Centralized Packaging of Retail Meat Cuts: A Review

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1 418 Journal of Food Protection, Vol. 62, No. 4, 1999, Pages Copyright, International Association of Milk, Food and Environmental Sanitarians Review Centralized Packaging of Retail Meat Cuts: A Review G. TEWARI, 1 D. S. JAYAS, 1 * AND R. A. HOLLEY 2 1 Department of Biosystems Engineering, 438 Engineering Building, University of Manitoba, Winnipeg, MB, Canada R3T 5V6; and 2 Department of Food Science, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 MS : Received 30 June 1998/Accepted 18 November 1998 ABSTRACT Centralized packaging of retail meat cuts is growing more popular because of its economies and potential to maintain quality, enhance safety, and extend the shelf life of fresh meat. Requirements for optimizing shelf life of centrally prepared retail cuts for periods up to 15 weeks are slightly different from those needed to extend the shelf life of fresh, chilled meat. Chilled meat primarily deteriorate at the cut or uncut muscle surface. In long-term storage, primal cuts are placed in an atmosphere saturated with carbon dioxide and containing very low residual oxygen. These cuts are held at C. When the meat is removed, it is fabricated into retail or food service cuts. New fresh surfaces are created in the process, revitalizing the meat s appearance. After being prepared for retail display, the meat normally has four more days of shelf life. Depending on the meat species, shelf life is usually limited by development of undesirable organoleptic changes, usually defects in color, which are independent of microbial presence. The microbes consist of a lactic acid bacterial population that maximizes under storage conditions at about 10 8 CFU/cm 2 well before shelf life ends. Circumstances are different with centralized distribution of retail-ready fresh meat. The wholesale storage period following initial packaging of the retail cuts is about 20 to 30 days. Prepared products must withstand retail display for up to 2 days without further manipulation of package contents. Retail packages are simply moved from their storage container (usually a unit or overwrap containing a modified atmosphere) to retail display, where desirable meat color develops upon exposure to air. Three gas atmospheres have some potential to satisfy storage needs for centralized distribution of retail-ready packages: 100% CO 2, 100% N 2, or 70% N 2 30% CO 2. Shelf life is limited by undesirable changes in surfaces exposed at initial packaging, caused by growth of psychrotrophic bacteria. If 100% CO 2 is used, these are all lactic acid bacteria (LAB). Therefore, initial bacterial numbers on the meat and storage temperature become critical to success. The most attractive storage option is 100% CO 2 used at C. This review presents the reason for that recommendation, along with basic concepts of meat chemistry, a discussion of modified atmosphere packaging, meat microbiology, and current results with simulated centralized packaging of retail-ready meats. Useful shelf life is the time required for a food to become unacceptable from a sensory, nutritional, microbiological, or safety perspective (46). Shelf life can be extended when the mechanism causing spoilage of a food product is known and manipulated using techniques that do not affect its sensory or nutritional characteristics. Shelf life can be extended using techniques such as thermal processing (retort and aseptic processing), freeze-drying, cryogenic freezing (individual quick-frozen technique, or IQF), and others. These techniques are well adapted by food industries to extend the shelf life of liquid foods (retort or aseptic processing), liquid foods with particulates (canning and retort), dehydrated foods (freeze drying), cut fruits and vegetables (IQF), and meat (refrigeration or freezing). However, these techniques result in loss of nutrients and freshness, meaning a fresh taste. The value of freshness is demonstrated by the fact that fresh fruits, vegetables, and meats are premium-priced products in both local and international markets. * Author for correspondence. Tel: ; Fax: ; Digvir Jayas@Umanitoba.ca. A new food-preservation technique, irradiation, has recently been approved by the U.S. Food and Drug Administration (FDA) for red meat; however, there is debate about the availability of suitable polymers for irradiated packages. There are currently only a handful of polymers approved in the U.S. Code of Federal Regulation (CFR) Title for use with irradiated foods. Of these, only one EVA (ethylene vinyl acetate) can receive electronbeam treatment. Most of the polymers listed in this section were approved in the 1960s. It is difficult to make a contemporary multilayer structure with currently approved polymers. According to radiation chemistry, electron-beam, gamma, and X-ray treatments should all have the same effect on polymer packaging materials. They are treated differently in the CFR because initial requests only mentioned gamma treatment; other methods were added separately. These difficulties with U.S. regulations effectively limit the use of irradiation for red meat. Therefore, until today, modified atmosphere packaging (MAP) is the only available technique that delays microbiological growth, ensures freshness, and provides a long shelf life of fresh meat (5, 21, 28, 37). Nevertheless, MAP

