Prevalence, Persistence and Control of Salmonella and Lis

Food Control 21 (2010) 343361
Contents lists available at ScienceDirect
Food Control
journal homepage: www.elsevier.com/locate/foodcont
Review
Prevalence, persistence and control of Salmonella and Listeria in shrimp and

shrimp products: A review
M.N. Wan Norhana a,b, Susan E. Poole c, Hilton C. Deeth a, Gary A. Dykes d,*
a
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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5.
6.
M.N. Wan Norhana et al. / Food Control 21 (2010) 343361
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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1. Introduction
1.2. Shrimp trade
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.
There is a strong market demand for shrimp. World exports of

fresh and frozen shrimp (two major trade categories) have shown
a remarkable increase over the last 10 years (Table 2). In 1986,
world shrimp exports totalled about 1.4 million metric tonnes
but tripled to almost 4.5 million tonnes in 2006 fuelled by increased world production, primarily from farming activities and
favourable economic conditions. Shrimp remains as one of the
most popular seafood throughout the world and in 2006 contributed about 6.03% of the total seafood export compared to cod
(9.71%), molluscs (10.19%), tuna (6.96%) and salmon (4.60%).
Although smaller in export volume percentage, the value of shrimp
(US$ 16.47 billion) in the same year far exceeded that of cod (US$
10.43 billion), mollusc (US$ 9.66 billion), tuna (US$ 8.07 billion)
and salmon (US$ 12.18 billion), making it the highest commercial
value product in seafood trade (FAO, 2009).
1.1. Shrimp production

Recent statistical data on shrimp production from both wild
harvest and farm culture estimate levels at approximately 6624
million metric tonnes totalling a value of more than US$ 23 billion.
Wild harvest shrimp had traditionally been the major source for
the world shrimp market but as the levels from this source are seasonal and uctuate, production from it has remained more or less
constant over the years (Table 1). In 2000, for example, production
of wild harvest shrimp was estimated at around 3000 million metric tonnes, followed by a slight dip in 2001 and 2002 before
remaining almost constant at 3.5 million tonnes from 2003 to
2006 (FAO, 2009). Due to the inconsistency of the natural supply,
increased efforts have been directed towards the production of
shrimp through aquaculture. In the year 2000, cultured shrimp
only represented slightly more than a quarter (27.3%) of the total
shrimp production but it had increased to almost half (48.0%) by
the year 2006 (Table 1).
1.3. Shrimp consumption

The increase in consumption of shrimp has been specically reported in several countries. The United States (US) National Marine
Fisheries Services (NMFS) reports that shrimp consumption per capita has increased steadily over the years from an average of 1.0 kg
per year in 1989 to a record high of 1.8 kg in 2005 (NMFS, 2007).
For the rst time in 2001, shrimp surpassed canned tuna as the
most consumed seafood in the US and has continued to grow in
more recent years (Hanson, House, Sureshwaran, G., & S., 2006).
Similarly in the European Union (EU) the appetite for shrimp has
continued to expand, evidenced by growth in most key markets
during 2005. Figures for 2006 indicate new import levels especially
for Spain and France (OSullivan, 2006). Consumption of shrimp in
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
World export of shrimp
Share of total shery product exported (%)
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
Australia has always been popular. A survey of Sydneys seafood

retailers (shmongers, supermarkets and sh and chips outlets)
in 1999 indicated that cooked farmed prawns, baby octopus and
Nile perch were the outstanding new-stars among all the three retailer types (Anon., 2002a). Green (uncooked) prawns also entered
the list of best-selling seafood for Sydney shmongers and supermarkets, whereas they had not rated a mention in a 1991 survey.
A similar trend was also evident in other parts of Australia (Perth
and Melbourne).
Shrimp is enjoyed for the uniqueness of its avour and texture.
It can be served as appetizers or easy snacks. More importantly, in
terms of human health, the high cholesterol content of shrimp is
compensated by the very low total lipid content and the predominance of polyunsaturated fatty acids, especially the n-3 fatty acids.
Findings suggest that moderate shrimp consumption will not adversely affect the overall lipoprotein prole in humans and can
be included in a heart healthy nutritional guideline (Bragagnolo
& Rodriguez-Amaya, 2001). These results agree with that of e-Silva,
Seidman, Tian, Hudgins, and Sacks (1996), who drew the same conclusion after testing the effects of diets matched for macronutrient
composition, but with different amounts and sources of cholesterol
(i.e., shrimp and egg), in normolipidemic human subjects. Another
advantage of shrimp meat is that the mercury content is relatively
lower than other seafood. The US National Health and Nutrition
survey (19992002), which evaluated most commonly consumed
seafood species as sources of methyl mercury (MeHg) and omega-3 fatty acids, indicated that salmon followed by shrimp are
the principal sources of omega-3 fatty acids and are lesser sources
of MeHg compared to tuna which provides omega-3 fatty acids but
also considerably higher levels of MeHg (Mahaffey, Clickner, & Jeffries, 2008).
1.4. Problems faced by the shrimp industry
One of the major problems faced by the shrimp industry, besides insufcient production and disease outbreaks, is shrimp
product safety. A substantial proportion of shrimp product originates from developing countries and there is therefore a possibility
of spreading pathogens between countries with an associated risk
of foodborne illness. This concern has contributed to the enforcement of standards and regulatory procedures for shrimp products.
The US Food and Drug Administration (FDA), for example, may
place individual shrimp processing facilities or entire countries
with a history of Salmonella-positive products on a list for detention without physical examination. This means that every shipment of shrimp will be detained automatically and denied entry
into the US unless evidence is provided that the shipment is free
of Salmonella (FDA, 2004a). Due to these, as well as to ensure good
economic returns, shrimp quality and safety improvement are always at the forefront of concerns by processing companies and
exporting countries. Shrimp are important with respect from two
perspectives: regulatory and public health.
1.4.1. Shrimp safety from a regulatory perspective
Seafood is among the most common product that causes notication of import alerts in importing countries. The EU Committee
on Rapid Alert System for Food and Feed (RASFF) indicates that
seafood caused more notications from 2001 to 2005 than other
products such as meats, herbs and spices, fruits, vegetables, and
nuts. In the EU, shrimp constitutes about 3040% of total seafood
alert notications and 510% of alerts for all food imports (Anon.,
2002b, 2003, 2005). Meanwhile import detentions by the FDA for
seafood products accounted for almost 27% of the total detentions
in 2001, second only to the vegetable/vegetable products category.
Again shrimp (wild-harvest plus aquaculture combined) constituted by far the largest proportion of import items detained,
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).
accounting for more than half of all detentions (Fig. 1) (Allshouse,

