1-s2.0-s0168160503001077-main
TRANSCRIPT
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llb, Gary C. Smitha
Salmonella in all treatments. Bacterial populations decreased below the detection limit ( 0.4 log CFU/cm2) as early as 7 h
International Journal of Food Microbioagar media. The results indicated that acid adaptation may not cause increased resistance of Salmonella to the microbial hurdles
involved in jerky processing and that use of modified marinades in manufacturing jerky may improve the effectiveness of
drying in inactivating Salmonella.
D 2003 Elsevier Science B.V. All rights reserved.
Keywords: Salmonella; Beef; Jerky; Drying; Storage; Marination; Acid adaptation
1. Introduction Because it is nutritious (high in protein and iron, low
in fat), shelf-stable (0.751.0 moisture protein ratio),during drying or remained detectable even after 60 days of storage, depending on acid adaptation, pre-drying treatment, andaCenter for Red Meat Safety, Department of Animal Sciences, Colorado State University, Fort Collins, CO 80523-1171, USAbDepartment of Food Science and Nutrition, Colorado State University, Fort Collins, CO 80523, USA
Received 12 March 2002; received in revised form 1 November 2002; accepted 8 February 2003
Abstract
This study evaluated the influence of pre-drying marinade treatments on inactivation of acid-adapted or nonadapted
Salmonella on beef jerky during preparation, drying and storage. The inoculated (five-strain composite, 6.0 log CFU/cm2) slices
were subjected to the following marinades (24 h, 4 jC) prior to drying at 60 jC for 10 h and aerobic storage at 25 jC for 60days: (1) no marinade, control (C), (2) traditional marinade (TM), (3) double amount of TM modified with added 1.2% sodium
lactate, 9% acetic acid, and 68% soy sauce with 5% ethanol (MM), (4) dipping into 5% acetic acid and then TM (AATM), and
(5) dipping into 1% Tween 20 and then into 5% acetic acid, followed by TM (TWTM). Bacterial survivors were determined on
tryptic soy agar with 0.1% pyruvate and xylose lysine tergitol 4 (XLT4) agar. Results indicated that drying reduced bacterial
populations in the order of pre-drying treatments TWTM (4.86.0 log CFU/cm2)zAATMzMM>TMzC (2.65.0 log CFU/cm2). Nonadapted Salmonella were significantly (P< 0.05) more resistant to inactivation during drying than acid-adaptedPatricia A. KendaEffect of acid adaptation on inactivation of Salmonella during
drying and storage of beef jerky treated with marinades
Mehmet Calicioglua, John N. Sofosa,*, John Samelisa,Historically, jerky is among the oldest of meat
products that are preserved by salting and drying.
0168-1605/$ - see front matter D 2003 Elsevier Science B.V. All rights re
doi:10.1016/S0168-1605(03)00107-7
* Corresponding author. Tel.: +1-970-491-7703; fax: +1-970-
491-0278.
E-mail address: [email protected] (J.N. Sofos).www.elsevier.com/locate/ijfoodmicro
logy 89 (2003) 5165and known as microbiologically safe ( < 0.70 aw),
jerky is in high demand as a snack food and widely
available to consumers in convenience stores in North
America. Today, jerky is produced by consumers at
home as well as by industrial establishments. Con-
sequently, numerous recipes for making jerky are
available and are based on using meat from several
served.
-
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 516552species, e.g., beef, poultry, game animals, variable
preparation procedures of meat, e.g., thick or thin
slices, different marination techniques, e.g., various
ingredients, volume, time and temperature, and varia-
tions in drying processes, e.g., oven, food dehydrator
and smokehouse, and drying temperature (high vs.
low temperature). Such a large diversity in process
parameters may cause variation in effectiveness of
drying for inactivating pathogenic bacteria that may
be present on the raw material (Centers for Disease
Control and Prevention (CDC), 1995; Keene et al.,
1997). For example, Eidson et al. (2000) reported that
eight foodborne disease outbreaks occurred due to
consumption of contaminated beef jerky (six Salmo-
nella and two Staphylococcus aureus) between 1966
and 1995 in the state of New Mexico alone. A recent
report (Levine et al., 2001) by the Food Safety and
Inspection Service of the United States Department of
Agriculture (FSIS/USDA) indicated that for the period
1990 to 1999, cumulative prevalence of Salmonella in
jerky produced in the US federally inspected plants
was 0.31%.
Efficacy of the jerky-making process in inactivat-
ing foodborne pathogens has been evaluated by a
number of researchers (Holley, 1985a,b; Harrison
and Harrison, 1996; Harrison et al., 1997, 1998,
2001; Keene et al., 1997; Faith et al., 1998; Albright,
2000). Results of these studies are somewhat contra-
dictory in making recommendations to consumers
with respect to drying temperature and time. For
example, Harrison and Harrison (1996) reported that
a traditional jerky-preparation process, such as dry-
ing at 60 jC for 10 h, was sufficient to deliver a 5-log reduction of Escherichia coli O157:H7, Salmo-
nella typhimurium and Listeria monocytogenes in
marinated whole-muscle beef jerky. In contrast,
Keene et al. (1997) reported that drying at V 63jC was not a reliable method for eliminating E. coliO157:H7 in marinated (pH 4.2) whole-muscle ven-
ison jerky.
