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255

Journal of Food Protection, Vol. 75, No. 2, 2012, Pages 255–260


doi:10.4315/0362-028X.JFP-11-272
Copyright G, International Association for Food Protection

Dispersion and Survival of Escherichia coli O157:H7 and


Salmonella Typhimurium during the Production of Marinated Beef
Inside Skirt Steaks and Tri-Tip Roasts
TIFFANY M. MURAS, KERRI B. HARRIS,* LISA M. LUCIA, MARGARET D. HARDIN, AND JEFFREY W. SAVELL

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Center for Food Safety, Meat Science Section, Department of Animal Science, Texas AgriLife Research, 2471 TAMU, Texas A&M University,
College Station, Texas 77843-2471, USA

MS 11-272: Received 3 June 2011/Accepted 23 September 2011

ABSTRACT
To determine the depth of pathogen dispersion and the ability of pathogens to survive in enhanced beef products and spent
marinade, beef inside skirt steaks and tri-tip roasts were vacuum tumbled with two commercial marinades. The marinades were
inoculated with Escherichia coli O157:H7 and Salmonella Typhimurium, resulting in an approximate count of 5.2 log CFU/ml.
Both inside skirt steaks and tri-tip roasts were vacuum tumbled for 1 h and sampled immediately after tumbling (day 0), or were
vacuum packaged, stored (ca. 4uC), and sampled on days 7 and 14. Samples of the spent marinade were taken after tumbling (day
0) and on days 3 and 7. For both marinades, Salmonella Typhimurium and E. coli O157:H7 were dispersed throughout the inside
skirt steaks during vacuum tumbling. Although Salmonella Typhimurium and E. coli O157:H7 for the skirt steaks were still
detectable after 14 days of storage, the log values were lower than those on days 0 and 7. For the tri-tip roasts, the pathogen
distribution varied, depending on the thickness of the roasts, and pathogens were detectable on days 0, 7, and 14. The spent
marinade sampled on days 0, 3, and 7 showed that the pathogens survived at refrigerated temperatures. Because pathogens can
transfer to the interior of beef inside skirt steaks and tri-tip roasts when vacuum tumbled with contaminated marinade and
survived during refrigerated storage, establishments should consider the potential food safety risks associated with reuse of
marinade during the production of vacuum-tumbled beef products.

Since the foodborne outbreak in late 1992 and early beef products, a great deal of research has addressed the risk
1993 caused by Escherichia coli O157:H7 associated with associated with the production of nonintact beef. Whereas
ground beef, the safety of beef products has been highly the results of studies have shown that the prevalence of
scrutinized. In 1994, the U.S. Department of Agriculture, pathogens such as E. coli O157:H7 on the surface of beef
Food Safety and Inspection Service (FSIS) declared E. coli subprimals is rare (5, 7, 16), recalls and illnesses associated
O157:H7 an adulterant in raw ground beef (17). In 1999, the with nonintact beef products have been reported (18–20).
FSIS clarified that the public health risk by raw beef In January 2002, the National Advisory Committee on
products contaminated with E. coli O157:H7 was not Microbiological Criteria for Foods (10) reviewed available
limited to ground beef, but also included nonintact beef data (primarily from Sporing (16)) and concluded that
products (17). These nonintact beef products include beef nonintact, blade-tenderized beef steaks do not present a
that has been injected, mechanically tenderized, or recon- greater risk to consumers if the meat is oven broiled and
structed. This definition of ‘‘nonintact’’ is consistent with cooked to an internal temperature of 60uC or higher.
the U.S. Food and Drug Administration’s Food Code, which Sporing (16) also determined that when cooked to an
defines ‘‘whole muscle, intact beef’’ as ‘‘beef that is not internal temperature below 60uC, blade-tenderized beef
injected, mechanically tenderized, reconstructed, or scored, steaks present a greater risk when compared with intact beef
and marinated’’ (21). steaks. Luchansky et al. (9) emphasized that the risk of
Since the outbreaks of 1993, beef producers and illness because of consumption of blade-tenderized steaks is
packers have spent more than $420 million on beef safety extremely small, because E. coli O157:H7 contamination of
research (12, 15). These investments resulted in the beef subprimals is very infrequent and at low levels.
publication of a significant amount of research data, best Studies have demonstrated that blade tenderization and
practices, and information to assist the industry in assessing needle injection can transfer pathogens from the surface of
the overall risk of their processes and products. Because of beef steaks to the interior tissue (8, 14). However, several
the FSIS’s expansion of adulteration to include nonintact gaps and questions remain related to the production of
nonintact products, specifically marinating. The importance
* Author for correspondence. Tel: 979-862-3643; Fax: 979-862-3075; of food safety and the emphasis of production practices to
E-mail: kharris@tamu.edu. reduce pathogens are crucial to the success of the industry.
256 MURAS ET AL. J. Food Prot., Vol. 75, No. 2

