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Meat Science 85 (2010) 640–644

Contents lists available at ScienceDirect

Meat Science
journal homepage: www.elsevier.com/locate/meatsci

Spray application of liquid smoke to reduce or eliminate Listeria monocytogenes

surface inoculated on frankfurters
Elizabeth M. Martin a, Corliss A. O’Bryan b,*, Robert Y. Lary Jr. c, Carl L. Griffis a, Katherine L.S. Vaughn a,
John A. Marcy d, Steven C. Ricke b,d, Philip G. Crandall b
a
Department of Biological and Agricultural Engineering, University of Arkansas, Fayetteville, AR 72704, USA
b
Department of Food Science and Center for Food Safety, University of Arkansas, 2650 Young Ave., Fayetteville, AR 72704, USA
c
Sysco Corporation, 1390 Enclave Parkway, Houston, TX 77077, USA
d
Department of Poultry Science, Division of Agriculture, University of Arkansas, Fayetteville, AR 72704, USA

a r t i c l e i n f o a b s t r a c t

Article history: In a simulated post process contamination scenario liquid smoke was sprayed on the frankfurters after
Received 30 April 2009 peeling, and then inoculated with Listeria monocytogenes (Lm). Samples that did not receive a liquid
Received in revised form 6 November 2009 smoke spray remained at approximately 2 log cfu/cm2 during the 48 h of storage while the levels on
Accepted 11 March 2010
the liquid smoke treated frankfurters continued to decline until they were below detection level
(1 cfu/100 cm2). A shelf-life study lasting 140 days indicated that liquid smoke suppressed the growth
of Lm for up to 130 days. An application of 2 or 3 ml liquid smoke at packaging resulted in at least a
Keywords:
1 log reduction of Lm within 12 h post packaging.
Liquid smoke
Listeria monocytogenes
Ó 2010 Elsevier Ltd. All rights reserved.
Frankfurters

1. Introduction
Listeria monocytogenes (Lm) is a Gram-positive, non spore form-
ing rod that can cause a disease in humans known as listeriosis.
Although listeriosis can occur in healthy adults, most (80%) of
the cases occur in immunocompromised persons, pregnant wo-
men, newborns, or the elderly (Schuchat, Swaminathan, & Broome,
1991). A pregnant woman is likely to experience only mild discom-
fort, but the Listeria infection can cause a miscarriage, premature
birth or stillbirth; in addition newborns infected during pregnancy
are at increased risk of dying (Painter & Slutsker, 2007). Although
there is considerable data obtained from outbreaks of listeriosis,
the vast majority of the cases are isolated and sporadic (Painter
& Slutsker, 2007). Mead et al. (1999) estimated that twice as many
cases of listeriosis actually occurred as were reported and pro-
jected that 2518 cases of listeriosis occur each year, with 504 cases
resulting in death.
The realization that Listeria infections could be considered as a
foodborne illness stems from the 1981 investigation of a large
number of cases of listeriosis in Canada which was subsequently
traced to coleslaw (Schlech et al., 1983). Since this recognition,
investigations of Listeria outbreaks as well as sporadic cases of lis-
teriosis have implicated a variety of foods, but a common charac-
teristic of the foods is that the consumer eats them without
* Corresponding author. Tel.: +1 479 575 5328; fax: +1 479 575 6936.
E-mail address: cobryan@uark.edu (C.A. O’Bryan).
cooking (Norton & Braden, 2007). Many of these ‘‘ready to eat”
foods are cooked, cured or pasteurized during manufacturing but
are susceptible to post processing contamination before packaging
(Wenger et al., 1990). The United States Department of Agricul-
ture’s Food Safety and Inspection Service (USDA/FSIS) has desig-
nated frankfurters and hot dogs to be at the top of their ‘‘high
risk” foods list (USDA/FSIS, 2003) because of their long shelf life,
being marketed as ready to eat, and their high levels of consump-
tion by children or immunocompromised persons such as the
elderly.
USDA issued a ruling in 2003 that affects foods that are ready to
eat and that might be exposed to Lm in the food processing plant
after cooking, but before or during packaging (Anonymous, 2003).
These USDA guidelines give processors three alternative methods
of Lm control. Alternative 1 dictates the use of a ‘‘post-lethality
treatment” that reduces or eliminates Listeria on the product and
an antimicrobial agent that suppresses or limits the growth of Liste-
ria throughout the shelf life of the product. Alternative 2 allows
either a post-lethality treatment or an agent that suppresses or lim-
its growth of Listeria throughout shelf life. Alternative 3 allows the
use of sanitation measures only. Extensive research has been done
on post-lethality treatments and agents that suppress Lm growth,
including the use of organic salts and acids. Sodium lactate, sodium
diacetate, lactic acid, and acetic acid have been reported to have
antimicrobial effects on Lm when used alone or in combination
(Barmpalia et al., 2004; Geornaras et al., 2006; Lu, Sebranek,
Dickson, Mendonca, & Bailey, 2005; Porto et al., 2002; Samelis &

