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Journal of Food Protection, Vol. 69, No. 5, 2006, Pages 1113±1117 Copyright ᮊ, International Association for Food Protection

A National Survey of the Microbiological Quality of Beef Carcasses and Frozen Boneless Beef in Australia

DAVID PHILLIPS,1* DAVID JORDAN,2 STEPHEN MORRIS,2 IAN JENSON,3 AND JOHN SUMNER3

1Symbio Alliance, P.O. Box 4312, Eight Mile Plains, , Australia 4064; 2Wollongbar Agricultural Institute, Department of Primary Industries, 1243 Bruxner , Wollongbar, , Australia 2477; and 3Meat and Livestock Australia, Locked Bag 991, North , Australia 2059

MS 05-418: Received 11 August 2005/Accepted 22 December 2005 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/69/5/1113/1680506/0362-028x-69_5_1113.pdf by guest on 28 September 2021

ABSTRACT

The third national baseline microbiological survey of Australian beef carcasses and frozen boneless beef was conducted in 2004. Carcasses (n ϭ 1,155) sampled at 27 slaughter establishments had a mean aerobic plate count (at 25ЊC) of 1.3 log CFU/cm2. Escherichia coli was isolated from 8.0% of the carcasses, with a mean count of Ϫ0.8 log CFU/cm2 for positive samples. On samples from 24 boning (fabrication) plants (n ϭ 1,082), the mean aerobic plate count for frozen boneless beef was 1.3 log CFU/g, and the mean count for the 1.8% of samples with detectable E. coli was 1.5 log CFU/g. E. coli O157: H7 was isolated from 1 of 1,143 carcasses and from 0 of 1,082 boneless samples. Salmonella was isolated from 0 of 1,155 carcasses and from 1 of 1,082 samples of boneless product. No Campylobacter spp. were isolated from carcasses or boneless beef. Coagulase-positive staphylococci were isolated from 28.7% of beef carcasses and 20.3% of boneless beef samples, and positive samples had a mean count of 0.3 log CFU/cm2 and 0.8 log CFU/g, respectively.