Buzby, Harvey, & Zorn, 2004). Similarly, under the Imported Food
Program (IFP) implemented by the Australian Quarantine and
Inspection Service (AQIS), seafood (smoked sh, crustaceans and
molluscs) is the food item with the highest rejection rate (13.1%),
compared to peanuts (7.1%), paprika (4.5%) and marinara mix
(3.7%) (Bull, Crerar, & Beers, 2002). Ababouch, Gandini, and Ryder
(2005) in their report on causes of detention and rejection in international seafood trade based on the number of border cases in the
EU, US, and Japan indicated that the presence of pathogenic bacteria as one of the main causes of detention. The term border case
is used to cover any situation where a product is detained, rejected,
destroyed, returned to sender or otherwise removed from trade
ow. The main bacterial species that cause detention in the US
are Salmonella (35.6%) and followed by Listeria (4.1%) (Table 3). Salmonella was also the second main cause of shrimp rejection (under
microbial contamination) in EU countries from 1999 to 2002 (Huss,
Ababouch, & Gram, 2004). In addition to rejection and detentions,
recall of products due to contamination with Salmonella and Listeria monocytogenes has also been reported (Table 4). Although the
impact of Salmonella and Listeria (through shrimp products detention, rejection, and recalls) on shrimp trade has not been quantied, it is believed to be substantial. Direct and indirect nancial
losses can result from these events through re-inspection, analysing samples, reviewing records, expiry of shelf-life and the cost
of handling products.
Currently there is no international agreement on acceptable
levels of Salmonella or L. monocytogenes on food, including
shrimps. While details on the policy for the presence of Salmonella
and L. monocytogenes in food from all countries are not available,
examples from some individual countries and food authorities
are listed in Table 5. A regulatory requirement for the absence of
Salmonella (sometimes referred to as a zero tolerance policy) has
been established for raw or cooked/ready-to-eat (RTE) shrimps in
Australia, New Zealand, the EU, Hong Kong and the US. The International Commission of Microbiological Specication for Food
(ICMSF) also suggests that Salmonella should not be detected in
25 g raw or cooked shrimp products. Some countries such as the
US, Austria, Australia, New Zealand, and Italy have requirements
for the absence of L. monocytogenes in 25 g of foods (FAO, 1999).
On the other hand, other European countries (Germany, Netherland and France) have a regulatory tolerance of less than 100 cfu/
g of this pathogen at the point of consumption. Others still (Canada
346
Table 3
Seafood import refusals by US FDA from July 2001 to June 2003 (Ababouch et al., 2005).
Year
Month
No. of refusal cases
Reasons for refusals
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
Contaminated with L. monocytogenes

Contaminated with Salmonella
Bacterial and decomposition
n.s. Not specied.

Source: http://www.fda.gov.opacom/Enforce.html.
Table 5
Microbiological criteria/guidelines for Salmonella and L. monocytogenes in shrimp and shrimp products.
Countries/food authority/
food retail establishments
Microbiological criteria/guidelines/specication/maximum limits

Raw shrimp (fresh/frozen)
RTE shrimp/cooked shrimp
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
M = acceptability limit beyond which the results are considered unsatisfactory.

m = limit below which all results are considered satisfactory.
n = number of units comprising the sample.
c = number of sampling units giving bacterial counts between m and M.
References
Standard 1.6.1. Australia New Zealand

Food Standards Code, (1995)
New Zealand Food Safety Authority
EC (1993)
FAO (1999)
Hong Kong Food and Environmental
Hygiene Department (2001)
FDA (2004b)
FAO (1999)
ICMSF (1986)
Woolworths (2007)
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
carapace. This adaptation could lead to increase tolerance to heat

