CHAPTER

19Modified AtmospherePackaging of Meat, Poultryand Fish

Kay CookseyDepartment of Food, Nutrition, and Packaging Sciences,

Clemson University, Clemson, SC, USA

CHAPTER OUTLINE

Introduction............................................................................................................475

Background ............................................................................................................476

Color .........................................................................................................476

Role of gases .............................................................................................477

Poultry ...................................................................................................................478

Fish........................................................................................................................479

Carbon monoxide ....................................................................................................479

Use of argon in MAP meat .......................................................................................482

Combination of processes or additives with MAP ......................................................483

Antimicrobial applications with MAP........................................................................485

Summary ................................................................................................................489

References .............................................................................................................490

IntroductionModified atmosphere packaging (MAP) for meat has existed since 1882, when it was

first documented that carbon dioxide helps preserve fresh meat. During the 1930s,

distribution of meat from Australia and New Zealand to the United Kingdom neces-

sitated the development of methods for distributing meat overseas, for which a longer

shelf life was required (Rao and Sachindra, 2002). During the 1980s, developments

in polymer technologies, a shift to centralized meat packing, and the introduction of

case-ready meat expanded the use of carbon dioxide and led to the greatest advance-

ments in the field. The term case-ready meat refers to meat that is packaged in a

modified-atmosphere package, is prepared at a central meat packing location, and is

Innovations in Food Packaging. DOI: http://dx.doi.org/10.1016/B978-0-12-394601-0.00019-9

© 2014 Elsevier Ltd. All rights reserved.475

ready for display in a retail case upon arrival at a retail location. This process was

developed for a variety of reasons, but the main reason was cost savings. Case-ready

meats eliminate the need for a butcher at retail, provide savings on labor costs,

extend the product’s shelf life so there is less waste, and provide more uniform pre-

sentation of meat cuts (McMillian, 2008). In the early days of case-ready meat, pro-

ducers hoped to brand fresh red meat, similar to the poultry industry, to increase

brand loyalty and recognition among consumers. The expected paradigm shift did

not occur, but the economic advantages have been realized.

It has been estimated that MAP can increase the shelf life of fresh meats by 50

to 400% compared to atmospheric packaging (Rao and Sachindra, 2002). Increased

shelf life allows the distribution of fresh meats over long distances (with refrigera-

tion) without the use of additional processing and additives while maintaining color

and overall quality. These advantages allow marketing and sales of products in

markets previously unavailable. It is essential that refrigeration temperature condi-

tions be maintained with as little variation as possible and that the proper materials,

headspace, and machinery are selected for each product. Some food safety chal-

lenges still remain but research continues to help address these concerns.

In the last few years, gas mixtures and packaging machinery systems and tray

and lidding materials have remained relatively unchanged. New developments

have focused on carbon monoxide (CO) combinations and understanding con-

sumer behavior based on consumer awareness and media involvement. Active

packaging in the form of oxygen scavenger materials, antioxidant-releasing film,

and antimicrobial combinations with MAP have been studied for poultry and fish.

Much of the research in active packaging has not been commercialized, and sev-

eral challenges must be faced before this can be realized.

BackgroundColorMyoglobin is a protein that forms the pigment responsible for the color of red

meat. It is made up of four pyrrole groups, which are united to form a porphyrin

ring. The color of the meat is dependent upon the state of the iron in the center of

the porphyrin ring (Figure 19.1). Oxymyoglobin has a bright red color and is

formed when iron is reduced and is in an oxygenated state. Myoglobin, the natu-

ral form of the pigment, is purplish-blue in color; the iron is in a reduced state

and is not oxygenated, unlike oxymyoglobin. Metmyoglobin is a brown to brown-

red color with iron in the oxidized state. Both myoglobin and metmyoglobin are

considered undesirable to most consumers, as meat with a red color is perceived

to be the freshest and safest to purchase, although meat in the myoglobin form

actually has a longer shelf life from a quality and safety standpoint. The muscle

and flesh of poultry and fish have lower concentrations of myoglobin, so packag-

ing is not designed to control the color of such products.

476 CHAPTER 19 Modified Atmosphere Packaging of Meat, Poultry

Role of gasesModified atmosphere packaging (MAP) for meat products involves the injection

of a specific mix of gases into a package along with selection of a packaging

material that will help maintain the desired atmosphere. Table 19.1 summarizes

the three main gases and their functions. Oxygen is mainly used to control the

color of fresh red meats, because color is important to consumers in determining

their selection of the product. MAP for fresh red meat is usually classified as high

or low oxygen, with high oxygen being 80% O2, 20% CO2 and low oxygen being

30 to 65% CO2 and the balance N2. Concentrations of oxygen in the range of 0.5

to 1% cause irreversible formation of metmyoglobin, thus oxygen should either

be provided in high enough levels to maintain oxygmyglobin or eliminated

(Anon., 2001). Poultry and fish are not classified in this manner, as they have

lower concentrations of myoglobin in their flesh and color is not a primary selec-

tion criterion used by consumers for such products.