0309-1740/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.meatsci.2010.03.017
 Author's personal copy

E.M. Martin et al. / Meat Science 85 (2010) 640–644 641

Metaxopoulos, 1999). Lauric arginate, a newly introduced Gener-
ally Recognized as Safe (GRAS) antimicrobial agent has proven to
be effective as a post-lethality treatment in ham and frankfurters
(Bakal & Diaz, 2005; Luchansky et al., 2005; Martin et al., 2008).
Smoking meats for preservation is a traditional method of pres-
ervation and smoking is still practiced (Maga, 1988). Commercially
manufactured liquid smoke extracts have been approved as GRAS
and are being used as antimicrobial agents by the ready to eat
(RTE) industry. Recent studies have indicated reductions of Lm uti-
lizing commercially available liquid smoke extracts (Zesti-B and
AM3) as a surface application on frankfurters that were formulated
with or without lactate/diacetate (Gedela, Escoubas, & Muriana,
2007). Frankfurters without lactate/diacetate allowed growth of
Lm to the level of 9 log CFU in 10 weeks, while Lm levels on frank-
furters treated with liquid smoke remained below 1 log CFU during
this time. Murphy et al. (2005) combined the use of liquid smoke
(Select 23P, Red Arrow Intl., Manitowoc, Wis., USA) with steam
pasteurization on surface inoculated frankfurters and found no
growth of Lm during 47 days of storage. These studies all present
data for controlling Listeria in RTE foods. However, there is still a
need for additional research to address an effective mechanical
application of liquid smoke, the optimum time period for applica-
tion, and a way devised to integrate the antimicrobial application
equipment onto existing plant machinery, which were the objec-
tives of this research.
The specifications of this fraction were titratable acidity 1.8–2.1%,
specific gravity 1.095–1.120 at 25 °C, phenol level 0.3–0.8 mg/ml,
pH 4.25–4.85 and color light amber to yellow. The fraction was
stored at room temperature and used as received. Liquid smoke
was sprayed onto frankfurters using either a hand held spray bottle
(Fig. 1) or an AutoJet PWM control panel with a Pulsajet
10000AUH-03 spray nozzle (Spraying Systems Co., Wheaton, IL)
(Fig. 2). The pressure to the spray gun was maintained at 30 psig
and controller was set to ‘‘one shot mode”. Spray time was cali-
brated with a gram scale to deliver 1.5 ml per shot. One shot was
dispensed in the sterile weigh boat, frankfurters were added to
the boat and one shot dispensed over the top of the frankfurters.
For simulated post processing contamination frankfurters were
individually sprayed with liquid smoke using a bottle sprayer,
placed in a sterile stainless steel pan and inoculated (see Section
2.6). For shelf-life studies, frankfurters were individually sprayed
with liquid smoke using a bottle sprayer, inoculated with Lm,
placed in a sterile pouch and vacuum sealed (see Section 2.7).
For the simulated two-stage application process, the AutoJet
sprayer was used as described (see Section 2.7).
2.4. Microbiological analysis
At set times (as described in each experimental design) vacuum
pouches (3 mil Barrier Pouches, Ultravac Solutions) containing

2. Materials and methods

2.1. Frankfurters

Frankfurters were formulated without lactate/diacetate and

thermally processed in a commercial processing plant using the
following formulation: mechanically separated chicken (55.7%),
high fat pork trim (14.7%), 50% fat beef (2.0%), modified food starch
(2.7%), dextrose (2.0%), corn syrup solids (1.5%), salt (2.35%), spices
(0.75%), phosphate (0.32%), nitrite (0.039%), and water (19%). After
stuffing, the frankfurters were thermally processed in a continuous
run oven, cooked to a minimum internal temperature of 170 °F and
held at that temperature for 10–15 min. Frankfurters were deliv-
ered to our lab, refrigerated and held at 4 °C prior to the study.

