CO in Fresh Meat Packaging | Encyclopedia MDPI

CO in Fresh Meat Packaging: History

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Modified atmosphere packaging (MAP) of foods has been a promising area of research, but much remains to be known regarding the use of unconventional gases such carbon monoxide (CO). The use of CO for meat and seafood packaging is not allowed in most countries due to the potential toxic effect, and its use is controversial in some countries. The commercial application of CO in food packaging was not then considered feasible because of possible environmental hazards for workers. CO has previously been reported to mask muscle foods’ spoilage, and this was the primary concern raised for the prohibition, as this may mislead consumers.

muscle foods
modified atmosphere packaging
CO
shelf-life
best practice
regulation

1. Introduction

Oxidative browning is the primary basis for consumer rejection of fresh beef in retail display. The meat industry has made a great effort to develop techniques that can improve color stability. Consumers prefer that raw meat of good quality is bright red, which is an indicator of freshness [1].

Traditionally in developed countries, fresh meat is wrapped in O₂-permeable film allowing the meat to turn bright red. This bright red color is retained under these conditions for about a few days (~3 days). The shelf-life of perishable fresh meat is limited in the presence of normal air. Chilled storage will significantly reduce the rate at which detrimental changes occur in the food, but will not extend the shelf-life sufficiently for retail distribution and display purposes.

Over the past decade, the use of case-ready modified atmosphere packaging (MAP) has increased by the meat industry in various countries. Carbon dioxide (CO₂), nitrogen (N₂) and oxygen (O₂) are the gases most commonly used in MAP fresh meats. Indeed, the majority of red meat products are packaged in a high O₂ environment (~80% O₂) to reduce myoglobin (Mb) oxidation and provide a stable, attractive, “bloomed” red meat color, in a proportion of at least 20% CO₂ to prevent the growth of Gram-negative bacteria responsible for aerobic spoilage such as Pseudomonas spp. However, high O₂-MAP (HiO₂-MAP) can increase lipid and protein oxidation, with negative effects on meat flavor [2,3] and texture, which reduces the tenderness and juiciness of the meat [4,5]. Another concern of HiO₂ packaging is the possible development of premature browning (PB); the phenomenon develops when meat is cooked, resulting in meat that appears done before it has reached a temperature that renders it microbiologically safe [6,7,8,9], thus causing the risk of consumption of undercooked meat with pathogenic bacteria.

To extend red color stability and avoid the drawbacks of aerobic packaging, an anaerobic MAP technology with 0.4% CO (CO-MAP) was approved [10] for use with fresh meats in the USA [11]. Previous studies have proven that CO can significantly increase the color stability of beef compared with other packaging methods. The possible reason that CO-MAP could enhance red color stability was related to the higher stability of carboxymyoglobin (COMb) than oxymyoglobin (O₂Mb) [12,13], owing to the stronger binding of CO to the iron-porphyrin site on the Mb molecule [14]. The main advantages of CO include the maintenance of the desirable attributes mentioned above in relation to color stability, growth reduction of spoilage organisms and prevention of oxidative processes [11]. However, due to the potential toxic effect of CO, its use is controversial in some countries.

Vacuum packaging (VP) is another common method used to distribute meats and in supermarkets for their retail/display. Storage of beef in gas-impermeable packages confers to product a purple color owing to the formation of deoxymyoglobin (DeoxMb). The anaerobic environment delays aerobic microbial growth such as Pseudomonas spp. and psychrotrophic aerobic bacteria and improves microbial shelf-life. However, consumers prefer the appearance of bright red beef compared to the darker vacuum-packaged beef products [15]. It is possible that a pre-treatment with CO will make it possible to overcome the unattractive color in the vacuum-packed meat pieces. This will maintain an attractive red color throughout the exposure and sales period, allowing for a more tender meat due to optimum ripening during this period.

