Documente Academic
Documente Profesional
Documente Cultură
Food Control
journal homepage: www.elsevier.com/locate/foodcont
Review
The University of Queensland, School of Land, Crop and Food Science, Qld 4072, Australia
Fisheries Research Institute, 11960, Batu Maung, Penang, Malaysia
c
Department of Primary Industries and Fisheries, Hamilton, 4007 Queensland, Australia
d
Food Science Australia, Brisbane, 4173 Queensland, Australia
b
a r t i c l e
i n f o
Article history:
Received 2 February 2009
Received in revised form 17 June 2009
Accepted 19 June 2009
Keywords:
Salmonella
Listeria
Shrimp
Prawns
a b s t r a c t
Shrimp are an important commodity in the international sheries trade and there is an indication of an
increase in worldwide consumption of this crustacean. Salmonella and Listeria have been isolated from
shrimps and shrimp products on a regular basis since the 1980s. The continued reporting of the presence
of these pathogens in fresh and frozen shrimps, and even in the lightly preserved and ready-to-eat products, indicates that the existing practices used by the manufacturers or processors are insufcient to
eliminate these pathogens. This paper reviews the information available on Salmonella and Listeria in
shrimp and makes recommendations on control options and avenues for future research in order to
improve shrimp safety and quality.
2009 Elsevier Ltd. All rights reserved.
Contents
1.
2.
3.
4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1.1.
Shrimp production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1.2.
Shrimp trade . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1.3.
Shrimp consumption. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1.4.
Problems faced by the shrimp industry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1.4.1.
Shrimp safety from a regulatory perspective . . . . . . . . . . . . . . . . . .
1.4.2.
Shrimp safety from a public health perspective . . . . . . . . . . . . . . . .
Prevalence of pathogens in the shrimp production chain . . . . . . . . . . . . . . . . . . . . .
2.1.
Salmonella . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.1.
Characteristics and importance of Salmonella . . . . . . . . . . . . . . . . . .
2.1.2.
Prevalence of Salmonella in the shrimp production chain . . . . . . . .
2.1.3.
Growth and survival of Salmonella in shrimp and shrimp products
2.2.
Listeria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.1.
Characteristics and importance of Listeria . . . . . . . . . . . . . . . . . . . . .
2.2.2.
Prevalence of Listeria in the shrimp production chain . . . . . . . . . . .
2.2.3.
Growth and survival of Listeria in shrimp and shrimp products . . .
Attachment and persistence of Salmonella and Listeria on shrimp . . . . . . . . . . . . . .
Control of Salmonella and Listeria in shrimp. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.
Physical approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.1.
Cooking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.2.
Refrigeration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.3.
Irradiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.4.
Modified atmosphere packaging (MAP) . . . . . . . . . . . . . . . . . . . . . . .
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* Corresponding author. Address: Food Science Australia, P.O. Box 3312, Tingalpa DC, 4173 Queensland, Australia. Tel.: +61 7 32142037; fax: +61 7 3214 2150.
E-mail address: gary.dykes@csiro.au (G.A. Dykes).
0956-7135/$ - see front matter 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodcont.2009.06.020
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344
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348
351
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5.
6.
4.1.5.
High-pressure processing (HPP) . . . . . . . . . . .
4.1.6.
High-pressure carbon dioxide (CO2). . . . . . . .
4.2.
Chemical approaches. . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.1.
The use of chlorine . . . . . . . . . . . . . . . . . . . . .
4.2.2.
The use of ozone . . . . . . . . . . . . . . . . . . . . . . .
4.2.3.
The use of phosphates. . . . . . . . . . . . . . . . . . .
4.2.4.
The use of quaternary ammonia compounds
4.2.5.
Others. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Research needs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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357
1. Introduction
According to the United Nations Food and Agricultural Organisation (FAO) glossary for aquaculture, a shrimp is a decapod crustacean of the suborder Natantia, in the largest phylum in the
animal kingdom, the Arthropoda, and is characterized by jointed
appendages and a periodically molted exoskeleton (FAO, 2008).
The terms shrimp and prawn are used interchangeably for different species in different parts of the world; however the FAO convention is to call the marine and brackish-water forms of these
decapods shrimps and the freshwater forms prawns. For the
purpose of this review, the term shrimp is used to refer to all species of shrimp and prawns.
Table 1
World shrimp production from 2000 to 2006 (FAO, 2009).