In response to the Salmonella and E. coli
O157:H7 outbreaks linked to jerky (CDC, 1995;
Keene et al., 1997), USDA/FSIS (1998) has sug-
gested cooking meat to 71.1 jC before drying toeliminate the risk of pathogens. Harrison et al. (2001)
tested the effectiveness of pre-drying heating of
inoculated beef strips at 71.1 jC, boiling in tradi-
tional marinade, post-drying heating at 57.4 jC for10 min, and traditional marinade for reducing num-
bers of foodborne pathogens during drying at 60 jCfor 10 h. The authors reported that all preparation
procedures yielded equal to or greater than 5.8, 3.9
and 4.6 log reductions of E. coli O157:H7, L. mono-
cytogenes and Salmonella, respectively, as measured
on selective agar media. Pre-heating of meat and/or
drying of jerky at high temperatures for extended
periods of time may result in a product that differs in
texture from traditional jerky and, thus, it may be of
reduced consumer acceptability. Use of chemical
intervention strategies as pre-drying treatments, how-
ever, has not been studied adequately (Albright,
2000). Such interventions can be a viable option to
avoid severe heat treatments while they may further
provide residual antimicrobial effects during storage.
These chemicals may include organic acids or salts
(e.g., acetic acid, lactates), ethanol, and food grade
surfactants (e.g., polysorbates). Gould (2001) empha-
sized the importance of designing new food preser-
vation methods/technologies to inactivate bacteria
while avoiding severe treatments that may change
desired characteristics of the food, since most of the
classical food preservation methods (e.g., chilling,
freezing, drying) slow down or inhibit growth of
bacteria rather than inactivating them. Leistner
(2000) indicated that preservation methods/technolo-
gies that simultaneously or sequentially expose bac-
teria to multiple stress factors (hurdles) lead bacterial
cells to metabolic exhaustion or homeostatic disturb-
ance, followed by cellular death.
Acid adaptation of Salmonella has been reported to
enhance its survival in acidic foods as well as to
increase cross-protection to other types of stresses
such as heat (Leyer and Johnson, 1992, 1993; Tsai
and Ingham, 1997; Wilde et al., 2000; Casadei et al.,
2001; Mazzotta, 2001). Another concern is that
stressed pathogens may exhibit lower infectious doses
and, thus, be of increased virulence, because it has
been hypothesized that populations of enteric bacteria
that are resistant to acid may not be reduced signifi-
cantly by the acidity of the gastric environment to
eventually cause infection (Gorden and Small, 1993).
Therefore, the objective of the present study was to
evaluate the effectiveness of several chemical-based
pre-drying treatments (modified marinades) on inacti-
vation of acid-adapted or nonadapted Salmonella cellsduring drying and storage of whole-muscle beef jerky.
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M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 5165 532. Materials and methods
2.1. Bacterial strains used and preparation of
inoculum
A five-strain composite inoculum of S. typhimu-
rium (ST) was used for inoculating beef slices. These
strains were SF530 (UK1), R-4 (Copenhagen,
DT104), R-5 (Copenhagen, DT104), ATCC700408,
and ATCC14028. Each strain was propagated (35 jC,24 h) and maintained on tryptic soy agar (TSA, Difco
Laboratories, Sparks, MD) slants at 4 jC. Strains weresubcultured monthly. The cultures were activated by
transferring a loopful of each strain into 9 ml of tryptic
soy broth (TSB, Difco) and incubating at 35 jC for 24h. A 0.1 ml portion of each culture was then transferred
into 9-ml tubes of glucose-free TSB for nonacid-
adapted cells and in glucose-free TSB with 1% added
glucose (Sigma, St. Louis, MO) for acid-adapted cells
(Wilde et al., 2000). After incubation at 35 jC for 2224 h, individual cultures were combined in a sterile
oak-ridge tube prior to centrifuging at 6000 rpm
(2900 g) (Eppendorf, model 5402) for 15 min at21 jC. The resulting pellet was washed once with0.1% phosphate buffered saline (PBS, Sigma) to
remove residual organic material, recentrifuged, and
then resuspended in PBS to a final volume of 100 ml.
The average level of inoculum was 7.5 log CFU/ml.
Supernatant pH values were approximately 5.1 and 7.1
for acid-adapted and nonadapted cultures, respectively.
2.2. Preparation of meat slices
Vacuum packaged and frozen ( 18 jC) beefinside rounds ( < 3 months) were purchased from the
Colorado State University Meat Science Laboratory
(Fort Collins, Colorado). Following thawing at 4 jCovernight, inside rounds were sliced at 0.6 cm thick-
ness using a food slicer (model 610, Hobart, Troy,
OH) and cut into pieces of 8.7 4.0 cm using a plastictemplate and knife. Approximately 100 slices (2.2 kg)
of meat were vacuum packaged and kept frozen at
18 jC until used (13 weeks).
2.3. Inoculation procedure
Frozen beef slices were thawed at 4 jC for 24 h
and placed on plastic trays that were covered withaluminum foil. In a laminar-flow hood, 0.5 ml of the
Salmonella inoculum was placed on the upper surface
of each slice and spread onto the entire surface area
using a sterile bent glass rod. Bacteria were allowed to
attach to the meat surface for 15 min at ambient
temperature. The beef slices were then flipped over
and the other side was inoculated following the same
procedure. The resulting level of inoculum was ap-
proximately 6.0 log CFU/cm2.
2.4. Pre-drying treatment description
Pre-drying treatments included: (i) control, no
treatment (C), (ii) marination with traditional mari-
nade (TM) (pH 4.3), (iii) increased (double the
amount) marination with modified marinade (MM)
(pH 3.0), (iv) 10-min immersion in 5% acetic acid
solution (pH 2.5), followed by TM (AATM), and (v)
sequential 15-min immersion in 1% Tween 20 solu-
tion (polyoxyethylene-20-sorbitan monolaurate) (pH
6.6), then 10-min immersion in 5% acetic acid sol-
ution (pH 2.5), followed by marination with TM
(TWTM).