Since 1985, Norwegian meat industries have used 0.4% CO in MAP of muscle foods (fresh beef, pork and lamb) with 60–70% CO₂ and the balance as N₂. About 60% of the fresh meat in Norway has been sold using this gas composition [16]. The use of CO for MAP of meat has been prohibited in Norway since 1 July 2004, due to the implementation of European Union (EU) food regulations.

The scope and purpose of this paper and the controversy about the use of CO in meat packaging were discussed. The use of CO in fresh meat packaging gives promising results due to its positive effects on overall meat quality, enhancement red color, reduced lipid oxidation and microorganism growth inhibitions, which result in shelf-life prolongation during wider distribution of case-ready products. However, in realistic concentrations, CO as such has no antimicrobial effect, and CO₂ in sufficient concentrations is required for delaying the growth of Gram-negative bacteria.

The use of CO in the food industry is controversial. Some countries approve the application such as the U.S., Canada, Australia and New Zealand, while the EU member states ban it from food processing. CO has previously been reported to mask meat spoilage, and this was the primary concern raised for the prohibition as this may mislead consumers. Another consideration is that the application of CO in meat packaging was not considered feasible because of possible environmental hazards for workers.

Risk of CO toxicity from the packaging process or from consumption of CO-treated meats is negligible. Moreover, the addition of CO pre-treatments prior to VP may be beneficial to allow a desirable color to be induced while allowing aging to occur within the package and increasing meat tenderness. Additionally, CO is not present in the pack during storage. Several authors do not consider CO only as a toxic gas for our organism. It was quickly discovered that CO is produced endogenously as a cellular protectant by nearly every cell in our bodies when they are subjected to situations of oxidative stress or injury. Although there is increasing interest in the use of CO-MAP for fresh beef, the debates during the last few years concerning the use of CO in meat packaging have not seriously taken into account the preferences of consumers [17]. However, several studies on the attitude of European consumers regarding the use of CO for meat packaging have reported positive relationships that suggest its future potential within the EU. Facilitation of information can help to develop future policies to ensure consumer protection, and therefore, the debate over the use of CO as a protective gas in meat packaging within the EU could be re-considered.

2. Fresh Meat Packaging Methods

2.1. Raw Meat Spoilage-Associated Storage Conditions

Fresh meat suffers during refrigerated storage some modifications, which can be either physical (water loss) or chemical (color and odor modification) or microbiological. The shelf-life of fresh meat is not unlimited. As is known, its alteration is due to a greater or lesser extent to the presence of atmospheric O₂, as a consequence of a series of well-known mechanisms: 1. the oxidizing chemical effect of the atmospheric O₂; 2. the growth of aerobic spoilage microorganisms; 3. photo-oxidation. All of these factors, either alone or in combination, can result in detrimental changes in the color, odor, texture and flavor of meat. Maintaining meat’s quality attributes throughout its shelf-life has been a perennial challenge for the meat industry. In this context, the best packaging methods in combination with low temperatures have been considered an important technology with respect to maintaining quality standards with optimal distribution and extending shelf-life for the retailers.

2.2. Fresh Meat Shelf-Life

Maintaining quality attributes throughout its shelf-life has been a perennial challenge for the meat industry and government agencies (Figure 1). Shelf-life is a frequently-used term that can be understood and interpreted differently. In 1974, the U.S. Institute of Food Technologists defined shelf-life as “the period between the manufacture and the retail purchase of a food product, during which the product is in a state of satisfactory quality in terms of nutritional value, taste, texture and appearance”. According to The Institute of Food Science and Technology in the United Kingdom, shelf-life is “the period during which the food product will remain safe; be certain to retain desired sensory, chemical, physical, microbiological and functional characteristics; and comply with any label declaration of nutritional data when stored under the recommended conditions”.

Figure 1. Factors influencing shelf-life of fresh meat.