Source
Value
2000
2001
2002
2003
2004
2005
2006
Capture
1000 tonnes
US$ million
3087
11,175
2955
10,411
2966
9788
3543
11,621
3527
11,357
3420
11,458
3460
11,764
Aquaculture
1000 tonnes
US$ million
1162
7310
1347
7492
1496
7879
2129
8355
2446
9536
2716
10,501
3164
12,486
Total
1000 tonnes
US$ million
4249
18,485
4302
17,893
4462
17,667
5672
19,976
5973
20,893
6136
21,959
6624
24,250
Table 2
International exports of shrimp by FAO ISSCAAP (International Standard Statistical Classication of Aquatic Animals and Plant) (FAO, 2009).
Value
Tonnes
US$ 1000
1986
1996
2006
1986
1996
2006
938,102
4,740,789
1,601,147
9,957,324
3,244,871
14,138,751
3.18
20.71
3.68
18.87
6.03
16.47
345
Other
19%
Eel
2%
Catfish
2%
Squid
3%
Shrimp &
Prawns
58%
Oysters
3%
Tilapia
4%
Milkfish
4%
Lobster
5%
Fig. 1. Share of FDA violations for Salmonella by seafood product in 2001 (from
Allshouse et al., 2004).
346
Table 3
Seafood import refusals by US FDA from July 2001 to June 2003 (Ababouch et al., 2005).
Year
Month
2001
July
August
September
October
November
December
122*
146
59
136
121
83
74
79
27
59
51
57
20
40
14
50
39
18
5
3
7
2
4
2
2
3
0
3
0
2
4
4
2
4
1
5
21
25
11
26
26
7
2002
January
February
March
April
May
June
July
August
September
October
November
December
177
184
213
126
174
143
136
121
115
260
125
153
84
84
90
60
72
80
87
66
58
72
71
58
71
35
38
20
41
41
53
27
39
108
15
30
2
12
8
0
1
3
1
1
5
1
5
2
6
4
4
0
1
2
12
3
3
3
2
0
1
0
4
5
5
2
3
6
2
17
8
16
42
64
73
43
64
34
126
74
50
103
57
82
2003
January
February
March
April
May
June
298
194
210
320
281
202
77
55
61
54
88
79
42
27
37
119
76
57
11
4
11
4
7
3
7
0
1
0
2
4
14
20
18
11
19
10
197
143
145
200
181
115
Filthy
Salmonella
Listeria
Histamine
Poison
Other
Note that for some products several reasons, e.g., both lthy and Salmonella are given as reasons for rejection but computed as one border case only. This explains why
number of border cases is not the total of causes presented horizontally.
Table 4
Shrimp products recalled from the market due to contamination with pathogenic bacteria.
Year
Product
Type
1987
1988
1988
1993
1993
May 1993
July 1993
January 1995
July 2000
Shrimp
Shrimp
Cooked and peeled IQF shrimp
Shrimp salad
IQF shrimp
IQF shrimp
Cooked shrimp
Breaded shrimp
Cooked-peeled shrimp (IQF)
Class
Class
Class
Class
Class
Class
Class
Class
Class
1
1
1
1
1
11
11
1
Quantity
Reason
>14,099.4 kg
41 cartons (6 5 pounds plastic bag/carton)
n.s.
n.s.
n.s.
280 kg (50,272 cases)
1319 cases
6153 cases
1665 kg
Table 5
Microbiological criteria/guidelines for Salmonella and L. monocytogenes in shrimp and shrimp products.