treatments.
1.4.2. Shrimp safety from a public health perspective
From a public health point of view, shrimp safety is becoming
more of a concern. The expanded international seafood trade has
facilitated the introduction of pathogens into new geographic areas
and human communities. Meanwhile the extensive use of antibiotics in intensive aquaculture has increased the development of multiple-resistant pathogenic bacteria. This concern has been
highlighted by an elevated prevalence of antimicrobial-resistant
Salmonella in shrimp (Wan Norhana, Johara, & Ramlah, 2001; Zhao
et al., 2003) and other claims that RTE shrimp is an international
vehicle of antibiotic resistant bacteria (Duran & Marshall, 2005).
Furthermore, global warming and climate change may also have
a potential negative impact on water- and food-borne diseases
caused by microbiological agents (Rose et al., 2001). With shrimp
always being produced in and processed using water; these
changes may affect shrimp safety. To make it worse, the expanding
population of highly susceptible people due to aging, malnutrition,
immuno-compromisation (HIV/AIDS, transplant and cancer patients) and illnesses such as diabetes will result in more people
needing protection from unsafe food.
Sporadic diseases outbreaks associated with crustacean (including shrimp) consumption have been reported (Table 6), however,
the exact global incidence of disease from this source is not known.
In the US, 1019% of the estimated 76 million foodborne illnesses
reported yearly involved seafood (Durborow, 1999). Mead et al.
(1999) disagreed with this and stated that some unknown portion
of the estimated 76 million is attributable to seafood. Furthermore,
the data reported by Durborow (1999) also did not capture unreported outbreaks or sporadic cases of foodborne illnesses. This
raises an important issue in that in some countries, although there
is some sort of reporting system, there is the likelihood of severe
under-reporting, whereas in other countries there is no obligation
to report foodborne diseases to public health authorities. All of
these scenarios illustrate why the global picture of outbreaks from
seafood in general and shrimp in particular is less than clear and
complete.
Besides signicant under-reporting, disease surveillance reports
from Europe and North America indicate that human infection
associated with consumption of shrimp occurs very rarely as compared to pork, beef and poultry. This nding was based on the
observation that Salmonella strains isolated from most of the
clinical cases appear to be different from those found in shrimp
Table 6
Main documented cases of outbreaks associated with crustacean (including shrimp).
Agent
No. of outbreaks
No. of cases
Countries reporting outbreaks
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
Riedo et al. (1994)

Wallace, Guzewich, Cambridge, Altekruse, and Morse (1999)
Potasman, Paz, and Odeh (2002)

NACMCF (2008)a
Crustacean (shrimp, lobster crab) associated outbreaks reported to CDC (19982004).

Of the 119 crustacean-associated outbreaks of unknown etiology, ve were suspected S. aureus, two were suspected B. cereus, 10 were suspected V. parahaemolyticus,
three were suspected Salmonella, and one was suspected Shigella.
b
348
resulting in the conclusion that shrimp constitutes a very low risk

to public health (Feldhusen, 2000). However this might not be true
for all countries. For example S. weltevreden which is a common
isolate from shrimp culture environments and shrimp products
(Phan et al., 2005; Reilly & Twiddy, 1992; Shabarinath, Kumar,
Khushiramani, Karunasagar, & Karunasagar, 2007; Wan Norhana
et al., 2001), is also the most common serotype involved in human
infection in Thailand (Bangtrakulnonth et al., 2004), Vietnam (Phan
et al., 2005) and Malaysia (Yassin, Tiew, & Jegathesan, 1995). Statistics from the World Health Organization (WHO) also conrm
that S. weltevreden is gaining importance as the most signicant
cause of non-typhoidal disease in South East Asia and the Western
Pacic, in sharp contrast to Western Europe and US, where it is
infrequently found (Aarestrup et al., 2003). The S. weltevreden
serovar was also the most common Salmonella serovar found in
seafood imported from Thailand and Malaysia (Heinitz, Ruble,
Wagner, & Tatini, 2000). These observations could point to food
or waterborne reservoirs of S. weltevreden in countries with high
levels of this serovar which are not linked to seafood. This is probably why although S. weltevreden has historically been a leading
isolate in shrimp coming to US there are not many cases of disease
associated with this serovar. In addition, countries in North America and the EU that report a large number of salmonellosis cases to
data-bank typically do not report rare serovars thus resulting in
under-reporting of these serovars in these countries (Galanis
et al., 2006).
Although the number of outbreaks due to shrimp consumption
are low, they still present a potential risk to the public and especially to those who eat raw (sashimi), lightly and partially cooked
(seared on the outside and rare on the inside) shrimp. With widespread prevalence of Salmonella and Listeria in shrimp, this product
should be cooked sufciently and handled properly so that ingestion of viable pathogens that survive cooking processes and cross
contamination in the kitchen are avoided.
In addition to fresh and raw shrimp, cooked shrimp products
are also gaining an important place in the market resulting from
consumer demand for RTE food. Certain features in cooked shrimp
production, such as cooking on board shing vessels, chilling with
sea water, intensive handling and long transportation, make them
susceptible to microbial contamination. Furthermore, these products are capable of supporting growth of microorganisms, including pathogenic bacteria. Worse still, they are often consumed
directly without further heating or cooking thus making them a
potentially high-risk food. Similarly organic shrimps, which are
produced with no disinfectants or antimicrobial agents, could represent a serious health or economic threat if not handled and manufactured under stringent conditions.
2. Prevalence of pathogens in the shrimp production chain

Although many signicant pathogens are associated with the
shrimp production chain (Reilly & Kaferstein, 1997) only a few,
for example Salmonella, Listeria, and Vibrio, have been thoroughly
studied with respect to their prevalence and impact on regulation
and public health. This review discusses only Salmonella and Liste-
ria in the shrimp production chain with respect to their persistence

