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Carbon dioxide sensors for intelligent food packaging applications
Food Control 25 (2012) 328e333
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Food Control journal homepage: www.elsevier.com/locate/foodcont
Review
Carbon dioxide sensors for intelligent food packaging applications Pradeep Puligundla, Junho Jung, Sanghoon Ko* Department of Food Science and Technology, Sejong University, 98 Gunja-dong, Gwangjin-gu, Seoul 143-747, South Korea
a r t i c l e i n f o
a b s t r a c t
Article history: Received 30 June 2011 Received in revised form 12 October 2011 Accepted 18 October 2011
Recently, the demand for safe and high quality foods, as well as changes in consumer preferences have led to the development of innovative and novel approaches in food packaging technology. One such development is the smart or intelligent food packaging technology. Intelligent packaging has enabled to monitor and communicate information about food quality. This technology also helps to trace a product’s history through the critical points in the food supply chain. In general, occurrence of elevated CO2 gas level is the prime indicator of food spoilage in packed foods and also its maintenance at optimal levels is essential to avoid spoilage in foods packed under modified-atmosphere packaging (MAP) conditions. Hence, a CO2 sensor incorporated into food package can efficiently monitor product quality until it reaches the consumer. Although much progress has been made so far in the development of sensors monitoring CO2, most of them are not versatile for food packaging applications and suffers from limitations such as high equipment cost, bulkiness, and energy input requirement, including safety concerns. Therefore, the development of efficient CO2 sensors that can intelligently monitors the gas concentration changes inside a food package and specific to food packaging applications is essential. In the present review, progress on the development of different types of CO2 sensors such as optical sensors, polymer opal films, polymer hydrogels, etc., which can be readily applicable to food packaging applications, is discussed. Crown Copyright Ó 2011 Published by Elsevier Ltd. All rights reserved.
Keywords: Carbon dioxide sensor Intelligent food packaging Optical sensors Polymer opal films Polymer hydrogels
Contents 1.
2.
3. 4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329 1.1. Novel food packaging techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329 1.2. Carbon dioxide (CO2) as a direct indicator of food quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329 1.3. Driving force for innovation in food quality monitoring . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329 CO2 sensors for intelligent food packaging applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330 2.1. Conventional CO2 sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330 2.2. Innovative optical CO2 sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330 2.2.1. Wet optical CO2 indicators (pH-based) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330 2.2.2. Principle in pH dye-based indicators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331 2.2.3. Fluorescent CO2 sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331 2.2.4. Dry optical CO2 sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331 2.2.5. Solegel-based optical CO2 sensor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331 2.2.6. Photonic crystal sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Polymer opal films . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Polymer hydrogel-based CO2 sensor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 2.2.7. Color changing metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Safety & regulatory aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332
* Corresponding author. Tel.: þ82 2 3408 3260; fax: þ82 2 3408 4319. E-mail address: [email protected] (S. Ko). 0956-7135/$ e see front matter Crown Copyright Ó 2011 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2011.10.043
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1. Introduction 1.1. Novel food packaging techniques Conventionally, a food package helps protect food from environmental influences, such as moisture, light, oxygen, microbes, mechanical stresses and dust. These factors lead to or enhance the deterioration of food or drink. An ideal food packaging material should be inert, not to allow the transfer, i.e. must have a perfect barrier property, and recyclable. Food package makes distribution easier. Apart from these, there are other important functions of packaging, including containment, convenience, marketing, and communication. However, in recent years, the area of active and intelligent packaging is becoming increasingly significant. According to the definitions of the European ‘Actipak’ project, the active packaging changes the condition of the packed food to extend shelf life or to improve safety or sensory properties, while maintaining the quality of the packaged food. And, the intelligent packaging systems monitor the condition of packaged foods to give information about the quality of the packaged food during transport and storage (Ahvenainen, 2003). Active food packaging plays a dynamic role in food preservation and allows packages to interact with food and the environment. Active packaging technique enables the regulation of various aspects that may play a role in determining the shelf life of packaged foods, such as physiological (e.g., respiration of fresh fruit and vegetables), chemical (e.g., lipid oxidation), and physical (e.g., dehydration) processes as well as microbiological aspects. Other developments in packaging technologies include odor absorbers, ethylene removers, and carbon dioxide emitters/absorbers. On the other hand, intelligent packaging systems attached as labels, incorporated into, or printed onto a food packaging material offer enhanced possibilities to monitor product quality, trace the critical points, and provide product information like product history (Han, Ho, & Rodrigues, 2005). The commonly used intelligent visual indicators are time/temperature indicators and leak detectors, and these are indirect indicators, based on polymerization rate, diffusion, chemical or enzymatic reaction. However, the direct indicators are preferred because of their ability to provide more precise and targeted information on quality attributes (Gontard, 2004). 1.2. Carbon dioxide (CO2) as a direct indicator of food quality To decrease microbial growth rate and subsequent spoilage, food products are often packed under modified-atmosphere packaging (MAP) conditions. The carbon dioxide (CO2) gas can be solely (100%) or in different combinations with other gases such as nitrogen (N2) and oxygen (O2) is typically used (as flush gas) for creating protective atmosphere surrounding the food inside of a pack with an aim to exclude or minimize the oxygen content, thereby the shelf life of food can be extended through inhibiting the aerobic spoilage microbes. And also, oxygen has been suggested to be a major factor for deterioration of meat quality through lipid oxidation (Andersen & Skibsted, 1991). Carbon dioxide is considered as an active packaging gas because high levels reduce the metabolic rates of microbes even if oxygen is present (Wayne, 2000). Depending on the type of food and the delivery stage of food item, the composition of protective atmosphere varies (Mills, 1998). The quality of MAP-packed food ultimately depends on the integrity of package and, therefore, leakage detection is the essential part of MAP technology (Bültzingslöwen et al., 2002). In modified-atmosphere food packages, freshness and safety of food can be assessed by determination of CO2 concentrations (Smolander, Hurme, & Ahvenainen, 1997). A decrease in its original
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concentration could be a sign of leakage in a package (Neethirajan, Jayas, & Sadistap, 2009). Conventionally, package headspace gas analysis is generally carried out at various points of the food supply chain by using electrochemical fuel cell for oxygen analysis, and by infrared absorption spectrometry for carbon dioxide content measurement, to ensure package integrity. However, in this method, the food packs are sampled destructively by inserting needle probe for gas collection (Smolander et al., 1997). A major disadvantage with this method is, if a package fails the leak test, a large number of packages before and after the tested one will have to be considered failed and need to be destroyed or repacked (Mills, 1998); sometimes may include food products of an entire batch also. Moreover, apart from destructive and time consuming nature of conventional method, trained technician and expensive analytical equipment is required to monitor the equality. Under normal atmosphere packing conditions, when the food within a sealed container starts to spoil, several by-products are formed and they accumulate inside. Therefore, theoretically it is possible to detect spoilage by detecting one or more of these byproducts. Production of heat, acidity, pressure, and carbon dioxide is commonly observed as by-products in food spoilage. Ideally, a spoilage detector should be useable with as many different food products as possible, without requiring different detectors for each different type of food material. As the small amounts of heat evolve during deterioration process, heat detection is not likely to be practical. And also, pH of the various foods varies widely and, therefore impractical. Pressure detection is also impractical. Limited amount of published work is available regarding food spoilage indicators. Based on volatile compounds produced in microbial spoilage, indicators have been fabricated on a trial basis. A myoglobin-based indicator for modified-atmosphere-packed poultry meat has been developed, which can indicate spoilage by detecting presence of hydrogen sulfide (H2S) formed upon spoilage (Smolander et al., 2002). For monitoring fish spoilage, Pacquit et al. (2006, 2007) developed a colorimetric dye-based sensor that detects the presence of total volatile basic nitrogen (TVB-N), a product of spoilage. Knowledge about the quality-indicating metabolites is an essential prerequisite for the development of food spoilage indicators. Under non-MAP or nitrogen-flushing conditions, aerobic and facultative anaerobic microbes thrive during storage of the food products and often resulted in the formation of lactic and acetic acids by lactic acid bacteria (LAB). However, carbon dioxide is generally known to be produced during any kind of bacterial, mold growth on foods. Therefore, to indicate deterioration of foods, simply detection of CO2 levels is the ideal way, and such detectors would have to operate without interference of the other properties of food, such as pH, salt content (corrosiveness), pressure or vacuum etc (Eaton, Kilgore, & Livingston, 1977). A correlation between CO2 concentration and the growth of microorganisms was made in pea or tomato soup that is packaged aseptically either in air or in a mixture of 5% oxygen and nitrogen (Mattila & Ahvenainen, 1989; Mattila, Tawast, & Ahvenainen, 1990); bromothymol blue, the pH-sensitive dye was used as indicator for detecting the formation of CO2. 1.3. Driving force for innovation in food quality monitoring The prime driving force is the growing consumer demand for mildly preserved, minimally processed, easily prepared and readyto-eat fresher foods (Nopwinyuwong, Trevanich, & Suppakul, 2010). Also, the innovations are fueled by globalization of food business and, therefore, food products are needed to be kept fresh over long distances and time. Conventional packaging techniques are inadequate to meet this requirement. In addition, consumers’ complaints