Carbon dioxide inhibits the growth of Gram-negative bacteria such as

Pseudomonas spp., Aeromonas spp., Campylobacter spp., Enterobacteriaceae spp.,

and Salmonella spp., which are responsible for spoilage of fresh red meat and food-

borne illness. Lactic acid bacteria such as Lactobacillus spp. can grow and outcompete

high O2 low O2Oxymyglobin(bright red, Fe2+)

Myoglobin(purple-blue, Fe2+)

Metmyoglobin(brownish-red, Fe3+)

low O2 myglobinreductase

carbon monoxide

Carboxymyoglobin(bright cherry red)

FIGURE 19.1

Different states of pigment in fresh, uncooked red meat.

Table 19.1 Main Gases and their Functions in MAP of Meat, Poultry, and Fish

Gas Function

Oxygen Maintains color of fresh red meat.Controls microbial growth depending upon type of meat and targetbacteria.Plays a role in oxidation of fat.

Carbon dioxide Inhibits spoilage bacteria.Nitrogen Displaces oxygen and serves as an inert filler to prevent package

collapse.

477Background

other, more harmful bacteria, and they only cause spoilage after long-term storage

(Anon., 2001). The exact mechanism of how carbon dioxide prevents microbial

growth is not completely understood, but the generally accepted mechanisms include:

• Exclusion of oxygen by replacement with carbon dioxide

• Penetration of microbial cell walls, thus affecting cell metabolism

• Rapid reduction of pH in microbial cells, thus affecting normal metabolic

activity

• Alteration of enzymatic activity in microbial cells.

Carbon dioxide is highly soluble in high-moisture and fatty foods such as

meats, and solubility is increased as temperature decreases. Nitrogen is commonly

added to the gas atmosphere to prevent package collapse as the carbon dioxide is

dissolved into muscle. Additionally, many packages are overflushed with CO2,

which causes the lidding of a tray packed product to appear concave. High con-

centrations of CO2 can reduce pH due to the formation of carbonic acid when

CO2 dissolves in the moisture contained within the meat. The reduced muscle pH

results in precipitation of sarcoplasmic protein, leading to a grayish tinge in the

color of the fresh meat and increased drip and exudate, ultimately affecting the

texture and flavor of the meat when cooked.

High-oxygen MAP for fresh red meat has the advantage of retaining the red

color of the meat and extending its shelf life due to the addition of CO2; however,

if meat is stored too long, brown-colored metmyoglobin can form, fat can become

oxidized, and aerobic spoilage bacteria can begin to cause spoilage. The shelf life

of high-oxygen MAP fresh red meat is 10 to 14 days for ground beef and 12 to

16 days for whole muscle cuts when stored at refrigeration temperature (Belcher,

2006; Cornforth and Hunt, 2008). Low-oxygen MAP has a longer shelf life of 25

to 35 days, but due to the low oxygen concentration it does not appear bright red

at retail. To overcome this problem, a tray with double lidding can be implemen-

ted. During packaging, the tray containing the meat is flushed with carbon dioxide

and nitrogen and sealed with a lidding that has an impermeable layer that is

peeled off at retail so the oxygen-permeable lidding can allow oxygen into the

package. This allows shipment of the product in a low-oxygen environment and

display of the meat at retail without adverse effects on the color (Anon., 2001;

Delmore, 2009). In recent years, the dual-lidding tray has been replaced by use of

the MasterPack, a bag that contains multiple trays of fresh meat that have

oxygen-permeable lidding. The MasterPack is flushed with a specific mix of

gases similar to low-oxygen packaging, and once the product reaches the retail

display environment removal of the trays with oxygen-permeable lidding allows

the meat to bloom and appear red during display (Anon., 2009).

PoultryIn most cases, poultry is packaged using high CO2 to inhibit Salmonella spp. and

Enterobacteriaceae such as Escherichia coli. Campylobacter jujuni is one of the

top five causes of foodborne illness in food and can be present on poultry

478 CHAPTER 19 Modified Atmosphere Packaging of Meat, Poultry

products. Byrd et al. (2011) studied the effect of gas atmospheres on the microbial

quality of fresh broiler carcasses stored at refrigeration temperature for up to

14 days. Atmospheres studied included air, 100% oxygen, 100% CO2, and a typi-

cal gas flush for poultry (5% O2, 10% CO2, 85% N2). Carcasses were placed in

polyethylene bags and treated with one of the indicated environments. Microbial

analysis included detection of Camphylobacter, E. coli, psychrophiles, and total

aerobes. All of the treatments reduced Camphylobacter, but 100% O2 provided

more significant reduction than the other atmospheres. The 100% CO2 atmo-

sphere reduced the growth of psychrophiles, total aerobes, and E. coli more than

the other atmospheres did.

FishModified atmosphere packaging for fresh fish has received increased attention due

to the health benefits of consuming fish along with its potential to build a more

diverse market with a wider variety of fish. The main spoilage organisms in fresh

fish from temperate waters are Pseudomonas, Moraxella, Acetobacter, Shewanella

putrefaciens, Vibrio parahemolyticus, Flavobacterium, and Aeromonas species.

