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Intelligent food packaging; a review of smart sensing technologies for monitoring food quality Hanie Yousefi, Hsuan-Ming Su, Sara M Imani, Kais Alkhaldi, Carlos D.M. Filipe, and Tohid F. Didar ACS Sens., Just Accepted Manuscript • DOI: 10.1021/acssensors.9b00440 • Publication Date (Web): 13 Mar 2019 Downloaded from http://pubs.acs.org on March 17, 2019

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Intelligent food packaging; a review of smart sensing technologies for monitoring food quality Hanie Yousefi1,2,3, Hsuan-Ming Su2, Sara M. Imani4, Kais Alkhaldi2, Carlos D. M. Filipe3, Tohid F. Didar 2,4,5* 1Leslie

Dan Faculty of Pharmacy, University of Toronto, 144 College Street, Toronto, ON, Canada

2Department

of Mechanical Engineering, 3Department of Chemical Engineering, 4School of Biomedical Engineering, for Infectious Disease Research, McMaster University, 1280 Main Street West, ON, Canada 5Institute

ABSTRACT: Food safety is a major factor affecting public health and the well-being of society. A possible solution to control food-borne illnesses is through real-time monitoring of the food quality throughout the food supply chain. The development of emerging technologies, such as active and intelligent packaging has been greatly accelerated in recent years, with a focus to inform consumers about food quality. Advances in the fields of sensors and biosensors has enabled the development of new materials, devices, and multifunctional sensing systems to monitor the quality of food. In this review, we place the focus on an in-depth summary of the recent technological advances that hold the potential for being incorporated into food packaging to assure food quality, safety, or monitoring of spoilage. These advanced sensing systems usually target monitoring gas production, humidity, temperature, and microorganisms’ growth within packaged food. The implementation of portable and simple-to-use handheld devices is also discussed in this review. We highlight the mechanical and optical properties of current materials and systems, along with various limitations associated with each device. The technologies discussed here hold great potential for applications in food packaging and bring us one step closer to enable real-time monitoring of food throughout the supply chain.

KEYWORDs: functional packaging, food quality, flexible sensors, real-time monitoring, smart packaging, hand-held detection devices, biosensors 1 ACS Paragon Plus Environment

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As reported by the World Health Organization (WHO) in 2017, an estimated 600 million cases of illness were caused due to contaminated food supplies and 420,000 people die every year as they are affected by of foodborne contamination.1 In addition, diarrheal diseases, which are primarily caused by consuming contaminated food, result in over 550 million illnesses.1 Even in a highly developed country such as Canada, foodborne illnesses have led to over 238 deaths per year 2, with 1 out of every 8 Canadians being affected by food related sicknesses.2 Total food quality is defined by several factors such as food health, consumer standards, nutritional values, stability and other factors that differ in various countries.3 Food quality is a reliable indicator for food health which is a crucial factor to control the effect of the food on consumers’ health. Therefore, quantifying the food quality has been a goal for the food industry.4 Currently, expiration dates have been used for estimation of food quality and determining the food recall time.5 The lack of real-time information about the food source and the inability of reporting the real-time condition of the food put the consumers in risk of foodborne illnesses even when they follow standard regulations. On the other hand, early food recalls lead to billions of dollars of waste each year which is another undesired result of inaccurate and pre-determined expiration date.6 All this generated the urge for developing systems that can be incorporated to food source while it is in storage period. Recently, researchers have been trying to develop systems that can report of the food health or its quality in realtime. Currently, these efforts led to the start of a merging field with the goal to potentially incorporate the recent advancements and prototypes in developing sensors into the food packaging industry.7 Traditionally, packaging materials have been primarily used as passive, inactive, and inert barriers designed to prevent moisture, oxygen, and contaminants from reaching the food product, thereby preserving the food quality in an acceptable range and protecting it against chemical and mechanical stresses.8,9 The level of functionality that can be incorporated in packaging materials is rapidly expanding with the development of new materials and innovative methods to detect and report the food quality in a real-time fashion. Active and intelligent packaging will play a key role towards improving food safety, 2 ACS Paragon Plus Environment

