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FOOD
MICROBIOLOGY
Food Microbiology 24 (2007) 703710
www.elsevier.com/locate/fm

Combined effect of packaging atmosphere and storage temperature on


growth of Listeria monocytogenes on ready-to-eat shrimp
Thomas J. Rutherforda, Douglas L. Marshalla,, Linda S. Andrewsb,
Patti C. Cogginsa, M. Wes Schillinga, Patrick Gerardc
a
Department of Food Science, Nutrition, and Health Promotion, Mississippi Agricultural and Forestry Experiment Station,
Mississippi State University, Box 9805 Mississippi State, MS 39762-9805, USA
b
Experimental Seafood Processing Laboratory, Coastal Research and Extension Center,
Mississippi State University, 3411 Frederick St., Pascagoula, MS 39567, USA
c
Experimental Statistics Unit, Mississippi Agricultural and Forestry Experiment Station,
Mississippi State University, Box 9653, Mississippi State, MS 39762-9745, USA

Received 25 January 2007; received in revised form 27 March 2007; accepted 28 March 2007
Available online 5 April 2007

Abstract

Cooked, peeled, and deveined shrimp were inoculated with a 5 strain mixture of Listeria monocytogenes and packaged in air, vacuum,
and a 100% carbon dioxide modied atmosphere. The packaged shrimp were then stored at 3, 7, and 12 1C for 15 days to monitor the
growth of L. monocytogenes and psychrotrophic bacteria. Uninoculated shrimp were also subjected to sensory evaluation by a trained
panel to measure odor and appearance over the storage period. Results demonstrated that shrimp packaged in CO2 and stored at 3 1C
did not permit growth of L. monocytogenes during the 15-day storage period, while all other packaging/temperature combinations
allowed for multiplication of the bacterium. Carbon dioxide packaging also resulted in the slowest growth of psychrotrophic bacteria and
resulted in shrimp having acceptable sensory odor and appearance scores at the end of storage. When strict temperature control is
difcult, such as during processing, transportation, retail display, or home use, additional antimicrobial hurdles may be necessary to
ensure safety.
r 2007 Elsevier Ltd. All rights reserved.

Keywords: Shrimp safety; Listeria monocytogenes; MAP; Sensory quality

1. Introduction When developing new products that promote shrimp as


the primary ingredient, the product developer has two
The harvesting of shrimp holds great economic impor- main concerns, product safety and shelife. It is widely
tance for the U.S. Gulf of Mexico region, amounting to accepted that fresh shrimp are highly perishable (Bazemore
72% of the total U.S. catch (NOAA, 2003). However, et al., 2003), thus the predominant market form is as frozen
this domestic supply does not meet increasing consumer raw or cooked products. A refrigerated ready-to-eat (RTE)
demand for shrimp. As a result, much of the shrimp sold product would be more convenient for the consumer.
in the U.S. comes from foreign markets (NOAA, 2003). Unfortunately, even frozen RTE shrimp can harbor human
In addition to the sheer number of imports avai- pathogens (Duran and Marshall, 2005). In addition to
lable, imported shrimp can usually be obtained for enteric pathogens, Listeria monocytogenes is also of
lower prices than domestic shrimp. This puts added concern for RTE seafoods (Farber, 1991b; Dillon and
pressure on domestic processors to develop new value- Patel, 1992; Gecan et al., 1994; Shineman and Harrison,
added products. 1994; Valdimarsson et al., 1998; Notermans and Hoorn-
stra, 2000; Hathed et al., 2003; Suwansonthichai and
Corresponding author. Tel.: +1 662 325 8722; fax: +1 662 325 8728. Rengpipat, 2003), with an occurrence rate of up to 11% in
E-mail address: microman@ra.msstate.edu (D.L. Marshall). raw Gulf Coast shrimp (Motes, 1991; Gecan et al., 1994).

