The fate of Salmonella Typhimurium and Escherichia coli O157 on hot boned versus conventionally chilled beef

Meat Science 126 (2017) 50–54

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The fate of Salmonella Typhimurium and Escherichia coli O157 on hot boned versus conventionally chilled beef Rachael Reid a, Séamus Fanning b, Paul Whyte b, Joe Kerry c, Declan Bolton a,⁎ a b c

Teagasc Food Research Centre, Ashtown, Dublin 15, Ireland University College Dublin, Belfield, Dublin 4, Ireland University College Cork, Cork, Ireland

a r t i c l e

i n f o

Article history: Received 27 October 2016 Received in revised form 13 December 2016 Accepted 19 December 2016 Available online 21 December 2016 Keywords: Hot boning Beef TVC Salmonella VTEC

a b s t r a c t This study investigated the fate of Salmonella Typhimurium and Escherichia coli O157 on hot boned versus conventionally chilled beef. Beef samples were individually inoculated with S. Typhimurium ATCC 14028, S. Typhimurium 844, E. coli O157 EDL 933 or E. coli T13. Half the samples were subject to the same time-temperature chilling profile used for conventionally chilling beef carcasses while the other half was subject to hot boned conditions. The surface pH (5.5) and aw (0.95 to 0.97) were stable. S. Typhimurium and E. coli O157 counts, which decreased by up to 1.0 and 1.5 log10 cfu cm−2, respectively, were statistically similar (P N 0.05), regardless of the chilling regime applied, with the exception of E. coli O157 EDL 933, where the counts on hot boned beef were significantly (P b 0.05) higher. It was concluded that any decrease in pathogenic bacteria during beef chilling may be significantly (P b 0.05) less for hot boned beef depending on the bacterial strain. Hot boning may therefore result in an increased risk to the consumer. © 2016 Elsevier Ltd. All rights reserved.

1. Introduction Beef carcasses are usually chilled immediately after slaughter for a period of at least 24 h before cutting into primals in the boning hall (Savell, Mueller & Baird, 2005). Hot boning, a process in which carcasses are deboned immediately after slaughter, has several advantages over conventional chilling, including a requirement for less chiller space, more flexible logistics and reduced costs (Pisula & Tyburcy, 1996). However, this technology has not been adopted in most countries, as a failure to immediately chill the surface temperature of the beef could promote bacterial growth (EFSA, 2014). A recent scientific opinion by the European Food Safety Authority (EFSA) identified Salmonella and Escherichia coli O157 as high priority hazards for beef (EFSA, 2013a). In the European Union (EU) up to 60% of bovine hides have been reported to be Salmonella positive (Rhoades et al., 2009) and 0.6% of an estimated 6 million salmonellosis cases in Europe have been associated with beef (EFSA, 2011; EFSA 2014); with E. coli O157 prevalence rates ranging from 0.2 to 2.3%, 1.5% to 13.7% and 5.5% to 20.2% for individual animal, herd and slaughter batches, respectively (EFSA, 2013b). Salmonella and E. coli O157 are carried asymptomatically in the gastrointestinal tract of cattle and shed in the faeces. Although EC 853/2004 requires that cattle presented for slaughter should be clean and dry, soiled hides are still a major source of carcass ⁎ Corresponding author at: Teagasc Food Research Centre, Ashtown, Dublin 15, Ireland. E-mail address: [email protected] (D. Bolton).

http://dx.doi.org/10.1016/j.meatsci.2016.12.010 0309-1740/© 2016 Elsevier Ltd. All rights reserved.

contamination with these organisms which are readily transferred during dehiding (Koohmaraie et al., 2005). Control is dependent on the implementation of an effective prerequisite programme (PRP) and hazard analysis and critical control point as required by EC 852/2004 and EC 853/2004. Although lactic acid, applied as a spray or mist, at concentrations of 2% to 5% and temperatures of up to 55 °C, may be applied to beef carcasses (EC 101/2013) this is rarely used as it is not accepted by retail customers. In contrast, chilling has been incorporated into many beef slaughter HACCP plans (Lenahan et al., 2010), not least because several studies have shown that more efficient chilling results in improved carcass hygiene (Philips et al., 2006, Ruby, Zhu & Ingham, 2007; Sheridan, 2004). Current legislation, Regulation EC 853/2004, requires that carcasses be immediately chilled after post-mortem inspection to ensure a temperature throughout of not N 7 °C in the case of meat and not N 3 °C for offal. Beef carcass surface temperatures range between 15 °C and 20 °C immediately after slaughter (Reid et al., 2017), temperatures that will support the survival and growth of both Salmonella spp. and E. coli O157. It is therefore important that the temperature be reduced to below 5 °C, their minimum growth temperature, as soon as possible (EFSA, 2014; James & James, 2004). However, in practice beef carcasses are usually chilled to not below 10 °C in the first 10 h (to prevent cold shortening) and to 0 to 2 °C thereafter. In contrast hot boning of carcasses employs boning out and cut up of carcasses into various pieces and primals followed by vacuum packaging and placement in cardboard boxes before chilling. It has been suggested that the higher