In the EU, shelf-life is not defined in law, nor is there legislation about how shelf-life should be determined. According to EU regulations (Directive 2001/95/EC of the European Parliament and of the Council on General Product Safety), the manufacturer is responsible for putting safe products on the market. More recently, fresh beef shelf-life was determined based on sensory analysis, chemical, physical and microbiological properties. Shelf-life was therefore defined as “the period between slaughter of animal and the simulated retail purchasing, during which the meat retains all its qualities attributes” [18]. However, in commercial practice, this definition overlooks the fact that the consumer may store the product at home for some time before consumption.

2.3. Packaging Options

The role of centralized packaging systems in the longer modern food supply chains is being increasingly recognized as it has multiple functions and is very important in terms of increasing product shelf-life by retarding food-quality degradation and ensuring food safety [40]. The four major packaging systems include vacuum packaging (VP), vacuum skin packaging (VSP), modified atmosphere packaging (MAP) and polyvinyl chloride over-wrap film (PVC). The four approaches differ in their preservative capabilities and their applicability to the centralized packaging of retail meat. Moreover, fresh meat commercialization strategies have notably changed during the last few decades. Therefore, maintaining quality and color appearance is fundamental during the distribution and marketing of meat. For this reason, packaging innovation has become indispensable to increase the shelf-life of this product.

3. CO in Fresh Meat Packaging

3.1. What Is Carbon Monoxide?

CO is a toxic gas. It is produced by the incomplete combustion of carbon-based materials (fossil fuels, industrial and biological processes, wood, etc.) [11,54]. CO is an odorless, colorless, tasteless gas, non-irritating and non-suffocating. Its density is very close to that of air (0.967). It diffuses very quickly in the ambient environment occupying all the space available, which is potentially dangerous in a closed environment. In the biological medium, it is easily bound by coordination to the divalent iron (Fe²⁺) or to the copper (Cu²⁺) of the hemoproteins. In addition to its production by the incomplete combustion of hydrocarbon materials, significant quantities are also produced during the operation of internal combustion engines due to incomplete combustion of the fuel. A small quantity of CO is naturally produced endogenously in humans [55], regulating blood flow and blood fluidity [56]. CO can be produced during irradiation of meat [57,58,59,60,61]. The production of CO in irradiated samples was irradiation-dose dependent [58,62]. The major sources of CO in irradiated meat are amino acids and phospholipids [63]. CO is also produced by reactions between meat components and free radicals produced by radiolysis [58,62,64].

3.2. Health Implications of CO

CO is called the “silent killer” because if the early signs are ignored, a person may lose consciousness and be unable to escape the danger. The first descriptions of CO and its toxic nature appeared in the literature over 100 years ago; recognized since 1895 by Haldane [65]. The ancient Greeks and Romans used CO to execute criminals. Application of CO for sedation and killing of animals has mainly been carried out in scientific studies, but has been practiced at an industrial level for killing of mink. Use of CO for sedation and killing may be important, especially in order to enhance both the animal welfare and the overall meat quality. Utilization of CO for euthanizing of animals may also be carried out by veterinarians at laboratory facilities [66]. In most countries, stunning prior to sacrificing of animals is required. The method to stunning should ensure that the animals reach an unconscious state fast, without any pain, and the animals should not recover consciousness before death. Meanwhile, Kosher and Halal practices of the slaughter of animals without stunning are in use.

