Microbiological contamination of pig and cattle carcasses in different small-scale Swiss abattoirs

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MEAT SCIENCE Meat Science 78 (2008) 225–231 www.elsevier.com/locate/meatsci

Microbiological contamination of pig and cattle carcasses in different small-scale Swiss abattoirs C. Zweifel, R. Fischer, R. Stephan

*

Institute for Food Safety and Hygiene, Vetsuisse Faculty University of Zurich, Winterthurerstr. 272, 8057 Zurich, Switzerland Received 12 March 2007; received in revised form 18 June 2007; accepted 18 June 2007

Abstract A total of 750 pig carcasses and 535 cattle carcasses from 17 small-scale abattoirs were sampled by excision at four sites (pig: neck, belly, back, ham; cattle: neck, brisket, flank, rump). Samples were examined for total viable counts (TVC) and Enterobacteriaceae. Mean TVCs ranged from 2.4 to 4.2 log10 CFU cm2 on pig carcasses and from 2.7 to 3.8 log10 CFU cm2 on cattle carcasses. With regard to EU Regulation (EC) No 2073/2005, TVCs were mainly considered satisfactory (pig: 81.3%; cattle: 71.4%). Amongst sites, the back (pigs) and neck (cattle) tended to yield higher TVCs. Enterobacteriaceae were detected in low counts on 23.9% of pig carcasses and 21.7% of cattle carcasses. Amongst abattoirs, Enterobacteriaceae prevalence on pig and cattle carcasses ranged from 2.0% to 56.0% and from 0.0% to 55.0%, respectively. Consequently, criteria of the EU Regulation proved to be a suitable tool for the appraisal of microbiological results (TVCs) from pig and cattle carcasses from small-scale abattoirs. Because the occurrence of Enterobacteriaceae on carcasses was too infrequent to ensure log normality, frequencies should be compared for these organisms.  2007 Elsevier Ltd. All rights reserved. Keywords: Pig and cattle carcasses; Small-scale abattoirs; Total viable counts; Enterobacteriaceae; Regulation (EC) No 2073/2005

1. Introduction The new food safety legislation of the European Union (EU) regulates every level of the food chain, sets down specific rules for food of animal origin, and affects all member countries and third parties wishing to export food into the EU. The onus of compliance is placed on food operators. They must apply compulsory self-checking programs following the hazard analysis critical control point (HACCP) approach. In terms of slaughtering, risk-based monitoring of hygiene conditions in accordance with HACCP principles is required. Strict maintenance of good practices of slaughter hygiene is of central importance to ensure both public health protection and meat quality. To enable risks involved to be estimated and appropriate measures to be

*

Corresponding author. Tel.: +41 44 635 8651; fax: +41 44 635 8908. E-mail address: [email protected] (R. Stephan).

0309-1740/$ - see front matter  2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2007.06.025

taken, analysis of the slaughter process has to be complemented by microbiological verification data (Brown et al., 2000; Spescha, Stephan, & Zweifel, 2006; Vanne, Karwoski, Karppinen, & Sjoberg, 1996). Microbiological data are necessary for the implementation and maintenance of HACCP-based systems and can be used for verification of carcass contamination in compliance with performance criteria (Brown et al., 2000; Vanderlinde, Jenson, & Sumner, 2005; Zweifel, Baltzer, & Stephan, 2005). For these purposes, indicator organisms rather than pathogens should be monitored (Brown et al., 2000; Untermann, Stephan, Dura, Hofer, & Heimann, 1997). To ensure EU-wide standards, Regulation (EC) No 2073/2005 set out performance criteria for total viable counts (TVC), Enterobacteriaceae, and Salmonella on carcasses (Anon, 2005). Hence, mean log TVCs are satisfactory, acceptable, and unacceptable, when they are <4.0, 4.0–5.0, and >5.0 cm2 (pig carcasses) or <3.5, 3.5–5, and >5.0 cm2 (cattle carcasses), respectively. For Enterobacteriaceae, mean log counts <2.0, 2.0–3.0, and >3.0 cm2 (pig carcasses) or