R. Reid et al. / Meat Science 126 (2017) 50–54

Fig. 1. Chill profiles of beef samples in 13 L of water at 2 °C (solid line) achieved the same time-temperature profile as chilling the hot boned primals in a commercial abattoir (dashed line).

temperatures associated with hot boned beef could promote bacterial survival and growth, including Salmonella and E. coli O157 (Sheridan & Sherington, 1982; Spooncer, 1993; Yang, Balamurugan, & Gill, 2011). The aims of this study were therefore; [1] to investigate the survival of bacteria used as general indicators of hygiene (total viable count, TVC and total Enterobacteriaceae count, TEC) during the chilling of beef and [2] to determine if the higher temperatures associated with hot boning versus conventional chilling could facilitate the survival and/or growth of S. Typhimurium and E. coli O157. 2. Materials and methods 2.1. Bacterial cultures S. Typhimurium strains, reference strain ATCC 14028 and bovine isolate 844 (from the Teagasc culture collection) and E. coli O157 reference strain EDL 933 and bovine isolate (T13) also from our culture collection were used in these experiments. All strains were made resistant to 1000 μg mL−1 streptomycin sulphate (Sigma Aldrich, Ireland) according to the method described by Blackburn & Davies (1994) to facilitate selective recovery from beef samples. The growth rates of the mutant strains were compared to the wild type strains to ensure that there was no significant differences (P b 0.05) (data not shown). Stains were stored on Protect beads (Technical Service Consultants Ltd., UK) at −20 °C until required. 2.2. Inoculum preparation One bead containing the a specific strain (ATCC 14028, 844, EDL 933 or T13) was spread plated onto Tryptone Soya Agar (TSA) plates (Oxoid) and incubated at 37 °C for 24 h. A single colony was then aseptically transferred to 10 mL Tryptone Soya Broth (TSB) (Oxoid) and incubated at 37 °C for 24 h. The culture was then centrifuged (Eppendorf centrifuge 5403) at 5000g at 4 °C for 10 mins. The recovered pellet was washed twice with 10 mL phosphate buffered saline (PBS) (Oxoid) and then resuspended in 10 mL PBS to produce a culture containing approximately 9 log10 cfu mL−1. The suspension was then serially diluted 1:10 in Maximum Recovery Diluent (MRD) to create a suspension containing 6 log10 cfu mL−1. Exactly 1 mL of this suspension was added to 1 L of MRD to create the final inoculum suspension with a final concentration of approximately 3 log10 cfu mL−1, which was used to dip inoculate the beef samples. The final average concentration of the dip inoculum was determined by plating out 100 μl aliquots onto TSA supplemented with 1000 μg mL−1 streptomycin sulphate and incubating at 37 °C for 24 h.

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Teagasc Food Research Centre, Ashtown, Dublin 15, Ireland. After evisceration, each heifer was centrally split into left and right sides (n = 12). On the right side, the M. longissimus thoracis et lumborum (LTL) (striploin), M. psaoa major (fillet), M. semitendinosus (inside round), M. quadriceps (knuckle) and Biceps Femoris muscles were hot boned (HB) out within 90 min of slaughter and vacuum packaged (Pi-Vac Elasto-pack system, Nofima) to prevent cold shortening. These primals were then placed in a commercial chiller at 0 °C for 24 h. The left side was treated as the conventional side and was placed in a commercial chiller for 24 h. The surface temperature of the hot boned muscles (24 h chill at 0 °C) and the conventionally treated carcasses (10 °C for 10 h followed by 0 °C for the remaining 14 h) were monitored (every 10 min for 96 h) using Testo-T175 (Eurolec Instrumentation LTD) data loggers. 2.4. Development of a model system to mimic the time-temperature profiles of hot boned and conventionally chilled beef The method of Hudson et al. (2013) was used to mimic the chilling curves of conventional and hot boned beef carcasses, samples (10 × 10 × 1 cm), prepared from the conventionally chilled B. Femoris muscle, placed in containers filled with 5 L of water (pre-heated to 22 °C) and were chilled in a programmable incubator that was set to 10 °C for 10 h followed by 0 °C to mimic the commercial chilling surface temperature. Hot boned samples were placed in containers of 13 L of water (pre-heated to 22 °C) and chilled at 2 °C for 24 h. Previous work has established that these volumes of water gave the best results for mimicking conventional beef carcass chilling and hot boning surface temperatures. Surface temperatures were monitored as described above. 2.5. Beef sample preparation Exactly 140 beef samples (10 × 10 × 1 cm) were prepared from the conventionally chilled B. Fermoris muscle. From these, 14 samples were randomly assigned to each of the following treatment combinations; [1] S. Typhimurium ATCC 14028 – hot boned; [2] S. Typhimurium ATCC 14028 – conventionally chilled; [3] S. Typhimurium 844 – hot boned; [4] S. Typhimurium ATCC 844 – conventionally chilled; [5] E. coli O157 EDL 933 – hot boned; [6] E. coli O157 EDL 933 – conventionally chilled; [7] E. coli O157 T13 – hot boned and [8] E. coli O157 T13 – conventionally chilled. The remaining 2 sets of 14 were used as uninoculated controls to monitor psychrophilic TVC (TVCp), mesophilic TVC (TVCm) and TEC, set 1 being subject to the hot boned time-temperature profile and set 2 subject to conventional chilling. These control samples were also used to