The past twenty-seven years have been marked by an explosion in the number and quality of studies regarding the actions of CO in mammalian systems. The toxic action of CO is due to the blockage of the O₂-carrying function of hemoglobin (Hb) through the formation of COHb instead of oxyhemoglobin (O₂Hb) and prevents the body from using O₂. Thus, cells, tissues and vital organs may become hypoxic and undergo irreversible anatomical, biochemical and physiological changes, leading to death and morbidity. Thus, symptoms appear when COHb is >10% [67]. The fetus and infant are the most predisposed to harmful effects of CO compared to adults due to higher metabolism and the presence of fetal hemoglobin, which has a greater affinity for CO than adult hemoglobin [68]. On the other hand, the risk of developing autism in children is also linked to CO exposure [69]. The affinity of hemoglobin for CO is 240-times greater than that for O₂. A small amount of CO (~0.5%) is formed naturally in the human body from the breakdown of hemoproteins [56]. The average COHb level in nonsmokers is 1.2–1.5% (from both endogenous and environmental CO) and 3–4% in smokers [54]. Clinical results showed that children born to women smokers exhibited low intellectual development and poorer performance on cognitive tasks [70]. The half-life of COHb is 4–6 h in the mother, but much longer in the fetus (18–24 h), which accentuates the effects of hypoxia on cerebral functioning and explains the rates still being higher COHb in the fetus than in the mother. Today, we now know that CO has a number of different action sites. More knowledge about the physiological process involving CO is necessary especially after the discovery of the heme protein neuroglobin (Ngb) in the brain of vertebrates [71]. Neuroglobin is thought to act as a reservoir for O₂ and in that way prolongs the activity of the nervous system. CO reacts with the heme protein Ngb in the brain and might also take part in biological signaling. It is possible that CO has an important function in humans. CO may have a physiological influence on the mind’s functioning since CO acts as a biological signal in regulating the cyclic guanosine monophosphate (GMP) and most likely works as a neuronal messenger [72,73]. It was discovered that CO is produced endogenously as a cellular protectant by nearly every cell in our bodies when they are subjected to situations of oxidative stress or injury [74,75,76]. Recently, CO has emerged as a potential therapeutic agent for the treatment of various cardiovascular disorders [77,78,79]. CO is a necessary molecule for normal cell signaling and can play a therapeutic role in humans [80]. Kim et al. [81], Onyiah et al. [82], Soni et al. [79] and Steiger et al. [83] established that CO can be used as a potential pharmacological cytoprotective (anti-inflammatory protection) agent against several diseases.

3.3. CO Application in Meat Packaging

The use of CO for meat packaging is not allowed in most countries due to the potential toxic effect, and its use is controversial in some countries. Nevertheless, according to Sørheim et al. [16,54], the method of adding 0.4% CO to a commercial gas blend with 60% CO₂ and 39.6% N₂ for case-ready packaging systems of beef, pork and lamb was developed by the Norwegian meat industry, starting in 1985. The use of CO for meat was discontinued in July 2004 due to pressure from European trading partners [84]. In Norway, the low CO packaging process grew to 60% of the retail red meat market [85]. The commercial success and safety record of the Norwegian process was a factor in the renewed interest in fresh meat packaging using CO in the United States. CO has a long history of application within the meat industry for its color-stabilizing effect coupled with its antioxidant abilities. Most CO-modified atmospheres contain no O₂, which limits the oxidation and growth of aerobic microorganisms. CO binds to the sixth coordinate of the heme group centrally located within Mb and forms a bright cherry-red color (COMb). The affinity of DeoxMb for CO is 28–51 times greater than for O₂ [86]. MbCO is more stable than MbO₂, making it is less likely to oxidize to the brown pigment, MetMb, during display [87]. Important findings in extending the shelf-life of fresh meats by MAP alone and by other treatments since 2000 are summarized in Table 1.

Table 1. Important findings in evaluating CO-modified atmosphere packaging (MAP) on extending the shelf-life of fresh meats.

