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Microbiological and organoleptic qualities of vacuum-packaged ground beef prepared from pasteurized manufacturing beef
International Journal of Food Microbiology 74 (2002) 111 – 118 www.elsevier.com/locate/ijfoodmicro
Microbiological and organoleptic qualities of vacuum-packaged ground beef prepared from pasteurized manufacturing beef C.O. Gill*, M. Badoni Agriculture and Agri-Food Canada Lacombe Research Centre, 6000 C&E Trail, Lacombe, Alberta, Canada T4L 1W1 Received 18 July 2001; received in revised form 5 October 2001; accepted 19 October 2001
Abstract Manufacturing beef was pasteurized by immersion in water of 85 °C for 60 s, or was not pasteurized before being coarsely ground. The coarsely ground beef was vacuum-packaged and stored at 2 °C for up to 6 weeks. Before storage and at weekly intervals, three packs of pasteurized and three of unpasteurized beef were opened. The meat from each pack was finely ground and displayed in two overwrapped packs at 4 °C for 3 days after storage for up to 3 weeks, or for 2 days after longer storage times. Samples for microbiological analysis were obtained at the times of preparation of display packs and at the end of display. Displayed meat was assessed daily for colour, discolouration and retail acceptability, and for odour intensity and acceptability at the end of display. Before storage, the numbers of total aerobic bacteria, presumptive pseudomonads and presumptive Brochothrix thermosphacta recovered from pasteurized meat were >1 log unit less than the corresponding numbers recovered from unpasteurized meat, but the numbers of presumptive lactic acid bacteria and presumptive enterobacteria were < 1 log unit less from pasteurized than from unpasteurized meat. After all periods of storage and display, the numbers of bacteria recovered from pasteurized and unpasteurized meat at each time were mostly similar. The colour of pasteurized meat was perceived as being paler than that of unpasteurized meat, but discolouration and retail acceptability of pasteurized and unpasteurized meat were perceived as similar at most times. The odours of displayed, pasteurized and unpasteurized meat were perceived to be similar at all times that odours were assessed. The findings indicate that pasteurizing of manufacturing beef to improve the microbiological safety of ground beef would not unacceptability degrade the appearance of the ground product, but that the storage life of ground beef would not be greatly extended by the treatment. Crown Copyright D 2002 Published by Elsevier Science B.V. All rights reserved. Keywords: Manufacturing beef; Pasteurizing; Grinding; Vacuum packaging
1. Introduction Ground beef is prepared from manufacturing beef which is comprised of both trimmings from beef cattle carcasses and large portions from the carcasses of culled cows. Because of concerns about the microbiological safety of beef, particularly ground beef and pro*
Corresponding author. Tel.: +1-403-782-8113; fax: +1-403782-6120. E-mail address: [email protected] (C.O. Gill).
ducts prepared from it, most large beef packing plants in North America have installed equipment for pasteurizing dressed carcass sides with steam or hot water. Such equipment can be operated to largely remove generic Escherichia coli and, presumably, associated enteric pathogens from the meat (Gill and Bryant, 2000; Nutsch et al., 1997). However, most of the manufacturing beef produced from pasteurized carcasses continues to be contaminated with substantial numbers of generic E. coli, while Salmonella is recovered relatively frequently, and E. coli O157:H7 is recovered
0168-1605/02/$ - see front matter Crown Copyright D 2002 Published by Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 6 0 5 ( 0 1 ) 0 0 7 3 6 - X
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occasionally from the product (Anonymous, 2001; Scanga et al., 2000). Although some of the enteric organisms found on manufacturing beef may be survivors of ineffective pasteurizing treatments (Nutsch et al., 1998), most probably originate from bacterial populations that persist in carcass breaking equipment despite routine cleaning that is thought to be adequate by both plant staff and regulatory authorities (Gill et al., 1999a; Gill and McGinnis, 2000). In those circumstances, assurance of the microbiological condition of carcasses cannot and does not assure the microbiological safety of manufacturing beef and raw products prepared from it. Instead, some decontaminating treatment of manufacturing beef or of finished products seems to be required. In view of the efficacy of pasteurizing treatments for carcasses, pasteurizing of manufacturing beef is an obvious treatment to consider. For pasteurizing with hot water, it has been shown that treatment of manufacturing beef with water of >80 °C for about 60 s is necessary (Gill and Badoni, 1997a), whereas with carcasses, water of the same temperature need be applied for only 10 s (Gill et al., 1999b). Despite the relatively severe treatment needed for manufacturing beef, the eating qualities of frozen hamburger patties prepared from pasteurized product were found to be indistinguishable from those of patties prepared from unpasteurized product (Gill et al., 2001). The treatment may, however, affect other qualities of comminuted beef that are important for the commercial performance of products different from frozen hamburger patties. Much of the ground beef now offered for retail sale is prepared at retail stores by fine grinding of product which was coarsely ground and vacuum-packaged at packing plants. To discern whether pasteurized manufacturing beef might be used for ground beef prepared and traded in those manners, the microbiological and organoleptic qualities of stored, vacuum-packaged, coarsely ground beef and displayed, finely ground beef prepared from it were examined.
2. Materials and methods 2.1. Vacuum-packaged, coarsely ground beef A 100-kg lot of manufacturing beef with a lean content of approximately 80% was obtained from a
beef packing plant. The lot was collected during a period of about 30 min from pieces of meat on a conveyor belt as they arrived at a packing station. Selected pieces weighed between 700 and 1000 g, with surface areas between 400 and 700 cm2. The meat was cooled by the addition of carbon dioxide snow, as in usual, commercial practice, and was processed within 2 h of being collected. Each piece of meat in the lot was divided in two, with each part being assigned to a different one of two batches, to obtain two batches of similar weights and compositions. The meat from one batch was pasteurized. For pasteurizing, groups of five or six pieces of meat were placed without touching in a wire mesh basket with a securable lid. The lidded basket was immersed in water of 85°C for 60 s (Gill and Badoni, 1997a). The meat in the second batch was not pasteurized. The pasteurized meat was ground through a plate with 9-mm holes in a grinder head that had been cleaned and immersed in boiling water for 5 min before it was used. Subsequently, the unpasteurized meat was ground through the same plate. The batches of meat were separately collected and mixed by hand, with the use of sterile gloves. Each batch of ground meat was divided into 24 portions, each of 2 kg. Each portion was vacuumpacked in a pouch that measured 300 150 mm (l w), which was made of a polyvinyledene chloride laminate that has an oxygen transmission rate of about 40 cc/m2/24 h/atm at 25 °C and 100% r.h. (Cryovac, Mississauga, ON, Canada). All packs were stored at 2 F 0.5 °C. 2.2. Retail-packaged, finely ground beef At the time that vacuum packs of coarsely ground meat were prepared and at weekly intervals up to 6 weeks, three vacuum packs of pasteurized and three of unpasteurized meat were selected at random and were withdrawn from storage. The meat in each pack was ground through a plate with 3-mm holes, with the grinder head being cleaned and placed in boiling water for 5 min before the grinding of the meat from each pack, and with the separate collection of each portion of meat. Six samples of 5 g were obtained from each finely ground portion immediately after grinding, and were combined to give a 30-g composite sample. Then, meat
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from each portion was used to fill each of two, solid polystyrene trays, which measured 210 150 25 mm (l w h), with about 400 g of finely ground meat. The trays were overwrapped with a stretchable film that has an oxygen transmission rate of 8000 cc/ m2/24/atm at 25 °C and 75% r.h. (Vitafilm Choice Wrap, Goodyear Canada, Toronto, ON, Canada). The overwrapped trays were placed on the sole, horizontal shelf of a chest-type display case (model LPM 12 T, Hill Refrigeration, Barrie, ON, Canada) that was illuminated for 12 h/day by incandescent lights which gave a light intensity of 750 lux at the shelf surface. The mean temperature of the air in the vicinity of the displayed meat was 4 F 1 °C. The meat in each display pack was assessed for colour, discolouration and retail acceptability at the time of packing and at daily intervals, up to 3 days for meat stored in vacuum pack up to 3 weeks, but up to 2 days for meat stored in vacuum packs for 4, 5 or 6 weeks. After assessment of the appearance on the third or second day, each pack was opened and the odour intensity and acceptability were assessed. Three samples, each of 5 g, were then obtained from the meat in each tray, and samples from each pair of trays that contained meat from the same portion were combined to give a 30-g composite sample.