on shrimp and shrimp products, as well as strategies to control
them.
2.1. Salmonella
2.1.1. Characteristics and importance of Salmonella
Salmonellae are Gram-negative, non-sporeforming rods (usually
0.71.5 25 lm in dimensions) and belong to the family Enterobacteriaceae. They are facultative anaerobes, mostly motile and
can be present in various environmental conditions outside living
hosts including in a desiccated state. They are facultative anaerobes, mostly motile and can be present in various environmental
conditions outside living hosts including in a desiccated state. They
are, however, unable to grow under desiccated conditions. Table 7
indicates the various factors, with upper, lower and optimal limits,
that support the growth of this genus. Salmonella is frequently
found in the intestinal tract of numerous animals including birds
and man. There are more than 2500 serovars and are considered
potential pathogens in animal and human.
Salmonellosis constitutes a major public health burden and represents a signicant cost to society in many countries. Very few
countries report data on the economic cost of the disease. In the
USA, an estimated 1.4 million non-typhoidal Salmonella infections
are reported annually resulting in 168,000 visits to physicians,
15,000 hospitalizations and 580 deaths (WHO, 2005). In 2007,
the total cost associated with Salmonella was estimated at US$ 3
billion (Economic Research Services (ERS), 2009). Salmonella was
the most frequent cause of outbreaks of seafood illnesses in the
US from 1998 to 2004 (National Advisory Committee on Microbiological Criteria for Food (NACMCF), 2008).
2.1.2. Prevalence of Salmonella in the shrimp production chain
Several researchers have studied Salmonella prevalence in
shrimp culture environments especially in the tropics (Table 8).
Salmonellae have been isolated from shrimp pond water including
source water and holding ponds (Bhaskar et al., 1995, 1998; Iyer &
Varma, 1990; Koonse, Burkhardt, Chirtel & Hoskin, 2005; Leangphibul, Nilakul, Sornachi, Tantimavanich, & Kasemsuksakul,
1986; Wan Norhana et al., 2001), shrimp pond sediment/mud
(Bhaskar et al., 1995; Bhaskar et al., 1998; Iyer & Varma 1990;
Koonse et al. 2005; Leangphibul et al., 1986; Llobrerra, Bulalacao,
& Tan, 1990; Putro, Anggawati, Fawzya, & Ariyani, 1990; Reilly &
Twiddy, 1992; Sugumar, Abraham, & Shanmugam, 2001; Wan
Norhana et al., 2001), feed (Bhaskar et al., 1995; Bhaskar et al.,
1998; Wan Norhana et al., 2001), manures used for the fertilization
of shrimp ponds (Llobrerra et al., 1990; Reilly, Twiddy, & Fuchs,
1992) and in probiotics used to promote shrimp health (Koonse
et al., 2005). These reported incidences indicate that Salmonella
can be found in shrimp farms irrespective of the culture methods
as they have been isolated from extensive (Reilly & Twiddy,
1992), semi-intensive (Bhaskar et al., 1998; Reilly & Twiddy,
1992) and intensive shrimp farms (Reilly & Twiddy, 1992).
Due to the wide prevalence of Salmonellae in the shrimp culture
environment, it is not surprising they are also detected in farmed
shrimp species such as white shrimp (Penaeus merguensis) from
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)
5.2 (most serotypes will not grow at <7.0)

3.8
*
0.94
3537
5.57.5
*
*
4547
9.5
45
>0.99
: Not reported.
349

Table 8
Prevalence of Salmonella in the shrimp production chain.
Point of sampling
Type of sample
Origin of sample
No. of
Positive
samples (%)
Common serotype
isolated
References
Shrimp culture environment
Pond water
Sediment
Freshly harvested shrimp
Pond water
Mud
Thailand
139
144
23
n.s.
n.s.
Leangphibul et al. (1986)
S.
S.
S.
S.
Iyer and Varma (1990)
Mud/water
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

Manure
Shrimp heads and gut
Farmed P. merguiensis
During Farming
Pond water
Sediment
Shrimp
Clam meat
Formulated feed
At harvest
Pond water
Sediment
Shrimp
Pond water
Sediment
Feed
Freshwater shrimp
(Machrobrachium rosenbergii)
Feces
Pond water
Source water
Holding pond water
Pond grow-out water
Waste water
Processing water
Pond sediment
Source sediment
Probiotic samples
Feeds
Shrimps
Philippines
Thailand
India
Malaysia
India
103 farms from six

countries
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.
Llobrerra et al. (1990)
S. weltevreden
Rattagool et al. (1990)

Bhaskar et al. (1998)
n.s.
Jeyasekaran and Ayyappan

(2002)
S. weltevreden
Koonse et al. (2005)
8.1
4.3
2.0
11.0
n.s.
S. weltevreden
S. senftenberg
n.s.
Gecan et al. (1994)

Heinitz et al. (2000)
n.s.
S. blockley
S. weltevreden
S. agona
S. chincol
S. newport
S. kentucky
S. senftenberg
Iyer and Shrivastava (1989)

Arumugaswamy et al. (1995)
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
Putro et al. (1990)
n.s.
US
US
M. rosenbergii
Parapenaeopsis stylifera
P. indicus
P. monodon
Fresh shrimp
Fresh shrimp
Shrimp
n.s.
Wan Norhana et al. (2001)
Fresh and frozen shrimp

Imported raw shrimp
Imported RTE cooked seafooda
Fresh shrimp
Fresh raw shrimp
Reilly and Twiddy (1992)
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
Jonnalagadda and Bhat (2004)
Hatha and
Lakshmanaperumalsamy
(1997)
Kumar et al. (2003)

Jonnalagadda and Bhat (2004)
Phan et al. (2005)
Pinu et al. (2007)

Shabarinath et al. (2007)
(continued on next page)
350
Table 8 (continued)
Point of sampling
Manufacturers/processors/
exporters
Type of sample
Origin of sample
No. of
Positive
samples (%)
Common serotype
isolated
References
Fresh White shrimp, Tiger

shrimp
Frozen shrimp sushi
Fresh shrimp
Captured shrimp
Cultured
Japan
212
2.4
S. weltevreden
Asai et al. (2008)
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
Atanassova et al. (2008)