Publication	Results/Conclusions
Luño et al. [88]	The presence of CO and 50% CO₂ extends the shelf-life by inhibition of spoilage bacteria growth, delayed metmyoglobin (MetMb) formation; maintains red color and odor of fresh meat and slows down oxidative reactions. CO concentrations of 0.5–0.75% were able to extend shelf life of packaged fresh meat by 5–10 days at 1 °C.
Nissen et al. [89]	At 4 °C, the shelf-life of ground beef packed in MA, based on color stability and background flora development, was prolonged for the high CO₂ (60%)/low CO (0.4%) mixture compared to high O₂ packaging (70% O₂/30% CO₂), but at 10 °C (abuse temperature), the shelf-life was <8 days for both packaging methods. The growth of Y. enterocolitica and L. monocytogenes in ground beef stored in the high CO₂/low CO mixture was not increased as a result of prolonging the shelf-life. However, the growth of strains of Salmonella at 10 °C in this mixture does emphasize the importance of temperature control during storage.
Sørheim et al. [85]	By adopting the use of CO in combination with high CO₂ for meat packaging under MAP, retailers must adopt packaging systems indicating the deadlines for optimal use of the packaged product. However, as with other perishable foods in MAP, food products must be handled according to strict hygienic standards, and low storage temperatures must be maintained in a continuous chill chain.
Jayasingh et al. [90]	Ground beef packaged in 0.5% CO would maintain color stability for several weeks. The penetration of CO and depth of formation of COMb in the meat is dependent on the concentration of CO in the atmosphere, the time of CO exposure and the structure of the meat. For safety issue concerns, the workers were not exposed to dangerous levels of CO during MA packaging, which was verified by CO detectors.
Kusmider et al. [91]	The low levels of CO (<1%) incorporated into MAP will maintain a stable, cherry-red color along with extended shelf-life of irradiated ground beef during 28 days of storage, thus countering the potentially negative color effects of irradiation.
Krause et al. [92]	0.5% CO significantly improved color stability and sensory attributes for both injected and non-injected pork chops. The depth (bright red band: COMb) of CO penetration from the surface increases as exposure time increases. The depth of the COMb layer steadily increased from the surface to the interior of the chops during exposure to CO. 0.5% CO packages increased in penetration depth from 5 mm on Day 1 to about 10 mm at 14 days, 15 mm at 28 days and 25 mm at Day 36.
John et al. [93]	Raw ground beef packaged in 80% O₂ maintained desirable bright red color until 10 days, but began to darken by Day 14 and lost all red color by Day 21. However, ground beef stored in highO₂-MAP was very susceptible to premature browning (PB) during cooking. PB is a food safety concern, because the cooked product appears done at temperatures where food poisoning organisms may survive. Raw ground beef held in 0.4% CO remained bright red throughout the 21 days of storage. PB and rancidity associated with ground beef packaged in highO₂-MAP were prevented by packaging in 0.4% CO.
John et al. [94]	Premature browning and rancidity associated with beef packaged in highO₂-MAP were prevented by packaging in 0.4% CO, 30.3% CO₂ and 69.3% N₂.
Mancini et al. [13]	Packaging atmospheres containing high levels of O₂ promote beef bone marrow discoloration. Exclusion of O₂ from MA packages and the addition of low concentrations of CO (0.4%) minimized this discoloration by limiting hemoglobin oxidation through packaging atmosphere and will promote a bright red lumbar vertebrae color for as long as 6 weeks after packaging.
Martínez et al. [95]	The retention of color and odor of fresh pork sausages packaged in MA was better achieved using atmospheres containing low CO₂ concentrations (20%). However, increasing concentrations of CO₂ (60%) promoted Mb and lipid oxidation, despite the better antimicrobial effects promoted by the high level of CO₂. The atmosphere containing 0.3% CO together with 30% CO₂ maintained the red color for 20 days, but failed to keep the fresh odor longer than 16 days, in agreement with its small effect on Thiobarbituric Acid Reactive Substances (TBARS) formation and microbial growth.