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Streptomycin Thallous Acetate Actidione Agar (STAA; Gardner, 1966), which were incubated at 25 °C for 2 days for the enumeration of Brochothrix thermosphacta. 2.4. Organoleptic analysis All assessments were made by an experienced, fivemember panel (Jeremiah and Gibson, 2000). Colour was assessed on an eight-point scale, where 1 = white, 2 = pale pink, 3 = pink, 4 = pale red, 5 = bright red, 6 = slightly dark red, 7 = moderately dark red, 8 = very dark red. Discolouration was assessed on a seven-point scale, where 1 = no discolouration, 2 = 1 –10% discolouration, 3 = 11 – 15% discolouration, 4 = 26 – 50% discolouration, 5 = 51 – 75% discolouration, 6 = 76 – 99% discolouration and 7 = completely discoloured. Retail acceptability was assessed on a seven-point scale, where 1 = very undesirable, 2 = undesirable, 3 = slightly undesirable, 4 = neither undesirable nor desirable, 5 = slightly desirable, 6 = desirable and 7 = very desirable. Off odour intensity was assessed on a fourpoint scale, where 1 = no off odour, 2 = slight off odour, 3 = moderate off odour and 4 = strong off odour. Odour acceptability was assessed on a five-point scale, where 1 = acceptable, 2 = slightly acceptable, 3 = neither acceptable nor unacceptable, 4 = slightly unacceptable and 5 = unacceptable.
2.3. Microbiological analysis 2.5. Analysis of data Each composite sample obtained from meat before or after display was placed in a stomacher bag with 270 ml of 0.1% (w/v) peptone water. After stomaching for 2 min, the fluid from the bag was filtered through four layers of sterile cheese cloth. Suitable 10-fold dilutions were prepared in 0.1% (w/v) peptone water and were spread on duplicate plates of: Plate Count Agar (PCA; Difco Laboratories, Detroit, MI, USA), which were incubated at 25 °C for 3 days for the enumeration of total aerobic bacteria; deMan, Rogosa and Sharpe Agar (MRS; Difco), which were incubated anaerobically at 25 °C for 3 days for the enumeration of lactic acid bacteria; Violet Red Bile Glucose Agar (VRBG; Difco), which were incubated at 30 °C for 2 days for the enumeration of Enterobacteriaceae; Cephaloridine Fucidin Cetrimide Agar (CFC; Difco) which were incubated at 25°C for 2 days for the enumeration of pseudomonads; and
All bacterial counts were transformed to log values. The means of the log values for the counts obtained for each group or species of bacteria, from pasteurized or unpasteurized product at each sampling time were plotted. Mean values for each type of organoleptic score obtained on each day of display from pasteurized or unpasteurized product that had been stored for the same time were separated using the Tukey option of the General Linear Model (GLM) procedure in Statistical Analysis Systems (SAS) version 6 (SAS Institute, Cary, NC, USA). Pairs of mean values for odour scores obtained at the end of display for pasteurized or unpasteurized meat that had been stored for the same time were separated by a t-test for paired comparisons, using the PROC MEANS procedure in SAS, version 6.
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3. Results At the time of vacuum packaging, the numbers of total aerobic bacteria and of presumptive pseudomonads and B. thermosphacta recovered from pasteurized meat were each >1 log unit less, but the numbers of presumptive lactic acid bacteria and enterobacteria were each only about 0.5 log unit less than the numbers of the same bacteria recovered from unpasteurized meat (Fig. 1). After storage of unpasteurized meat at 2 °C for 1 week, and before as well as after storage of pasteurized meat, the numbers of total aerobic bacteria and of presumptive lactic acid bacteria recovered from each sample were similar. The counts of those organisms were near or at their maximum numbers after storage of both types of meat for 3 weeks. With unpasteurized meat, the numbers of enterobacteria increased during the first 2 weeks of storage, but
Fig. 2. Numbers of total aerobic bacteria (6) and presumptive lactic acid bacteria (.), enterobacteria (5), pseudomonads (n) and B. thermosphacta (D) recovered from finely ground manufacturing beef that was displayed at 4 °C for 3 (—) or 2 days (- - -) after being prepared from vacuum-packaged, coarsely ground beef that was stored at 2 °C after being prepared from (A) unpasteurized or (B) pasteurized manufacturing beef.
Fig. 1. Numbers of total aerobic bacteria (6) and presumptive lactic acid bacteria (.), enterobacteria (5), pseudomonads (n) and B. thermosphacta (D) recovered from vacuum-packaged, coarsely ground beef stored at 2 °C after being prepared from (A) unpasteurized or (B) pasteurized manufacturing beef.
changed little thereafter; and the numbers of pseudomonads increased between weeks 1 and 2 of storage, to numbers that were similar to those of the enterobacteria. With pasteurized meat, the numbers of enterobacteria increased greatly during the first 3 weeks of storage, but changed little thereafter; and the numbers of pseudomonads also increased during the first 3 weeks, to numbers that were similar to those of the enterobacteria. With both types of meat the numbers of B. thermosphacta increased during the first 3 weeks of storage, and then declined during the following weeks. The maximum numbers attained by each of the three groups of organisms on both types of meat were similar. With unpasteurized meat that had not been stored, the total aerobic bacteria increased to 7 log cfu/g after display for 3 days at 4 °C (Fig. 2). At that time, the numbers of lactic acid bacteria, psuedomonads and B. thermosphacta were all about 6 log cfu/g, while
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Table 1 Means of the scores recorded by a five-member panel for the colours of displayed, finely ground beef derived from stored, vacuum-packaged, coarsely ground beef which had been prepared from unpasteurized (U) or pasteurized (P) manufacturing beef Storage time (weeks)
0 1 2 3 4 5 6
Mean scores for colour Displayed 0 day
Displayed 1 day
Displayed 2 days
Displayed 3 days
U
P
U
P
U
P
U
P
5.0C 4.9BC 5.1B 4.1B 4.2B 3.8A 4.1B
4.2A 4.3AB 4.6AB 3.8B 3.8AB 3.4A 4.3B
5.0C 5.0BC 5.0B 3.9B 3.6AB 3.9A 2.0A
4.3A 4.5ABC 3.9A 2.8A 3.1A 3.5A 2.8A
5.2C 5.3C d d d d d
4.4AB 3.9A d d d d d
6.2D d d d – – –
4.9B d d d – – –
Scores were 1 = white, 2 = pale pink, 3 = pink, 4 = pale red, 5 = bright red, 6 = slightly dark red, 7 = dark red, 8 = very dark red. d = discolouration too extensive for the meat colour to be assessed. ( – ) Meat not assessed. Values on the same line with the same letter are not significantly different ( P >0.05).