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specifically to enhance food quality and minimize the need to use food preservatives.8–10 In active packaging, the product, package, and environment interact with each other, and actively work towards the enhancement of the food’s condition and increase its shelf life. The characteristics studied in active packaging can be utilized as an extension on the traditional and common way of food packaging systems.8,11 The goal of intelligent packaging is to allow for monitoring of the packaged food and/or the surrounding environment, by providing the costumers with information regarding the quality and safety of the food through a variety of signals.12 A rapidly growing number of scientific articles have been published in the past decade with focus on food safety/health monitoring.11,13,14 There has also been extensive research on monitoring packaged food15–18 and some reports on the development of handheld devices that can be used in conjunction with packing materials to make the sensing and reporting of spoilage possible.19–22 We are, however, still far away from achieving the final goal of having a generic intelligent packaging that will enable food safety and quality monitoring in a commercial scale. In this review, we first focus on basic concepts regarding the main food quality indicators and how these can be used to make recall decisions more accurate. These indicators are commonly mentioned in the literature and incorporated in prototypes of smart food packaging to report food quality, safety, or spoilage of food. The second section of this review will address the efforts made towards developing sensors that have been incorporated in food packaging or have the potential to be incorporated in packaging. Lastly, we compiled a list of handheld devices with potential for being used in commercial places (such as supermarkets) or in central distributing locations. These devices can increase the efficiency of monitoring food quality throughout the entire supply chain. 1. Food Quality Indicators To create sensors incorporated within food packaging, specific indicators are necessary to represent the state of the food product, either quantitatively or qualitatively. Indicators associated with food spoilage are usually linked to physical or chemical changes in the characteristics of the specific food. Early detection of these indicators can prevent the consumption of unsafe food and consequently decrease the 3 ACS Paragon Plus Environment

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chances of food-borne illnesses in consumers and prohibit potential outbreaks.23 The most commonly used indicators for food quality and safety are discussed in the following section. 1.1. Oxygen and Carbon Dioxide Oxygen is essential for combustion or for certain biological activities. Some examples of oxidation reactions that causes food quality degradation are: fat oxidation, browning reactions and pigment oxidation.24 Carbon dioxide, on the other hand, is a colorless and odorless gas that inhibits bacterial and fungal growth, while at the same time capable of decreasing the pH in food environment. Carbon dioxide inhibits Gram-negative aerobes such as Pseudomonas spp. that easily initiates microbial spoilage.25 The antimicrobial eﬀect of CO2 is due to its ability to create an anaerobic environment that prevents decarboxylation (enzymatic). The accumulation of CO2 may also perturb the permeability of the membranes of certain microorganims.26 Controlling the amount of CO2 is, therefore, very important to prolong the shelf life of food products.27 A MAP for non-respiring foods typically consists of a low O2 concentration (0-2%) and a high CO2 concentration (20-80%), with some variations occurring between different food products.28 Any changes to the gas concentration/composition may thus be a reflection of deteriorated food quality, signaling the consumer of potential of unwanted microbial activity.29 1.2. pH Change Many microbial metabolites can affect the pH of the food environment, which suggests that monitoring the change in pH can be an effective method of identifying food spoilage.30 Within food packaging, certain aerobic and anaerobic microorganisms are able to proliferate during storage period of the food products. Organic acids (e.g. lactic acid and acetic acid) are the major compounds that result from glucose fermentation.31 These metabolites can decrease the pH of the food samples. Moreover, ethanol is another end product of the metabolism of lactic acid. However, the change in pH due to ethanol is subtle, as it is only slightly more basic than water.

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Carbon dioxide (CO2) gas is produced by microbial growth, which can dissolve in food samples and form carbonic acid.9 The hydrogen ions from the carbonic acid then may dissociate to form hydrogen and bicarbonate ions. A hydrogen ion, as a proton, combines with a water molecule to form a hydronium ion, which then subsequently decreases the pH of the sample.32 1.3. Humidity Maintaining constant humidity levels inside the food packaging is an essential requirement to preserving the condition and texture of food products,33,34 as it promotes longer shelf life. The influence of the humidity level is highly important in diverse areas of food industry, from dairy, meat, to dried food.35 The humidity inside the packaging can be altered in different ways. One common mean is the breakage of the sealed package of the food as a result of poor manipulation.36 Another reason that can possibly alter humidity levels in the inner compartments of the packaging is prolonged exposure to extreme temperature fluctuations. This can cause condensation to occur, compromising the integrity of the packaging system. Humidity is a key indicator that should be followed when testing for food quality as increased moisture provides a favorable growing environment for microbial and fungal,37 thus becoming a safety issue for the consumption of the product. In addition to microbial growth, humidity also leads to shorter shelf life due to deterioration of the dry product, causing softening and dampening of the product. 1.4. Temperature Another indicator to be investigated in relation to food spoilage is temperature. Temperature extremes and fluctuations have a strong impact on the shelf life of refrigerated food products. Temperature fluctuations can occur at any point in the distribution chain, such as loading, unloading, temperature cycling in walk-in coolers, storage displays and home transport.38 Monitoring and control of storage temperature of food products, such as fish, is crucial,39 since temperature largely determines the rate of microbial activity.39 A particular threat in major food product types is also present during refrigeration, since the relevant temperature range is between 4-12°C, which is an ideal range for growing some psychotropic bacteria and thermo-tolerant fungi..40 5 ACS Paragon Plus Environment

