Zn2+ -ions upon their partial dissolv- films were homogeneous and continuous and showed
ing (Vidic et al., 2014). Namely, ZnO NPs can release Zn2+ - good thermal stability. Antibacterial activity of the con-
ions intracellularly that disturb bacterial redox poten- structed films was dependent on the migration of ZnO NPs
tial (Randazzo et al., 2020). Seray et al. (2020) described that was the highest in the acidic environment.
poly(butylene adipate-co-terephthalate)/ZnO NPs films. Electrospinning method has been used for the encap-
The NP embedding into the polymer assured the controlled sulation of ZnO NPs into biopolymer fibers. For instance,
release of Zn2+ -ions, resulting in the safe application of the it was applied for addition of ZnO NPs into hydrophobic
film. ethyl cellulose/gelatin nanofibers (Yuyu Liu et al., 2018).
Several novel nano-biocomposites combining ZnO NPs The tensile properties (average elastic modulus, tensile
and essential oils have been developed for food packaging strength, and elongation at break) were enhanced in the
in the last few years. C. Wu et al. (2019) used protein isolate- fibers containing ZnO NPs. The hydrophobic surface prop-
based biocomposite films, synthesized through a liquid erty was achieved by decreasing the number of gelatin
precipitation method that incorporated both plant-sourced chains and the reduced N atom content on the nanofiber
cinnamaldehyde and hexagonal wurtzite ZnO NPs. The surface by ZnO NPs. Antibacterial properties observed
aim was to obtain an antibacterial and antifungal mate- against E. coli and S. aureus were dependent on the ZnO
rial harnessing the synergistic effect of ZnO NPs and cin- concentration and the UV irradiation (Yuyu Liu et al.,
namaldehyde. ZnO NPs improved mechanical character- 2018).
istics and oxygen and water vapor barrier properties of As shown in these examples, ZnO NPs improved
the biopolymer. The composite films exhibited homoge- mechanical, thermal, antibacterial, and antifungal param-
neous, uniform, compact, and nonporous surfaces. Inter- eters when incorporated into the packaging material. How-
estingly, both cinnamaldehyde and ZnO NPs prevent light ever, some concerns exist regarding the ZnO NP cytotoxi-
transmission, providing a beneficial feature of these films city and it was observed in in vitro and in vivo studies in
because the oxidative deterioration of food was diminished animal and human cells (Jeon et al., 2020; McClements &
along with an extension of the food shelf life. The anti- Xiao, 2017). Moreover, the generation of ROS can induce
fungal activity of the film against Aspergillus niger was oxidative stress, lipid peroxidation, increase in Ca2+ -
increased in comparison to the pristine film. In another concentration inside the cell, alteration of mitochondrial
study, a polylactide/polyethylene glycol/polycaprolactone membrane potential, lysosomal destabilization, inflamma-
blend with incorporated ZnO NPs and clove essential oil in tory cytokine release, DNA damage, and cell death. All
the form of a film was developed using the solution casting these mechanisms underlying ZnO NPs cytotoxicity are
technique (Ahmed et al., 2019). Addition of ZnO NPs sig- dose-dependent. In contrast, the biopolymer composites
nificantly improved tensile strength, but decreased elonga- containing ZnO NPs did not exert a toxic effect on the
tion at the break of the nano-biopolymer film compared to human cells to such extent. Cierech et al. (2019) tested
release and cytotoxicity of ZnO NPs and of poly(methyl mesopores of MSN while their release rate can be con-
methacrylate)–ZnO nanocomposites on HeLa cells. They trolled, and hence their antimicrobial activity can be gov-
found out that the ZnO release level was more than erned through different means. Previous research show-
three times lower than the concentration of ZnO NPs cased that MSNs can be employed for loading and deliv-
in the nanocomposite, which suggests the possibility of ery of different types of drugs and even large biomolecules,
nanocomposites’ safe application in food packaging. and that the release of cargo molecules from MSNs can
be governed by different surface modifications of MSNs
(Knežević & Durand, 2015; Knežević et al., 2012). Capabili-
3.1.6 Magnesium oxide NPs ties for stimuli-responsive drug delivery were also demon-
strated upon exposure to light, magnetic field, enzymes,
MgO is a natural mineral produced on large scale and rec- change of environmental conditions (pH value, temper-
ognized by the FDA as GRAS for food applications. MgO ature), which may also be of interest for antimicrobial
NPs integrated into a biocomposite usually enable fabrica- applications (Knežević & Kalud̄erović, 2017; Q. Yu et al.,
tion of a highly transparent film. Still, MgO NPs are less 2020). These attributes highlight MSNs as great candidates
used in food packaging applications than TiO2 or ZnO for constructing active packaging composites, considering
NPs because of their less pronounced antibacterial activ- the plethora of possible antimicrobial cargo molecules for
ity (Vidic et al., 2013), although MgO NPs generates ROS loading MSNs, possibilities for versatile functionalization
(Auger et al., 2018, 2019; He et al., 2016; Vidic et al., 2013). of MSNs and the use of various biopolymers for construct-
An ROS-independent mechanism was also proposed for ing composite materials with desired attributes.
