***Salmonella* spp. Risk Assessment for Production and Cooking of Blade
Tenderized Prime Rib**

*Principal Investigators:*

> James L. Marsden, Ph.D. <jmarsden@oznet.ksu.edu>
>
> Randall K. Phebus, Ph.D. [rphebus@oznet.ksu.edu]{.underline}
>
> Harshavardhan Thippareddi, Ph.D. [hthippar@oznet.ksu.edu]{.underline}
>
> Curtis L. Kastner, Ph. D. [ckastner@oznet.ksu.edu]{.underline}
>
> J. Wendelberg, GRA [jwendelb@oznet.ksu.edu]{.underline}

*Collaborators:*

> Kansas State University
>
> Food Safety Consortium

***Research Update* *Submitted to USDA-FSIS ***

***July 18, 2001***

***Washington, DC***

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Department of Animal Sciences and Industry

Kansas State University

Manhattan, KS 66506

**INTRODUCTION**

The meat industry must provide consistent quality and uniformity in its
products to remain competitive. The quality characteristic that has
received primary focus is tenderness. The primary technologies used to
ensure tenderness and retail cut uniformity are blade tenderization and
restructuring; technologies very effective and critical to the economic
well being of the meat industry.

Blade tenderization is one of the most effective methods of meat
tenderization, particularly for cuts higher in connective tissue. It
also can significantly reduce the variability in tenderness regardless
of the muscle. Even though the generic microbiological quality of blade
tenderized muscle has been shown to be equivalent to non-tenderized
controls on a per gram basis (Boyd et al., 1978), bacteria may be
translocated into the muscle. Therefore, research was done to define
effective cooking schedules for resultant products.

In November 1997, the National Advisory Committee on Microbiological
Criteria for Foods (NACMCF), Meat and Poultry Subcommittee stated that
*Due to the low probability of pathogenic organisms being present in or
migrating from the external surface to the interior of beef muscle, cuts
of intact muscle (steaks) should be safe if the external surfaces are
exposed to temperatures sufficient to effect a cooked color change.*
However, if the surface of an intact muscle or muscle system is violated
by mechanical tenderization (blade tenderization), contamination may be
carried from the surface to the interior of the cut. The NACMCF Meat and
Poultry Subcommittee also stated in 1997 that there is a lack of
scientific data to address the hazards associated with those processes
that may cause translocation of pathogens to the interior of meat cuts.
Because of the widespread use of mechanical tenderization, and the
potential food safety risks it may pose, the Beef Industry Food Safety
Council (BIFSCO) identified this research as a priority for the beef
industry.

Kansas State University has successfully performed a similar project
\"*Escherichia coli* O157:H7 Risk Assessment for Production and Cooking
of Blade Tenderized and Fibrinogen Process Beef Steaks\" and presented
results to USDA-FSIS during the public meeting held in Washington, D.C.
on March 8, 1999. Results indicate that the blade tenderization process
transfers 3-4% of surface contamination to the interior of the muscle.
Cooking studies indicated that a target internal temperature of 120°F
produced greater (p≤0.05) log reductions (CFU/g) in non-tenderized (NT)
vs. tenderized (T) steaks (5.2 log reduction vs. 3.2 log reduction),
showing that blade tenderized steaks presented an increased risk.
However, at endpoint temperatures of 140°, 150°, 160° and 170°F, log
reductions were greater than 6 logs in both T and NT steaks, which
represented virtually complete destruction. At cooking temperatures
ranging from rare (130°F) to well done (170°F), there were no
differences in *E. coli* O157:H7 between intact and non-intact steaks
using the oven broiling method. Both intact and non-intact steaks are
safe for consumers when cooked to the endpoint temperatures evaluated in
the study by the oven broiling method. Although this study evaluated the
risk of *E. coli* O157:H7, other foodborne pathogens such as
*Salmonella* and *Listeria monocytogenes* have not been considered. It
is possible that the translocation of these pathogens could be different
compared to *E. coli* O157:H7 and further, the cooking protocols
required for inactivation of *Salmonella* and *Listeria monocytogenes*
could be different.