2 J. Food Prot., Vol. 62, No. 4 CENTRALIZED MEAT PACKAGING 419 should be coupled with strict temperature control to achieve maximum microbial inhibition. The rate of spoilage in muscle foods is high because they are a protein-rich medium that encourages microbial growth. Muscle tissue continues to metabolize just after slaughter, using stored carbohydrates and fats. Without further processing, microbial growth results as the energy stores are depleted and metabolic products (low-molecular-weight organic compounds) accumulate in the tissues. This growth produces undesirable odors and flavors, and eventually microbiological decay occurs on the meat surface (46). Optimized storage of fresh meat can yield 9 to 15 weeks of useful product life if meats are held at C in atmospheres saturated with CO 2 and devoid of O 2. These systems for long-term storage and intercontinental transport are most useful for primal cuts of meat. After such storage, products can be trimmed of surface imperfections, sliced, and repackaged in convenient retail sizes on trays, using films permeable to oxygen, and yield satisfactory meat color for up to 4 days of display in the store. In contrast, with centralized packaging of retail-ready cuts, final trimming and portioning take place during initial packaging. The packaging film contacting the meat surface is oxygen-permeable. Fabricated products must withstand 20 to 30 days storage in their original packages (which are usually grouped together in a modified atmosphere) before retail display at about 7 C. Because there is no further manipulation of the cuts other than moving packages to the display case, meat surfaces exposed at the central preparation facility must retain their attractiveness and appeal not only during storage but also for about 2 days of retail display. Centrally packaged retail cuts of fresh red meats are economical because they require less manpower, equipment, and space, and they reduce chances of cross-contamination due to continuous process operation. Tesco, a British supermarket chain, has converted its entire fresh-meat operations to central packaging using MAP (7). Brody reported that the three most interesting technologies involved are Cryovac s vacuum skin packaging, Tesco s barrier foam trays, and master packs spawned by CVP Systems and M- Tek from the success of case-ready poultry packaging (7). Recently, W. R. Grace Limited, Australia (in collaboration with the Commonwealth Science and Industry Research Organization in Canberra, Australia) has designed a retailready master-pack system for transporting meat to distant countries. Although centralized preparation techniques are available, distribution of meats like pork and beef that have a relatively short shelf life is still questionable because there is no efficient and reusable refrigerated distribution system with strict-enough temperature control ( C) (22, 25). Following is a discussion concerning the basic concepts of meat chemistry, meat microbiology, MAP systems, and meat distribution systems that must dictate the design of a refrigeration system for distributing centrally packaged retail meat cuts. Also, work done by researchers related to such central packaging is critically examined, and recommendations are made for future design of reusable refrigerated containers. BASIC MEAT CHEMISTRY Package designers must understand the chemistry behind postmortem changes in meat before designing a centralized meat distribution system to extend its shelf life (12, 15). Reactions during contraction and relaxation of muscle. Contraction and relaxation of voluntary muscle is based upon interaction among adenosine triphosphate (adenine-d-ribose-p P P) (ATP); myosin, a key muscle protein that catalyzes the splitting of ATP; and actin, a filamentous key muscle protein that contributes the nutritive value of meat. Hydrolytic splitting of ATP provides energy for muscle contraction, because hydrolysis of phosphate groups is a very exergonic reaction. When muscle is relaxed, ATP is in the form of an inert magnesium complex (Mg-ATP). When the muscle receives a nerve stimulus, calcium ions are released into the sarcoplasmic reticulum (a fine network of tubules surrounding intracellular myofibrils and joined to the plasma membrane of the muscle cell). The calcium-ion release has two results: (i) Ca 2 releases ATP from Mg-ATP, and (ii) Ca 2 stimulates myosin- ATPase (myosin adenosine triphosphatase). As a result, energy is released from the high-energy phosphate bond, which initiates muscle contraction due to the sliding action of actin filaments over myosin filaments, and a temporary actin myosin (actinomyosin) complex is formed. During relaxation, Ca 2 ions are removed by a relaxing factor (calsequestrin). That is, Ca 2 is pulled back to the membrane of the sarcoplasmic reticulum. Then inhibition of myosin-atpase activity takes place and the actin myosin complex dissociates. Next, new ATP has to be regenerated to allow subsequent contraction. It can come from two sources: aerobic respiration (the primary source), or the Lohmann reaction (Eq. 1), utilizing residual adenosine diphosphate (ADP) and creatine phosphate (creatine P) in the tissue: (ADP creatine P) s (ATP creatine) (1) Conversion of muscle to meat. After the death of an animal, muscle tissue is in the relaxed stage; i.e., ATP is in the form of a Mg-ATP complex. At this time, muscle tissue is soft and pliable, capable of a high degree of extension. Before meat is acceptable for human consumers, there are three main stages through which the tissue passes: prerigor, rigor mortis, and postrigor. In the prerigor stage, muscle tissue is still soft and pliable. In biochemical terms, there is a continuing decline in the levels of ATP and creatine P. Also, anaerobic respiration takes place because muscle tissue is not receiving O 2. Rigor mortis begins within 10 to 12 h after the death of an animal and lasts about 15 to 20 h. Glycogen also begins to be converted to lactic acid. Actinomyosin forms as Ca 2 ions are released into the sarcoplasmic reticulum, which yields muscle inflexibility. During the postrigor state, muscle tissue becomes more

3 420 TEWARI ET AL. J. Food Prot., Vol. 62, No. 4 tender and acceptable, in part due to proteolytic enzyme activity. Also, the ph of meat falls from about 7.2 to 7.4 to about 5.3 to 5.5 as glycogen is converted to lactic acid. Low ph retards the growth of some microorganisms; therefore, the ph of meat plays an important role in its shelf life (a high ph [6.0 to 6.5] usually means a greater risk of microbial spoilage). Also, there is a relationship between ph and meat color: ph of 5.3 is associated with a light pink-red color, whereas ph 6.0 is indicated by an unacceptable dark color. There are other changes during postmortem glycolysis: (i) color change from dark red to a lighter greyish-pink; (ii) exudation, or water loss, resulting from a decrease in the meat s water-holding capacity; and (iii) textural changes, as the meat becomes more tender. In addition to the meat s becoming tender, it also develops flavor during the postrigor state. ATP or its degradation products, such as inosine monophosphate, and