2.5. Pre-drying treatment preparation and application
The TM was prepared for 1.0 kg of meat (Andress
and Harrison, 1999) as follows: 60 ml soy sauce
(Kikkoman Foods, Walworth, WI), 15 ml Worcester-
shire sauce (Heinz, Pittsburgh, PA), 0.6 g black
pepper (Heller Seasoning and Ingredients, Chicago,
IL), 1.25 g garlic powder (Excalibur Seasoning,
Pekin, IL), 1.5 g onion powder (Excalibur), and
4.35 g old hickory smoked salt (Tone Brothers,
Ankeny, IA). In the present study, 34 ml of this
marinade was spread manually onto 450 g inoculated
beef slices to cover the entire surface area using
flame-sterilized forceps. Approximately 30 ml of the
marinade remained on the meat slices.
The modified marinade was prepared for 1.0 kg
of meat as follows: 120 ml of milder soy sauce
(Kikkoman) containing approximately 4.75.0%
ethanol as preservative, 30 ml of Worcestershire
sauce, 0.6 g black pepper, 1.25 g garlic powder,
1.5 g onion powder, 4.35 g smoke-flavored salt, 3.6
ml food grade sodium-L-lactate of a 60% preparation
(Purac, Lincolnshire, IL), and 16 ml of glacial aceticacid (Mallinckrodt Baker, Paris, KY) to adjust the
-
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 516554pH to 3.0. A 77 ml portion of this marinade solution
was spread onto 450 g of beef, and mixed to cover
the surfaces of the meat slices. Approximately 60 ml
of the MM (double that of traditional marinade)
remained on the meat as determined by difference.
For treatment (iv) (AATM), meat slices were dipped
at ambient temperature for 10 min into a 5% (v/v)
acetic acid solution prepared using glacial acetic acid
(Mallinckrodt Baker) (450 ml per 450 g of meat) in
a glass container. These slices were drained for 2
min to remove excessive fluid using an empty de-
hydrator tray. Slices were then placed on a tray
covered with aluminum foil and marinated with
traditional marinade in the same manner described
for TM. For treatment (v) (TWTM), meat slices were
dipped into 1% (v/v) Tween 20 (Fisher Scientific,
Fair Lawn, NJ) solution (450 ml per 450 g of meat)
[for 15 min at ambient temperature]. Slices were
drained for 2 min, before marination as for (iv)
(AATM). Tween 20 (polysorbate 20, or polyoxy-
ethylene-20-sorbitan monolaurate) is permitted to be
used in food as an adjuvant (Anonymous, 2001). The
black pepper, garlic and onion powder had been
irradiated by their manufacturers. Following each
treatment, the slices on the trays were covered with
aluminum foil and held at 4 jC for 24 h prior todrying.
2.6. Drying
Treated and refrigerated (24 h) meat slices were
dried at 60 jC for 10 h in American Harvest Garden-master dehydrators (model FD-1000, Nesco, Chaska,
MN). The dehydrators were cylindrical in shape and
consisted of a base unit and three drying trays. The
dehydrator base unit generated hot air, which venti-
lated upward through the sides and a hole in the
middle of the trays. The target temperature was based
on the air temperature measurement taken from the
middle hole of the dehydrator. The dehydrators with
empty trays were preheated for approximately 20 min
to 60 jC (140 jF). The empty trays were thenreplaced with other trays pre-loaded with meat slices.
During drying, temperature of the dehydrator air,
through the middle hole, and the surface temperature
of meat slices on each of the bottom, middle, and top
trays were monitored using thermocouples (Type Kbeaded probes, Pico Technology Cambridge, UnitedKingdom) and real-time data-recording software (Pico
Technology). After drying, the jerky strips were held
in the dehydrators overnight to allow the moisture
level in the jerky slices to equilibrate, and then placed
into 24-oz Whirl-Pak sterile plastic bags (Nasco, Fort
Atkinson, WI) for storage at ambient temperature
(25F 1 jC).
2.7. Analysis
Two samples (1 slice per sample) per treatment
were aseptically transferred into sterile plastic bags
(Nasco) at each sampling interval. These intervals
included after inoculation, and 0 [24 h after (4 jC)inoculation and marination)], 4, 7 and 10 h during
drying for each treatment, and days 15, 30 and 60
during storage. A 25 ml portion of 0.1% sterile
buffered peptone water (BPW) (Difco) was added to
sample bags prior to pummeling for 2 min at ambient
temperature. Serial decimal dilutions were made using
9-ml BPW tubes and 0.1 ml portions were surface
plated onto each of duplicate plates of each agar
medium. Bacteria were enumerated using tryptic soy
agar (Difco) with 0.1% sodium pyruvate (Fisher
Scientific) (TSAP) (Leyer and Johnson, 1992), and
xyloselysinetergitol 4 (XLT4) (Difco) agar. All
plates were incubated at 35 jC for 48 h. The enumer-ation detection limit was 0.4 log CFU/cm2. Lowercounts on selective media were due to injury. When
numbers of bacteria dropped below the detection limit
by direct plating, enrichment of samples was done.
Briefly, the remaining portion of the pummeled sam-
ple with 25 ml BPW was incubated within the sample
bag at 35 jC for 24 h. Aliquots of 0.5 ml and 0.1 mlwere transferred to 10 ml tetrathionate (TT) broth
(Difco) and Rappaport Vassiliadis (RV) broth (Difco),
respectively, and incubated at 42 jC for 24 h. Sus-pensions were then streak plated onto brilliant green
sulfa (BGS) agar (Difco) and XLT4 agar and incu-
bated at 35 jC for 2448 h for characteristic (black)colonies of Salmonella.