0740-0020/$ - see front matter r 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.fm.2007.03.011
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704 T.J. Rutherford et al. / Food Microbiology 24 (2007) 703710

Several properties make L. monocytogenes a concern in Brevudimonas, Carnobacterium, Chryseomonas, Corynebac-


refrigerated RTE shrimp (Buchanan, 1991; Gecan et al., terium, Flavobacterium, Micrococcus, Moraxella; Proteus,
1994; Lionberg et al., 2003). These properties include: (1) Pseudomonas, Serratia, Shewanella, Staphylococcus, and
L. monocytogenes is commonly found in shrimp and other Vibrio (Alvarez and Koburger, 1981; Lakshmanan et al.,
seafood products; (2) it is routinely found in processing 2002; Bazemore et al., 2003; Mejlholm et al., 2005).
environments as a post-processing contaminant; (3) it has Sensory evaluation is one of the most important items to
the ability to multiply at refrigerator temperatures; and (4) consider when developing a novel product or making
it possesses the ability to reach infectious doses without changes to an existing product. The product may fulll all
spoiling foods. These factors along with the bacteriums objectives, but if it is not accepted by the consumer, it is of
ability to grow in the presence of salt and reduced oxygen little value. Sensory analysis of shrimp products has been
atmospheres makes control of L. monocytogenes a formid- conducted by several researchers (Alvarez and Koburger,
able problem in RTE seafoods (Dorsa et al., 1993; 1979; Edmunds and Lillard, 1979; Matches and Layrisse,
Fernandez et al., 1997; Marshall, 2004; Mejlholm et al., 1985; Fatima et al., 1988; Venugopal, 1993; Benner et al.,
2005). 1994; Gundavarapu et al., 1998; Bak et al., 1999; Lin et al.,
Many methods of packaging and storage have been 1999). These analyses usually focus on attributes most
investigated to control the proliferation of pathogens and easily noticed by the consumer such as aroma, color,
spoilage bacteria in RTE foods. Modied atmosphere texture, and avor.
packaging (MAP) entails removal of air from a container A treatment system that will reduce the growth of
followed by reintroduction of an altered or modied spoilage bacteria and decrease or eliminate the growth of
atmosphere. This new atmosphere may contain carbon L. monocytogenes needs to be developed for RTE shrimp.
dioxide, nitrogen, and/or oxygen (Genigeorgis, 1985; An application of this nature should enhance safety as well
Daniels et al., 1985; Farber, 1991a). The actual percentage as extend shelife. This study included two objectives: (1)
of each gas in the mixture is dependent upon the to compare the combined inuence of packaging atmo-
application; however, CO2 is almost always present in the sphere (air, vacuum, and CO2) and storage temperature (3,
greatest quantity because it is effective at extending shelife 7, and 12 1C) to control the growth of L. monocytogenes
by increasing the lag phase and the generation time of most and psychrotrophic spoilage bacteria on RTE shrimp; and
aerobic spoilage microorganisms (Lannelongue et al., 1982; (2) to evaluate the sensory quality of RTE shrimp stored