Microflora found on fish from tropical marine conditions include Staphylococcus

spp., Micrococcus, Bacillus, Clostridium, Brochotrix thermospacta, and

Streptococcus (Masniyom, 2011). Of greatest concern is Clostridium botulinum

type E, a nonproteolytic bacteria that can cause spoilage without producing the typ-

ical odor and slime that normally indicate spoilage. Gas mixtures and tight temper-

ature control are necessary for providing safe and high-quality MAP fish. Shelf life

can be 10 to 14 days at refrigeration temperature but can also be 18 to 20 days if

stored at 2 to �0.9�C. Gas mixes for non-fatty fish are typically 30% O2, 40%

CO2, 30% N2, and are 40% CO2 and 60% N2 for smoked and fatty fish (Robertson,

2004). Yesudhason et al. (2009) packaged fresh seer fish in high-density polyethyl-

ene trays, flushed the package with 60% CO2 and 40% N2, and sealed the tray with

a polyester-laminated film. A similar set of seer fish was packaged without gas

flush as the control. Mesophilic microbial counts were significantly lower for MAP

compared to the atmospheric packaged fish. MAP improved the shelf life of the

fresh seer fish from 12 days without MAP to 21 days under refrigerated storage

with MAP.

Carbon monoxideCarbon monoxide has been used in MAP packaging of fresh red meat since 1985

in Norway, although the effects of CO on the color of meat were known in the

early 1900s. Carbon monoxide has been used at low levels (0.3 to 0.5%) with 60

to 70% CO2 and 30 to 40% N2 to maintain the cherry-red color of meat without

the adverse effects of high-oxygen MAP packaging (Cornforth and Hunt, 2008).

In 2004, CO gas-flushed MAP packages were more widely used in the United

479Carbon monoxide

States for case-ready fresh meats. In 2002, Pactiv Corporation petitioned the U.S.

Food and Drug Administration (FDA) and U.S. Department of Agriculture Food

Safety and Inspection Service for Generally Recognized as Safe (GRAS) status

for CO treatment of fresh red meat in case-ready packages. The U.S. regulatory

agencies determined that the 0.4% CO portion of the Pactiv system posed no

threat and complied with GRAS requirements, so the agencies did not object to

the use of CO for meat from all livestock species (Cornforth and Hunt, 2008;

Weiss, 2006). Other companies such as Precept Foods and Tyson also received

“no objection” status. The safety of CO-treated meat has been well documented

by, for example, Cornforth and Hunt (2008), European Commission (2001), and

Day (2004).

In 2006, Kalsec, an ingredient manufacturer, filed a petition with the U.S. FDA

to ban the use of CO for fresh red meat and was joined by many consumer groups.

The premise of the objection was that the permanent red color deceived consumers

and prevented them from determining whether the meat was safe, if it had been

maintained at the proper temperature. Kalsec sold antioxidant ingredients that pre-

vented browning in high-oxygen MAP fresh red meat packaging (Weiss, 2006).

The European Union had already prohibited the use of CO, not because it was

deemed unsafe, but because it was determined that consumers were not willing to

accept the technology at the time (European Commission, 2001).

During this time, CO treatment of meat was not widely used in the United

States but today it is becoming more common again. The current regulatory status

is that CO is allowed in the United States and Canada at a level of 0.4% and the

package must be labeled to indicate that the color of the meat should not be used

to judge spoilage (Figure 19.2). A study performed by Carpenter et al. (2001)

indicated that consumers had preferences related to meat color (including

CO-treated meat) but did not have a packaging treatment bias that affected their

FIGURE 19.2

Case-ready meat taken from a local grocery store (Clemson, SC) showing inkjet-printed

label along with shelf-life date code.

480 CHAPTER 19 Modified Atmosphere Packaging of Meat, Poultry

eating satisfaction of the cooked meat. The authors concluded that this was a pos-

itive indicator for future consumer acceptance of new technology for red meat

packaging. Clearly, the objections to CO-treated meat in the United States during

the mid-2000s were not foreseen by Carpenter et al. (2001) or the meat industry,

but they have since died down and, with appropriate labeling, CO is in common

use in the United States, Canada, and Norway today. Concerns regarding the

safety of CO-treated meat are valid if the meat has been temperature abused,

which has spurred interest in implementing intelligent packaging applications that

signal when temperature abuse has occurred through the use of thermochromic

ink or enzyme-based time/temperature indicators.

Innovations in the use of carbon monoxide treatment in the last five years

have focused on applications besides red meat. Fraqueza and Barreto (2011) pack-

aged turkey meat using three different MAP conditions along with an atmospheric

package condition. Uncooked turkey muscle was packaged in polypropylene trays

covered with polyvinyl chloride film using 50:50% N2:CO2; 49.5:0.5:50% N2:

CO:CO2; 19.5:0.5:80% N2:CO:CO2; and 100% N2. The packages were placed in

barrier bags and then flushed with the specified atmospheres; microbial analysis,

color, and lipid oxidation were evaluated for up to 25 days of refrigerated storage.

Both treatments of CO combined with N2 and CO2 provided significantly lower

mesophilic and psychrotropic counts compared to the 50:50% N2:CO2 treated tur-

key. CO treatment along with oxygen concentration of less than 0.5% and high

levels of CO2 (80%) had a significant effect on inhibiting Brochothrix thermo-

sphacta. Shelf life (based on microbial quality) of turkey was longest for MAP at

19.5:0.5:80% N2:CO:CO2 (25 days) compared to 12 days for the 100% N2 atmo-

sphere; however, turkey in 100% N2 was the only sample that did not exhibit lipid

oxidation. The CO-treated turkey had a bright pink appearance, which was found

to be more desirable by consumers in an earlier study by Fraqueza et al. (2005).