the breakdown of cytoplasmic proteins contribute to the final flavor. Therefore, when designing a centralized meat packaging system, it is very important to select an efficient packaging technique that delays color and flavor changes so that they are best when the meat is presented to the consumer. CENTRALIZED MODIFIED ATMOSPHERE PACKAGING Central packaging of retail meat cuts involves MAP, which reduces the growth rate of microorganisms that cause spoilage. MAP must be combined with strict temperature control because anaerobic LAB are dominant under reduced O 2 levels, and they cause early spoilage of meat unless its temperature is controlled. MAP and controlled atmosphere storage. MAP is defined as the packaging of a perishable product in an atmosphere which has been modified so that its composition is other than that of air (33). This contrasts with controlled atmosphere storage (CAS), which involves active and continuous control of the atmosphere surrounding the food and is prominent in warehouse storage of vegetables and fruits. The CAS systems for meat use static atmospheres saturated with CO 2. In MAP, the initial atmosphere surrounding a food is altered by the addition of CO 2 or a combination of gases (O 2,N 2, and CO 2 ). The function of CO 2 is to decrease the growth rate of microorganisms by increasing their lag phase and reducing product respiration, whereas N 2 is used to displace O 2. It acts as an inert filler, preventing the package from collapsing when some of the CO 2 is absorbed by moisture in the product. Earlier developments in MAP. The preservative effect of CO 2 has been known for over a century. Real development of MAP started in 1922 when Brown (8) investigated the effect of different concentrations of O 2 and CO 2 at various temperatures on the germination and growth of fruit-rotting fungi. He recommended gas storage combined with cold storage to extend the shelf life of fruits. Kidd and West (43) examined the effect of atmosphere modification on the storage life of fruits. This experimentation resulted in the first commercial CAS of apples, in Kent, England, in Killefer (44) found that pork and lamb remained fresh twice as long in 100% CO 2 at4to7 C than it did when stored in air at the same temperatures. Callow (11) reported similar improvements in keeping pork and bacon. Tomkins (62) and Moran and colleagues (47) reported that mold growth on meat could be retarded with as little as 4% CO 2 in the storage atmosphere. The higher the CO 2 concentration, and the lower the storage temperature, the more effective the inhibition. Haines (32) found that it took twice as long for some common meat bacteria to multiply in 10% CO 2 at 0 C than in air at the same temperature. Controlled atmospheres have been used in commercial storage to delay physiological changes such as ripening in fruits and vegetables (14, 62), for example, or to transport chilled beef carcasses from New Zealand and Australia (56). By 1938, 26% of chilled carcass beef shipped from Australia and 60% of that shipped from New Zealand were being held in a controlled atmosphere of 10% CO 2 for 40 to 50 days without any spoilage (51). Coyne (13) demonstrated that fish fillets or whole fish could be kept twice as long as usual at ice temperature if stored in an atmosphere containing 25% CO 2. By the 1960s, vacuum packaging had become popular for fresh meat. Ogilvy and Ayres (49) did a comprehensive study on the use of CO 2 -enriched atmospheres for extending the shelf life of chicken portions and found that shelf life was a linear function of CO 2 concentration. (However, meat discoloration was observed at high CO 2 concentrations.) In the 1970s, bulk packs of fresh chicken evacuated and then flushed with CO 2 were introduced commercially in the USA, extending its shelf life to 18 to 21 days in chill storage (51). Marks and Spencer test-launched MAP meat in 1979; they are responsible for Britain s dominance today in the world marketplace for modified-atmosphere products. Within 2 years, they had extended their product line to include bacon, loin chops, sliced cooked cured meats, fresh and smoked fish, and cooked shellfish (51). In North America, the science and technology of gas preservation evolved slowly, perhaps because of highly developed refrigeration and transportation/distribution systems (15, 50). Over time, though, the rising costs of raw food products, labor and energy, tighter controls on some preservatives and additives by the U.S. FDA, and the availability of less O 2 -permeable packaging films, as well as the versatility of packaging equipment, have promoted MAP products in North America. Modern MAP systems eliminate the cumbersome continuous control of the atmosphere surrounding the product, which makes it much cheaper for a large-scale operation to be developed. Research and development on MAP accelerated during the 1980s and 1990s, resulting in successful commercial applications (50). Methods of atmosphere modification. Various MAP techniques are available. Each one s advantages and disadvantages should be considered when adapting these techniques for centralized meat packaging. Vacuum packaging was the earliest form of MAP de-

4 J. Food Prot., Vol. 62, No. 4 CENTRALIZED MEAT PACKAGING 421 veloped commercially and is still used for products such as primal cuts of fresh red meat, cured meats, hard cheeses, and ground coffee (51). Since the product is packed in film with low O 2 permeability and the air evacuated, entry of O 2 from outside is restricted. With vacuum-packed fresh meat, CO 2 increases to 10 to 20% within the package as respiration of the meat quickly consumes the residual O 2. Vacuum-packaged fresh beef is unsuitable for the retail market because it changes color from red to purple (myoglobin deoxymyoglobin) due to the low O 2 level, which is considered unacceptable by consumers. This is a reversible reaction; however, formation of the oxidation product metmyoglobin (which is brown) does occur to a small extent and is less easily reversed with time. These changes also take place, but less noticeably, in pork. Finally, exudate accumulates during prolonged vacuum-pack storage of meat, probably related to the lack of package headspace (51). In vacuum skin processing (VSP), a vacuum is used to apply a