Wilkinson et al. [84]	Use of CO in MAP provides sufficient shelf-life extension of at least 8 weeks of refrigerated retail-ready pork chops in a master-packaging system. The inclusion of CO in the master-packs has not inhibited the growth of pathogenic organisms. However, given the stable fresh color of CO-treated meat and the lack of inhibition of pathogen growth by CO, there is concern that CO-MAP under certain conditions may pose a food safety risk. As such, safe refrigeration and handling must be emphasized with this type of product.
Wicklund et al. [96]	Chops packaged in CO-MAP were redder and darker than chops packaged in HiO₂-MAP. Based on sensory attributes, the CO-MAP pork was pinker than the HiO₂ pork after cooking to an internal temperature of 70 °C. CO-MAP chops also experienced less purge loss than pork in HiO₂-MAP, which may have contributed to the increased juiciness perceived by the panelists.
Sørheim et al. [97]	CO can be used as an alternative colorant to nitrite in meat products. A gas mixture containing 1% CO was sufficient for achieving a red/pink color of cooked or fermented meat products. Sausages with CO discolored faster during air and light display than nitrite controls. However, discoloration of CO sausages was reduced by anaerobic storage in darkness, showing that absence of O₂ is a necessity for optimum color formation and stability of these sausages.
De Santos et al. [86]	Enhanced pork chops were packaged in 0.36% CO and stored at 4 °C for 0, 12, 19 or 26 days, displayed for 2 days, then cooked to six endpoint temperatures (54, 60, 63, 71, 77 and 82 °C). As storage time increased, Pork chops packaged in CO-MAP retained their internal pink color even after cooking to 82 °C.
Stetzer et al. [98]	Steaks were packaged in 0.4% CO/30% CO₂/69.6% N₂ or 80% O₂/20% CO₂, stored in the dark for 12 and 26 days and placed in a lighted retail display case. Steaks were visually evaluated by trained panelists. Steaks were cooked for consumer color evaluation. CO had no effect on flavor or acceptability and minimal effects on other characteristics, such as color, sheen and purge loss. If the CO environment provides microbiological stability through storage, it can be expected that the raw product appearance will not differ from steaks in traditional HiO₂-MAP.
Aspé et al. [99]	Beef chops (longissimus dorsi) were pre-treated with 5% CO/24 h, vacuum packed and stored at 2 °C. Chops pre-treated with CO were redder during all of the storage period than controls without CO, and microbial shelf-life was 11 weeks. The pre-treatment did not affect pH, water-holding capacity, drip loss or rancidity of the meat stored in vacuum.
Mantilla et al. [100]	Color stability of tilapia fillets (Oreochromis niloticus) was significantly improved by pre-mortem CO treatment (CO-euthanized tilapia). The color of CO-treated fillets was also retained during frozen storage compared to untreated fillets. Hence, pre-mortem CO treatment could be used as a valuable method for improving the color of tilapia during storage.
Linares et al. [101,102]	The effect of the type of stunning (electrically vs. gas), MA and their interactions on meat quality of suckling lamb of the Spanish Manchego breed was determined at 7, 14 and 21 days of storage. Stunning by CO₂ gas prevented the negative effects that electrical systems have on meat quality in lamb apparent during storage. Furthermore, a low CO (30% CO₂/69.3% N₂/0.7% CO) level could give the best meat quality characteristics, even at 3 weeks of storage in the electrically-stunned group. In addition, in the gas-stunned group, it is possible to obtain a product of better color and more tenderness with a post-packing life of 7 days and possibly 15 days using CO in the gas mixture.
Grobbel et al. [103]	Steaks packaged in HiO₂ MAP discolored faster and to a greater extent than steaks packaged by vacuum package (VP) or ultra-low O₂ with CO (ULO₂CO) MAP. Non-enhanced muscles packaged by VP and ULO₂CO MAP had more stable display color and very desirable tenderness and flavor compared with those packaged in HiO₂ (80% O₂/20% CO₂).
Ramamoorthi et al. [104]	The combined irradiation with CO-MAP showed that, after 14 days of storage, aerobically-packaged beef was visually greener and less red than CO-MAP packaged beef. CO-MAP preserved color until 21 days of storage. CO-MAP could be also used to preserve color of beef irradiated at sufficient doses (~2 kGy) to reduce microbial loads to safe levels during 28 days of storage.