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1.5. Specific Chemicals Animal products such as poultry, beef, fish, and dairy are a group of consumables that bare a wide range of microorganisms in them. These group of products are also prone to undergo undesired growth of pathogenic microorganisms which release specific chemicals while growing. The growth of this group of microorganisms can be studied by tracking the presence and concentration of these chemicals. 41 Fish is one of the most perishable aquatic products that is susceptible to specific spoilage organisms (SSO),42 which spread into various tissues after death, degrading and compromising the integrity of the product. As the microbial degradation occurs, these SSOs release chemicals that have been directly linked to the spoilage in fish products. These chemicals include volatile amines (trimethylamine, dimethylamine and ammonia),43 histamine putrescine, cadaverin, short chain carbonyls, N-cyclic compounds, and unsaturated aldehydes.44 All of these chemicals are possible indicators for monitoring fish spoilage. 2. Methods Used for Monitoring Food Quality As stated above, there are several indicators that can signal a decrease in quality of consumer food products. Table 1 provides a summary of the currently developed sensors for monitoring packaged food quality and their developmental stage. These sensors are created on a wide range of materials, such as plastic, polymer, paper, glass, and microfluidic devices. Depending on the characteristics of the selected substrate, these sensors can have a variety of applications, serving different purposes. 2.1. O2 Detectors Modified Atmosphere Packaging (MAP) has been introduced by Young et al (1984) to prolong the quality of food products.29 In MAP, most of the air is either removed before sealing the product, or replaced with another gas mixture.45 The most stringently controlled gases in MAP are: oxygen, nitrogen, and carbon dioxide. Sensors capable of monitoring the changes in the oxygen gas level in a MAP are currently available. In general, these sensors operate under 3 types of mechanisms.46 The luminescent probe molecules are usually trapped in a gas and ion permeable material ( e.g. silicone rubber), or an 6 ACS Paragon Plus Environment

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organic polymer ( e.g. poly(vinyl chloride)), to create thin films, such as the OxySense system.46 The drawbacks of a luminescence-based indicator system is the lack of a response that is visibly discernible and so they require the use of expensive analytical instrumentation to interrogate the labels, rather than the simple use of the human eye.46 Table 1: Developed sensors for monitoring packaged food quality Detection target

Sensing mechanism

Reporting method

Substrate/material

Development stage

Ref.

Timetemp

Redox reaction to oxygen defusion

Color change

Paper or plastic

Commercially available

47–50

CO2

pH

Color change

Plastic film, aqueous solution

Luminescence dye

Fluorescence signal

Plastic film, organically modified silica matrix

Proof of concept 31,51

Proof of concept 52–54

Proof of concept O2

Oxygen molecule quenches electronically excited lumophore

Redox dye, reducing agent, alkaline environment

Luminescence

46,55

Silicone rubber, organic polymer Commercially available

Color change

56–61

Plastic, organic polymer Proof of concept 13

Humidity

Change in the dielectric constant

Wireless detector device

Paper


RFID tag wirelessly connected to a VNA

Paper

Proof of concept

62


RFID reader

Paper

Proof of concept

63

Proof of concept ChemicalTVBN

Chemosensitive Compounds

Color Change

Polyaniline film

64


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ChemicalArray

Bacteria

41

Color Change

Silica gel plate

Bright-field imaging, electrochemical signal

Microfluidic device

Aggregation of paramagnetic silica beads correlates with the amount of DNA of interest

Cellular device

Paramagnetic silica beads

Graphene nanosheet traps E. coli

Change in impedance spectroscopy

Graphene based flexible acetate sheet

Proof of concept

E. coli specific DNAzyme

Fluorescence

Cyclo-olefin polymer (COP)

Proof of concept

Chemosensitive Compounds Antibody interaction

Proof of concept 65–68

Proof of concept 69

70

71

Colorimetric redox based indicator sensors, such as the Ageless Eye (Figure 1a),61 are based on simple reversible redox chemistry. The system is typically comprised of a redox dye, such as methylene blue (MB), and a strong reducing agent, such as glucose in an alkaline medium.32,72 This system changes color from purple to pink after 2–3 hours, when the ambient gas is changed where the level of oxygen is 0.1%, and reverts back to purple in 5 minutes upon exposure to an ambient atmosphere containing 0.5% oxygen. These systems require anaerobic storage and handling condition, since after less than 10 minutes of exposure to air, the absorbance of this indicator decreases drastically.60 This poses a major problem to their routine use in MAP. Another type of oxygen sensors are phosphorescent sensors that can be installed on the packing and can report the oxygen absence in the container. In this type of sensors usually an O2 sensitive dye is incapsulated in a polymeric host that is O2 permeable and allows the dye to have access to O2.73


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a)

b)

c)

Figure 1. (a) Ageless Eye utilizes a colorimetric redox dye system to monitor the concentration of oxygen gas. Adapted from ref 61 with permission from Mitsubishi Gas Chemical Company Inc. (b) Visual color changes of colorimetric mixed-dye–based indicator labels when exposed to CO2 levels ranging from 0-23% (v/v). Adapted with permission from ref 74. Copyright 2014 Elsevier. (c) Colorimetric carbon dioxide sensor using food grade mixture constituted of an amino acid (L-Lysine) a polypeptide (-poly-l-lysine, EPL) and natural occurring dyes (anthocyanins). Photo was taken after 10 min. From left to right: cap not exposed to CO2, caps exposed to 50 mg, 150 mg and 300 mg of CO2, respectively. Adapted with permission from ref 51. Copyright 2018 Elsevier.

