Transmission of COVID-19 by food and food packaging

Summary

The corona pandemic, along with human health and wealth, is also affecting the food sector. There is a continuous and enormous rise in the COVID-19 infections on a global scale reported for food workers. Although, there is no report about spreading the virus through food consumption, different gastrointestinal symptoms have been reported, thus the finding of SARS-CoV-2 in food or food packaging may raise concerns about food safety. There is a variety of physical factors and antiviral food components that effect SARS-CoV-2 transmission. The transmission of COVID-19 is also impacted by the food packaging. At present, significant research has been performed concerning antimicrobial food packaging but there is still a shortage in antiviral food packaging development. In this sense, the input of the nanotechnologies and nanomaterials (nanoparticles, and nanocomposites) in exploring antiviral food packaging is undoubtful and promising, since it contributes to the improvement of foodstuff quality, safety, and sustainability.

Key words/phrases: food-mediated corona virus transmission, food nanopackaging, nanoparticles’ antiviral activity

1. Introduction

The corona pandemic, along with human health and wealth, is also affecting the food sector [11]. There is a continuous and enormous rise in the COVID-19 infections on a global scale reported for food workers. Due to the rapid spread of the infection, various myths about the transmission of the virus during consumption of meat and poultry products have been spread. As has been shown by a survey performed in Arabian countries, the majority of the people are not aware of the SARS-CoV-2; they are neither concerned about the food-related transmission. This indicated that the local authorities and government bodies need to control the false rumors about food and its safety [28].

Hence, up to now, there is no report about spreading the virus through food consumption. However, different gastrointestinal symptoms like nausea, vomiting, and diarrhea have been reported [75]. Thus, the finding of SARS-CoV-2 in food or food packaging may raise concerns about food safety, but it doesn’t indicate a risk for public health. It is not a reason for restricting food trade or initiating a food recall but integrating food security and sustainability in a food chain must be considered as an important part of the approaches for controlling putative future pandemics.

2. Predicted modes of food-mediated corona virus transmission

Viruses are intercellular parasite that needs an alive host cell to ensure replication of its genome by the means of a host cell. This specific feature of the viruses does not permit their cultivation in an environment without a living cell.

Generally, viral diagnosis is difficult due to the availability of limited diagnosing and analytical tools for virus detection [74]. It is known that norovirus (gastroenteritis), hepatovirus A (hepatitis A), and orthoreovirus A (hepatitis E) are the typical food-borne viruses that can be transmitted to food commodities via different pathways like contaminated water, oral-faecal route, infected food handlers (Fig. 1).

Figure 1. The typical food borne viruses transmitted by food chain.

Previous outbreaks like SARS and MERS were not established to be transmitted by food. In this respect, there are no clear findings for SARS-CoV-2 to be transmitted also through such a mechanism. While the transmission of SARS-CoV-2 through food is not scientifically proven, this opportunity must not be excluded since SARS-CoV-2 is linked with animal trade and consumption [11]. Following this, the frozen fresh food as a source of SARS-CoV-2, by the analogy of MERS and SARS COV-1, can also be a medium to transmit the virus as it was found that it remains infectious in a frozen state for up to 2 years [33].
The transmission pathway of the viruses via food can take place during the handling in production, processing, packaging, and transportation. Also, cross-contamination from already infected food handlers is one of the major routes of transmission [72]. There is also a risk of spreading COVID-19 infection via food packaging through infected operational staff, for which cases the consumers were highlighted by the EU Commission [25]. Fig. 2 describes the various possible routes for transmission of COVID-19 via food.

Figure 2. Possible modes of transmission of SARS COV-2 in the food production chain.