TABLE 1. Means and standard deviations for pH and salinity by (provided by Dr. Phillip I. Tarr, Seattle Children’s Hospital and
marinade for inside skirt steaks and tri-tip roasts Medical Center, Seattle, WA, which was originally isolated from
ground beef implicated in the 1993 Washington State outbreak)
Salinity
Beef product pH SD (ppm) SD were used as marker organisms to inoculate marinade A and
marinade B. Growth curves, heat resistance, and acid sensitivity of
Inside skirt steak the mutant strains were previously determined to be virtually
Marinade A 6.58 0.10 3,361.50 104.01 indistinguishable from the parent strains (4, 6). The selected
Marinade B 6.96 0.36 2,653.17 66.24 rifampin-resistant stock working cultures were maintained on
tryptic soy agar (BD, Franklin Lakes, NJ) slants and stored at 25uC
Tri-tip roast (2–4). Before inoculation into the marinades, these cultures were
Marinade A 6.24 0.19 3,333.33 103.86 transferred individually into tryptic soy broth (BD) and incubated
Marinade B 6.43 0.03 2,738.33 75.48 at 37uC for 18 h. A bacterial cocktail was prepared by mixing equal
volumes into the respective marinade, resulting in an inoculum
level of approximately 5 log CFU/ml of each pathogen. A portion
More knowledge gained on food safety production practices

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of the uninoculated as well as the inoculated marinades were
will ensure consumer confidence and reduce the risk of assayed each test day to confirm the amount of marker organisms
foodborne illness. To provide additional information that per milliliter.
establishments can use to strengthen their food safety
programs, this project evaluated the effect of inoculated Product inoculation. The inoculated marinade (A or B) and
marinade used in vacuum tumbling on pathogen penetration either three inside skirt steaks or tri-tip roasts were added to the
into two different commonly marinated beef cuts, and the vacuum tumbler (Biro, The Biro MFG Co., Marblehead, OH) and
ability of Salmonella Typhimurium and E. coli O157:H7 to tumbled for 1 h (a combination of 15 min of tumble, 5 min of rest,
and repeating of the process). One piece of product was sampled
survive in the marinated products and spent marinade during
immediately after tumbling, representing day 0. The two remaining
storage.
pieces were vacuum packaged (Cryovac B620, Sealed Air,
Duncan, SC) individually and held at 4uC to be sampled on days
MATERIALS AND METHODS
7 and 14.
Preparation of meat and marinade. Vacuum-packaged,
beef inside skirt steaks (n ~ 18, Institutional Meat Purchase Sampling and microbiological analysis. Before inoculation,
Specification 121C), and tri-tip roasts (n ~ 18, Specification negative-control surface samples of tri-tip roasts and inside skirts
185D) (13) were obtained for this project. Two different marinade were collected to measure possible presence of marker organisms
formulations, Reo TAMU Fajita Marinade (Reo Spice and by excising a sample 10 cm2 by 3 mm in depth by using a sterile
Seasoning, Inc., Huntsville, TX) and Legg’s Cajun Marinade (A. stainless steel borer, scalpel, and forceps. After tumbling, the
C. Legg, Inc., Calera, AL), hereafter referred to as marinade A and product was removed aseptically from the tumbling drum and
marinade B, respectively, were used in this study. The dry placed on sterile foil. Two plugs (5 by 5 cm by thickness of meat)
marinade was mixed according to manufacturer’s instructions. were excised from the center of either the tri-tip roast or inside skirt
Marinade A consisted of 272.15 g of dry seasoning, 29.93 g of steak.
sodium tripolyphosphate, and 1,391.14 ml of distilled water. During preliminary trials (data not shown), a two-step flaming
Marinade B consisted of 215.40 g of dry seasoning added to procedure was developed in order to reduce or eliminate cross-
986.87 ml of distilled water. contamination during dissection of the tri-tip roast plug. The
bottom and sides of each tri-tip roast plug were initially immersed
Bacterial strains and inoculum preparation. Rifampin in 95% ethanol to within 2 mm of the top surface of the plug and
(100 mg/ml)–resistant strains derived from parent strains of flame sterilized with a Bunsen burner. After flamed sterilization,
Salmonella Typhimurium (ATCC 13311) and E. coli O157:H7 the second step of the process involved heating the exterior sides