Kumar et al. (2008)
Ubeyratne et al. (2008)
Process water, ice, oor utensil,

table top, animal droppings
India
n.s.
n.s.
S. weltevreden
Iyer and Varma (1990)
S. bareilly
S. typhimurium
n.s.
Iyer and Shrivastava (1989)
n.s.
S. typhimurium
S. typhimurium
Reilly et al. (1992)

Hatha et al. (1998)
Hatha et al. (2003)
Peeled and deveined shrimp

Headless shell-on shrimp
Peeled undeveined shrimp
Cooked and peeled shrimp
Dried non-penaeid shrimp
Utensils
Floor
Water
Processed shrimp products
IQF and cooked shrimp
IQF and cooked shrimp
India
South East Asia

India
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
n.s. not specied; n.d not detected.

a
Includes cooked shrimp, breaded shrimp and shrimp balls.
Thailand (Rattagool, Wongchida, & Sanghtong, 1990), freshwater

prawn (Macrobrachium rosenbergii) from India (Jeyasekaran &
Ayyappan, 2002), brackish-water-cultured shrimp from India
(Bhaskar et al., 1995; Bhaskar et al., 1998), Indonesia (Murachman
& Darius, 1991; Putro et al., 1990), Malaysia (Wan Norhana et al.,
2001), the Philippines (Llobrerra et al., 1990) and other major
shrimp producing countries (Koonse et al., 2005; Reilly & Twiddy,
1992; Reilly et al., 1992). The percentage of occurrence of Salmonella in pond water is higher (0.567.0%) than in shrimp (1.6
37.5%), feed (fresh and formulated) (5.031.2%) and sediment/
mud (0.128.8%). It should be noted that there are also reports
indicating the absence of Salmonella in shrimp culture environments (Dalsgaard, Huss, H-Kittikun, & Larsen, 1995; DeLa Cruz,
Santos, Augdo, & Dagla, 1990; Fonseka, 1990). However, Dalsgaard
(1998) argued that these studies could not represent the true scenario as in some of these studies the numbers of samples taken and
ponds examined were low and no repeated testing was performed.
Based on their studies Bhaskar et al. (1995, 1998), Iyer and
Varma (1990), Reilly and Twiddy (1992) and Wan Norhana et al.
(2001) concluded that Salmonella was a part of the natural ora
of the shrimp culture environment. This conclusion is supported
by the WHO declaration which recognized Salmonella as geonotic
disease, as well as the fact that foodborne zoonoses that are not
easily eliminated from the food chain. However, Dalsgaard et al.
(1995) strongly maintained that Salmonella did not appear to constitute a normal part of the microora in tropical brackish-water
environment, a point of view supported by the low occurrence of
Salmonella in some studies (Leangphibul et al., 1986; Putro et al.,
1990). The latter suggestion was strongly backed up by the ndings from a comprehensive study of 103 shrimp aquaculture farms
in six countries (two from Southeast Asia, one in central Asia, one
in Central America and one in North America). A signicant relationship was found between the log number of fecal bacteria and
the probability that any given sample would contain Salmonella.
There also was a clear connection between Salmonella serotypes
in source water and grow-out pond water and in other samples.
The study concluded that Salmonella was not part of the natural
ora of the shrimp culture environment, but that its occurrence
was signicantly related to the concentration of fecal bacteria in
the source and grow-out pond water (Koonse et al., 2005).
The sources of Salmonella introduction into the shrimp culture

environment have been investigated. Some studies suggest that
animal manure and contaminated feeds added to grow-out ponds
are possible sources of Salmonella (Bhaskar et al., 1995; Bhaskar
et al., 1998; Llobrerra et al., 1990; Reilly & Twiddy, 1992), while
others claim that sediment (Iyer & Varma, 1990; Reilly et al.,
1992) and water (Bhaskar et al., 1995) are possible sources of
contamination.
In addition to shrimp culture environments, there are reports of
Salmonella in fresh and frozen shrimp collected from landing centres, retailers, wholesalers, importers, and processors (Table 8).
The occurrence of this pathogen at landing centres and retail
(wet markets and supermarkets) has been reported in Bangaladesh
(Pinu, Yeasmin, Bar, & Rahman, 2007), Japan (Asai et al., 2008), India (Hatha & Lakshamanaperumalsamy, 1997; Jonnalagadda &
Bhatt, 2004; Kumar, Sunil, Venugopal, Karunasagar, & Karunasagar,
2003; Kumar, Surendran, & Thampuran, 2008), Malaysia (Arumugaswamy, Rusul, Abdul Hamid, & Cheah, 1995), Sri Lanka (Ubeyratne et al., 2008), and Vietnam (Phan et al., 2005). There are
also reports on the occurrence of Salmonella at wholesale markets,
importers and distributors (Gecan, Bandler, & Staruszkiewicz,
1994; Heinitz et al., 2000; Jonnalagadda & Bhat, 2004). In addition,
its prevalence has also been demonstrated in shrimp processing
environments. Iyer and Shrivastava (1989) reported on the incidence of Salmonella on processed shrimps, utensils and oor and
in water used in a processing plant. The incidence was highest in
fresh shrimp products (1014%), followed by oor swab samples
(4%), utensils (2%) and processing water (1%). Salmonella however
was not detected in cooked shrimp products. Subsequently, with
the implementation of HACCP in shrimp processing plants in India,
much lower occurrences were observed (Hatha, Maqbool, & Kumar, 2003; Hatha, Paul, & Rao, 1998).
Generally, the prevalence of Salmonella in fresh shrimp and
shrimp products isolated from processing plants is comparable
(10.014.0%) to that from the wholesalers/importers (4.311.0%)
but much lower than that from retailers (2.459.0%). This may be
due to temperature abuse and cross contamination that could
easily occur at retail level as compared to the controlled environment of the shrimp processing plant. In addition to fresh and frozen shrimp, Salmonella has also been shown to be present in
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.
2.1.3. Growth and survival of Salmonella in shrimp and shrimp