2.2. Bacterial cultures

Six strains of Lm were used in these studies; five strains (ARS Fig. 1. Spray bottles for hand delivery of antimicrobials, control sterile water on the
V67, ARS V72, ARS V113, ARS V125, and ARS 105) were obtained left, liquid smoke (AM3) on the right.
from Dr. M.E. Berrang at USDA Agricultural Research Service, Ath-
ens, GA. Lm strain LCDC 81-861 (4b) was obtained from Dr. M.
Johnson at the Department of Food Science, University of Arkansas,
Fayetteville, AR.
Stock cultures were maintained frozen at 80 °C. One loop of
the frozen stock cultures of each strain of Lm was inoculated into
tryptic soy broth with 0.06% yeast extract (TSBYE; Becton Dickin-
son, Sparks, MD) and incubated at 37 °C for 18–20 h. One loop of
each strain was streaked for isolated colonies onto Modified Oxford
agar (MOX: Becton Dickinson, Sparks, MD). Individual colonies
were picked and grown in TSBYE for two or three additional pas-
sages to build up inoculum levels. One ml was taken from each
six cultured strains and placed in a tube and vortexed to form
the inoculum ‘‘cocktail”. The cocktail was diluted with sterile
0.1% peptone water (PW) to a concentration of 105/ml.

2.3. Liquid smoke

Fig. 2. Spray technique for frankfurters, using an AutoJet PWM control panel with a
Pulsajet 10000AUH-03 spray nozzle (Spraying Systems Co., Wheaton, IL). Half of the
A refined liquid smoke fraction (AM-3, Mastertaste, Inc., Cross- liquid smoke was dispensed in the weigh boat, frankfurters added, and other half of
ville, TN) with reduced color and flavor was used in these studies. liquid smoke sprayed on top of frankfurters.
 Author's personal copy