To solve the problem associated with these colorimetric systems, researchers have created a colorimetric light-activated, redox dye-based system.56–58 In general, this system comprises of photo-excitable dyes, that makes the film not functional unless and until it is irradiated with UV or with visible light.46 This UV-activated oxygen indicator ink is generally coated onto the inner side of food packaging films. The main, and very serious problem associated with this type of set up is that the redox dyes encapsulated in the water-insoluble polymer film leach out when in contact with water from the food. As the indicator is placed inside the package, the leached dye can not only stain food undesirably, but also become a potential 9 ACS Paragon Plus Environment

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health hazard.75,76 Most recently, Vu and Won had successfully applied alginate polymers to prevent dyes from leaching out of the colorimetric oxygen indicator films. The cation-binding ability of alginate can bind to redox dye and thus prevent the dye from leaching with the water.59 2.2. CO2 Detectors Optical sensors used in the monitoring of CO2 within food packaging can be categorized into two groups: (i) sensors based on luminescent dyes that change their fluorescence upon exposure to CO2, (ii) colorimetric indicators based on a pH indicator that generate visible color changes.31,51–53,74,77 Although luminescent dyes provide very good analytical performance, they require the use of sophisticated instrumentation (for excitation and sensing, e.g. portable instruments and hand-held scanning devices).51– 53

One of the earliest examples of such devices was created by Mills and Change, where they incorporated

HPTS (8-Hydroxypyrene-1,3,6-trisulfonic acid) into a plastic film to produce a fluorometric CO2 sensor with a 0 to 90% response and recovery time of 4.3 and 7.1 s, respectively.54 The stability of the HPTS system was improved when Bultzingslowen et al. immobilized the fluorophore molecule in a hydrophobic organically modified silica (ormosil) matrix.52 They also improved the sensitivity by incorporating a dual luminophore referencing system, where the analyte-sensitive intensity signal is changed into the phase domain by co-immobilizing an inert stable reference luminophore with similar spectral characteristics. Unfortunately, the chemical ingredients employed for sensor fabrication are not food grade, thus it is critical that such chemicals do not come in contact with the food product.51 Recent efforts for the development of CO2 sensors incorporated into food packaging, has mainly focused on the use of colorimetric indicators. Colorimetric indicators are in general not very sensitive, but employ cheaper ingredients and do not require the use of additional instrumentation (Figure 1b).74 Colorimetric pH dyes such as m-cresol purple, have been used to generate a range of thin, colored plastic films that changes color upon protonation/deprotonation.78 Good shelf life can be also achieved with water-based systems especially for application in food products that need to be stored in a controlled temperature and humidity.51 10 ACS Paragon Plus Environment

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Additionally, researchers have shown functional designs using food grade mixture constituted of an amino acid (L-Lysine) a polypeptide (-poly-l-lysine, EPL) and natural occurring dyes (anthocyanins), as seen in Figure 1c.51 They are suitable candidates for a large-scale production of labels that can be applied inside food packages in order to give simple signals to the consumer related to food preservation. 2.3. Specific Chemicals and pH Changes that Indicate Spoilage Certain chemical changes that occur during food spoilage, especially in the case of fish, are linked to specific microbial growth known as specific spoilage organisms. One food spoilage indication system that has been developed to detect these chemicals is the colorimetric assay. The colorimetric detection of this chemical provides a valid alternative to real time sensory method that can be embedded in packaging. Kuswandi et al. constructed an indicator out of polyaniline film that is embedded in the packaging, which then produces a visible color change in response to the presence of amine, indicating the degree of spoilage in the product.64 Another application of colorimetric assay was performed using an array of sixteen different chemo sensitive compounds for colorimetric detection of known food spoilage compounds that include trimethylamine (TMA), dimethylamine (DMA), cadaverin (Cad), and putrescine(Put).41 The negative controls placed in this study were hexanal & 1-octane-3-ol, due to their presence in fresh unspoiled fish products. The study found that in response to TMA, methyl red, bromocresol green, crystal violet lactone, and alizarin exhibited the highest signal response to TMA. In the case of DMA, the strongest response was elicited by Rosolic acid, Cresol Red, Chlorophenol Red, Methyl Red, and Xylenol Blue. Although other compounds such as Curcumin, Bromothymol Blue sodium salt, and Bromocresol Purple had the weakest response in relation to the spoilage compounds being tested. With that said, they should still be included since food spoilage is much more diversified in food samples around the world. These additional chemo sensitive compounds could react to other food spoilage compound varieties that were not present in the samples being tested. This increases the reliability of this sensor system in detecting a broader range