numbers of enterobacteria were about 4.5 log cfu/g. With pasteurized meat that had not been stored, the total aerobic bacteria increased to about 6.5 log cfu/g after display for 3 days at 4 °C. At that time, the numbers of pseudomonads were similar to the numbers of the total aerobic bacteria, while the numbers of lactic acid bacteria, B. thermosphacta and enterobacteria were all < 6 log cfu/g. With both types of meat stored at 2 °C for 1 week or more then displayed at 4 °C, the numbers of total aerobic bacteria and lactic acid bacteria recovered were about 8.5 and 8.0 log cfu/g, respectively, after all times of storage and display (Fig. 2). The numbers of pseudomonads recovered from both types of meat that had
been stored for 1 or 2 weeks, then displayed, were about 7 log cfu/g, but the numbers on meat that had been stored for 3 weeks or longer, then displayed, were < 5 log cfu/g. The numbers of enterobacteria on unpasteurized or pasteurized meat that had been stored for 1 or 2 weeks then displayed were >4 or >6 log cfu/ g, respectively. For meat stored for 2 weeks or more then displayed, the numbers of enterobacteria and pseudomonads were similar at each time of storage and display. With unpasteurized meat, the numbers of B. thermosphacta were >5 and < 4 log cfu/g, after display following storage for < 2 weeks and >3 weeks, respectively. With pasteurized meat, the numbers of B. thermosphacta were 7 log cfu/g after storage for 2
Table 2 Means of the scores recorded by a five-member panel for the discolouration of displayed, finely ground beef derived from stored, vacuumpackaged, coarsely ground beef which had been prepared from unpasteurized (U) or pasteurized (P) manufacturing beef Storage time (weeks)
0 1 2 3 4 5 6
Mean scores for colour Displayed 0 day
Displayed 1 day
Displayed 2 days
Displayed 3 days
U
P
U
P
U
P
U
P
1.0A 1.1A 1.1A 1.0A 1.0A 1.0A 1.9A
1.2A 1.3A 1.0A 1.0A 1.0A 1.1A 1.8A
1.1A 1.4B 3.6B 4.8C 4.5C 3.6C 5.7C
1.2A 1.5B 3.3B 3.4B 2.9B 2.8B 4.8B
2.0B 3.1C 6.8D 7.0D 6.9D 6.9D 7.0D
2.0B 3.1C 6.2C 6.8D 6.3D 6.9D 7.0D
4.1D 6.6D 7.0D 7.0D – – –
3.6C 6.6C 6.8D 7.0D – – –
Scores were 1 = no discolouration, 2 = 1 – 10% discolouration, 3 = 11 – 25% discolouration, 4 = 26 – 50% discolouration, 5 = 51 – 75% discolouration, 6 = 76 – 99% discolouration, 7 = wholly discoloured. ( – ) Meat not assessed. Values on the same line with the same letter are not significantly different (P >0.05).
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Table 3 Means of the scores recorded by a five-member panel for the retail acceptability of displayed, finely ground beef derived from stored, vacuumpackaged, coarsely ground beef which had been prepared from unpasteurized (U) or pasteurized (P) manufacturing beef Storage time (weeks)
0 1 2 3 4 5 6
Mean scores for acceptability Displayed 0 day
Displayed 1 day
Displayed 2 days
Displayed 3 days
U
P
U
P
U
P
U
P
6.6A 6.5A 6.5A 5.7A 6.0A 5.0A 4.3A
6.2AB 6.3A 6.2A 5.2A 5.6A 4.8A 4.1A
6.4A 5.7B 2.4C 2.1B 2.1C 2.7B 1.3B
5.8B 5.5B 3.1B 2.6B 2.8B 3.1B 1.4B
4.7C 3.2C 1.0D 1.0C 1.0D 1.0C 1.0B
4.6C 3.1C 1.1D 1.0C 1.0D 1.0C 1.0B
2.2E 1.0D 1.0D 1.0C – – –
2.9D 1.0D 1.0D 1.0C – – –
Scores were 1 = very undesirable, 2 = undesirable, 3 = slightly undesirable, 4 = neither undesirable nor desirable, 5 = slightly desirable, 6 = desirable, 7 = very desirable. ( – ) Meat not assessed. Values on the same line with the same letter are not significantly different (P >0.05).
weeks and display, but < 3 log cfu/g after storage for 3 or more weeks and display. When meat was not stored before display, meat colours could be discerned on all days up to and including the third day of display (Table 1). However, after storage for 1 week or more, discolouration was too extensive for colours to be assessed on the third or second day of display, respectively. For meat stored for up to 5 weeks, after most times of display, some panelists perceived the colour of unpasteurized meat to be darker than that of pasteurized meat stored and displayed for the same times. However, the mean differences were mostly small and sometimes not significant ( P > 0.05). When meat was first displayed after storage for up to 5 weeks, there was little discolouration of either unpasteurized or pasteurized meat (Table 2). After display for 1 day of meat that had not been stored or stored for 1 week, discolouration of both unpasteurized and pasteurized meat was little and similar; but meat displayed for 1 day after storage for 2 or more weeks was extensively discoloured by browning, with discolouration being more extensive on unpasteurized than pasteurized meat that had been stored for the same time. When meat was first displayed without being stored or after storage for 1 or 2 weeks, both unpasteurized and pasteurized meat was assessed as very desirable or desirable, although the higher score was assigned more frequently to unpasteurized than to pasteurized meat (Table 3). When meat was stored and/or displayed for
longer times, scores for retail acceptability were progressively lower. All meat displayed for 3 days was assessed as slightly or more undesirable. When the odours of meat that had not been stored or stored for 1 or 2 weeks were assessed after display for 3 days, off odours were assessed as being of slight or moderate intensity and neither acceptable nor unacceptable or slightly unacceptable. At those times, the mean scores for odour intensity for unpasteurized and pasteurized meat stored and displayed for the same times were not significantly different ( P > 0.05), but the mean scores for odour acceptability were significantly larger ( P < 0.05) for unpasteurized than for pasteurized meat. Odours of meat that had been stored and/or displayed for longer times were assessed as being moderate or strong and slightly or more unacceptable. At those times, the mean scores for odour intensity or acceptability for unpasteurized and pasteurized meat stored and displayed for the same times were not significantly different ( P > 0.05).