2.1. Effect of temperature, pressure, humidity, and acidity on SARS-CoV-2 transmission

Food-borne viruses can be disabled using extrinsic and intrinsic factors of the food, and different chemical approaches as well as during technologies for food processing. Factors influencing SARS-CoV-2 virus are multidisciplinary. Hence, it is necessary to take under consideration the various environmental states, comprising temperature, pressure, humidity, and acidity, that forecast the vitality, survival, and infection rate of the virus.
The important extrinsic features of food, like water activity, рН, and frapped and frozen storage temperatures, are considered to control and keep the food microbiologically safe. The effect of these factors is related to their capacity to inhibit microbial contamination of food. When viruses are the contaminating agents, some of these controlling practices can be omitted since the viral infectivity strongly differs in comparison to that of the food-spoilage or pathogenic bacteria. The viruses, like various bacterial pathogens, are comparatively stable under refrigeration and freezing storage. Data are present in the literature for the persistence of various viruses in different food commodities after different storage regimens. For instance, no reduction of murine Norovirus (MNV) in spinach and spring onions was registered after 6 months of frozen storage; after 28 days of storage, а decrease of <1.2 log10N was measured for strawberries. SARS-CoV-2 was found to be stable up to 72 hours during refrigeration (4oC) and 2 years in deep freezing (-20oC). SARS-CoV is deactivated for 15 min at a temperature of 75oC while MERS can be inactivated at 65oC for 1 min.
A thermostability assay performed for SARS-CoV-2 indicated that it is inactivated at a minimum temperature of 70oC for at least 5 minutes. These data pointed out that standard temperatures for cooking are adequate to deactivate the virus. However, fresh and frozen foods may be used as vehicles for virus transmission. For them, rigorous keeping to the safety protocols and strong hand-washing after handling is very important. There is a lower possibility for viral transmission by food when its shipment takes place over а couple of days.
Like the food, drinking water is not treated as a way for transmission of the SARS-CoV-2 according to the reports of the Environmental Protection Agency (ЕРА) and the Centre for Disease Control (CDC). This is because the common water treatment procedures are adequate for the deactivation of the viruses. Thus, the thermal processing of food is considered one of the best useful techniques for foodborne viruses’ deactivation. The HAV, Hepatitis Е (HEV), and NoV viruses are as vulnerable to this treatment as the pathogenic bacteria. During pasteurization temperatures, MNV and HAV were shown to record more than 3.5 log10N at 72oC after 1 minute in the water. Also, MNV and TuV were deactivated after heating at 70°С for 2 min.
Steam blanching of produce like spinach for 1 minute at 80oC reduced the infectivity of MNV by а minimum of 2.4 log10N. Similarly, FCV and HAV were also immensely inactivated after blanching at 95oC for 2.5 minutes.
The strategic combination of acidification (рН decrease) of foods in addition to thermal treatment was also reported to be very effective against the inactivation of HAV.
Regardless of the minimum temperature and time requirements for inactivation of different viruses, in most cases, а minimum of 90 sec of thermal processing at а minimum temperature of 90oC is generally sufficient in inactivating enteric viruses irrespective of the complexity of the food matrix. It is generally believed that а boiling liquid medium such as water is capable of effectively inactivating the virus after about just 1 minute for more than 4 log10N for most enteroviruses including, human NoV, human rhinovirus (HRV), HEV, and HAV. Тhe dried virus was reported to retain its infectivity at 22-25oC and relative humidity of 40-50 % over 5 days. At higher temperatures (38oC) and relative humidity (> 95 %), they quickly lose their viability (> 3 log10N).
Extrinsic changes in рН levels that occur during fermentation or acidification of the carbohydrate substrates and the water activities levels of foods, for example by means of adding solutes like sugar or salt or their combinations, or even coupling of these treatments with dynamics of the storage conditions, have different effects on the viruses’ infectivity. MNV and TuV for example were found to tolerate low рН levels (рН 2) due to lactic acid fermentation. Even though fermentation was reported to be capable of producing compounds with potential usage as food additives, thus stimulating the antiviral properties, the underlying antiviral mechanisms are still yet to be fully understood.

2.2. Effect of irradiation on SARS-CoV-2 transmission

Ultraviolet (UV) radiation has been reported to be effective in activating some viruses. Its efficacy against the SARS-CoV-2 has not yet been tested. SARS coronavirus was extremely susceptive to ultraviolet irradiation. It has been recommended as an additional level of safety during the physical process of disinfection. Comparing the efficiency of disinfection: manual chemical methods reduced the contamination by 36% and а 96 to 99.99% reduction by ultraviolet irradiation from PurpleSun® ЕЗОО system UV system was achieved. At lower viral concentrations, low doses of UVC radiation (200 – 280 nm) completely inactivated the SARS-CoV-2, and higher doses altogether disabled higher concentrations of the virus.
Gamma irradiation between 3 000 to 15 000 rad did not affect the inactivation of the SARS-CoV, indicating that the irradiation dose range was too low to affect the virus. Whereas the virus was inactivated by UVC (unlike UVA D, 320 – 400 nm) after about 6 minutes of exposure. This implies that low wavelength UVC radiation could be effective in deactivating the virus from suspected food products.