National microbiological surveys of meat products as- ysis critical control point systems, with commensurate in- sist in the identi®cation of opportunities for improving food vestment in operator training, improved refrigeration, and safety. They provide data that can be used to validate reg- on-site laboratory facilities. The United States had imple- ulatory systems and to de®ne the performance standards mented a pathogen reduction ®nal rule (known as the that are incorporated into regulations. Individual processors MegaReg) (14), which required many changes to Australian can use the ®ndings to re®ne process control and to judge processing of meat for export to the United States. The progress in improving product hygiene relative to the re- industry's second baseline, designed primarily to assess the mainder of their industry. The data from these surveys may initial impact of these changes, was based on data from also be useful for risk assessment and for de®ning future sponge samples taken from chilled carcasses to be consis- research priorities. When the surveys are repeated at regular tent with the MegaReg and on samples drilled from cartons intervals using comparable techniques, they provide valu- of frozen meat. To provide a basis for comparison with the able insight into medium- and long-term trends in product ®rst baseline study, excision samples also were taken from hygiene. In 1993 through 1994, the Australian meat indus- beef carcasses. try commissioned its ®rst baseline study of the microbio- The second national baseline established that mean log logical quality of Australian meat (16). Data were collected APCs for carcasses and frozen manufacturing meat as a from samples excised from chilled carcass surfaces and whole remained in the range of 2 to 3 log units. E. coli was from core samples drilled from cartons of frozen boneless detected on 10.3% of carcass samples and on 5.3% of fro- meat destined for manufacturing. In this study, mean aer- zen meat samples, and pathogen prevalence was similar to obic plate counts (APCs) for beef carcasses and boneless that in the ®rst baseline study (11). beef were in the 2 to 3 log units; Escherichia coli was Since these surveys, the factors that drive changes in detected on 22% of beef carcasses and in 17% of boneless meat hygiene both in Australia and abroad have again al- beef samples. Pathogens were present at a very low prev- tered. All Australian processing establishments are now re- alence. The ®rst baseline study established a benchmark for quired to operate under a single Australian standard for the Australian meat against which subsequent performance of production of meat products for human consumption (6). the industry could be compared. Thus, unlike in earlier surveys, there is presently no dif- In 1998, the industry commissioned a second baseline ference in mandatory quality assurance practices between study in the wake of substantial changes in domestic reg- establishments that service the export market and those that ulation and reforms initiated in major export markets. For serve the domestic market. Concerns about product safety example, all slaughter and boning facilities had recently in the international meat market and among consumers have implemented quality assurance plans based on hazard anal- not abated. The third national survey of microbiological attributes * Author for correspondence. Tel: (ϩ617) 3340 5700; Fax: (ϩ617) 3219 of beef carcasses and frozen boneless beef in Australia was 0333; E-mail: [email protected]. conducted to provide objective evidence of the combined 1114 PHILLIPS ET AL. J. Food Prot., Vol. 69, No. 5 effectiveness of the Australian regulatory system and in- bit and transferred to sterile plastic bags with a sterile pair of dustry initiatives for improving the safety of these products. kitchen tongs. The aims of the present study were to (i) assess the change Transport of samples to the laboratory. All samples were in microbiological quality of chilled beef carcasses since packed in insulated containers with chiller packs and a tempera- 1998 as measured by the sponge-swabbing method and (ii) ture logger for transportation to a laboratory accredited by the assess the change in microbiological quality of frozen bone- National Association of Testing Authorities. Upon arrival at the less beef since the 1993 through 1994 survey. laboratory, samples were held at 2 to 4ЊC until examination. To standardize the times between sample collection and analysis, MATERIALS AND METHODS samples were analyzed between 18 and 24 h of collection. In most cases, analyses were conducted on the day of arrival at the labo- Design of the study. Samples were collected from February ratory. Internal air temperature histories of the sample transit con- through April (summer sampling) and from July through October tainer obtained during transit were used to determine whether tem- (winter sampling) 2004. Samples were collected from abattoirs in perature abuse had occurred. Samples whose temperatures had each of the ®ve mainland Australian states. In all, samples were exceeded 10ЊC were not analyzed. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/69/5/1113/1680506/0362-028x-69_5_1113.pdf by guest on 28 September 2021 collected from 27 abattoirs and 24 boning (fabricating) establish- ments whose combined production accounted for Ͼ75% of Aus- Microbiological analysis of sponge samples. Three sponge tralian beef production; participation in the survey was optional. samples were collected from each carcass; one was used for de- Almost all of the establishments in the survey were under the tection of E. coli O157:H7, one was used for Salmonella, and the jurisdiction of the Australian Quarantine and Inspection Service. third was used for all other analyses (APC, E. coli, Enterobacte- The number of carcasses sampled at each abattoir was weighted riaceae, coagulase-positive staphylococci, and Campylobacter). according to the volume of processing, which varied from 300 to To eliminate bias between the right and left sides of the carcass, 3,800 head per day. At larger abattoirs, a limit of 30 carcasses per sponges were randomly directed to each test. day was imposed to ensure the plant was visited on more than one occasion. Detection of E. coli O157:H7. A 225-ml volume of modi®ed The livestock processed during this study re¯ected the full EC broth (Oxoid, Adelaide, Australia) with 0.02 g/liter novobiocin range of husbandry practices, age, breed, and climatic effects (Calbiochem, Bad Soden, Germany) was added to one of the across Australia. Cattle were most typically from grass-fed or sponge bags, which was then squeezed by hand 10 times and Њ rangeland production systems (beef breeds) or were dairy types incubated at 37 C overnight according to AOAC method 991.14 culled from predominantly grass-fed milking herds. Approximate- (7). The following day, the Dynalbeads anti-O157 method of im- munomagnetic separation (Dynal Australia, Melbourne, Australia) ly 10% of all cattle processed in Australia have spent a minimum was followed as per the manufacturer's instructions. Positive sam- 70 days in a feedlot prior to slaughter. ples were subcultured, and isolates were sent to the laboratories Samples from beef carcasses. Selection of carcasses and of Queensland Health (, Australia) or to Food Science subsequent sampling was performed by a team of trained tech- Australia (Brisbane) for the detection of genes encoding Shiga nicians. Samples were collected after approximately 14 h of active toxins. E. coli strains positive for the O157 antigen and containing chilling (range, 12 to 24 h). Sample collection days were Tuesday a gene for Shiga toxin were reported as number of E. coli O157: 2 through Friday (kill days were Monday through Thursday) to al- H7 cells detected in 300 cm . low for adequate carcass chilling. Individual carcasses were se- Detection of Salmonella. Buffered peptone water (225 ml) lected for sampling using a systematic random approach. From was added to the sponge bag, which was then squeezed by hand the total lot of carcasses accessible to the technicians at a plant at 10 times and incubated for 20 h at 37ЊC to allow resuscitation of any time, samples were collected at regular intervals until the damaged cells. Aliquots of resuscitated cultures were inoculated required number of carcasses had been sampled. Separate poly- into mannitol selenite cystine broth (Oxoid) and incubated at 37ЊC urethane sponges (Whirlpak speci-sponge, Nasco, Fort Atkinson, for 24 h or into Rappaport-Vassiliadis medium (Oxoid) and in- Wis.) moistened with buffered peptone water (25 ml) were used cubated at 42ЊC for 24 h according to Australian Standard method to obtain swab samples from each side of the selected carcasses; AS 1766.2.5 (2). Each enriched culture was inoculated onto bril- 2 a composite sample was taken by sponging a 100-cm area at each liant green agar and xylose lysine desoxycholate agar (Oxoid) and of the butt, ¯ank, and brisket regions of each carcass side as de- incubated at 37ЊC for 24 h. The identity of typical colonies was tailed in the MegaReg methodology. A third sponge was used to con®rmed biochemically with Microbact 24E or 12A strips (Ox- swab areas adjacent to those swabbed with the second sponge on oid). Positive samples were subcultured onto nutrient agar slopes the same carcass side. and sent to the Queensland Public Health Laboratory (Brisbane, Although excision samples are considered more accurate than Australia) for serotyping. Results were reported as presence or swabs (10), swabs are now the standard method for appraising absence of Salmonella cells per 300 cm2. carcass hygiene in many countries, including Australia, New Zea- land, and the United States. For large-scale surveys in commercial Determination of APCs and concentrations of coliforms, settings, the swab technique is preferred. E. coli, Enterobacteriaceae, coagulase-positive staphylococci, and Campylobacter on carcasses. Buffered peptone water (25 ml) Samples from frozen boneless beef. Samples of boneless was added to the sponge bag, which was squeezed by hand 10 beef were collected from randomly selected frozen cartons that times. Serial dilutions were prepared in 0.1% peptone water with had been in a freezer for usually no longer than 1 month. A sys- 1-ml aliquots. For APCs, duplicate pour plates were prepared ac- tematic random selection process similar to that used for carcasses cording to the Australian Standard method AS 1766.1.3 (1) and and constrained by the degree of access to cartons within a cold incubated at 25ЊC for 96 h. Colonies were then counted, and the room was applied but with no intentional bias with regard to the number of CFU per square centimeter was recorded. The limit of day of processing. Approximately 150 g of meat was drilled from detection (LOD) was 0.4 CFU/cm2. E. coli concentrations were eight or nine different locations in each carton with a sterile drill estimated by placing 1-ml aliquots of both the initial solution and J. Food Prot., Vol. 69, No. 5 MICROBIOLOGICAL QUALITY OF AUSTRALIAN BEEF 1115