The issue of consumer acceptance of CO-treated red meat has been of concern

to the U.S. consumer, but there was no scientific research regarding consumer

attitudes until a study was published by Grebitus et al. (2013). The research study

was designed to answer the following questions:

• Do consumers currently prefer the extended shelf life and stabilized color of

fresh meat without being specifically informed about the packaging

technology?

• Will consumers accept MAP for extending the shelf life and CO-MAP for

stabilizing the color after being informed about the technology?

• Do personal knowledge and media coverage influence consumer acceptance of

MAP and CO-MAP?

The hypothesis was that once consumers were aware of the packaging technol-

ogy their willingness to pay for the increased shelf life and stability would increase.

Ground beef was chosen as the MAP and CO-MAP product to be evaluated. The

study showed that consumers definitely purchase ground beef based on the red

color and are willing to pay more for a brighter red color (aerobic and CO) package

481Carbon monoxide

by $0.16/lb. However, once consumers were informed of the technology that helps

extend shelf life (MAP), their willingness to pay more was reduced to $0.11/lb, and

it dropped further to $0.05/lb when they were informed of CO-MAP technology. In

all cases, after learning of MAP and CO-MAP consumers still remained positive

with regard to willingness to pay for the technology. An increase in personal

knowledge and awareness of mass media coverage regarding CO-MAP technology

negatively affected willingness to pay. Grebitus et al. (2013) indicated that consu-

mers have difficulty understanding the technology as it was explained to them, and

admitted that wording used in the explanation could have led to some confusion

and that consumers only valued the technology if they could understand it. This is

a very important revelation for the food industry, as any new technology that bene-

fits product quality and safety can be easily misunderstood by the consumer.

Use of argon in MAP meatWhen the use of CO was eliminated in Europe, the use of argon as a gas in MAP

gained more attention. According to Morgan (2007), argon is tasteless, odorless,

and more soluble in water and oil than nitrogen. It also interacts with oxidase

enzymes, which can prevent spoilage due to the fact that argon is more dense

than nitrogen and is more effective for displacing oxygen. According to Fraqueza

and Barreto (2009). A study performed by Fachon (2002) found that argon helped

extend the shelf life of precooked sliced ham through control of oxidative reac-

tions and microbial inhibition. Based on this information, Farqueza and Barreto

(2009) sought to establish whether the same beneficial effects could be observed

in uncooked turkey meat using MAP. Turkey breast samples were packaged using

polypropylene trays with a polyvinyl chloride overwrap. The samples were placed

in high barrier bags containing one of four different gas flush combinations: (1)

100% N2; (2) 50% Ar, 50% N2; (3) 50% Ar, 50% CO2; or (4) 50% N2, 50% CO2.

All samples were stored under refrigeration and tested for microbial growth, pH,

color, and lipid oxidation for up to 25 days of storage. At the end of the 25 days,

turkey in the Ar�CO2 atmosphere (number 3) had one log lower growth for psy-

chrotrophic, total anaerobic counts as well as for Brochothrix thermosphacta. The

presence of argon did not differ from all other atmospheres with regard to lipid

oxidation.

A study by Tomankova et al. (2012) conflicts with the results of Fraqueza and

Barreto (2009). Atmospheres of 70% O2 and 30% CO2 were compared with 70%

Ar and 30% CO2 for packaging poultry meat. The poultry in packages with argon

had a higher microbial content and had an unpleasant aroma compared to the 70%

O2 samples. Ruiz-Capillas and Jimenez-Colmenero (2010) also found no beneficial

effects from argon in fresh pork sausages with regard to microbial inhibition com-

pared to 20% O2 and 80% CO2 or vacuum packaging. However, their sensory

results showed a positive response to the 30% CO2 and 70% argon versus the

oxygen-containing MAP packages. Herbert et al. (2013) studied the effects of six

482 CHAPTER 19 Modified Atmosphere Packaging of Meat, Poultry

different gas atmospheres on fresh chicken breast filets. The atmospheres were as

follows: (1) 15% Ar, 60% O2, 25% CO2; (2) 15% N2, 60% O2, 25% CO2; (3) 25%

Ar, 45% O2, 30% CO2; (4) 25% N2, 45% O2, 30% CO2; (5) 82% Ar, 18% CO2; or

(6) 82% N2, 18% CO2. As with the other studies, there was no significant differ-

ence between the argon-treated chicken filets compared to the N2 counterparts, but

the appearance of Brochothrix thermosphacta was significantly delayed using 82%

Ar, 18% CO2 (atmosphere 5) gas mixture. The only sensory benefit provided by

argon was found in retention of the pink color of the chicken samples for the 15%

argon atmosphere (number 1), compared to all other atmospheres studied. The

authors indicated that appearance was a benefit to consumers but the increased cost

of the gas should be considered as it relates to cost/benefit determination.