2.3. Antiviral food components and food packaging

Food-borne viruses are proven to cause the majority of food-borne outbreaks. In 2010, 15% of food-borne outbreaks reported viruses as the causative agents [21] and according to those reports, Human noroviruses (HuNoVs) and Hepatitis A virus (HAV) was found to be of the greatest concern in the context of food safety. HEV was recently identified as a food-borne virus causing zoonotic transmission from pork meat products to humans upon consumption.
Natural bioactive compounds (flavonoids, polyphenols, tannins, catechins, saponins, polysaccharides, proanthocyanins, proteins, and peptides) are present in plant extract of cranberry, pomegranate, blueberry, black raspberry, grape seeds showed a great extent of antiviral activities by the destruction of viral structure or by preventing the entry of the virus into the host body [18]. Besides plant extracts, there are various essential oils, algal extracts, and proteins that are reported as antiviral. Various algal products such as carrageenan, navicular, and laminarin are also found to have antiviral activity [3]. An extended list of such natural compounds is presented in Table 1.
Currently, there is a lot of ongoing research on antimicrobial food packaging that aims to increase the shelf life of food products and retain food safety and quality. Antimicrobial packaging plays an important role in microbial growth inhibition and food spoilage. In the development of antimicrobial food packaging, there should be direct contact of the packaging material with the surface of the food for the migration of the antimicrobial compounds.
Antiviral food packaging materials are designed with the purpose to control the human enteric virus. Therefore, in the case of antiviral food packaging, it is necessary to inactivate the presence of the human enteric virus in food contaminated by raw and processed food products. Intrinsic material characteristics (which deal with polarity, and chemical composition) are responsible for the release properties of the biocidal compounds [29] and processing conditions for material development, which directly affect its mechanical, thermal, and physical properties (stability and release properties of the antiviral compound) are the relevant factors to be considered while designing antimicrobial packaging material [22]. However, there is less study on antiviral compounds into biopolymers due to their non-compatibility with polymeric structure and the quick release or degradation of antiviral agents.
Martinez-Abad et al. [51] developed 1% silver-PLA film and it was found to eliminate Feline calicivirus (FCV) from lettuce after 6 days of storage. Antiviral packaging materials were also developed by incorporating plant extracts in the biopolymers. A multilayer packaging material developed with cinnamaldehyde and zein ultrathin nanostructure layered covered with an outer layer of polyhydroxy-butyrate (PHB) worked against norovirus surrogates [27]. One of the promising candidates is the chitosan since it possesses excellent antifungal, antimicrobial, and antioxidative properties and is versatile to make coatings or films. It was observed that chitosan coating or films reduced the food-borne pathogens with the addition of essential oils or propolis into it [70].
Recently, the chitosan matrix was utilized in a study for protecting (-) – epigallocatechin gallate [35] having antiviral activity against HAV and MNV. Though only a few packaging materials have been developed which have antiviral activity, many of them were found to change the physicochemical properties of the food products. This change can be controlled through the application of edible films or coating. It is an emerging technology with controlled release of antimicrobial compounds by using various techniques like nanotechnology, encapsulation, and immobilization of antimicrobial agents from the matrix [4, 34]. The development of editable coating or film can be arranged by the addition of antimicrobial compounds in them that can reduce the food-born contamination. Though many pieces of literature are available for antibacterial and antifungal compounds incorporation in edible coating no data is present regarding antiviral edible coating or films. Therefore, research on antiviral edible coating is expected to have a great future. For making antiviral edible packaging materials, carvacrol, green tea extract, and grape seed extract can be used as natural antiviral agents. Similarly, many natural compounds such as clove, and oregano which were found to have antiviral activity against MNV, FCV can be incorporated into the development of antiviral food packaging [23]. Many researchers are fascinated by the micro- and nano-encapsulating sensitive antiviral compounds. Indeed, it not only helps to stabilize the compounds but also enhances their activity. Encapsulation is found to increase the stability of antimicrobial compounds even in irradiation [34]. However, there is limited data about the encapsulation of antiviral compounds and their applications in the food industry.

Table 1. Typical antiviral mechanisms of action of nanomaterials.

Virus	Natural source	Type
-PIV 3 - Parainfluenza virus type 3 -FIPV – Feline infectious peritonitis virus -VSV – Versicolor stomatitis virus -HSV – Herpes simplex virus -FHV – flock house virus -PR8, H1N1 and H6N1respiratory syncytial virus	Curcuma longa (L.)	Rhizome extract and Curcumin
-CHIKV - Chikungunya virus	Kalanchoe pinnata (L.) Pers.	Whole plant extract
-CHIKV - Chikungunya virus	Aristolochia tomentosa Sims	Whole plant extract
-CHIKV - Chikungunya virus	Paris polyphylla Sm.	Whole plant extract
-Yellow fiver virus	Clerodendrum serratum (L.) Moon	Whole plant extract
-Enterovirus 71	Terminalia chebula Retz.	Whole plant extract
-HRV 3 – Human rhinovirus 3	Chamaecyparis obtuse (Siebold & Zucc.) Endl.	Whole plant extract
-HRV 3 – Human rhinovirus 3	Chrysanthemum boreale (Makino)	Whole plant extract
-HRV 3 – Human rhinovirus 3	Cryptomeria japonica (L.f.) D.Don	Whole plant extract
-HSV – Herpes simplex virus	Swertia chirayita (Roxb. ex Fleming) H. Karst.	Whole plant extract
-VHSV - Viral Haemorrhagic Septicaemia Virus	Olea europaea L.	Leaf extract
-HIV – Human immunodeficiency virus	Salvia Rosmarinus Spenn.	Whole plant extract
-HSV-1 – Herpes simplex virus type 1	Camellia sinensis (green tea)	Whole plant extract
-HSV-1 – Herpes simplex virus type 1	Melaleuca alternifolia	Essential oils
-HSV-1 – Herpes simplex virus type 1	Thymus sp.	Essential oils
-Influenza viruses	Origanum acutidens. (Hand.-Mazz.) Ietsw.	Essential oils
	Artemisia obtusiloba var. glabra	Essential oils
	Houttuynia cordata Thunb.	Essential oils
	Salvia sclarea L.	Essential oils
	Cynanchum stauntonii (Decne.) Schltr. ex H.Lév.	cinnamaldehyde
-Corona virus	Nigella sativa L.	Essential oils
	Anthemis hyalina DC.	Essential oils
	Citrus × sinensis (L.)	Essential oils