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<1.5, 1.5–2.5, and >2.5 cm2 (cattle carcasses) are satisfactory, acceptable, and unacceptable, respectively. Whereas EU requirements are generally fulfilled in highcapacity abattoirs, the risk-based approach including microbiological verification and implementation of HACCP principles poses a challenge to small-scale abattoirs. The aim of this study was (i) to obtain data on the microbiological contamination of pig and cattle carcasses at small-scale Swiss abattoirs, (ii) to investigate abattoir-, site- and species-specific differences, and (iii) to compare the results with EU performance criteria. 2. Materials and methods 2.1. Abattoirs and carcass sampling This study is based on investigations carried out in 17 abattoirs distributed throughout Switzerland. The median value of annually slaughtered pigs and cattle accounted for 600 and 220, respectively. At abattoirs A–M, samples were obtained from pigs and cattle, whereas, only one species was sampled at abattoirs N, O, P, and Q. Sampling of pig carcasses was performed during a six-month period (December 2005 to May 2006), and comprised 50 carcasses at each abattoir and five at each visit. At abattoirs A, H, I, and N, which were selected due to their different contamination levels, sampling was continued for another six months. Sampling of cattle carcasses was performed during 12 months and the number of carcasses sampled varied. In total, 3000 samples from 750 pig carcasses and 2140 samples from 535 cattle carcasses were examined. Samples were obtained by excision at the neck, belly, back, and ham for pigs, and the neck, brisket, flank, and rump for cattle. A sterile coring punch was used to mark a tissue area of 5 cm2, which was then excised using a scalpel and forceps. Sampling was performed after dressing or within 3 h of chilling. 2.2. TVCs and Enterobacteriaceae Each individual sample was homogenized in 10 ml of 0.85% sodium chloride solution in a stomacher. Suspensions were plated with a spiral plater (IUL SA, Barcelona, Spain) onto plate count agar (Oxoid Ltd., Hampshire, UK) and violet red bile glucose agar (VRBG agar, BBL, Cockeysville, Md.). Plate count agar was incubated aerobically for 72 h at 30 C, and VRBG agar was incubated anaerobically for 48 h at 30 C. The detection limit was at 4.0 · 101 CFU cm2.

positive, when Enterobacteriaceae were detected on one of the sites. Values were compared by reference to the values for mean log ðxÞ and log mean ðlog A ¼ x þ ln 10  SD2 =2Þ. Evaluation was based on log N (log of the summed counts), when the occurrence was too infrequent (<80%) to ensure log normality (Gill & Jones, 2000; McEvoy, Sheridan, Blair, & McDowell, 2004). Corresponding statistics that differed by <0.5ðxÞ or <1.0 log CFU cm2 (log A and log N) were regarded as similar for practical purposes. Statistical analysis was performed using Stat View 4.02 (Abacus Concepts Inc., Berkeley, CA). An analysis of variance and the Bonferroni procedure were used to analyze TVC differences among abattoirs and sites. Possible relationship between TVCs and animal species or seasons was analyzed by the t-test. To compare Enterobacteriaceae occurrence among abattoirs, sites, species and seasons, contingency tables (Chi square test, Fisher’s exact test) were used. 3. Results 3.1. TVCs from pig carcasses For pig carcasses, mean log ðxÞ and log mean (log A) TVCs ranged from 2.4 to 4.2 log CFU cm2 and from 2.8 to 4.3 log CFU cm2, respectively (Table 1). To compare results of each abattoir, TVCs were depicted as box plots (Fig. 1). TVC differences between abattoirs were significant (P < 0.05) in 59.0% of the comparisons. Carcasses from abattoirs A, G, L, and N yielded TVCs >3.8 log CFU cm2 (P < 0.05). At abattoirs A, H, I, and N, TVCs were higher (P < 0.05) during summer/fall than during winter/spring (Fig. 2). However, differences amongst seasons were only of minor practical significance. Amongst sites, the highest mean log TVCs were found in 10 abattoirs on the back and in four abattoirs on the neck. Generally, TVCs from the back and ham differed significantly (P < 0.05). Variance of mean log TVCs amongst sites accounted for <0.5 and 0.5–1.0 log CFU cm2 in four and nine abattoirs, respectively. With regards to EU legislation, the proportion of satisfactory pig carcasses ranged from 26.0% to 100%, where carcasses from abattoirs A and L were mainly rated as acceptable (Fig. 1). The overall percentage of satisfactory, acceptable, and unsatisfactory carcasses was 81.3%, 18.4%, and 0.3%, respectively. For the daily mean values (n = 150), which should be rated according to EU requirements, these percentages were 86.0%, 14.0%, and 0.0%. 3.2. Enterobacteriaceae results from pig carcasses