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over the reduction in shelf life of foods and an increase in the risk of food-borne illnesses from microorganisms reporting around the world in recent years are also an important issue. Food traceability throughout the food supply chain is increasingly becoming a necessary task, mandatory in European Union (EU) since 2005 (Giraud & Halawany, 2006). In the light of the above, to maintain safety and freshness and to evaluate real-time freshness of food products, there is a constant need to develop a cost-effective, accurate, rapid, reliable, non-invasive and non-destructive methods or devices. Therefore, in order to achieve these goals, a measurable technology, visually or instrumentally, should be developed which provide in-situ information about the gas composition and, therefore, information on food quality of packaged foods through any point of food supply chain until reaching the consumer. Indicator should be very inexpensive, and not add significantly to the overall cost of the package. It should be non-toxic, and have non-water soluble nature. The sensor components should have approval for use in food-contact materials. Also, it should not require an expensive instrumentation for analysis and should be able to check it even by an untrained person. It also should exhibit an irreversible response toward analytes. 2. CO2 sensors for intelligent food packaging applications 2.1. Conventional CO2 sensors Broadly, the CO2 sensors can be divided into two types, optical and electrochemical, based on the type of transducer. The electrochemical CO2 sensors are further sub-categorized into potentiometric, amperometric, and conductometric types. Non Distributive Infra Red (NDIR) and Severinghaus-type sensors are used conventionally, commercially for gaseous and dissolved CO2 detection, respectively. However, the NDIR instrument is expensive, large in volume, vulnerable to contamination, and water vapor interference despite its high precision. Furthermore, the process requires the destruction of a sealed package for gas analysis, and not suitable for routine sample analysis. Therefore, compact and cheap sensors are in high demand. Severinghaus CO2 sensor consists of a bicarbonate solution filled glass electrode covered by a thin CO2 permeable membrane. The membrane is impermeable to water and electrolytes. The sensor functions on principle that in an aqueous solution, CO2 forms carbonic acid, which is then dissociates into a bicarbonate anion and a proton (Dieckmann & Buchholz, 1999). The proton-induced pH change in electrolyte solution can be measured by a pH probe. A CO2 sensor principle that slightly differs from Severinghaus concept was presented by Varlan and Sansen (1997). The concept is based on conductivity change as a result of the reaction of carbon dioxide and bicarbonate solution inside a cavity covered with a gas permeable membrane. This kind of sensors can measure CO2 concentrations between 0 and 11 kPa with a very fast response time. The advantage with this kind of sensors is that the use of a separate reference electrode is not required. Unfortunately, however, keeping the cavities clean is a major concern. Electrochemical potentiometric CO2 sensors using solid electrolytes are one among promising methods because of their compact structure, ability of continuous monitoring, high selectivity, and low cost (Hong, Kim, Jung, & Park, 2005). However, they require power for signal generation, and often require above 400 C operating temperature and, therefore, are not suited for food packaging applications. The environmental factors such as temperature and humidity can affect the sensors performance, especially in the case of metal oxide sensors, by cross-sensitivity reactions.
2.2. Innovative optical CO2 sensors The concept of on-pack, continuous gas composition indicating optical sensors are attractive and have been developed, tested by many researchers for monitoring MAP package integrity. Optical CO2 sensors can be classified into two types, namely, the sensors which function based on the color (colorimetric) change of a pH indicator dye, such as thymol blue, phenol red, cresol red, etc. (Kawabata, Kamichika, Imasaka, & Ishibashi, 1989; Mills, Chang, & McMurray, 1992, Mills, Lepre, & Wild, 1997); and those based on the CO2induced fluorescence change of a luminescent dye (Marazuela, Moleno-Bondi, & Orellana, 1995; Mills & Chang, 1993) such as ruthenium (II) complexes and 1-hydroxypyrene trisulfonate. 2.2.1. Wet optical CO2 indicators (pH-based) All wet optical sensors function on the principle of Severinghaus carbon dioxide electrode, and therefore diffusion of CO2 from the test medium (gaseous or aqueous) through a thin (ca. 10 mm) gas permeable membrane, and a quick establishment of equilibrium with the entrapped aqueous layer, which contains pH-sensitive dye, usually occurs in a typical wet optical sensor for CO2 (Mills, 2009). The detection process involves mixing of gas to be tested with a chemical reagent/dye which results in a color change/shift of the chemicals. This change of color can be measured and compared to a standard. The usefulness of colorimetric analysis for CO2 measurement has been shown (Hauser & Liang, 1997; Mills & Monaf, 1996; Uttamial & Walt, 1995). Tufflex GS pouches that contain a visible CO2 indicator were developed by Sealed Air Limited. The pouches can be used to identify machine faults and gas supply problems, to indicate non-integrity of the package, and to check the presence of desired gas mixture in modified-atmosphere packaging. A reversible CO2 indicator comprising five indicator strips for use in modified-atmosphere packages was fabricated and patented by Balderson and Whitwood (1995); the strips are coated with CO2-sensitive indicator material, for instance, anion of an indicator and a lipophilic organic quaternary cation (Mills & McMurray, 1991), and each strip is designed in such a way that changes their color when the CO2 level is below a certain limit (e.g., 25%, 20% or 15%). A mixed pH dye-based, on-package colorimetric indicator was developed for real-time monitoring of intermediatemoisture dessert spoilage (Nopwinyuwong et al., 2010). This indicator responds through visible color change to carbon dioxide (CO2) as a spoilage metabolite; and the change correlates well with microbial growth patterns in dessert samples. To sense ripeness of fermented vegetable foods such as kimchi several physical properties such as color, volume, turbidity; chemical properties such as pH, acidity, CO2, sugars, salts, etc., and microbiological properties have been tested (Mheen & Kwon, 1984). However, commercial packed kimchi products generally undergo a continuous natural fermentation process even during storage and distribution. So, the ripeness/over-ripeness cannot be detected by general testing methods without destroying the packaging materials (Hong & Park, 1999). Therefore, a sensor which can monitor the CO2 gas continuously, and indicate levels through exhibiting different colors accordingly, non-destructively, has been under development. Changes in CO2 concentration within the kimchi package showed a sigmoid increase during fermentation. A color indicating sachet responding to CO2 levels has been developed for application to kimchi packaging (Hong & Park, 1997). However, the technique suffered from disadvantages of inconvenience, handling difficulty and safety concerns for commercial products. The same research group had developed a color indicator film consisting of polypropylene (PP) resin, Ca(OH)2 as a CO2 absorbent and bromocresol purple or methyl red indicators, and the film was attached to the lid.
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Majority of colorimetric CO2 optical indicators are solventbased (i.e. non-aqueous) systems, incorporating a phase transfer agent (PTA) to solubilize the usually lipophilic dye and base (Mills et al., 1992). However, poor shelf life stability of such systems is a major drawback when stored under dark and/or ambient conditions (Mills & Monaf, 1996; Weigl & Wolfbeis, 1995). Thus, the dye in such indicators changes irreversibly to its acidified form, rendering the indicator ineffective in short time. Therefore, usually an inert atmosphere is used in packaging, but with additional cost to production. Interestingly, water-based CO2 indicators have shown markedly greater lifetimes, than their solvent-based counterparts. A water-based ink containing base-sodium hydrogen carbonate and plasticizerglycerol, having improved operational lifetimes, quick response and recovery times (2 min), reversible color change on all tested surfaces, and works under ambient condition has been reported (Mills & Skinner, 2010). However, sensitivity to humidity and temperature is needed to be addressed before realizing potential usage for intelligent food packaging applications. But, luckily, a fixed temperature (chilled, 4 C) and unchanged % RH is usually maintained for MAP food packages and, therefore, water-based CO2 sensors could be used. The sensitivity of CO2 sensor is linked to the equilibrium constant (pKA) of the pH indicator used and to the nature of surrounding buffer (Mills & Chang, 1994). An aqueous bicarbonate buffer usually contained in first generation optical carbon dioxide sensors. The aqueous buffer containing sensors have been replaced by quaternary ammonium hydroxide containing solid sensor membranes (Mills et al., 1992). Earlier, colorimetric leak indicators in the form of sachets and tablets have been used for sensors development in food packaging technology. Latest approaches, for more compatible with industrial demand, would consist of printable sensor membranes on the packaging material and should provide information about analytes at any given stage in the packaging and delivery process. 2.2.2. Principle in pH dye-based indicators The carbon dioxide gas dissolves in the aqueous buffer or hydrophilic filter layer in strip or membrane type sensor and forms carbonic acid.
CO2 ðgÞ4CO2 ðaqÞ CO2 ðaqÞ þ H2 O4H2 CO3 The two hydrogen atoms from the formed carbonic acid (diprotic) may dissociate to form hydrogen ions (Hþ) and bicarbonate ions (HCO3) with pKa of 6.36 at 25 C (Mook & de Vries, 2000). þ H2 CO3 4HCO 3 þH
Then, a hydrogen ion, as a proton, combines with a water molecule to form a hydronium ion, H3Oþ
Hþ þ H2 O/H3 Oþ Hydronium ions react with the basic (dissociated) form (In) of the indicator dye, resulting in an acid (protonated) form (HIn) which in turn produces a color change of the indicator containing solution or label.