MgO NPs antibacterial effect on E. coli because it was The aminopropytriethoxysilane-functionalized surface
shown that MgO NPs damaged cell membrane in the of MSN (SBA-15 type) was recently utilized for attaching
absence of oxidative stress (Leung et al., 2014). MgO NPs antimicrobial molecule vanillin through a reversible imine
are highly biocompatible as shown in various in vivo and linker and its slow release from the composite with PCL
in vitro studies (Mazaheri et al., 2019; Mittag et al., 2019; was demonstrated, in an effort to develop active respon-
Vidic et al., 2013). sive packaging materials (Stanzione et al., 2017). A bio-
Using the solvent casting method MgO NPs were incor- nanocomposite film with pH-controlled release function
porated in PLA polymer to optimize the tensile strength, and antimicrobial activity was developed using compos-
oxygen barrier, and antibacterial properties because neat ites containing chitosan and curcumin-loaded MSNs (C.
PLA has certain limitations, such as high moisture affin- Wu et al., 2019). For this, curcumin was first loaded inside
ity, low thermal stability, poor barrier properties (Swaroop the pores of MSNs by gradual evaporation of the solvent
& Shukla, 2018). Interestingly, MgO NPs made no chemi- and the films were subsequently prepared by the solu-
cal bond with PLA, but only interacted physically. Packag- tion casting method. Antimicrobial activity of the films
ing films exhibited no physical defects, while white dots determined by measuring the zone of growth inhibition
formed of aggregated NPs throughout the samples con- of S. aureus and E. coli O157:H7 indicated that the addi-
tributed to surface roughness. Tensile strength of the films tion of curcumin into the chitosan films improved their
increased, while elongation at break and thermal stability antimicrobial activity compared to the pure chitosan films.
significantly decreased, most probably due to the agglom- The chitosan/curcumin blend films showed slightly higher
eration of NPs. Moreover, MgONPs/PLA film showed only antimicrobial activity than the films with curcumin incor-
a moderate antibacterial effect against E. coli, but had porated into MSN NPs. The release of curcumin was evi-
improved oxygen barrier and increased water vapor per- dently slower in the case of the composites containing
meability. The opposite effect of MgO NPs incorporation in MSN, which would be beneficial for achieving prolonged
PLA on various gas permeability can be attributed to differ- antimicrobial activity of the packaging material. The FTIR
ent polarities of water vapor and oxygen gas. analysis of the films revealed the formation of additional
hydrogen bonds between SBA-15-Cur and chitosan, which
lead to the improved mechanical properties of the films.