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of possible spoilage compounds that are associated with the degradative metabolic processes,79 thus improving the safety and quality control of the food product in question. In addition to colorimetric assays, electrochemical sensors have also been used to detect volatile amine (Figure 2).80–83 Bhadra et al., for example, created a hydrogel-coated pH-electrode passive sensor capable of monitoring basic volatile concentration (Figure 2a).83 The system uses a passive resonator whose resonance frequency varies based on the concentration of volatile amine in the surrounding environment. The change in the resonance frequency can be detected by monitoring the impedance of an external coil coupled to the sensor. This system is wireless, low cost, passive, and capable of detecting ammonia gas concentration with a detection limit of 0.001 mg/L (Figure 2c).83 Several groups are recently developing chicken, pork, and beef spoilage sensors with same mechanisms by simply embedding pH sensitive material into the packaging.

84,85

Although, these reports are basing the measurement on the simple

chemical or pH changed that can indirectly indicate food spoilage.

Figure 2. Examples of devices designed to monitor for chemical analytes that can be indicators of spoilage in fish. (a) A Wireless device to detect spoilage in Tilapia. Adapted with permission from ref 83. Copyright 2015 Elsevier. (b) Colorimetric sensor to detect volatile amines that can be used to monitor freshness in Salmon samples. Adapted with permission from ref 41. Copyright 2016 Elsevier. (c) A semiconducting device to detect fish freshness through the ammonia release. Adapted with permission from ref 82. Copyright 2002 Elsevier.


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2.4. Humidity Sensors Humidity is an important environmental factor in the prevention of food spoilage. This has led to the development of numerous humidity sensors for real-time monitoring of packaged foods in order to promote shelf life.13,62,86–89 The work by Tan et al. discusses the application of a low-cost material, in development of a wireless sensor for in situ humidity monitoring of dry food quality.13 The construction of the sensor consists of a planar inductor and capacitor on a paper substrate, placed on the inside wall of the package in question, as seen in Figure 3a. The response is detected wirelessly using a coil that is connected to the detector. As the humidity increases due to food quality degradation, the substrate absorbs water vapor, thus, changing the capacitor’s capacitance and resonant frequency of the sensor.13 Furthermore, the resonant frequency is measured by reading the impedance in the detection coil with the analyzer. Feng et al. proposed the application of a humidity sensor integrated in a fully printed Radio Frequency Identification (RFID) tag.62 Five types of paper substrates were used in varying humidity levels from 20-70%. The paper substrates included: polyethylene terephthalate (PET),90 polyimide non-organic coated inkjet paper, commercial inkjet photo paper, and commercial UV-coated packaging paper. The use of paper as a substrate provides a low-cost platform, while retaining high sensitivity and a reasonable response time. The construction of the humidity sensor tag utilized two planar inductor-capacitor resonators using inductive coupling to work wirelessly. One resonator encodes the ID data with the use of the frequency spectrum signatures, and the other one operating as a humidity sensor. The sensing mechanism works similarly to the humidity sensor discussed by Tan et al., mentioned above, i.e. by measuring the resonant frequency caused by the change in the dielectric constant of the substrate due to humidity.91,92 The measurements were obtained wirelessly using a copper loop antenna connected to a port vector network antenna (VNA) as a reader antenna. Out of all of the substrates studied, it was observed that PET was the best substrate to use, due to its lower water absorbance.62 Salmerón et al. also reported on the use of RFID tags as humidity sensors.63 They utilized a screen printed spiral inductor working as an antenna with two different inkjet printer using resonant circuits (LC resonators). The first 13 ACS Paragon Plus Environment

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resonator was used as a threshold tag with an RFID chip, which can be detected using an RFID reader if there is humidity present.63 On the other hand, the other approach utilizes the resonant structure as quantitative humidity sensors based on the change in resonant frequency due to humidity, similar to previously discussed applications.62,86–89

Figure 3. (a) LC humidity sensor is attached to the inside wall of the package. The response is wirelessly measured through the detection coil connected to the sensor reader. Adapted with permission from ref 13. Copyright 2007 MDPI. (b) Experimental setup for real-time humidity monitoring. Adapted with permission from ref 13. Copyright 2007 MDPI.

The applications of this type of sensor systems include dry packaged food, such as cereals and fried or baked snacks, since these foods must remain dry in order for the quality of the product not to be compromised. The inexpensive fabrication processes used to make these previous sensors indicate that they are viable options for commercial applications. There is still work needed to be done to optimize humidity sensors to prolong shelf life.13,62,93 2.5. Time-temperature Sensors Time-temperature indicators (TTIs) are devices attached to food products that provide a visible response to the temperature history, which resulted from at least one changeable observable property similar to either irreversible mechanical, chemical, electrochemical, enzymatic or microbiological change.47,94–96 One TTI device currently in use goes by the name of Fresh Check,96 manufactured by TempTime Corporation in USA. The indicator is made by solid state polymerization of a thin colorless acetylenic 14 ACS Paragon Plus Environment