2.3. Recording the time-temperature profiles for conventionally chilled (cold boned) and hot boned beef carcasses. On 3 separate occasions, 2 heifers (n = 6) of commercial breeds were slaughtered in the Meat Industry Development Unit (MIDU) in

Fig. 2. Chill profiles of beef samples in 5 L of water (solid line) for 10 °C for 10 h and then to a target temperature of 0 °C for 38 h achieved the same time-temperature profile as chilling using the same time-temperature targets in a commercial abattoir (dashed line).

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R. Reid et al. / Meat Science 126 (2017) 50–54

Table 1 Average surface pH and aw (water activity) of conventionally chilled and hot boned beef samples. Time (h)

0

Boning

Cold

Hot

2 Cold

Hot

4 Cold

Hot

6 Cold

Hot

8 Cold

Hot

10 Cold

Hot

24 Cold

Hot

pH aw

5.53 0.97

5.49 0.97

5.55 0.95

5.46 0.96

5.59 0.96

5.49 0.96

5.56 0.95

5.52 0.96

5.54 0.96

5.53 0.95

5.56 0.96

5.53 0.95

5.61 0.95

5.57 0.95

monitor surface pH and aw. This experiment was repeated on 3 separate occasions.

6.5 °C for 10 days, respectfully. TEC were performed by plating onto VRBGA (Oxoid) and incubating at 37 °C for 24 h.

2.6. Inoculating samples

2.10. Statistical analysis

In a laminar flow unit, samples were aseptically removed from the vacuum bags using a sterile scalpel and forceps. Each sample was dip inoculated for 30 s to a final concentration of approximately 103 cfu cm−2 cells. Samples were then placed into sterile aluminium foil trays, covered and placed in the incubator at 22 °C for 30 min to allow for bacterial cell adhesion before vacuum packaging the sample in a BB3055x CryoVac vacuum bag (Sealed Air Ltd.) using the VacStar S220 (Suigez, Switzerland). Samples were then subject to either the conventional chilling or hot boned chilling time-temperature chilling conditions using the method of Hudson et al. (2013) as described above.

This study used a split-split plot design. In this 3 factor factorial, factor A was the bacteria inoculated (S. Typhimurium ATCC 14028, S. Typhimurium 844, E. coli O157 EDL 933 and E. coli O157 T13) (wholeplots). These were randomly assigned to factor B (hot boned or conventionally chilled) (split-plots), which, in turn, were randomly assigned to factor c (the different sampling times (t) = 0, 2, 4, 6, 8, 10 and 24 h (subsub-plots). Each experiment was performed in duplicate and repeated on 3 separate occasions (n = 6). All samples were plated in duplicate and the bacterial counts converted into log10 cfu cm− 2 values. The data was analysed by ANOVA using GenStat for Windows 14th Edition. (VSN International, Hemel Hempstead, UK. Web page: GenStat.co.uk) with significance set at the 5% level (P b 0.05).

2.7. Surface pH analysis

3. Results and discussion

Surface pH was measured using a Sentek P-17 electrode (Lennox, Ireland). The electrode was calibrated using pH, 4, 7 and 10 standards (Lennox, Ireland) before use.