4. Discussion Coarsely ground beef prepared at packing plants is often cooled to about 0 °C by the addition of carbon dioxide snow to the meat during grinding, and such temperatures are often maintained during the subsequent transportation of the product (Gill et al., 2002a). However, at retailers’ warehouses and retail stores in Canada, and probably elsewhere in North America,
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the median temperatures of meat are about 2 °C, while the median temperature of displayed meat is about 4 °C (Gill et al., 2002b). Therefore, in investigating the possible effects of pasteurizing on the storage performance of ground beef, the meat was stored and displayed at 2 °C and 4 °C, respectively. Ground meat is generally distributed from packing plants relatively rapidly, with the median age of the product being 8 days at the time it is prepared for retail sale (Gill et al., 2002a). However, the time that coarsely ground meat is stored in vacuum packs can extend to several weeks. Therefore, in this study, the vacuumpackaged product was stored for up to 6 weeks. As was found in previous studies, pasteurizing reduced the numbers of total aerobic bacteria recovered from meat by more than an order of magnitude (Gill et al., 2001a), and the reductions in the numbers of presumptive pseudomonads and B. thermosphacta were similar. However, the numbers of presumptive lactic acid bacteria and enterobacteria recovered were reduced by less than an order of magnitude. The apparent reduction in numbers of enterobacteria might be misleading, as few were recovered before, and very few were recovered after pasteurizing, while pasteurizing has been previously found to reduce the numbers of coliforms on meat by about two orders of magnitude (Gill et al., 2001). However, it is evident that the presumptive lactic acid bacteria were less affected by the pasteurizing treatment than the other groups of organisms, and consequently were predominant in the flora of pasteurized meat at all times instead of only at later storage times, as in the unpasteurized meat. Despite that, the behaviors of the other groups of organisms on pasteurized and unpasteurized meat were broadly similar, with all three reaching maximum numbers by the third week of storage. The increases in numbers of presumptive pseudomonads might, however, be misleading as the strictly aerobic pseudomonads would be expected to grow little or not at all in vacuum packs (Gill and Molin, 1991), while the coincident numbers of presumptive pseudomonads and enterobacteria recovered from both types of meat at later storage times suggests that enterobacteria, as well as surviving pseudomonads, were enumerated on CFC (Mead, 1985). After display without storage or following storage for 1 week, the numbers of presumptive pseudomonads recovered from both pasteurized and unpasteur-
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ized meat greatly exceeded the numbers of presumptive enterobacteria recovered at those times. Thus, pseudomonads evidently grew to form major fractions of the flora when both pasteurized and unpasteurized meat were displayed after no or a short period of storage. However, after 2 weeks of storage, with the flora on the stored meat approaching maximum numbers, growth of enterobacteria accompanied or surpassed the growth of pseudomonads, while little growth of either group of organisms would seem to have occurred during the display of pasteurized or unpasteurized meat that had been stored for 3 weeks or more. Only with B. thermosphacta recovered from displayed meat that was not stored or had been stored for 2 weeks before display, were the numbers from pasteurized and unpasteurized meat very different. It would appear then that pasteurizing of manufacturing beef would not greatly extend the time before the onset of microbial spoilage in vacuum-packaged beef prepared from it, nor greatly delay the onset of microbial spoilage in ground meat displayed after storage in vacuum packs. The finding that off-odours of similar intensities were apparent at the same times in pasteurized and unpasteurized meat, with the odours of pasteurized meat being somewhat more acceptable after the shorter periods of storage, is in agreement with that conclusion. Pasteurizing discolours the surfaces of meat pieces by bleaching much and browning some of the muscle tissue (Gill and Badoni, 1997b). Because of the bleached tissue, the ground beef prepared from pasteurized product was perceived as being of lighter colour than the ground beef prepared from unpasteurized product, while flecks of browned tissue were perceived in some ground beef prepared from pasteurized, but not in ground beef prepared at the same time from unpasteurized tissue. Despite these differences, the retail acceptabilities of ground beef prepared from pasteurized and unpasteurized product were similar, while brown discolouration developed at the same rate or more slowly in ground beef prepared from pasteurized, than in that prepared from unpasteurized product. A somewhat later development of extensive browning in ground beef prepared from pasteurized product may be a consequence of the modest differences in the numbers and compositions of the spoilage flora on the two types of meat (Faustman et al., 1990).
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The extent to which the colour of ground beef is lightened and discoloured because of pasteurizing of the product from which it is prepared will vary with the sizes of pieces of meat in batches of manufacturing beef, as the surface area, and so the amount of tissue denatured during pasteurizing will be relatively large in relation to the meat mass when meat pieces are small. Lightening of colour and discolouration of ground beef as a result of pasteurizing manufacturing beef could then be more or less than the change of colour and discolouration perceived in this study. However, the findings of this study suggest that the effects on ground beef appearance of the pasteurizing of manufacturing beef would, generally, be too small to affect its appeal to consumers. Therefore, pasteurizing of manufacturing meat might well be a commercially viable means of substantially enhancing the microbiological safety, although probably not the storage stability of ground beef.
Acknowledgements We thank Ms. M. Brockway for technical assistance, and the Alberta Agricultural Research Institute for financial support of the study.
References Anonymous, 2001. News: little E. coli. Meat Processing, March 10. Faustman, C., Johnson, J.L., Cassens, R.G., Doyle, M.P., 1990. Color reversion in beef. Fleischwirtschaft 70, 676 – 679. Gardner, G.A., 1966. A selective medium for the enumeration of Microbacterium thermosphactum in meat and meat products. Journal of Applied Bacteriology 29, 455 – 460. Gill, C.O., Badoni, M., 1997a. The hygienic and organoleptic qualities of ground beef prepared from manufacturing beef pasteurized by immersion in hot water. Meat Science 46, 67 – 75. Gill, C.O., Badoni, M., 1997b. The effects of hot water pasteurizing treatments on the appearances of pork and beef. Meat Science 46, 77 – 87.
Gill, C.O., Bryant, J., 2000. The effects on product of a hot water pasteurizing treatment applied routinely in a commercial beef carcass dressing process. Food Microbiology 17, 495 – 504. Gill, C.O., McGinnis, J.C., 2000. Contamination of beef trimmings with Escherichia coli during a carcass breaking process. Food Research International 33, 125 – 130. Gill, C.O., Molin, G., 1991. Modified atmospheres and vacuum packaging. In: Russel, N.J., Gould, G.W. (Eds.), Food Preservatives. Blackie Academic, Glasgow, pp. 172 – 199. Gill, C.O., Badoni, M., McGinnis, J.C., 1999a. Assessment of the adequacy of cleaning of equipment used for breaking beef carcasses. International Journal of Food Microbiology 46, 1 – 8. Gill, C.O., Bryant, J., Bedard, D., 1999b. The effects of hot water pasteurizing treatments on the appearances and microbiological conditions of beef carcass sides. Food Microbiology 16, 281 – 289. Gill, C.O., Bryant, J., Badoni, M., 2001. Effects of hot water pasteurizing treatments on the microbiological condition of manufacturing beef used for hamburger patty manufacture. International Journal of Food Microbiology 63, 243 – 256. Gill, C.O., Jones, T., Rahn, K., Campbell, S., LeBlanc, D.I., Holley, R.A., Stark, R., 2002a. Temperatures and ages of boxed beef packed and distributed in Canada. Meat Science, 60 (in press). Gill, C.O., Jones, T., LeBlanc, D.I., Rahn, K., Campbell, S., Holley, R.A., Stark, R., Houde, A., 2002b. Temperatures and ages of packs of beef displayed at stores in Canada. Meat Science (in press). Jeremiah, L.E., Gibson, L.L., 2000. The display performance of retail-ready beef following storage: muscle influences. Journal of Muscle Foods 11, 273 – 291. Mead, G.C., 1985. Enumeration of pseudomonads using cephaloridin – fucidin – cetrimide agar (CFC). International Journal of Food Microbiology 2, 21 – 26. Nutsch, A.L., Phebus, R.K., Riemann, M.J., Schafer, D.E., Boyer Jr., J.E., Wilson, R.C., Leising, J.D., Kastner, C.L., 1997. Evaluation of a steam pasteurization process in a commercial beef processing facility. Journal of Food Protection 60, 485 – 492. Nutsch, A.L., Phebus, R.K., Riemann, M.J., Kotrola, J.S., Wilson, R.C., Boyer Jr., J.E., Brown, T.L., 1998. Steam pasteurization of commercially slaughtered beef carcasses: evaluation of bacterial populations at five anatomical locations. Journal of Food Protection 61, 571 – 577. Scanga, J.A., Grona, A.D., Belk, K.E., Sofos, J.N., Bellinger, G.R., Smith, G.C., 2000. Microbiological contamination of raw beef trimmings and ground beef. Meat Science 56, 145 – 152.