In addition to microbiological analyses, pH and
water activity (aw) of beef jerky slices were deter-
mined at the same sampling intervals. The pH was
measured from samples used for microbiological
analysis (25 ml BPW added and pummeled for 2
min) using a digital pH meter (Accumet 50; FisherScientific, Houston, TX) with a glass pH electrode
-
(Hanna Instruments, Ann Arbor, MI). The aw of a
beef slice was determined using standardized meth-
ods as described in the 16th edition of Association
of Official Analytical Chemists method 978.18
(Mulvaney, 1998). One jerky slice was cut into
small pieces to fit into the plastic container and
measurement was done using a water activity meter
(Model D2100, Rotronic Instrument, Huntington,
NY).
2.8. Statistical analysis
Two independent replicates of the study were
conducted. Microbiological data were converted to
log CFU/cm2 and evaluated using a 2 2 5 5 2[(acid adaptation numbers of replicates pre-dryingtreatments drying (sampling) times agar media,respectively)] factorial design. Data were analyzed
by analysis of variance for main (fixed) effects (acid
adaptation, pre-drying treatment, drying time, and
was used for all statistical analyses. Storage data were
analyzed separately. Mean counts of surviving bacte-
rial populations between 0 and 7 h during drying were
used to determine D-values by calculating the inverse
of the slope of the linear regression line. Standard
deviations of the pH and water activity data were
calculated.
3. Results
Statistical analysis of the microbial data revealed
that the main effects of pre-drying treatment, acid
adaptation, drying time and agar media, and the
interactions of acid adaptation pre-drying treat-ment drying time and pre-drying treatment dryingdrying time agar media were significant (P < 0.05),as listed from the most effective to the least. However,
data from each agar medium are presented separately
because the sizable volume of data did not allow
emper
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 5165 55agar media) and four-way interactions between acid
adaptation, pre-drying treatment, drying time, and
agar media using the Statistical Analysis System
(version 6.1, SAS Institute, Cary, NC). Least squares
means were separated using Fishers least significance
difference test (LSD) using the general linear models
(GLM) procedure of SAS. A significance level of 0.05
Fig. 1. Mean (n= 4) temperatures of dehydrator air (middle hole air tusing a home-type food dehydrator.ature) and the surface of beef slices during drying at 60 jC for 10 hpresentation in a single figure.
3.1. Temperature
Changes in dehydrator air temperature and meat
surface temperatures during drying are shown in Fig.
1. After loading the preheated dehydrator with meat
-
slices, air temperature decreased from 60 to 40 jC atthe beginning of drying, and then gradually
increased back to 60 jC within approximately 4 h.Surface temperatures of meat from all trays reached
60F 2 jC within approximately 6 h. At the end ofdrying, temperatures of meat surfaces decreased to
room temperatures (ca. 2530 jC) within approx-imately 1 h.
Fig. 2. Survival of bacteria during preparation (marination at 4 jC, 24 h) and drying (60 jC, 10 h) of beef jerky inoculated with nonacid-des, a
h and
(1.2
acid
ic aci
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 516556adapted (A) and acid-adapted (B) Salmonella and treated with marina
pre-drying treatment or marinade prior to refrigeration at 4 jC for 24jC for 24 h, and then dried; MM, marinated with modified marinadeheld at 4 jC for 24 h, and then dried; AATM, dipped into 5% aceticdipped into 1% Tween 20 (pH 6.6) for 15 min, and then 5% acetinoculation; 0: after marination. Results are meanF standard deviation, ns determined on tryptic soy agar with 0.1% pyruvate (TSAP). C, no
drying; TM, marinated with traditional marinade (pH 4.3), held at 4
% lactate, 9% acetic acid, and soy sauce with 5% ethanol) (pH.3.0),
solution (pH 2.5) for 10 min, and then marinated with TM; TWTM,
d solution for 10 min followed by marination with TM. AI: after= 4.
-
3.2. Effect of agar media
Numbers of bacteria recovered on XLT4 in the
products inoculated with nonadapted culture were
significantly (P < 0.05) lower than those recovered
on TSAP in MM, AATM, and TWTM treatments after
4 h of drying, in all treatments after 710 h of drying
(Figs. 2 and 3), and during the entire storage period
(except for TWTM on 60 days) (Figs. 4 and 5). In the
products inoculated with acid-adapted cultures, sig-
nificantly (P < 0.05) lower counts of bacteria were
recovered on XLT4 than those on TSAP in MM,
AATM, and TWTM before drying (0 h), in all treat-
ments after 4 h of drying, in C and TM after 7 and 10
h of drying (Figs. 2 and 3) and up to 30 days during
storage (Figs. 4 and 5). MM, AATM, and TWTM
treatments became more destructive on acid-adapted
Salmonella after 7 h of drying since the difference
between the two agar media was not significant
(P>0.05). These results suggest that pre-drying treat-
ments MM, AATM and TWTM resulted in faster and
greater levels of cellular injury in Salmonella during
h) an
s det
marination. Results are meanF standard deviation, n= 4.
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 5165 57Fig. 3. Survival of bacteria during preparation (marination at 4 jC, 24(A) and acid-adapted (B) Salmonella and treated with marinades, a
treatments were as described in Fig. 2. AI: after inoculation; 0: afterd drying (60 jC, 10 h) of beef jerky inoculated with nonacid-adaptedermined on xylose lysine tergitol 4 agar (XLT4) (B). Pre-drying
-
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 516558drying, as estimated by the differences between non-
selective (TSAP) and selective (XLT4) agar media.
This is particularly true for acid-adapted cell popula-
tions in treatments C and MM.