Mancini et al. [105]	Packaging steaks in CO (0.4% CO/30% CO₂/69.6% N₂) did not counteract the darkening effects of lactate enhancement. Nevertheless, CO improved color stability of beef steaks compared with high-oxygen packaging (80% O₂/20% CO₂).
Fontes et al. [106]	Fresh blood saturation with CO produces a dried blood of a pleasant pinkish-red color after 12 weeks of storage when packed in low O₂ transmission rates (OTR) bags, with great potential as an additive in meat product formulations.
Raines and Hunt [107]	Increased CO concentration in combination with reduced headspace volume has a greater influence on COMb development. Smaller headspaces with higher concentrations of CO (i.e., 0.8% vs. 0.4% CO) optimize the package size while maintaining or improving the appearance of beef packaged in CO-MAP without compromising consumer safety. This would result in greater efficiency of case-ready meat distribution, making the CO-MAP system more economically feasible and advantageous.
Jeong and Claus [108]	The color of CO-packaged ground beef upon opening the package deteriorated with display time and became less red. However, the initial rate of color deterioration was faster in vacuum-packaged ground beef when it was opened compared to CO-MAP-packaged product. When a CO-packaged product is opened, this color deterioration would provide consumers with a visual indicator of freshness.
Bjørlykke et al. [109]	CO could increase animal welfare when used to slaughter salmon or other fish. Exposure of fish to CO also could improve the quality of products.
Suman et al. [110]	The incorporation of chitosan increased the interior redness of ground beef patties stored in CO-MAP (0.4% CO + 19.6% CO₂ + 80% N₂). This incorporation was also minimizes premature browning (PB) in patties stored under CO-MAP systems instead of under high-O₂ MAP.
Ramamoorthi et al. [111]	Use of CO in MAP gasses has the potential to allow beef subjected to low doses of irradiation to retain its color.
Pivarnik et al. [112]	Filtered smoke (FS) presumably containing high % CO has been used to preserve taste, texture and/or color in tuna (Thunnus albacares). Therefore, a general statement indicating that FS treatments would extend shelf-life of tuna in the studied ways of storage: room temperature (21–22 °C), refrigerated (4–5 °C) and iced (0 °C).
Venturini et al. [113]	Packaging under 0.2% CO increased the color stability of beef steaks and ground beef for 28 days at 1 °C, even with residual O₂ concentrations that are considered excessive for anaerobic packaging systems (above 0.1%). After 28 days of storage under CO-MAP and 24 h of air exposure, beefsteaks and ground beef maintained an acceptable appearance and a visual color similar or superior to that of fresh meat. However, after 24 h of air exposure, both the appearance and the smell of steaks and ground beef were considered “slightly unpleasant”.
Lavieri and Williams [114]	The CO-MAP (0.4% CO) treatment had no effect on maintaining the COMb “cherry red” fresh meat color during meat spoilage. No potential health hazards or deceptions were revealed due to simultaneous onset of spoilage and the presence of COMb “cherry red” fresh meat pigment in the CO-MAP. The CO absorbed in the meat ranged from 0.22–0.46 ppm CO/g of meat on Day 0 and increased to 2.08–2.40 ppm CO/g of meat on Day 25. The maximum level of CO detected in the meat in this study was below the Environmental Protection Agency (EPA) National Ambient Air Quality Standard of 9 ppm.
Liu et al. [115]	The CO-MAP (0.4% CO/30% CO₂/69.6% N₂) significantly increased red color stability of all muscles. Steaks in CO-MAP maintained a higher MetMb reducing activity (MRA) compared with those in HiO₂-MAP during storage. After opening packages, the red color of steaks in CO-MAP deteriorated more slowly compared with that of steaks in HiO₂-MAP.
Concollato et al. [116]	CO-treated fish resulted in an earlier onset of rigor mortis, lower final post-mortem muscle pH and higher drip loss after filleting. The assimilation of CO by Atlantic salmon’s muscles, through injection in the water, slightly increased lightness (L) and yellowness (b) values, limited however to the fresh samples. No significant difference in redness (a*) at any considered time was found between CO and the control group, probably because of the content of astaxanthin that may have minimized the color differences amongst the different groups.
Rogers et al. [117]	CO-MAP (0.4% CO, 30% CO₂, 69.6% N₂) exhibited more desirable color and consumer acceptability throughout lighted retail display of ground beef during 20 days.