TABLE 2. Least-squares means for initial weight, final weight, retention, and thickness of product for inside skirt steaks and tri-tip roasts
processed with marinade A and marinade B
Marinade A Marinade B

Beef product Day 0 Day 7 Day 14 Day 0 Day 7 Day 14

Inside skirt steak


a
Initial wt (g) 437.00 A 595.00 A 413.00 A 673.00 A 568.00 A 585.00 A
Final wt (g) 636.33 A 893.33 A 636.33 A 952.67 A 827.00 A 866.33 A
Retention (%) 32.17 A 33.67 A 34.85 A 32.72 A 31.29 AB 29.33 B
Thickness (cm) 1.36 A 1.50 A 1.33 A 1.42 A 1.38 A 1.33 A

Tri-tip roast
Initial wt (g) 1,162.00 A 983.00 A 839.00 A 1,196.00 A 1,030.00 A 1,080.67 A
Final wt (g) 1,369.67 A 1,168.67 A 1,012.00 A 1,389.00 A 1,236.00 A 1,323.67 A
Retention (%) 15.87 A 15.61 A 17.43 A 14.25 A 16.94 A 17.99 A
Thickness (cm) 4.17 A 3.83 A 3.17 A 4.17 A 3.67 A 2.67 A

a
Least-squares means within a row lacking a common letter differ (P # 0.05).
J. Food Prot., Vol. 75, No. 2 PATHOGEN TRANSFER DURING VACUUM TUMBLING 257

TABLE 3. Means and standard deviations for counts of Salmonella Typhimurium and Escherichia coli O157:H7 by marinade for beef
inside skirt steaks and tri-tip roasts
Marinade A Marinade B

Salmonella Typhimurium E. coli O157:H7 Salmonella Typhimurium E. coli O157:H7


(log CFU/ml) (log CFU/ml) (log CFU/ml) (log CFU/ml)

Beef product Mean SD Mean SD Mean SD Mean SD

Inside skirt steak


Initial inoculuma 6.8 0.1 6.6 0.1 6.9 0.3 6.8 0.2
Before tumbleb 5.4 0.1 5.4 0.4 5.5 0.9 5.3 1.1
After tumblec 4.9 0.3 4.6 0.2 5.0 0.2 5.2 0.4
Tri-tip roast

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Initial inoculum 7.3 0.5 7.3 0.5 6.6 0.2 6.5 0.3
Before tumble 5.4 0.5 5.3 0.5 4.7 0.2 4.7 0.1
After tumble 4.8 0.2 4.9 0.3 4.7 0.3 5.0 0.1
a
Initial inoculum, concentration of cocktail prior to adding to marinade.
b
Before tumble, concentration of cocktail after adding to marinade, but before tumbling.
c
After tumble, concentration of cocktail after tumbling.