Traditional Prime Rib processing requires cooking of the rib to a
desired degree of doneness and holding at a temperature for long periods
of time. The product is normally served over the whole day or chilled at
the end of the day\'s operation and re-heated the following day in
restaurant operations. Blade tenderization is normally used when a lower
grade muscle is used or when a consistent tenderness is desired. There
were two outbreaks reported to Centers for Disease Control and
Prevention in 1971 and 1986 where Prime Rib has been implicated as a
possible source of contamination and *Clostridium perfringens* has been
identified as the etiologic agent. The cooking temperatures vary from
110 °F to 145 °F and holding for over 10 to 12 hours at approximately
120 °F. The low cooking temperature in addition to long holding times
presents unique opportunity for the pathogens to survive and cause
foodborne outbreaks. Presently, regulations are not in place regarding
the cooking and safe heating parameters have not been identified.

**Therefore, research was performed to determine the process and
preparation protocols to ensure the safety of this product**. By
validating these processes and cooking protocols against *Salmonella*
spp., suppliers and food service industries will be able to effectively
establish standard cooking recommendations for food service HACCP
programs for preparation of this product.

The objective of this research was to determine the effectiveness of
rare to well done cooking temperatures on reducing *Salmonella* spp.
populations contaminating the interior of prime rib as a result of blade
tenderization of artificially contaminated beef sub-primal surfaces.

**MATERIALS AND METHODS**

***Preparation and Cooking of Blade Tenderized Prime Rib*:** Boneless
beef ribs, roast ready (NAMP 109D) were obtained from a wholesale
vendor. The product was surface inoculated (non-fat side) to target
contamination level of 10^7^ *Salmonella* spp./cm^2^. After an
attachment period of 2 hrs, one set of prime rib was blade tenderized
(fat side down) using one pass through a Ross tenderizer with the units
conveyor moving 1.25 inches (31.75 mm) forward and 0.5 inches (12.7 mm)
laterally between each blade cycle. The 448 blades of the tenderizer
produce 32 incisions per square inch. The unit was thoroughly sanitized
and disinfected between each subprimal processed. Tenderized prime ribs
were fabricated using North American Meat Processors guidelines.

Product was held at 4°C until cooking (ca. 1 hr). A Type T thermocouple
was inserted into the geometric center of each product through the side.
Products were cooked in a conventional kitchen oven at 375 °F to a
specific end-point temperature (uncooked, 110 and120 °F) with the
individual cooking curves for each product being monitored and recorded.
At this end-point, the product was removed from the oven and tempered at
room temperature for 1 hour. The product was then be placed in a holding
oven set at 120°F for a further 2 h.

Microbiological samples were obtained after blade tenderization, after
reaching target temperature, after 1 h of tempering, after 30, 60, 120
and 180 min of holding at 120 °F. A center core of each product then was
diluted in chilled peptone water buffer to bring the meat temperature
down quickly. This sample was microbiologically analyzed for
*Salmonella* spp.

***[Salmonella spp. Cultures:]{.underline}*** A five strain cocktail of
*Salmonella* spp. was used in all investigations. Cultures were grown in
tryptic soy broth at 35°C for 18 h to stationary phase, centrifuged and
cell pellets from all five strains resuspended in 0.1% peptone water to
establish a cocktail inoculum. The suspension and inoculation volumes
for this inoculum preparation protocol are well established in our
laboratory to provide accurate target inoculation rates on meat products
by applying a light mist of the inoculum onto the exterior meat
surfaces.

**[*Enumeration of* *Salmonella spp.:*]{.underline}** Surviving
*Salmonella* spp. populations were enumerated by direct plating on
Xylose Lysine De-oxycholate Agar (XLD) and modified Xylose Lysine
De-oxycholate Agar (mXLD) for *Salmonella* spp. Although XLD is
selective for *Salmonella* spp., we have found that recovery of injured
cells is fairly inefficient on XLD which can provide an erroneous
indication of process lethality. By duplicate plating on mXLD, a much
less selective agar, a more accurate estimate of process lethality can
be obtained.