Countries/food authority/
food retail establishments
Australia
Salmonella: nil in 25 g (n = 5, c = 0, m = 0)
Salmonella: nil in 25 g (n = 5, c = 0, m = 0)
New Zealand
Salmonella: nil in 25 g
Salmonella: nil in 25 g
L. monocytogenes: nil in 25 g
Salmonella spp.: absent in 25 g (n = 5, c = 0)
L. monocytogenes: absent in 25 g
Salmonella: absent in 25 g
L. monocytogenes: absent in 25 g
Salmonella: adulterant
L. monocytogenes: zero tolerance policy
Salmonella (n = 10, c = 0, m = 0, M = )
L. monocytogenes: not detected in 25 g
Salmonella spp.: not detected in 25 g
EU
Austria, Italy
Hong Kong
US
ICMSF
Woolworths
Salmonella: adulterant
L. monocytogenes: zero tolerance policy
Salmonella (n = 5, c = 0, m = 0, M = )
L. monocytogenes: not detected in 25 g
References
and Denmark) have a regulatory tolerance of less than 100 cfu/g for
some food, and a zero tolerance for other foods especially those
with extended shelf-lives that can support the growth of L. monocytogenes. As indicated in Table 5, the criteria are differ substantially from country to country and between food authorities. It is
defensible to have a zero tolerance policy for cooked products,
since they have extended shelf-lives that can support growth of
pathogens. However, a zero tolerance requirements for raw or
fresh shrimp may be too stringent since these products are going
to be washed and cooked before consumption. In fact, from the
limited outbreak data available, there is little evidence that low
number of L. monocytogenes in shrimp will cause listeriosis even
in susceptible individuals (FAO, 1999). Such requirements can
effectively limit, or even block, shrimp trade resulting in substantial economic losses to the exporting countries, manufacturers
and producers. With a science based risk assessment approach
more countries, such as Australian and New Zealand (FSANZ,
2002) and the EU (EC (European Commission), 2005), have started
to implement an action level of 100 cfu/g for L. monocytogenes in
cooked shrimp products. A risk based approach considers the potential for growth of L. monocytogenes in cooked shrimp based on
criteria such as pH, water activity and shelf-life of the product.
As the minimum infectious dose for L. monocytogenes is low (based
on low number of listeriosis cases), therefore the likehood of any
food contaminated with low number of L. monocytogenes is considered remote (FAO, 1999). There therefore seems little justication
for regulating against products in which the pathogen cannot grow
if the level is at or below 100 cfu/g. The regulatory criteria for Salmonella in cooked and raw shrimp have still been maintained by
most countries. This is due to a strong opinion, that Salmonella is
not part of the natural ora of the shrimp culture environment,
nor is it inherently present in shrimp grow-out ponds, and that
their presence clearly indicates fecal contamination.
There is a possibility that contamination of imported cooked
shrimp are partly due to the US policy on forcing importers to have
contaminated shrimp cooked before approving their entry into the
US. Studies have shown that there is an additional risk that cross
contamination between raw and cooked products will occur in
processing plants. For instances public health authorities in the
UK have found the same serotypes of Salmonella in cooked prawns
and those which have been isolated from ponds during their survey (Communicable Disease Report 1989, 1990 as cited in Reilly
& Twiddy, 1992). In addition, the attachment and colonization of
bacteria to surfaces increases their resistance to stress, especially
if the surfaces have naturally protective microhabitats like shrimp
347
Table 6
Main documented cases of outbreaks associated with crustacean (including shrimp).
Agent
No. of outbreaks
No. of cases
References
L. monocytogenes (4b)
Salmonella
Pleisomonas shigelloides
Staphylococcus aureus
Shigella exneri
Bacillus cereus
Clostridium perfringens
Escherichia coli
Salmonella
Shigella sonnei
Vibrio cholerae
Vibrio parahaemolyticus
Multiple bacteria
Unknown agents
2
3
1
1
1
1
1
1
10
1
1
9
3
119b
57
3
2
40
118
204
12
214
2
6
142
38
921
USA
USA
USA
USA
France
USA
348
Table 7
Growth limits for Salmonella (adapted from Jay, Diane, Dundas, Frankish, & Lightfoot, 2003).
Parameter (other conditions being optimal)
Minimum
Optimum
Maximum
Temperature (C)
pH
Salt tolerance (%)
Water activity (Aw)
3537
5.57.5
*
*
4547
9.5
45
>0.99
: Not reported.
349
Type of sample
Origin of sample
No. of
Positive
samples (%)
Common serotype
isolated
References
Pond water
Sediment
Freshly harvested shrimp
Pond water
Mud
Thailand
139
144
23
n.s.
n.s.
S.
S.
S.
S.
Mud/water
Freshly harvested shrimp
Pond water
Sediment
India
Major aquaculture
region
22.1
16.0
n.s.
One
sample
One
sample
023.0
3.0
11.0
n.s.
Indonesia
Philippines
Thailand
India
Malaysia
India
n.s.
0.5
0.1
n.d
n.s.
30
30
18
30
30
37.4
28.8
37.5
31.2
25.6
6
6
18
280
40
340
25
n.s.
54.5
16.7
12.5
67.0
5.0
23.0
5.0
n.s.
65
9.2
145
120
40
261
3
22
225
25
25
63
247
8.2
5.0
2.5
3.5
33.0
13.6
1.0
24.0
4.0
0
1.6
n.s.