Hþ þ In /HIn There are certain drawbacks are associated with use of pH-based sensors that CO2 levels cannot be measured directly, but in its ionic form and, therefore, the pH-value measurement could
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be impaired by other volatile acid or basic gases produced during spoilage. And also, maintenance costs are very high. 2.2.3. Fluorescent CO2 sensors Similar to the colorimetric method except that a fluorescent dye is used to generate its own radiative energy at a different wavelength to that of the excitation wavelength. The generated excitation spectra will depend on the sample gas concentration. CO2 measuring instrumentation also fabricated using this principle (Choi & Hawkings, 1995a,b; Wolfbeis & Weis, 1998). A printable oxygen and carbon dioxide sensors formulations have been developed for application in food packaging (McEvoy et al., 2003); the oxygen was measured by detecting the degree of quenching of a fluorescent ruthenium complex entrapped in a solegel matrix. For monitoring CO2 gas, a fluorescence-based and pH-sensitive 8-hydroxypyrene-1, 3, 6-trisulfonic acid (HPTS) indicator dye encapsulated in organically modified silica (ORMOSIL) glass matrix was used. In the context of in-situ monitoring of analytes, issues such as cross-reactivity, robustness, and humidity interference need to be addressed before realizing the full potential. 2.2.4. Dry optical CO2 sensors A novel plastic film incorporated with fluorescent dye HPTS was used to sense CO2 gas with a 0e90% response and recovery times of the film when exposed to an alternating atmosphere of air and 5% CO2 are typically 4.3 and 7.1 s, respectively (Mills & Chang, 1993). Phase transfer agent (PTA) such as tetraoctyl ammonium hydroxide (TOAH) plays vital role in the fabrication of solid, dry CO2 sensors. PTA agent in its general form, QþOH, can be used to dissolve the anionic form (D) of a colorimetric pH indicator dye, such as m-cresol purple (MCP), in a hydrophobic solvent, such as toluene, that is mutually compatible with that of a water-insoluble polymer, such as ethyl cellulose (EC) or poly vinyl butyral (PVB) (Mills, 2009). Thus, it was found that mixing of pH-sensitive, hydrophilic indicator dye anion with phase transfer agent result in formation of ion pairs, QþD, which can be dissolved in hydrophobic solvents. Therefore, a color-based dry CO2 sensor comprises a pH-sensitive dye/phase transfer agent/polymer/solvent, which could be cast, by printing, spin-coating, to generate a range of thin, colored plastic films containing a pH-sensitive dye in its deprotonated anionic form, i.e. as QþD. Carbon dioxide levels in dry and humid gases can be determined by using these types of solid dry sensors. The sensor sensitivity toward CO2 decreased with increase of temperature. Also, acidic and oxidizing gases have a marked and irreversible deleterious effect on the response features. A luminescence intensity-based dry optical sensor film was designed using the luminescent dye, HPTS, the phase transfer agent, TOAH, the polymer, EC, and the plasticizer, tributyl phosphate (TBP) (Mills & Chang, 1993). 2.2.5. Solegel-based optical CO2 sensor An optical solegel-based CO2 sensor strip was fabricated using a fluorescent pH indicator, 1-hydroxypyrene-3, 6, 8-trisulfonate (HPTS) (Bültzingslöwen et al., 2002). The sensor exhibited a fast and reversible response to carbon dioxide over a wide range of concentrations (0e100% CO2) with sufficient resolution (2%). The dye was immobilized in hydrophobic organically modified silica matrix. Cetyltrimethylammonium hydroxide (CTA-OH), a quaternary ammonium base, was used as an ion-pairing agent for a polar pH indicator in a non-polar gas permeable membrane, and also it functions as internal buffer. The Dual Luminophore Referencing (DLR) sensing method, an internal ratiometric method, is used for measuring the fluorescence. In which, the analyte-sensitive fluorescence intensity signal is converted into the phase domain by co-immobilizing an inert long-lifetime reference luminophore
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having similar spectral characteristics. Ruthenium complex and HPTS dye are the excellent candidates for a DLR-type CO2 sensor because their excitation and emission wavelengths are well matched. Oxygen cross-sensitivity is minimal and compatible with established optical oxygen sensor technology. 2.2.6. Photonic crystal sensors 2.2.6.1. Polymer opal films. Color changing polymer opal films have been developed by various research groups and were initially developed at the University of Southampton in the United Kingdom and the Deutsches Kunststoff-Institut (DKI) in Darmstadt, Germany. The polymer opals are a type of photonic crystal consisting of a 3D lattice of plastic spheres but have a large contrast in their components’ optical properties. This causes a range of frequencies to occur and, therefore, causes variations in the light that is reflected from these regions, also called photonic band gaps. Tiny carbon nanoparticles can be wedged between the crystalline spheres. Thus, incident light cannot reflect at the interfaces between the crystalline spheres and the surrounding materials, but scattering of light can occur. Due to a high surface to volume ratio of nanoparticles, an intense color is generally observed in produced opal films. The color depends on manner of arrangement of the spheres and the placement of the nanoparticles. Stretching of flexible films will cause orientation of the lattice structure and changes to the distance between the spheres. This will cause a change in color to appear. 2.2.6.2. Polymer hydrogel-based CO2 sensor. In response to external stimuli, polymer hydrogels can exhibit large reversible change in their volume, and thus regarded as suitable materials for chemical sensors. These kinds of sensors are best suited for food packaging applications due to the fact that they don’t require sophisticated and expensive detection systems. They offer fast response times, and are robust. Also, sensors have a long lifetime (>6 months) without degradation of response time or reproducibility. Volume change in hydrogel is exerted by Donnan potential between the analyte ions and their receptor which is covalently bound to the hydrogel building block (Shin, Braun, & Lee, 2010). In order to compensate the local ion inhomogeneity, there is influx of water molecules to the hydrogel. Color change of sensor is observed due to volume change in periodic structure, known as photonic crystal. These hydrogels are imprinted with photonic crystal; such color is often called ‘structural color’. Relatively simple optical detection techniques are possible using hydrogel photonic crystal sensor, for a wide variety of analytes such as protons (Debord & Lyon, 2000; Xu, Goponenko, & Asher, 2008), metal ions, glucose, and volatile organic compounds (VOC). Therefore, a proton-based photonic crystal CO2 gas sensor could be fabricated for use in food packaging. 2.2.7. Color changing metals Recently, a research group identified the color changing nature of modified rhodium metal to different gases. The modified rhodium changes to yellow in the presence of nitrogen, deep blue in the presence of oxygen, and brown in the presence of carbon monoxide. According to head of the team, the gases bind to the compound’s central metal without disrupting the exact placement of each individual atom in the compound’s crystalline lattice in an unprecedented way (Queen’s University, 2011, July 21). This discovery could form the basis for development of early warning system if failure of MAP system occurs. However, this metal usage in food systems could be subject to food safety clearance. 3. Safety & regulatory aspects Indicators or sensors are intended to be placed inside the package exposing to headspace atmosphere and, therefore, safety
criteria have to be fulfilled. Often, packaging materials are in direct contact with food inside the pack, so the embedded or attached indicators to these packing materials must be suitable for direct food contact applications. A major role by nanotechnologies is expected in fulfilling the additional safety considerations and existing gap in knowledge (Danielli, Gontard, Syropoulos, Zonderwan Van Den Beuken, & Toback, 2008). For innovative food packaging technologies to be successful, they must comply with strict regulations. Most of the active and intelligent agents are considered as food-contact material constituents, not as additives, and, therefore, food packaging systems must comply with the existing food-contact materials regulations. According to the EU framework directive, all the food-contact materials shall not be hazardous to human health and shall not affect the composition or sensory character of the packed foodstuff in an unacceptable way (De Kruijf et al., 2002). 4. Conclusions It can be concluded that the optical carbon dioxide gas sensors are suitable for food package indicator applications. Especially, dry optical sensors containing pH-sensitive dye indicators are better suited for CO2 monitoring and/or as spoilage indicators in food packaging application. However, issues such as humidity interference, lifetime, cost, safety, and proton generation during other oxidative reactions have to take into consideration before realizing the complete potential of pH-based sensors. Water-based, CO2 indicator inks can be used potentially in food package applications. Although they are relatively less sensitive toward CO2 than their solvent-based counterparts, posses more stable shelf life and quick response/recovery time. On the other hand, photonic crystal sensors are promising due to low cost, long lifetime, suitability to wide variety of analytes, and effective indication with quick response time. However, there is still more research efforts are necessary for the development of food application-specific sensors. Acknowledgments This research was supported by the Agriculture Research Center program of the Ministry for Food, Agriculture, Forestry and Fisheries, Korea. References Ahvenainen, R. (2003). In R. Ahvenainen (Ed.), Novel food packaging techniques. Finland: CRC Press. Andersen, J. J., & Skibsted, L. H. (1991). Oxidative stability of frozen pork patties: effect of light and added salt. Journal of Food Science, 56, 1182e1184. Balderson, S. N., & Whitwood, R. J. (1995). Gas indicator for a package (Trigon Industries Limited, Auckland, New Zealand). US Patent 5439648. Bültzingslöwen, C. V., McEvoy, A. K., McDonagh, C., MacCraith, B. D., Klimant, I., Krause, C., et al. (2002). Solegel based optical carbon dioxide sensor employing dual luminophore referencing for application in food packaging technology. Analyst, 127, 1478e1483. Choi, M. F., & Hawkings, P. (1995a). Novel dye-solvent solutions for the simultaneous detection of oxygen and carbon dioxide. Analytical Chemistry, 67, 3897e3902. Choi, M. F., & Hawkings, P. (1995b). A novel oxygen and/or carbon dioxide-sensitive optical transducer. Talanta, 42(3), 483e492. Danielli, D., Gontard, N., Syropoulos, D., Zonderwan Van Den Beuken, E., & Toback, P. (2008). Active and intelligent food packaging: legal aspects and safety concerns. Trends in Food Science & Technology, 19, 99e108. Debord, J. D., & Lyon, L. A. (2000). Thermoresponsive photonic crystals. The Journal of Physical Chemistry B, 104, 6327e6331. De Kruijf, N., Van Beest, M., Rijk, R., Sipiläinen-Malm, T., Paseiro Losada, P., & De Meulenaer, B. (2002). Active and intelligent packaging: applications and regulatory aspects. Food Additives and Contaminants, 19(Suppl.), 144e162. Dieckmann, M., & Buchholz, R. (1999). Apparatus for measuring the partial pressure of gases dissolved in liquids. US Patent 6003362. Eaton, J. C., Kilgore, M. B., & Livingston, R. B. (1977). Visual spoilage indicator for food containers. US Patent 4003709.