Fresh rainbow trout fed astaxanthin and canthaxanthin were packaged in poly-

styrene trays, gas flushed with either 60% N2 and 40% CO2 or 60% Ar and 40%

CO2, sealed with a lidding material (oxygen transmission rate: 5 cc/m2/24 hr), and

stored at 2�C (Choubert et al., 2008). Samples were measured at regular intervals

for pH, drip loss, lipid oxidation, color, gas atmosphere, and microbiological qual-

ity from day 0 to day 26. There was no significant difference between the

two gas atmospheres as it related to total aerobic plate count. Both atmospheres

inhibited total aerobic microflora equally well, and there were no significant

differences between atmospheres in pH or drip loss. The trout contained in the

argon-flushed packages had less change in color and lower lipid oxidation values

compared to trout in the nitrogen-containing gas mix. As with other authors of

papers involving the use of argon, it was noted that argon was beneficial with

regard to improving shelf-life quality but might require combinations with other

gases to reduce the overall packaging cost.

Overall, it appears that there is not strong evidence in support of argon reduc-

ing microbial production, except for Brochothrix thermosphacta; however, it may

have some benefit related to sensory properties. It is difficult to reach a definitive

conclusion, as all of the studies presented involve different meat products.

Combination of processes or additives with MAPIrradiation of meats has been used for meat products for many years to control

pathogenic bacteria such as Escherichia coli, Listeria monocytogenes,

Camphylbacter jejuni, and Salmonella spp. The degree of irradiation required to

destroy these bacteria can cause lipid oxidation and therefore reduce the quality

of the meat. To counteract this, MAP has been used to increase the sensitivity of

meat to treatment with irradiation. Studies by Chiasson et al. (2004) found that

ground beef treated with 30% CO2, 60% O2, and 10% N2 demonstrated increased

sensitivity of E. coli and Salmonella Typhimurium to irradiation compared to

ground beef in 100% CO2 or vacuum packaging atmospheres. However, the high

oxygen content of the atmosphere can contribute to lipid oxidation; thus, 100%

CO2 atmospheres have been suggested as a more feasible approach. The problem

483Combination of processes or additives with MAP

is that high CO2 levels can cause undesirable changes in the color of the meat. To

solve this problem, MAP atmospheres with high CO2 mixed with CO have been

studied to achieve the sensitivity of irradiation to microorganisms provided by

high CO2 while maintaining the fresh color of the meat. Kudra et al. (2011) found

that irradiation of fresh chicken breast meat was effective for reduction (3 log) of

Salmonella Typhimurium with a 1.5 kGy dose. When high CO2 plus CO-MAP

was tested, no difference was found with regard to microbial reduction when

compared to CO2 alone or vacuum packaged chicken.

Fish has also been effectively treated by irradiation to reduce Gram-negative

bacteria such as Pseudomonas spp., Salmonella, Staphylococcus aureus,

Campylobacter, Listeria monocytogenes, and Escherichia coli O157:H7 (Farkas,

1998). As with red meats and poultry, irradiation can negatively affect the sensory

properties of fish. Reale et al. (2008) studied the effects of two different MAP

atmospheres, gamma radiation, and atmospheric conditions (control) on the micro-

biological, sensory, and chemical properties of fresh sea bass. The modified atmo-

spheric conditions were 40:40:20% CO2:N2:O2 and 60:35:5% CO2:N2:O2. Overall,

gamma radiation at a dose of 3 kGy was most effective for reducing microbial

populations and reducing malondialdehyde formation (an indicator of lipid oxida-

tion), but it had very negative effects on the color, odor, and texture of the sea bass.

Of the two MAP conditions, it was determined that the 60:35:5% CO2:N2:O2 atmo-

sphere was the best for increasing shelf life with regard to microbiological, sensory,

and lipid oxidation.

It is important to chill fish as quickly as possible upon harvest to prevent micro-

bial deterioration and loss of product sensory characteristics. Fish begins to spoil as

soon as it is caught due to high water activity, high levels of non-protein nitroge-

nous substances, high ratio of unsaturated fats, and metabolic activity of natural

microbial flora (Ashie et al., 1996). Superchilling is considered a novel refrigera-

tion technique that involves chilling fish at subzero temperatures. According to

Sivertsvik et al. (2002), examples of superchilling systems include slurry ice or

ozone-ice combination, dry ice alone, or dry ice combined with water ice.

According to Olafsdottier et al. (2006), combined blast and contact (CBC) cooling

followed by superchilling at �1.5�C, extended the shelf life of cod fillets compared

to filets stored at 0�C. It is believed that dissolution of CO2 is enhanced under

superchilled conditions compared to standard chill conditions, thus enhancing inhi-

bition of certain spoilage bacteria. Wang et al. (2008) studied the effect of super-

chilling alone and MAP combined with superchilling compared to standard chill

conditions alone. Fresh cod loins were packed in polystyrene boxes 3 days post-

catch and chilled (1.5�C) and superchilled to (0.9�C). MAP conditions were used

for both storage conditions using a 50:45:5% CO2:N2:O2 gas mixture in plastic

trays. Superchilling alone increased shelf life from 9 to 16 or 17 days compared to

chilling alone. MAP combined with chilling increased shelf life from 9 to 14 days,

while MAP combined with superchilling increased shelf life to 21 days. The

authors noted that the superchilled MAP cod loins had a significant meaty texture

compared to the other samples which indicates that temperature fluctuation is

484 CHAPTER 19 Modified Atmosphere Packaging of Meat, Poultry

important to control in order to prevent ice crystal formation during superchilling,

thus negatively affecting texture. Fernandez et al. (2009) also found that superchil-

ling combined with an atmosphere of 90% CO2 and 10% N2 provided a shelf life

of 22 days compared to 11 days without superchilling or MAP for Atlantic salmon.