2.3. Data analysis Colony counts of individual samples were expressed as log CFU cm2. Values of calculated pooled samples were obtained by calculating log mean from the four sites of each carcass. For Enterobacteriaceae, counts and frequencies were determined. Carcasses were considered as

The proportion of Enterobacteriaceae-positive sites and carcasses ranged from 0.0% to 44.0% and from 2.0% to 56.0%, respectively (Table 2). For carcasses, frequencies at abattoirs G and N were generally higher than those at the other abattoirs (P < 0.05). No consistent trends were evident subject to the sampling period. In abattoir D, a

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Table 1 TVC results (log CFU cm2) obtained from pig carcasses at 15 small Swiss abattoirsa n

Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Total a b

A B C D E F G H I J K L M N O

Neck

Belly

Back

Carcassb

Ham

x

SD

log A

x

SD

log A

x

SD

log A

x

SD

log A

x

SD

log A

50 50 50 50 50 50 50 50 50 50 50 50 50 50 50

4.35 2.84 2.66 2.90 2.81 3.08 3.70 3.20 2.49 2.36 2.74 3.62 2.64 3.77 2.61

0.46 0.59 0.66 0.80 0.75 0.86 0.61 0.67 0.50 0.62 0.61 0.63 0.76 0.59 0.83

4.59 3.24 3.16 3.64 3.46 3.93 4.13 3.72 2.78 2.80 3.17 4.08 3.31 4.17 3.40

4.23 2.75 2.68 2.96 2.38 2.97 3.36 3.03 2.27 2.78 2.56 3.36 2.45 3.27 1.83

0.37 0.78 0.51 0.87 0.66 0.96 0.64 0.84 0.59 0.56 0.65 0.77 0.69 0.63 0.32

4.39 3.45 2.98 3.83 2.88 4.03 3.83 3.84 2.67 3.14 3.05 4.04 3.00 3.73 1.95

3.89 2.99 2.82 3.29 2.82 3.54 3.63 2.99 2.83 3.48 3.07 4.03 3.09 4.01 1.95

0.48 0.67 0.61 0.89 0.66 0.80 0.53 0.65 0.64 0.61 0.54 0.77 0.97 0.55 0.41

4.16 3.51 3.25 4.20 3.32 4.28 3.95 3.48 3.30 3.91 3.41 4.71 4.17 4.36 2.14

3.31 2.68 2.97 2.46 2.45 2.95 3.65 2.53 2.62 2.23 2.31 3.53 2.31 3.25 1.80

0.77 0.71 0.75 0.83 0.94 0.91 0.58 0.73 0.59 0.77 0.60 0.85 0.57 0.80 0.36

3.99 3.26 3.62 3.25 3.47 3.90 4.04 3.14 3.02 2.91 2.72 4.36 2.68 3.99 1.95

4.20 3.08 3.03 3.24 2.96 3.58 3.81 3.26 2.80 3.16 2.92 3.99 2.97 3.83 2.39

0.30 0.47 0.51 0.76 0.60 0.57 0.38 0.56 0.44 0.52 0.43 0.52 0.66 0.45 0.56

4.30 3.33 3.33 3.91 3.37 3.95 3.98 3.62 3.02 3.47 3.13 4.30 3.47 4.06 2.75

750

3.05

0.86

3.90

2.86

0.87

3.73

3.22

0.85

4.05

2.74

0.90

3.67

3.28

0.71

3.86

x, mean log CFU cm2; SD, standard deviation; log A ¼ x þ ln 10  SD2 =2, estimated log mean value. Carcass, log mean of four individual site samples.

high Enterobacteriaceae prevalence was combined with average TVCs, whereas in abattoirs A and L average frequencies were combined with high TVCs. Compared with the other sites, the back and the neck yielded the highest frequencies in 10 abattoirs. However, differences among sites were not significant in abattoirs A, B, E, F, I, K, L, M, and O. Only 65 (2.2%) samples exceeded 2.0 log CFU cm2, and eight of them, which originated mainly from the back and the neck, exceeded 3.0 log CFU cm2. With regard to EU legislation, these values mark the limits for acceptable and unsatisfactory results. The highest log N values were observed in 10 abattoirs on the back and the neck. Fig. 1. TVCs from pig carcasses of the different abattoirs (calculated pooled samples, n = 750; a, b: limits for acceptable and unsatisfactory results of Regulation (EC) No 2073/2005).