and bottom of the tri-tip roast plug by using a handheld cooking plating appropriate serial dilution on prepoured and dried
torch (Bon Jour Professional Cooking Torch, Taipei, Taiwan). The lactose–sulfite phenol red rifampin agar plates (1), which were
top of the plug was removed aseptically by making a cross- incubated for 24 h at 35uC before colonies were counted. Samples
sectional cut through the plug (ca. 3 mm deep) and it was then of the spent marinade were taken immediately after the tumbling,
placed in a sterile petri dish. After removal of top surface, the stored in glass bottles at 4uC, and sampled again on days 3 and 7.
exposed sides and bottom were again torched and then sampled as The spent marinade was plated as above.
described above, taking care not to torch the top 3-mm surface. Tri-tip and inside skirts were weighed on a calibrated digital
This procedure was continued to the geometric center of the plug. scale, both before and after tumbling to determine percent pickup.
For the inside of the skirt steak, a meat plug (5 by 5 cm by Salt concentrations and pH and were determined for each of the
thickness of meat) was removed aseptically from the center of each inoculated marinades. The pH was determined on all batches of
steak. Because of the thickness of the inside skirt steak (ca. 1.5 cm), noninoculated marinade by using a Symphony pH meter (VWR,
only the top exterior and interior samples were taken without the Suwannee, GA). Salt concentration was determined with a
two-step flaming process. The samples (5 by 5 by 0.5 cm) were concentration meter (Orion Research, Inc., Beverly, MA).
placed into a sterile petri dish, as described above. To remove the
cooked edges from the cross-sectional sample (inside skirt steaks Replication of experiment. The inoculation process of the
and tri-tip roasts), a 10-cm2 sample was excised with a sterile marinade occurred each time prior to tumbling. This process was
borer, surgical blade, and forceps, and was placed into a stomacher run in triplicate for each meat by marination combination (tri-tip
bag to which 99 ml of buffered peptone water was added. These roasts with marinade A, tri-tip roasts with marinade B, inside skirt
samples were pummeled for 1 min in a stomacher (Seward steaks with marinade A, and inside skirt steaks with marinade B).
Medical, Ltd., London, UK). Counts of rifampin-resistant E. coli The number of cross-sectional samples taken from the square plug
O157:H7 and Salmonella Typhimurium were determined by (5 by 5 cm) of the tri-tip roast varied from four to seven samples,
depending on the thickness of the roasts. When evaluating the
inside skirt steak, two samples were taken from each plug, an
exterior and an interior.
TABLE 4. Least-squares means and standard errors for interior
and exterior layer effect on Salmonella Typhimurium and
Statistical analysis. Microbiological count data were trans-
Escherichia coli O157:H7 for marinated inside skirt steaksa
formed in logarithms before performing statistical analysis. Data
Interior layer Exterior layer were analyzed with PROC GLM of SAS (SAS Institute Inc., Cary,
NC). Least-squares means were generated for main effects (day,
Marinade Mean SEM Mean SEM depth, day | depth, and rep) and separated with the PDIFF option
when appropriate, with an alpha level (P # 0.05). For the purpose
A
of discussion, it was determined that at least a 1-log difference
Salmonella would indicate a microbiological difference (11), while statistically
Typhimurium 4.1 A 0.1 4.2 A 0.2 less than a 1-log change may have differed (P # 0.05).
E. coli O157:H7 3.5 A 0.2 3.6 A 0.2
B RESULTS AND DISCUSSION
Salmonella Samples of the marinade were plated as controls, and
Typhimurium 3.9 A 0.1 3.9 A 0.1 the pH and salt concentration of the marinade (Table 1)
E. coli O157:H7 3.5 A 0.2 3.4 A 0.2
were measured. Also, there were no statistical differences in
a
Values are in log CFU per square centimeter. Least-squares the initial weights or final weights between marinade A and
means within a row lacking a common letter differ (P # 0.05). marinade B for either the inside skirt steaks or the tri-tip
258 MURAS ET AL. J. Food Prot., Vol. 75, No. 2

TABLE 5. Least-squares means and standard errors for storage day effect on counts of Salmonella Typhimurium and Escherichia coli
O157:H7 for marinated beef inside skirt steaks and tri-tip roastsa
Day 0 Day 7 Day 14

Beef product Mean SEM Mean SEM Mean SEM

Inside skirt steak


Marinade A
Salmonella Typhimurium 4.4 A 0.1 4.2 A 0.1 3.8 B 0.1
E. coli O157:H7 4.2 A 0.1 3.5 B 0.1 3.0 C 0.1
Marinade B
Salmonella Typhimurium 4.3 A 0.1 3.9 B 0.1 3.6 C 0.1
E. coli O157:H7 4.4 A 0.1 3.2 B 0.1 2.9 C 0.1

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Tri-tip roast
Marinade A
Salmonella Typhimurium 2.7 B 0.2 3.8 A 0.2 2.8 AB 0.4
E. coli O157:H7 2.8 B 0.2 3.6 A 0.2 2.8 AB 0.3
Marinade B
Salmonella Typhimurium 3.0 A 0.2 2.5 B 0.2 2.7 AB 0.2
E. coli O157:H7 3.0 A 0.1 2.2 B 0.1 2.2 B 0.2
a
Values are in log CFU per square centimeter. Least-squares means within a row lacking a common letter differ (P # 0.05).