S. weltevreden
n.s.
S. weltevreden
8.1
4.3
2.0
11.0
n.s.
S. weltevreden
S. senftenberg
n.s.
n.s.
S. blockley
S. weltevreden
S. agona
S. chincol
S. newport
S. kentucky
S. senftenberg
Hydrebad, India
211
3683
1766
35
Retailers
Dried shrimp
Raw shrimp
Bombay, India
Malaysia
25
16
4.0
25.0
19
10.5
Fresh shrimp
Fresh shrimp
n.s.
US
US
M. rosenbergii
Parapenaeopsis stylifera
P. indicus
P. monodon
Fresh shrimp
Fresh shrimp
Shrimp
n.s.
S. weltevreden
Wholesale market/
distributors/importers
Shrimp paste
weltevreden
farmsen
newport
weltevreden
Coimbatore, India
Mangalore, India
Hydrebad, India
Vietnam
30
32
85
90
20
35
110
20.0
6.3
21.2
11.1
5.0
11.0
24.5
Dhaka
Mangalore, India
27
11.0
59.0
S. typhimurium
S. weltevreden
S. paratyphi B
S. typhi
n.s.
n.s.
S. weltevreden
S. tennesse
S. dessau
n.s.
S. weltevreden
Hatha and
Lakshmanaperumalsamy
(1997)
350
Table 8 (continued)
Point of sampling
Manufacturers/processors/
exporters
Type of sample
Origin of sample
No. of
Positive
samples (%)
Common serotype
isolated
References
Japan
212
2.4
S. weltevreden
Germany
Cochin, India
Sri Lanka
16
58
180
18.8
18.934.4
14.4
11.1
n.s.
n.s.
S. newport
S. weltevreden
India
n.s.
n.s.
S. weltevreden
S. bareilly
S. typhimurium
n.s.
n.s.
S. typhimurium
S. typhimurium
India
150
130
100
180
25
150
50
120
n.s.
2178
2390
12.0
10.0
14.0
0.0
4.0
2.0
4.0
1.0
0.52.8
1 sample
1 sample
351
preserved shrimp products such as dried shrimp (4%) (Iyer & Shrivastava, 1989) and shrimp paste (10.5%) (Arumugaswamy et al.,
1995). Furthermore, its occurrence has also been reported in prepared RTE items such as cooked shrimp (0.12.0%) (Hatha et al.,
1998; Hatha et al., 2003; Heinitz et al., 2000) and frozen Nigiri
shrimp sushi (18.8%) (Atanassova, Reich, & Klein, 2008). The presence of Salmonella in the latter products is alarming as they are
usually directly consumed without further heating.
As shrimp is traded in various forms such as de-headed, shelled,
peeled and whole, it is important to understand which parts of the
shrimp anatomy harbour the most contamination. Rattagool et al.
(1990) indicated that Salmonella might be located both internally
and externally. This is in agreement with Hatha and Lakshmanaperumalsamys (1997) observation which indicated 33.8% of Salmonella occurred on the shrimp body surface, 35.1% in the gills and
31.2% in the alimentary canal. However, Venkateshwaran, Manavalan, and Natarajan (1985) and Llobrerra et al. (1990) claim that the
cephalic region tends to harbour more Salmonella than other body
parts.
As indicated in Table 8, the most frequently isolated Salmonella
serotypes from shrimp and shrimp products are S. weltevreden and
S. typhimurium. The prevalence of S. typhi in Hatha and Lakshmanaperumalsamys (1997) study led to speculation that some contamination of the shrimp might be from human sources since S.
typhi is only associated with human contamination. Meanwhile,
Heinitz et al. (2000) found S. weltevreden and S. senftenberg to
be the most frequently isolated serovars from Asian and central Pacic seafood products.
Table 9
Growth conditions for Listeria (adapted from Sutherland, Miles, & Laboyrie, 2003).
Parameter (other conditions being optimal)
Temperature (C)
pH
Salt tolerance (%)
Water activity (Aw)
*
Minimum
0.4
4.4
*
0.92
Optimum
Maximum
37
7.0
10
0.92
45
9.6
25% at 4 C
0.97
: Not reported.
352
Table 10
Prevalence of Listeria in the shrimp production chain.