Source: Jyoti and Bhaswati (2021) [45]

The lessons learned on the COVID-19 pandemic indicated helped issue some valuable recommendations for future outbreaks. There is а need for а cross-platform strategy to mitigate the spread of the virus along the food chain. This may involve international and governmental agencies, the food industry, retailers, food handlers, and consumers. The use of artificial intelligence (AI) to monitor and trace any exposure to SARS-CoV-2 is recommended, especially in the industry dealing with fresh products such as meat and vegetables.

3. COVID-19 impact on food packaging

3.1. Food packaging

As per definition, food packaging is the way, in which the food products are prepared for transportation, distribution, and retailing in a manner that assures their safe delivery to the consumer [64]. The systems for packaging are organized into three definite groups concerning their functions and levels of packaging. These are as follows [60].

• Primary packaging: this is the first packaging level. It comprises the layer of packaging that is in direct contact with the packed food products;
• Secondary packaging: this packaging involves a series of primary packages and serves to protect them from damage during transportation and storage. This group of packaging is designed in a way to assure a customer-friendly view of the package since the second packaging is displayed on the retail shelves.
• Tertiary packaging: this packaging executes the role of a distribution carrier that contains several primary and secondary packages.

The purposes of food packaging are multifunctional. Its major roles are related to [71]:

• Protect and maintained food safety from physical, chemical, and biological deterioration;
• To keep food products’ quality by extending their shelf-life;
• To ensure food products safety by diminishing the risk of interference and contamination;
• To serve as convenient containment, protection, and/or preservation device that is easily communicated among producers, retailers, and consumers;
• To help reduce the disposal of municipal solid waste, i.e. to reduce the cost of the food products by promoting the efficiency of bulk distribution, hence facilitating large-scale production.

Besides these important advantages, several drawbacks have to be considered as well. They are related mainly to non-biodegradable food packaging. It raises environmental concerns since non-biodegradable food packaging contributes to changes in the carbon dioxide cycle, raises composting problems, and elevates the levels of toxic emissions [26].

All these negative environmental impacts are directly related to the health safety concerns of consumers, and a lot of research studies are currently focused on the development of biodegradable packaging. Being renewable and environmental-friendly, biodegradable polymers will be progressively becoming the preferred choice of the packaging industry. For instance, the natural biopolymer sources, such as starch and chitin (polysaccharides), waxes and paraffins (lipids), collagen and gelatin (proteins), or their mixtures are subjected to comprehensive research nowadays [38, 73]. Among them, the potential of the proteins to be applied for packaging purposes is the greatest one due to their specific characteristics to form films with good barrier and mechanical properties [77].

3.2. Food packaging and transmission of COVID-19

The understanding of the transmission of COVID 19 through food packaging is based on the Good Manufacturing Practices (GMPs) regarding SARS-CoV-2 to avoid cross-contamination and transmission. Although there is no report of transmission of COVID-19 through food and food packaging, the importance of following Good Manufacturing Practices (GMPs) to avoid the cross-contamination and transmission of SARS-COV-2 still holds good. An individual may get infected if touches a surface or object, including food packaging. According to a report, the persistence of the coronavirus on plastic (72 hours) and steel (48 hours) is for a longer period than on the cardboard surface (24 hours). The persistence on the surface of copper (4 hours) is shorter possibly due to its antimicrobial actions [6].
During this pandemic, according to the report of the Food Packaging Forum, the reusable system is claimed to be much safer than the single-use packaging system; however, it affects the target of zero–a waste lifestyle. In fact, it is not possible to trace the handling of the single-use packaging products; at the same time reusable packaging can be washed with soap and hot water, and thus, can be used again.
Implementation of lockdown and execution of stringent government rules resulted in the shutdown of dine-in restaurants. Although food delivery chains operated, consumers avoided visiting them as well; that in turn negatively effectuated the food packaging industry [10]. As per a survey in the U.S. on COVID-19 risk perceptions about food packaging and food delivered in restaurants, more than 50% of consumers were moderately concerned about the food packaging in dine-in restaurants and about 23% of the consumer population were found to be seriously concerned about the restaurant packaging of food [10]. According to a study conducted in China’s five-star hotels regarding the transformation from offline to online food delivery systems as a pandemic response, people were concerned about the packaging and service delivery quality as compared for instance to the food taste, freshness, and brand credibility. About $900 billion per year of the food packaging industry is on the front line worldwide, where the Corona pandemic showed the sharpest decline in the eco-friendly food packaging market. According to a Jewish market report from 17 July 2020, the global eco-friendly food packaging market was valued at $163.5 billion in 2018 which was expected to gain revenue of $248.7 by 2026 but due to the current scenario, it reached only $159.8 billion. Market analysts have expected the market to restore from the losses and grow significantly by the third or last quarter of the year 2022.