Fig. 2. TVCs from pig carcasses during the first (h, December–May) and second sampling period (n, June–November) of four abattoirs (calculated pooled samples, n = 400; a, b: limits for acceptable and unsatisfactory results of Regulation (EC) No 2073/2005).

3.3. TVCs from cattle carcasses For cattle carcasses, mean log ðxÞ and log mean (log A) TVCs ranged from 2.7 to 3.8 log CFU cm2 and from 3.2 to 4.4 log CFU cm2, respectively (Table 3). TVC differences between abattoirs were significant in only a small percentage (16.2%). Amongst sites, the highest mean log TVCs were found in nine abattoirs on the neck and in four abattoirs on the brisket. Generally, TVCs from the neck and flank differed significantly (P < 0.05). Variance of mean log TVCs amongst sites accounted for <0.5 and 0.5–1.0 log CFU cm2 in five and six abattoirs, respectively. Amongst the 12 abattoirs, in which 30 or 60 cattle carcasses were examined, the proportion of satisfactory cattle carcasses ranged from 33.3% to 93.3%, whereupon carcasses from abattoirs B, J, and Q were mainly rated as acceptable (Fig. 3). The overall percentage of satisfactory, acceptable, and unsatisfactory carcasses was 71.4%, 28.6%, and 0.0%. Based on the 10 abattoirs, in which both species and at least 30 cattle carcasses were examined, TVCs from pig and

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Table 2 Enterobacteriaceae results obtained from pig carcasses at 15 small Swiss abattoirs Necka

n

Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir

A B C D E F G H I J K L M N O

Total

Bellya

Backa

Hama

Carcassb

% POS

Max

log N

% POS

Max

log N

% POS

Max

log N

% POS

Max

log N

% POS

50 50 50 50 50 50 50 50 50 50 50 50 50 50 50

8.0 8.0 4.0 10.0 6.0 4.0 12.0 12.0 2.0 4.0 6.0 14.0 8.0 12.0 2.0

2.08 2.45 2.08 3.81 3.02 1.90 3.00 2.08 1.90 1.60 2.20 2.30 1.90 2.45 1.60

2.30 2.60 2.20 3.84 3.17 2.08 3.15 2.51 1.90 1.90 2.38 2.72 2.30 2.72 1.60

8.0 8.0 0.0 8.0 4.0 4.0 10.0 0.0 2.0 6.0 2.0 10.0 10.0 22.0 0.0

2.86 2.20 NDc 2.30 2.30 2.38 1.90 ND 1.60 1.90 1.60 1.90 1.90 2.56 ND

2.92 2.45 ND 2.56 2.38 2.45 2.51 ND 1.60 2.20 1.60 2.45 2.38 2.98 ND

10.0 8.0 18.0 24.0 2.0 6.0 18.0 0.0 4.0 16.0 6.0 10.0 6.0 32.0 0.0

1.90 1.90 3.18 3.08 1.90 1.90 2.86 ND 1.60 2.56 2.30 3.24 2.45 2.90 ND

2.38 2.80 3.31 3.44 1.90 2.20 3.08 ND 1.90 3.09 2.45 3.29 2.60 3.45 ND

4.0 10.0 20.0 10.0 4.0 2.0 44.0 2.0 6.0 4.0 2.0 4.0 4.0 28.0 0.0

1.60 1.90 3.20 3.09 1.90 1.60 2.68 1.60 2.56 2.38 1.60 2.08 1.90 2.86 ND

1.90 2.45 3.56 3.17 2.08 1.60 3.30 1.60 2.64 2.51 1.60 2.20 2.08 3.20 ND

22.0 22.0 32.0 44.0 8.0 14.0 56.0 14.0 14.0 26.0 10.0 22.0 16.0 56.0 2.0

750

7.5

3.81

4.10

6.3

2.86

3.61

10.7

3.24

4.18

9.6

3.20

4.01

23.9

% POS, percentage of samples from which Enterobacteriaceae could be detected; max, maximum (log CFU cm2); log N, log of the total number recovered per square centimeter. b Carcass considered as positive, when Enterobacteriaceae were detected on one sampling site. c ND, no data for calculation (Enterobacteriaceae not detected). a