thermoformable film softened by heating as a skin over meat on a rigid backboard (58). This method promotes longer storage life, depending on meat species and muscle ph, because exudate development and precipitation of denatured meat pigment on the meat surface is not as pronounced as in the regular vacuum packages. However, dark meat color is more noticeable in meat cuts using VSP. Its application is more popular for cured products, where color differences are not as apparent. Gas packaging can be done either by mechanically replacing air with gas mixtures or by generating the atmosphere within the package (passively or actively, for example with O 2 absorbents). In-package generation is not very effective for meat. Mechanical air replacement can be done either by gas flushing or by compensated vacuum (51). Gas flushing is usually performed on a form fill seal machine by injecting a continuous stream of gas into the package to replace the air. After most of the air has been removed, the package is sealed. In the compensated vacuum process, a vacuum is first created in a preformed or thermoformed container holding the food, then the desired gas or gas mixture is introduced. Gas-flushing techniques can be very fast and lend themselves to continuous operation. Ordinarily, O 2 levels in gas-flushed packs are 2 to 5%; therefore, that method is unsuitable for packaging O 2 -sensitive foods. For longer storage of fresh meats, more sophisticated flushing systems (e.g., Captech) are used to reduce O 2 levels to 300 ppm. Master packaging involves placing MAP products (wrapped in a permeable film) into a gas-impermeable package that eliminates O 2 from the surrounding atmosphere (3). The MAP products are placed in this impermeable package before shipping; the internal atmosphere can be up to 100% CO 2, which minimizes the growth of microorganisms. Retailers remove the gas-impermeable barrier, developing the desirable bright red color when O 2 passes through the permeable package. Master packs must be coupled with an excellent temperature control system during distribution ( C) to achieve optimal shelf life extension. MICROBIOLOGICAL AND SENSORY CHARACTERISTICS OF MEAT Borch and colleagues (6), Kraft (45), Gill (16, 20), Offer and Knight (48), and Stiles (60) have reviewed meat microbiology and techniques for shelf-life extension. Foodborne illness is caused by a combination of intrinsic and extrinsic factors. The intrinsic factors are related to the food: chemical and physical composition, water activity (a w ), ph, O 2 -reduction potential, and natural inhibitory factors. The extrinsic factors are related to the surrounding environment: storage temperature, packaging, gas atmospheres, preservatives, cleaning, disinfection, and hygiene. These factors influence survival or growth of microorganisms in the food. By manipulating them, barriers to microbial growth can be created (56). For MAP foods, strict refrigeration at temperatures close to those causing freezing is important to assuring product quality. This is because psychrotrophic bacteria can grow at temperatures lower than 2 C, at which most meat freezes. Adequate refrigeration must be maintained throughout the food distribution system. Good sanitation practices during slaughter are necessary to control surface contamination, because the exterior of animals is often heavily soiled (1, 39). Chilling meat creates a selective environment that favors the growth of psychrotrophic microorganisms (60). Psychrotrophic bacteria have optimum growth temperatures of 25 to 30 C but they can grow even at 3 C (38). Psychrotrophic fungi cannot grow if relative humidity is 80%, but carcasses are not stored in dry conditions because the meat loses sensory quality (38). Composition of the gas atmosphere also affects which microbes grow on meat. Gram-negative, rodshaped bacteria such as Pseudomonas, Moraxella, and Acinetobacter spp. favor aerobic, chilled storage (1, 2). Offflavor develops at 10 7 CFU/cm 2 of meat. Reduced O 2 and high CO 2 conditions discourage growth of aerobic spoilage bacteria but encourage slower-growing spoilage bacteria such as Lactobacillus (53). Microflora changing from aerobic to anaerobic organisms in the packaged meat is the main factor that extends the storage life of vacuum-packed and MAP meat with high levels of CO 2. Benedict and colleagues (4) reported that LAB do not produce off-flavors or off-odors in vacuum-packaged meat stored at 0 to 5 C as quickly because the aerobic spoilage microflora and myoglobin conversion to metmyoglobin are delayed. Gill (19) suggested that red meats (prepared with high hygiene standards) in 100% CO 2 in a gas-impermeable film, packaged using the Captech system and stored at 1.5 C, can have a storage life of up to 6 months. Anaerobic spoilage is often unnoticed until bacteria reach 10 8 cells/cm 2. Several researchers have studied the effects of different gas compositions on the microbiological and sensory quality of meat during centralized packaging. Shay and Egan (58) used MAP to extend retail storage life of beef and lamb. They stored meat under 80% O 2 and 20% CO 2 at 5 C and found that storage life was three times better than it was in conventional overwrap trays. They also noted that in most situations, storage life was limited by poor color

5 422 TEWARI ET AL. J. Food Prot., Vol. 62, No. 4 rather than excessive microbial growth. Also, storage life was dependent on muscle type, species, and the length of time meat had been stored previously in vacuum. Pork color was more stable than beef or lamb in low levels of O 2 (52). Scholtz and colleagues (55) examined the potential value of prepackaging pork centrally by comparing the retail shelf life of pork loin chops packaged under an atmosphere of 25% CO 2 75% O 2 with control samples packaged using VSP or polyvinyl chloride (PVC) overwrap. All samples were stored at 0 C for up to 21 days. Results from this group of trials were compared with those from similarly prepared retail-packaged chops placed on PVC-overwrapped trays, packaged in groups of six in a master pack containing a 100% CO 2 atmosphere. Samples stored using either VSP or 25% CO 2 75% O 2 were acceptable 7 days after packaging and retail display. Microbiological results were similar to those obtained from