4. Nanotechnology for safe food packaging

Nanotechnology progress has contributed to various aspects of food science and industry. One of its major applications is the production of food packages with improved physical properties and enhanced safety. These applications offer new promises for improvement of the efficiency of food packaging. Thus, nanostructures embedded in food packaging systems are used to transform them in intelligent packaging ones because they can detect and neutralize chemical, biochemical, and microbiological alterations and make the consumers aware for these problems [69].

World economy is strongly effectuated by packaging industry. In the USA, about 55–65% of $130 billion are invested in food and beverage packaging [9]. Recently, the use of operative and smart packaging systems for the food, based on meat products, which can be easily contaminated, showed remarkable market increase. The packaging of meat products aimed to suppress the blundering, shunt the contamination, increase the delicacy by enabling enzymatic activity, diminish the weight loss, and keep the specific ‘cherry red’ color in the red meats [36].

4.1. Use of nanomaterials in food packaging

The use of nanomaterials improves packaging flexibility and gas barrier properties – two of the most important characteristics of the process. The innovative nano-packages possess additional exclusive properties, e.g. capabilities to destroy microorganisms that are present in the food substances [41, 42]. Nanomaterials applied in wrapping matters allow the existence of food products for longer periods without causing any harmful modifications of the products’ inherent features [58].

An overview of the applications of nanomaterials in the food industry indicates that concerning food packaging, the electrochemical nano-sensors, nano-films, fluorescent particles, and antimicrobials are the most exploited ones.

Various types of nanomaterials find application in food packaging. Among the pleura, the nanomaterials, nanoparticles, and nanocomposites are those that have a major contribution to the improvement of foodstuff quality and safety. Both possess low molecular weight, mechanical strength, and high barrier capacity against O2, CO2, moisture, UV radiation, and volatiles.

4.1.1. Nanoparticles

Nanoparticles (Fe, Ag, MgO, ZnO, TiO, SiO2) are generated and applied in the industry because of their ability to encapsulate in active compounds; the latter possessing enhanced functionality, stability, and bioavailability [2]. The nanoparticles, incorporated into packaging materials designed for food products, provide for a longer shelf life of these products and their enhanced quality [16]. Those nanoparticles have an antimicrobial effect, that is why they have captured the attention of both the R&D and business for practical applications. Thus, metal nanoparticles, in particular the Ag ones, have been incorporated in polymer coverings (films) due to their antimicrobial properties via an active system (see below) [30]. Ag nanoparticles have been used for material packaging for a long time. It is well known that substances covered by Ag nanoparticles are preserved from contamination. In food packaging, many researchers focused their attention on Ag nanoparticles. However, just a few methods for the application of Ag nanoparticles are certified by European Food Safety Agency (EFSA) to be subjectable to recycling [20]. Various chemical modifications and deposition techniques have been introduced to enhance the attachment of Ag nanoparticles to the surface of plastic materials that help slow the release of the metal ions and their accumulation in the packed food [7].

Using of silicate nanoparticles in food packaging is acting as a hurdle for gases or moisture, and in this way – is reducing considerably the food spoilage and drying.

The application of a big number of nanoparticles in the food industry is characterized by significant antimicrobial power. They can also work as carriers of antimicrobial polypeptides and ensure protection against microbial food damage. For instance, a packaging material is prepared through a coating of starch colloids with an antimicrobial agent, which is acting as a hurdle to microbes by controlling the release of antimicrobials from the packaged material [46].

Nanoparticles are employed as vehicles of different substances: enzymes, antioxidants, anti-browning agents, flavors, and other bioactive materials aiming to improve their shelf life even after the package is opened [23, 24]. The formed reactive oxygen species (ROS) by TiO2 nanoparticles is destroying the pathogenic microbes, thus making them an effective antimicrobial agent.

The above-mentioned inorganic nanoparticles (iron, silver, zinc oxides, carbon, magnesium oxides, titanium oxides, and silicon dioxide) are broadly applied not only as antimicrobial agents but in some cases as food ingredients as well [61].

Nanoparticles are used as well for packaging food substances for modification of the penetration abilities of different packaging foils, increasing their mechanical properties, resistance to heating, and biochemical and microbial obstacle effects [59].