Pereira et al. [118]	Addition of CO-treated blood allows the production of better-colored sausages (mortadella) having lower residual nitrite levels.
Fontes et al. [119]	Saturated porcine blood with CO (99%) could substitute meat by up to 20% for mortadella’s processing. Therefore, from the nutritional point of view, meat replacement with up to 20% of CO-treated blood is nutritionally adequate for being used in sausage production.
Yang et al. [120]	Aerobically-packaged beef steaks exhibited a bright-red color at the first 4 days. However, discoloration and oxidation became major factors limiting their shelf-life to 8 days. Compared with aerobic packaging, VP extended shelf-life of beef steaks, due to better color stability, together with lower oxidation and microbial populations. Among all packaging methods, CO-MAP (0.4% CO + 30% CO₂ + 69.6% N₂) had the best preservation for steaks, with more red color than other packaging types.
Sakowska et al. [121]	The raw steaks’ CO penetration depth increased as exposure times and CO concentration in gas mixtures increased. However, the COMb that formed did not always turn brown during thermal treatment. In cooked samples treated with 0.3% and 0.5% CO-MAP, a red COMb border was visible at the cross-section, whereas other CO packaging treatments had partial or total browning. To create a red color in raw beef and avoid a red boarder in cooked beef, up to 0.5% CO in VP and only 0.1% for MAP can be recommended.
Lyu et al. [122]	The pretreatment of CO combined with O₃ at certain concentrations can be a promising technique to maintain the quality of beef meats under vacuum during storage.
Van Rooyen et al. [123]	The addition of CO pre-treatments prior to VP may be beneficial to allow a desirable color to be induced while allowing aging to occur within the package and increase meat tenderness. The 5-h CO pretreatment exposure time achieved the desirable color, and discoloration reached unacceptable levels by the use-by date. Therefore, applying 5% CO pretreatments may be a potential solution to current packaging issues within the meat sector for safety and enhancing meat quality. In addition, this anoxic packaging technology should prevent any negative quality issues related to high O₂-MAP packaging.
Sakowska et al. [124]	Using CO significantly increased the brightness and the redness of beef steaks in both CO-vacuum packaging and CO-MAP systems during storage for 21 days. They evaluated the effects of 0.5% CO exposure in two MAP (0.5% CO + 30% CO₂ + 69.5% N₂), as compared with conventional VP, on the quality of packaged beef steaks stored for 21 days at 2 °C. The consumers have the greatest desire to purchase the vacuum-packed steaks after exposure in CO.
Van Rooyen et al. [125]	CO as a pretreatment applied prior to VP or VSP may play an important role in overcoming some of the challenges the meat industry faces. This technology provides a prolonged storage, improves the tenderness of the meat and prevents the negative problems associated with other packaging technologies (reduces the risk of the cross-linking/aggregation of myosin due to Hi-O₂ MA, decreases energy usage, storage facilities and distribution costs).

The use of CO gives promising results in the primary package of fresh meat due to its positive effects on shelf-life prolongation during wider distribution of case-ready products. This, in turn, would reduce product and economic losses. By using CO in a modified atmosphere, the need for O₂ to achieve a bright color is eliminated, thus the opportunity to eliminate the detrimental product effects that O₂ imparts to the product. El-Badawi et al. [87] published for the first time an article on the use of CO (air + 2% CO) for the packaging of meat. Previous work reported that MAP with 0.4% CO and VP were the most stable packaging systems for ground beef containing 10–30% fat levels [114]. Modified atmosphere packaging with 0.4% CO is recommended for extended storage of fresh meat in a master-pack arrangement such that export to distant markets can be accommodated [85]. The inclusion of CO in MAP is controversial because the stable cherry-color can last beyond the microbial shelf-life of the meat and thus mask spoilage [23].

This entry is adapted from the peer-reviewed paper 10.3390/foods7020012

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