Modified atmosphere packaging for food preservation

Modified atmosphere packaging for food preservation

7

Umezuruike Linus Opara*, Oluwafemi J. Caleb†, Zinash A. Belay* *Postharvest Technology Research Laboratory, South African Research Chair in Postharvest Technology, Department of Horticultural Science, Faculty of AgriSciences, Stellenbosch University, Stellenbosch, South Africa †Post-harvest and Agro-Processing Technologies (PHATs), Agricultural Research Council (ARC), Infruitec-Nietvoorbij, Stellenbosch, South Africa Chapter outline 1 Introduction  235 2 Principles of MAP  238 2.1 Passive MAP  238 2.2 Active MAP  240

3 Emerging MAP systems  241 3.1 High O2/CO2  241 3.2 High humidity  241 3.3 Intelligent and smart MAP  242

4 MAP of fresh and minimally processed fruit  243 5 MAP of fresh and minimally processed vegetables  244 6 MAP of fresh and minimally processed mushroom  247 7 MAP of meat and fishery products  248 8 Microbiological and other consequences of MAP  251 9 Future prospects for MAP in food preservation  252 Acknowledgments  253 References  253 Further reading  259

1 Introduction Global production and marketing of fresh produce has continued to rise over the past few decades in response to growing consumer demand. In addition to contributing to food and nutrition security, the production and marketing of agricultural, horticultural, and aquatic produce contributes to livelihoods through income generation. Packaging plays a crucial role by facilitating the containment, transportation, and logistics of fresh and processed commodities (Opara, 2009; Opara et al., 2007). Modified atmosphere packaging (MAP) of fresh and minimally processed commodities refers to the technique of sealing the products in a packaging system that alters normal air composition and provide optimal gas composition around the product. Under conditions of reduced O2 and high CO2, the metabolic processes of the horticultural product and microbial Food Quality and Shelf Life. https://doi.org/10.1016/B978-0-12-817190-5.00007-0 © 2019 Elsevier Inc. All rights reserved.

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activity are slowed down, which contributes to extended shelf life (Antmann et al., 2008; Ares et al., 2007). In contrast, when MAP is used for non-respiring products, such as meat and aquatic food products, the aim is to retain the introduced optimal atmosphere inside the package during storage. Therefore, high barrier films composed of different layers of materials are used. Several gases have been used in MAP systems, each one having a different role in the preservation of food products. The main gases often used are oxygen, carbon dioxide, and nitrogen (O2, CO2, and N2). MAP richer in CO2 and poorer in O2 than air can potentially reduce physiological and biochemical processes and retards senescence for fruit and vegetables (Antmann et al., 2008). Carbon dioxide is known for its fungistatic and bacteriostatic properties in food systems and is, therefore, the most important gas used in MAP systems. The reduction of O2 slows down lipid oxidation and the development of rancidity as well as inhibiting the growth of aerobic microorganisms in fish, meat, and derived products. For these products, simple flushing with nitrogen is used as an alternative to vacuum packaging to replace O2 in the package. Furthermore, nitrogen gas is used in a gas mixture for MAP as a filler (e.g., CO2 and N2) because of its low solubility in water and fat, which prevents packaging collapsing. Recently, particular attention has been paid to the use of some inactive or noble gases, such as argon (Ar), helium (He), and nitrous oxide (N2O) (González-Buesa et al., 2014). These gases do not directly affect metabolism through modification of enzymes, however, they may increase the diffusivity of O2, C2H4, and CO2 from plant tissues because of their higher density than nitrogen, or inhibit respiration by affecting cytochrome oxidase activity in the mitochondria (Ma et al., 2017). Furthermore, it is well established that package permeability and the breathable film area play an important role in MAP system design and successful application (Caleb et al., 2012). Therefore, the choice of film is a key factor in order to obtain optimum modification of the atmosphere and relative humidity (RH) to avoid extremely low concentrations of gases and accumulation of water. Most polymeric materials used in fresh produce packaging have lower water vapor transmission (Table 1). Therefore, most water molecules evaporated from the produce do not escape through the film and remain within the package, creating high in-package RH. Therefore, recent studies reported various approaches to control in-package RH during MAP. These include using perforated packaging films (Hussein et al., 2015; Bovi et al., 2016), creating humidity regulating packaging materials via direct incorporation of active substances into the package (Rux et al., 2015; Bovi et al., 2018), and designing humidity packaging systems incorporating two or more different packaging materials in one design (Belay et al., 2018; Rux et al., 2015). The most dominant external factor influencing MAP systems is storage temperature. Temperature influences both gas exchange of the produce and the permeability of the film for O2, CO2, and water vapor (Jacxsens et al., 2000). Most of the physical, biochemical, microbiological and physiological reactions contributing to deterioration of produce quality are largely dependent on temperature (Tano et al., 2007). Metabolic processes including respiration, transpiration, and ripening are particularly ­temperature-dependent (Beaudry et al., 1992). MAP in combination with cold storage temperatures could be used to inhibit microbial growth (Caleb et al., 2013). The market for MAP is categorized into health and personal care, food and beverages, pharmaceuticals, and other applications. This chapter focuses on MAP applied

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Table 1  Barrier and functional properties of packaging film for modified atmosphere packaging Types of film

Barrier properties

Functional properties

Polyethylene: Low-density polyethylene (LDPE) Linear low-density Polyethylene (LLDPE) High-density polyethylene (HDPE)

LDPE has low permeability to water vapor and high permeability to gases HDPE has better gas-barrier properties than LLDPE but poor clarity

LDPE has high sealing qualities, can be laminated, extrusion coated, or coextruded LLDPE has better impact strength, tear resistance, higher tensile strength and elongation, greater resistance to environmental stress cracking, and better puncture resistance HDPE has a higher softening point than LDPE and is not suitable as a sealant layer PP can be extruded or coextruded to provide a sealant layer OPP is grease resistance

Polypropylene (PP)

Oriented polypropylene (OPP) Coextruded-oriented polypropylene (COPP)

OPP is a high-water vapor and gas barrier COPP is a good water vapor barrier and gas barrier properties

Styrene polymers: Polystyrene Polyethylene terephthalate (PET)

Polystyrene is a poor barrier to gases and water vapor

Vinyl polymers: Vinyl acetate Copolymer (VAC) Ethylene vinyl alcohol (EVOH) Polyvinyl chloride (PVC) Polyvinylidene chloride (PVDC) copolymer

VAC has high permeability to gas and water vapor EVOH is a high gases barrier but is moisture sensitive PVDC is low permeability to water vapor and gases PVC is good gas barrier and moderate barrier to water vapor

Cellulose based film Cellulose acetate, cellulose butyrate, cellulose propionate

COPP can be laminated as a part of the lidding material and can be used as breathable packaging Polystyrene is brittle PET has high clarity and can be used as a low-gaugeoriented film. It can be used in crystalline or amorphous phase VAC can be used as a sealant layer, highly flexible EVOH can be used between the main formable and sealant layer as a laminated sandwich PVDC used as a coating on polyester and OPP for lidding films PVC can be used as a thermoformable base

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to preserve food products, including fresh and fresh-cut fruit and vegetables, meat, poultry, seafood, and other food and beverages. It highlights the principles of MAP, discusses the latest and emerging technologies, and summarizes the applications of MAP in the fresh and minimally processed food industry.

2 Principles of MAP Modified atmosphere packaging (MAP) of fresh produce relies on change of the atmosphere inside the package (Fig. 1). This could be achieved by the natural interplay between two processes, the respiration of the product and the transfer of gases through the packaging, which leads to an increase in CO2 and decline in O2 concentrations. This atmosphere can potentially reduce respiration rate, ethylene sensitivity, and physiological changes. MAP generally involves the packaging of a whole or fresh-cut product in plastic film bags, and can be either passive or active. The success of atmospheric modification inside a package depends on factors summarized in Table 2. Under optimal storage temperatures, MAP systems have been successfully applied to preserve various fruit and vegetables, and non-respiring products such as meat and aquatic food products. Since responses differ for each type of fresh produce when packaged under MAP conditions, it is necessary to quantify the effect of the applied atmosphere for the individual product. Based on the product requirement, there are two approaches (passive and active MAP), their main differences are summarized in Table 3, and are discussed further in the next two sub-sections.

2.1 Passive MAP Passive MAP can be created by using natural air composition and relying on produce respiration to attain the desired gas mixture. Effective atmosphere modification is derived from RR of products and gas permeability of the packaging film, which induces a passively established steady-state gas composition after a long transient period (Mahajan et al., 2008). After a given time, gas composition in the package of a fresh product reaches a definite balance between RR and permeability of packaging

Fig. 1  The dynamics of atmosphere inside modified atmosphere packaging.

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Table 2  Factors influencing optimal MAP for fresh or minimally processed fruit and vegetables Factor(s)

Variables

Produce

Produce weight Produce density Respiration rate Transpiration rate Ripeness stage Initial microbial load Gas ration and concentration Storage temperature Relative humidity Storage duration Volume Thickness of the film Film surface area for gas flux Gas permeability Number of perforations Radius of perforations Number of tubes Length of tubes Diameter of tubes and porosity of the tube packing

Extrinsic

Packaging

Perforation

From Fonseca, S.C., Oliveira, F.A., and Brecht, J.K., 2002. Modelling respiration rate of fresh fruits and vegetables for modified atmosphere packages: a review. J. Food Eng. 52(2), 99–119; Mahajan, P.V., Oliveira, F.A.R., and Macedo, I., 2008. Effect of temperature and humidity on the transpiration rate of the whole mushrooms. J. Food Eng. 84(2), 281–288.