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monomer layer, which changes to a highly-colored opaque polymer over time. The rate of polymerization is dependent on the temperature that the sensor is exposed to.

a)

b)

c)

d)

Figure 4. A collage of currently implemented Temperature-Time Indicator sensors. (a) illustrates the fading of the color in the time temperature indicator at 25◦C. Adapted with permission from ref 97. Copyright 2008 Elsevier. (b) Tempix® indicator reveals if a particular product has been exposed to temperatures exceeding the threshold limit. Adapted from ref 49 with permission from Tempix AB. (c) Timestrip® PLUS™ indicates periods of time where the product exceeds a certain specified temperature. Adapted from ref 50 with permission from Timestrip UK Ltd. (d) Vitsab® L5-8 Smart TTI Seafood Label. Orange indicates that thermal exposure is over the safe limits recommended by the FDA. Adapted from ref 48 with permission from Vitsab International AB.

2.6. Biosensors for Bacteria Detection Microbial growth can contribute to food quality in two possible ways: (1) microbial growth of the organisms that is normally present in the food supply. This determines the microbial quality of food and is associated to food spoilage. (2) pathogenic microorganisms’ growth which can happen due to poor handling and contamination in any stage of the food chain (e.g. Pathogenic strands of E.coli).15 Currently, bacteria are among the leading cause of food-contamination related deaths, making them an important target for detection in monitoring food safety.98 Unfortunately, traditional methods for bacteria detection rely heavily on sophisticated laboratory techniques such as nucleic acid sequence-based amplification, 15 ACS Paragon Plus Environment

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immunological analysis, bacterial culture, and colony counting.99–102 While these methods are excellent as they provide high sensitivity, they are generally very time consuming and not accessible to the general public. Over the past few years, researchers have attempted to address these accessibility problems through creation of bacteria-detecting devices that required minimal user intervention and that are easy to read, however majority of them are destructive and require the food package to be opened for analysis. Several researchers have detected bacteria using lateral-flow strip (LFTS) assays.65,66,103,104,105 Here, bacterial cells are mixed with antibody labeled with colloidal gold or palladium nanoparticles (PdNPs) and applied to a test strip. Through capillary action, these complexes migrate on the test strip and are captured by another antibody previously immobilized onto the strip, creating a colored line or spot that is then visible to the user (Figure 5a). This process takes approximately 15 minutes and does not require special equipment. Researchers so far have used this technology to detect Listeria monocytogene and bacteria in the Klebsiella group.65,66 Several researchers have created portable microfluidic devices that can be used for bacterial detection.106,107 Tokel et al. created a device with a gold-coated surface that is functionalized with antibodies that responds to certain antigens on the surface of the Escherichia coli.67 The accumulation of bacteria can then be visualized using bright-field imaging. Altintas et al. utilized the similar principle of immobilizing E. coli specific antibody onto gold-coated surfaces.68 Additionally, they reported to have embedded sensor chips that offer real-time electrochemical detection, shown in Figure 5b. Other devices include an E.coli sensor on graphene based flexible acetate sheets, created by Basu et al., that uses electrodes as the main method of detection.70 Their graphene nanosheet is able to trap E. coli cells which will cause a change in impedance spectroscopy, which can be detected. DuVall et al. created a phone application that calculates the presence of bacteria based on the aggregation of paramagnetic silica beads.69 The cells are first lysed, followed by a target DNA strand amplified through loop-mediated isothermal amplification (LAMP). The amplified target DNA subsequently causes the beads to aggregate (Figure 5c). Lastly, Yoon, Lee, and Park utilized laser speckle decorrelation to monitor the presence of micro-organisms in tissues.108 Under a static turbid medium, such as an uninfected food sample, the 16 ACS Paragon Plus Environment

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reflected laser will show a static speckle pattern. In the presence of living microorganisms, the reflected light experiences dynamic speckle pattern, which can then be quantified to determine the amount of contamination (Figure 5d). While these approaches have been successful in improving the ease of bacterial detection and have the potential to be used in monitoring food quality, they all still require active user intervention and complex laboratory/analytical techniques. Techniques such as surface functionalization,109 micro-contact printing,110–113 and automated printers71 have also been extensively used to pattern and functionalize surfaces for detection of target cells. Recently, Yousefi et al. created a simple E.coli-detecting device that is capable of being incorporated into food packaging, shown in Figure 5e.71 This method of detecting bacteria involves the use of DNAzymes, which are synthetic, singlestranded DNA molecules capable of performing a specific reaction. The implemented DNAzyme molecules specifically react with E. coli and cleaves an RNA nucleotide that exposes an embedded fluorophore upon coming into contact with the target bacteria, leading to an increase in fluorescence signal that can be detected by the user.71 In this work, DNAzyme microarrays were immobilized onto thin, flexible, and transparent polymer films that can then be package with the food product. This technology has shown promising application in detecting target bacteria within food samples without the need to open the package which sets a significant milestone in the development of smart packing sensors.71