3.3. Effect of pre-drying treatments
There was no significant (P>0.05) reduction in the
initial numbers of bacteria as determined by TSAP in
Fig. 4. Fate of surviving bacteria during aerobic storage at 25 jC for 60 day(B) Salmonella after treating with marinades and drying at 60 jC for 10 h,drying treatments were as described in Fig. 2. AI: after inoculation; 0: afteany treatment, irrespective of acid adaptation (00.9
log) (Figs. 2 and 3). However, regardless of acid
adaptation, initial bacterial numbers as determined
by XLT4 were significantly (P < 0.05) reduced after
application of MM and TWTM and holding of meat
slices at 4 jC for 24 h (0.92.1 log) (Figs. 2 and 3).Counts on AATM were significantly ( P < 0.05)
reduced in products inoculated with the acid-adapted
culture only (1.9 log) (Fig. 3).
s on beef jerky inoculated with nonacid-adapted (A) and acid-adapted
as determined on tryptic soy agar with 0.1% pyruvate (TSAP). Pre-
r marination. Results are meanF standard deviation, n= 4.
-
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 5165 593.4. Effect of drying
Regardless of acid adaptation or the recovery
media used, initial bacterial counts were significantly
(P < 0.05) reduced in all treatments after 4 h of drying
and the largest reductions caused by each treatment
were observed during this period (Figs. 2 and 3).
Bacterial populations declined further between 4 and
7 h of drying in all treatments. In contrast to declines
Fig. 5. Fate of surviving bacteria during aerobic storage at 25 jC for 60 daySalmonella after treating with marinades and drying at 60 jC for 10 h, atreatments were as described in Fig. 2. AI: after inoculation; 0: after maridetected for the first 4 h of drying, reductions between
4 and 7 h of drying were not significant (P>0.05) in
all treatments. Populations of acid-adapted bacteria
dropped below the detection limit ( 0.4 log CFU/cm2) on XLT4 in MM, AATM and TWTM products
after 7 h of drying (Fig. 3), and remained undetectable
by direct plating during storage (Fig. 5). No signifi-
cant reduction in bacterial populations was found in
any treatment inoculated with either acid-adapted or
s on beef jerky inoculated nonacid-adapted (A) and acid-adapted (B)
s determined on xylose lysine tergitol 4 agar (XLT4). Pre-drying
nation. Results are meanF standard deviation, n= 4.
-
nonadapted cultures between 7 and 10 h of drying. In
general, MM, AATM, and TWTM resulted in signifi-
cantly lower bacterial populations as determined with
both TSAP and XLT4 than the C and TM at 4, 7 and
10 h of drying, for both culture types (Figs. 2 and 3).
Populations of previously acid-adapted bacteria, as
determined by use of both agar media (Fig. 3) were
significantly (P < 0.05) lower within each treatment at
4, 7, and 10 h of drying compared to those of non-
adapted cultures (Fig. 2). Significantly (P < 0.05)
lower numbers of acid-adapted bacteria were recov-
ered even before drying (0 h) in MM, AATM, and
TWTM treatments (Fig. 3). These results indicate that
acid adaptation may sensitize Salmonella to the pro-
cessing conditions described in the present study.
Indeed, total log reductions in the numbers of bacteria
in the products inoculated with nonadapted Salmo-
nella at the end of 10 h of drying, as determined on
nonselective (TSAP) and selective (XLT4) media
were 2.63.1 for control, 3.03.1 for TM, 4.44.9
for MM, 4.14.9 for AATM and 4.85.6 for TWTM.
The corresponding numbers in products inoculated
with acid-adapted cells, which were 3.35.0 for con-
trol, 3.85.0 for TM, 6.16.0 for MM, 5.56.0 for
AATM, and 6.06.0 for TWTM clearly indicate a
negative influence of acid adaptation on Salmonella
survival during jerky processing, and in accordance to
the marinade treatment applied.
Irrespective of acid adaptation, MM, AATM and
TWTM treatments resulted in smaller D-values than
did the C and TM treatments, indicating faster inacti-
vation of bacteria during drying (Figs. 2 and 3). D-
values in products inoculated with acid-adapted cells
were smaller than in products inoculated with non-
adapted cells, indicating a possible increase in suscept-
ibility of acid-adapted cells to hot-air drying for 7 h.
3.5. Effect of storage
With the exception of treatment C, which had more
survivors than other treatments after drying, and
TWTM at 60 days, no treatment resulted in significant
reduction of the populations of nonadapted, surviving-
bacteria determined using TSAP (Fig. 4) during the
60-day storage period. On XLT4 (Fig. 5), however,
significant declines occurred in products at 15 days
nocul
10 h
d
jC f24 h
, and
bient
ic aci
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 516560Table 1
Mean pH values [(n= 4, (standard deviation)] of beef jerky slices i
various pre-drying marination treatments before drying at 60 jC for
Steps Time Inoculated with acid-adapted Salmonella
Ca TMb MMc AATM
Processing 0 h 5.56
(0.18)
5.37
(0.12)
4.34
(0.09)
4.35
(0.05)
4 h 5.75
(0.21)
5.41
(0.14)
4.68
(0.05)
4.71
(0.17)
7 h 5.81
(0.30)
5.73
(0.18)
4.69
(0.08)
4.74
(0.20)
10 h 5.87
(0.33)
5.80
(0.30)
4.84
(0.14)
4.79
(0.20)
Storage Day 15 5.86
(0.30)
5.81
(0.21)
4.89
(0.08)
4.83
(0.21)
Day 30 5.91
(0.19)
5.88
(0.17)
4.94
(0.09)
4.83
(0.09)
Day 60 5.91
(0.14)
5.90
(0.15)
4.98
(0.06)
4.89
(0.03)
a No pre-drying treatment or marinade prior to refrigeration at 4b Marinated with traditional marinade (pH 4.3), held at 4 jC forc Marinated with modified marinade (1.2% lactate, 9% acetic acid
dried.d Dipped into 5% acetic acid solution (pH 2.5) for 10 min at am
marinade.e Dipped into 1% Tween 20 (pH 6.6) for 15 min, and then 5% acetwith traditional marinade.ated with acid-adapted or nonadapted Salmonella and subjected to
and storage at 25 jC for 60 days
Inoculated with nonacid-adapted Salmonella
TWTMe C TM MM AATM TWTM
4.36
(0.06)
5.59
(0.21)
5.38
(0.22)
4.55
(0.12)
4.73
(0.11)
4.63
(0.14)
4.55
(0.10)
5.75
(0.08)
5.52
(0.01)
4.76
(0.14)
4.79
(0.09)
4.91
(0.05)
4.53
(0.05)
5.70
(0.08)
5.56
(0.03)
4.81
(0.10)
4.89
(0.10)
4.93
(0.07)
4.71
(0.21)
5.61
(0.13)
5.49
(0.18)
4.76
(0.21)
4.85
(0.19)
4.86
(0.23)
4.78
(0.21)
5.53
(0.08)
5.55
(0.10)
4.71
(0.17)
4.84
(0.11)
4.82
(0.15)
4.77
(0.10)
5.32
(0.27)
5.55
(0.03)
4.79
(0.10)
4.80
(0.05)
4.95
(0.15)
4.89
(0.04)
5.64
(0.03)
5.59
(0.10)
4.93
(0.12)
4.95
(0.07)
5.00
(0.08)
or 24 h and drying.