Table 3  Type of modified atmosphere packaging (MAP) for fresh-cut produce

Definition

Equilibrium time Products suitable for

Passive

Active

Modification of the gas composition inside a package due to interplay between the product respiration and the package permeability 1–2 days to 10–12 days Mushrooms, carrots, strawberry, spinach

Modification of the gas composition inside the package by flushing the package headspace with desired gas mixture

Cost

No extra cost involved if the package is properly designed

Labeling requirements

No

1–2 h Cut apples, minimally processed leafy green vegetables, pomegranate arils Extra investment is required for special machinery, i.e., gas mixer, gas flushing and packaging machine Yes

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film. In this state of equilibrium, the total amounts of CO2 produced and O2 consumed by respiration are the same as that permeated through membrane exchange (Fonseca et  al., 2002). The gas equilibrium state is thus influenced by RR of fresh produce, storage environmental factors (such as temperature and RH), and the permeability of the packing materials (Zhang et al., 2015a). Passive MAP can effectively maintain the quality attributes and shelf life of horticultural commodities at lower storage temperature than unpacked commodities. Passive MAP in amide-PE bags improve the firmness and retain good fresh quality of fresh-cut kohlrabi (Escalona et al., 2007), control dehydration, and reduce mesophilic and psychrotrophic bacteria yeast growth. Passive MAP extends the shelf life of freshcut cantaloupe by sealing it with Cryovac LDX-5406 film for 9 days at 5°C (Bai et al., 2003). However, there are disadvantages of using passive MAP, including the protracted transient period required to achieve a desired atmosphere inside the packages and the risk of anoxia (Horev et al., 2012).

2.2 Active MAP Active MAP involves gas flushing or scavenging, or the use of emitters. Active gas flushing relies on displacement of air with desired gas mixture to accelerate the establishment of the optimum gas composition and avoid exposure to unsuitable gas compositions for extending shelf life or improving safety, while maintaining quality (Fonseca et al., 2005). Numerous studies report the benefit of using replacement of normal air by low O2 and enriched CO2 atmosphere (Oms-Oliu et al., 2008; Costa et al., 2011), aiming to reduce the RR by providing a favorable atmosphere inside the package. On the other hand, the use of super atmospheric O2 (>70%) is mainly aimed at reducing loss of firmness, reducing microbial growth, and maintaining antioxidants (Escalona et al., 2007). In the case of a gas-scavenging or emitting system, the most commercially important form of active packaging are small sachets of oxidizable iron based compounds used as O2 scavengers (Kartal et al., 2012), which can prevent fruit discoloration and minimize chilling injuries. The O2 scavengers have proven to be especially effective for reducing spoilage, delaying senescence, and reducing browning and mold incidence in fresh produce (Lee et al., 2014). On the other hand, CO2 absorbers can prevent a build-up of CO2 to injurious levels (Brody et al., 2001). Similarly, ethylene absorbers can help delay the climacteric rise in respiration and associated ripening for some fruit by scrubbing ethylene inside the package. The application of scavengers have been proven to be effective for kiwifruit, bananas, avocados, mushrooms, and persimmons (Ozdemir and Floros, 2004). However, the use of scavenging sachets suffers from inadequate consumer acceptance and they are not appropriate for liquid foods, as direct contact of the liquid with the sachets usually causes spoilage of sachet contents (Ozdemir and Floros, 2004). Munro et al. (2009) reported that these sachets may be accidentally consumed with food or may be ingested by children. Synergistic effects of using oxygen scavenger sachets/pads utilizes the process of rusting or oxidation of iron compound in the presence of oxygen and water (Suppakul et al., 2003). Concerns are also expressed about oxygen scavengers allowing potential over growth of anaerobic pathogenic organisms (Munro et al., 2009). Thus, understanding the dynamics of MAP and individual food

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product characteristics and selecting the type of MAP according to the objective to be achieved is essential to benefit from MAP application.

3 Emerging MAP systems 3.1 High O2/CO2 Successful application of MAP requires selection of optimum gas as well as appropriate packaging film with gas permeability and water vapor transmission rate (WVTR) to balance moisture loss and water vapor condensation. Perforated (micro or macro) packaging films are commonly used to enhance O2 and CO2 gas permeability and control moisture around FFV. Such packaging films have the advantage of avoiding accumulation of CO2 and maintaining higher concentration of O2 (Hussein et al., 2015). Perforation of polymeric film is based on a compromise principle, since perforations affect the film’s permeability to O2 and CO2 to a higher extent than water vapor transmission. Super atmospheric O2 atmospheres (O2 > 70%) have been investigated as alternatives to low O2 in MAP for fresh products. Jacxsens et al. (2001) reported on the effects of super atmospheric O2 on microbial and sensory properties of fresh-cut vegetables and mushrooms. The authors showed that super atmospheric O2 atmospheres (80% and 92%) inhibited the growth of A. flavus and B. cinerea, prevented anaerobic fermentation, and inhibit enzymatic discoloration. Ayhan and Eştürk (2009) reported increases in antioxidant activity and bacteria counts for minimally processed pomegranate arils (cv. Hicaznar) stored under super atmospheric O2 gas composition (70%). Other studies have explored the use of high or absolute concentration 100% N2 atmospheres in MAP systems, because of the gas’ ability to maintain produce quality (Ayhan and Eştürk, 2009; Ahmed et al., 2011). For instance, quality attributes of persimmon fruit packaged in 100% N2 were maintained and shelf life extended, at 0°C for 90 days (Ahmed et al., 2011). Fresh-cut cabbage and lettuce MA-packaged with 100% N2 stored at 1°C and 5°C, respectively, maintained their quality and appearance by the end of storage day 5 (Koseki and Itoh, 2002). Generally, N2 is used to displace O2; thereby, it helps to delay oxidative processes inside the package (Caleb et al., 2013).

3.2 High humidity Conventional polymeric films used in fresh produce packaging often have lower water vapor transmission rates in comparison to the transpiration rates of fresh products. High in-package relative humidity due to water vapor released by horticultural products, if not adequately managed, can result in water condensation on the packaging material and products. This represents a risk to product quality and safety (Bovi et al., 2016; Linke and Geyer, 2013). In addition, excess moisture in packages can have a detrimental impact on powdered/flour products, which could lead to caking and/or softening. Water vapor condensation will occur on the surface of any product and packaging material that is at or below the dew point temperature of the surrounding

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air (Bovi et  al., 2016). There is a critical challenge balancing between low (below required limits) and excessively high humidity. Humidity below required limits could result in excessive water loss and shriveling of fresh commodities; on the other hand, excessively high humidity is a favorable condition for accelerated microbial growth and decay. Hence, the effective management of high humidity in MAP systems for food application is essential. Various strategies for managing high humidity inside packaged fresh produce have been reported in literature. For instance, micro-perforations are commonly used in fresh produce packaging to enhance mass transfer across the packaging material (­Ben-Yehoshua et al., 1998; Almenar et al., 2007; Hussein et al., 2015). The application of moisture absorbers presents another innovative and versatile approach for managing high humidity. The absorbers can be classified into two main application approaches, based on: (i) the use of contact moisture absorbers (Mahajan et al., 2008; Song et al., 2001); and (ii) the use of non-contact moisture absorbers (Bovi et al., 2018; Rux et al., 2015).

Generally, water contact absorbers are commercially used for packaging of meat products, such as fish, beef, and pork (Fang et al., 2017). The different forms of contact absorbers used to regulate moisture in fish and meat foods include pads, superabsorbent polymeric laminate films, and sachets (Ozdemir and Floros, 2004). The use of non-­ contact moisture absorbers is most suitable for fresh produce application as these products actively respire and transpire, releasing water vapor inside the package headspace in the process (Bovi et al., 2018). In addition, a packaging material with high water vapor permeability or a combination of different polymeric films is used to optimize the in-package humidity (Caleb et al., 2016; Belay et al., 2018; Volpe et al., 2018).