TABLE 1. Microbiological pro®le of Australian chilled beef carcasses (n ϭ 1,147) Concn (log CFU/cm2)

Prevalence 90th 95th 99th Microorganisms (%) Mean Median SD percentile percentile percentile Maximum

APCa,b 96.0 1.3 1.2 0.8 2.3 2.8 3.5 5.8 Coliformsc,d 15.2 Ϫ0.6 Ϫ0.8 0.8 0.6 1.0 2.1 2.2 E. colic,d 8.0 Ϫ0.8 Ϫ1.1 0.7 0.4 0.7 1.7 1.7 Enterobacteriaceaec,d 20.5 Ϫ0.6 Ϫ0.8 0.8 0.6 1.2 2.2 2.3 Coagulase-positive staphylococcib,c 28.7 0.3 0.3 0.7 1.4 1.6 2.4 3.0 a All counts were incremented by 1 CFU/cm2 before log transformation. b Limit of detection is 0.4 CFU/cm2. c Counts are for positive samples only. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/69/5/1113/1680506/0362-028x-69_5_1113.pdf by guest on 28 September 2021 d Limit of detection is 0.04 CFU/cm2. appropriate dilutions onto duplicate E. coli Petri®lms (3M, Syd- than or equal to the LOD of the other year. Prevalence for the ney, Australia) that were then incubated at 37ЊC for 48 h. Colonies survey year with the lowest LOD was then derived from these were counted as per the manufacturer's instructions and AOAC recoded data. All data were analyzed with the statistical package method 991.14 (7). The LOD was 0.04 CFU/cm2. Enterobacte- SPSS Base 13.0 for Windows (SPSS Australiasia, North Sydney, riaceae numbers were estimated by placing 1-ml aliquots of both Australia), and the results were cross-checked twice by separate the initial solution and appropriate dilutions onto duplicate En- analyses in STATA (release 8.1, Stata Corporation, College Sta- terobacteriaceae Petri®lms that were then incubated at 37ЊC for tion, Tex.) and SPlus (version 6.2, Insightful Corporation, Seattle, 24 h according to AFNOR method 3M 01/6-09/97 (5). Colonies Wash.). were counted as per the manufacturer's instructions. The LOD was 0.04 CFU/cm2. Coagulase-positive staphylococci concentrations RESULTS AND DISCUSSION were determined using Australian Standard method AS 1766.2.4 Microbiological status of beef carcasses and frozen (4), where 0.1-ml aliquots were spread onto dried plates of Baird boneless beef. All samples received at the laboratory had Њ Parker agar (Merck, Melbourne, Australia) and incubated at 37 C been kept below 10ЊC and were analyzed. A microbiolog- for 48 h. Colonies with typical morphology (gray black, shiny, ical pro®le of Australian beef carcasses produced at 27 es- and convex with a narrow entire margin surrounded by a zone of clearing) were picked off the plate for coagulase testing using tablishments is presented in Table 1. The mean APC was 2 rabbit blood plasma. The LOD for coagulase-positive staphylo- 1.3 log CFU/cm ; counts at the 90th, 95th, and 99th per- cocci was 0.4 CFU/cm2. Campylobacter concentrations were de- centiles were 2.3, 2.8, and 3.5 log CFU/cm2, with a max- termined according to Australian Standard method AS 1766.2.13 imum of 5.8 log CFU/cm2. Coliforms were detected on (3), in which 100 ml of Preston medium (Oxoid) was added to 15.2% of samples, for which