P. Puligundla et al. / Food Control 25 (2012) 328e333 Giraud, G., & Halawany, R. (2006). Consumers’ perception of food traceability in Europe. Paper presented at the 98th EAAE Seminar, Chania, 29 Junee2 July. Gontard, N. (2004). Active packaging for food processing and preservation. In International congress on engineering and food: ICEF 9, 7e11 March, Montpellier, France. Han, J. H., Ho, C. H. L., & Rodrigues, E. T. (2005). Intelligent packaging. In J. H. Han (Ed.), Innovations in food packaging. Elsevier Academic Press. Hauser, P., & Liang, C. (1997). All solid-state instrument for absorbance based optical gas sensor membranes. Instrumentation Science & Technology, 25(2), 147e156. Hong, H. S., Kim, J. W., Jung, S. J., & Park, C. O. (2005). Thick film planar CO2 sensors based on Na b-alumina solid electrolyte. Journal of Electroceramics, 15(2), 151e157. Hong, S.-I., & Park, W.-S. (1997). Sensitivity of color indicators to fermentation products of kimchi at various temperatures. Korean Journal of Food Science and Technology, 29, 21e25. Hong, S.-I., & Park, W.-S. (1999). Development of color indicators for kimchi packaging. Journal of Food Science, 64, 255e257. Kawabata, Y., Kamichika, T., Imasaka, T., & Ishibashi, N. (1989). Fiber-optic sensor for carbon dioxide with a pH indicator dispersed in a poly (ethylene glycol) membrane. Analytica Chimica Acta, 219, 223e229. Marazuela, M. D., Moleno-Bondi, M. C., & Orellana, G. (1995). Enhanced performance of a fiber-optic luminescence CO2 sensor using carbonic anhydrase. Sensors and Actuators B, 29, 126e131. Mattila, T., & Ahvenainen, R. (1989). Preincubation time and the use of oxygen indicators in determining the microbiological quality of aseptically packed pea and tomato soup. International Journal of Food Microbiology, 9, 205e214. Mattila, T., Tawast, J., & Ahvenainen, R. (1990). New possibilities for quality control of aseptic packages: microbiological spoilage and seal defect detection using head-space indicators. Lebensmittel-Wissenschaft & Technologie, 23, 246e251. McEvoy, A. K., Von Bueltzingsloewen, C., McDonagh, C. M., MacCraith, B. D., Klimant, I., & Wolfbeis, O. S. (2003). Optical sensors for application in intelligent foodpackaging technology. Proceedings of SPIE, 4876, 806. doi:10.1117/12.464210. Mheen, T. I., & Kwon, T. W. (1984). Effect of temperature and salt concentration on kimchi fermentation. Korean Journal of Food Science and Technology, 16, 443e450. Mills, A. (1998). International symposium on printing and coating technology, conference proceedings, Swansea, UK, 12-1e12-11. Mills, A. (2009). Optical sensors for carbon dioxide and their applications. In M.I. Baraton (Ed.), Sensors for environment, health and security (pp. 347e370). Mills, A., & Chang, Q. (1993). Fluorescent plastic film sensors for carbon dioxide. Analyst, 118, 839e843. Mills, A., & Chang, Q. (1994). Tuning colourimetric and fluorimetric gas sensors of carbon dioxide. Analytica Chimica Acta, 285, 113e123. Mills, A., & McMurray, H. N. (1991). Carbon dioxide monitor (Abbey Biosystems Ltd, Dyfed, UK). PCT International patent application WO 91/05252. Mills, A., & Monaf, L. (1996). Thin plastic film colorimetric sensor for carbon dioxide: effect of plasticizer on response. Analyst, 121, 535e540.
333
Mills, A., & Skinner, G. A. (2010). Water-based colourimetric optical indicators for the detection of carbon dioxide. Analyst, 135, 1912e1917. Mills, A., Chang, Q., & McMurray, N. (1992). Equilibrium studies on colorimetric plastic film sensors for carbon dioxide. Analytical Chemistry, 64, 1383e1389. Mills, A., Lepre, A., & Wild, L. (1997). Breath-by-breath measurement of carbon dioxide using a plastic film optical sensor. Sensors and Actuators B, 38-39, 419e425. Mook, W. G., & de Vries, J. J. (2000). Environmental isotopes in the hydrological cycle: principles and applications. In W. G. Mook (Ed.), Introduction, theory, methods, review, Vol. I (pp. 143e166). Vienna, Austria: UNESCO/IAEA. Neethirajan, S., Jayas, D. S., & Sadistap, S. (2009). Carbon dioxide (CO2) sensors for the agri-food industry e a review. Food and Bioprocess Technology, 2, 115e121. Nopwinyuwong, A., Trevanich, S., & Suppakul, P. (2010). Development of a novel colorimetric indicator label for monitoring freshness of intermediate-moisture dessert spoilage. Talanta, 81(3), 1126e1132. Pacquit, A., Frisby, J., Diamond, D., Lau, K. T., Farrell, A., & Quilty, B. (2007). Development of a smart packaging for the monitoring of fish spoilage. Food Chemistry, 102, 466e470. Pacquit, A., Lau, K. T., McLaughlin, H., Frisby, J., Quilty, B., & Diamond, D. (2006). Development of a volatile amine sensor for the monitoring of fish spoilage. Talanta, 69(2), 515e520. Queen’s University. (2011, July 21). Modified metals change color in the presence of particular gases. ScienceDaily, Retrieved July 26, 2011, from. http://www. sciencedaily.com/releases/2011/07/110721131159.htm. Shin, J., Braun, P. V., & Lee, W. (2010). Fast response photonic crystal pH sensor based on template photo-polymerized hydrogel inverse opal. Sensors and Actuators B, 150, 183e190. Smolander, M., Hurme, E., & Ahvenainen, R. (1997). Leak indicators for modified atmosphere packages. Trends in Food Science & Technology, 8(4), 101e106. Smolander, M., Hurme, E., Latva-Kala, K., Luoma, T., Alakomi, H.-L., & Ahvenainen, R. (2002). Myoglobin-based indicators for the evaluation of freshness of unmarinated broiler cuts. Innovative Food Science and Emerging Technologies, 3(3), 279e288. Uttamial, M., & Walt, D. (1995). A fibre-optic carbon dioxide sensor for fermentation monitoring. Biotechnology, 13(6), 597e601. Varlan, A. R., & Sansen, W. (1997). Micromachined conductometric p(CO2) sensor. Sensors and Actuators B, 44, 309e315. Wayne, R. P. (2000). Chemistry of atmospheres (3rd ed.). Oxford: Oxford University Press. Weigl, B. H., & Wolfbeis, O. S. (1995). Sensitivity studies on optical carbon-dioxide sensors based on ion-pairing. Sensors and Actuators B: Chemical, 28, 151e156. Wolfbeis, O., & Weis, L. (1998). Fiber-optic fluorosensor for oxygen and carbon dioxide. Analytical Chemistry, 60, 2028e2030. Xu, X., Goponenko, A. V., & Asher, S. A. (2008). Polymerized PolyHEMA photonic crystals: pH and ethanol sensor materials. Journal of the American Chemical Society, 130, 3113e3119.