3.3 Intelligent and smart MAP Intelligent and smart MAP is a packaging system that is capable of carrying out intelligent functions (such as detecting, sensing, recording, tracing, communicating, and applying scientific logic) to facilitate decision making to extend shelf life, enhance safety, improve quality, provide information, and warn about possible problems (Yam et al., 2005; Sandhya, 2010). The conceptual framework describing the flow of information in an intelligent and smart system consists of four components: smart package devices, data layers, data processing, and information highway (wire or wireless communication networks) in the food supply chain (Ahvenainen, 2003; Urmila et al. (2015). Smart package devices are inexpensive labels or tags that are attached onto primary packaging (for example, pouches, trays, and bottles) (Caleb et al., 2012). There are two basic types of smart package devices: data carriers (such as barcode labels and radio frequency identification [RFID] tags) that are used to store and transmit data, and package indicators (such as time–temperature indicators, gas indicators, biosensors) that are used to monitor the external environment and, whenever appropriate, issue warnings (Arvanitoyannis and Stratakos, 2012; Salinas et al., 2012). In a MAP product, the respiration of the fresh produce, gas flux through the packaging film, gas generation by spoilage microbes, or leakage, may cause a change in

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gaseous composition within the package (Caleb et al., 2012). Gas indicators in the form of labels or print on the packaging films can help to monitor the safety and quality of the packed produce (Yam et al., 2005). Oxygen indicators are the most frequently used gas indicator, this is due to the ability of oxygen to cause oxidative color change and enhance microbial spoilage. Smiddy et al. (2002) suggested the use of a non-­destructive oxygen sensor as a leakage indicator. These sensors were able to detect very low oxygen levels (0.07%), and their function was based on the measurement of phosphorescence intensity and phase shift. On the other hand, a carbon dioxide indicator can be used to detect early spoilage as well as to monitor the levels of carbon dioxide within modified atmosphere packages in transit and within storage facilities (Hong and Park, 2000; Neethirajan et al., 2009; Poyatos-Racionero et al., 2018). Kuswandi et al. (2013) developed a bromophenol blue based dye to monitor guava (Psidium guajava L.) freshness. The dye was immobilized onto a cellulose membrane by absorption, and changes from blue to green were observed when the pH decreased as a consequence of the over-ripening of the guava due to the production of volatile organic compounds. For meat, colorimetric indicators have most often been applied in chicken and pork. Chen et al. (2014) and Urmila et al. (2015) developed an optoelectronic nose composed by pH indicators and metalloporphyrins. The authors developed a system by printing chemically responsive dyes (9 metalloporphyrins and 3 pH indicators (bromocresol green, bromocresol purple, and neutral red)) on a silica-gel flat plate. Salinas et al. (2012) developed an array composed of 16 sensing materials using the combination of different dyes for chicken meat packed in MAP (30% CO2 and 70% N2). Color changes of the array were characteristics of chicken meat aging in MAP. In general, the function of most of these indicators is based on color alteration as a result of a chemical or enzymatic reaction (Ahvenainen, 2003).

4 MAP of fresh and minimally processed fruit Minimally processed fruit are different from intact fruit and vegetables, since processing results in tissue disruption and compromised cell integrity, with a concomitant increase in metabolic and microbiological activity (Chonhenchob et  al., 2007). Furthermore, cutting could induce elevated ethylene production rates that could stimulate respiration rate and promote ripening of climacteric fruits, and consequently accelerate microbial growth (Brecht 1995). Studies conducted by Iqbal et al. (2009) demonstrated that fresh-cut fruit and vegetables being sliced, finely shredded, coarsely shredded, cubed, and grated could affect respiration rate and senescence. Minimal processing of fresh produce involves sorting, cleaning, washing, trimming/peeling/deseeding/coring, and cutting (such as chopping, slicing, shredding, chunking, and dicing). MAP has been applied more extensively to whole fresh fruit and less to fresh, minimally processed fruit. This includes fresh produce such as strawberries (Sanz et al., 1999; Sanz et al., 2000; Almenar et al., 2007), loquat fruit (Amoros et al., 2008), mandarin (Del-Valle et al., 2009), and many other high and medium-respiring produce. However, researchers have recommended various optimal gas compositions for freshcut produce (Fig. 2). Cliff et al. (2010) reported on the quality of fresh-cut Gala apple

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Fig. 2  Optimal gas composition for fresh-cut produce.

slices stored in micro-perforated MAP systems. They found that packages with a high O2 and high CO2 atmosphere had better fruitiness, sweetness, firmness, and higher fruitiness-by-mouth quality, as compared to the standard solid film (non-perforated) with low O2 and high CO2 atmosphere. Quality attributes of fresh-cut Gala apple slices were best maintained under MAP composition (14% O2 and 7% CO2). Successful use of MAP to maintain quality and extend shelf life of fresh produce must be accompanied by appropriate storage temperature, use of good quality of produce with minimal physiological damage, and the application of appropriate treatments to reduce microbial spoilage (Krasnova et  al., 2012). Various measures can be taken to reduce deterioration of fresh produce, including good agricultural and processing practices (such as harvesting produce at optimum maturity stage and minimizing mechanical injuries), proper sanitation procedures, adherence to HACCP principles, as well as the application of the optimal postharvest treatment (Artés et  al., 2009; Weerakkody et al., 2010; Mahajan et al., 2014). This would help to minimize quality deterioration and the risk of microbial contamination in perforated modified atmosphere packages (Boonruang et al., 2012; Oliveira et al., 2012).

5 MAP of fresh and minimally processed vegetables Fresh and minimally processed vegetables are living, respiring, and the edible tissues continue to be metabolically active after harvest. These metabolic and biochemical processes can be influenced by changing the environmental conditions during handling and storage. The specific environmental conditions vary widely, not only between the different types and cultivars, but also within the same cultivar grown in different seasons or locations, as well as between the fresh and processed forms (Jayas and Jeyamkondan,

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2002). Therefore, delaying the metabolic processes delays the postharvest quality loss, which is desirable during distribution and for short-term storage before marketing. Unlike fresh vegetables, minimally processed vegetables are exposed to one or more processes such as trimming, peeling, washing, or slicing. The minimal processing steps induce or accelerate many physiological changes in vegetables, due to the disruption of plant cells and damage to membranes. This disruption increases the availability of nutrients, which in turn accelerates microbial growth, degrades product quality, and limits shelf life. One of the major challenges facing the production and marketing of fresh and minimally processed produce is rapid quality deterioration and reduced shelf life resulting from physiological disorders and presence of mechanical injuries (Hussein et al., 2015). Practical experience has demonstrated that tissues with high respiratory rates and/or low energy reserves have shorter postharvest lives (Rico et al., 2007). MAP for fresh and minimally processed vegetables, flushed with low O2 (1%–5%) and/or elevated CO2 (5%–10%) levels, maintains quality and consequently extend shelf life (Ghidelli et al., 2018; Zhang et al., 2015a). As presented in Table 4, passive MAP shows a beneficial effect for fresh-cut Athena cantaloupe cubes, retaining saleable quality for 9 days at 5°C, whereas, active MAP (4% O2 and 10% CO2) maintained quality better than passive MAP with better color retention and reduced translucency, RR, and microbial populations. For Parthenon broccoli, low O2 MAP containing 10% O2 and 5% CO2, reduced loss of quality parameters (overall appearance, odor, weight loss and color) and the decrease of functional compounds contents (chlorophyll and carotenoid pigments, vitamin C, total phenol content, and intact glucosinolates), compared to storage in air, at the end of storage (12 days) (Fernández-león et al., 2013). However, storage of some vegetables, such as spinach (Tudela et al., 2013) and fresh cut egg plants (Ghidelli et al., 2018) at low O2 concentration and high CO2 (1%–5% and 11%–15%, respectively) accelerated decay and accumulation of fermentative metabolites. For most vegetables, increasing CO2 concentration significantly increases Table 4  Recommended gas mixture for various fresh and minimally processed vegetables during modified atmosphere packaging Commodity

Storage atmosphere (O2:CO2) (%)

Storage temperature (°C)

Broccoli Shredded cabbage Sliced carrots Chopped butterhead lettuce Chopped green leaf lettuce Chopped red leaf lettuce Chopped romaine lettuce Sliced red onion Diced peppers Sliced or whole peeled potato Sliced zucchini

2–3: 6–7 5–7.5:15 2–5:15–20 1–3:5–10 0.5–3:5–10 0.5–3:10–15 0.5–3:5–10 2–5:10–15 3:5–10 1–3:6–9 0.25–1:0

0–5 0–5 0–5 0–5 0–5 0–5 0–5 0–5 0–5 0–5 5

Adapted from Oliveira, F., Sousa-Gallagher, M.J., Mahajan, P.V., and Teixeira, J.A., 2012. Development of shelf-life kinetic model for modified atmosphere packaging of fresh sliced mushrooms. J. Food Eng. 111(2), 466–473.

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Table 5  Types of gases in modified atmosphere packaging and their effect on fresh and minimally processed vegetables Types of gases Effect of carbon dioxide

Absence of CO2

High CO2

Effect of oxygen

Low O2

Super atmospheric O2

General effects

References

Advantages: Reduce degradation of chlorophyll, which is related to greenness of harvest vegetables Advantages: bacteriostatic effect, results inhibition of Gram-negative bacteria, such as Pseudomonas spp., or Enterobacteriaceae Advantages: with or without CO2 can reduce the number of psychrophiles and Pseudomonas microorganisms CO2 Disadvantages: off odor development Advantages: inhibits microbial growth and decay reduce deterioration of fresh processed vegetables and proliferation of aerobic spoilage microorganisms

Tudela et al. (2013)

Scifò et al. (2009) and Goulas et al. (2005)

Tudela et al. (2013)

Belay et al. (2018)

–

–

tissue damage, ammonia production, and darkening of tissues, and decreases protein content (La Zazzera et al., 2010; Albornoz and Cantwell, 2015). Recently, the application of super atmospheric O2 (>70%) has shown beneficial effects, particularly for controlling anaerobic microorganisms (Table  5), preventing anaerobic fermentation and controlling enzymatic browning. Super atmospheric O2 MAP (>85% O2) showed a beneficial effect for fresh-cut red chard baby leaves by lowering the natural microflora growth throughout 7 days at 5°C (Tomás-callejas et al., 2011). The effect of O2 concentrations reducing microbial growth can be related to the accumulation of reactive oxygen species that damage vital cell components, affecting cellular antioxidant protection systems of cell metabolism (Kader and Ben-Yehoshua, 2000). Another advantage of MAP is providing desired RH inside the package when appropriate permeable packaging film is selected; this helps to prevent weight loss and

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subsequent change in appearance. MAP significantly controls the weight loss and wilting of broccoli for 28 days by using micro-perforated polypropylene and non-­ perforated polypropylene films (Serrano et al., 2006). Similarly, MAP techniques (7% and 9% CO2) using OPP as amide-PE allowed extending the shelf life of kohlrabi sticks to 14 days at 0°C by reducing the RR and C2H4 production, whereas, sticks in perforated bags with a poor appearance reduced the shelf life (Escalona et al., 2007). Weight loss of pepper was reduced by 20% using perforated polyethylene packages at 8°C, 14°C, and 20°C, compared to unpacked pepper (Lownds et al., 1994).