Point of sampling
Shrimp pond
Wholesalers/distributors/
importers
Type of sample
Origin of sample
During farming
Sediment
Water
Fresh raw shrimp
Clam meat
Formulated feed
At harvest
Sediment
Water
Shrimp
India
Raw shrimp
Imported products
(US)
Manufacturer/processors
Processed seafood
Plant environment
Water
Utensils
Shrimp
Cooked-peeled shrimp
Raw material (fresh shrimp)
Shrimp shell
Plant environment
Cooked-peeled shrimp
(end product)
Brazil
US
Imported
to US
Imported
Imported
Imported
products
into US
into US
into Canada
Cochin, India
US
Costa Rica
No. of
samples
References
Listeria spp.
L. monocytogenes
30
30
18
30
30
0
0
0
10.0
0
0
0
0
0
0
6
6
18
50.0
0
16.6
0
0
0
n.s.
28.5
6.6
n.s.
16.7
25.0
8.8
9.0
6.7
205
74
274
4
6.8
20.0
n.s.
n.s.
5.0
1.5
5
4
4
40.0
50.0
25.0
n.d
7
8
45
49
30
India
Iran
Goa, India
12
2
20
68
13
11
19
74
59
16
70
38
102
17
35
16
27
30
28
191
59
380
11
27
30
12
10
n.s.
n.s.
n.s.
n.s.
23.0
9.0
10.5
n.s.
28.844.1
n.s.
8.6
n.s. 15.8
n.s. 10.8
23.5
54.3
n.s.
n.s.
n.s.
3.646.4
n.s.
n.s.
n.s.
9.1
11.1
73.3
8.3
30.0
6.7
n.d
n.d
Brazil
178
47.2
18.0
US
Brazil
152
56
21
33
178
3331
43
18
552
82
5.918.4
n.s.
n.s.
25.0
23.8
24.2
17.4
26.5h
20.9
16.7
12.0
n.d
n.s.
Taiwan
Iceland
India
US Gulf Coast
US
Norway
Japan
Japan
Trinidad
France
Malaysia
England
Mangalore, India
Denmark
Chile
Australia
India
Iceland
Iceland
8.1
23.2
16.7
13.4
n.d
33.0
50
20.0
34.0
23.0
9.0
0
11.0
n.s.
18.0
1.4
2.6
2.0
11.8
11.4
44.0
22.0
6.0
10.7
4.0
28.8
3.0
n.d
Farber (1991)
Wong et al. (1990)
Hartemink and Georgsson (1991)
Manoj et al. (1991)
Motes (1991)
Noah et al. (1991)
Rrvik and Yndestad (1991)
Masuda et al. (1992)b
Ryu et al. (1992)
Adesiyun (1993)
Ravomanana et al. (1993)b
Arumugaswamy et al. (1994)
McLauchlin and Nichols (1994)
Jeyasekaran et al. (1996)
Jrgenson and Huss (1998)
Cordano and Rocourt (2001)
Anon. (2002c)
Dhanashree et al. (2003)
353
354
uid forces e.g., rinsing. The second stage occurs as the bacteria are
locked onto the surface with the help of exo-polysaccharides or
specic structures such as pili or mbrae. Here, much stronger
physical or chemical forces are required to remove the bacteria
e.g., scraping, scrubbing, or chemical cleaners.