Microbiological and organoleptic qualities of vacuum-packaged ground beef prepared from pasteurized manufacturing beef C.O. Gill*, M. Badoni Agriculture and Agri-Food Canada Lacombe Research Centre, 6000 C&E Trail, Lacombe, Alberta, Canada T4L 1W1 Received 18 July 2001; received in revised form 5 October 2001; accepted 19 October 2001
Abstract Manufacturing beef was pasteurized by immersion in water of 85 °C for 60 s, or was not pasteurized before being coarsely ground. The coarsely ground beef was vacuum-packaged and stored at 2 °C for up to 6 weeks. Before storage and at weekly intervals, three packs of pasteurized and three of unpasteurized beef were opened. The meat from each pack was finely ground and displayed in two overwrapped packs at 4 °C for 3 days after storage for up to 3 weeks, or for 2 days after longer storage times. Samples for microbiological analysis were obtained at the times of preparation of display packs and at the end of display. Displayed meat was assessed daily for colour, discolouration and retail acceptability, and for odour intensity and acceptability at the end of display. Before storage, the numbers of total aerobic bacteria, presumptive pseudomonads and presumptive Brochothrix thermosphacta recovered from pasteurized meat were >1 log unit less than the corresponding numbers recovered from unpasteurized meat, but the numbers of presumptive lactic acid bacteria and presumptive enterobacteria were < 1 log unit less from pasteurized than from unpasteurized meat. After all periods of storage and display, the numbers of bacteria recovered from pasteurized and unpasteurized meat at each time were mostly similar. The colour of pasteurized meat was perceived as being paler than that of unpasteurized meat, but discolouration and retail acceptability of pasteurized and unpasteurized meat were perceived as similar at most times. The odours of displayed, pasteurized and unpasteurized meat were perceived to be similar at all times that odours were assessed. The findings indicate that pasteurizing of manufacturing beef to improve the microbiological safety of ground beef would not unacceptability degrade the appearance of the ground product, but that the storage life of ground beef would not be greatly extended by the treatment. Crown Copyright D 2002 Published by Elsevier Science B.V. All rights reserved. Keywords: Manufacturing beef; Pasteurizing; Grinding; Vacuum packaging
1. Introduction Ground beef is prepared from manufacturing beef which is comprised of both trimmings from beef cattle carcasses and large portions from the carcasses of culled cows. Because of concerns about the microbiological safety of beef, particularly ground beef and pro*
Corresponding author. Tel.: +1-403-782-8113; fax: +1-403782-6120. E-mail address: [email protected] (C.O. Gill).
ducts prepared from it, most large beef packing plants in North America have installed equipment for pasteurizing dressed carcass sides with steam or hot water. Such equipment can be operated to largely remove generic Escherichia coli and, presumably, associated enteric pathogens from the meat (Gill and Bryant, 2000; Nutsch et al., 1997). However, most of the manufacturing beef produced from pasteurized carcasses continues to be contaminated with substantial numbers of generic E. coli, while Salmonella is recovered relatively frequently, and E. coli O157:H7 is recovered
0168-1605/02/$ - see front matter Crown Copyright D 2002 Published by Elsevier Science B.V. All rights reserved. PII: S 0 1 6 8 - 1 6 0 5 ( 0 1 ) 0 0 7 3 6 - X
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occasionally from the product (Anonymous, 2001; Scanga et al., 2000). Although some of the enteric organisms found on manufacturing beef may be survivors of ineffective pasteurizing treatments (Nutsch et al., 1998), most probably originate from bacterial populations that persist in carcass breaking equipment despite routine cleaning that is thought to be adequate by both plant staff and regulatory authorities (Gill et al., 1999a; Gill and McGinnis, 2000). In those circumstances, assurance of the microbiological condition of carcasses cannot and does not assure the microbiological safety of manufacturing beef and raw products prepared from it. Instead, some decontaminating treatment of manufacturing beef or of finished products seems to be required. In view of the efficacy of pasteurizing treatments for carcasses, pasteurizing of manufacturing beef is an obvious treatment to consider. For pasteurizing with hot water, it has been shown that treatment of manufacturing beef with water of >80 °C for about 60 s is necessary (Gill and Badoni, 1997a), whereas with carcasses, water of the same temperature need be applied for only 10 s (Gill et al., 1999b). Despite the relatively severe treatment needed for manufacturing beef, the eating qualities of frozen hamburger patties prepared from pasteurized product were found to be indistinguishable from those of patties prepared from unpasteurized product (Gill et al., 2001). The treatment may, however, affect other qualities of comminuted beef that are important for the commercial performance of products different from frozen hamburger patties. Much of the ground beef now offered for retail sale is prepared at retail stores by fine grinding of product which was coarsely ground and vacuum-packaged at packing plants. To discern whether pasteurized manufacturing beef might be used for ground beef prepared and traded in those manners, the microbiological and organoleptic qualities of stored, vacuum-packaged, coarsely ground beef and displayed, finely ground beef prepared from it were examined.
2. Materials and methods 2.1. Vacuum-packaged, coarsely ground beef A 100-kg lot of manufacturing beef with a lean content of approximately 80% was obtained from a
beef packing plant. The lot was collected during a period of about 30 min from pieces of meat on a conveyor belt as they arrived at a packing station. Selected pieces weighed between 700 and 1000 g, with surface areas between 400 and 700 cm2. The meat was cooled by the addition of carbon dioxide snow, as in usual, commercial practice, and was processed within 2 h of being collected. Each piece of meat in the lot was divided in two, with each part being assigned to a different one of two batches, to obtain two batches of similar weights and compositions. The meat from one batch was pasteurized. For pasteurizing, groups of five or six pieces of meat were placed without touching in a wire mesh basket with a securable lid. The lidded basket was immersed in water of 85°C for 60 s (Gill and Badoni, 1997a). The meat in the second batch was not pasteurized. The pasteurized meat was ground through a plate with 9-mm holes in a grinder head that had been cleaned and immersed in boiling water for 5 min before it was used. Subsequently, the unpasteurized meat was ground through the same plate. The batches of meat were separately collected and mixed by hand, with the use of sterile gloves. Each batch of ground meat was divided into 24 portions, each of 2 kg. Each portion was vacuumpacked in a pouch that measured 300 150 mm (l w), which was made of a polyvinyledene chloride laminate that has an oxygen transmission rate of about 40 cc/m2/24 h/atm at 25 °C and 100% r.h. (Cryovac, Mississauga, ON, Canada). All packs were stored at 2 F 0.5 °C. 2.2. Retail-packaged, finely ground beef At the time that vacuum packs of coarsely ground meat were prepared and at weekly intervals up to 6 weeks, three vacuum packs of pasteurized and three of unpasteurized meat were selected at random and were withdrawn from storage. The meat in each pack was ground through a plate with 3-mm holes, with the grinder head being cleaned and placed in boiling water for 5 min before the grinding of the meat from each pack, and with the separate collection of each portion of meat. Six samples of 5 g were obtained from each finely ground portion immediately after grinding, and were combined to give a 30-g composite sample. Then, meat
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from each portion was used to fill each of two, solid polystyrene trays, which measured 210 150 25 mm (l w h), with about 400 g of finely ground meat. The trays were overwrapped with a stretchable film that has an oxygen transmission rate of 8000 cc/ m2/24/atm at 25 °C and 75% r.h. (Vitafilm Choice Wrap, Goodyear Canada, Toronto, ON, Canada). The overwrapped trays were placed on the sole, horizontal shelf of a chest-type display case (model LPM 12 T, Hill Refrigeration, Barrie, ON, Canada) that was illuminated for 12 h/day by incandescent lights which gave a light intensity of 750 lux at the shelf surface. The mean temperature of the air in the vicinity of the displayed meat was 4 F 1 °C. The meat in each display pack was assessed for colour, discolouration and retail acceptability at the time of packing and at daily intervals, up to 3 days for meat stored in vacuum pack up to 3 weeks, but up to 2 days for meat stored in vacuum packs for 4, 5 or 6 weeks. After assessment of the appearance on the third or second day, each pack was opened and the odour intensity and acceptability were assessed. Three samples, each of 5 g, were then obtained from the meat in each tray, and samples from each pair of trays that contained meat from the same portion were combined to give a 30-g composite sample.