6 MAP of fresh and minimally processed mushroom Mushroom is a fruiting body, mostly above ground, of higher fungi formed from spacious underground mycelia (hyphae) by the process of fructification (Kalač, 2009). Mushrooms are a rich source of nutrients, particularly proteins and minerals, as well as vitamins B, C, and D, and contain bioactive constituents such as phenolic compounds, terpenes, steroids, and polysaccharides, which have various biological activities (Lin et  al., 2017). Mushrooms are also known to exhibit antifungal, anti-inflammatory, antitumor, antiviral, antibacterial, hepatoprotective, anti-diabetic, hypolipedemic, antithrombotic, and hypotensive activities (Rathore et al., 2017). However, they are highly perishable, with a shelf life of 1–3 days at ambient temperature. Due to high metabolic activity and RR (Ares et al., 2007), overall structure (Oliveira et al., 2012), high moisture content, and high TR (Mahajan et al., 2008), causing difficulties in their distribution and marketing as fresh produce (Antmann et al., 2008). Loss of quality for mushrooms include browning, softening, cap development, off flavor, and secondary mold growth (Kim et al., 2006). MAP is the simplest, most economical, and effective way of extending the shelf life of fresh mushrooms (Kim et al., 2006). As summarized in Table 6, various studies report MAP containing low O2 and high CO2 for different mushroom cultivars, and the Table 6  Recommended modified atmosphere packaging conditions for different mushroom cultivars Mushrooms cultivars

Storage temperature (°C)

Storage atmosphere (O2:CO2) (%)

Oyster mushrooms (Pleurotus ostreatus) White mushrooms Kohlrabi Mushroom Shiitake mushrooms (Lentinus edodes) Shiitake mushrooms (Lentinus edodes) Button mushrooms (Agaricus bisporus)

4

15:5

4 5 4

5:4 21:0 21:0

Villaescusa and Gil (2003) Tao et al. (2006) Escalona et al. (2007) Li et al., 2014

4

2:10–13

Ye et al. (2012)

0 and 5

3–5:<12

Oliveira et al. (2012)

References

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r­ ecommended MAP condition for mushroom includes 3%–5% O2 and <12% CO2 (Ares et al., 2007; Oliveira et al., 2012). On the other hand, the deterioration of sensory characteristics of shiitake mushroom stored under both passive and active (5% O2 and 2.5% CO2) atmospheres using polyethylene and polypropylene at 5°C has been ­reported by Ares et al. (2007). For button mushroom, high CO2 (95%–100%) treatment significantly reduced browning index and increased antioxidant ability, maintained flavor, quality, and consumer acceptance during postharvest storage (Lin et  al., 2017). Using super O2 atmospheric (>70%) concentration effectively inhibited enzymatic browning and preserving microbial quality of shredded Agaricus mushrooms has been reported by Jacxsens et al. (2001). Similarly, MAP with 50% and 100% O2 concentration inhibited ethanol production, whereas active MAP with 3% O2 and 5% CO2 and passive MAP induced anaerobic fermentation for shitake mushroom stored at 10°C (Li et al., 2014). One major effect of MAP for mushrooms is reducing weight loss by reducing water transpiration rate and CO2 loss during respiration (Jiang et al., 2011). The weight loss of shiitake mushrooms significantly reduced by MAP compared to unpacked mushrooms (Ye et al., 2012). Even if MAP has been used for maintaining quality of mushrooms, one challenge of implementing MAP for mushrooms has been reported as the accumulation of moisture inside the package. Mushrooms are very sensitive to humidity levels; they have very high TR—over >90% of the weight at harvest is water—and they lack a skin as a barrier to diffusion (Mahajan et al., 2008). Therefore, the use of perforated packaging or moisture absorbers has been recommended in order to avoid quality deterioration (Antmann et al., 2008). Rux et  al. (2015) reported that mushrooms stored at 100% RH lost moisture at the rate of 0.03–0.22 mg kg−1 s−1. Thus, considering the nature of mushrooms, proper selection and maintenance of temperatures, proper internal humidity, and optimum atmosphere are the most important parameters for extending the shelf life of mushrooms. Optimum MAP design by using perforated packaging material has been reported for button mushrooms by Oliveira et al. (2012) and for Shiitake mushroom by Antmann et al. (2008). Oliveira et al. (2012) recommended 1 (58 perforations per m2) at 0°C, 1 (58 perforations per m2) at 5°C, 3 (174 perforations per m2) at 10°C and 6 (349 perforations per m2) at 15°C in order to avoid exceeding the recommended limit for CO2 concentration. Comparing the effect of active and passive MAP, active MAP (15% and 25% O2) led to a smaller reduction of shiitake mushroom deterioration than passive MAP in films which have 17 perforations/m2, 0.1 mm2 surface than 9.0 × 103 perforations/m2, 0.1 mm2 surface film at 5°C (Antmann et al., 2008). The use of MAP accompanied with low temperature storage can effectively retard the quality changes and extend shelf life of fresh-cut mushrooms (Kim et al., 2006; Mahajan et al., 2008).

7 MAP of meat and fishery products For meat and aquatic food products, elimination of O2 from the MAP and enriching it with high CO2 concentration helps to reduce microbial growth and oxidation of fat and retain color (Arvanitoyannis et al., 2011; Łopacka et al., 2017). The efficacy of

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MAP in prolonging the shelf life of packaged meat and aquatic products mainly relies on the antimicrobial properties of CO2 present inside the package. The presence of CO2 in the headspace of the packages inhibits microbial growth and causes a change in the microbial content to bacteria with lower spoilage capacity (McMillin, 2008; Fernández et al., 2009; Sivertsvik et al., 2002). In some cases, additional gases are used in combination with the above-mentioned gases, such as nitrous, nitric oxides, ethane, chlorine, carbon monoxide, and sulfur dioxide, to inhibit microbial growth and prevent oxidation. Moreover, helium, argon, xenon, and neon have also been used under MAP because they are very inert and serve well as filler gases. Studies on muscle meat showed that a CO2 range of 10% to 80% in a package enhances its bacteriostatic effect (Kerry et al., 2006). Therefore, the inclusion of CO2 discharging sachets is beneficial in such systems. Aquatic products are highly perishable, because of their high water activity, neutral pH, and presence of autolytic enzymes, and their deterioration is primarily because of bacterial action. Typical shelf life under icing and refrigerated storage conditions ranges from 2 to 14 days (Sivertsvik et al., 2002). The spoilage of fresh aquatic products is usually microbial; however, in some cases chemical changes, such as auto-­oxidation or enzymatic hydrolysis of the lipid fraction, may result in off odors and flavors (Fernández et al., 2010). Moreover, fish and seafoods normally have a particularly heavy microbial load, owing to the method of capture and transport to shore, slaughtering methods, evisceration, and the retention of skin in the retail portions. Microbial activity causes the breakdown of fish protein and trimethylamine oxide (TMAO), with a resulting release of undesirable fishy odors (DeWitt and Oliveira, 2016). Various active MAPs containing low O2 and high CO2 for aquatic food products have been shown to inhibit the normal spoilage flora and increase shelf life significantly (Table 7). Under MAP conditions, the growth of spoilage microorganisms is inhibited and the shelf life of fish can be extended by 1.5 to 2-fold compared with chilled storage in normal air (Fernández et al., 2010; Zhang et al., 2015b). However, the shelf life of fish products in MAP can be extended depending on raw material, temperature, gas mixtures, and packaging materials (Goulas et al., 2005). To avoid growth of anaerobes, the combination of CO2/N2 for fat fish products, and CO2/N2/O2 for low-fat fish, is used (Zhang et al., 2015b). Most significantly, CO2 is the most important gas used in MAP of aquatic products, because of its bacteriostatic and fungistatic properties. It inhibits growth of many spoilage bacteria and the inhibition is increased with increased CO2 concentration in the atmosphere (Sivertsvik et al., 2002). Its inhibitory effect is further related to its high solubility in both water-phase and lipids of muscle foods, which is further affected by temperature, where the lower the temperature, the higher the solubility. The sensitivity of bacteria in aquatic products to CO2 vary (Fernández et al., 2010; Özogul et al., 2002). In addition, MAP has been shown to maintain the texture, odor, and overall sensory quality and appearance of aquatic products. For fish and seafood, most gas mixtures do not include O2 (Table 4). This may be explained by the high rate of perishability of seafood, which results from psychrophilic spoilage bacteria growth, combined with muscle degradation by endogenous enzymes, and oxidative deterioration of the lipids (Torrieri et al., 2011). On the contrary, high O2 concentrations, in combination with