4.1.2. Nanocomposites

The nanocomposites are overtime reactive natural components compared to their macroscale counterparts, a property that is linked to the high surface/volume ratio [49]. Various nanocomposites (Fe-Cr/Al2O3, Ni/Al2O3, ZnO, SiO2) are used for packaging and coating purposes [17, 58]. Among them, SiO2 clay and nanoplates, carbon nanotubes, starch nanocrystals, grapheme, chitin or chitosan nanoparticles, cellulose-based nanofibers, and other inorganic nanocomposites are utilized. Generally, they are filled in a polymeric matrix, and in this way, the matrix becomes lighter and fire-resistant with better thermal properties and low permeability to gases [32]. The charging of active nanoparticles into the polymer matrices rises the completion of the food packaging material and gives functional opportunities like anti-oxidant, antimicrobial, and scavenging, resulting in the longer shelf life of the packed food products [43].

Nanoparticles (< 100 nm) may be involved in different plastics to result in polymer nanocomposites with improved characteristics. For instance, the so-called thermoplastic polymers contain 2–8% nano-scale chargers, such as carbon nanoparticles, nanoclays, polymeric resins, and nanoscale metals and oxides.

The silver in the silver zeolite is amenable to the antimicrobial activity, due to the ROS production. Silver zeolite coated ceramics are applied in food preservation, material decontamination as well as and disinfection of medical products. The extended antimicrobial activity of silver-based nanocomposite is unique to the silver zeolite [8].

The use of carbon nanotubes causes the removal of CO₂ or nasty flavors. The nanoclay in the nanocomposites (bentonite), put-upon in the manufacture of bottles and other packaging materials for food, considerably increases the gas barrier features. In this way, it inhibits oxygen and moisture from diffusion, drink destabilization, and food spoilage. The use of nanocrystals entrapped in nanocomposite plastic beer bottles, proposed by Nanocor (Arlington Heights, USA), diminishes the loss of CO2 and inflow of O2 into the beer bottles, like the natural biopolymer-based nanocomposites [53].

The inclusion of clay nanoparticles in the ethylene-vinyl alcohol copolymer and polylactic acid (PLA) biopolymer was found to refine the oxygen gate and enhance the shelf life of food materials [5]. The modified nanoclays, included in a polymer matrix, ensure mechanical strength and serve as a barrier to gases, volatiles, and moisture. Besides, PLA bionanocomposite, obtained through the inclusion of nanofillers into the biodegradable polymer PLA, indicated faster bio-degradation than its counterpart PLA without nanofillers [44].

Mechanical, thermal, and barrier features of the packaging material have been raised considerably by charging polymer–clay nanocomposites [56]. Hampering of oxidation, tuning of moisture migration, respiration rate, microbial growth, volatile flavor, and aromas are considerably affected by the use of nanotechnology in the packaging industries [13]. Such killing activities towards pathogenic microorganisms were founded also on the chitosan-based nanocomposite films, especially Ag-containing nanocomposites [48]. Essential oil from garlic stiffed with PEG-coated nanoparticles can be used to limitation of stored-product pests [15].

The enhanced shelf life of the food products was efficiently achieved through the use of phytoglycogen octenyl nanoparticles incorporated within Ɛ-polylysine.

Carbon-based graphene nanoplates are resistant to heat and have potential applications in the packaging of food products in the food industry [76].

An oxygen reduction of packaging material is achieved through the application of water-based nanocomposites formed by 1–2-µm nano-coatings on the surface. Other nano-preparations are the nanoemulsions used in food packaging as well as the disinfection of food packaging equipment. Nanomicelle-based products including glycerine restrict pesticide residues in fruits and vegetables and oil/dirt from cutlery. The supplementation of nanoemulsified bio-actives and flavors to beverages mustn’t alter the products’ look [67, 37]. Various food pathogens like gram-negative bacteria must be strongly enthralled by the nanoemulsions.

For everyday applications, zinc oxide is termed a safe material, certified by FDA, and is considered a food additive [50]. These nanoparticles are incorporated in matrices of polymers to provide nanocomposites with good properties such as antimicrobial activity and enhanced packaging properties [52].

Nanocomposites are also used in the packaging of food products. They possess specific characteristics to resist thermal stress during food processing, and transportation and storage of food products, as well. For instance, nanocomposites are used in beer bottles, enhancing their shelf life by up to 6 months.

4.2. Food nanopackaging approaches

The implementation of nanotechnologies in food production leads to smart packaging approaches and systems constituting the so-called active and intelligent packaging. Both systems foresee the improvement of food quality, from production to consumption, applying nanoparticles/nanocomposites for assurance of food protection and safety (Fig. 3).

Figure 3. Various food nanopackaging approaches.

4.2.1. Active food packaging systems

Active packaging is one of the innovative approaches used for packaging foodstuff. Its main characteristic is that the status of the packaged food items changes to improve the sensory quality and the safety of the food products, thus increasing their shelf life [66]. Bioactive packaging provides a positive impact on the health of consumers with the production of packaged foods that are good for health [1].