Contents lists available at SciVerse ScienceDirect
Food Control journal homepage: www.elsevier.com/locate/foodcont
Review
Carbon dioxide sensors for intelligent food packaging applications Pradeep Puligundla, Junho Jung, Sanghoon Ko* Department of Food Science and Technology, Sejong University, 98 Gunja-dong, Gwangjin-gu, Seoul 143-747, South Korea
a r t i c l e i n f o
a b s t r a c t
Article history: Received 30 June 2011 Received in revised form 12 October 2011 Accepted 18 October 2011
Recently, the demand for safe and high quality foods, as well as changes in consumer preferences have led to the development of innovative and novel approaches in food packaging technology. One such development is the smart or intelligent food packaging technology. Intelligent packaging has enabled to monitor and communicate information about food quality. This technology also helps to trace a product’s history through the critical points in the food supply chain. In general, occurrence of elevated CO2 gas level is the prime indicator of food spoilage in packed foods and also its maintenance at optimal levels is essential to avoid spoilage in foods packed under modified-atmosphere packaging (MAP) conditions. Hence, a CO2 sensor incorporated into food package can efficiently monitor product quality until it reaches the consumer. Although much progress has been made so far in the development of sensors monitoring CO2, most of them are not versatile for food packaging applications and suffers from limitations such as high equipment cost, bulkiness, and energy input requirement, including safety concerns. Therefore, the development of efficient CO2 sensors that can intelligently monitors the gas concentration changes inside a food package and specific to food packaging applications is essential. In the present review, progress on the development of different types of CO2 sensors such as optical sensors, polymer opal films, polymer hydrogels, etc., which can be readily applicable to food packaging applications, is discussed. Crown Copyright Ó 2011 Published by Elsevier Ltd. All rights reserved.
Keywords: Carbon dioxide sensor Intelligent food packaging Optical sensors Polymer opal films Polymer hydrogels
Contents 1.
2.
3. 4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329 1.1. Novel food packaging techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329 1.2. Carbon dioxide (CO2) as a direct indicator of food quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329 1.3. Driving force for innovation in food quality monitoring . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329 CO2 sensors for intelligent food packaging applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330 2.1. Conventional CO2 sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330 2.2. Innovative optical CO2 sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330 2.2.1. Wet optical CO2 indicators (pH-based) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330 2.2.2. Principle in pH dye-based indicators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331 2.2.3. Fluorescent CO2 sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331 2.2.4. Dry optical CO2 sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331 2.2.5. Solegel-based optical CO2 sensor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331 2.2.6. Photonic crystal sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Polymer opal films . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Polymer hydrogel-based CO2 sensor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 2.2.7. Color changing metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Safety & regulatory aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332
* Corresponding author. Tel.: þ82 2 3408 3260; fax: þ82 2 3408 4319. E-mail address: [email protected] (S. Ko). 0956-7135/$ e see front matter Crown Copyright Ó 2011 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2011.10.043
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1. Introduction 1.1. Novel food packaging techniques Conventionally, a food package helps protect food from environmental influences, such as moisture, light, oxygen, microbes, mechanical stresses and dust. These factors lead to or enhance the deterioration of food or drink. An ideal food packaging material should be inert, not to allow the transfer, i.e. must have a perfect barrier property, and recyclable. Food package makes distribution easier. Apart from these, there are other important functions of packaging, including containment, convenience, marketing, and communication. However, in recent years, the area of active and intelligent packaging is becoming increasingly significant. According to the definitions of the European ‘Actipak’ project, the active packaging changes the condition of the packed food to extend shelf life or to improve safety or sensory properties, while maintaining the quality of the packaged food. And, the intelligent packaging systems monitor the condition of packaged foods to give information about the quality of the packaged food during transport and storage (Ahvenainen, 2003). Active food packaging plays a dynamic role in food preservation and allows packages to interact with food and the environment. Active packaging technique enables the regulation of various aspects that may play a role in determining the shelf life of packaged foods, such as physiological (e.g., respiration of fresh fruit and vegetables), chemical (e.g., lipid oxidation), and physical (e.g., dehydration) processes as well as microbiological aspects. Other developments in packaging technologies include odor absorbers, ethylene removers, and carbon dioxide emitters/absorbers. On the other hand, intelligent packaging systems attached as labels, incorporated into, or printed onto a food packaging material offer enhanced possibilities to monitor product quality, trace the critical points, and provide product information like product history (Han, Ho, & Rodrigues, 2005). The commonly used intelligent visual indicators are time/temperature indicators and leak detectors, and these are indirect indicators, based on polymerization rate, diffusion, chemical or enzymatic reaction. However, the direct indicators are preferred because of their ability to provide more precise and targeted information on quality attributes (Gontard, 2004). 1.2. Carbon dioxide (CO2) as a direct indicator of food quality To decrease microbial growth rate and subsequent spoilage, food products are often packed under modified-atmosphere packaging (MAP) conditions. The carbon dioxide (CO2) gas can be solely (100%) or in different combinations with other gases such as nitrogen (N2) and oxygen (O2) is typically used (as flush gas) for creating protective atmosphere surrounding the food inside of a pack with an aim to exclude or minimize the oxygen content, thereby the shelf life of food can be extended through inhibiting the aerobic spoilage microbes. And also, oxygen has been suggested to be a major factor for deterioration of meat quality through lipid oxidation (Andersen & Skibsted, 1991). Carbon dioxide is considered as an active packaging gas because high levels reduce the metabolic rates of microbes even if oxygen is present (Wayne, 2000). Depending on the type of food and the delivery stage of food item, the composition of protective atmosphere varies (Mills, 1998). The quality of MAP-packed food ultimately depends on the integrity of package and, therefore, leakage detection is the essential part of MAP technology (Bültzingslöwen et al., 2002). In modified-atmosphere food packages, freshness and safety of food can be assessed by determination of CO2 concentrations (Smolander, Hurme, & Ahvenainen, 1997). A decrease in its original
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concentration could be a sign of leakage in a package (Neethirajan, Jayas, & Sadistap, 2009). Conventionally, package headspace gas analysis is generally carried out at various points of the food supply chain by using electrochemical fuel cell for oxygen analysis, and by infrared absorption spectrometry for carbon dioxide content measurement, to ensure package integrity. However, in this method, the food packs are sampled destructively by inserting needle probe for gas collection (Smolander et al., 1997). A major disadvantage with this method is, if a package fails the leak test, a large number of packages before and after the tested one will have to be considered failed and need to be destroyed or repacked (Mills, 1998); sometimes may include food products of an entire batch also. Moreover, apart from destructive and time consuming nature of conventional method, trained technician and expensive analytical equipment is required to monitor the equality. Under normal atmosphere packing conditions, when the food within a sealed container starts to spoil, several by-products are formed and they accumulate inside. Therefore, theoretically it is possible to detect spoilage by detecting one or more of these byproducts. Production of heat, acidity, pressure, and carbon dioxide is commonly observed as by-products in food spoilage. Ideally, a spoilage detector should be useable with as many different food products as possible, without requiring different detectors for each different type of food material. As the small amounts of heat evolve during deterioration process, heat detection is not likely to be practical. And also, pH of the various foods varies widely and, therefore impractical. Pressure detection is also impractical. Limited amount of published work is available regarding food spoilage indicators. Based on volatile compounds produced in microbial spoilage, indicators have been fabricated on a trial basis. A myoglobin-based indicator for modified-atmosphere-packed poultry meat has been developed, which can indicate spoilage by detecting presence of hydrogen sulfide (H2S) formed upon spoilage (Smolander et al., 2002). For monitoring fish spoilage, Pacquit et al. (2006, 2007) developed a colorimetric dye-based sensor that detects the presence of total volatile basic nitrogen (TVB-N), a product of spoilage. Knowledge about the quality-indicating metabolites is an essential prerequisite for the development of food spoilage indicators. Under non-MAP or nitrogen-flushing conditions, aerobic and facultative anaerobic microbes thrive during storage of the food products and often resulted in the formation of lactic and acetic acids by lactic acid bacteria (LAB). However, carbon dioxide is generally known to be produced during any kind of bacterial, mold growth on foods. Therefore, to indicate deterioration of foods, simply detection of CO2 levels is the ideal way, and such detectors would have to operate without interference of the other properties of food, such as pH, salt content (corrosiveness), pressure or vacuum etc (Eaton, Kilgore, & Livingston, 1977). A correlation between CO2 concentration and the growth of microorganisms was made in pea or tomato soup that is packaged aseptically either in air or in a mixture of 5% oxygen and nitrogen (Mattila & Ahvenainen, 1989; Mattila, Tawast, & Ahvenainen, 1990); bromothymol blue, the pH-sensitive dye was used as indicator for detecting the formation of CO2. 1.3. Driving force for innovation in food quality monitoring The prime driving force is the growing consumer demand for mildly preserved, minimally processed, easily prepared and readyto-eat fresher foods (Nopwinyuwong, Trevanich, & Suppakul, 2010). Also, the innovations are fueled by globalization of food business and, therefore, food products are needed to be kept fresh over long distances and time. Conventional packaging techniques are inadequate to meet this requirement. In addition, consumers’ complaints