642 E.M. Martin et al. / Meat Science 85 (2010) 640–644

control or treated frankfurters were removed from refrigeration
(4 °C) and aseptically opened. Sterile 0.1% PW was added to the
pouch at the rate of 9 ml per frankfurter and the pouches were
hand massaged to release attached Lm. Serial 10-fold dilutions
were made with 0.1% sterile PW and plated onto MOX for Lm
counts. Plates were incubated at 37 °C for 72 h and enumerated.
Sampling was done in triplicate. Total aerobic plate counts were
done on Petrifilm™ aerobic plate count which was incubated at
37 °C for 48–72 h. Lactic acid bacteria were enumerated on Man–
Rogosa–Sharp agar plates (MRS: Becton Dickinson and Co., Sparks,
MD) incubated at 30 °C for 5 days, using the MGC AnaeroPack Sys-
tem (Mitsubishi Gas Chemical Company of America, Inc., New York,
NY 10017).
2.5. Antimicrobial activity on post application contaminated
frankfurters
All manipulations were carried out in a Labconco Class II Bio-
safety Cabinet (Labconco Corporation, 8811 Prospect Avenue, Kan-
sas City, Missouri 64132-2696). To simulate application just after
peeling the frankfurters from the casings the liquid smoke was ap-
plied to the frankfurters prior to inoculation. Frankfurters were
individually hand-sprayed to simulate in process plant application
of the liquid smoke with either 3 ml of liquid smoke or 3.0 ml ster-
ile deionized water. Frankfurters were then placed in sterile stain-
less steel pans, and surface inoculated with 105 CFU/ml of the six
strain Lm ‘‘cocktail” to provide 1 ml of inoculum per three frank-
furters, and the inoculum was dispersed over the frankfurters by
gently shaking the pans. Containers were sealed with sterile lids,
covered with aluminum foil to retain moisture within the contain-
ers, and placed at refrigerated storage temperatures, approxi-
mately 4 °C. After 0, 2, 24, 48 h, nine frankfurters were chosen
randomly from treatment or control containers. Three frankfurters
per treatment were placed into a sterile plastic bag and 9 ml of PW
was added to each bag for a 10 1 dilution of the inoculum, serial
10-fold dilutions were made and plated onto MOX agar.
The weigh dishes containing the samples were carefully placed
into new vacuum pouches and sealed at 100 kPa with a Koch
Ultravac sealer (Ultravac Solutions, Kansas City, MO). Pouches
were either analyzed immediately (0 h) or stored at 4 °C until the
8 or 12 h sampling time. Samples were processed as described
above, using only MOX agar for plating.
3. Results
3.1. Antimicrobial effect on frankfurters contaminated post application
Fig. 3 is a graphical representation of the effect of liquid smoke
applied to frankfurters after their casings (used during cooking)
have been removed. After the liquid smoke application the frank-
furters were subsequently surface inoculated with Lm. This simu-
lated the post process scenario where an antimicrobial spray
would immediately follow the casing peeler and then contamina-
tion of the frankfurters could take place in the processing plant be-
fore packaging. The control samples remained at approximately
2 log cfu/cm2 during the 48 h of storage while the Lm levels on
the liquid smoke treated frankfurters continued to decline until
they were below detection level (1 cfu/100 cm2) at 48 h.
3.2. Shelf life of post treatment contaminated frankfurters
The 140 day shelf-life study indicated that liquid smoke sup-
pressed the growth of Lm for up to 130 days (Fig. 4). Aerobic plate
counts (data not shown) on liquid smoke treated samples exhib-
ited counts similar to those on MOX, and characterization of sev-
eral colonies from the aerobic plate counts indicated these
colonies were primarily Lm. Aerobic counts of samples not treated
with liquid smoke were also too numerous to count at the dilutions

2.6. Shelf life of post application surface contaminated frankfurters

Frankfurters were hand-sprayed with approximately 1.8 ml per

frankfurter with either liquid smoke or sterile deionized water.
Frankfurters were allowed to drip momentarily and then were
placed in vacuum pouches (three frankfurters per pouch). Pouches
were placed in a Biosafety cabinet where 0.5 ml of the approxi-
mately 106 CFU/ml Lm ‘‘cocktail” inoculum was added to each
pouch, manually massaged for 2 min and vacuum sealed. Samples
were stored at approximately 4 °C for shelf life testing. After 0, 30,
60, 90, 100, 110, 120, 130, and 140 days, pouches were opened Fig. 3. Effect of liquid smoke on survival of Lm surface inoculated on frankfurters.
aseptically, 18 ml of PW was added and the pouches were hand
massaged to release attached Lm. Serial 10-fold dilutions were
made with PW and plated onto MOX agar for Lm counts, Petri-
film™ for aerobic plate counts and MRS for lactic acid bacteria
counts.