The systems for active packaging contain agents for moisture regulation, scavengers of CO₂ and O₂, as well as emitters and antimicrobials.

The active packaging systems are used mainly for storage purposes [13]. For instance, envelop systems for packaging are applied for short-term chilled storage. The modified atmosphere packaging (MAP) systems, vacuum packaging, MAP systems utilizing 100% CO₂, and bulk gas flushing ones are used for long-term chilled storage. The commercially used polymeric films for packaging are inert and hydrophobic and have less surface energy in comparison to low-density poly-ethylene (LDPE) and polypropylene (PP). To include antimicrobial substances for stopping food spoilage, modifications of the packaging material surface with functional properties and polar groups are exploited [13].

The modified atmosphere packaging (MAP) system founds wide applications and is used for the distribution, storage, and maintenance of meat products under low temperatures [14]. The lipid oxidation, dehydration, discoloration, and loss of aroma are factors associated with the potential spoilage of processed meats and should be taken into account to extend and maintain the shelf life of meat products. MAP promotes the shelf life and quality of the meat products by saturation the packaging environment of the meat products with formulated gas mixtures. Commonly, in the MAP technology, the non-inert gases such as O₂ and CO₂ are used. Their profiles are changing depending on the factors like the type of product, respiration, materials used for packaging, size of the pack, storage conditions, and package integrity. The uniform dispersion of clay nanoparticles on the transparent plastic film produced by the chemical giant Bayer (Leverkusen, Germany) prevents O₂, CO₂, and moisture from reaching fresh meats and other foods. There are several patents on the applications of nanomaterials in the food packaging filed in the USA, Europe, and Asia, and most of them report the utilization of nanoclays and nanosilver [40].

Another example of active food packaging systems is the use of allyl isothiocyanate and carbon nanotubes to limit microbial contamination and color changes, regulate oxidation, and support the storage of shredded, cooked chicken meat for 40 days [19].

4.2.2. Smart / Intelligent food packaging systems

The smart packaging includes nanosensors that are intended to sense microbial as well as biochemical alterations and provide signals for them [43]. Nanosensors detect microorganisms, toxic substances, and contaminants present in different foodstuffs because of their high resolution and detection capacity [39]. The application of nano-sensors for detecting toxins, pesticides, and microbial contamination in food products, provides a versatile alarm tool for the consumers to detect food spoilage or contamination linked with flavor production and coloring [31].

Improvements in the sensor technology present in the smart packaging of food materials provide information on the quality and safety as well as the half-life of materials [62].

Nanoparticles are applied in the preparation of nanosensors to disclose food contaminants. The nanosensors made for definite purposes are necessary for food analysis, determination of flavors or colors, drinking water, and clinical diagnosis [24]. The usage of nanosensors in food packaging helps in spotting the physical, chemical, and biological modifications during food processing. Nanosensors and nanodevices with the specialized design used in smart packaging assist in finding toxins, chemicals, and food pathogens [57]. This system with sensors and indicators is also applied to follow and display information concerning the quality of the packaged foods over the storage and transport.

Different functional nanomaterials can be used as nanosensors and active packaging materials. They possess considerable technical and hurdle properties, therefore are resourced and targeted to nutrient delivery systems [66]. It was shown that smart or intelligent packaging saves food quality during distribution.

The nanosensors work by monitoring the changes linked with the internal or external environmental stimuli. In brief, the following indicators are used in food packaging:

– Integrity (package integrity determination);

– Freshness (quality of the packaged products);

– Time-temperature (time and temperature-dependent changes).

They are recorded during the production and distribution chain to keep the quality and increase the shelf life of products.

Another smart nano-packaging system is the so-called nanobarcodes, ID tags that are introduced on the base of barcodes developed by nanoparticles [47].

The application of nanosensors in packaging encompasses as well enzymes raising the breakdown of food compounds that makes food improper for human consumption.

The application of nanosensors in the smart packaging systems encompasses as well the identification of gases, chemical contaminants, aromas, temperature and light intensity, pathogens, or the products of microbial metabolism [55].

Advanced analytical techniques like GC/MS, portable headspace O2, and CO2 gas analyzers are used to study the gas phases in the MAP products. However, these methods have certain blemishes; in real-time processes, optical sensor-based methods are more effective than these methods. The same is the effect in the large-scale usage [13].

The filing of food is the main trouble in the food industry and it is mainly a result of bacterial contamination. It is due to leakage of adverse odor but is not easily detected by the human nose, and sometimes causes poisoning. To indicate such kinds of odors linked with food poisoning, strongly sensitive biosensors are necessary [39]. In advanced food packaging, an integrated electronic ‘tongue’ comprises a set of nanosensors that are predominantly sensitive to the gases released from food waste. The device comprises sets of chemical sensors attached to a data processing system that gives a clear and visible signal indicating whether the food is fresh or not, using a sensor strip that changes color [54]. This device is used for a highly accurate determination of volatiles and monitoring the quality control processes in the food industry. Nanosensors were applied in the European project GOODFOOD (2004–2007) for food safety and quality control applications [65].