, and then dried.
soy sauce with 5% ethanol) (pH 3.0), held at 4 jC for 24 h, and then
temperature, drained for 2 min, and then marinated with traditional
d solution for 10 min at ambient temperature, followed by marination
-
(MM, TWTM) or 30 days (C, TM, AATM). At the end
of 60 days of storage, bacteria were still detectable in
all treatments by direct plating on TSAP. Therefore,
when the products were inoculated with nonadapted
cultures, complete elimination of the pathogen was not
achieved by any treatment within 60-day storage. In
contrast, populations of surviving bacteria in products
inoculated with acid-adapted cultures rapidly declined
within all treatments as determined on both agar media
(Figs. 4 and 5). Counts were below the detection limit
in MM, AATM, and TWTM treatments during the
entire storage period, and in C and TM by 60 days.
Salmonella populations were completely eliminated
(enrichment negative) by 15 days in MM and TWTM,
and by 30 days in AATM products, whereas viable
cells were recovered from C and TM products by
enrichment after 60 days of storage.
3.6. pH and aw
Table 1 shows pH values of each treatment
throughout the experiment. The pH values of products
from all treatments slightly increased during drying
and storage. Water activity of all products decreased
rapidly during drying, falling below bacterial growth
permitting ( < 0.84) values after 7 h of drying (Table
2). There were no clear differences in aw reductions
among individual treatments during drying and no
notable difference was found among treatments dur-
ing storage. The ultimate aw of the finished products
varied between 0.600 and 0.700. Fluctuations in awbetween sampling times were probably due to varia-
tion among slices.
4. Discussion
Results of the present study indicate that inactiva-
tion of Salmonella during drying of beef jerky is
affected by the culture history and by the type of
pre-drying treatment. Although drying reduced bacte-
rial populations in all treatments, use of MM, AATM,
and TWTM resulted in faster and greater levels of
reduction under the conditions described in this study.
Increasing the efficacy of food preservation meth-
ods, such as drying to inactivate bacteria, may be
ocula
10 h
d
)
)
)
) (0.022) (0.127) (0.018) (0.029) (0.095) (0.038)
)
0.687 0.674 0.554 0.667 0.608 0.631
)
)
jC fo24 h
, and
bient
ic aci
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 5165 61Table 2
Mean aw values (n= 4, (standard deviation)) of beef jerky slices in
various pre-drying marination treatments before drying at 60 jC for
Steps Time Inoculated with acid-adapted Salmonella
Ca TMb MMc AATM
Processing 0 h 0.961
(0.011)
0.958
(0.011)
0.952
(0.008)
0.941
(0.006
4 h 0.898
(0.016)
0.829
(0.048)
0.765
(0.012)
0.854
(0.030
7 h 0.806
(0.037)
0.732
(0.035)
0.724
(0.030)
0.730
(0.012
10 h 0.663
(0.032)
0.637
(0.095)
0.577
(0.010)
0.728
(0.010
Storage Day 15 0.664
(0.019)
0.640
(0.017)
0.554
(0.040)
0.710
(0.035
Day 30 0.649
(0.005)
0.641
(0.011)
0.578
(0.004)
0.601
(0.016
Day 60 0.652
(0.003)
0.639
(0.023)
0.606
(0.008)
0.621
(0.030
a No pre-drying treatment or marinade prior to refrigeration at 4b Marinated with traditional marinade (pH 4.3), held at 4 jC forc Marinated with modified marinade (1.2% lactate, 9% acetic acid
dried.d Dipped into 5% acetic acid solution (pH 2.5) for 10 min at am
marinade.e Dipped into 1% Tween 20 (pH 6.6) for 15 min, and then 5% acetwith traditional marinade.(0.016) (0.040) (0.030) (0.021) (0.024) (0.027)
0.665
(0.021)
0.670
(0.021)
0.600
(0.020)
0.678
(0.032)
0.636
(0.013)
0.682
(0.005)
0.645
(0.007)
0.665
(0.028)
0.693
(0.011)
0.674
(0.022)
0.637
(0.019)
0.654
(0.040)
r 24 h and drying.