conventionally packed PVC-overwrapped trays after only 4 days of storage at 0 C. The 100% CO 2 treatment yielded the most promising results, with samples stored for 21 days still capable of 4 days subsequent retail display. Shelf life was limited by color acceptability. In an attempt to improve pork color stability following suggestions by Taylor (61), Buys and colleagues (9) included 25% or 80% O 2 in PVC-wrapped retail pork chop packages, then overwrapped them with barrier bags having an O 2 transmission rate (OTR) of 39 ml/(m 2 24h) atm at 23 C, 75% relative humidity. The packages were subsequently backflushed with either 100% CO 2 or 25% CO 2 50% N 2 25% O 2. No significant color differences were seen after 21 days storage, and samples achieved 2 days subsequent acceptable retail display. Less pigment stability was seen in high-o 2 packages. Buys and colleagues (10) then explored the use of either vacuum or 100% CO 2 to preserve unsliced pork loins for up to 21 days at 0 or 5 C. After that time, they sliced the loin into chops and evaluated them for color and microbiological condition during retail display, again in PVC-overwrapped trays. Chops prepared from loins stored at 0 C for 21 days were still acceptable after 4 days of retail display. Different initial packaging treatments did not yield different retail shelf lives. Unfortunately, the barrier bags used to simulate master packs in the trials by Buys and colleagues (9, 10) and Scholtz and colleagues (55) had OTRs significantly greater than the 15 ml/(m 2 24h) atm at 23 C and 75% relative humidity currently used to create an acceptable O 2 barrier. Results from these studies did not clearly demonstrate effects that could be attributed to differences in package atmosphere composition. Gill and Penney (26) studied the effects of ph and the ratio of initial gas volume to meat mass on the storage life of chilled beef packaged under CO 2. They reported larger Enterobacteriaceae fractions on high-ph ( 6.0) meat than on normal-ph meat (5.5 to 5.7) during storage at 1 C. Grau (29) reported that Enterobacteriaceae were unable to grow on muscle tissue with a normal ph under anaerobic conditions. Later, Grau (30) and Vanderzant and colleagues (63) observed that Enterobacteriaceae grow slowly on normal-ph muscle tissue vacuum-packed using film of low, but measurable, O 2 permeability. Gill and Penney (26) reported that all vacuum-packaged meat was spoiled by putrid flavors (high-ph meat was spoiled at 7 weeks; normal-ph meat, at 12 weeks). They also reported that increasing the amount of added CO 2 progressively retarded putrid spoilage by slowing microbial growth rate, but more CO 2 increased the relative number of LAB in the flora. This effect was caused by CO 2 s inhibitory effect on Gram-negative organisms on both normal- and high-ph meat; CO 2 extends the lag phase of microbial growth. The LAB dominate these environments at low temperatures and form less offensive metabolic by-products than organisms of other genera. This study showed that CO 2 can greatly extend the shelf life of packaged chilled meat, but saturating levels (about 2 liters CO 2 per kilogram of meat) are required for extended storage. Gill and McGinnis (24) studied the changes in microflora on commercial beef trimmings during collection, distribution, and preparation for its retail sale as ground beef. They reported that during storage of 18 days before grinding, meat trimmings developed LAB flora of up to 10 7 CFU/g. Normally, these materials would spoil within 3 days if packaged in O 2 -permeable film and stored under the same refrigeration. They recommended centralized meat distribution systems for retail-ready cuts and strict control over storage and distribution temperatures for extending the shelf life of meat. Gill and Jones (23) compared the display life of retailready beef steaks using vacuum packaging ( 1.5 C) or master packing (2 C) under atmospheres of N 2,CO 2,orO 2 CO 2. The product was assessed after a storage time of 60 days. At each assessment, a vacuum package and a master pack were withdrawn from storage. Three retail packs were prepared from vacuum-packaged meat and displayed with retail-packaged meat from a master pack in a retail cabinet at air temperatures between 3 and 5.7 C. Steaks from vacuum packs were considered desirable, with little metmyoglobin in the surface pigment. Numbers of bacteria on steaks from vacuum packs and N 2,CO 2, and O 2 CO 2 atmospheres were, respectively, 10 4, 10 6, 10 5, and 10 4 CFU/cm 2. The flora from steaks stored under CO 2 were composed entirely of LAB. Small fractions ( 5%) of Enterobacteriaceae and Brochothrix thermosphacta were present in the steak prepared from vacuum-packaged product stored for 39, 46, or 53 days. Large fractions ( 20%) of Enterobacteriaceae or B. thermosphacta were present in the flora of steaks stored under O 2 CO 2 atmospheres for 8, 12, or 20 days. The numbers attained by spoilage flora on steaks under CO 2 were insufficient to cause organoleptic effects. Gill and Jones therefore concluded that master packs under CO 2 could be an appropriate technique for extending shelf life of beef for up to 7 weeks and is useful when distribution takes 4 days. Holley and colleagues (34, 35) did microbiological analysis of CO 2 -packaged retail-ready pork. They stored wrapped boneless pork loin roasts and slices in bulk at 4 C. Constant CO 2 concentrations of 50% and 100% were maintained for 1 or 2 weeks. In both treatments, levels of psy-