roasts (Table 2). No rifampin-resistant organisms were vacuum tumbled with marinade A, and microbiological
detected in the uninoculated marinade or meat samples counts were not different (P . 0.05), as shown in Table 4. It
(data not shown). The concentrations (in log CFU per is evident that once the vacuum-tumbled marinade A inside
milliliter) were determined for the initial inoculum cocktail, skirt steak was stored (ca. 4uC) for 7 days, there was a
in the inoculated marinade before tumbling, and in the similar log count, both statistically and microbiologically, of
inoculated marinade after tumbling for both inside skirt Salmonella Typhimurium compared with that of day 0 for
steaks and tri-tip roasts (Table 3). It is important to note that samples (Table 5). However there was a difference (P #
the initial log value used to inoculate the marinades in this 0.05) when comparing day 7 with day 14, but there was not
experiment is higher than what would be expected in a microbiological difference shown. A decrease (P # 0.05)
contaminated marinade found in a processing establishment. in the log count in E. coli O157:H7 occurred on the inside
However, inoculum levels higher than those commonly skirt steaks after being stored for 7 days, and again after
found in industry are used in laboratory experiments to the product was stored for 14 days. There also was a
determine levels of log reductions, because using lower microbiological difference when comparing day 0 with day
levels makes it difficult to evaluate reductions in a 14 (Table 5).
laboratory setting. After processing, the microbiological counts of both
The dispersion of E. coli O157:H7 and Salmonella microorganisms were similar for the exterior and interior
Typhimurium was evident throughout the inside skirt steak samples of inside skirt steak treated with marinade B

TABLE 6. Least-squares means and standard errors for depth effect on counts of Salmonella Typhimurium and Escherichia coli O157:H7
for marinated tri-tip roastsa
Depth:

0–3 mm 3–6 mm 6–9 mm 9–12 mm 12–15 mm 15–18 mm 18–21 mm

Marinade Mean SEM Mean SEM Mean SEM Mean SEM Mean SEM Mean SEM Mean SEM

A
Salmonella
Typhimurium 4.1 A 0.2 3.5 AB 0.2 3.2 BC 0.2 2.7 CD 0.2 2.4 D 0.2 2.3 D 0.3 2.5 CD 0.4
E. coli O157:H7 3.9 A 0.2 3.4 AB 0.2 3.1 BC 0.2 2.7 BC 0.2 2.5 C 0.2 2.4 C 0.3 2.3 BC 0.5
B
Salmonella
Typhimurium 3.3 AB 0.2 3.5 A 0.2 2.9 B 0.2 2.4 C 0.2 2.1 C 0.2 1.9 C 0.3 1.6 C 0.4
E. coli O157:H7 2.9 A 0.2 3.2 A 0.2 2.7 A 0.2 2.2 B 0.2 2.0 B 0.2 1.9 B 0.3 1.4 B 0.4
a
Values are in log CFU per square centimeter. Least-squares means within a row lacking a common letter differ (P # 0.05).
J. Food Prot., Vol. 75, No. 2 PATHOGEN TRANSFER DURING VACUUM TUMBLING 259

TABLE 7. Least-squares means and standard errors for storage day effect on counts of Salmonella Typhimurium and Escherichia coli
O157:H7 for spent marinade A and marinade B for beef inside skirt steaks and tri-tip roastsa
Day 0 Day 3 Day 7

Beef product Mean SEM Mean SEM Mean SEM

Inside skirt steaks


Marinade A
Salmonella Typhimurium 4.9 A 0.2 4.6 A 0.2 4.4 A 0.2
E. coli O157:H7 4.6 A 0.4 3.8 A 0.3 4.6 A 0.3
Marinade B
Salmonella Typhimurium 5.0 A 0.2 4.7 A 0.2 4.7 A 0.2
E. coli O157:H7 5.2 A 0.2 4.4 A 0.2 5.2 A 0.2

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Tri-tip roasts
Marinade A
Salmonella Typhimurium 4.8 A 0.2 4.5 A 0.2 4.4 A 0.2
E. coli O157:H7 4.9 A 0.2 4.9 A 0.2 4.5 A 0.2
Marinade B
Salmonella Typhimurium 4.0 A 0.2 4.5 A 0.2 4.4 A 0.2
E. coli O157:H7 4.4 A 0.4 3.7 A 0.4 4.2 A 0.4
a
Values are in log CFU per milliliter. Least-squares means within a row lacking a common letter differ (P # 0.05).