3.2 Mesoporous silica NPs as Zhang et al. (2019) synthesized packaging films by the
antibacterial nanofillers casting method, using potato starch and CEO loaded
into MSNs. To determine the functionality of the pre-
High specific surface area (approximately 1000 m2 /g) of pared films, their antimicrobial activity against Mucor
mesoporous silica NPs (MSN) and their large pore volumes spp. molds was tested. These mold strains are commonly
(approximately 1 cm3 /g) are of substantial benefit for the found in white mushrooms during storage. In contrast to
construction of efficient antimicrobial composites. A large pure potato starch and MSNs/potato starch films, MSNs–
number of different antimicrobials can be filled inside the CEO/potato starch films showed antimicrobial activity
F I G U R E 5 Structure of the starch–MSN composite material containing cinnamon essential oil loaded inside the mesopores of MSN for
antimicrobial activity against bacteria specific for white mushroomsNote: Illustration adapted from Zhang et al. (2019).
due to the release of the CEO from MSNs (Figure 5). charged amino groups with the negative moieties of bitter
In addition, the incorporation of MSNs–CEO into potato vetch proteins. The addition of both types of NPs positively
starch enhanced the tensile strength and thermal sta- affected the gas and water vapor barrier properties of the
bility of the films, due to the intermolecular hydrogen films.
bonding between surface silanols of MSNs–CEO and the The antimicrobial packaging system based on poly(3-
biopolymer. hydroxybutyrate-co-3-hydroxyvalerate), PHBV, and MSN
Recently, novel bioactive films were obtained by a solu- (MCM-41 type) containing eugenol as an antibacte-
tion casting method from the protein concentrate extracted rial molecule showed antimicrobial performance against
from bitter vetch (Vicia ervilia) seeds. The used concen- S. aureus and E. coli for 15 days (Melendez-Rodriguez et al.,
trate was either in the native form, or enzymatically cross- 2019). After loading eugenol into the NPs, they were incor-
linked by the microbial transglutaminase, (Fernandez- porated into PHBV by electrospinning. The obtained fibers
Bats et al., 2018). MSNs and their amino-functionalized were annealed below the polymer melting point to produce
derivative were used to reinforce mechanical and barrier continuous films. The PHBV film and PHBV/MSN films
properties of protein-based films. Also, bioactive oligopep- without eugenol showed no growth inhibition, whereas
tide nisin (bacteriocin effective against many Gram pos- films with eugenol-containing MSN exhibited remarkably
itive bacteria) was added to the film-forming solution. increased antibacterial activity. The results from the tested
Antimicrobial activity of the films was tested by the agar closed system showed higher antimicrobial activity than
diffusion method using an inoculum of Micrococcus that observed in the open system. This was ascribed to
luteus. The nanoreinforced bitter vetch proteins them- the volatile nature of eugenol that accumulated in the sys-
selves exhibited antimicrobial activity, due to their phe- tem and sustained the release capacity of the films. The
nolic compounds. The inhibition zone was significantly results of the mechanical analysis showed that the incorpo-
wider for the films with added nisin. Incorporation of both ration of eugenol-loaded MSNs increased the mechanical
MSNs and APTES-MSNs improved the film mechanical strength of the PHBV films while the ductility was slightly
properties, due to the ionic interaction of their positively reduced.
3.3 Carbonbased NPs as antibacterial followed by an in situ co-precipitation of Fe3+ /Fe2+ ions
nanofillers onto the surface of GO nanosheets. Hydrogel system
formation of chitosan–GO was done in the presence of
Graphene is one-atom thick, two-dimensional nanosheet glycerol as a chain extender. Glycerol assists the joining of
of graphite having exceptional thermal conductivity, the chitosan polymeric chains by electrostatic interactions
superior mechanical properties, large specific surface area, and H-bonding. Obtained chitosan–iron oxide coated
good electron transfer ability, and good biocompatibil- nanocomposite enabled fabrication of a compact packing
ity (Pinto et al., 2013). In addition, GO or reduced GO film with a significantly improved thermostability, tensile
(rGO) can be obtained from graphite upon chemical oxida- strength and Young’s modulus. Substantial antimicrobial
tion or electrochemical exfoliation. In the past few years, activity of the composite hydrogel films was observed
graphene-based materials attracted much attention and against S. aureus, E. coli, and C. albicans. The possibility of
were used in the food industry to ensure food quality and using these novel composite films in food industry applica-
safety (Sundramoorthy & Gunasekaran, 2014). Graphene- tions is strengthened by the in vitro hemolysis potentiality
based NPs exert antimicrobial activity by damaging bacte- test and the MTT assay, in which their noncytotoxicity
rial membrane and causing the leakage of the cell content, was observed.