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Figure 5. (a) Schematic representation of lateral-flow test strips (LFTS) where the formation of a visible line in the testing zone signals the presence of target bacteria. Adapted with permission from ref 104. Copyright 2015 Korean Society for Agricultural Machinery. (b) E.coli specific antibody immobilized onto a gold sensor chip inside a microfluidic device for realtime electrochemical detection. Adapted with permission from ref 68. Copyright 2018 Elsevier. (c) Aggregation of paramagnetic silica beads that increases with the presence of target bacteria DNA. Adapted with permission from ref 69. Copyright 2015 PLOS. (d) Laser speckle imaging used to monitor moving particles. Under a static turbid medium (i.e. tissue), reflected laser have static speckle pattern. In the presence of living micro-organisms, reflected light experiences dynamic speckle pattern. Adapted with permission from ref 108. (e) DNAzyme sensor on cyclo-olefin polymer (COP) that is wrapped inside food package. The increase in fluorescence signal upon exposure to E. coli informs user of the presence of bacteria. Adapted with permission from ref 71. Copyright 2018 American Chemical Society.

3. Tracing Devices 3.1. Handheld Devices 18 ACS Paragon Plus Environment

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The use of handheld devices, such as smartphones in conducting real-time testing is an area of increasing interest. Not only are smartphones powerful and reliable, but they are also widely available for the general public.114 According to the Global Smartphone User Penetration Forecast, it is predicted that world smartphone usage will increase by 58% from 2016-2022.115 Furthermore, it is also predicted that 44% of the world population will own smartphones by 2017.115 Thus, being able to implement a piece of software into the smartphone that works in tandem with a sensor is highly desirable, since the sensor will gather all the data and the phone/software will then be able to process it into readable information for the user. Although the technological advances in smartphones are immense, they cannot function alone as laboratory grade equipment and need to be augmented with certain attachments in order to be a viable options for real time food monitoring applications.116 Studies have been done to investigate smartphones’ properties in different monitoring applications, such as fluorescent imaging, and colorimetric assays.114,116,117 Zhu et al. developed a detection platform to determine the concentration of E.coli in water samples.117 This platform is attached to the readily available camera system of the smartphone. The water sample is then inserted into capillary tubes, which are functionalized with anti E. coli antibodies. Afterwards, secondary antibodies combined with quantum dots are loaded into the capillaries, producing a fluorescent signal. The signal is due to the nature of the optical and chemical properties of the quantum dots, which are inorganic nanocrystals, thus providing an intense fluorescence signal due to excitation through the phone’s UV-LEDs.117 The fluorescence is then passed through another lens into the phone’s camera lens. The subsequent concentration of the of E.coli is determined by quantifying the fluorescent light emission from the capillary tubes (Table 2).116 The imaging capacity of cellphones can be utilized not just for pathogen testing, as described in the example above, but also for applications in the food allergen testing field, which is of great importance due to the serious life threatening allergic reactions triggered by very small traces of allergens.118,119 The


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U.S. Centers for Disease Control and Prevention reported an 18% increase in food allergies for children between 1997-2007.120 The Ozcan lab, at the University of California Los Angeles has designed and manufactured a device that attaches to a cellphone which is called iTube121. This device provides a sensitive, cost efficient, and compact system for the detection of food allergens in samples. The attachable device contains two tubes, a plastic Plano-convex lens, two LED diodes, two light diffusers, and circular apertures to spatially control the imaging field of view. Once the control and the test tubes are prepared according to an allergen specific sample preparation, they are inserted into the device. The transmission intensities is then captured by the cellphone camera, which is then digitally processed using a custom application to quantify the amount of allergen present in the sample, in comparison of the control and the test tube (Table 2).121 Table 2 provides a summary of proposed handheld applications in detecting contaminants and monitoring the sample. For each application discussed, the table outlines the detection target, methodology, materials, accuracy/detection limit, smartphone usage, and a schematic diagram of the proposed system. 3.2. RFID RFID technology enables automated identification, with the help of sensors, to gather information without the need for human intervention.122,123 RFID technology can be grouped in essentially three different approached: passive, semi active and active. The passive approach relies on radio waves emitted from the reader. These waves will cause the coiled antenna within the identification tag to create a magnetic field that is used for energy, sending the information to the reader.124 Semi active RFIDs, on the other hand, use a battery to maintain memory and modulate the waves emitted from the readers antenna.125 In active tags, while also containing a battery, the battery serves the purpose of powering the microchip circuitry and signal broadcasting.11