The mean beef carcass surface chilling profiles for conventionally and hot boned carcasses were accurately modelled using a laboratory scale water-bath (Figs. 1 and 2). The average surface pH and aw of the samples are shown in Table 1. For conventionally chilled and hot boned beef, the surface pH ranged from 5.53–5.61 and 5.46–5.57, respectively, over the first 24 h chilling. The aw ranged from 0.95–0.97 regardless of the chilling profile. TVCp, TVCm and TEC were relatively stable throughout the first 10 h of chilling, ranging from 1.15 to1.84, 1.39 to 1.85 and 1.44 to 2.08 log10 cfu cm− 2, respectively, on hot boned beef and from 1.1 to 1.93, 1.10 to 1.96 and 1.23 to 1.47 log10 cfu cm−2, respectively, on the conventionally chilled equivalent (Table 2). Interestingly, with the exception of TVCm (cold boned), a decrease in bacterial counts was observed between 10 h and 24 h. Other studies have also noted a decrease in TVC and TEC on beef (Kinsella et al., 2006; McEvoy, Sheridan, Blair & McDowell, 2004), lamb (Biss & Hathaway, 1995; Gill & Jones, 1997) and pork (Lenahan et al., 2009) carcasses. In contrast, Lenahan et al. (2010) in a study of 100 lamb carcasses, reported mixed results with a reduction in TVCs on 40% of carcasses while 2% remained unchanged and 58% showed an increase. The corresponding analysis for TEC found 51% of carcasses showed decreased counts; 23% remained unchanged and 26% showed increased counts. It is well established that the combination of low temperature and a low aw leads to drying out of the carcass surface that can result in injury of bacterial cells although these cells may be capable of

2.8. Water activity (aw) analysis A 5 cm2 excision sample was taken using a 25 mm cork borer (VWR), sterile scalpel and forceps. Each sample was placed in a sterile plastic Aqualab cup (Labcell, Basingstoke, England) for transport back to the lab. The aw of the samples were obtained using an Aqualab model CX2 water activity meter (Labcell), calibrated before use using a saturated solution of sodium chloride (NaCl, aw = 0.984 ± 0.003 at 20 °C). 2.9. Microbiological analysis Duplicate samples were removed at seven time points (0, 2, 4, 6, 8, 10 and 24 h), placed into sterile stomacher bags and stomached with 90 mL MRD for 30 s using a pulsifier. Serial dilutions were prepared using 9 mL MRD and plated out onto the appropriate media. For the enumeration of S. typhimurium, samples were plated onto XLD (Oxoid) supplemented with 1000 μg mL−1 streptomycin sulphate and incubated for 24 h at 37 °C. For E. coli O157, samples were plated onto Sorbitol McConkey Agar (SMAC) supplemented with SMAC supplement and 1000 μg mL− 1 streptomycin sulphate and incubated for 24 h at 37 °C. TVCm and TVCp were enumerated by plating onto Plate Count Agar (Oxoid) and subject to either incubation at 30 °C for 72 h or

Table 2 Mean total viable counts (TVC) and total Enterobacteriaceae counts (TEC) (log10 cfu cm−2) on beef samples during chilling. TVCp Time (h)

0 2 4 6 8 10 24

TVCm

HB

CB

TEC

HB

CB

HB

CB

Mean

SE

Mean

SE

Mean

SE

Mean

SE

Mean

SE

Mean

SE

1.15 1.58 1.73 1.68 1.83 1.84 1.16

0.05 0.05 0.16 0.19 0.09 0.03 0.02

1.10 1.69 1.49 1.93 1.52 1.71 1.22

0.27 0.23 0.33 0.10 0.06 0.10 0.20

1.77 1.85 1.68 1.46 1.39 1.46 1.01

0.19 0.34 0.40 0.09 0.15 0.18 0.13

1.34 1.96 1.01 1.91 1.64 1.54 1.64

0.20 0.30 0.35 0.19 0.21 0.27 0.10

1.99 1.44 2.08 1.99 1.81 1.68 1.58

0.19 0.05 0.23 0.12 0.10 0.18 0.10

1.23 1.25 1.26 1.35 1.47 1.40 0.89

0.01 0.03 0.13 0.03 0.02 0.06 0.10

R. Reid et al. / Meat Science 126 (2017) 50–54

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Table 3 Salmonella Typhimurium and E. coli O157 counts (log10 cfu cm−2) on beef samples during chilling. Time (h)