The intelligent food packaging nano-based systems aim to minimize food losses due to microbial contamination. A variety of nanoparticles (TiO2, MgO, ZnO, Ag, Fe0, C-nanotubes, and fullerene derivatives) have proved their effectiveness as antimicrobial agents [61]. In addition, the application of specific nanomaterials for both detection and elimination of destructive chemicals and pathogenic bacteria has been extensively used recently.

5. Antiviral mechanism of nanoparticles’ activity

The factors like product nature (formulation), processing conditions (intrinsic factors), type of package, and storage and distribution strongly influence the shelf life of a food product.

• The common intrinsic factors include water activity, pH, microbes, enzymes, and the level of reactive compounds. They can be tuned by the utilization of specific raw materials and components and convenient processing parameters.
• The common extrinsic factors are temperature, total pressure, light, partial pressure of various gases, relative humidity, and mechanical stress (human handling). They impacted the rate of degradation reactions during food material storage [76]. Exploiting antimicrobial packaging resulted in effective decontamination in parallel to the usage of antimicrobials as food additives. This result is because the surface microbial growth on the contaminated products is easily accessible for sterilization by surface-acting antimicrobial substances.

Meanwhile, antimicrobial packaging strongly interplays with the food product as well as the environment [12].

Antimicrobial nanoparticles, namely Cu, CuO, MgO, Ag, ZnO, Pd, Fe, and TiO₂, or nanoemulsions/nanoencapsulations, enclosing natural anti-microbial substances that can be adhered to via electrostatic, hydrogen bonding, and covalent interactions are developed to produce antimicrobial packaging systems.

The nanocomposites of organic (chitosan and essential oils) and inorganic (ZnO, TiO₂, and Ag) nature are successfully applied for food preservation through innovative packaging. The polymer coatings due to their chemical structure control the release of the active compounds and thus, regulate the function of the nanocomposites. Polymer matrixes that have been used for nanocomposite production are polyolefins, nylons, ethylene-vinyl acetate (EVA) copolymer, polyethyl-eneterephthalate (PET), polystyrene (PS), polyamides, and polyimides. Following this principle, extended antimicrobial efficiency against E. coli and Staphylococcus aureus has been observed with Ag nanoparticles immobilized in cellulose and collagen coatings for sausages. Although their bactericidal activity, these nanocomposites were not harmful to the consumers and the environment. [12]. Similar antimicrobial activity that lasted for 28 days was found for Ag nanoparticles entrapped in a polyamide matrix. Films of low-density polyethylene (LDPE) coated with Ag nanoparticles exhibit remarkable antimicrobial potential against Gram-positive and Gram-negative bacteria. The same effect was observed for chitosan–silver nanocomposite [29]. Antimicrobial activity coupled with significant mechanical stability was found in ZnO-encapsulated halloysite–polylactic acid nanocomposites. Extended shelf life, slowed down bacterial growth, and lipid oxidation has been observed for meat and poultry products packed in LDPE/ZnO+Ag nanocomposites coatings.

These findings indicate that the antimicrobial characteristics of the nanopackagings comprising nanocomposites depend to a great extent on the characteristics of both the polymer matrix and the nanoparticles. In addition, the storage conditions and storage duration impact the antimicrobial activity of the nanocomposite coating films. For instance, a study of the stability and antimicrobial activity of pullulan films with incorporated Ag or ZnO nanoparticles and essential oils of oregano and rosemary was performed for 7 weeks at various storage temperatures (4, 25, 37, and 55°C). Its findings indicated that the antimicrobial potential of the pullulan nanocomposite films against the common food pathogens L. monocytogenes and S. aureus was maintained at temperature < 25°C, and reduced significantly at > 25°C. [68].

Food nanopackaging with low Ag concentration, with enhanced and stable bioavailability, is a challenge for the application of Ag in food packaging. At present, the citrate-mediated silver complex is the most frequently used standardized silver formulation with antimicrobial action.

6. Conclusion

The respiratory virus SARS-CoV-2 has completely changed the scenario of food industries whether in production, processing, or packaging. There is a need to understand the transmission route of SARS-CoV-2 through food, where street food and openly sold items are of the main concern. Although various vaccines are currently available, there is a strong need to spread awareness regarding the pandemic to enforce the rules for personal hygiene, and avoiding cross-contamination. At present, significant research has been performed concerning antimicrobial food packaging but there is still a shortage in antiviral food packaging development. This imposes the great need to explore the antiviral food packaging incorporated with natural antiviral bioactive compounds to ensure both food safety and sustainability.

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Test LO 5.2

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