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Table 7  Modified atmosphere packaging conditions in aquatic products Aquatic food products

Storage Temperature (°C)

Storage atmosphere (O2:CO2) (%)

Shelf life (days)

Salmon fillets Sea bream Chinese shrimp Fresh sea bass fillets Atlantic salmon Striped red mullet Tuna Chub mackerel Cod loins Scallops Rainbow trout fillets Cod loins Abalone Sardines Sea bass slices Mediterranean Swordfish Nile tilapia Cod Atlantic Cod Bass (gutted) Dolphinfish Halibut (fillets) Mullet, red striped Shrimp, brown

4 4 2 ± 1 4 2 ± 2 1 2 4 −2 0 4 1.5 2 ± 1 2 ± 2 4 4

0:60 30:40 30:40 0: 60 0: 75 0: 50 60: 40 5: 50 5: 70 10: 60 2.5:7.5 5:50 30:40 0: 60 0: 80–100 0: 80–100

14 27–28 17 14 >28 9–10 >14 12 21 14 14 14 15 14 20 18

1 0 2 3 1 4 1 4

0: 50 50: 50C 0: 60 30:50 5:45 0:50 0:50 0:40

23 11 17 9 18 23 24 7

From Zhang et al., 2015a; Fernández et al., 2009; Özogul et al., 2002, Goulas et al., 2005; DeWitt and Oliveira, 2016.

CO2, are reported to preserve the red color of haem pigments (DeWitt and Oliveira, 2016). Similarly, Sivertsvik (2007) reported significant improvement in the overall quality of MAP pre-rigor farmed Atlantic cod fillets by the use of high oxygen content in a gas mixture of CO2 and O2. MAP for aquatic products also contributes to reduction of histamine formation than normal air packages (Özogul et al., 2002). The importance of estimating the concentration of histamine in fish and fish products is related to its impact on human health and food quality. Fish containing relatively high concentrations of histamine can cause poisoning or allergic reactions when consumed by some individuals (DeWitt and Oliveira, 2016). Another important factor in MAP of aquatic food products is storage temperature, since rate of deterioration is temperature-dependent and can be inhibited by the use of low storage temperature (e.g., fish stored on ice). However, the single most important concern with the use of MAP products is the potential for the outgrowth and toxin production by the non-proteolytic, Clostridium botulinum type E, which can

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grow at low temperatures (Özogul et al., 2002). Therefore, MAP can be combined with super chilling processes to extend further the shelf life and safety of fresh fish and seafood. In this technique, also known as partial freezing, the temperature is reduced to 1–2°C below the initial freezing point without allowing partial freezing (Zhang et al., 2015b). As can be seen in Table 5, most of the studies in the literature recommended low temperature (<5°C) storage of various aquatic products coupled with MAP for self-life extension. However, only high quality fish and seafood should be used to benefit from the MAP application. The desirable quality and shelf life of these products under MAP conditions depends on the species, fat content, initial microbial load, gas mixture applied, and storage temperature. Therefore, for ensuring the safety and extending shelf life of fish and seafood, maintenance of recommended chilling temperature and atmosphere with good hygiene practice during the supply chain is essential.

8 Microbiological and other consequences of MAP Microorganisms such as Pseudomonas spp., Erwinia herbicola, Flavobacterium, Xanthomonas, Enterobacter agglomerans, Lactobacillus spp., Leuconostoc mesenteroides, molds and yeasts are largely associated with spoilage of horticultural commodities (Caleb et al., 2013). The effectiveness of MAP to maintain safety of fresh and fresh-cut produce is mostly combined with optimal cold chain. Studies have shown that MAP could be used effectively to maintain the quality of fresh and fresh-cut fruit and vegetables (Kader and Watkins, 2000; Yahia, 2006). In contrast, the effect of MAP on spoilage microorganisms can vary depending on the type of produce packaged, the initial microbial load, and other extrinsic factors (Caleb et al., 2013). For instance, Francis and O'Beirne, 1998suggested that MAP conditions of 3% O2 and 5%–20% CO2 might increase the growth rate of L. monocytogenes. However, they observed that at higher CO2 concentrations, the growth of lactic acid bacteria increased and inhibited the growth of L. monocytogenes. Similarly, Bourke and O'beirne (2004) investigated the effects of packaging type, atmospheric composition, and storage temperatures on survival and growth of Listeria spp. in shredded dry coleslaw and its components. The authors observed a decline in Listeria spp. in shredded dry coleslaw at 3°C between days 10 and 12, while growth remained at initial inoculation levels under 8°C. The inhibition of Listeria spp. was attributed to the optimal gas composition between days 10 and 12, and the presence of competitive microflora. Artin et al. (2008) reported that CO2 concentration had a significant impact on neurotoxin gene expression and neurotoxin formation in non-proteolytic C. botulinum type E. The authors showed that the expression of cntE mRNA and the formation of extracellular neurotoxin were 2-fold higher with a headspace CO2 concentration of 70% (vol/vol) in comparison to headspace of 10% (vol/vol). A follow up study by Artin et al. (2010) reported that non-proteolytic C. botulinum differ from proteolytic C. botulinum type A1 ATCC 3502. They observed that CO2 concentration had little effect on the expression of cntE mRNA and the formation of extracellular neurotoxin, and the expression of

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C. botulinum type A1 ATCC 3502 neurotoxin cluster genes was dependent on growth phase rather than CO2 concentration. Generally, CO2 is the main gas component used in MAP systems that confers a significant measure of antimicrobial effect against spoilage/pathogenic microbes. Various theories to explain the mechanism of its antimicrobial have been suggested over the years; these include direct inhibition of the enzymatic reactions; alteration of cell membrane function such as uptake and absorption of nutrient; CO2 dissolving into bacterial membranes leading to decrease in intracellular pH; and direct changes in the physical and chemical properties of proteins. The inhibitory effect of CO2 is overall dependent on the types of natural microbial population present and the characteristics of the fresh produce (such as topology, texture, and macro/micro pores). Furthermore, food-associated pathogens such as C. perfringens, C. botulinum, and L. monocytogenes are minimally affected by CO2 concentration below 50% (Charles et al., 2003; Farber et al., 2003), which is detrimental to fruit tissue. Hence, the use of CO2 is most effective on produce with aerobic and psychrotrophic Gram-negative bacteria. Adequate background knowledge of natural microflora for each MA-packaged produce is essential for a successful MAP design. Extensive literature has shown MAP to control produce respiration rate and ethylene production and maintain high quality fresh fruit and vegetables. However, there are critical concerns on the management of microorganisms, which may be stimulated with moderate CO2 concentration inside packages. Especially under inconsistent storage or transit temperature conditions, packaging material that performs optimally at a given temperature may default when respiration rate of produce does not correlate with packaging film permeability at higher temperature. Furthermore, it has been established that erratic temperature contributes to fresh produce accelerated deterioration, increased metabolic rate, which can enhance microbial proliferation in fresh or minimally processed MAP. Hence, the importance of maintaining a strict cold chain along the whole distribution continuum cannot be over emphasized.

9 Future prospects for MAP in food preservation The global market for year-round supply of fresh, fresh-cut, and minimally processed produce has continued to rise, exceeding the financial value of the market for cereals and other agricultural products since the late the 1980s. Changes in consumer preference for fresh and safe foods has led to innovations in packaging technologies to deliver value to consumers. This trend assures the demand for modified atmosphere packaging (MAP) and related technologies for the handling and marketing of these commodities. Modified atmosphere packaging (MAP) has been applied in the food industry for over 90 years to extend shelf life, and maintain quality and safety of fresh and freshcut produce. Recently, MAP has experienced a rapid development in both scientific research and industrial applications as a leading tool for packaging high value fresh and fresh-cut produce. MAP technologies have been applied to manage the postharvest quality and marketing of a wide range of commodities including fresh and f­resh-cut

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fruits, vegetables, mushrooms, meat, and aquatic products. With foundations in passive and active modified atmospheres, more recent MAP systems include high‑oxygen MAP, controlled MAP, and intelligent MAP. Passive MAP relies on applying knowledge of the produce respiration and permeability of the packaging material to determine the equilibrium atmosphere inside the MAP. On the other hand, active MAP refers to the incorporation of additives into the package with the aim of maintaining or extending the product quality and shelf life. Intelligent MAP systems incorporate technologies that monitor the condition of packaged food to give information regarding the quality during handling, transport, and storage. The combination of advances in technological innovations and changing consumer demand have created push-pull factors that propel the demand for MAP in fresh, fresh-cut and, minimally processed foods. Developments in information and communication technologies for real time data and image capture, analysis, and transmission provide new possibilities, with better interaction between the consumer, product, and supply chains. The incorporation of biosensors into MAP for rapid detection and diagnosis of biological hazards offer new prospects for just-in-time management of food safety risks, including contamination. Drip loss continues to be a problem affecting fresh-cut MA packaged produce; in combination with MAP, this calls for the application of hurdle technologies such as edible coating to control the problem. Further research is warranted to improve our understanding of the impact of short-term breaks in the cold chain on the quality and safety of MA packaged produce.