With the widespread prevalence of Salmonella and Listeria in
shrimp production chains, surprisingly little is known about their
attachment and persistence on shrimp and shrimp products. By
contrast, studies on Salmonella and Listeria attachment to animal
(chicken, beef, pork) food surfaces (Benedict, Schultz, & Jones,
1991; Chung, Dickson, & Crouse, 1989; Notermans & Kampelmacher, 1974; Dickson & Macneil, 1991) have been conducted since the
1970s. More recently studies on the attachment of these bacteria
to fruits (Pao & Davis, 2001), vegetables (Barak, Whitehand, &
Charkowski, 2002; Ells & Hansen, 2006; Garrood, Wilson, & Brocklehurst, 2004; Gorski, Palumbo, & Mandrell, 2003; Iturriaga,
Escartin, Beuchat, & Martinez-Peniche, 2003) and sh (Kim & Marshall, 2001; Kim & Marshall, 2002; Verhaegh, Marshall, & Oh, 1996)
have been reported. Although information on the attachment of
Salmonella and Listeria to shrimp is very limited, we speculate that
the process is similar to that associated with meat and plant products. It is not known whether Salmonella and Listeria are able to attach to and hence externally colonize shrimp carapace and tissue,
although some strains of L. monocytogenes have been demonstrated to possess chitinolytic activity (Leisner et al., 2008) and
previous work has suggested chitin particles enhances the attachment of L. monocytogenes (McCarthy, 1992). Our recent investigation on the relationship between the physicochemical
characteristics of non-chitinolytic Salmonella (S. typhimurium
and S. senftenberg) and Listeria (L. monocytogenes (Scott A and
V7) and attachment to shrimp carapace suggested that the chitinolytic activity of Salmonella and Listeria might not play a major role
in initial attachment to and colonization on the carapace. On the
other hand, the bacterial cell surface charges, hydrophobicity, electron donor/acceptor potential as well as the carapace roughness
are signicantly related to attachment capabilities of these bacteria
to carapaces. Nevertheless, the same properties could not be related to subsequent colonization on the carapace (Wan Norhana,
Goulter, Poole, Deeth, & Dykes, 2009). The attachment of bacteria
to surfaces increases their resistance to stress, especially if the surfaces have naturally protective microhabitats (Watnick & Kolter,
1999). This adaptation could have important consequences, such
as extended survival periods in the environment and increased tolerance to treatments that would otherwise be lethal during the
preparation of shrimp in the home, food service establishments
or processing plants. Currently, there is limited information on
the increase of tolerance observed in Salmonella or Listeria due to
attachment to shrimp carapace. There is however a study related
to this topic by McCarthy (1992) who investigated the effects of
sanitizers on L. monocytogenes cells attached to chitin and observed
more than 10-fold increase in resistance to chlorine, iodine, and
quaternary ammonium compound sanitizers compared to suspended cells. This author concluded that the recommended concentrations and time of exposure for disinfectants might not
effectively eliminate Listeria attached to porous surfaces such as
chitin.
4.1.2. Refrigeration
Refrigeration and freezing are well-known techniques for
extending the shelf-life of food products. These processes lower
the temperature to levels at which bacterial metabolic processes
are stopped and the rates of chemical and biochemical reactions
reduced. Listeria is known to have the capability to grow at refrigeration temperatures on shrimp and this has been established by
several authors (Table 10). A study examining the effect of refrigerating and freezing L. monocytogenes on shrimp established that
this pathogen could survive both processes with little increase
in numbers on iced shrimp and a slight decrease (less than 1.0
log) on frozen product (Harrison et al., 1991). Similarly, Mejlholm,
Boknaes, and Dalgaard (2005) demonstrated that L. monocytogenes
increased by 1000-fold at 5 and 8 C before shrimp, which was
stored under a modied atmosphere, was determined to be
spoiled by sensory evaluation. However, in the same product
stored at 2 C, spoilage was not detected. It can be concluded from
these studies that cooked shrimp contaminated prior to frozen
355
Materials/chemicals/dose/
temperature/time
Test microorganisms
References
Irradiation
0.14.0 kGy
0.54.0 kGy
2.55.0 kGy (cobalt-60
irradiation)/2 C
S. enteritidis, S. typhimurium
L. monocytogenes
L. monocytogenes (strain 19115)
High-pressure CO2
Steam pasteurization
L. monocytogenes
Ozone
L. monocytogenes
Packaging
L. monocytogenes
L. monocytogenes (4 strains)
L. monocytogenes (5 strains)
Pandalus borealis
RTE shrimp
Microwave
Chemicals
Mu et al. (1997)
Kim (2007)
S. typhimurium
Beverly (2004)
Paranjpye et al. (2008)
4.1.3. Irradiation
Irradiation of food has been legally allowed in many countries
and the WHO has sanctioned radiation of up to 7.0 kiloGray
(kGy) as safe (Jay, 1996). This process is one of the most effective
methods for decontaminating both the surface and deep muscle
of fresh meat and poultry. There is substantial literature on the effects of irradiation in reducing Salmonella and Listeria on shrimp. A
study by Nerkar and Bandekar (1989), for example, showed complete elimination of Salmonella on frozen shrimp when irradiated
at 4.0 kGy. Similarly Ito, Adulyatham, Sangthong, and Ishigaki
(1989) reported that doses of 4.05.0 kGy were required to reduce
the numbers of S. typhimurium on shrimp by 6.0 log cycles. In
addition, a slightly lower dose (3.0 kGy) was reported to reduce
L. monocytogenes inoculated at a level of 104/g in frozen shrimp
(Rashid, Ito, & Ishigaki, 1992). However, irradiation at 5.0 kGy
was found to be insufcient to totally eliminate L. monocytogenes
in frozen shrimp (Brandao-Areal, Charbonneau, & Thibault, 1995).