Layrisse and Matches, 1984; Matches and Layrisse, 1985; under the conditions stated in objective 1.
Marshall et al., 1991; Bak et al., 1999). Reduced oxygen
atmospheres may control the growth of aerobic spoilage 2. Materials and methods
bacteria; however, the same environment may be benecial
for proliferation of psychrotrophic, facultatively anaerobic 2.1. Inoculation of shrimp
or strictly anaerobic pathogens, such as nonproteolytic
Clostridium botulinum and L. monocytogenes in seafoods Five strains (ATCC 15313, 51414, 43256, 19115, and
(Dorsa and Marshall, 1995; Pothuri et al., 1995; Gimenez 7644) of L. monocytogenes were used to make a cocktail for
et al., 2002; Mejlholm et al., 2005). It is well known, inoculation. Prior to each experiment, frozen stock cultures
however, that high CO2 MAP can reduce the growth rate of each strain were individually inoculated into 200 ml of
of L. monocytogenes relative to growth in air or under trypticase soy broth with 0.6% yeast extract (BD, Sparks,
vacuum (Marshall et al., 1991, 1992; Oh and Marshall, Maryland, USA). Once inoculated, cultures were incubated
1995; Pothuri et al., 1995). at 32 1C for 24 h to achieve an initial starting culture of
Another major area of focus in regard to a refrigerated approximately 108 cfu/ml. Two milliliters of each strain
RTE shrimp product is shelife. Two factors contribute to culture were added to a sterile test tube and vortexed for
quality degradation in stored shrimp. The rst defect, 10 s to ensure thorough mixing of strains, producing 10 ml
melanosis, is a black discoloring on the surface of shrimp of a ve strain cocktail. Two milliliters of cocktail were
that is caused by the activity of polyphenoloxidase, and then distributed into 2 l of 0.01 M phosphate buffered
occurs only in raw shell-on shrimp (Benner et al., 1994). saline (PBS, Sigma, St. Louis, Missouri, USA) in a 3 l
Another group of signicant enzymatic reactions result in steamer bucket (Progressive International, Kent, Washing-
the production of protein breakdown products such as ton, USA). This distribution produced an immersion
ammonia, indole, methanethiol, putrescine, trimethyl solution containing 106 cfu/ml of L. monocytogenes.
amine and other off-odor compounds that are caused by Several 454 g packages of individually quick frozen
the growth of spoilage bacteria (Chang et al., 1983; cooked, peeled, and deveined shrimp (100150 count) were
Lakshmanan et al., 2002; Bazemore et al., 2003). The key obtained from a local retail store and kept frozen until
enzymes responsible for these reactions are arginase, used. Prior to the beginning of each experiment, packages
adenosine deaminase, and AMP deaminase (Yeh et al., were placed in a 4 1C refrigerator to thaw overnight. Before
1978; Ward et al., 1979; Bazemore et al., 2003). The most immersion into control (2 l PBS) or inoculation buffers,
commonly found spoilage bacterial genera include Achro- four packages of shrimp were aseptically opened under a
mobacter, Acinetobacter, Aeromonas, Alcaligenes, Bacillus, laminar ow hood by thoroughly wiping with 70% ethanol
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T.J. Rutherford et al. / Food Microbiology 24 (2007) 703710 705