by inducing ROS hyper-production or by trapping microor- S. Sharma et al. (2018) used GO as a carrier of salicy-
ganisms in its aggregated sheets (Shi et al., 2016; Zhu et al., laldehyde preservative to develop a packaging that released
2017). salicylaldehyde from GO only in the presence of over-
Exceptional tensile strength makes graphene a very ripe fruits. The composite was vacuum-filtered to obtain
attractive candidate for development of food packag- a robust wrapper for the fruit storage. The overripe fruits
ing materials because its addition to films significantly produce acid that cleaves the labile hydrazone and triggers
increases endurance of the material whilst reducing the release of salicylaldehyde from GO (Figure 6). The bio-
the weight. For instance, multiwalled carbon nanotubes composite improved the fruit shelf life due to the efficient
(MWCNTs) incorporated in chitosan/PLA composite via preservative release. In addition, it shows less toxicity as
electrospinning gave fibers uniform size, smooth sur- compared to the free preservative.
face, and good nanotube distribution (Yaowen Liu et al., Carbon dots, as representatives of quantum dots, are
2019). This material was tested for antimicrobial activity another type of carbon nanomaterial used to develop active
against E. coli, S. aureus, B. cinerea, and Rhizopus. Antimi- packaging. Carbon dots possess several superior character-
crobial activity was manifested through the decrease of istics, such as simple mass production, low toxicity, antiox-
the membrane and cell wall permeability, which caused idant activity, optical features, photo-stability, and antibac-
changes in the internal osmotic pressure. PLA/carbon nan- terial properties mostly due to their ultra-small sizes and a
otubes (CNTs)/chitosan composite fibers exhibit benefi- surface rich in functional groups. The mechanisms of their
cial fruit and vegetable packaging properties confirmed antimicrobial activity comprise adhesion of carbon dots to
by the conducted preservation experiments. Antimicrobial the surface of bacterial cells, followed by photo-induced
nanopackaging films were also developed by incorporat- ROS production and modification of the membrane per-
ing GO nanosheets and clove essential oil into PLA via meability as well as cell internalization accompanied by
solution casting (Arfat et al., 2018). The addition of GO intracellular oxidative damage (Al Awak et al., 2017; H. Li
into PLA matrix improved the flexibility of the compos- et al., 2018; Li et al., 2016; Shi et al., 2016).
ite films by lowering glass transition temperature, complex Bacterial nanocellulose used by Kousheh et al. (2020)
viscosity, oxygen permeability, and porosity. In addition, served as a carrier biopolymer for the incorporation
the developed composite film showed excellent antibac- of carbon dots. Carbon dots were obtained by a one-
terial activity against S. aureus and E. coli. All the men- step hydrothermal method using the cell-free supernatant
tioned features indicate a high potential of graphene and of a probiotic bacterium Lactobacillus acidophilus. The
GO for use as active packaging material for food safety and supernatant was rich in succinamic acid, cyclopentane,
preservation. 1-cyclododecanone, undecanoic acid, cycloheptane, phe-
Konwar et al. (2016) combined GO and iron oxide in nol, and benzoic acid, all of which are suitable for the
a form of iron oxide coated GO with a chitosan hydrogel formation of carbon dots. This protocol uses bacterial
structure to develop a novel GO nanocomposite hydrogel biomass that is abundant and represents a green resource
for applications in the food industry. The nanocomposite for easy development. The as-synthesized carbon dots were
was fabricated using the co-precipitation method, whereas incorporated into the bacterial nanocellulose membrane
the nanocomposite films were successfully synthesized made from Komagataeibacter xylinus and proposed as a
by gel casting technique. For this, GO was first derived novel nanopaper with antimicrobial and antioxidant activ-
by oxidation and exfoliation of a graphite nanopowder, ity that potentially improves the food shelf life. Concerning
F I G U R E 6 Active packaging based on graphene oxide (GO) and salicylaldehyde (SA) developed for preservation of fruits. With
permission from (Sharma et al., 2018).