6 J. Food Prot., Vol. 62, No. 4 CENTRALIZED MEAT PACKAGING 423 chrotrophs, mesophils, and LAB were 10 4 CFU/cm 2 during the initial 2 weeks storage under CO 2. Enterobacteriaceae were 10 2 CFU/cm 2 in all samples, but Brochothrix spp. were one log higher in 50% CO 2 -stored samples than in 100% CO 2 -stored samples at 14 days. Holley and coworkers concluded that samples stored under 50% CO 2 and 100% CO 2 for 2 weeks could then be aerobically displayed without being unacceptable for 3 and 6 days, respectively. Earlier, Spahl and colleagues (59) and Greer and colleagues (31) also reported long shelf life of pork stored under CO 2 - saturated atmospheres. Jeremiah and colleagues (40) showed that a master-pack system maintaining high levels of CO 2, very low levels of O 2, and chill temperatures can extend the shelf life of pork up to 15 weeks. Holley and colleagues (36) examined the microbiological, biochemical, and physical characteristics of fresh pork loin slices packaged under 100% N 2, 100% CO 2,or50% N 2 50% CO 2 at storage temperatures of 1 or4 C in reusable, gas-impermeable metal boxes. They found that samples stored under N 2,CO 2, and N 2 -CO 2 atmospheres gave shelf lives of 18, 21, and 21 days, respectively, at 4 C. Shelf life was improved by 3 to 4 days at 1 C. They also concluded that physicochemical characteristics do not limit the shelf life of pork. Earlier, Gill (18) reported that during prolonged storage (20 to 24 weeks) under vacuum or CO 2, chilled red meats become very tender, lose desirable texture, and develop liver-like aged flavors highly objectionable to some consumers. Jeremiah and colleagues (41) studied the effect of prolonged storage under vacuum or CO 2 on the flavor and texture profiles of pork chilled at 1.5 C. They found that all vacuum-packaged samples showed 10 7 CFU/cm 2 of bacteria at 18 weeks. No adverse sensory changes were apparent until week 15, after which off-odors were noted (40, 41). For samples packaged under CO 2, the maximum number of LAB (10 5 CFU/cm 2 ) was obtained after 18 weeks; this figure was not exceeded even after 24 weeks storage. Samples stored for 6 and 21 weeks gave the highest flavor and texture scores. This study showed that pork is resistant to autolytic and oxidative deterioration during prolonged chilled storage in vacuum or CO 2. Thus, chilled pork could be stored up to 18 to 24 weeks at 1.5 C. Jeremiah and Gibson (39) studied the influence of different packaging atmospheres upon shelf life of retail-ready pork cuts. They used 100% N 2, 100% CO 2, and a mixture containing 70% O 2 and 30% CO 2. They suggested that 20 days of storage life would be enough time to prepare and distribute centrally packed retail-ready cuts to North American customers and yield satisfactory retail display. Tests were conducted at 1.5 C, 2 C, or 5 C storage in master packs for up to 28 days, followed by 30 h aerobic chilled display at 6.8 C. All three packaging atmospheres and storage temperatures yielded similar results, with some differences in texture and flavor. They concluded that storage life of those products was limited by growth of LAB and implied that using pork with low initial numbers of bacteria would yield consistent success in satisfying consumer quality requirements. Jeremiah and Gibson also concluded that any of the three atmospheres tested should be satisfactory for centralized distribution of retail-ready pork cuts. Storage temperatures of up to 5 C would be somewhat satisfactory, but consistent satisfactory performance would be best achieved using 100% CO 2 with storage at 1.5 C to retard LAB growth. DISTRIBUTION SYSTEMS FOR CENTRALLY PACKAGED RETAIL MEAT CUTS Although master-pack technology for centralized meat packaging exists, an efficient meat distribution system with strict temperature control is still needed to maximize product quality. Gill and Jones (22) studied the efficiency of a commercial process for storing and distributing vacuumpackaged beef. The researchers used a time temperature integration technique to assess the microbiological consequences of different temperature regimes. They collected and integrated appropriate product temperature histories with Gill s earlier models describing temperature s effects on the microbial growth (17). The data showed that product would achieve only about 25% of its potential storage life, on average, if it wasn t equilibrated near the optimum storage temperature before being loaded for transport (22). They used the models developed by Gill and colleagues (27) to assess the remaining storage life of chilled red meats from product temperature histories. Loading product for transport when its temperature was above the optimum affected storage life because refrigerated transport systems are designed to maintain product temperature, not reduce it (57). Gill and Jones (22) examined a typical North American vacuum-packaged beef handling process where a product temperature of 2 C was considered satisfactory (54); however, that temperature was not always achieved because speedy dispatch of product was a management priority. This rapid dispatch failed to properly control product temperature and provided only about 25% of the product s potential storage life. If product temperature is adequately controlled, such product can attain a storage life of about 12 weeks (23, 42). Woolfe (64) has given a detailed description of temperature monitoring and measurement techniques during meat distribution. He reported that liquid-n 2 -cooled vehicles were much quieter and had better temperature control than mechanically refrigerated vehicles. However, an adequate supply of liquid N 2 is required for shipping, which can limit the range and number of stops these trucks can make. Recently, Bailey (3) designed a refrigerated chamber using liquid N 2 for distributing centrally packaged retail meat cuts. He discussed the advantages of liquid N 2 as a refrigerant over mechanical systems, but also pointed out the liquid N 2 usage for maintaining the product temperature in a narrow range ( C) was not economically feasible. However, the fans he used to distribute liquid N 2 within the chamber may have generated heat and increased demand for the fluid. This work needs to be extended using different techniques for distributing liquid N 2 that do not generate unnecessary heat, that reduce liquid N 2 consumption, and that maintain the temperature in a narrow range ( C) to maximize potential shelf life. For brief airplane shipments, well-insulated containers filled with