Table 3 TVC results (log CFU cm2) obtained from cattle carcasses at 15 small Swiss abattoirsa n

Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Total a b

A B C D E F G H I J K L M P Q

Neck

10 30 60 30 30 6 60 30 60 30 30 9 60 60 30 535

Brisket

Flank

Carcassb

Rump

x

SD

log A

x

SD

log A

x

SD

log A

x

SD

log A

x

SD

log A

3.02 3.01 2.94 3.00 3.02 1.94 2.58 2.44 3.51 2.64 2.71 2.67 2.41 3.20 3.47

1.18 0.74 0.64 0.69 0.67 0.45 0.90 0.85 0.80 1.00 0.88 1.14 0.78 0.84 1.00

4.62 3.64 3.41 3.55 3.54 2.17 3.51 3.27 4.25 3.79 3.60 4.17 3.11 4.01 4.62

3.37 3.08 2.83 2.83 2.17 3.06 2.36 2.32 2.46 3.00 2.85 2.79 2.37 2.34 2.92

0.99 0.77 0.83 0.82 0.82 1.18 0.74 0.92 0.74 0.79 0.95 0.84 0.68 0.81 1.04

4.50 3.76 3.62 3.60 2.94 4.66 2.99 3.29 3.09 3.72 3.89 3.60 2.90 3.10 4.17

2.85 2.84 2.56 2.31 2.11 2.80 2.10 2.04 1.98 3.53 2.01 1.84 2.04 2.00 2.42

1.22 1.13 0.79 0.96 0.85 1.40 0.73 0.72 0.56 1.08 0.74 0.49 0.53 0.55 0.92

4.56 4.31 3.28 3.37 2.94 5.06 2.71 2.64 2.34 4.87 2.64 2.12 2.36 2.35 3.39

3.81 2.69 2.57 2.52 2.22 2.76 2.43 2.26 2.43 2.86 2.75 2.43 2.34 2.49 2.46

0.57 1.05 0.82 0.90 0.83 0.96 0.81 0.69 0.79 0.79 1.03 0.92 0.85 0.82 0.84

4.18 3.96 3.34 3.45 3.01 3.82 3.19 2.81 3.15 3.58 3.97 3.40 3.17 3.26 3.27

3.78 3.42 3.02 3.10 2.96 3.23 2.80 2.78 3.20 3.57 3.18 3.04 2.65 3.07 3.46

0.56 0.63 0.66 0.58 0.61 1.00 0.66 0.63 0.60 0.57 0.78 0.74 0.69 0.57 0.74

4.14 3.88 3.52 3.49 3.39 4.38 3.30 3.24 3.61 3.94 3.88 3.67 3.20 3.44 4.09

2.90

0.90

3.83

2.61

0.86

3.46

2.28

0.87

3.15

2.51

0.90

3.44

3.07

0.70

3.63

2

2

x, mean log CFU cm ; SD, standard deviation; log A ¼ x þ ln 10  SD =2, estimated log mean value. Carcass, log mean of four individual samples.

cattle carcasses differed significantly (P < 0.05) in the abattoirs B, G, H, I, J, and M. However, except for abattoir G, variance of mean log TVCs amongst species accounted for <0.5 log CFU cm2. 3.4. Enterobacteriaceae results from cattle carcasses The proportion of Enterobacteriaceae-positive sites and carcasses ranged from 0.0% to 50.0% and from 0.0% to 55.0%, respectively (Table 4). For carcasses, prevalence at abattoirs C and Q was generally higher (P < 0.05) than those at the other abattoirs. A high Enterobacteriaceae

prevalence was combined with average TVCs in abattoir C, whereas a very low frequency was combined with high TVCs in abattoir J. Compared with the other sites, the neck tended to yield higher frequencies. However, differences among sites were not significant in abattoirs A, B, F, G, H, J, K, L, M, and Q. Based on the 10 abattoirs, in which both species and at least 30 cattle carcasses were examined, Enterobacteriaceae frequencies from pig and cattle carcasses differed significantly only in abattoirs C, G, and J (P < 0.05). Only 39 (1.8%) samples exceeded 2.0 log CFU cm2, and 11 of them, which originated mainly from the neck, exceeded 2.5 log CFU cm2.