products
Although specic studies on the growth rate or survival of Salmonella in shrimp and shrimp products are limited, a few authors
have indirectly showed that some Salmonella serotypes might have
the ability to survive refrigeration and freezing temperatures (Gecan et al., 1994; Hatha et al., 1998; Iyer & Shrivastava, 1989). Iyer
and Shrivastava (1989) investigated the viability of Salmonella in
cooked shrimp homogenates at frozen temperatures ( 20 C and
40 C). All ten serotypes studied were demonstrated to be resistant to freezing ( 40 C). However, some differences were observed among serotypes during subsequent storage at 20 C.
S. paratyphi B was the most resistant strain and managed to
survive storage for up to 9 months, while the S. saintpaul was
the least resistant (up to 5 months). In addition, the ability of
Salmonella to survive a relatively high salt condition has also been
demonstrated (Arumugaswamy et al., 1995).
2.2. Listeria
2.2.1. Characteristics and importance of Listeria
Listeria are Gram-positive, non-sporing short rods (0.40.5 lm)
that are ubiquitous in nature. They are motile by means of peritrichous agella that give a tumbling form of motility (Seeliger &
Jones, 1986). They are facultatively anaerobic bacteria with psychotropic and mesophilic features. The genus contains six species:
L. monocytogenes, Listeria innocua, Listeria seeligeri, Listeria welshimeri, Listeria ivanovii, and Listeria grayi. Table 9 shows limits and
optimal factors that support the growth of Listeria. L. monocytogenes is widely recognized as the principal human pathogen of the
Listeria genus. Annually listeriosis accounts for about 2500 cases
of illness at a cost of approximately US$ 200 million in the US
(CCCDC, 2002). Although rare as compared to salmonellosis, listeriosis manifests as a severe illness with an exceptionally high level
of mortality (2040%), particularly of those who are most vulnerable, for both epidemic and sporadic cases (Slutsker & Schuchat,
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.
1999). Listeriosis is mainly reported from industrialized countries

with few or no reports from Africa, Asia and South America. This
observation may reect different consumption patterns, dietary
habits, host susceptibility and lack of testing facilities (Rocourt, Jacquet, & Bille, 1997), or alternatively a lack of reporting in nonindustrialized countries.
2.2.2. Prevalence of Listeria in the shrimp production chain
Unlike Salmonella, Listeria spp. are indigenous to the marine
and estuarine environments (Reilly & Kaferstein, 1997) and their
association with shrimp is therefore to be expected. Table 10 lists
studies reporting the prevalence of Listeria in the shrimp production chain. Compared to Salmonella, there are limited studies on
the occurrence of Listeria in the shrimp culture environment.
Bhaskar et al. (1995) and (1998) investigated the prevalence of
Listeria spp. during the course of shrimp culture and found that
L. monocytogenes was absent from all samples. Of the samples
analyzed during farming, only feed (clam meat) showed the
presence of L. innocua and L. seeligeri in 10.0% of the samples
tested whereas at harvest 50.0% of sediments samples contained
L. seeligeri, L. innocua and Listeria murrayii. The L. seeligeri species
was also detected in 16.6% of shrimp samples at harvest. These
ndings coincided with the earlier work of Manoj, Rosaling,
Karunasagar, and Karunasagar (1991) and Fuchs and Surendran
(1989) who observed that Listeria spp. other than L. monocytogenes appear to be common in tropical areas. Similarly, Ben Embarek
(1994) reported a higher prevalence of L. monocytogenes in shrimp
from temperate (412%) than tropical countries (02%). Nevertheless, some studies conducted after 1994 demonstrated that the
prevalence of L. monocytogenes in tropical shrimp equal to that
in temperate shrimp, thus refuting the initial hypothesis.
Jeyasekaran, Karunasagar, and Karunasagar (1996) claimed that
the absence of L. monocytogenes in earlier reports could be due
to inadequate methodology used. These authors demonstrated
that both L. monocytogenes and other Listeria spp. could be found
simultaneously in shrimp and other seafood tested, and this nding indicates that these species might share the same ecological
niche. This is very signicant because the presence of L. innocua
and other non-pathogenic species of Listeria may serve as indicators of the presence of L. monocytogenes. A relatively high prevalence of L. monocytogenes was later reported in other tropical
areas such as Brazil (17.418.0%) (Destro, Leitao, & Farber,
1996), Costa Rica (33.050.0%) (Ellner, Utzinger, & Garcia, 1991
as reported in Destro, 2000), India (6.7%) (Moharem, Charith Raj,
& Janardhana, 2007) and Malaysia (44.0%) (Arumugaswamy, Ali,
& Abd Hamid, 1994). On the other hand, Dhanashree, Otta,
Karunasagar, Goebel, and Karunasagar (2003) and Parihar,
Barbuddhe, Danielsson-Tham, and Tham (2008) failed to detect
L. monocytogenes in fresh and dried shrimp in India. The ndings
of the latter study could be due to the limited number of samples
tested.
The occurrence of L. monocytogenes in shrimp and shrimp products has been well demonstrated (Table 10). The presence of this
genus in fresh and frozen raw shrimp at retailers, wholesalers
and importers is quite common and prevalence varies from very
low to almost 50.0% (Adesiyun, 1993; Berry, Park, & Lightner,
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)
Cooked and peeled shrimp

Frozen shrimp (for export)
Raw shrimp
Frozen raw shrimp
Frozen raw shrimp
Cooked shrimp
Peeled shrimp
Retailers
Manufacturer/processors
Fresh raw (Metapenaeus sp.)