, and then dried.
soy sauce with 5% ethanol) (pH 3.0), held at 4 jC for 24 h, and then
temperature, drained for 2 min, and then marinated with traditional
d solution for 10 min at ambient temperature, followed by marinationted with acid-adapted or nonadapted Salmonella and subjected to
and storage at 25 jC for 60 days
Inoculated with nonacid-adapted Salmonella
TWTMe C TM MM AATM TWTM
0.954
(0.003)
0.963
(0.004)
0.949
(0.005)
0.950
(0.005)
0.955
(0.004)
0.959
(0.003)
0.856
(0.037)
0.890
(0.033)
0.776
(0.154)
0.866
(0.016)
0.900
(0.009)
0.893
(0.046)
0.719
(0.006)
0.811
(0.018)
0.832
(0.028)
0.547
(0.095)
0.708
(0.111)
0.755
(0.017)
0.692 0.664 0.528 0.671 0.628 0.547
-
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 516562achieved by use of two approaches. The first could
include increasing the severity of existing processing
parameters (e.g., higher temperature, longer time),
which is not desirable because it can adversely affect
the quality of the food (Gould, 2001). The second
approach could be to render bacteria more vulnerable
to the effects of existing parameters. This approach
can be accomplished by designing hurdles that can
reduce the ability of bacteria to resist processing
parameters, including drying temperature. These hur-
dles may target bacterial attachment and/or homeo-
stasis (Leistner, 2000). Treatments MM, AATM and
TWTM, used in the present study, may be considered
applications of this approach. For example, Casadei et
al. (2001) reported that heat sensitivity of S. typhimu-
rium increased 100-fold in liquid media when the pH
dropped from 7.0 to 3.0 and/or in the presence of up
to 10% ethanol. Similarly, Jordan et al. (1999) and
Barker and Park (2001) reported that combinations of
organic acids or organic acid salts (e.g., 50 mmol
lactate), ethanol (5%), and low pH (3.0, HCl) pro-
vided significant reductions of stationary phase cells
of E. coli O157:H7 and L. monocytogenes in liquid
media (e.g., up to 5 logs in 4 min), suggesting cellular
death by disruption of pH homeostasis and by leading
to changes in gene expression and enzyme activity.
These findings were adopted in the present study in
order to design a relevantly modified jerky pre-drying
treatment (MM) by using commercially available soy
sauce containing approximately 5% ethanol, and add-
ing 2% of a 60% solution of sodium lactate, and 9%
acetic acid to TM. The volume of marinade solution
was also increased by using double the volume of soy
sauce and Worcestershire sauce to deliver a higher
marinade solution amount per slice than was used in
the treatment TM. The MM used in the present study
was significantly more effective in reducing the pop-
ulations of Salmonella cells on beef slices during
drying than were TM and C treatment, regardless of
acid adaptation. These findings indicated that combi-
nations of lactate, ethanol and acetic acid may have a
potential for use in destruction of pathogenic bacteria
in processed foods.
It is known that bacterial cells attached to the
surface of a product such as meat become more
resistant to stress factors such as heat than nonat-
tached cells (Humphrey et al., 1997). Another studyshowed that pre-spraying of beef carcasses inoculatedwith high levels of E. coli 0157:H7, with 5% Tween
20 followed by spraying with 2% lactic acid resulted
in significantly higher reduction of the pathogen
compared to spraying with lactic acid alone or water
(Calicioglu et al., 2002). It has been speculated that
Tween 20 might loosen or prevent cellular attachment
on the meat surface via its surfactant and hydrophobic
effects, thus making cells more vulnerable to the
effect of subsequent acid exposure. This proposed
carcass decontamination method was applied as a
pre-drying treatment in the present study (TWTM)
prior to acetic acid dip and marinating with a tradi-
tional recipe. Tween 20 (polysorbate 20, or polyoxy-
ethylene-20-sorbitan monolaurate) is permitted in
food as an adjuvant under US food legislation (Anon-
ymous, 2001). In the present study, TWTM was
slightly more effective than AATM but differences
were not significant (P>0.05). Both treatments were
significantly (P < 0.05) more effective at inactivating
Salmonella than C and TM.
Survival of the pathogen during drying was not
significantly (P>0.05) different between C and TM
jerky in the present study, indicating no additional
antimicrobial effect from TM. Although TM contains
Worcestershire sauce, it was not acidic enough (pH
4.3) to cause an appreciable reduction in the pH of the
TM product compared to the control product, given
the limited volume used per beef slice. Other research-
ers studied the effectiveness of TM in reducing
numbers of Salmonella and other pathogens. Harrison
and Harrison (1996) reported that drying of tradition-
ally marinated whole-muscle jerky at 60 jC for 10 hwas sufficient to deliver >5.0 log units reduction of E.
coli O157:H7, L. monocytogenes, and S. typhimurium,
as determined with selective agar media (bismuth
sulfite agar for Salmonella). A more comprehensive
study with E. coli O157:H7, L. monocytogenes, and
Salmonella, was carried out by Harrison et al. (2001).
The effectiveness of traditional marinade, oven-heat-
ing at 71 jC before drying, boiling in marinade priorto drying, and post-drying heating of traditionally
marinated jerky at 57.3 jC for 10 min in reducingnumbers of the bacteria was compared with whole-
muscle beef jerky during drying at 60 jC for 10 h. Atthe end of drying, total reductions from all treatments
were equal or greater than 5.8, 3.9, and 4.6 log units
for E. coli O157:H7, L. monocytogenes, and Salmo-nella, respectively, even with traditional marinade. In
-
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 5165 63the present study, although effectiveness of TM and
other treatments is greatly increased on acid-adapted
cultures, C and TM resulted in lower bacterial reduc-
tions compared to MM, AATM and TWTM during
drying and, thus, appeared to cause more rapid decline
of survivors during storage. While MM, AATM and
TWTM caused immediate bacterial injury followed
by death, C and TM caused a delayed injury resulting
in longer survival of bacteria. Unlike heat-based
interventions, which have immediate effect, modified
marinades described in this study (MM, AATM,
TWTM) may provide residual antimicrobial effect
against possible post-drying contamination.