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Streptomycin Thallous Acetate Actidione Agar (STAA; Gardner, 1966), which were incubated at 25 °C for 2 days for the enumeration of Brochothrix thermosphacta. 2.4. Organoleptic analysis All assessments were made by an experienced, fivemember panel (Jeremiah and Gibson, 2000). Colour was assessed on an eight-point scale, where 1 = white, 2 = pale pink, 3 = pink, 4 = pale red, 5 = bright red, 6 = slightly dark red, 7 = moderately dark red, 8 = very dark red. Discolouration was assessed on a seven-point scale, where 1 = no discolouration, 2 = 1 –10% discolouration, 3 = 11 – 15% discolouration, 4 = 26 – 50% discolouration, 5 = 51 – 75% discolouration, 6 = 76 – 99% discolouration and 7 = completely discoloured. Retail acceptability was assessed on a seven-point scale, where 1 = very undesirable, 2 = undesirable, 3 = slightly undesirable, 4 = neither undesirable nor desirable, 5 = slightly desirable, 6 = desirable and 7 = very desirable. Off odour intensity was assessed on a fourpoint scale, where 1 = no off odour, 2 = slight off odour, 3 = moderate off odour and 4 = strong off odour. Odour acceptability was assessed on a five-point scale, where 1 = acceptable, 2 = slightly acceptable, 3 = neither acceptable nor unacceptable, 4 = slightly unacceptable and 5 = unacceptable.
2.3. Microbiological analysis 2.5. Analysis of data Each composite sample obtained from meat before or after display was placed in a stomacher bag with 270 ml of 0.1% (w/v) peptone water. After stomaching for 2 min, the fluid from the bag was filtered through four layers of sterile cheese cloth. Suitable 10-fold dilutions were prepared in 0.1% (w/v) peptone water and were spread on duplicate plates of: Plate Count Agar (PCA; Difco Laboratories, Detroit, MI, USA), which were incubated at 25 °C for 3 days for the enumeration of total aerobic bacteria; deMan, Rogosa and Sharpe Agar (MRS; Difco), which were incubated anaerobically at 25 °C for 3 days for the enumeration of lactic acid bacteria; Violet Red Bile Glucose Agar (VRBG; Difco), which were incubated at 30 °C for 2 days for the enumeration of Enterobacteriaceae; Cephaloridine Fucidin Cetrimide Agar (CFC; Difco) which were incubated at 25°C for 2 days for the enumeration of pseudomonads; and
All bacterial counts were transformed to log values. The means of the log values for the counts obtained for each group or species of bacteria, from pasteurized or unpasteurized product at each sampling time were plotted. Mean values for each type of organoleptic score obtained on each day of display from pasteurized or unpasteurized product that had been stored for the same time were separated using the Tukey option of the General Linear Model (GLM) procedure in Statistical Analysis Systems (SAS) version 6 (SAS Institute, Cary, NC, USA). Pairs of mean values for odour scores obtained at the end of display for pasteurized or unpasteurized meat that had been stored for the same time were separated by a t-test for paired comparisons, using the PROC MEANS procedure in SAS, version 6.
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3. Results At the time of vacuum packaging, the numbers of total aerobic bacteria and of presumptive pseudomonads and B. thermosphacta recovered from pasteurized meat were each >1 log unit less, but the numbers of presumptive lactic acid bacteria and enterobacteria were each only about 0.5 log unit less than the numbers of the same bacteria recovered from unpasteurized meat (Fig. 1). After storage of unpasteurized meat at 2 °C for 1 week, and before as well as after storage of pasteurized meat, the numbers of total aerobic bacteria and of presumptive lactic acid bacteria recovered from each sample were similar. The counts of those organisms were near or at their maximum numbers after storage of both types of meat for 3 weeks. With unpasteurized meat, the numbers of enterobacteria increased during the first 2 weeks of storage, but
Fig. 2. Numbers of total aerobic bacteria (6) and presumptive lactic acid bacteria (.), enterobacteria (5), pseudomonads (n) and B. thermosphacta (D) recovered from finely ground manufacturing beef that was displayed at 4 °C for 3 (—) or 2 days (- - -) after being prepared from vacuum-packaged, coarsely ground beef that was stored at 2 °C after being prepared from (A) unpasteurized or (B) pasteurized manufacturing beef.
Fig. 1. Numbers of total aerobic bacteria (6) and presumptive lactic acid bacteria (.), enterobacteria (5), pseudomonads (n) and B. thermosphacta (D) recovered from vacuum-packaged, coarsely ground beef stored at 2 °C after being prepared from (A) unpasteurized or (B) pasteurized manufacturing beef.
changed little thereafter; and the numbers of pseudomonads increased between weeks 1 and 2 of storage, to numbers that were similar to those of the enterobacteria. With pasteurized meat, the numbers of enterobacteria increased greatly during the first 3 weeks of storage, but changed little thereafter; and the numbers of pseudomonads also increased during the first 3 weeks, to numbers that were similar to those of the enterobacteria. With both types of meat the numbers of B. thermosphacta increased during the first 3 weeks of storage, and then declined during the following weeks. The maximum numbers attained by each of the three groups of organisms on both types of meat were similar. With unpasteurized meat that had not been stored, the total aerobic bacteria increased to 7 log cfu/g after display for 3 days at 4 °C (Fig. 2). At that time, the numbers of lactic acid bacteria, psuedomonads and B. thermosphacta were all about 6 log cfu/g, while
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Table 1 Means of the scores recorded by a five-member panel for the colours of displayed, finely ground beef derived from stored, vacuum-packaged, coarsely ground beef which had been prepared from unpasteurized (U) or pasteurized (P) manufacturing beef Storage time (weeks)
0 1 2 3 4 5 6
Mean scores for colour Displayed 0 day
Displayed 1 day
Displayed 2 days
Displayed 3 days
U
P
U
P
U
P
U
P
5.0C 4.9BC 5.1B 4.1B 4.2B 3.8A 4.1B
4.2A 4.3AB 4.6AB 3.8B 3.8AB 3.4A 4.3B
5.0C 5.0BC 5.0B 3.9B 3.6AB 3.9A 2.0A
4.3A 4.5ABC 3.9A 2.8A 3.1A 3.5A 2.8A
5.2C 5.3C d d d d d
4.4AB 3.9A d d d d d
6.2D d d d – – –
4.9B d d d – – –
Scores were 1 = white, 2 = pale pink, 3 = pink, 4 = pale red, 5 = bright red, 6 = slightly dark red, 7 = dark red, 8 = very dark red. d = discolouration too extensive for the meat colour to be assessed. ( – ) Meat not assessed. Values on the same line with the same letter are not significantly different ( P >0.05).