Frozen peeled prawn
Fresh shrimp
Frozen shrimp
Cooked shrimp
Frozen semi-ready foodsc
Shrimp salad
Fresh raw
Freshly caught shrimp
Raw seafoodd
Peeled shrimp in brine
Frozen shrimp
Raw shrimp
Fresh seafoode
Fresh raw shrimp
Cooked shrimp
Fresh raw shrimp
RTE foodf
Cooked, peeled, frozen shrimp
Fresh raw shrimp
Cured seafoodg
Fresh shrimp
Cooked-peeled and shell-on
Fresh shrimp
Dried shrimp
Fresh shrimp (P. monodon)
Fresh shrimp and frozen
Fresh shrimp
Frozen shrimp (P. brasiliensis)
d
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
Positive for (%)
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
Weagant et al. (1988)
6.6
n.s.
16.7
25.0
8.8
9.0
6.7
Hofer and Ribeiro (1990)a

Farber (1991)
Berry et al. (1994)
205
74
274
4
6.8
20.0
n.s.
n.s.
5.0
1.5
Gecan et al. (1994)

Jinneman et al. (1999)
Farber (2000)
5
4
4
40.0
50.0
25.0
n.d
Fuchs and Surendran (1989)
Buchanan, Stahl, Bencivengo,

and Dell Corral (1989)b
Ellner et al. (1991)a
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
Moharem et al. (2007)

Jalali and Abedi (2008)
Parihar et al. (2008)
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
Destro, Piva, Leitao, and Landgraf

(1994)a
Noah et al. (1991)
Destro et al. (1996)
n.s.
Taiwan
Iceland
India
US Gulf Coast
US
Norway
Japan
Japan
Trinidad
France
Malaysia
England
Mangalore, India
Denmark
Chile
Australia
India
Iceland
Iceland
n.s. not specied n.d. not detected.

a
Cited from Destro (2000).
b
Cited from Ben Embarek (1994).
c
Various types of dumplings including shrimp.
d
Including shrimp, prawns and breaded shrimp.
e
Including fresh shrimp.
f
Including shrimp dishes.
g
Including brined shrimp and oil-marinated shrimp.
h
Species identication was done on 49 of the 270 (8.1%) positive samples.
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
Bhaskar et al. (1998)
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)
Valdimarsson et al. (1998)

Gudmundsdottir et al. (2006)
1994; Buchanan, Stahl, Bencivengo, & Dell Corral, 1989 as reported

in Ben Embarek, 1994; Cordano & Rocourt, 2001; Farber, 1991;
Hartemink & Georgsson, 1991; Hofer & Ribeiro, 1990 as reported
in Destro, 2000; Jalali & Abedi, 2008; Jinneman, Wekell, & Eklund,
1999; Masuda, Iwaya, Miura, Kokubo, & Maruyama, 1992; Motes,
1991; Noah, Perez, Ramos, McKee, & Gipson, 1991; Ravomanana,
Richard, & Rosec, 1993 as reported in Ben Embarek, 1994; Ryu,
Igimi, Inoue, & Kumagai, 1992; Weagant et al., 1988). Although L.
monocytogenes occurs in raw and frozen shrimp, these products
do not pose a threat to the majority of people as they undergo
some processing before being eaten. However, they still pose some
risk to susceptible populations when consumed raw or lightly
cooked. In addition, the possibility of cross contamination in the
processing plant, kitchen or food service establishment is also of
concern.
Of greater consequence is that L. monocytogenes has been isolated from RTE shrimp products such as cooked shrimp (Anon,
2002c; Farber, 1991, 2000; Ravomanana et al., 1993 as reported
in Ben Embarek, 1994; McLauchlin & Nichols, 1994; Weagant
et al., 1988) and shrimp salad Hartemink and Georgsson (1991).
The prevalence is considered high for cooked shrimp (1.5- 25.0%),
and shrimp salad (23.0%) that have undergone a commercial
cooking process. Furthermore, the occurrence of L. monocytogenes
has also been documented in frozen semi-ready foods such as
shrimp dumplings (Wong, Chao, & Lee, 1990) and lightly preserved
shrimp products such as brined shrimp and oil-marinated shrimp
(Jorgensen & Huss, 1998; Rorvik & Yndestad, 1991).
L. monocytogenes occurs in shrimp processing plant environments (25%), water used in processing (23.8%), utensils (24.2%)
and on shrimp products (17.426.5%) (Destro et al., 1996; Gudmundsdottir, Gudbjornsdottir, Einarsson, Kristinsson, & Kristjansson,
2006; Valdimarsson, Einarsson, Gudbjornsdottir, & Magnusson,
1998). The sources of L. monocytogenes introduction into the
shrimp processing environment have been investigated. Some
studies have demonstrated that persistent in-house strains of L.
monocytogenes may contaminate seafood during processing (Autio
et al., 1999; Fonnesbech Vogel, Huss, Ojeniyi, Ahrens, & Gram,
2001). Other studies have suggested that transient L. monocytogenes from raw seafood contaminate the nal products (Gudmundsdottir et al., 2006; Markkula, Autio, Lunden, & Korkeala, 2005).
Regardless of the source, some authors have hypothesized that
the presence of Listeria in cooked products is due to undercooking
of the product (Budu-Amoako, Toora, Walton, Ablett, & Smith,
1992; Fuchs & Reilly, 1992).
2.2.3. Growth and survival of Listeria in shrimp and shrimp products
The growth of Listeria in shrimp may be inuenced by factors
including the availability of essential nutrient, pH, temperature,
water activity, competitive microora and the presence of food
additives that enhance or inhibit growth (Lovett, Francis, & Bradshaw, 1990). L. monocytogenes can grow at salt concentrations of
1314% and survive in salt at concentrations of up to 30% (Farber,
Coates, & Daley, 1992; Fuchs & Reilly, 1992). Salt alone is therefore
unlikely to be a control measure for the growth of L. monocytogenes
in processed seafood. L. monocytogenes has also been observed to
survive for long periods in processing plants, household refrigerators and freezers (FDA, 1999). Packaging methods do not affect the
growth of L. monocytogenes (Harrison, Huang, Chao, & Shineman,
1991), although some of the latest packaging technologies, such
as antimicrobial lms/wraps or smart packaging, may be effective
in reducing the growth of Listeria and provide essential protection
during storage and transportation.
Quantication of the growth and survival of L. monocytogenes
in shrimp and shrimp products have been reported. Dorsa, Marshall, Moody, and Hackney (1993) reported that L. monocytogenes
has a shorter generation time in seafood products than in other
353
protein meats. This observation is in agreement with Shineman