the mechanical properties, the developed nanopaper was Vasiljevic et al., 2020). To be accepted by the food indus-
flexible and stretchable and had decreased ultimate ten- try and consumers, new packaging materials containing
sile strength. The presence of blackish carbon dots colored nanofillers should not only exert high efficiency in food
the nanopaper to dark brown color. Under UV light, the preservation, but also should be inert concerning food sen-
nanopaper was fluorescent due to carbon dots, extending sory properties, as well as stable during the storage condi-
this film’s possible use to forgery-proof packaging. tion. The major concern on nanofillers comes from their
For use in food packaging, carbon-based NPs possess potential toxicity because of the high surface-to-volume
other numerous useful properties such as alleviating food ratio that provides a high reactivity. There is a limited num-
waste with improved packaging, forming a selective bar- ber of studies done on the cytotoxicology and migration of
rier for moisture and air thereby enhancing food preser- nanofillers into food from the packaging film. Thus, the
vation. It can greatly help in reducing the use of plas- utilization of nanofillers in active packaging films requires
tic and increasing biodegradability and recyclability of deeper consideration of their safety.
packaging.
Nowadays, many novel nanostructured materials are
under investigation for application in active food pack- 4 REGULATORY AND MARKET
aging. Most of the research on nano-biocomposites for STATUS
active food packaging has focused on oxygen scavengers,
water absorbers, carbon dioxide or ethanol generators, and Food packaging is the third largest industry in the world,
antimicrobials (López de Dicastillo et al., 2020; Nikolic amounting to approximately 2% of the gross national
et al., 2019; Realini & Marcos, 2014; Suppakul et al., 2003; product of the developed countries (Robertson, 2016).
Novel approaches, frequently based on nanotechnology, EFSA. The application should be prepared according to the
are being extensively developed for use in food packaging “Guidelines on submission of a dossier for safety evalua-
in order to achieve sustainable and cost-effective protec- tion by the EFSA of active or intelligent substances present
tion of foodstuffs. Such novel technologies require appro- in active and intelligent materials and articles intended
priate regulatory and legislative frameworks, which is why to come into contact with food,” adopted by EFSA on
governing agencies all over the world intensively work July 21, 2009 (European Food Safety, 2009). After EFSA
on defining new regulations to encompass the emerg- delivers its opinion, the Commission may adopt it and
ing nanotechnology aspects. This global process has been authorize the use of the component in question, by adding
in motion ever since Kraft foods (now Mondelēz Inter- it to the union list. Furthermore, the Regulation (EC)
national) in 2000 started their first nanotech laboratory No. 450c2009 (European Commission, 2009) sets guid-
and the Nanotek consortium made up of 15 universi- ance about the labeling of products that contain active
ties and national labs, to fund research into personal- and intelligent materials, stating that such products are to
ized or “smart” foods, such as nanotechnology-enabled be labeled appropriately to allow the consumer to iden-
products that could respond to a person’s nutritional tify nonedible parts, for example, by adding the words
needs (Suran, 2014). Nowadays, the European Union (EU) “DO NOT EAT” to the label. Additionally, the products
together with Switzerland has been the only region that must clearly show on the label that they are active and/or
included nanospecific definitions in the existing legisla- intelligent.