and cutting horizontally below the dorsal seal with sterile per package. On the day of sampling, approximately 68 g
scissors. Under the laminar ow hood, 908 g of shrimp of shrimp were placed into each of two separate
were placed into each of two 3 l steamer baskets autoclaved, cleaned, and deodorized 125 ml Teon snifng
(Progressive International). One basket was then dipped bottles (Fisher Co., Pittsburgh, Pennsylvania, USA) for
into the control bucket (2 l PBS) and the other basket was odor analysis. Random 3 digit codes were assigned to each
dipped into the inoculation bucket. The steamer baskets bottle. The two identical sets of sample bottles were each
were then immersed for 5 min with constant hand agitation allowed to sit at room temperature for one hour prior to
and then removed and placed on sterile paper towels to analysis. For appearance evaluation, the remaining con-
drain for 10 min in the laminar ow hood. tents of each package were placed into a clear 0.95 l plastic
bag (Ziploc, Racine, Wisconsin, USA) and sealed.
2.2. Packaging A random 3 digit code was assigned to each bag. The
number codes were different on both the snifng bottles
After draining, Cryovac (Duncan, South Carolina, USA) and the bags so panelists could not correlate the two.
B2650 bags (20.3 cm tall  16.5 cm wide; water vapor Sensory analysis of shrimp samples was conducted using
transmission of 0.50.6 g per 254 cm2 at 37.8 1C, 100% relative an 11 member panel of university employees and students.
humidity, 24 h; oxygen transmission of 36 cc per m2 at 4.4 1C, The panelists were trained 1 h per day for 1 week prior to
24 h) were aseptically lled with 20 g of shrimp and sealed data collection. During training, the panelists were given
using a Multivac model A300/16 (Kansas City, Missouri, the same number of samples that they would receive while
USA). Three packaging atmospheres were used: air, vacuum, actually participating on the panel. Shrimp samples were
and 100% CO2 (Nexair, Columbus, Mississippi, USA). Air prepared in the same manner as previously described
packaging was done at 999 mbar vacuum for 1 s with a 2.5 s above. After sample evaluation, a daily discussion was held
seal. Vacuum packaging was done at 15 mbar vacuum for 1 s about ratings, with the package identities of the shrimp
with a 2.5 s seal. Modied atmosphere packaging was done at being revealed. The panelists rated shrimp samples on a 15
15 mbar vacuum for 1 s followed by a 700 mbar 100% CO2 point hedonic scale (15 cm) for both odor and appearance.
ush and a 2.5 s seal. Packages with each atmosphere were During training, the panelists proposed that there should
randomly placed into 3, 7, and 12 1C incubators for storage. be three categories of scoring for both odor and
appearance. Scores less than 7 were termed unspoiled
2.3. Bacterial enumeration and acceptable. Scores falling between 7 and 8 were
termed borderline, and scores above 8 were termed spoiled
For each treatment, duplicate packaged shrimp samples and unacceptable.
were analyzed for microbial counts on days 0, 3, 6, 9, 12, and On each panel day (30 total), panelists received nine
15. Twenty milliliters of PBS were added to each 20 g shrimp different samples. The nine samples consisted of air,
sample in a stomacher bag. The bags were then homogenized vacuum, and modied atmosphere packages stored at 3,
for 30 s using a stomacher (Tekmar, STO-400, Cincinnati, 7 and 12 1C for the day being evaluated (0, 3, 6, 9, 12, or
Ohio, USA). Serial dilutions of the homogenate were made 15). For day 0, panelists were given nine differently labeled
in PBS and plated onto Modied Oxford Agar (MOX, BD) samples that had no treatment applied. The gathering of
and Plate Count Agar (PCA, BD) with the aid of a model D sensory data from ve replications was accomplished by
spiral plater (Spiral Biotech, Norwood, Massachusetts, assigning a number to each mark placed on the line scale by
USA). MOX plates were incubated at 28 1C for 48 h to panelists for each sample. A ruler was used to measure each
allow for growth of L. monocytogenes colonies, which appear mark. Thus, it was possible to calculate scores from 0 to 15.
grayish-black. PCA plates were incubated at 7 1C for 5 days Data were analyzed using the mixed procedure (SAS
to allow for growth of psychrotrophic bacteria. Microbial version 8.0) to calculate least-square means for odor
counts were determined using procedures outlined in the and appearance scores. This procedure allowed for the
model D spiral plater manual. determination of product shelife as rated by the panelists
Data consisting of log10 cfu/g of L. monocytogenes and for each package, temperature, and day. A comple-
psychrotrophic bacteria from three replications were tely randomized design with a 3-way factorial structure
analyzed using the mixed procedure of the SAS statistical was used.
package, version 8.0 (SAS Institute Inc., Cary, North
Carolina, USA). A completely randomized design with a 3- 3. Results and discussion
way factorial structure was used. This procedure allowed
for the comparison of all factors (temperature, atmosphere, 3.1. Growth of L. monocytogenes
and day) utilized in this study.
Fig. 1 illustrates the effects of different packaging
2.4. Sensory evaluation atmospheres on the growth of L. monocytogenes in RTE
shrimp stored at 3, 7, and 12 1C. Uninoculated control
Uninoculated shrimp were packaged and stored as samples showed no L. monocytogenes growth after 15 days
previously described except that 50 g of shrimp were used of storage at any temperature, which indicated that
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706 T.J. Rutherford et al. / Food Microbiology 24 (2007) 703710