Acknowledgments This work is based on the research supported wholly by the National Research Foundation of South Africa (Grant Number: 64813). The opinions, findings, and conclusions or recommendations expressed are those of the author(s) alone, and the NRF accepts no liability whatsoever in this regard.

References Ahmed, M., Yousef, A.R., Sarrwy, S.M.A., 2011. Modified atmosphere packaging for maintaining quality and shelf life extension of persimmon fruits. Asian J. Agric. Sci. 3 (4), 308–316. Ahvenainen, R., 2003. Active and intelligent packaging: an introduction. In: Ahvenainen, R. (Ed.), Novel Food Packaging Techniques. Woodhead, Cambridge, pp. 5–21. Albornoz, K., Cantwell, M.I., 2015. Fresh-cut kale quality and shelf-life in relation to leaf maturity and storage temperature. In: Proceedings of III International Conference on Fresh-Cut Produce: Maintaining Quality and Safety. Vol. 1141. pp. 109–116. Almenar, E., Del-Valle, V., Hernández-Muñoz, P., Lagarón, J.M., Catalá, R., Gavara, R., 2007. Equilibrium modified atmosphere packaging of wild strawberries. J. Sci. Food Agric. 87 (10), 1931–1939. Amoros, A., Pretel, M.T., Zapata, P.J., Botella, M.A., Romojaro, F., Serrano, M., 2008. Use of modified atmosphere packaging with microperforated polypropylene films to maintain postharvest loquat fruit quality. Food Sci. Technol. Int. 14 (1), 95–103.

254

Food Quality and Shelf Life

Antmann, G., Lema, P., Lareo, C., 2008. Influence of modified atmosphere packaging on sensory quality of shiitake mushrooms. Postharvest Biol. Technol. 49, 164–170. Ares, G., Lareo, C., Lema, P., 2007. Modified atmosphere packaging for postharvest storage of mushrooms. A Review. Fresh Produce 1 (1), 32–40. Artés, F., Gómez, P., Aguayo, E., Escalona, V., Artés-Hernández, F., 2009. Sustainable sanitation techniques for keeping quality and safety of fresh-cut plant commodities. Postharvest Biol. Technol. 51 (3), 287–296. Artin, I., Carter, A.T., Holst, E., Lövenklev, M., Mason, D.R., Peck, M.W., Rådström, P., 2008. Effects of carbon dioxide on neurotoxin gene expression in nonproteolytic Clostridium botulinum type E. Appl. Environ. Microbiol. 74 (8), 2391–2397. Artin, I., Mason, D.R., Pin, C., Schelin, J., Peck, M.W., Holst, E., Carter, A.T., 2010. Effects of carbon dioxide on growth of proteolytic Clostridium botulinum, its ability to produce neurotoxin, and its transcriptome. Appl. Environ. Microbiol. 76 (4), 1168–1172. Arvanitoyannis, I.S., Bouletis, A.D., Papa, E.A., Gkagtzis, D.C., Hadjichristodoulou, C., Papaloucas, C., 2011. Anaerobe The effect of addition of olive oil and “Aceto balsamico di Modena” wine vinegar in conjunction with active atmosphere packaging on the microbial and sensory quality of “Lollo Verde” lettuce and rocket salad. Anaerobe 17 (6), 303–306. Arvanitoyannis, I.S., Stratakos, A.C., 2012. Application of modified atmosphere packaging and active/smart technologies to red meat and poultry: a review. Food Bioproc. Tech. 5 (5), 1423–1446. Ayhan, Z., Eştürk, O., 2009. Overall quality and shelf life of minimally processed and modified atmosphere packaged “ready-to-eat” pomegranate arils. J. Food Sci. 74 (5), 399–405. Bai, J., Saftner, R.A., Watada, A.E., 2003. Characteristics of fresh-cut honeydew (Cucumis xmelo L.) available to processors in winter and summer and its quality maintenance by modified atmosphere packaging. Postharvest Biol. Technol. 28, 349–359. Beaudry, R.M., Cameron, A.C., Shirazi, A., Dostal-Lange, D.L., 1992. Modified-atmosphere packaging of blueberry fruit: effect of temperature on package O2 and CO2. J. Am. Soc. Hortic Sci. 117 (3), 436–441. Belay, Z.A., Caleb, O.J., Mahajan, P.V., Opara, U.L., 2018. Design of active modified atmosphere and humidity packaging (MAHP) for ‘wonderful’ pomegranate arils. Food Bioproc. Tech. 1–17. Ben-Yehoshua, S., Rodov, V., Peretz, J., 1998. Constitutive and induced resistance of citrus fruit against pathogens. In: Disease Resistance in Fruit: Proceedings of an International Workshop held at Chiang Mai, Thailand. Australian Centre for International Agriculture Research, Canberra. 18–21 May 1997. 1998. Boonruang, K., Chonhenchob, V., Singh, S.P., Chinsirikul, W., Fuongfuchat, A., 2012. Comparison of various packaging films for mango export. Pack. Technol. Sci. 25 (2), 107–118. Bovi, G.G., Caleb, O.J., Ilte, K., Rauh, C., Mahajan, P.V., 2018. Impact of modified atmosphere and humidity packaging on the quality, off-odour development and volatiles of ‘Elsanta’ strawberries. Food Pack. Shelf Life 16, 204–210. Bovi, G.G., Caleb, O.J., Linke, M., Rauh, C., Mahajan, P.V., 2016. Transpiration and moisture evolution in packaged fresh horticultural produce and the role of integrated mathematical models: a review. Biosyst. Eng. 150, 24–39. Bourke, P., O'beirne, D., 2004. Effects of packaging type, gas atmosphere and storage temperature on survival and growth of Listeria spp. in shredded dry coleslaw and its components. Int. J. Food Sci. Technol. 39 (5), 509–523. Brecht, J., 1995. Physiology of lightly processed fruits and vegetables. HortScience 30 (1), 18–22. Brody, A.L., Strupinsky, E.P., Kline, L.R., 2001. Active Packaging for Food Applications. CRC press.

Modified atmosphere packaging for food preservation255

Caleb, O.J., Opara, U.L., Witthuhn, C.R., 2012. Modified atmosphere packaging of pomegranate fruit and arils: a review. Food Bioproc. Tech. 5 (1), 15–30. Caleb, O.J., Mahajan, P.V., Al-Said, F.A.J., Opara, U.L., 2013. Modified atmosphere packaging technology of fresh and fresh-cut produce and the microbial consequences—a review. Food Bioproc. Tech. 6 (2), 303–329. Caleb, O.J., Ilte, K., Fröhling, A., Geyer, M., Mahajan, P.V., 2016. Integrated modified atmosphere and humidity package design for minimally processed Broccoli (Brassica oleracea L. var. italica). Postharvest Biol. Technol. 121, 87–100. Charles, F., Sanchez, J., Gontard, N., 2003. Active modified atmosphere packaging of fresh fruits and vegetables: modeling with tomatoes and oxygen absorber. J. Food Sci. 68 (5), 1736–1742. Chen, Q., Hui, Z., Zhao, J., Ouyang, Q., 2014. Evaluation of chicken freshness using a low-cost colorimetric sensor array with AdaBoost–OLDA classification algorithm. LWT-Food Sci. Technol. 57 (2), 502–507. Chonhenchob, V., Chantarasomboon, Y., Singh, S.P., 2007. Quality changes of treated fresh-cut tropical fruits in rigid MAP containers. Packag. Technol. Sci. 20 (1), 27–37. Cliff, M.A., Toivonen, P.M., Forney, C.F., Lu, C., 2010. Quality of fresh-cut apple slices stored in solid and micro-perforated film packages having contrasting O2 headspace atmospheres. Postharvest Biol. Technol. 58 (3), 254–261. Costa, C., Lucera, A., Conte, A., Mastromatteo, M., Speranza, B., Antonacci, A., Del Nobile, M.A., 2011. Effects of passive and active modified atmosphere packaging conditions on ready-to-eat table grape. J. Food Eng. 102 (2), 115–121. Del-Valle, V., Hernández-Muñoz, P., Catalá, R., Gavara, R., 2009. Optimization of an equilibrium modified atmosphere packaging (EMAP) for minimally processed mandarin segments. J. Food Eng. 91 (3), 474–481. DeWitt, C., Oliveira, A., 2016. Modified atmosphere systems and shelf life extension of fish and fishery products. Foods 5 (3), 48. Escalona, V.H., Aguayo, E., Artés, F., 2007. Quality Changes of fresh-cut kohlrabi sticks under modified atmosphere packaging. J. Food Sci. 72 (5), S303–S307. Fang, Z., Zhao, Y., Warner, R.D., Johnson, S.K., 2017. Active and intelligent packaging in meat industry. Trends Food Sci. Technol. 61, 60–71. Farber, J.N., Harris, L.J., Parish, M.E., Beuchat, L.R., Suslow, T.V., Gorney, J.R., Busta, F.F., 2003. Microbiological safety of controlled and modified atmosphere packaging of fresh and fresh-cut produce. Compr. Rev. Food Sci. Food Saf. 2, 142–160. Fernández-león, M.F., Fernández-león, A.M., Lozano, M., Ayuso, M.C., Amodio, M.L., Colelli, G., 2013. Retention of quality and functional values of broccoli ‘Parthenon’ stored in modi fi ed atmosphere packaging. Food Control 31 (2), 302–313. Fernández, K., Aspe, E., Roeckel, M., 2009. Shelf-life extension on fillets of Atlantic Salmon (Salmo salar) using natural additives, superchilling and modified atmosphere packaging. Food Control 20 (11), 1036–1042. Fernández, K., Aspé, E., Roeckel, M., 2010. Scaling up parameters for shelf-life extension of Atlantic Salmon (Salmo salar) fillets using superchilling and modified atmosphere packaging. Food Control 21 (6), 857–862. Fonseca, S.C., Oliveira, F.A., Brecht, J.K., 2002. Modelling respiration rate of fresh fruits and vegetables for modified atmosphere packages: a review. J. Food Eng. 52 (2), 99–119. Fonseca, S.C., Oliveira, F.A., Brecht, J.K., Chau, K.V., 2005. Influence of low oxygen and high carbon dioxide on shredded Galega kale quality for development of modified atmosphere packages. Postharvest Biol. Technol. 35 (3), 279–292.