numbers of enterobacteria were about 4.5 log cfu/g. With pasteurized meat that had not been stored, the total aerobic bacteria increased to about 6.5 log cfu/g after display for 3 days at 4 °C. At that time, the numbers of pseudomonads were similar to the numbers of the total aerobic bacteria, while the numbers of lactic acid bacteria, B. thermosphacta and enterobacteria were all < 6 log cfu/g. With both types of meat stored at 2 °C for 1 week or more then displayed at 4 °C, the numbers of total aerobic bacteria and lactic acid bacteria recovered were about 8.5 and 8.0 log cfu/g, respectively, after all times of storage and display (Fig. 2). The numbers of pseudomonads recovered from both types of meat that had
been stored for 1 or 2 weeks, then displayed, were about 7 log cfu/g, but the numbers on meat that had been stored for 3 weeks or longer, then displayed, were < 5 log cfu/g. The numbers of enterobacteria on unpasteurized or pasteurized meat that had been stored for 1 or 2 weeks then displayed were >4 or >6 log cfu/ g, respectively. For meat stored for 2 weeks or more then displayed, the numbers of enterobacteria and pseudomonads were similar at each time of storage and display. With unpasteurized meat, the numbers of B. thermosphacta were >5 and < 4 log cfu/g, after display following storage for < 2 weeks and >3 weeks, respectively. With pasteurized meat, the numbers of B. thermosphacta were 7 log cfu/g after storage for 2
Table 2 Means of the scores recorded by a five-member panel for the discolouration of displayed, finely ground beef derived from stored, vacuumpackaged, coarsely ground beef which had been prepared from unpasteurized (U) or pasteurized (P) manufacturing beef Storage time (weeks)
0 1 2 3 4 5 6
Mean scores for colour Displayed 0 day
Displayed 1 day
Displayed 2 days
Displayed 3 days
U
P
U
P
U
P
U
P
1.0A 1.1A 1.1A 1.0A 1.0A 1.0A 1.9A
1.2A 1.3A 1.0A 1.0A 1.0A 1.1A 1.8A
1.1A 1.4B 3.6B 4.8C 4.5C 3.6C 5.7C
1.2A 1.5B 3.3B 3.4B 2.9B 2.8B 4.8B
2.0B 3.1C 6.8D 7.0D 6.9D 6.9D 7.0D
2.0B 3.1C 6.2C 6.8D 6.3D 6.9D 7.0D
4.1D 6.6D 7.0D 7.0D – – –
3.6C 6.6C 6.8D 7.0D – – –
Scores were 1 = no discolouration, 2 = 1 – 10% discolouration, 3 = 11 – 25% discolouration, 4 = 26 – 50% discolouration, 5 = 51 – 75% discolouration, 6 = 76 – 99% discolouration, 7 = wholly discoloured. ( – ) Meat not assessed. Values on the same line with the same letter are not significantly different (P >0.05).
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Table 3 Means of the scores recorded by a five-member panel for the retail acceptability of displayed, finely ground beef derived from stored, vacuumpackaged, coarsely ground beef which had been prepared from unpasteurized (U) or pasteurized (P) manufacturing beef Storage time (weeks)
0 1 2 3 4 5 6
Mean scores for acceptability Displayed 0 day
Displayed 1 day
Displayed 2 days
Displayed 3 days
U
P
U
P
U
P
U
P
6.6A 6.5A 6.5A 5.7A 6.0A 5.0A 4.3A
6.2AB 6.3A 6.2A 5.2A 5.6A 4.8A 4.1A
6.4A 5.7B 2.4C 2.1B 2.1C 2.7B 1.3B
5.8B 5.5B 3.1B 2.6B 2.8B 3.1B 1.4B
4.7C 3.2C 1.0D 1.0C 1.0D 1.0C 1.0B
4.6C 3.1C 1.1D 1.0C 1.0D 1.0C 1.0B
2.2E 1.0D 1.0D 1.0C – – –
2.9D 1.0D 1.0D 1.0C – – –
Scores were 1 = very undesirable, 2 = undesirable, 3 = slightly undesirable, 4 = neither undesirable nor desirable, 5 = slightly desirable, 6 = desirable, 7 = very desirable. ( – ) Meat not assessed. Values on the same line with the same letter are not significantly different (P >0.05).
weeks and display, but < 3 log cfu/g after storage for 3 or more weeks and display. When meat was not stored before display, meat colours could be discerned on all days up to and including the third day of display (Table 1). However, after storage for 1 week or more, discolouration was too extensive for colours to be assessed on the third or second day of display, respectively. For meat stored for up to 5 weeks, after most times of display, some panelists perceived the colour of unpasteurized meat to be darker than that of pasteurized meat stored and displayed for the same times. However, the mean differences were mostly small and sometimes not significant ( P > 0.05). When meat was first displayed after storage for up to 5 weeks, there was little discolouration of either unpasteurized or pasteurized meat (Table 2). After display for 1 day of meat that had not been stored or stored for 1 week, discolouration of both unpasteurized and pasteurized meat was little and similar; but meat displayed for 1 day after storage for 2 or more weeks was extensively discoloured by browning, with discolouration being more extensive on unpasteurized than pasteurized meat that had been stored for the same time. When meat was first displayed without being stored or after storage for 1 or 2 weeks, both unpasteurized and pasteurized meat was assessed as very desirable or desirable, although the higher score was assigned more frequently to unpasteurized than to pasteurized meat (Table 3). When meat was stored and/or displayed for
longer times, scores for retail acceptability were progressively lower. All meat displayed for 3 days was assessed as slightly or more undesirable. When the odours of meat that had not been stored or stored for 1 or 2 weeks were assessed after display for 3 days, off odours were assessed as being of slight or moderate intensity and neither acceptable nor unacceptable or slightly unacceptable. At those times, the mean scores for odour intensity for unpasteurized and pasteurized meat stored and displayed for the same times were not significantly different ( P > 0.05), but the mean scores for odour acceptability were significantly larger ( P < 0.05) for unpasteurized than for pasteurized meat. Odours of meat that had been stored and/or displayed for longer times were assessed as being moderate or strong and slightly or more unacceptable. At those times, the mean scores for odour intensity or acceptability for unpasteurized and pasteurized meat stored and displayed for the same times were not significantly different ( P > 0.05).