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over the reduction in shelf life of foods and an increase in the risk of food-borne illnesses from microorganisms reporting around the world in recent years are also an important issue. Food traceability throughout the food supply chain is increasingly becoming a necessary task, mandatory in European Union (EU) since 2005 (Giraud & Halawany, 2006). In the light of the above, to maintain safety and freshness and to evaluate real-time freshness of food products, there is a constant need to develop a cost-effective, accurate, rapid, reliable, non-invasive and non-destructive methods or devices. Therefore, in order to achieve these goals, a measurable technology, visually or instrumentally, should be developed which provide in-situ information about the gas composition and, therefore, information on food quality of packaged foods through any point of food supply chain until reaching the consumer. Indicator should be very inexpensive, and not add significantly to the overall cost of the package. It should be non-toxic, and have non-water soluble nature. The sensor components should have approval for use in food-contact materials. Also, it should not require an expensive instrumentation for analysis and should be able to check it even by an untrained person. It also should exhibit an irreversible response toward analytes. 2. CO2 sensors for intelligent food packaging applications 2.1. Conventional CO2 sensors Broadly, the CO2 sensors can be divided into two types, optical and electrochemical, based on the type of transducer. The electrochemical CO2 sensors are further sub-categorized into potentiometric, amperometric, and conductometric types. Non Distributive Infra Red (NDIR) and Severinghaus-type sensors are used conventionally, commercially for gaseous and dissolved CO2 detection, respectively. However, the NDIR instrument is expensive, large in volume, vulnerable to contamination, and water vapor interference despite its high precision. Furthermore, the process requires the destruction of a sealed package for gas analysis, and not suitable for routine sample analysis. Therefore, compact and cheap sensors are in high demand. Severinghaus CO2 sensor consists of a bicarbonate solution filled glass electrode covered by a thin CO2 permeable membrane. The membrane is impermeable to water and electrolytes. The sensor functions on principle that in an aqueous solution, CO2 forms carbonic acid, which is then dissociates into a bicarbonate anion and a proton (Dieckmann & Buchholz, 1999). The proton-induced pH change in electrolyte solution can be measured by a pH probe. A CO2 sensor principle that slightly differs from Severinghaus concept was presented by Varlan and Sansen (1997). The concept is based on conductivity change as a result of the reaction of carbon dioxide and bicarbonate solution inside a cavity covered with a gas permeable membrane. This kind of sensors can measure CO2 concentrations between 0 and 11 kPa with a very fast response time. The advantage with this kind of sensors is that the use of a separate reference electrode is not required. Unfortunately, however, keeping the cavities clean is a major concern. Electrochemical potentiometric CO2 sensors using solid electrolytes are one among promising methods because of their compact structure, ability of continuous monitoring, high selectivity, and low cost (Hong, Kim, Jung, & Park, 2005). However, they require power for signal generation, and often require above 400 C operating temperature and, therefore, are not suited for food packaging applications. The environmental factors such as temperature and humidity can affect the sensors performance, especially in the case of metal oxide sensors, by cross-sensitivity reactions.
2.2. Innovative optical CO2 sensors The concept of on-pack, continuous gas composition indicating optical sensors are attractive and have been developed, tested by many researchers for monitoring MAP package integrity. Optical CO2 sensors can be classified into two types, namely, the sensors which function based on the color (colorimetric) change of a pH indicator dye, such as thymol blue, phenol red, cresol red, etc. (Kawabata, Kamichika, Imasaka, & Ishibashi, 1989; Mills, Chang, & McMurray, 1992, Mills, Lepre, & Wild, 1997); and those based on the CO2induced fluorescence change of a luminescent dye (Marazuela, Moleno-Bondi, & Orellana, 1995; Mills & Chang, 1993) such as ruthenium (II) complexes and 1-hydroxypyrene trisulfonate. 2.2.1. Wet optical CO2 indicators (pH-based) All wet optical sensors function on the principle of Severinghaus carbon dioxide electrode, and therefore diffusion of CO2 from the test medium (gaseous or aqueous) through a thin (ca. 10 mm) gas permeable membrane, and a quick establishment of equilibrium with the entrapped aqueous layer, which contains pH-sensitive dye, usually occurs in a typical wet optical sensor for CO2 (Mills, 2009). The detection process involves mixing of gas to be tested with a chemical reagent/dye which results in a color change/shift of the chemicals. This change of color can be measured and compared to a standard. The usefulness of colorimetric analysis for CO2 measurement has been shown (Hauser & Liang, 1997; Mills & Monaf, 1996; Uttamial & Walt, 1995). Tufflex GS pouches that contain a visible CO2 indicator were developed by Sealed Air Limited. The pouches can be used to identify machine faults and gas supply problems, to indicate non-integrity of the package, and to check the presence of desired gas mixture in modified-atmosphere packaging. A reversible CO2 indicator comprising five indicator strips for use in modified-atmosphere packages was fabricated and patented by Balderson and Whitwood (1995); the strips are coated with CO2-sensitive indicator material, for instance, anion of an indicator and a lipophilic organic quaternary cation (Mills & McMurray, 1991), and each strip is designed in such a way that changes their color when the CO2 level is below a certain limit (e.g., 25%, 20% or 15%). A mixed pH dye-based, on-package colorimetric indicator was developed for real-time monitoring of intermediatemoisture dessert spoilage (Nopwinyuwong et al., 2010). This indicator responds through visible color change to carbon dioxide (CO2) as a spoilage metabolite; and the change correlates well with microbial growth patterns in dessert samples. To sense ripeness of fermented vegetable foods such as kimchi several physical properties such as color, volume, turbidity; chemical properties such as pH, acidity, CO2, sugars, salts, etc., and microbiological properties have been tested (Mheen & Kwon, 1984). However, commercial packed kimchi products generally undergo a continuous natural fermentation process even during storage and distribution. So, the ripeness/over-ripeness cannot be detected by general testing methods without destroying the packaging materials (Hong & Park, 1999). Therefore, a sensor which can monitor the CO2 gas continuously, and indicate levels through exhibiting different colors accordingly, non-destructively, has been under development. Changes in CO2 concentration within the kimchi package showed a sigmoid increase during fermentation. A color indicating sachet responding to CO2 levels has been developed for application to kimchi packaging (Hong & Park, 1997). However, the technique suffered from disadvantages of inconvenience, handling difficulty and safety concerns for commercial products. The same research group had developed a color indicator film consisting of polypropylene (PP) resin, Ca(OH)2 as a CO2 absorbent and bromocresol purple or methyl red indicators, and the film was attached to the lid.
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Majority of colorimetric CO2 optical indicators are solventbased (i.e. non-aqueous) systems, incorporating a phase transfer agent (PTA) to solubilize the usually lipophilic dye and base (Mills et al., 1992). However, poor shelf life stability of such systems is a major drawback when stored under dark and/or ambient conditions (Mills & Monaf, 1996; Weigl & Wolfbeis, 1995). Thus, the dye in such indicators changes irreversibly to its acidified form, rendering the indicator ineffective in short time. Therefore, usually an inert atmosphere is used in packaging, but with additional cost to production. Interestingly, water-based CO2 indicators have shown markedly greater lifetimes, than their solvent-based counterparts. A water-based ink containing base-sodium hydrogen carbonate and plasticizerglycerol, having improved operational lifetimes, quick response and recovery times (2 min), reversible color change on all tested surfaces, and works under ambient condition has been reported (Mills & Skinner, 2010). However, sensitivity to humidity and temperature is needed to be addressed before realizing potential usage for intelligent food packaging applications. But, luckily, a fixed temperature (chilled, 4 C) and unchanged % RH is usually maintained for MAP food packages and, therefore, water-based CO2 sensors could be used. The sensitivity of CO2 sensor is linked to the equilibrium constant (pKA) of the pH indicator used and to the nature of surrounding buffer (Mills & Chang, 1994). An aqueous bicarbonate buffer usually contained in first generation optical carbon dioxide sensors. The aqueous buffer containing sensors have been replaced by quaternary ammonium hydroxide containing solid sensor membranes (Mills et al., 1992). Earlier, colorimetric leak indicators in the form of sachets and tablets have been used for sensors development in food packaging technology. Latest approaches, for more compatible with industrial demand, would consist of printable sensor membranes on the packaging material and should provide information about analytes at any given stage in the packaging and delivery process. 2.2.2. Principle in pH dye-based indicators The carbon dioxide gas dissolves in the aqueous buffer or hydrophilic filter layer in strip or membrane type sensor and forms carbonic acid.
CO2 ðgÞ4CO2 ðaqÞ CO2 ðaqÞ þ H2 O4H2 CO3 The two hydrogen atoms from the formed carbonic acid (diprotic) may dissociate to form hydrogen ions (Hþ) and bicarbonate ions (HCO3) with pKa of 6.36 at 25 C (Mook & de Vries, 2000). þ H2 CO3 4HCO 3 þH
Then, a hydrogen ion, as a proton, combines with a water molecule to form a hydronium ion, H3Oþ
Hþ þ H2 O/H3 Oþ Hydronium ions react with the basic (dissociated) form (In) of the indicator dye, resulting in an acid (protonated) form (HIn) which in turn produces a color change of the indicator containing solution or label.