256

Food Quality and Shelf Life

Francis, G.A., O'Beirne, D., 1998. Effects of the indigenous microflora of minimally processed lettuce on the survival and growth of Listeria innocua. Int. J. Food Sci. Technol. 33 (5), 477–488. Ghidelli, C., Pérez-gago, M.B., Ghidelli, C., 2018. Recent advances in modified atmosphere packaging and edible coatings to maintain quality of fresh-cut fruits and vegetables quality of fresh-cut fruits and vegetables. Crit. Rev. Food Sci. Nutr. 58 (4), 662–679. González-Buesa, J., Page, N., Kaminski, C., Ryser, E.T., Beaudry, R., Almenar, E., 2014. Effect of non-conventional atmospheres and bio-based packaging on the quality and safety of Listeria monocytogenes-inoculated fresh-cut celery (Apium graveolens L.) during storage. Postharvest Biol. Technol. 93, 29–37. Goulas, A.E., Chouliara, I., Nessi, E., Kontominas, M.G., Savvaidis, I.N., 2005. Microbiological, biochemical and sensory assessment of mussels (Mytilus galloprovincialis) stored under modified atmosphere packaging. J. Appl. Microbiol. 98 (3), 752–760. Hong, S.-I., Park, W.-S., 2000. Use of colour indicators as an active packaging system for evaluating kimchi fermentation. J. Food Eng. 46 (1), 67–72. Horev, B., Sela, S., Vinokur, Y., Gorbatsevich, E., Pinto, R., Rodov, V., 2012. The effects of active and passive modified atmosphere packaging on the survival of Salmonella enterica serotype Typhimurium on washed romaine lettuce leaves. Food Res. Int. 45 (2), 1129–1132. Hussein, Z., Caleb, O.J., Linus, U., 2015. Perforation-mediated modified atmosphere packaging of fresh and minimally processed produce—a review. Food Pack. Shelf Life 6, 7–20. Iqbal, T., Rodrigues, F.A.S., Mahajan, P.V., Kerry, J.P., 2009. Mathematical modelling of the influence of temperature and gas composition on the respiration rate of shredded carrots. J. Food Eng. 91, 325–332. Jacxsens, L., Devlieghere, F., De Rudder, T., Debevere, J., 2000. Designing equilibrium modified atmosphere packages for fresh-cut vegetables subjected to changes in temperature. LWT-Food Sci. Technol. 33 (3), 178–187. Jacxsens, L., Devlieghere, F., Van der Steen, C., Debevere, J., 2001. Effect of high oxygen modified atmosphere packaging on microbial growth and sensorial qualities of fresh-cut produce. Int. J. Food Microbiol. 71 (2–3), 197–210. Jayas, D.S., Jeyamkondan, S., 2002. PH—postharvest technology: modified atmosphere storage of grains meats fruits and vegetables. Biosyst. Eng. 82 (3), 235–251. Jiang, T., Zheng, X., Li, J., Jing, G., Cai, L., Ying, T., 2011. Integrated application of nitric oxide and modified atmosphere packaging to improve quality retention of button mushroom (Agaricus bisporus). Food Chem. 126 (4), 1693–1699. Kader, A.A., Ben-Yehoshua, S., 2000. Effects of super atmospheric oxygen levels on postharvest physiology and quality of fresh fruits and vegetables. Postharvest Biol. Technol. 20 (1), 1–13. Kader, A.A., Watkins, C.B., 2000. Modified atmosphere packaging—toward 2000 and beyond. HortTechnology 10 (3), 483–486. Kalač, P., 2009. Chemical composition and nutritional value of European species of wild growing mushrooms: a review. Food Chem. 113 (1), 9–16. Kartal, S., Aday, M.S., Caner, C., 2012. Postharvest biology and technology use of microperforated films and oxygen scavengers to maintain storage stability of fresh strawberries. Postharvest Biol. Technol. 71, 32–40. Kerry, J.P., O’grady, M.N., Hogan, S.A., 2006. Past, current and potential utilisation of active and intelligent packaging systems for meat and muscle-based products: a review. Meat Sci. 74 (1), 113–130. Kim, K.M., Ko, J.A., Lee, J.S., Park, H.J., Hanna, M.A., 2006. Effect of modified atmosphere packaging on the shelf-life of coated, whole and sliced mushrooms. LWT-Food Sci. Technol. 39 (4), 365–372.

Modified atmosphere packaging for food preservation257

Koseki, S., Itoh, K., 2002. Effect of nitrogen gas packaging on the quality and microbial growth of fresh-cut vegetables under low temperatures. J. Food Prot. 65 (2), 326–332. Krasnova, I., Dukalska, L., Seglina, D., Juhnevica, K., Sne, E., Karklina, D., 2012. Effect of passive modified atmosphere in different packaging materials on fresh-cut mixed fruit salad quality during storage. World Acad. Sci. Eng. Technol. 67, 1095–1104. Kuswandi, B., Maryska, C., Abdullah, A., Heng, L.Y., 2013. Real time on-package freshness indicator for guavas packaging. J. Food Meas. Characterization 7 (1), 29–39. La Zazzera, M., Rinaldi, R., Amodio, M.L., Colelli, G., 2010. Influence of high CO2 atmosphere composition on fresh-cut artichoke quality attributes. Acta Hortic. 934, 633–640. Lee, J., Rudell, D.R., Watkins, C.B., 2014. Metabolic changes in 1-methylcyclopropene (1-MCP)treated ‘Empire’ apple at different storage temperatures. Acta Hortic. 1048, 113–120. Li, Y., Ishikawa, Y., Satake, T., Kitazawa, H., Qiu, X., Rungchang, S., 2014. Effect of active modified atmosphere packaging with different initial gas compositions on nutritional compounds of shiitake mushrooms (Lentinus edodes). Postharvest Biol. Technol. 92, 107–113. Lin, Q., Lu, Y., Zhang, J., Liu, W., Guan, W., Wang, Z., 2017. Effects of high CO2 in-package treatment on flavor, quality and antioxidant activity of button mushroom (Agaricus bisporus) during postharvest storage. Postharvest Biol. Technol. 123, 112–118. Linke, M., Geyer, M., 2013. Condensation dynamics in plastic film packaging of fruit and vegetables. J. Food Eng. 116 (1), 144–154. Łopacka, J., Półtorak, A., Wierzbicka, A., 2017. Effect of reduction of oxygen concentration in modified atmosphere packaging on bovine M. longissimus lumborum and M. gluteus medius quality traits. Meat Sci. 124, 1–8. Lownds, N.K., Banaras, M., Bosland, P.W., 1994. Postharvest water loss and storage quality of nine pepper (Capsicum) cultivars. HortScience 29 (3), 191–193. Ma, L., Zhang, M., Bhandari, B., Gao, Z., 2017. Recent developments in novel shelf life extension technologies of fresh-cut fruits and vegetables. Trends Food Sci. Technol. 64, 23–38. Mahajan, P.V., Oliveira, F.A.R., Macedo, I., 2008. Effect of temperature and humidity on the transpiration rate of the whole mushrooms. J. Food Eng. 84 (2), 281–288. Mahajan, P.V., Caleb, O.J., Singh, Z., Watkins, C.B., Geyer, M., 2014. Postharvest treatments of fresh produce. Philos. Trans. R. Soc. A 372 (2017), 20130309. McMillin, K.W., 2008. Where is MAP going? A review and future potential of modified atmosphere packaging for meat. Meat Sci. 80 (1), 43–65. Munro, I.C., Haighton, L.A., Lynch, B.S., Tafazoli, S., 2009. Technological challenges of addressing new and more complex migrating products from novel food packaging materials. Food Addit. Contam. 26 (12), 1534–1546. Neethirajan, S., Jaya, D.S., Sadistap, S., 2009. Carbon dioxide sensors for the agric-food industry—a review. Food Bioproc. Tech. 2, 115–121. Oliveira, F., Sousa-Gallagher, M.J., Mahajan, P.V., Teixeira, J.A., 2012. Development of shelflife kinetic model for modified atmosphere packaging of fresh sliced mushrooms. J. Food Eng. 111 (2), 466–473. Oms-Oliu, G., Soliva-Fortuny, R., Martín-Belloso, O., 2008. Edible coatings with antibrowning agents to maintain sensory quality and antioxidant properties of fresh-cut pears. Postharvest Biol. Technol. 50 (1), 87–94. Opara, U.L., 2009. Quality management: an industrial approach to produce handling. Chapter 8 In: Florkowski, W.J., Shewfelt, R.L., Brueckner, B., Prussia, S.E. (Eds.), Postharvest Handling: A Systems Approach. second ed.. Elsevier, pp. 154–204. Opara, L.U., Al-Jufaili, S.M., Rahman, M.S., 2007. Postharvest handling and preservation of fresh fish and seafoods. Chapter 6 In: Rahman, M.S. (Ed.), Handbook of Food Preservation. second ed.. CRC Press, Boca Raton, FL, pp. 151–172.