4. Discussion Coarsely ground beef prepared at packing plants is often cooled to about 0 °C by the addition of carbon dioxide snow to the meat during grinding, and such temperatures are often maintained during the subsequent transportation of the product (Gill et al., 2002a). However, at retailers’ warehouses and retail stores in Canada, and probably elsewhere in North America,
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the median temperatures of meat are about 2 °C, while the median temperature of displayed meat is about 4 °C (Gill et al., 2002b). Therefore, in investigating the possible effects of pasteurizing on the storage performance of ground beef, the meat was stored and displayed at 2 °C and 4 °C, respectively. Ground meat is generally distributed from packing plants relatively rapidly, with the median age of the product being 8 days at the time it is prepared for retail sale (Gill et al., 2002a). However, the time that coarsely ground meat is stored in vacuum packs can extend to several weeks. Therefore, in this study, the vacuumpackaged product was stored for up to 6 weeks. As was found in previous studies, pasteurizing reduced the numbers of total aerobic bacteria recovered from meat by more than an order of magnitude (Gill et al., 2001a), and the reductions in the numbers of presumptive pseudomonads and B. thermosphacta were similar. However, the numbers of presumptive lactic acid bacteria and enterobacteria recovered were reduced by less than an order of magnitude. The apparent reduction in numbers of enterobacteria might be misleading, as few were recovered before, and very few were recovered after pasteurizing, while pasteurizing has been previously found to reduce the numbers of coliforms on meat by about two orders of magnitude (Gill et al., 2001). However, it is evident that the presumptive lactic acid bacteria were less affected by the pasteurizing treatment than the other groups of organisms, and consequently were predominant in the flora of pasteurized meat at all times instead of only at later storage times, as in the unpasteurized meat. Despite that, the behaviors of the other groups of organisms on pasteurized and unpasteurized meat were broadly similar, with all three reaching maximum numbers by the third week of storage. The increases in numbers of presumptive pseudomonads might, however, be misleading as the strictly aerobic pseudomonads would be expected to grow little or not at all in vacuum packs (Gill and Molin, 1991), while the coincident numbers of presumptive pseudomonads and enterobacteria recovered from both types of meat at later storage times suggests that enterobacteria, as well as surviving pseudomonads, were enumerated on CFC (Mead, 1985). After display without storage or following storage for 1 week, the numbers of presumptive pseudomonads recovered from both pasteurized and unpasteur-
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ized meat greatly exceeded the numbers of presumptive enterobacteria recovered at those times. Thus, pseudomonads evidently grew to form major fractions of the flora when both pasteurized and unpasteurized meat were displayed after no or a short period of storage. However, after 2 weeks of storage, with the flora on the stored meat approaching maximum numbers, growth of enterobacteria accompanied or surpassed the growth of pseudomonads, while little growth of either group of organisms would seem to have occurred during the display of pasteurized or unpasteurized meat that had been stored for 3 weeks or more. Only with B. thermosphacta recovered from displayed meat that was not stored or had been stored for 2 weeks before display, were the numbers from pasteurized and unpasteurized meat very different. It would appear then that pasteurizing of manufacturing beef would not greatly extend the time before the onset of microbial spoilage in vacuum-packaged beef prepared from it, nor greatly delay the onset of microbial spoilage in ground meat displayed after storage in vacuum packs. The finding that off-odours of similar intensities were apparent at the same times in pasteurized and unpasteurized meat, with the odours of pasteurized meat being somewhat more acceptable after the shorter periods of storage, is in agreement with that conclusion. Pasteurizing discolours the surfaces of meat pieces by bleaching much and browning some of the muscle tissue (Gill and Badoni, 1997b). Because of the bleached tissue, the ground beef prepared from pasteurized product was perceived as being of lighter colour than the ground beef prepared from unpasteurized product, while flecks of browned tissue were perceived in some ground beef prepared from pasteurized, but not in ground beef prepared at the same time from unpasteurized tissue. Despite these differences, the retail acceptabilities of ground beef prepared from pasteurized and unpasteurized product were similar, while brown discolouration developed at the same rate or more slowly in ground beef prepared from pasteurized, than in that prepared from unpasteurized product. A somewhat later development of extensive browning in ground beef prepared from pasteurized product may be a consequence of the modest differences in the numbers and compositions of the spoilage flora on the two types of meat (Faustman et al., 1990).
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The extent to which the colour of ground beef is lightened and discoloured because of pasteurizing of the product from which it is prepared will vary with the sizes of pieces of meat in batches of manufacturing beef, as the surface area, and so the amount of tissue denatured during pasteurizing will be relatively large in relation to the meat mass when meat pieces are small. Lightening of colour and discolouration of ground beef as a result of pasteurizing manufacturing beef could then be more or less than the change of colour and discolouration perceived in this study. However, the findings of this study suggest that the effects on ground beef appearance of the pasteurizing of manufacturing beef would, generally, be too small to affect its appeal to consumers. Therefore, pasteurizing of manufacturing meat might well be a commercially viable means of substantially enhancing the microbiological safety, although probably not the storage stability of ground beef.
Acknowledgements We thank Ms. M. Brockway for technical assistance, and the Alberta Agricultural Research Institute for financial support of the study.
References Anonymous, 2001. News: little E. coli. Meat Processing, March 10. Faustman, C., Johnson, J.L., Cassens, R.G., Doyle, M.P., 1990. Color reversion in beef. Fleischwirtschaft 70, 676 – 679. Gardner, G.A., 1966. A selective medium for the enumeration of Microbacterium thermosphactum in meat and meat products. Journal of Applied Bacteriology 29, 455 – 460. Gill, C.O., Badoni, M., 1997a. The hygienic and organoleptic qualities of ground beef prepared from manufacturing beef pasteurized by immersion in hot water. Meat Science 46, 67 – 75. Gill, C.O., Badoni, M., 1997b. The effects of hot water pasteurizing treatments on the appearances of pork and beef. Meat Science 46, 77 – 87.
Gill, C.O., Bryant, J., 2000. The effects on product of a hot water pasteurizing treatment applied routinely in a commercial beef carcass dressing process. Food Microbiology 17, 495 – 504. Gill, C.O., McGinnis, J.C., 2000. Contamination of beef trimmings with Escherichia coli during a carcass breaking process. Food Research International 33, 125 – 130. Gill, C.O., Molin, G., 1991. Modified atmospheres and vacuum packaging. In: Russel, N.J., Gould, G.W. (Eds.), Food Preservatives. Blackie Academic, Glasgow, pp. 172 – 199. Gill, C.O., Badoni, M., McGinnis, J.C., 1999a. Assessment of the adequacy of cleaning of equipment used for breaking beef carcasses. International Journal of Food Microbiology 46, 1 – 8. Gill, C.O., Bryant, J., Bedard, D., 1999b. The effects of hot water pasteurizing treatments on the appearances and microbiological conditions of beef carcass sides. Food Microbiology 16, 281 – 289. Gill, C.O., Bryant, J., Badoni, M., 2001. Effects of hot water pasteurizing treatments on the microbiological condition of manufacturing beef used for hamburger patty manufacture. International Journal of Food Microbiology 63, 243 – 256. Gill, C.O., Jones, T., Rahn, K., Campbell, S., LeBlanc, D.I., Holley, R.A., Stark, R., 2002a. Temperatures and ages of boxed beef packed and distributed in Canada. Meat Science, 60 (in press). Gill, C.O., Jones, T., LeBlanc, D.I., Rahn, K., Campbell, S., Holley, R.A., Stark, R., Houde, A., 2002b. Temperatures and ages of packs of beef displayed at stores in Canada. Meat Science (in press). Jeremiah, L.E., Gibson, L.L., 2000. The display performance of retail-ready beef following storage: muscle influences. Journal of Muscle Foods 11, 273 – 291. Mead, G.C., 1985. Enumeration of pseudomonads using cephaloridin – fucidin – cetrimide agar (CFC). International Journal of Food Microbiology 2, 21 – 26. Nutsch, A.L., Phebus, R.K., Riemann, M.J., Schafer, D.E., Boyer Jr., J.E., Wilson, R.C., Leising, J.D., Kastner, C.L., 1997. Evaluation of a steam pasteurization process in a commercial beef processing facility. Journal of Food Protection 60, 485 – 492. Nutsch, A.L., Phebus, R.K., Riemann, M.J., Kotrola, J.S., Wilson, R.C., Boyer Jr., J.E., Brown, T.L., 1998. Steam pasteurization of commercially slaughtered beef carcasses: evaluation of bacterial populations at five anatomical locations. Journal of Food Protection 61, 571 – 577. Scanga, J.A., Grona, A.D., Belk, K.E., Sofos, J.N., Bellinger, G.R., Smith, G.C., 2000. Microbiological contamination of raw beef trimmings and ground beef. Meat Science 56, 145 – 152.