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The Yan group at the University of Toronto constructed a wireless, passive, vapor sensor that comprised of carbon black, which is known to swell in the presence of certain volatile chemicals, in addition to a polymer that acts as the sensing element.126 When both elements were integrated as the circuitry of RFID tags, they produced resistant changes that changed the outputs signal frequency of the tag.126 For the identification of different vapors, the sensor system was exposed to an array of tags with 16 different polymers, where different gas to solid partition coefficients of the polymers produced an identifiable pattern of signal changes to identify which vapor is present. This method was successful in detecting water, ammonia, ethanol and toluene. All of these vapors have applications and implications related to packaging and food quality. Another application of this technology, that is currently under development, is the detection of different biogenic amines that are associated with food spoilage. The construction was very similar to the vapor sensor system, but instead of polymer composites, maleic anhydride was used as the sensing material.127 RFID applications are economically feasible since RFID tags can be printed on packaging using conventional methods (e.g. screen printing and inkjet).122 By combining RFID technology with compatible materials, labs can provide real time information to readers, which are vital in determining the quality and safety of the food. Currently, RFID technologies are available in the market for monitoring temperature, humidity, light exposure, pressure, and pH.124,126,128 Thus, with the technologies that are already being implemented, as well as the economic and commercial feasibilities of RFIDs, vast implementation of RFID tags in packaged food products can be achievable.11 4. Conclusions and Future Directions

Various emerging technologies in different fields of food monitoring applications have been discussed above, as well as a framework of the devices and materials currently being used for on shelf food monitoring in response to contamination or spoilage of any sort. Different fields of science are converging in the efforts to develop breakthroughs for integrating sensing and packaging technologies throughout numerous sectors across the food supply chain.12 These innovations are important to extend shelf life, and 21 ACS Paragon Plus Environment

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furthermore, to improve the quality and safety of food products, while providing information about the product in question. Current implemented technologies are limited in terms of their commercial application due to the cost of developing and manufacturing such integrated sensory systems. However, with the technological advances discussed above, it is expected that the field of intelligent packaging will experience tremendous growth in terms of commercial implementation over the next decade.11 While there are still many hurdles to overcome, the next generation of intelligent packaging will nevertheless provide a higher avenue of quality assurance and maximization of shelf life, all in order to meet the demands of an ever-growing food supply chain.11 With the current biosensing probes and elements that have been developed, researchers can create smart packaging or smart barcodes that can be installed in the food packaging and scanned when needed to clarify the security of the food source.

Table 2. Summary of detection methods proposed in conjugation with smartphone usage applications Device Design

Target, Report Methods and Materials

Accuracy

E. coli

5–10 CFU.mL-1

Reference Reproduced from ref

Fluorescence

117

with

permission from The

Quantum dots, UV LED, Ab

Royal

Society

of

Chemistry.

Adapted rbST antibodies in milk

Microsphere fluorescent immunoassay

80% true (+) rate and 95% True (-) rate

with

permission from ref 129. Copyright 2014

Springer

Nature.

Ab, UV &white LED, quantum dots


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Food allergen

1ppm

Reproduced from ref

121

permission from

Colorimetric transmission intensities

The

Royal

Society

Immunoassay strip

of

Chemistry.

2 test tubes,2 LEDs, ELISA test kit

Okadaic acid and saxitoxin

with

2.800 ng mL-1 OA & 9.808 ng mL-1 STX

Reproduced from ref

130

permission from The Society

3D printed adaptor

with

Royal of

Chemistry.

Fluoride Colorimetric Water chamber adaptor

1.23×10-4 mg/L Adapted

with

permission from ref 131. Copyright 2016 American Chemical Society.

AUTHOR INFORMATION Corresponding Author Prof Tohid Didar Email: [email protected], Funding Soursces NSERC Discovery grant and McMaster Start-up funds. Author Contributions


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The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. VOCABULARY

Food Quality. The characteristics of the food source that is acceptable for the consumers. All properties and measurable attributes of a food item will contribute in its quality. Food quality is assessed by the three accepted categories of quality: sensory value, suitability value, and health value. Acceptable food quality is usually predicted by expiration dates.132 Food Safety. Also known as food hygiene and food health, indicates the safety of the consumers as the result of using the food source. Food safety is of great importance over the world, making healthcare institutions of many countries to find ways to monitor production chains.133 Real-time Monitoring: The constant screening for food health or quality is called real-time monitoring of food. To be able to constantly report on food source, a monitoring device should be installed inside the food packaging to eliminate the need for opening the packaging of the food.123,134 The device should be able to detect specific ligand that can correlate to the food source decrease in quality or health and also should be able to report that detection in a way that can be understood by operator (e.g. electrochemical signal or color change).135 Functional Packaging: Functional packaging is referend to package designs that have low impact on environment and high functionality to deliver food to consumers. The functionality can be enhanced by increasing the shelf life of the food source by preserving its quality during the supply chain. A method to introduce functionality to food packaging is to add the ability to monitor food health in a real-time manner so the consumers can confirm it before consumption.136,137 Foodborne Illness: Foodborne related illness is any health problem that is a result of consuming spoiled or contaminated food product. Foodborne illness can cause accurate or chronic conditions and might need medical attention and can cause serious conditions like hospitalization or death.138 24 ACS Paragon Plus Environment

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