Air Vac Map


10
9
8
7
6
5
4
12C
3
2

10
9
7C
8
7
Log10 cfu/g

6
5
4
3
2

10
9
8 3C

7
6
5

4
3
2
0 3 6 9 12 15
TIME (days)

Fig. 1. Effect of packaging atmosphere (air, vacuum, CO2 modied atmosphere) on the growth of Listeria monocytogenes on ready-to-eat shrimp stored at
3, 7, and 12 1C. Standard error 0.02.

L. monocytogenes was not likely present in the shrimp used. declines as storage temperature increases (Marshall et al.,
There was no signicant temperature plus atmosphere 1991; Hudson et al., 1994; Pothuri et al., 1995). The
interaction (p40.05). Thus, temperature and packaging importance of strict temperature control is further empha-
atmosphere acted independently on the growth of sized by the U.S. Food and Drug Administration, which
L. monocytogenes for all three storage temperatures and recommends that seafood products packaged under
all three packaging atmospheres. Regardless of tempera- vacuum or in CO2 atmospheres must be stored at
ture, CO2 packaging was most effective (pp0.05) at temperatures o3.3 1C to prevent growth of nonproteolytic
controlling the growth of L. monocytogenes, while vacuum C. botulinum (FDA, 2001). This requirement coupled with
packaging was second most effective, and air packaging present data on L. monocytogenes indicates that RTE
was least effective. Overall, the most effective packaging shrimp stored under modied atmospheres should be
and temperature combination to control the growth of stored at o3.3 1C to minimize pathogen growth. If one
L. monocytogenes was modied atmosphere combined with assumes that L. monocytogenes most likely would be a
storage at 3 1C. post-processing contaminant on RTE shrimp and be
It is widely accepted that CO2 packaging is an effective present in low numbers, using CO2 packaging and storage
control measure to slow the rate of L. monocytogenes at 3 1C may allow processors the opportunity to offer a
growth compared to air or vacuum packaging; however, it non-frozen alternative that is reasonably safe throughout
is also known that the effectiveness of this treatment its shelife. However, additional hurdles (Marshall, 2004;
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T.J. Rutherford et al. / Food Microbiology 24 (2007) 703710 707

Mejlholm et al., 2005) may be desirable if temperature temperature and CO2 atmosphere on controlling the
control is difcult during transportation, retail display, and growth of spoilage and pathogenic organisms has been
home use. well documented (Genigeorgis, 1985; Farber, 1991a;
Fernandez et al., 1997). The increased activity of CO2 at
3.2. Growth of psychrotrophs low temperature is presumably due to its greater aqueous
and lipid solubility as temperature decreases (Genigeorgis,
Fig. 2 demonstrates the effect of different packaging 1985; Daniels et al., 1985). When applied to biological
atmospheres on the growth of naturally present psychro- tissue, CO2 exists as a dissolved gas and as carbonic acid
trophic bacteria on RTE shrimp stored at 3, 7, and 12 1C. (2%) (Daniels et al., 1985; Farber, 1991a). These two states
There was a signicant (pp0.05) temperature plus gas and the resultant decrease in pH can alter bacterial cell
interaction. Thus, growth of psychrotrophs was dependent membrane function to affect nutrient uptake and absorp-
upon combinations of temperature and packaging atmo- tion, and can inhibit intracellular enzyme activity.
sphere. Packaging in CO2 was signicantly (pp0.05) more
effective against psychrotrophs when compared to vacuum 3.3. Sensory shelflife
and air packaging.
As with L. monocytogenes, the combination of CO2 Average sensory scores for overall odor are presented in
packaging with storage at 3 1C was the most effective Fig. 3. RTE shrimp stored at 12 1C in air became
combination for controlling the growth of psychrotrophic borderline by day 6 and were spoiled by day 9. When
bacteria in RTE shrimp. The effect of decreased storage using vacuum packaging at 12 1C, the shrimp remained

Air Vac Map

10
9
8
7
6 12C

5
4
3
2

10
9
8
Log10 cfu/g

7
6
7C
5
4
3
2

10
9
8
7
6
5 3C
4
3
2
0 3 6 9 12 15
TIME (days)