the mean APC was Ϫ0.6 log 13.5 ml of initial carcass sponge solution and incubated at 42ЊC CFU/cm2 and the maximum was 2.2 log CFU/cm2. E. coli for 48 h. Aliquots (1 ml) were plated on Preston agar and on was detected on 8.0% of samples, for which the mean APC Skirrow agar (Oxoid) plates, which were incubated at 42ЊC for 48 was Ϫ0.8 log CFU/cm2 and the maximum was 1.7 log h. Typical colonies were counted, and the results were expressed CFU/cm2. Enterobacteriaceae were detected on 20.5% of 2 as presence or absence per 162 cm . samples, for which the mean APC was Ϫ0.6 log CFU/cm2 Analysis of boneless beef. From each sample of approxi- and the maximum was 2.3 log CFU/cm2. Coagulase-posi- mately 150 g, a subsample of 25 g was examined for E. coli O157: tive staphylococci were detected on 28.7% of samples, for H7, Salmonella, and Campylobacter; results for each organism which the mean APC was 0.3 log CFU/cm2 and the max- were reported as presence or absence in 25 g. For APCs, 10 g of imum was 3.0 log CFU/cm2. boneless meat was added to peptone water (90 ml) and macerated A microbiological pro®le of boneless beef produced at in a Stomacher BA 7021 (Seward, Worthington, UK) for 2 min. 24 establishments is presented in Table 2. The mean APC Aliquots (1 ml) were plated for APCs and counts of coliforms, E. was 1.3 log CFU/g, and counts at the 90th, 95th, and 99th coli, coagulase-positive staphylococci, and Enterobacteriaceae. percentiles were 2.3, 2.7, and 3.5 log CFU/g, with a max- The LOD was 5 CFU/cm2. imum of 5.5 log CFU/g. Coliforms were detected on 5.5% Statistical analysis. All counts were converted to log values of samples, for which the mean APC was 1.3 log CFU/g for convenience of interpretation. For APC, a value of 1 was add- and the maximum was 2.9 log CFU/g. E. coli was detected ed to all counts so that nondetections were assigned a log value on 1.8% of samples, for which the mean APC was 1.5 log of 0. For all other microorganisms, nondetections were not as- CFU/g and the maximum was 2.8 log CFU/g. Enterobac- signed a value prior to log transformation. When prevalence data teriaceae were detected on 7.1% of samples, for which the from different survey years were compared and when these data mean APC was 1.3 log CFU/g and the maximum was 3.0 were from test protocols with different detection limits, the data were corrected to provide a fair basis of comparison by taking the log CFU/g. Coagulase-positive staphylococci were detected results as CFU per square centimeter or CFU per gram for the on 20.3% of samples, for which the mean APC was 0.8 log survey year with the lowest LOD and recoding each observation CFU/g and the maximum was 2.3 log CFU/g. as negative when the result was less than the LOD for the other On chilled beef carcasses, Salmonella and Campylo- year (the higher LOD) or as positive when the result was greater bacter were not recovered from any of 1,155 samples, and 1116 PHILLIPS ET AL. J. Food Prot., Vol. 69, No. 5