Although irradiation appears to be effective in eliminating
pathogens in shrimp, there is an unsubstantiated view amongst
the public that food irradiation is unsafe and undesirable. There
is also evidence some that irradiation may reduce the nutritional
value of some foods by the destruction of aromatic amino acids
356
monolaurin (MC12) (500 lg/g) was the most inhibitory monoglyceride, but was only bacteriostatic rather than bacteriocidal. When
combined with propyl gallate (200 lg/g) the activity of MC12 improved, reducing levels of L. monocytogenes 10100-fold in cooked
shrimp after 24 weeks storage at 4 C, as compared to untreated
control samples.
In another investigation, Beverly (2004) examined the antimicrobial effect of cranberry juice (27%) against L. monocytogenes
on raw peeled shrimp. At 37 C there were no signicant differences in L. monocytogenes population in the marinated shrimp after
30 or 60 min. At 4 C, however, there was a signicant difference
when the shrimp were marinated for 60 min. After 24 h marinating
the L. monocytogenes counts were reduced by 1 log cfu/ml.
There is a paucity of data regarding the efcacy of novel methods in achieving pathogen inactivation in shrimp products. From
the available literature, almost all control or intervention strategies
focus on the elimination of Salmonella and Listeria in shrimp and
shrimp products within the industrial processing environment.
There are advantages and disadvantages of each of the control options mentioned. Even though the current literature indicates that
Salmonella and L. monocytogenes can be reduced, but cannot always
be eradicated from nished product or the plant environment, the
industry should work towards elimination of these pathogens.
Combinations of natural antimicrobials and high-pressure treatment and high-pressure CO2 or vacuum packaging are probably
the most effective of the strategies available. With a 99% reduction
of L. monocytogenes by using high-pressure CO2 (Wei et al., 1991)
and substantial extension of shelf-life of shrimp using vacuum
packaging and high-pressure treatment (Lopez-Caballero, PerezMateos, Borderias, & Montero, 2000), these strategies could synergistically enhance the safety and quality of shrimp. In addition
there is no negative public perception of these types of treatment
as compared to irradiation and chemical applications. Other
emerging approaches that could be applied to shrimp are pulsed
light technology and UV light. In addition to being economical,
UV light offers several advantages because it leaves no residues,
does not affect moisture of the food product and studies have demonstrated that the reduction of surface microorganisms is possible
(Wong, Linton, & Gerrard, 1998). Pulse light technology was approved by the US FDA in 2003 for application in food products after
being evaluated for both safety and effectiveness. However the cost
of these technologies is high thus limiting their use. In addition,
there is a clear requirement for more information on control strategies that could be applied at home, in food service establishments
or at retail level. Furthermore, while there is a larger body of literature on L. monocytogenes; more studies investigating control of
Salmonella in shrimp are required.
5. Research needs
While research has assisted in understanding how and where
shrimp and shrimp products become contaminated with Salmonella and Listeria, a greater understanding of the mechanisms and
factors (physico-chemical and environmental) by which Salmonella
and Listeria attach to/colonize shrimp surfaces and how best to kill/
remove attached/colonized cells is required. This may assist in the
development of novel interventions to control these pathogens on
shrimp. By the same token, more research is required to determine
how resistant are the attached/colonized cells of Salmonella and
Listeria on shrimp surfaces to environmental stresses, such as increases and decreases of temperature, low pH conditions and the
biocidal activity of disinfectant solutions.
There is limited thermal inactivation data for Salmonella in seafood in general and shrimp and shrimp products in particular. As
Salmonella is the bacterial pathogen that causes the most outbreaks
357
358
359
Jay, J. M. (1996). Food preservation with chemicals. In Modern food microbiology (5th
ed., pp. 273275). New York, US: Chapman and Hall.
Jay, S., Diane, D., Dundas, M., Frankish, E., & Lightfoot, D. (2003). Salmonella. In A. D.
Hocking (Ed.), Foodborne microorganisms of public health signicance (6th ed.,
pp. 207266). Waterloo, NSW, Australia: Australian Institute of Food Science
and Technology Inc.
Jeyasekaran, G., & Ayyappan, S. (2002). Postharvest microbiology of farm-reared,
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