C. Zweifel et al. / Meat Science 78 (2008) 225–231

Fig. 3. TVCs from cattle carcasses of the different abattoirs (calculated pooled samples, n = 535, abattoirs C, G, I, M, P: n = 60, abattoirs B, D, E, H, J, K, Q: n = 30, abattoirs A, F, L: n < 30; a, b: limits for acceptable and unsatisfactory results of Regulation (EC) No 2073/2005).

4. Discussion Comparability of the results with published data is hampered by the fact that surveys differ in terms of sampling methods, sampling sites, and evaluation modes. Moreover, counts determined from a chilled carcass might be significantly different from those after dressing as a consequence of surface desiccation (Kinsella et al., 2006; Spescha et al., 2006). In Switzerland, only data from large-scale abattoirs were available and mean TVCs obtained by swabbing ranged from 2.2 to 3.7 log CFU cm2 for pigs and from 2.1 to 3.1 log CFU cm2 for cattle (Zweifel et al., 2005). In the present baseline survey, microbiological contamination

229

on pig and cattle carcasses averaged out at 3.3 and 3.1 log CFU cm2, respectively. Baseline data from small-scale abattoirs are rare and mainly restricted to swab samples. In a small-scale abattoir in Ireland, microbiological contamination at different sites of chilled pig carcasses was between 4.5 and 4.7 log CFU cm2 (Bolton et al., 2002). An Australian baseline study yielded an average TVC value of 3.1 log CFU cm2 for chilled cattle carcasses from very small plants (Phillips, Sumner, Alexander, & Dutton, 2001). In a further study, average TVCs accounted for only 1.8 log CFU cm2 (Sumner et al., 2003). Abundant data on the microbial quality of carcasses is available from large-scale abattoirs, albeit mainly swabbing was used. Especially for beef carcasses, comparisons with data from North America are additionally hampered by the common application of decontamination interventions (Koohmaraie et al., 2005). In Europe, the use of such treatments is not permitted or is discouraged (Bolton, Doherty, & Sheridan, 2001). In recent studies on the microbial quality of Irish carcasses, average TVCs from dressed pig carcasses (O’Brien, Lenahan, Sweeney, & Sheridan, 2007), chilled pig carcasses (Pearce et al., 2004), dressed cattle carcasses (McEvoy et al., 2004), and chilled beef carcasses (Murray, Gilmour, & Madden, 2001) accounted for about 3.7, 3.5, 3.2, and 2.8 log CFU cm2. Moreover, mean TVCs recently obtained by excision or swabbing in a study from the United Kingdom accounted for 4.5 and 2.4 log CFU cm2 on pig carcasses, and for 2.1 and 1.4 log CFU cm2 on cattle carcasses, respectively (Hutchison et al., 2005). In spite of the limited comparability, the results obtained from carcasses from small-scale Swiss abattoirs did not differ substantially from those from

Table 4 Enterobacteriaceae results obtained from cattle carcasses at 15 small Swiss abattoirs n