Fig. 2. Effect of packaging atmosphere (air, vacuum, CO2 modied atmosphere) on the growth of naturally present psychrotrophic bacteria on ready-to-
eat shrimp stored at 3, 7, and 12 1C. Standard error 0.05.
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708 T.J. Rutherford et al. / Food Microbiology 24 (2007) 703710

Air Vac Map


15
14
13
12 12C
11
10 Spoiled
9
8 Borderline
7
6 Unspoiled
5
4
3
2
1
0

15
14
13
12 7C
11
10 Spoiled
9
Score

8
Borderline
7
6
Unspoiled
5
4
3
2
1
0

15
14
13 3C
12
11
10 Spoiled
9
8 Borderline
7
6 Unspoiled
5
4
3
2
1
0
0 3 6 9 12 15
TIME (days)

Fig. 3. Average odor scores of ready-to-eat shrimp stored at 3, 7, and 12 1C under different atmospheres (air, vacuum, CO2 modied atmosphere).
Standard error 0.37.

unspoiled by day 6, but were spoiled by day 9. In contrast, which in turn results in greater protein degradation and
no packages stored under CO2 at 12 1C reached the formation of off-odors, especially malodorous amine
borderline stage during the entire 15 day study. Likewise, compounds (Lakshmanan et al., 2002; Bazemore et al.,
none of the shrimp stored at 3 or 7 1C in any atmosphere 2003). Over extended storage time, the breakdown of
were considered spoiled by day 15. structural protein in shrimp tissue may also cause loss of
Average sensory scores for overall appearance are physical integrity, resulting in a mushier product with
presented in Fig. 4. No product became visually unac- increased purge. This appearance defect usually does
ceptable throughout the 15 days of storage at any not precede off-odor formation, as was seen in the pre-
temperature or packaging atmosphere. Nevertheless, air sent study.
packs combined with a 12 1C storage temperature resulted
in borderline product on days 9 and 12. Product on the 4. Conclusions
verge of unacceptability was produced by vacuum packa-
ging and storage at 12 1C on day 12. The novelty of the present work was the focus
These sensory results were predictable. Increasing on refrigerated RTE shrimp. Overall, CO2 packaging
storage temperature results in faster bacterial growth, and storage at 3 1C was the most effective packaging
ARTICLE IN PRESS
T.J. Rutherford et al. / Food Microbiology 24 (2007) 703710 709

Air Vac Map


15
14
13 12C
12
11
10
9 Unacceptable
8
7 Borderline
6
5 Acceptable
4
3
2
1
0

15
14
13 7C
12
11
10 Unacceptable
9
Score

8 Borderline
7
6 Acceptable
5
4
3
2
1
0

15
14
13 3C
12
11
10 Unacceptable
9
8 Borderline
7
6 Acceptable
5
4
3
2
1
0
0 3 6 9 12 15
TIME (days)

Fig. 4. Average appearance scores of ready-to-eat shrimp stored at 3, 7, and 12 1C under different atmospheres (air, vacuum, CO2 modied atmosphere).
Standard error 0.44.

system for controlling growth of both L. monocytogenes Acknowledgments


and other psychrotrophic bacteria as well as offering
an extended shelife compared to air and vacuum Approved for publication as journal article no. J-11065
packaging. This packaging combination also would con- of the Mississippi Agricultural and Forestry Experiment
trol the growth of another psychrotrophic pathogen, Station. This work was supported in part by USDA-
nonproteolytic C. botulinum. Storage temperatures of CSREES special Grant no. 2003-34231-13064, by the
greater than 3.3 1C would not control either pathogen. Mississippi Agricultural and Forestry Experiment Station
For practical reasons, strict temperature control is under project MIS-081430, and by the National Fisheries
often difcult to achieve during the entire course of Institute.
processing, warehousing, shipping, retail display, and
home storage. The present study demonstrates that References
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