tion (Amenta et al., 2015), while in the other regions, It is necessary to discuss the regulation concerning
nanotechnology-based innovations are regulated in a more antimicrobial packaging as well; taking this into consider-
indirect manner, as shown below by the example of the US ation, we present in this review a number of components
regulatory initiatives. to be used as such. The regulation for the use of antimi-
In the EU, regulatory bodies provide joint legislation for crobial substances in food has always been quite strict in
materials and articles for active and intelligent packaging. the EU, with a relatively small number of preservatives
The Regulation (EC) No. 450/2009 establishes a union list currently allowed in foodstuff (European Commission,
of authorized components that strictly interact in a direct 2011b). These listed substances can be used in antimi-
manner with the food or with its environment (European crobial packaging, provided there is no other relevant
Commission, 2009). There is a derogation to this regula- limitation in food legislation. A novel substance with
tion concerning the substances that are separated from potential antimicrobial effects on packaged food needs to
the food by a functional barrier (the definition of which be approved as a food additive. Obtaining approval for a
is provided in another Regulation (EC) No. 10/2011) and new food additive in the EU is a costly and lengthy pro-
are not transferred to food in a detectable quantity, with cedure, which is why manufacturers usually require very
a detection limit of 10 mg/kg of food (European Commis- strong market justifications in order to start this process
sion, 2011a). This appears to specifically refer to the intelli- (Dainelli, 2015). This is, in principle, difficult to achieve for
gent packaging materials, which are usually used outside a new component, especially for the relatively small EU
of the primary packaging and are not very likely to be trans- market.
ferred to the foodstuffs. Furthermore, it is important to In addition, the EU has enforced a new REACH reg-
emphasize that the substances in nanosize, as well as the ulation as of January 1, 2020, which requires Euro-based
substances classified as carcinogens, mutagens, or toxic companies to provide more information on used nano-
to reproduction, should always be listed in the product materials (ECHA, 2020). At the same time, EFSA’s inven-
description regardless of whether they are used in direct tory of nanomaterials and their applications in the mar-
or indirect contact with food, or of their migration behav- ket shows that nanomaterials in contact with food as well
ior (Dainelli, 2015). However, many experts object to this as nanoscale food additives represent the most common
derogation, pointing out that it may cause omission of the application of nanomaterials (Peters et al., 2014). These two
necessary listing in the product description for any nonmi- directions, one being a very strict and lengthy compliance
grating components, not only those related to packaging. procedure and the other of increased research in nanoma-
In other words, there is concern that such a relatively vague terials for use in food packaging, are currently not well syn-
description of the regulation scope, that is, the compo- chronized in the EU. Thus, such a strict compliance pro-
nents it refers to, may lead to insufficiently detailed prod- cess in the EU is not favorable to the manufacturers and
uct descriptions (Dainelli, 2015). distributors who opt instead to market their new active and
The procedure for authorization of substances consti- intelligent nanoscale food packaging products outside the
tuting the components of active and intelligent materials EU.
and articles and their inclusion in the Community list of Other jurisdictions, such as the United States Food and
authorized substances starts with the application to the Drugs Administration (FDA), do not specifically address
active and intelligent materials but treat them within 5 CONCLUSION AND FUTURE
conventional legislation for food contact materials (FDA, TRENDS
2020). The material in the food packaging that is not
intended to be added to the food, nor to have a techni- The public is aware of the need to reduce general waste
cal effect on the food (so-called “indirect additives”), is stemming from the traditional plastic food packaging
regulated like all other food-contact substances (Restuc- made from petroleum that is non-biodegradable and non-
cia et al., 2010). Moreover, the FDA has rather flexible renewable. At the same time, the Food and Agriculture
guidance concerning the application of nanotechnology Organization has estimated that the post-harvest agri-
in FDA-approved products (FDA, 2020). These guidelines cultural loss accounts for 20%−50% of the food produc-
and regulatory approaches are being determined by the tion annually. Consequently, more efficient and sustain-
FDA Nanotechnology Task Force, formed in August 2006. able food packaging is continuously under development
This task force encourages regulatory science research in in order to reduce waste, diminish post-harvest losses and
nanotechnology via internal research grants and publishes increase safety. This review highlights the great poten-
annual reports (FDA, 2020). Such science-based, product- tial of biodegradable films with nanomaterials for active
focused regulatory policy for nanotechnology is also being packaging that provide extended shelf life and main-
implemented by another US regulatory body—the United tain or improve the condition of the packaged food. Bio-
States Department of Agriculture (USDA). The National based polymers are eco-friendly materials with high per-
Institute of Food and Agriculture (NIFA) within USDA formance that can replace traditional petroleum-based
manages four grant programs that fund nanotechnology packaging. Nanofillers are used to improve food packag-
research projects. NIFA also participates on the Nanoscale ing mechanical properties; enhance barriers to water, oxy-
Science, Engineering, and Technology Subcommittee of gen, and other environmental factors; absorb moisture;
the White House National Science and Technology Coun- protect against UV radiation; and release antimicrobials,
cil and the National Nanotechnology Initiative defined by while retaining their biodegradable properties. Antibacte-
the 21st Century Nanotechnology Research and Develop- rial NPs such as TiO2 , ZnO, MgO, Ag, graphene, and car-
ment Act (USDA, 2015). bon dots in bio-nanocomposite films could enhance food
Nevertheless, all the guidance documents stemming quality and safety over a longer period that would enhance
from described initiatives in the United States still only the marketability of the new active packaging materials.