Necka % POS

Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Abattoir Total a

A B C D E F G H I J K L M P Q

Brisketa Max

log N

% POS

Flanka Max c

Rumpa

Carcassb

log N

% POS

Max

log N

% POS

Max

log N

% POS

10 30 60 30 30 6 60 30 60 30 30 9 60 60 30

20.0 10.0 50.0 20.0 16.7 0.0 3.3 3.3 16.7 0.0 3.3 0.0 5.0 8.3 20.0

1.90 1.60 2.90 2.30 2.45 ND 1.90 1.60 1.90 ND 1.60 ND 1.90 2.72 2.30

2.08 2.08 3.78 2.75 2.81 ND 2.08 1.60 2.64 ND 1.60 ND 2.20 2.83 2.75

0.0 6.7 10.0 10.0 3.3 16.7 1.7 0.0 0.0 0.0 6.7 0.0 1.7 0.0 10.0

ND 2.20 2.30 1.60 1.90 1.60 1.60 ND ND ND 1.60 ND 1.60 ND 4.23

ND 2.30 2.72 2.08 1.90 1.60 1.60 ND ND ND 1.90 ND 1.60 ND 4.24

10.0 3.3 21.7 3.3 0.0 0.0 3.3 0.0 0.0 0.0 0.0 0.0 1.7 0.0 6.7

1.60 1.60 3.24 1.90 ND ND 2.30 ND ND ND ND ND 1.60 ND 2.83

1.60 1.60 3.43 1.90 ND ND 2.38 ND ND ND ND ND 1.60 ND 2.86

10.0 10.0 8.3 6.7 3.3 16.7 0.0 3.3 0.0 3.3 6.7 0.0 3.3 0.0 6.7

1.60 2.20 3.32 1.90 2.45 1.60 ND 1.60 ND 2.45 1.90 ND 2.08 ND 2.20

1.60 2.38 3.38 2.08 2.45 1.60 ND 1.60 ND 2.45 2.08 ND 2.20 ND 2.30

30.0 20.0 55.0 33.3 23.3 33.3 8.3 6.7 16.7 3.3 16.7 0.0 11.7 8.3 36.7

535

13.8

2.90

4.05

3.7

4.23

4.32

3.9

3.32

3.79

3.9

3.32

3.55

20.0

2

% POS, percentage of samples from which Enterobacteriaceae could be detected; max, maximum (log CFU cm ); log N, log of the total number recovered per square centimeter. b Carcass considered as positive, when Enterobacteriaceae were detected on one sampling site. c ND, no data for calculation (Enterobacteriaceae not detected).

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large-scale abattoirs. Interestingly, the microbiological contamination of pig carcasses was also on a comparable level in Swedish low- and high-capacity facilities, whereas numbers of bacteria from cattle carcasses differed by 0.9 log CFU cm2 (Hansson, 2001). With regard to performance criteria of Regulation (EC) No 2073/2005, the majority of TVCs from pig and cattle carcasses was rated as satisfactory. Due to the restricted and inconsistent number of slaughtered animals, not only daily mean values but also each carcass should be rated. Moreover, daily mean trends may conceal the presence of acceptable or unsatisfactory carcasses. Consequently, EU criteria proved to be a suitable tool for the appraisal of microbiological results from pig and cattle carcasses from small-scale abattoirs. However, these criteria can only be seen as baselines and it would be beneficial for each slaughter facility to establish its own reference data, and customize HACCP plans to match process- and site-specific circumstances (Pearce et al., 2004; Vanne et al., 1996). Enterobacteriaceae accounted only for a small subset of microorganisms. Because log normality was not ensured, frequencies and log N values were compared. In view of the comparison of log N values, interference by a single high value and the necessity of identical and sufficient numbers of sampled carcasses must be considered. The overall proportion of Enterobacteriaceae positive sites and carcasses accounted for 9% and 24% (pigs) and 6% and 22% (cattle), respectively. Enterobacteriaceae provided indications of abattoir-specific hygienic weak points leading to fecal contamination that were not clearly apparent from TVC data. Determination of Enterobacteriaceae constitutes therefore an essential part of slaughter hygiene verification also in small-scale abattoirs. In large-scale Swiss abattoirs, Enterobacteriaceae prevalence on pig and cattle carcasses ranged from 4% to 41% and from 12% to 54%, respectively (Zweifel et al., 2005). In recent studies from Ireland, Enterobacteriaceae were detected by swabbing (i) from pig carcasses in 76% of the pooled samples and in 40% to 80% of the site samples (O’Brien et al., 2007), and (ii) from cattle carcasses in 45 to 67% of the site samples (McEvoy et al., 2004). Moreover, Enterobacteriaceae were recently detected by excision or swabbing on 55% and 56% of pig carcasses, and on 23% and 8% of cattle carcasses, respectively (Hutchison et al., 2005). To evaluate the reasons for the increased carcass contamination observed in some small-scale abattoirs, a detailed analysis of the slaughtering process including microbiological data is necessary (Spescha et al., 2006), because carcasses may be contaminated despite the absence of visible contamination (Gill, 2004; Tergney & Bolton, 2006). Acknowledgements The authors thank the staffs of the slaughterhouses involved in this study for facilitating access to their operations and for assistance with the collection of data.