TABLE 2. Microbiological pro®le of Australian frozen boneless beef (n ϭ 1,082) Concn (log CFU/g)a

Prevalence 90th 95th 99th Microorganisms (%) Mean Median SD percentile percentile percentile Maximum

APCb 82.5 1.3 1.3 0.8 2.3 2.7 3.5 5.5 Coliformsc 5.5 1.3 1.2 0.6 2.4 2.6 2.9 2.9 E. colic 1.8 1.5 1.3 0.8 2.7 2.8 2.8 2.8 Enterobacteriaceaec 7.1 1.3 1.2 0.6 2.0 2.6 3.0 3.0 Coagulase-positive staphylococcic 20.3 0.8 0.7 0.3 1.0 1.7 2.2 2.3 a Limit of detection is 5 CFU/g. b All counts were incremented by 1 CFU/g before log transformation. c Counts are for positive samples only. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/69/5/1113/1680506/0362-028x-69_5_1113.pdf by guest on 28 September 2021

E. coli O157:H7 was recovered from only 1 sample (0.1%). for both the 1998 and 2004 surveys, all improved their E. coli O157:H7 and Campylobacter were not recovered mean APCs. For comparing the prevalence of E. coli be- from any of 1,082 drilled samples of frozen boneless beef, tween surveys, a common LOD of 5 log CFU/g was used. and Salmonella was recovered from 1 sample (0.1%). The prevalence was 11.6% in the 1993 through 1994 sur- vey and 1.8% in both the 1998 and 2004 surveys. Comparison with previous baseline surveys. Simi- A comparison of the results of this survey with those larities in the methodology used in all three surveys al- lowed comparison of the microbiological status of beef car- of previous surveys conducted in 1993 through 1994 and casses and boneless beef. In the 1998 and 2004 surveys 1998 revealed an improvement in the microbiological qual- when carcass samples were obtained by sponge sampling, ity of Australian beef. The most plausible explanation for there was a reduction in mean APC from 2.4 to 1.3 log the improvement is the investment made by the Australian CFU/cm2 (distribution of counts is shown in Fig. 1). Of 17 industry in food safety systems during the past decade and beef-processing establishments providing data for both the the heightened awareness of safety issues among personnel 1998 and 2004 surveys, 15 improved their mean APCs. at all levels of the cattle and beef industries. Investments From 1998 to 2004, the prevalence of E. coli on beef car- have been made by both regulators and industry of®cials. casses was reduced from 10.3 to 8.0%, whereas the mean In this coregulatory framework, new regulations have been APC for E. coli among positive samples was Ϫ0.4 log enacted and enforced by the regulators, and the industry CFU/cm2 in both 1998 and 2004. These comparisons for has implemented risk-based quality systems and staff train- E. coli prevalence were made after correcting for a differ- ing and has invested in buildings, equipment, and chilling ence in LODs between the 1998 and 2004 surveys, which systems. were 0.08 and 0.04 CFU/cm2, respectively. The coregulatory approach has been adopted across all In all three baseline surveys, samples of frozen bone- of the Australian meat industry. Most of the establishments less meat were obtained in exactly the same manner (dril- in the industry are part of the present survey, i.e., they are ling of cartons). However, there were differences in some medium and large plants with slaughter volumes of 300 to microbiological techniques between the 1993 through 1994 3,800 head per day. These products are exported to global survey and the 1998 and 2004 surveys. In the earliest sur- markets and used to supply the domestic market. Excluded vey, APCs were determined with agar plates rather than from this survey were the very small plants (VSPs), which Petri®lm, and E. coli concentrations were determined by a typically exist to service communities that are often remote most-probable-number method. from main population centers. Information on the hygienic In the 1993 through 1994 survey, the mean APC of performance of these VSPs in the coregulatory environment frozen boneless beef samples was 2.8 log CFU/g, whereas recently became available from a separate survey in South in 1998 and 2004 it was 2.5 and 1.3 log CFU/g, respec- Australia of 3 VSPs slaughtering 60 to 250 head per day tively. Of 11 beef-processing establishments providing data and 11 slaughtering 1 to 30 head per day (13).

FIGURE 1. Frequency distribution of APCs (log CFU per square centimeter) from Australian beef carcasses, 1998 to 2004. J. Food Prot., Vol. 69, No. 5 MICROBIOLOGICAL QUALITY OF AUSTRALIAN BEEF 1117

The mean APCs at abattoirs and VSPs were 1.7 and elle Blowes (Australian Quarantine and Inspection Service), and Paul Van- 1.8 log CFU/cm2, respectively, compared with 1.3 log derlinde (Food Science Australia) for their advice as part of a steering group that oversaw the design and implementation of the study. CFU/cm2 for the plants surveyed in the current national baseline study. In the current survey of large plants, E. coli REFERENCES was detected on 8.0% of carcasses compared with 8.4 and 1. Anonymous. 1991. Food microbiologyÐgeneral procedures and 28.4% carcasses at South Australian VSPs and abattoirs, techniquesÐcolony countÐpour plate method. Australian Standard respectively. At 9 of 11 VSPs, E. coli was not detected on method AS 1766.1.3. Standards Australia, Sydney. any of 54 carcasses sampled; prevalences at the other 2 2. Anonymous. 1991. Food microbiologyÐSalmonella. Australian Standard method AS 1766.2.5. Standards Australia, Sydney. plants were 16 and 50%. 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