7 424 TEWARI ET AL. J. Food Prot., Vol. 62, No. 4 chilled product (whose mass serves as refrigerant) may be all that is required to deliver satisfactory product. CONCLUSIONS AND RECOMMENDATIONS Researchers have shown that master packs are a promising technique for extending the shelf life of centrally packaged retail red meat cuts. However, there is no efficient distribution system available that provides the necessary temperature control. Liquid N 2 has the potential to maintain temperatures in the narrow range required and may be useful for truck-loaded product. However, we need an economic analysis of liquid N 2 s use in centralized meat distribution systems. A computer-based model could be developed to optimize uniform temperature distribution in master packs with minimum N 2 usage. Commercial evaluation of systems for both land and air transport of self-contained N 2 -refrigerated containers may solve the difficulties associated with maintaining optimal temperatures for fresh meat ( C) and fresh vegetables (5 to 7 C) in the same vehicle. Unitized refrigerated systems may serve as freshproduct inventory resources in remote retail locations. Also, adding antimicrobial, low-level radiation pretreatment and multiple barrier systems that limit microbial growth in addition to strict temperature control during storage, transportation, and distribution may increase the shelf life of fresh meat. Clearly, further research is needed in these areas. ACKNOWLEDGMENT We thank the Natural Sciences and Engineering Research Council of Canada for financial support. REFERENCES 1. Ayres, J. C Microbiological implications in handling, slaughtering and dressing meat animals. Adv. Food Res. 6: Ayres, J. C Temperature relationships and some other characteristics of the microbial flora developing on refrigerated beef. Food Res. 25: Bailey, C. G Design, fabrication, and testing of a returnable, insulated, nitrogen-refrigerated, controlled-atmosphere shipping container for distribution of fresh red meat. M.Sc. thesis. Department of Biosystems Engineering, University of Manitoba, Winnipeg, Manitoba, Canada. 4. Benedict, R. C., E. D. Strange, S. Palumbo, and C. E. Swift Use of in-package controlled atmospheres for extending the shelf life of meat products. J. Agric. Food Chem. 23: Blickstad, E., and G. Molin Carbon dioxide as a controller of the spoilage flora of pork, with special reference to temperature and sodium chloride. J. Food Prot. 46: Borch, E., M. L. Kant-Muermans, and Y. Blixt Bacterial spoilage of meat and cured meat products. Int. J. Food Microbiol. 33: Brody, A. L Integrating aseptic and modified atmosphere packaging to fulfill a vision of tomorrow. Food Technol. 50(4): Brown, W On the germination and growth of fungi at various temperatures and in various concentrations of oxygen and carbon dioxide. Ann. Bot. 36: Buys, E. M., J. Kruger, and G. L. Nortje The effect of centralised pre-packaging on the microbial, odor, color, and acceptability attributes of PVC-overwrapped pork loin chops, S8P02.wp. In Proceedings of the 39th meeting of the International Congress of Meat Science and Technology, Calgary, Alberta, Canada. 10. Buys, E. M., G. L. Nortje, and P. L. Steyn The effect of wholesale vacuum and 100% CO 2 storage on the subsequent microbiological, color and acceptability attributes of PVC-overwrapped pork loin chops. Food Res. Int. 26: Callow, E. H Gas storage of pork and bacon, I: preliminary experiments. J. Soc. Chem. Ind. 51:116T 119T. 12. Coulate, T. P Food: the chemistry of its components, 2nd ed. Royal Society of Chemistry, Cambridge, London. 13. Coyne, F. P The effect of carbon dioxide on bacterial growth. Proc. R. Soc., Ser B 113: Day, B. P. F A perspective of modified atmosphere packaging of fresh produce in Western Europe. Food Sci. Technol. Today 4(4): Eskin, N. A. M Biochemistry of foods, 2nd ed. Academic Press, San Diego, Calif. 16. Gill, C. O The control of microbial spoilage in fresh meats, p In A. M. Pearson and T. R. Dutson (ed.), Advances in meat research, vol. 2. Meat and poultry microbiology. AVI Publishing, Westport, Conn. 17. Gill, C. O Temperature function integration for hygiene evaluation of food processing procedures. Food Technol. Aust. 38: Gill, C. O CO 2 packaging the technical background, p In Proceedings of the 25th Meat Industry Research Conference, Meat Industry Institute of New Zealand, Hamilton, New Zealand. 19. Gill, C. O Packaging meat under CO 2 : the Captech system, p In Proceedings of Industry Day, 34th International Congress of Meat Science and Technology. Livestock and Meat Authority of Queensland, Brisbane, Australia. 20. Gill, C. O MAP and CAP of fresh, red meats, poultry and offals, p In J. M. Farber and K. L. Dodds (ed.), Principles of modified-atmosphere and sous vide product packaging. Technomic Publishing, Lancaster, Penn. 21. Gill, C. O., and J. C. L. Harrison The storage life of chilled pork packaged under carbon dioxide. Meat Sci. 26: Gill, C. O., and S. D. M. Jones Efficiency of a commercial process for the storage and distribution of vacuum-packaged beef. J. Food Prot. 55: Gill, C. O., and T. Jones The display life of retail-packaged beef steaks after their storage in master packs under various atmospheres. Meat Sci. 38: Gill, C. O., and C. McGinnis Changes in the microflora on commercial beef trimmings during their collection, distribution, and preparation for retail sale as ground beef. Int. J. Food Microbiol. 18: Gill, C. O., C. McGinnis, and A. K. W. Tong Consumer acceptance of display packs of beef stored under N 2 or CO 2 in master packs. Meat Sci. 38: Gill, C. O., and N. Penney The effect of initial gas volume to meat weight ratio on the storage life of chilled beef packaged under CO 2. Meat Sci. 22: Gill, C. O., D. M. Phillips, and J. C. L. Harrison A computer program for assessing the remaining storage life of chilled red meats from product temperature histories, p In Refrigeration for food and people. International Institute of Refrigeration, Paris. 28. Gill, C. O., and K. H. Tan Effect of carbon dioxide on growth of meat spoilage bacteria. Appl. Environ. Microbiol. 39: Grau, F. H Role of ph, lactate, and anaerobiosis in controlling the growth of some fermentative Gram-negative bacteria on beef. Appl. Environ. Microbiol. 42: Grau, F. H Microbial growth on fat and lean surfaces of vacuum-packaged chilled beef. J. Food Sci. 48: Greer, G. G., B. D. Dilts, and L. E. Jeremiah Bacteriology and retail case life of pork after storage in carbon dioxide. J. Food Prot. 43: Haines, R. B The influence of carbon dioxide preservation on the rate of multiplication of certain bacteria as judged by viable counts. J. Soc. Chem. Ind. 52:13T 17T. 33. Hintlian, C. B., and J. H. Hotchkiss The safety of modified atmosphere packaging: a review. Food Technol. 40(12): Holley, R. A., P. Delaquis, J. Gagnon, G. Doyon, and C. Gariepy.