Hþ þ In /HIn There are certain drawbacks are associated with use of pH-based sensors that CO2 levels cannot be measured directly, but in its ionic form and, therefore, the pH-value measurement could
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be impaired by other volatile acid or basic gases produced during spoilage. And also, maintenance costs are very high. 2.2.3. Fluorescent CO2 sensors Similar to the colorimetric method except that a fluorescent dye is used to generate its own radiative energy at a different wavelength to that of the excitation wavelength. The generated excitation spectra will depend on the sample gas concentration. CO2 measuring instrumentation also fabricated using this principle (Choi & Hawkings, 1995a,b; Wolfbeis & Weis, 1998). A printable oxygen and carbon dioxide sensors formulations have been developed for application in food packaging (McEvoy et al., 2003); the oxygen was measured by detecting the degree of quenching of a fluorescent ruthenium complex entrapped in a solegel matrix. For monitoring CO2 gas, a fluorescence-based and pH-sensitive 8-hydroxypyrene-1, 3, 6-trisulfonic acid (HPTS) indicator dye encapsulated in organically modified silica (ORMOSIL) glass matrix was used. In the context of in-situ monitoring of analytes, issues such as cross-reactivity, robustness, and humidity interference need to be addressed before realizing the full potential. 2.2.4. Dry optical CO2 sensors A novel plastic film incorporated with fluorescent dye HPTS was used to sense CO2 gas with a 0e90% response and recovery times of the film when exposed to an alternating atmosphere of air and 5% CO2 are typically 4.3 and 7.1 s, respectively (Mills & Chang, 1993). Phase transfer agent (PTA) such as tetraoctyl ammonium hydroxide (TOAH) plays vital role in the fabrication of solid, dry CO2 sensors. PTA agent in its general form, QþOH, can be used to dissolve the anionic form (D) of a colorimetric pH indicator dye, such as m-cresol purple (MCP), in a hydrophobic solvent, such as toluene, that is mutually compatible with that of a water-insoluble polymer, such as ethyl cellulose (EC) or poly vinyl butyral (PVB) (Mills, 2009). Thus, it was found that mixing of pH-sensitive, hydrophilic indicator dye anion with phase transfer agent result in formation of ion pairs, QþD, which can be dissolved in hydrophobic solvents. Therefore, a color-based dry CO2 sensor comprises a pH-sensitive dye/phase transfer agent/polymer/solvent, which could be cast, by printing, spin-coating, to generate a range of thin, colored plastic films containing a pH-sensitive dye in its deprotonated anionic form, i.e. as QþD. Carbon dioxide levels in dry and humid gases can be determined by using these types of solid dry sensors. The sensor sensitivity toward CO2 decreased with increase of temperature. Also, acidic and oxidizing gases have a marked and irreversible deleterious effect on the response features. A luminescence intensity-based dry optical sensor film was designed using the luminescent dye, HPTS, the phase transfer agent, TOAH, the polymer, EC, and the plasticizer, tributyl phosphate (TBP) (Mills & Chang, 1993). 2.2.5. Solegel-based optical CO2 sensor An optical solegel-based CO2 sensor strip was fabricated using a fluorescent pH indicator, 1-hydroxypyrene-3, 6, 8-trisulfonate (HPTS) (Bültzingslöwen et al., 2002). The sensor exhibited a fast and reversible response to carbon dioxide over a wide range of concentrations (0e100% CO2) with sufficient resolution (2%). The dye was immobilized in hydrophobic organically modified silica matrix. Cetyltrimethylammonium hydroxide (CTA-OH), a quaternary ammonium base, was used as an ion-pairing agent for a polar pH indicator in a non-polar gas permeable membrane, and also it functions as internal buffer. The Dual Luminophore Referencing (DLR) sensing method, an internal ratiometric method, is used for measuring the fluorescence. In which, the analyte-sensitive fluorescence intensity signal is converted into the phase domain by co-immobilizing an inert long-lifetime reference luminophore
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having similar spectral characteristics. Ruthenium complex and HPTS dye are the excellent candidates for a DLR-type CO2 sensor because their excitation and emission wavelengths are well matched. Oxygen cross-sensitivity is minimal and compatible with established optical oxygen sensor technology. 2.2.6. Photonic crystal sensors 2.2.6.1. Polymer opal films. Color changing polymer opal films have been developed by various research groups and were initially developed at the University of Southampton in the United Kingdom and the Deutsches Kunststoff-Institut (DKI) in Darmstadt, Germany. The polymer opals are a type of photonic crystal consisting of a 3D lattice of plastic spheres but have a large contrast in their components’ optical properties. This causes a range of frequencies to occur and, therefore, causes variations in the light that is reflected from these regions, also called photonic band gaps. Tiny carbon nanoparticles can be wedged between the crystalline spheres. Thus, incident light cannot reflect at the interfaces between the crystalline spheres and the surrounding materials, but scattering of light can occur. Due to a high surface to volume ratio of nanoparticles, an intense color is generally observed in produced opal films. The color depends on manner of arrangement of the spheres and the placement of the nanoparticles. Stretching of flexible films will cause orientation of the lattice structure and changes to the distance between the spheres. This will cause a change in color to appear. 2.2.6.2. Polymer hydrogel-based CO2 sensor. In response to external stimuli, polymer hydrogels can exhibit large reversible change in their volume, and thus regarded as suitable materials for chemical sensors. These kinds of sensors are best suited for food packaging applications due to the fact that they don’t require sophisticated and expensive detection systems. They offer fast response times, and are robust. Also, sensors have a long lifetime (>6 months) without degradation of response time or reproducibility. Volume change in hydrogel is exerted by Donnan potential between the analyte ions and their receptor which is covalently bound to the hydrogel building block (Shin, Braun, & Lee, 2010). In order to compensate the local ion inhomogeneity, there is influx of water molecules to the hydrogel. Color change of sensor is observed due to volume change in periodic structure, known as photonic crystal. These hydrogels are imprinted with photonic crystal; such color is often called ‘structural color’. Relatively simple optical detection techniques are possible using hydrogel photonic crystal sensor, for a wide variety of analytes such as protons (Debord & Lyon, 2000; Xu, Goponenko, & Asher, 2008), metal ions, glucose, and volatile organic compounds (VOC). Therefore, a proton-based photonic crystal CO2 gas sensor could be fabricated for use in food packaging. 2.2.7. Color changing metals Recently, a research group identified the color changing nature of modified rhodium metal to different gases. The modified rhodium changes to yellow in the presence of nitrogen, deep blue in the presence of oxygen, and brown in the presence of carbon monoxide. According to head of the team, the gases bind to the compound’s central metal without disrupting the exact placement of each individual atom in the compound’s crystalline lattice in an unprecedented way (Queen’s University, 2011, July 21). This discovery could form the basis for development of early warning system if failure of MAP system occurs. However, this metal usage in food systems could be subject to food safety clearance. 3. Safety & regulatory aspects Indicators or sensors are intended to be placed inside the package exposing to headspace atmosphere and, therefore, safety
criteria have to be fulfilled. Often, packaging materials are in direct contact with food inside the pack, so the embedded or attached indicators to these packing materials must be suitable for direct food contact applications. A major role by nanotechnologies is expected in fulfilling the additional safety considerations and existing gap in knowledge (Danielli, Gontard, Syropoulos, Zonderwan Van Den Beuken, & Toback, 2008). For innovative food packaging technologies to be successful, they must comply with strict regulations. Most of the active and intelligent agents are considered as food-contact material constituents, not as additives, and, therefore, food packaging systems must comply with the existing food-contact materials regulations. According to the EU framework directive, all the food-contact materials shall not be hazardous to human health and shall not affect the composition or sensory character of the packed foodstuff in an unacceptable way (De Kruijf et al., 2002). 4. Conclusions It can be concluded that the optical carbon dioxide gas sensors are suitable for food package indicator applications. Especially, dry optical sensors containing pH-sensitive dye indicators are better suited for CO2 monitoring and/or as spoilage indicators in food packaging application. However, issues such as humidity interference, lifetime, cost, safety, and proton generation during other oxidative reactions have to take into consideration before realizing the complete potential of pH-based sensors. Water-based, CO2 indicator inks can be used potentially in food package applications. Although they are relatively less sensitive toward CO2 than their solvent-based counterparts, posses more stable shelf life and quick response/recovery time. On the other hand, photonic crystal sensors are promising due to low cost, long lifetime, suitability to wide variety of analytes, and effective indication with quick response time. However, there is still more research efforts are necessary for the development of food application-specific sensors. Acknowledgments This research was supported by the Agriculture Research Center program of the Ministry for Food, Agriculture, Forestry and Fisheries, Korea. References Ahvenainen, R. (2003). In R. Ahvenainen (Ed.), Novel food packaging techniques. Finland: CRC Press. Andersen, J. J., & Skibsted, L. H. (1991). Oxidative stability of frozen pork patties: effect of light and added salt. Journal of Food Science, 56, 1182e1184. Balderson, S. N., & Whitwood, R. J. (1995). Gas indicator for a package (Trigon Industries Limited, Auckland, New Zealand). US Patent 5439648. Bültzingslöwen, C. V., McEvoy, A. K., McDonagh, C., MacCraith, B. D., Klimant, I., Krause, C., et al. (2002). Solegel based optical carbon dioxide sensor employing dual luminophore referencing for application in food packaging technology. Analyst, 127, 1478e1483. Choi, M. F., & Hawkings, P. (1995a). Novel dye-solvent solutions for the simultaneous detection of oxygen and carbon dioxide. Analytical Chemistry, 67, 3897e3902. Choi, M. F., & Hawkings, P. (1995b). A novel oxygen and/or carbon dioxide-sensitive optical transducer. Talanta, 42(3), 483e492. Danielli, D., Gontard, N., Syropoulos, D., Zonderwan Van Den Beuken, E., & Toback, P. (2008). Active and intelligent food packaging: legal aspects and safety concerns. Trends in Food Science & Technology, 19, 99e108. Debord, J. D., & Lyon, L. A. (2000). Thermoresponsive photonic crystals. The Journal of Physical Chemistry B, 104, 6327e6331. De Kruijf, N., Van Beest, M., Rijk, R., Sipiläinen-Malm, T., Paseiro Losada, P., & De Meulenaer, B. (2002). Active and intelligent packaging: applications and regulatory aspects. Food Additives and Contaminants, 19(Suppl.), 144e162. Dieckmann, M., & Buchholz, R. (1999). Apparatus for measuring the partial pressure of gases dissolved in liquids. US Patent 6003362. Eaton, J. C., Kilgore, M. B., & Livingston, R. B. (1977). Visual spoilage indicator for food containers. US Patent 4003709.