258

Food Quality and Shelf Life

Ozdemir, M., Floros, J.D., 2004. Active food packaging technologies. Crit. Rev. Food Sci. Nutr. 44 (3), 185–193. Özogul, F., Taylor, K.D.A., Quantick, P., Özogul, Y., 2002. Biogenic amines formation in Atlantic herring (Clupea harengus) stored under modified atmosphere packaging using a rapid HPLC method. Int. J. Food Sci. Technol. 37 (5), 515–522. Poyatos-Racionero, E., Ros-Lis, J.V., Vivancos, J.L., Martinez-Manez, R., 2018. Recent advances on intelligent packaging as tools to reduce food waste. J. Clean. Prod. 172, 3398–3409. Rathore, H., Prasad, S., Sharma, S., 2017. PharmaNutrition mushroom nutraceuticals for improved nutrition and better human health: a review. Biochem. Pharmacol. 5 (2), 35–46. Rico, D., Martin-Diana, A.B., Barat, J.M., Barry-Ryan, C., 2007. Extending and measuring the quality of fresh-cut fruit and vegetables: a review. Trends Food Sci. Technol. 18 (7), 373–386. Rux, G., Mahajan, P.V., Geyer, M., Linke, M., Pant, A., Saengerlaub, S., Caleb, O.J., 2015. Postharvest biology and technology application of humidity-regulating tray for packaging of mushrooms. Postharvest Biol. Technol. 108, 102–110. Salinas, Y., Ros-Lis, J.V., Vivancos, J.L., Martínez-Máñez, R., Marcos, M.D., Aucejo, S., Lorente, I., 2012. Monitoring of chicken meat freshness by means of a colorimetric sensor array. Analyst 137 (16), 3635–3643. Sandhya, 2010. Modified atmosphere packaging of fresh produce: current status and future needs. Food Sci. Technol. 43, 381–392. Sanz, C., Perez, A.G., Olias, R., Olias, J.M., 1999. Quality of strawberries packed with perforated polypropylene. J. Food Sci. 64 (4), 748–752. Sanz, C., Perez, A.G., Olias, R., Olias, J.M., 2000. Modified atmosphere packaging of strawberry fruit: effect of package perforation on oxygen and carbon dioxide/Envasado de fresas en atmósfera modificada: efecto de la perforación del envase en el contenido de oxígeno y dióxido de carbono. Food Sci. Technol. Int. 6 (1), 33–38. Scifò, G.O., Randazzo, C.L., Restuccia, C., Fava, G., Caggia, C., 2009. Listeria innocua growth in fresh cut mixed leafy salads packaged in modified atmosphere. Food Control 20 (7), 611–617. Serrano, M., Martinez-Romero, D., Guillen, F., Castillo, S., Valero, D., 2006. Maintenance of broccoli quality and functional properties during cold storage as affected by modified atmosphere packaging. Postharvest Biol. Technol. 39 (1), 61–68. Sivertsvik, M., Jeksrud, W.K., Rosnes, J.T., 2002. A review of modified atmosphere packaging of fish and fishery products–significance of microbial growth, activities and safety. Int. J. Food Sci. Technol. 37 (2), 107–127. Sivertsvik, M., 2007. The optimized modified atmosphere for packaging of pre-rigor filleted farmed cod (Gadus morhua) is 63 ml/100 ml oxygen and 37 ml/100 ml carbon dioxide. LWT-Food Sci. Technol. 40 (3), 430–438. Smiddy, M., Papkovskaia, N., Papkovsky, D.B., Kerry, J.D., 2002. Use of oxygen sensors for the non-destructive measurement of the oxygen content in modified atmosphere and vacuum packs of cooked chicken patties; impact of oxygen content on lipid oxidation. Food Res. Int. 35, 577–584. Song, Y., Lee, D.S., Yam, K.L., 2001. Predicting relative humidity in modified atmosphere packaging system containing blueberry and moisture absorbent. J. Food Process. Preserv. 25 (1), 49–70. Suppakul, P., Miltz, J., Sonneveld, K., Bigger, S.W., 2003. Active packaging technologies with an emphasis on antimicrobial packaging and its applications. J. Food Sci. 68 (2), 408–420. Tano, K., Oulé, M.K., Doyon, G., Lencki, R.W., Arul, J., 2007. Comparative evaluation of the effect of storage temperature fluctuation on modified atmosphere packages of selected fruit and vegetables. Postharvest Biol. Technol. 46 (3), 212–221.

Modified atmosphere packaging for food preservation259

Tao, F., Zhang, M., Hangqing, Y., Jincai, S., 2006. Effects of different storage conditions on chemical and physical properties of white mushrooms after vacuum cooling. J. Food Eng. 77 (3), 545–549. Tomás-callejas, A., Boluda, M., Robles, P.A., Artés, F., Artés-hernández, F., 2011. LWT—food science and technology innovative active modified atmosphere packaging improves overall quality of fresh-cut red chard baby leaves. LWT- Food Sci. Technol. 44 (6), 1422–1428. Torrieri, E., Antimo, P., Cavella, S., Fogliano, V., Attianese, I., Giuliana, G., Masi, P., 2011. Effect of modified atmosphere and active packaging on the shelf-life of fresh bluefin tuna fillets. J. Food Eng. 105 (3), 429–435. Tudela, J.A., Marín, A., Garrido, Y., Cantwell, M., Medina-martínez, M.S., Gil, M.I., 2013. Postharvest biology and technology off-odour development in modified atmosphere packaged baby spinach is an unresolved problem. Postharvest Biol. Technol. 75, 75–85. Urmila, K., Li, H., Chen, Q., Hui, Z., Zhao, J., 2015. Quantifying of total volatile basic nitrogen (TVB-N) content in chicken using a colorimetric sensor array and nonlinear regression tool. Anal. Methods 7 (13), 5682–5688. Villaescusa, R., Gil, M.I., 2003. Quality improvement of Pleurotus mushrooms by modified atmosphere packaging and moisture absorbers. Postharvest Biol. Technol. 28 (1), 169–179. Volpe, S., Mahajan, P.V., Rux, G., Gavella, S., Torrieri, E., 2018. Condensation and moisture regulation in packaged fresh-cut iceberg lettuce. J. Food Eng. 2016, 132–137. Weerakkody, P., Jobling, J., Infante, M.M.V., Rogers, G., 2010. The effect of maturity, sunburn and the application of sunscreens on the internal and external qualities of pomegranate fruit grown in Australia. Sci. Hortic. 124 (1), 57–61. Yahia, E.M., 2006. Modified and controlled atmospheres for tropical fruits. Stewart Postharvest Rev. 5 (6), 1–10. Yam, K.L., Takhistov, P.T., Miltz, J., 2005. Intelligent packaging: concepts and applications. J. Food Sci. 70 (1), R1–R10. Ye, J.J., Li, J.R., Han, X.X., Zhang, L., Jiang, T.J., Miao, X.I.A., 2012. Effects of active modified atmosphere packaging on postharvest quality of shiitake mushrooms (Lentinula edodes) stored at cold storage. J. Integr. Agric. 11 (3), 474–482. Zhang, M., Meng, X., Bhandari, B., Fang, Z., 2015a. Recent application of modified atmosphere packaging (MAP) in fresh and fresh-cut foods. Food Rev. Int. 31 (2), 172–193. Zhang, B., Ma, L., Deng, S., Xie, C., Qiu, X., 2015b. Shelf-life of pacific white shrimp (Litopenaeus vannamei) as affected by weakly acidic electrolyzed water ice-glazing and modified atmosphere packaging. Food Control 51, 114–121.

Further reading Soccol, M.C.H., Oetterer, M., 2003. Use of modified atmosphere in seafood preservation. Braz. Arch. Biol. Technol. 46 (4), 569–580. Soliva-Fortuny, R.C., Martı́n-Belloso, O., 2003. New advances in extending the shelf-life of fresh-cut fruits: a review. Trends Food Sci. Technol. 14 (9), 341–353.