The use of two natural additives (rosemary extract and natural bioactive proteins

[Sea-i]) did not enhance the shelf life of the salmon. Shelf life was determined by

microbial analysis in the study by Fernandez et al. (2009).

Ozone has been used successfully to reduce microbial flora on fish whether

used in an aqueous or a gaseous phase. Few studies have examined the effect of

combining ozone treatment with MAP. Bono and Badalucco (2012) packaged

striped red mullet in air, MAP using 50:50% CO2:N2, and ozone-treated MAP

using the same gas composition. Fish were ozone treated by immersing them in

ozonated seawater at 5�C for 10 minutes with agitation. All samples were stored

at 1�C for up to 24 days. Ozone MAP-treated striped mullet had significantly

lower microbial counts compared to the non-MAP refrigerated samples. In addi-

tion, chemical indices of spoilage were lower for ozone-MAP fish, and both MAP

and ozone-MAP fish had desirable appearance and odor, particularly during the

first 10 days of storage. Overall, it was concluded that ozone treatment combined

with MAP extended the shelf life of striped red mullet fish and provided a high-

quality and microbiologically safe product for 12 to 18 days of storage at 1�C.

Antimicrobial applications with MAPAnother avenue to enhance MAP has been the use of active packaging, including

antioxidant-releasing film, oxygen scavengers, and antimicrobial agents included

as part of the packaging. Active packaging involves detection of a specific event

and response to the event. Some active packaging components are incorporated

directly into the film, while others consist of sachets or coatings that are released

from the packaging film or are part of the headspace gas mixture. Most of the

MAP active packaging applications studied recently target fish or poultry more

than red meat.

Torrieri et al. (2011) studied the combined effect of MAP with antioxidant-

releasing film to determine if the combination would increase the shelf life of

bluefin tuna filets. Quality factors not satisfactorily controlled by MAP alone

include lipid oxidation leading to off-odors and flavors along with color alter-

ation. Low-density polyethylene was embedded with three different levels of

α-tocopherol (an antioxidant) in preliminary experiments which determined that

0.5% was the best loading level to use for the full-scale study. Fresh tuna filets

were packaged in air, 100% N2 MAP without antioxidant film, 100% N2 MAP

with antioxidant film, and antioxidant film without MAP. The results indicated

that MAP alone extended shelf life from 2 days for the control to 18 days when

stored at 3�C. The antioxidant film plus MAP provided an equal length of shelf

485Antimicrobial applications with MAP

life compared to the use of MAP alone but enhanced the quality of the product by

reducing oxidative reactions.

Oxygen scavengers can be very effective for reducing the oxygen level in a

variety of packages to inhibit aerobic bacteria and mold and to control oxidative

reactions. For MAP meat, oxygen scavengers have been used to create a very low

(anoxic) package condition. Most commercial MAP packaging systems cannot

create a low enough oxygen level alone, as they leave 1% oxygen inside the pack-

age. Even though 1% seems like a low level of oxygen, it is enough to allow for-

mation of metmyoglobin (brown pigment), which is undesirable with regard to

consumer preference. In addition, the rate of metmyoglobin formation increases

with decreasing oxygen concentration so the levels of oxygen have to be reduced

quickly to prevent this reaction from occurring. According to Brandon et al.

(2009), a 1935 reference (J. Brooks) indicated that maximum production of met-

myoglobin occurs at 0.18%, thus oxygen scavengers are needed to rapidly reduce

oxygen concentration to below this level. Brandon et al. (2009) used iron-based

oxygen scavenger sachets from four different manufacturers with MAP to deter-

mine if the atmospheres produced could be ultimately used for low-oxygen MAP

meat packaging. Pouches were filled with 1, 2, 6, 12, or 22% O2 and 40% CO2,

with the balance being N2, and they were stored at 3�C and 10�C. No product

was contained within the pouch and headspace gases were measured over a

24-hour period. None of the scavengers could remove O2 at a rate that would pre-

vent metmyoglobin in a red meat product at either temperature condition. In addi-

tion, it was difficult to repeat the results, indicating that the sachets have a certain

degree of variation when used as single sachets. It was recommended that multi-

ple sachets per package would provide more repeatable results.

A variety of natural antimicrobial compounds have been studied for many

years in a variety of foods. Chitosan is a natural antimicrobial and antioxidant

with Generally Recognized as Safe (GRAS) status. Essential oils such as thymol,

clove, cinnamon, and lemon all possess antioxidant properties and are considered

natural. Giatrakou et al. (2011) combined MAP with chitosan and thyme for a

ready-to-cook poultry product. Chitosan (75 to 85% deacetylated) was prepared

in solution of acetic acid, yielding a 2% final concentration. Ready-to-cook

chicken and pepper kabobs were placed in a bag (low-density polyethylene/nylon/

low-density polyethylene laminate) and sprayed with 1.5% v/w chitosan and 0.2%

v/w pure thymol oil. Bags containing the samples were massaged by hand to

ensure even distribution of the chitosan and thymol. The MAP condition was

30% CO2 and 70% N2. The treatments were (1) air without chitosan or thymol

(control), (2) MAP without chitosan or thymol, (3) MAP with thymol, (4) MAP

with chitosan, and (5) MAP with thymol and chitosan. Samples were stored at

4�C for up to 14 days. The MAP treatments with thymol or chitosan alone were

effective for reducing lipid oxidation and extending shelf life by 6 days compared