2.7. Simulated two-stage application of liquid smoke

For this portion of the study, eight frankfurters were transferred

into vacuum pouches (20.3  30.5 cm, 3 mil) and 1 ml Lm ‘‘cock-
tail” inoculum (approximately 105 CFU/ml) was added to each
pouch. Inoculated product was massaged, by hand, for 2 min. Poly-
styrene weigh dishes (14.6 cm square) were sprayed with ½ of the
total application of liquid smoke and inoculated frankfurters were
carefully transferred to the dish. The second ½ aliquot of liquid
smoke was sprayed on top of the frankfurters. The total amount
of liquid smoke added was 1, 2, or 3 ml. Positive control samples Fig. 4. Survival of Lm on frankfurters surface inoculated with Lm after treatment
were placed in weigh dishes without application of liquid smoke. with liquid smoke during 140 day shelf life.
 Author's personal copy
E.M. Martin et al. / Meat Science 85 (2010) 640–644
plated, and characterization of several of these colonies also re-
vealed them to be predominantly Lm. Lactic acid bacteria plate
counts (data not shown) of liquid smoke samples showed no
noticeable growth up to 110 days. After 110 days there were sim-
ilar plate counts to those of MOX. Only a small number (2–3 logs)
of colonies resembling lactic acid bacteria were seen at 130 days,
post-inoculation of the liquid smoke samples.
3.3. Simulated two-stage application of liquid smoke
Although shelf life results indicated that an ‘‘in-process” appli-
cation of liquid smoke could be capable of achieving an initial
1 log reduction of Lm and would suppress growth of Lm through-
out shelf life we considered a second alternative, application of li-
quid smoke at packaging. The two-stage application of 2 or 3 ml
liquid smoke at packaging resulted in at least a 1 log reduction of
Lm at 8 and 12 h post packaging (Fig. 5). To verify that the liquid
smoke would sufficiently cover the frankfurter surfaces, a food
dye was added to the liquid smoke and 3 ml of this dyed liquid
smoke was added to the packaged product and vacuum sealed.
From careful visual observation of the sample it was noted that
the dyed solution uniformly covered all areas of the frankfurters
including the crimped ends of the frankfurters (data not shown).
4. Discussion
Both the control and the liquid smoke treatments showed a 2-
log decrease from inoculation levels at 2 h, possibly due to loss
in purge dilution effects. In agreement with Gedela et al. (2007) li-
quid smoke administered as an antimicrobial for control of Lm also
exhibited an initial 1 log reduction and a suppression of Lm growth
when used post contamination. This demonstrated that there was
a positive impact of using liquid smoke as an antimicrobial just
after removing the casing and before packaging. Potentially, if
there were random, low levels of Lm contamination the liquid
smoke would provide an extra margin of safety.
The approximate shelf life of frankfurters is 90 days, therefore
the 140 days (20 weeks) went well beyond the 10 week shelf-life
study Gedela et al. (2007) reported, indicating that the liquid
smoke suppression from the initial lethality continued past the sta-
ted shelf life. As suggested by Gedela, the liquid smoke product has
a possible application for Alternative 1 as a post-lethality treat-
ment that reduces or eliminates Lm and can also suppress growth
of Lm on surface inoculated frankfurters through and beyond shelf
life.
A two-stage application of liquid smoke would position the
frankfurters to be sprayed with the liquid smoke at the time of pack-
aging after removal from the casing and transportation through the
plant environment. In addition, the two-stage application seems to
be a reasonable method for administering the liquid smoke in a
Fig. 5. Effects of two-stage application of liquid smoke on Lm surface inoculated
onto frankfurters.
643
fashion that would fit into existing plant equipment. This two-stage
application is similar to the Sprayed Lethality in Container (SLIC™)
method described by Luchansky et al. (2005) in their research on
hams. However, the SLIC™ method is a one-stage spray adminis-
tered within the intact package, while this two-stage application
is administered with a two section package system, where the bot-
tom ply and top ply are two separate units that are vacuum/heat
sealed after the frankfurters are placed into the bottom section.
In addition to the microbial testing, it is essential that the anti-
microbial agent does not change the product’s quality in an ad-
verse way. To address sensory concerns of liquid smoke,
consumer triangle sensory tests were performed in the Food Sci-
ence Sensory Laboratory, Department of Food Science, University
of Arkansas. Results indicated no significant difference between li-
quid smoke treated frankfurters and the control frankfurters (per-
sonal communication, Food Science Sensory Laboratory,
Department of Food Science, University of Arkansas).
5. Conclusions
This study indicated that liquid smoke was an effective antimi-
crobial for frankfurters in that it provided at least a one log initial
reduction of surface inoculated Lm and suppressed growth during
the extended shelf life of this product. A two-stage application at
the time of packaging rather than at the time of peeling also pro-
vided the initial one log reduction of Lm. No sensory changes were
noted with the use of liquid smoke on frankfurters.
Acknowledgements
This study was supported by Bar-S Foods, Inc. and Mastertaste,
Inc. Arun Ramadadran and Rick Grat from AutoJet Technologies
Division of Spraying Systems Co. were helpful with technical assis-
tance on the spray system. We would also like to thank Brandon
Beard, Carol Boger, Erik Friedly and Jim Smith for their technical
assistance.
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