8 J. Food Prot., Vol. 62, No. 4 CENTRALIZED MEAT PACKAGING Modified atmosphere packaging of fresh pork. Alimentech. 6(3): Holley, R. A., P. Delaquis, N. Rodrigue, G. Doyon, J. Gagnon, and C. Gariepy Controlled-atmosphere storage of pork under carbon dioxide. J. Food Prot. 57: Holley, R. A., C. Gariepy, P. Delaquis, G. Doyon, and J. Gagnon Static, controlled (CO 2 ) atmosphere packaging of retail ready pork. J. Food Sci. 59: Igbinedion, J. E., V. R. Cahill, H. W. Ockerman, N. E. Parrett, and B. D. Vanstavern Effects of packaging method, display light, and storage time on the microbial growth and rancidity of fresh pork. J. Food Sci. 48: International Commission on Microbiological Specifications for Foods (ICMSF) Microbial ecology of foods factors affecting life and death of microorganisms, vol. 1. Academic Press, London. 39. Jeremiah, L. E., and L. L. Gibson The influence of controlled atmosphere storage on the flavor and texture profiles of display-ready pork cuts. Food Res. Int. 30: Jeremiah, L. E., C. O. Gill, and N. Penney The effects on pork storage life of oxygen contamination in nominally anoxic packaging. J. Muscle Food 3: Jeremiah, L. E., N. Penney, and C. O. Gill The effects of prolonged storage under vacuum or CO 2 on the flavor and texture profiles of chilled pork. Food Res. Int. 25: Johnson, B. Y Chilled vacuum-packaged beef. C.S.I.R.O. (Aust.) Res. Q. 34: Kidd, F., and C. West Gas storage of fruit. Food investigation special report no. 30. Department of Science and Industry Research, UK. 44. Killefer, D. H Carbon dioxide preservation of meat and fish. Ind. Engl. Chem. 22: Kraft, A. A Meat microbiology, p In R. J. Betchel (ed.), Muscle as food. Academic Press, London. 46. Labuza, T. P An introduction to active packaging of foods. Food Technol. 50(4): Moran, T., E. C. Smith, and R. G. Tomkins The inhibition of mould growth on meat by CO 2. J. Soc. Chem. Ind. 51:114T 116T. 48. Offer, G. I., and P. Knight The structural basis of water-holding in meat, 1: general principles and water uptake in meat processing, p In R. Lawrie (ed.), Developments in meat science, vol. 4. Elsevier Applied Science, Essex, England. 49. Ogilvy, W. S., and J. S. Ayres Post morten changes in stored meats, II: the effect of atmospheres containing CO 2 in prolonging the storage life of cut-up chicken. Food Technol. 5: Oraikul, B., and M. E. Stiles (ed.) Modified atmosphere packaging of foods. Ellis Harwood Limited, West Sussex, England. 51. Parry, R. T Introduction, p In R. T. Parry (ed.), Principles and applications of modified atmosphere packaging of foods. Chapman & Hall, Glasgow, Scotland. 52. Penny, N., and R. G. Bell Effect of residual oxygen on the colour, odour and taste of carbon dioxide-packaged beef, lamb and pork during short term storage at chill temperatures. Meat Sci. 33: Roth, L. A., and D. S. Clark Studies on the bacterial flora of vacuum-packaged fresh beef. Can. J. Microbiol. 18: Savell, J. W Packaging, transportation, and distribution of edible meat byproducts, p In A. M. Pearson and T. R. Dutson (ed.), Advances in meat research, vol. 5. Elsevier Applied Science, London. 55. Scholtz, E. M., E. Jordaan, J. Kruger, G. L. Nortje, and R. T. Naude The influence of different centralised pre-packaging systems on the shelf life of fresh pork. Meat Sci. 32: Scott, V. N Interaction of factors to control microbial spoilage of refrigerated foods. J. Food Prot. 52: Scrine, G. R Refrigerated vehicles what next? p In Long distance refrigerated transport: land and sea. International Institute of Refrigeration, Paris. 58. Shay, B. J., and A. F. Egan The packaging of chilled red meats. Food Technol. Aust. 38(5): Spahl, A., G. Reineccius, and S. Tatini Storage life of pork chops in CO 2 -containing atmospheres. J. Food Prot. 44: Stiles, M. E Modified atmosphere packaging of meat, poultry, and their products, p In B. Oraikul and M. E. Stiles (ed.), Modified atmosphere packaging of foods. Ellis Horwood Limited, West Sussex, UK. 61. Taylor, A. A Developments in fresh meat technology, p In Proceedings of the 36th International Congress on Meat Science and Technology, Havana, Cuba. 62. Tomkins, R. G The inhibition of the growth of meat attacking fungi by carbon dioxide. J. Soc. Chem. Ind. 51:261T 264T. 63. Vanderzant, C., J. W. Savell, M. O. Hanna, and V. Potluri A comparison of growth of individual meat bacteria on the lean and fatty tissues of beef, pork and lamb. J. Food Sci. 51: Woolfe, M. L Temperature monitoring and measurement, p In C. Dennis and M. Stringer (ed.), Chilled foods: a comprehensive guide. Ellis Harwood, West Sussex, UK.

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