Bacterial population reductions due to cooking schedule were determined
based on a comparison to inoculated but uncooked control steaks
receiving the same processing treatment. The remainder of each product
was held at 4°C. If a specific cooking time/temperature reduces the
inoculated *E. coli* O157:H7 and *Salmonella* spp. population to below
the detection level of direct plating, these stored samples were
enriched according to modified USDA protocols. Four replications of the
experiment were performed with duplicate product being cooked and
analyzed for each cooking treatment within replications.

**RESULTS AND DISCUSSION**

Cooking of prime ribs to internal temperatures of 110 and 120°F and
subsequent holding at 120°F for 1 h resulted in reductions of 4.54 and
4.80 log CFU/g of *Salmonella* spp. from initial levels of 5.76 log
CFU/g in prime rib, respectively. Although the internal temperatures
reached during the cooking process are minimal, and are not expected to
result in destruction of *Salmonella* spp., the microbial cells on the
surface of the prime rib would be exposed to higher, lethal
temperatures. The heat transfer from the oven, to the internal sections
of the prime rib would result in a gradient, with higher temperatures
near the meat surface, with decreasing temperatures near the center,
with the center being the coldest spot.

Our initial studies with blade tenderized beef subprimals (inside
rounds) revealed translocation of *E. coli* O157:H7 present on the
surface throughout the interior of the muscle. The high level inoculum
was applied at a level of 6 log CFU/g over the top 1 cm strip, and
although a dilution effect was seen throughout the core, approximately 3
logs of *E. coli* O157:H7 were recovered at a depth of 6 cm. The
geometric center of the core, which in regard to steak cooking, is the
slowest to reach a target temperature, harbored 4 logs of *E. coli*
O157:H7. The low inoculum (3.2 log CFU/g on surface) produced a similar
trend, showing the relocation of approximately 1.8 logs to the geometric
center of the steaks. Overall, the process was found to carry 3-4% of
the surface organisms to the center of the core, regardless of surface
inoculation level.

Although cooking of tenderized steaks to a target end point temperature
of 120°F showed 3.2 log reduction, greater reductions observed in prime
rib were probably due to the larger size, resulting in longer cook times
(Phebus et al., 1999). Johnston et al. (1978) reported that salmonellae
survived on both the surface and in the core of mechanically tenderized
roasts oven cooked to an internal temperature of 130°F. The authors
hypothesized that the presence of viable salmonellae on surface could be
either due to purging of the cells from the center or survival on the
surface. However, the authors used convection cooking, where the
temperature rise would be faster compared to the conventional kitchen
oven used in the present study. Further, cooking of prime ribs involves
a \"tempering\" process, where the prime ribs are kept at room
temperature for varying times and then placed in a holding oven, at
approximately 120 °F. The \"tempering\" process, along with holding
results in greater temperature increases at the center of the prime rib,
compared to when the product is placed in a refrigerator as followed by
Johnston et al. (1978). This could have resulted in greater *Salmonella*
spp. reductions observed in the present study.

## SUMMARY AND CONCLUSIONS

Results of the present study indicate that although translocation of the
surface contamination does occur, cooking to internal temperatures ≥
110°F would result in significant reduction in potential public health
risk when accompanied by a 1 h minimum tempering step. Even though the
prime rib preparation process utilizes very low cooking temperatures,
the long cooking time and tempering period (accompanied by a significant
post-cook temperature rise) results in substantial process lethality and
a safe final product.

In this study, we intentionally inoculated prime rib with high levels of
*Salmonella* spp. in order to quantify the effect of mechanical
tenderization on the translocation of bacteria from the surface of the
beef cuts into interior of the muscle. The levels of contamination used
do not reflect levels that are likely to be present. In actual practice,
the source point of contamination for *Salmonella* spp. is at the
carcass level and contamination is prevented or reduced through
application of numerous processing steps, including validated
anti-microbial technologies and enforcement of USDA-FSIS's zero
tolerance policy for physical defects. The potential of contamination is
further reduced by the removal of the carcass surface by trimming before
mechanical tenderization.

This study only lends insight into control of risks in blade tenderized
prime rib using oven broiling. This method of cooking applies a uniform
temperature to the prime rib and also results in a longer cooking
process compared to convection ovens used in some restaurants. More
intensive evaluations of these cooking methods for adequate risk control
are warranted.

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