(Table 4). There was a difference (P # 0.05) in log values of organisms as the depth increased and samples were taken
both microorganisms when comparing samples from day 0 toward the geometric center of tri-tips treated with marinade
with samples taken on day 7. Although there was not a B (Table 6). There were similarities of Salmonella Typhi-
microbiological difference when comparing day 0 with day 7 murium between the first two layers; however, the third
of Salmonella Typhimurium, there was a microbiological layer was similar to the first, and all other subsequent layers
difference in E. coli O157:H7 on those days (Table 5). When were not similar to any of the first three, but were similar to
comparing the results of day 7 with that of the samples on day each other. There was a microbiological difference seen
14, there was a difference (P # 0.05) in log value of both between sample depths of 0 to 3 mm and 12 to 15 mm, as
microorganisms; however, there was not a microbiological dilution of microorganisms increased as depth increased.
difference. Comparing day 0 with day 14, there was a The first three layers had similar E. coli O157:H7 counts;
microbiological difference in presence of E. coli O157:H7. however, the subsequent layers were statistically different
For the tri-tip roasts enhanced with marinade A, there (P # 0.05). There was a microbiological difference seen
was a statistical difference (P # 0.05) and a microbiological between sample depths of 0 to 3 mm and 15 to 18 mm,
difference in log values of both organisms as the depth again because dilution of microorganisms increased as depth
increased and samples were taken toward the geometric increased. There were significant statistical differences (P #
center. There was a dilution effect seen in Salmonella 0.05) seen in tri-tips sampled on day 0 compared with those
Typhimurium and E. coli O157:H7 as samples were taken stored and sampled on day 7 for both microorganisms;
from depths further toward the center of the tri-tip roast, as however, on day 14, there were similarities seen in
shown in Table 6. There were statistical differences at depths Salmonella Typhimurium compared with both days 0 and
of 0 to 3 mm compared with 6 to 9 mm; however, there were 7, and there were similarities in E. coli O157:H7 seen from
similarities between samples taken from depths of 0 to 3 mm day 7 to day 14, as shown in Table 5.
and 3 to 6 mm, as might be expected from adjacent samples. There were no differences found when comparing spent
In general, adjacent samples were similar, and those not marinades stored at refrigerated temperatures sampled on
adjacent were different as seen throughout the tri-tip roast for days 3 and 7 compared with day 0 for all marination by
both microorganisms. This appeared to be a dilution effect for meat combinations (Table 7). The overall result showed that
the transfer because as the inoculated marinade was being during the process of vacuum tumbling with inoculated
pulled into the muscle, the microorganism levels were higher marinade, the microorganisms penetrated the same distance
toward the surface and lower toward the center. There was a as the marinade into the beef product. Also, the microor-
microbiological difference between samples at depths of 0 to ganisms survived in spent marinade and in beef product
3 mm and 9 to 12 mm. This microbiological difference was a while being stored under refrigerated conditions.
change in at least a 1-log difference. For the tri-tip roasts with E. coli O157:H7 and Salmonella Typhimurium are
marinade A, there was an unexplained increase in both major food safety concerns to the beef industry. Although
Salmonella Typhimurium and E. coli O157:H7 from day 0 to the E. coli O157:H7 prevalence is typically low on beef
day 7, and then another decrease on day 14. subprimals, processors must still be concerned about
There was a statistical significant difference (P # 0.05) contaminating marinade. If processors reuse spent marinade,
and a microbiological difference in log values of both they need to be aware of the potential risk of contaminating
260 MURAS ET AL. J. Food Prot., Vol. 75, No. 2

products during subsequent marination. The survival of Escherichia coli O157:H7 in blade-tenderized beef steaks cooked
pathogens in spent marinade, and the transfer of pathogens on a commercial open-flame gas grill. J. Food Prot. 72:1404–1411.
10. National Advisory Committee on Microbiological Criteria for Foods.
into the interior during vacuum tumbling, both contribute to 2002. Escherichia coli O157:H7 in blade-tenderized, non-intact beef.
potential food safety concerns. Processors of nonintact beef U.S. Department of Agriculture, Food Safety and Inspection Service,
products must consider all potential hazards and properly Washington, DC.
address them in their food safety program. 11. National Advisory Committee on Microbiological Criteria for Foods.
2010. Parameters for determining inoculated pack/challenge study
ACKNOWLEDGMENTS protocols. J. Food Prot. 73:140–202.
12. National Cattlemen’s Beef Association. 2004. A basic look at E. coli
This project was funded, in part, by The Beef Checkoff, the Texas O157:H7: facts for beef producers. Available at: http://www.
Beef Council, E. M. ‘‘Manny’’ Rosenthal Chair in Animal Science, and the beefresearch.org/CMDocs/BeefResearch/Safety/Fact Sheets/E Coli.
Manny and Rosalyn Rosenthal Endowed Fund in the Department of Animal pdf. Accessed 11 April 2011.
Science. 13. North American Meat Processors Association. 2010. The meat
buyer’s guide. North American Meat Processors Association, Reston,
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