Carbon Monoxide in Meat and Fish Packaging: Advantages and Limits
<p>The cycle of color in fresh red meat.</p> "> Figure 2
<p>Factors influencing shelf-life of fresh meat.</p> "> Figure 3
<p>Photos of beefsteaks corresponding to the 21 days of storage under modified atmospheres packaging (MAP) at 1 ± 1 °C [<a href="#B188-foods-07-00012" class="html-bibr">188</a>].</p> ">
Abstract
:1. Introduction
2. Fresh Meat Packaging Methods
2.1. Raw Meat Spoilage-Associated Storage Conditions
2.1.1. Microbial Spoilage
2.1.2. Lipid Oxidation
2.1.3. Pigment Oxidation
2.1.4. Photooxidation
2.2. Fresh Meat Shelf-Life
2.3. Packaging Options
2.3.1. Emergence of MAP Case-Ready Meat Products
2.3.2. High O2 MAP
Gases Used in MAP
2.3.3. Vacuum Packaging
2.3.4. Safety of MAP
3. CO in Fresh Meat Packaging
3.1. What Is Carbon Monoxide?
3.2. Health Implications of CO
3.3. CO Application in Meat Packaging
3.3.1. Color Stabilizing and Shelf-Life Effects
3.3.2. Antimicrobial Effects
3.3.3. Other Effects
3.3.4. CO in Other Foods
Fruits and Vegetables
Seafood and Poultry
3.3.5. Co Pre-Treatments
4. Consumer’s Perceptions
5. Analysis of CO in Food
6. Safety Consideration of CO-Treated Meat
7. Regulatory Status for the Use of CO in MAP Systems
8. Could the Application of CO for Meat Packaging Be Re-Considered?
9. Conclusions
- The main disadvantage of using CO for meat packaging is the concern about masking of the microbiological risk by the formation of the stable and longer, bright red color.
- A combination of low levels of CO with CO2 in high concentrations, which reduce the growth of microorganisms, is of key importance to justify approval by EU regulatory agencies.
- It is also imperative that CO risk management be implemented in the packaging operations. The supermarkets and consumers at home must handle meat with strict hygienic standards, and low storage temperatures must be kept in a continuous chill chain.
- CO followed by vacuum packaging is promising because of the possibility of better adjusting the color stability of the meat to the time of spoilage.
- By adopting CO for meat and fish MAP, the meat industry must label the packages with reliable times for maximum shelf-life (the use-by date).
- The EU considers packaging gases as additives, and CO is not on the list of such gases. In order for CO to be approved as an additive within the EU, the following criteria must be met according to Directive 94/34/EEC. “They present no hazard to the heath of consumer at the level of use proposed, so far as can be judged on the scientific evidence available; to provide aids in manufacture, processing, preparation, treatment, packing, transport or storage of food, provided that the additive is not used to disguise the effects of the use of faulty raw materials or of undesirable (including unhygienic) practices or techniques during the course of any of these activities and to assess the possible harmful effects by evaluation any cumulative, synergistic or potentiating effect of its use and the phenomenon of human intolerance to substances foreign to the body”.
- In the EU, current labeling regulations require packages with meat and meat products in MAP to be labeled with “Packaged in a protective atmosphere”. The specific gases do not need to be declared on the packages. Conventional gases will probably be the ones most concerned by this statement. Low concentrations of CO in food packaging systems could be required to appear on the product label to inform consumers of its use in the product.
- Analysis of CO can be used to control whether muscle food products have been treated with CO or not, despite not having been labeled as such. These considerations underline the suitability to develop better alternative fast methods to detect even small amounts of the CO-Mb adduct in muscle tissues, in regard to the fraudulent treatment of meat and fish in the MAP systems.
Acknowledgments
Author’s Contributions
Conflicts of Interest
References
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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). |
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
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Djenane, D.; Roncalés, P. Carbon Monoxide in Meat and Fish Packaging: Advantages and Limits. Foods 2018, 7, 12. https://doi.org/10.3390/foods7020012
Djenane D, Roncalés P. Carbon Monoxide in Meat and Fish Packaging: Advantages and Limits. Foods. 2018; 7(2):12. https://doi.org/10.3390/foods7020012
Chicago/Turabian StyleDjenane, Djamel, and Pedro Roncalés. 2018. "Carbon Monoxide in Meat and Fish Packaging: Advantages and Limits" Foods 7, no. 2: 12. https://doi.org/10.3390/foods7020012
APA StyleDjenane, D., & Roncalés, P. (2018). Carbon Monoxide in Meat and Fish Packaging: Advantages and Limits. Foods, 7(2), 12. https://doi.org/10.3390/foods7020012