n

S. Typhimurium

E. coli O157

ATCC 14028 HB1

0 2 4 6 8 10 24

6 6 6 6 6 6 6

844 CC2

EDL 933

HB

CC

T31

HB

CC

HB

CC

mean

SE

Mean

SE

mean

SE

mean

SE

mean

SE

mean

SE

mean

SE

mean

SE

2.32A 1.60A 1.52A 1.53A 1.61A 1.52A 1.56A

0.31 0.20 0.05 0.07 0.08 0.31 0.21

1.96A 1.93A 1.78A 1.92A 1.79A 1.64A 1.36A

0.18 0.15 0.12 0.15 0.14 0.09 0.10

1.92A 1.89A 2.02A 1.97A 1.83A 1.73A 1.32A

0.35 0.18 0.05 0.02 0.10 0.16 0.12

2.50A 2.19A 2.16A 1.90A 1.79A 1.77A 1.53A

0.15 0.09 0.10 0.13 0.16 0.11 0.07

2.94A 3.13A 2.87A 2.86A 2.69A 2.58A 2.34A

0.21 0.14 0.10 0.16 0.16 0.22 0.19

2.65A 2.61B 2.46B 2.12B 1.94B 1.67B 1.22B

0.30 0.21 0.18 0.06 0.08 0.11 0.07

3.12A 2.83A 2.74A 2.51A 2.18A 2.01A 1.57A

0.20 0.16 0.04 0.12 0.20 0.21 0.08

2.94A 2.37A 2.42A 2.03A 2.12A 1.55A 1.64A

0.09 0.27 0.12 0.20 0.12 0.12 0.10

HB1 = hot boned; CC2 = conventionally chilled. Different capital letters indicate statistical significant difference (P b 0.05) when comparing the bacterial counts on hot boned versus conventionally chilled samples at that given sampling time only.

recovery (Yu, Cooke & Tu, 2001). Moreover, variations in TVC and TEC during chilling may be the result of differences in bacterial populations and chilling parameters (Sheridan, 2000). Both S. Typhimurium strains ATCC 14028 and 844 decreased steadily over the course of the experiment regardless of chilling profile (Table 3). From time t = 0 to 24 h, ATCC 14028 counts decreased by 0.76 and 0.4 log10 cfu cm−2 on hot boned and conventionally chilled beef samples, respectively. The corresponding decreases for strain 844 were 0.6 and 0.97 log10 cfu cm−2, respectively. There was no significant difference (P N 0.05) in either Salmonella strain when comparing hot boned versus conventionally chilled samples at each sampling time. The surface temperature of our beef samples was above 5 °C, the minimum temperature for Salmonella growth (James & James, 2004) for approximately 12 h during this experiment and the aw (0.95–0.97) and pH 5.46–5.57, conditions that are expected to permit survival and growth (James and James, 2004). However, S. Typhimurium counts decreased by approximately 0.5 to 1 log10 cfu cm−2 regardless of chilling profile applied (hot boning or conventional chilling). Previous studies have attributed Salmonella reductions on chilled meat to the combined effect of cold shock and drying (Chang, Mills & Cutter, 2003; Kuitche, Letang & Daudin, 1996). Although beef data is relatively scarce, Kinsella et al. (2009) reported no change in S. Typhimurium counts on beef carcasses stored at 5 °C for 24 h. Similar studies on pork suggest the concentration of Salmonella may decrease (Arguello et al., 2012; Botteldoorn et al., 2003; Bouvet et al., 2003; De Busser et al., 2011; Duggan et al., 2010), remain unchanged (King et al., 2012) or increase (Algino, Badtram, Ingham & Ingham, 2009; Chang, Mills & Cutter, 2003) during chilling. These conflicting findings may be due to differences in bacterial strains, sampling methods, chilling profiles, etc. (Gonzales-Barron, Cadavez, Sheridan & Butler, 2013). E. coli O157 counts also decreased during chilling. This was expected as other studies have reported a reduction in the E. coli population on beef (Prendergast and Sheridan, 2008), pork (Gill et al., 2000) and lamb (Gill & Jones, 1997). However, the mean decrease observed in this study (1.2 log10 cfu cm−2), was considerably less than that reported in other similar studies (Eustace, McPhail & Knox, 2004; McEvoy, Sheridan, Blair & McDowell, 2004). Interestingly there was a significant (P b 0.05) difference in E. coli O157 EDL 933 counts on hot boned versus conventionally chilled samples at each sampling time with the exception of time t = 0. In contrast E. coli O157 T31 counts were statistically similar (P b 0.05) at each sampling time throughout the experiment. Although such variation may be due to difference in chilling parameters in this study it was more likely due to strain variation (Gonzales-Barron, Cadavez, Sheridan & Butler, 2013) To conclude, although the conditions (temperature, pH and aw) were expected to facilitate survival and possibly growth, chilling beef samples inoculated with S. Typhimurium or E. coli O157 for 24 h using time-temperature profiles similar to those used for the conventional chilling of beef carcasses or hot boned beef reduced the bacterial

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