to the air-packaged ready-to-cook kabobs. The combination of thymol, chitosan,

and MAP extended the shelf life to 14 days in addition to significantly reducing

microbial counts throughout the storage period. Mastromatteo et al. (2010) also

486 CHAPTER 19 Modified Atmosphere Packaging of Meat, Poultry

observed that packaging shrimp in MAP (5% O2 and 95% CO2) with thymol

(1000 ppm) improved the shelf life of fresh, peeled shrimp. Air-packaged shrimp

had a shelf life of 5 days; MAP alone, 7 days; and MAP combined with thymol,

14 days.

As mentioned previously, chitosan possesses antioxidant properties, which can

be useful in reducing lipid oxidation in meat products. It can also affect color

because it can chelate free iron released by myoglobin degradation during meat

storage (Kamil et al., 2002). The effect of chitosan on color stability and lipid

oxidation of ground beef under different packaging conditions was studied by

Suman et al. (2010). Ground beef was mixed with a final concentration of 1%

chitosan (75 to 85% deacetylated) and other ground beef was not treated with

chitosan. Packaging treatments were (1) vacuum, (2) high oxygen (80% O2, 20%

CO2), (3) MAP with CO (0.4% CO, 19.6% CO2, 80% N2), and (4) aerobic condi-

tions. All samples were stored at 1�C for 5 days and sampled for color, pH, and

lipid oxidation every day for 5 days. Chitosan (1%) improved the red color of

ground beef in CO and aerobic conditions but did not for high-oxygen and

vacuum-packaged samples. Chitosan reduced lipid oxidation in ground beef pack-

aged in all packaging treatments. It was determined that the effects of chitosan as

an antioxidant on ground beef color were packaging specific.

Chlorine dioxide is a vapor active compound that has been shown to be

extremely effective for elimination of pathogenic microorganisms. Due to its

strong oxidizing effect and fast biocidal effect in high-moisture environments,

controlled release is key to longer lasting effects without adverse consequences

on the sensory properties of the food. In a study by Ellis et al. (2005), fast or

slow release chlorine dioxide sachets were placed into barrier expanded polysty-

rene trays along with a single raw, split chicken breast. A control set of packages

did not contain a chlorine dioxide sachet. Each piece of chicken that was tested

was inoculated (on the top surface) with a 104-CFU/mL culture of Salmonella

Typhimurium (nalidixic acid-resistant strain). The chicken was packaged in a

modified atmosphere containing either 100% N2 or 75% N2 and 25% CO2.

Microbial analysis (natural chicken microflora and Salmonella Typhimurium ,

color analysis, appearance, and aroma were evaluated on days 0, 3, 6, 9, 12, and

15. Chicken samples treated with the fast and slow release of chlorine dioxide

contained lower natural microflora counts and lower Salmonella Typhimurium

counts in packages containing 100% N2 for each day of testing except day 3 and

day 9. Chicken samples treated with the fast and slow release of chlorine dioxide

contained lower Salmonella Typhimurium counts in packages containing the 75%

N2 and 25% CO2 gas mixture for each day of testing. The microbial counts fluc-

tuated between treatments for chicken packaged in the 75% N2 and 25% CO2 gas

mixture. The color of the chicken was adversely affected by chlorine dioxide, as

areas close to the sachet were yellow-green. The spoilage odor normally associ-

ated with chicken treated with chlorine dioxide, however, was masked based on

sensory panelists’ responses. A similar study was performed with a new genera-

tion of chlorine dioxide-releasing sachets (ICA Trinova, LLC) with boneless

487Antimicrobial applications with MAP

skinless chicken breasts placed in barrier trays that were flushed with a 30:70%

CO2:N2 gas mix before sealing (Shin et al., 2011). Chicken breasts were inocu-

lated with Listeria monocytogenes, Salmonella enterica ssp. Typhimurium at a

level of 104 CFU/mL. The results were similar to those of Ellis et al. (2005), in

that reduction of Salmonella Typhimurium was 1.87 log CFU/g and 0.68 log

CFU/g for L. monocytogenes, and reduction of aerobic microflora was around 2.5

log CFU/g compared to chicken in MAP alone. Color and pH of the chicken

breasts were adversely affected by the chlorine dioxide treatment (8 μg/hr) duringthe 21 days of storage at refrigeration temperature.