provide recommendations that are not binding. Such flex- The main future prospect in active packaging is the
ible regulations are seen as favorable for the industry and safety improvement of antimicrobial nanofillers because
manufacturers. The Canadian food packaging regulatory there are limited studies on the cytotoxic impact of the
system is similar to the one in the US but it includes con- nanomaterials in packaging films. The currently available
cerns of migrating food packaging components, which are bibliographic data reveal that the toxicity of nanofillers
not considered to be food additives (Rijk & Veraart, 2010). depends on their shape, size, surface-to-volume ratio,
Other countries, especially Japan and Australia, follow this and doping. Nanofiller toxicity is also concentration-
trend of flexible regulations due to the increasing demand and time-dependent. Moreover, to produce efficient and
for packaging solutions (for an extensive regulatory sta- durable antibacterial packaging, the controlled release
tus of nanomaterials, see Bumbudsanpharoke & Ko, 2015; of antibacterial agents must be achieved. Research is
Lugani et al. 2021). Iran, Taiwan, and Thailand have intro- directed to specific incorporation of nanofillers to the
duced systems for tracking and labeling consumer prod- packaging materials that will enable gradual release
ucts containing nanomaterials (e.g., NanoMark system), and reduce excessive particle concentration in contact
which are, however, substantially different from the label- with food. Further development of active packaging
ing requirement in the EU (Amenta et al., 2015). In Japan, will also depend on comprehensive, systematic, and
the safety of active packaging is regulated by the Japanese well-defined standards for antimicrobial activity and
Food Sanitation Law of 1947, and the Food Safety Base safety evaluation of nanofillers.
Law of 2003. These regulations are combined with risk The commercialization of active packaging technologies
assessment criteria that are in compliance with those of is challenging because of the implementation costs and
the EU and the United States. (Dainelli, 2015). With a high the complex legislative and regulatory issues. Despite cur-
interest in nanotechnology research on a global level (even rently existing complexities in achieving regulatory com-
among the developing countries) and a rise in acceptance pliance, particularly in the EU, the high benefits that
among consumers, a further refinement of legislation is can be achieved by the use of active packaging stimu-
expected, followed by a higher rate of adoption among late the dynamic pace of commercialization of various
manufacturers. packaging systems and accelerate their adoption by food
producers and consumers. Furthermore, the gap between Nikola Ž. Knežević https://orcid.org/0000-0002-1563-
commercial applications and research must be filled 7763
by close collaboration between academic and industrial Ivana Gadjanski https://orcid.org/0000-0003-0713-7897
groups. Jasmina Vidić https://orcid.org/0000-0002-8549-8199
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Comp Rev Food Sci Food Safe - 2021 - Omerovi - Antimicrobial Nanoparticles and Biodegradable Polymer Composites For Active

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Received: 20 August 2020 Revised: 25 January 2021 Accepted: 1 February 2021

COMPREH ENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY

Antimicrobial nanoparticles and biodegradable polymer

Nejra Omerović1 Mila Djisalov1 Kristina Živojević1

1 BioSense Institute, University of Novi

Sad, Novi Sad, Serbia Abstract

Foodborne diseases are a global public health concern,

2428 © 2021 Institute of Food Technologists

FIGURE 2 Various antibacterial mechanisms of nanoparticles used as inforcers in food packaging

TA B L E 2 Examples of active packaging containing nanofillers

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