Numbers of the pathogen were continually reduced
in all treatments until 4 or 7 h of drying and then
followed a much slower reduction, or remained
unchanged. This decelerated reduction has been
described as a tailing effect (Shadbolt et al., 2001).
In the present study, the tailing effect was seen in
almost all treatments, but to extents that were depend-
ent upon acid adaptation, pre-drying treatment and agar
media. The causes of tailing or its implications to food
safety have not been completely elucidated. Humphe-
son et al. (1998) investigated mechanisms of tailing
with Salmonella enteritidis PT4 in liquid media during
exposure to different temperatures. Their results indi-
cated that tailing was more evident at higher temper-
atures (e.g., 60 jC) than at lower temperatures (e.g., 49jC), and that tailing was reduced in the presence ofchloramphenicol, indicating that production of heat-
shock proteins may be responsible for cell protection
and the tailing (Humpheson et al., 1998). Similar
results have been reported for E. coli by Shadbolt et
al. (2001) who indicated that cells synthesize an intra-
cellular de novo protein under low aw conditions which
results in the tailing effect. The tailing effect observed
in this study, however, may have also been due to
product case hardening, potential effects of high alti-
tude, and the low humidity conditions of Colorado
(Albright, 2000). Survival characteristics of bacteria in
the tail part of the inactivation curve may raise the
question whether these bacteria become more resistant
to adverse conditions such as high acid compared to
initial bacterial populations, and thus increase their
hazardous potential. Although not evaluated in this
study, Buchanan et al. (1994) investigated nonthermal
inactivation of L. monocytogenes and reported that thetailing effect was not due to presence of amore resistantsubpopulation. Their results revealed that inactivation
rates and tailing of the pathogen in liquid media as
affected by pH and sublethal temperatures (up to 40
jC) were independent of initial population density.Nevertheless, the potential implications of tailing on
food safety and food preservation require additional
study.
There is evidence that acid adaptation of Salmo-
nella may enhance its survival in acidic foods as well
as increase cross-protection to other type of stresses
(Leyer and Johnson, 1992, 1993; Tsai and Ingham,
1997; Wilde et al., 2000; Casadei et al., 2001; Maz-
zotta, 2001). In the present study, however, the
opposite occurred. Acid-adapted cells were more
vulnerable to the secondary stress factors (drying)
alone or in combination with mild acidic environment
(marination) than nonadapted Salmonella. Similar
results were reported for Salmonella and other patho-
gens by other researchers (Dickson and Kunduru,
1995; Leyer and Johnson, 1997; Ryu et al., 1999;
Casadei et al., 2001). For example, Dickson and
Kunduru (1995) reported that acid-adapted Salmo-
nella, as compared to nonadapted Salmonella, had
equal or greater sensitivity to organic acid rinses on
the beef tissue. Likewise, Ryu et al. (1999) reported
that there was no significant difference in the survival
of acid-adapted, nonadapted and acid-shocked cells of
E. coli O157:H7 in dried beef powder during storage.
This difference might be the result of use of multiple
hurdles in the meat drying process, such as high acid,
temperature and aw, as well as the differences in acid
adaptation methods. It might be speculated that the
level of cross-protection from acid adaptation is
dependent on presence and severity of other stress
factors as a function of time. It seems that acid (e.g.,
pHV 4.8), heat (e.g., z 60 jC) and low aw (e.g.,< 0.800) may provide combinations of destructive
conditions that can overcome any cross-protection
provided by acid adaptation.
In conclusion, results of the present study indicated
that acid-adapted cells of Salmonella did not exhibit
any increased resistance to the drying process com-
pared to that of nonadapted cells. Our results also
revealed that using food grade chemicals as pre-
drying treatments (MM, AATM, and TWTM)
improved the effectiveness of the meat-drying process
for inactivating Salmonella compared to the processused in traditional jerky making. The effects of these
-
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Casadei, M.A., Ingram, R., Hitchings, E., Archer, J., Gaze, J.E.,
M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 5165642001. Heat resistance of Bacillus cereus, Salmonella typhimui-
rum, and Lactobacillus delbrueckii in relation to pH and etha-
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Centers for Disease Control and Prevention (CDC), 1995. Outbreak
of salmonellosis associated with beef jerkyNew Mexico.
Morb. Mort. Wkly. Rep. 44, 785788.
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Salmonellae to organic acid rinses on beef. J. Food Prot. 58,
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Eidson, M., Sewell, C.M., Graves, G., Olson, R., 2000. Beef jerky
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are being evaluated in another study. Based on the
findings of the present study, use of MM, AATM or
TWTM in the jerky-making process and storing it for
15 to 30 days at ambient temperature, or use of TM
and at least 60 days of storage prior to consumption
may provide at least a 5.0 log reduction in Salmonella
count.
Acknowledgements
This project was funded by USDA-CSREES
National Integrated Food Safety Initiative and by the
Colorado Agricultural Experiment Station. We thank
Excalibur Seasoning, and Heller Seasoning and
Ingredients, for providing irradiated spices.
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M. Calicioglu et al. / International Journal of Food Microbiology 89 (2003) 5165 65
Effect of acid adaptation on inactivation of Salmonella during drying and storage of beef jerky treated with marinadesIntroductionMaterials and methodsBacterial strains used and preparation of inoculumPreparation of meat slicesInoculation procedurePre-drying treatment descriptionPre-drying treatment preparation and applicationDryingAnalysisStatistical analysis
ResultsTemperatureEffect of agar mediaEffect of pre-drying treatmentsEffect of dryingEffect of storagepH and aw
DiscussionAcknowledgementsReferences