References Anon. (2005). Commission Regulation (EC) No. 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Journal of the European Union, L338, 1–26. Bolton, D. J., Doherty, A. M., & Sheridan, J. J. (2001). Beef HACCP: Intervention and non-intervention systems. International Journal of Food Microbiology, 66, 119–129. Bolton, D. J., Pearce, R. A., Sheridan, J. J., Blair, I. S., McDowell, D. A., & Harrington, D. (2002). Washing and chilling as critical control points in pork slaughter hazard analysis and critical control point (HACCP) systems. Journal of Applied Microbiology, 92, 893–902. Brown, M. H., Gill, C. O., Hollingsworth, J., Nickelson, R., II, Seward, S., Sheridan, J. J., et al. (2000). The role of microbiological testing in systems for assuring the safety of beef. International Journal of Food Microbiology, 62, 7–16. Gill, C. O. (2004). Visible contamination on animals and carcasses and the microbiological condition of meat. Journal of Food Protection, 67, 413–419. Gill, C. O., & Jones, T. (2000). Microbiological sampling of carcasses by excision or swabbing. Journal of Food Protection, 63, 167–173. Hansson, I. B. (2001). Microbiological meat quality in high- and lowcapacity slaughterhouses in Sweden. Journal of Food Protection, 64, 820–825. Hutchison, M. L., Walters, L. D., Avery, S. M., Reid, C.-A., Wilson, D., Howell, M., et al. (2005). A comparison of wet–dry swabbing and excision sampling methods for microbiological testing of bovine, porcine, and ovine carcasses at red meat slaughterhouses. Journal of Food Protection, 68, 2155–2162. Kinsella, K. J., Sheridan, J. J., Rowe, T. A., Butler, F., Delgado, A., Quispe-Ramirez, A., et al. (2006). Impact of a novel spray-chilling system on surface microflora, water activity and weight loss during beef carcass chilling. Food Microbiology, 23, 483–490. Koohmaraie, M., Arthur, T. M., Bosilevac, J. M., Guerini, M., Shackelford, S. D., & Wheeler, T. L. (2005). Post-harvest interventions to reduce/eliminate pathogens in beef. Meat Science, 71, 79–91. McEvoy, J. M., Sheridan, J. J., Blair, I. S., & McDowell, D. A. (2004). Microbial contamination on beef in relation to hygiene assessment based on criteria used in EU Decision 2001/471/EC. International Journal of Food Microbiology, 92, 217–225. Murray, K. A., Gilmour, A., & Madden, R. H. (2001). Microbiological quality of chilled beef carcasses in Northern Ireland: A baseline survey. Journal of Food Protection, 64, 498–502. O’Brien, S. B., Lenahan, M., Sweeney, T., & Sheridan, J. J. (2007). Assessing the hygiene of pig carcasses using whole-body carcass swabs compared with the four-site method in EC Decision 471. Journal of Food Protection, 70, 432–439. Pearce, R. A., Bolton, D. J., Sheridan, J. J., McDowell, D. A., Blair, I. S., & Harrington, D. (2004). Studies to determine the critical control points in pork slaughter hazard analysis and critical control point systems. International Journal of Food Microbiology, 90, 311–339. Phillips, D., Sumner, J., Alexander, J. F., & Dutton, K. M. (2001). Microbiological quality of Australian beef. Journal of Food Protection, 64, 692–696. Spescha, C., Stephan, R., & Zweifel, C. (2006). Microbiological contamination of pig carcasses at different stages of slaughter in two European Union-approved abattoirs. Journal of Food Protection, 69, 2568–2575. Sumner, J., Petrenas, E., Dean, P., Dowsett, P., West, G., Wiering, R., et al. (2003). Microbial contamination on beef and sheep carcases in South Australia. International Journal of Food Microbiology, 81, 255–260. Tergney, A., & Bolton, D. J. (2006). Validation studies on an online monitoring system for reducing faecal and microbial contamination on beef carcasses. Food Control, 17, 378–382. Untermann, F., Stephan, R., Dura, U., Hofer, M., & Heimann, P. (1997). Reliability and practicability of bacteriological monitoring of beef carcass contamination and their rating within a hygiene quality control

C. Zweifel et al. / Meat Science 78 (2008) 225–231 program of abattoirs. International Journal of Food Microbiology, 34, 67–77. Vanderlinde, P., Jenson, I., & Sumner, J. (2005). Using national microbiological data to set meaningful performance criteria for slaughter and dressing of animals at Australian export abattoirs. International Journal of Food Microbiology, 104, 155–159.

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Vanne, L., Karwoski, M., Karppinen, S., & Sjoberg, A.-M. (1996). HACCP-based quality control and rapid detection methods for microorganisms. Food Control, 7, 263–276. Zweifel, C., Baltzer, D., & Stephan, R. (2005). Microbiological contamination of cattle and pig carcasses at five abattoirs determined by swab sampling in accordance with EU Decision 2001/471/EC. Meat Science, 69, 559–566.