P. Puligundla et al. / Food Control 25 (2012) 328e333 Giraud, G., & Halawany, R. (2006). Consumers’ perception of food traceability in Europe. Paper presented at the 98th EAAE Seminar, Chania, 29 Junee2 July. Gontard, N. (2004). Active packaging for food processing and preservation. In International congress on engineering and food: ICEF 9, 7e11 March, Montpellier, France. Han, J. H., Ho, C. H. L., & Rodrigues, E. T. (2005). Intelligent packaging. In J. H. Han (Ed.), Innovations in food packaging. Elsevier Academic Press. Hauser, P., & Liang, C. (1997). All solid-state instrument for absorbance based optical gas sensor membranes. Instrumentation Science & Technology, 25(2), 147e156. Hong, H. S., Kim, J. W., Jung, S. J., & Park, C. O. (2005). Thick film planar CO2 sensors based on Na b-alumina solid electrolyte. Journal of Electroceramics, 15(2), 151e157. Hong, S.-I., & Park, W.-S. (1997). Sensitivity of color indicators to fermentation products of kimchi at various temperatures. Korean Journal of Food Science and Technology, 29, 21e25. Hong, S.-I., & Park, W.-S. (1999). Development of color indicators for kimchi packaging. Journal of Food Science, 64, 255e257. Kawabata, Y., Kamichika, T., Imasaka, T., & Ishibashi, N. (1989). Fiber-optic sensor for carbon dioxide with a pH indicator dispersed in a poly (ethylene glycol) membrane. Analytica Chimica Acta, 219, 223e229. Marazuela, M. D., Moleno-Bondi, M. C., & Orellana, G. (1995). Enhanced performance of a fiber-optic luminescence CO2 sensor using carbonic anhydrase. Sensors and Actuators B, 29, 126e131. Mattila, T., & Ahvenainen, R. (1989). Preincubation time and the use of oxygen indicators in determining the microbiological quality of aseptically packed pea and tomato soup. International Journal of Food Microbiology, 9, 205e214. Mattila, T., Tawast, J., & Ahvenainen, R. (1990). New possibilities for quality control of aseptic packages: microbiological spoilage and seal defect detection using head-space indicators. Lebensmittel-Wissenschaft & Technologie, 23, 246e251. McEvoy, A. K., Von Bueltzingsloewen, C., McDonagh, C. M., MacCraith, B. D., Klimant, I., & Wolfbeis, O. S. (2003). Optical sensors for application in intelligent foodpackaging technology. Proceedings of SPIE, 4876, 806. doi:10.1117/12.464210. Mheen, T. I., & Kwon, T. W. (1984). Effect of temperature and salt concentration on kimchi fermentation. Korean Journal of Food Science and Technology, 16, 443e450. Mills, A. (1998). International symposium on printing and coating technology, conference proceedings, Swansea, UK, 12-1e12-11. Mills, A. (2009). Optical sensors for carbon dioxide and their applications. In M.I. Baraton (Ed.), Sensors for environment, health and security (pp. 347e370). Mills, A., & Chang, Q. (1993). Fluorescent plastic film sensors for carbon dioxide. Analyst, 118, 839e843. Mills, A., & Chang, Q. (1994). Tuning colourimetric and fluorimetric gas sensors of carbon dioxide. Analytica Chimica Acta, 285, 113e123. Mills, A., & McMurray, H. N. (1991). Carbon dioxide monitor (Abbey Biosystems Ltd, Dyfed, UK). PCT International patent application WO 91/05252. Mills, A., & Monaf, L. (1996). Thin plastic film colorimetric sensor for carbon dioxide: effect of plasticizer on response. Analyst, 121, 535e540.
333
Mills, A., & Skinner, G. A. (2010). Water-based colourimetric optical indicators for the detection of carbon dioxide. Analyst, 135, 1912e1917. Mills, A., Chang, Q., & McMurray, N. (1992). Equilibrium studies on colorimetric plastic film sensors for carbon dioxide. Analytical Chemistry, 64, 1383e1389. Mills, A., Lepre, A., & Wild, L. (1997). Breath-by-breath measurement of carbon dioxide using a plastic film optical sensor. Sensors and Actuators B, 38-39, 419e425. Mook, W. G., & de Vries, J. J. (2000). Environmental isotopes in the hydrological cycle: principles and applications. In W. G. Mook (Ed.), Introduction, theory, methods, review, Vol. I (pp. 143e166). Vienna, Austria: UNESCO/IAEA. Neethirajan, S., Jayas, D. S., & Sadistap, S. (2009). Carbon dioxide (CO2) sensors for the agri-food industry e a review. Food and Bioprocess Technology, 2, 115e121. Nopwinyuwong, A., Trevanich, S., & Suppakul, P. (2010). Development of a novel colorimetric indicator label for monitoring freshness of intermediate-moisture dessert spoilage. Talanta, 81(3), 1126e1132. Pacquit, A., Frisby, J., Diamond, D., Lau, K. T., Farrell, A., & Quilty, B. (2007). Development of a smart packaging for the monitoring of fish spoilage. Food Chemistry, 102, 466e470. Pacquit, A., Lau, K. T., McLaughlin, H., Frisby, J., Quilty, B., & Diamond, D. (2006). Development of a volatile amine sensor for the monitoring of fish spoilage. Talanta, 69(2), 515e520. Queen’s University. (2011, July 21). Modified metals change color in the presence of particular gases. ScienceDaily, Retrieved July 26, 2011, from. http://www. sciencedaily.com/releases/2011/07/110721131159.htm. Shin, J., Braun, P. V., & Lee, W. (2010). Fast response photonic crystal pH sensor based on template photo-polymerized hydrogel inverse opal. Sensors and Actuators B, 150, 183e190. Smolander, M., Hurme, E., & Ahvenainen, R. (1997). Leak indicators for modified atmosphere packages. Trends in Food Science & Technology, 8(4), 101e106. Smolander, M., Hurme, E., Latva-Kala, K., Luoma, T., Alakomi, H.-L., & Ahvenainen, R. (2002). Myoglobin-based indicators for the evaluation of freshness of unmarinated broiler cuts. Innovative Food Science and Emerging Technologies, 3(3), 279e288. Uttamial, M., & Walt, D. (1995). A fibre-optic carbon dioxide sensor for fermentation monitoring. Biotechnology, 13(6), 597e601. Varlan, A. R., & Sansen, W. (1997). Micromachined conductometric p(CO2) sensor. Sensors and Actuators B, 44, 309e315. Wayne, R. P. (2000). Chemistry of atmospheres (3rd ed.). Oxford: Oxford University Press. Weigl, B. H., & Wolfbeis, O. S. (1995). Sensitivity studies on optical carbon-dioxide sensors based on ion-pairing. Sensors and Actuators B: Chemical, 28, 151e156. Wolfbeis, O., & Weis, L. (1998). Fiber-optic fluorosensor for oxygen and carbon dioxide. Analytical Chemistry, 60, 2028e2030. Xu, X., Goponenko, A. V., & Asher, S. A. (2008). Polymerized PolyHEMA photonic crystals: pH and ethanol sensor materials. Journal of the American Chemical Society, 130, 3113e3119.