Allyisothiocyante (AIT) is a natural component of plants and is found in foods

such as mustard, horseradish, and wasabi. It has a very strong odor and has been

shown to exhibit antimicrobial properties in many studies. The concern is that the

aroma can have negative effects on the sensory properties of the food; therefore,

it is important to control the amount and rate of vapor released into the headspace

of the package. Shin et al. (2010) put AIT into a glass vial and controlled its

release into the package headspace by adjusting the size of the opening in the lid

of the vial. Fresh chicken breasts were inoculated with Listeria monocytogenes

and Salmonella enterica ssp. Typhimurium at a level of 104 CFU/mL and placed

in trays which in turn were placed in a high-density polyethylene bag containing

the vial of AIT. The bag was flushed with 30:70% CO2:N2 gas mix before seal-

ing. The level of AIT was performed at two levels, determined to be 0.6 and

1.2 μg/hr, and the authors reported that it was easy to adjust the levels of release

by adjusting the size of the opening in the vial placed in the bag. The levels of

reduction for L. monocytogenes and Salmonella Typhimurium were 0.77 and

1.3 CFU/mL, respectively, for the 1.2-μg/hr chicken packages. Reduction of aero-

bic microflora was around 2.5 log CFU/g compared to chicken in MAP alone, as

was found with the chlorine dioxide study performed by Shin et al. (2011). In

addition, the authors indicated that the chicken exposed to 0.6-μg/hr AIT was not

adversely affected with regard to pH and color, but the more effective level for

microbial reduction, 1.2 μg/hr AIT, adversely affect the pH and color of the

chicken. Both forms of vapor active antimicrobial compounds, chlorine dioxide

and AIT, can reduce microbial growth, particularly aerobic flora, which can

extend shelf life, but more work is needed to control the amount and rate of

release before AIT can be further considered for meat products.

Nisin is an antimicrobial agent that is effective against Gram-positive bacteria,

but with chelating agents such as ethylenediaminetetraacetate (EDTA) it can also

penetrate the outer microbial membrane of Gram-negative bacteria. A number of

researchers have found nisin combined with EDTA to be very effective for reduc-

tion of spoilage and pathogenic bacteria in a variety of foods. Economou et al.

(2009) studied the effects of nisin and EDTA on the shelf life of fresh chicken

breasts packaged in 65:30:5% CO2:N2:O2 MAP. Combinations tested included no

nisin or EDTA (treated with distilled water), EDTA with or without nisin (10-mM

or 50-mM EDTA), and nisin with or without EDTA (500 or 1500 IU/g nisin).

EDTA and nisin were added to packaged chicken by pouring a solution of one of

488 CHAPTER 19 Modified Atmosphere Packaging of Meat, Poultry

the treatments onto the chicken, leaving the solution on the chicken for 30 min-

utes, and then decanting the liquid, except in the case of the control, which used

only distilled water. The treated and control chicken was packaged in a low-

density polyethylene/nylon/low-density polyethylene barrier bag, gas flushed, and

stored under refrigeration for up to 24 days. EDTA alone did not inhibit bacterial

growth and was not significantly different from untreated (control) samples. All

treatments with nisin and EDTA were inhibitory toward mesophilic bacteria,

Brochothrix thermosphacta, lactic acid bacteria, and Enterobacteriaceae.

Nisin�EDTA-treated samples also ranked higher with regard to odor and taste

when the chicken was microwaved and evaluated by a sensory panel. Overall, as

the level of nisin and EDTA treatment increased, shelf life increased. Shelf life

was increased compared to the control by 1 to 2 days for nisin alone (500 IU/g);

by 3 to 4 days for nisin alone (1500 IU/g) and for low nisin/low EDTA (500 IU/g

and 10 mM); by 7 to 8 days for high nisin and low EDTA (1500 IU/g and

10 mM); by 9 to 10 days for high nisin and high EDTA (1500 IU/g and 50 mM);

and by 13 to 14 days for low nisin and high EDTA (500 IU/g and 50 mM).

Potassium sorbate is not considered a natural antimicrobial agent, as are the

agents discussed earlier, but it is classified as Generally Recognized as Safe

(GRAS). Yesudhason et al. (2010) treated fresh seer fish steaks with a 2% potas-

sium sorbate dip prior to packaging and refrigerated storage. The control set was

atmospheric packaging (air), one set was MAP only, and another set included the

potassium sorbate-treated fish packaged in a modified atmosphere. MAP condi-

tions were based on a preliminary study that examined several gas mixtures where

a 70:30% CO2:O2 mixture provided the best sensory results. MAP packaging

extended the shelf life of the seer fish steaks by 10 days compared to the control,

and MAP with potassium sorbate treatment extended the shelf life by 18 days. In

addition, potassium sorbate-treated fish had a higher sensory score compared to

MAP alone after 25 days of refrigerated storage.

SummaryModified atmosphere packaging (MAP) of meat poultry and fish has remained

one of the best methods to increase shelf life and allow distribution of a consistent

and cost-effective product to retail. Gas mixtures, materials, and machinery have

not changed much in recent years; thus, innovation has focused on providing bet-

ter color and appearance as well as quality improvement using combination treat-

ments including irradiation, argon, ozone, and active packaging techniques.

Changes in MAP for red meat have addressed consumer response and industry

reaction to the use of CO to maintain the red color of meat. Consumers prefer a

bright red color but are confused by the technology involved and become less

willing to purchase products that involve technology that has the appearance of

deception. Combination treatments and processes have varying degrees of

489Summary

benefits, but in all cases cost must be weighed against the benefits. Of the active

packaging techniques studied, antimicrobial methods have attracted the most

interest in terms of research for poultry and fish products. Antimicrobial treat-

ments have shown promise for MAP meat products but face challenges relative to

commercializing methods developed on a small laboratory scale. Sustainability

and intelligent packaging features (e.g., time/temperature indicators, spoilage indi-

cators) are also a trend in MAP, but those areas are covered in greater detail in

other chapters of this book.

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