and Harrison (1994) who observed that regardless of whether
the shrimp are cooked or left raw, L. monocytogenes has a significantly (p < 0.01) greater ability to grow on them compared to
beef or chicken stored aerobically at 4 C. Similarly, the growth
rate of L. monocytogenes in cooked crustaceans (including shrimp)
(0.38 logs/day at 5 C) is reported to be higher that most RTE food
such as smoked seafood (0.155) and soft cheeses (0.105), but similar to liquid milk (0.262) and deli meats (0.244) (FSANZ, 2002).
Ideal growth conditions, such as pH range (6.87.0), water activity (0.99) and salt content (12%), may be among the factors that
promote growth of L. monocytogenes in cooked shrimp (FSANZ,
2002). Lovett et al. (1990) specically examined Listeria growth
in refrigerated shrimps and found that after storage for 12 weeks
at 7 C the number of L. monocytogenes increased from 103 to
106 8 cfu/g. Similarly Farber (1991) noted a 23 log increase of
L. monocytogenes in cooked shrimp after storage for 1 week at
4 C. He also observed that L. monocytogenes appeared to grow
slowly at 4 C in naturally contaminated shrimp but better in articially inoculated cooked shrimp. This could mean that naturally
occurring Listeria are more susceptible to cold. More importantly
this nding suggests that if L. monocytogenes is present in cooked
shrimp, even in low numbers, signicant levels may be reached if
the products are stored at temperatures commonly encountered
in chilled display cabinets at retail outlets. Even higher numbers
could be rapidly reached in the case of temperature abuse of
product.
The growth and survival of L. monocytogenes in lightly preserved
products, such as brined shrimp, have also been explored. Brined
shrimp is a popular product consisting of cooked and peeled
shrimp in brine, which contains salt and combinations of benzoic,
citric and sorbic acids. L. monocytogenes have been demonstrated
to grow in cold and warm water brined shrimp at temperatures
of 825 C (Dalsgaard & Jorgensen, 2000). In cold-water shrimp
with 3.3% water-phase salt (WPS), growth was observed at 15
and 25 C, and in warm water shrimp (2.3% WPS) an increase in
L. monocytogenes numbers was observed at temperatures P5 C.
Alarmingly, numbers of L. monocytogenes in shrimp with 2.3%
WPS increased more than 100-fold before the end of shelf-life as
determined by sensory evaluation. In addition, Burnet, Mertz, Bennie, Ford, and Starobin (2005) investigated the growth of L. monocytogenes in shrimp salad and found that it did not support the
growth of L. monocytogenes, with the overall population declining
throughout the 14-days storage period at 5, 7 and 10 C. The low
pH (4.8 and 4.5) of the shrimp salad used in the study may contribute to the reduction in the L. monocytogenes populations. On the
other hand, Hwang and Tamplin (2005) observed L. monocytogenes
growth in salads (imitation-shrimp crabmeat mixture) regardless
of storage temperature (4, 8 and 12 C) and mayonnaize pH (3.7,
4.0, 4.4, 4.7, and 5.1). Information on the survival and growth of Listeria in other shrimp products is limited.
3. Attachment and persistence of Salmonella and Listeria on

shrimp
Bacterial attachment to food production surfaces is regarded as
one of the rst steps in the contamination of food. It is widely accepted to occur in two stages, reversible and irreversible (Marshall,
Stout, & Mitchell, 1971). The former involves the bacteria being in
close enough proximity to allow initial attachment to take place,
and this is governed by van der Waals forces, electrostatic forces
and hydrophobic interactions (Gilbert, Evans, Evans, Duguid, &
Brown, 1991; Vanloosdrecht, Lyklema, Norde, & Zehnder, 1989).
This process is instantaneous and during initial contact bacteria
still show Brownian motion and can be easily removed by shear
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. Control of Salmonella and Listeria in shrimp

Owing to the common occurrence of Salmonella and Listeria in
shrimp and shrimp products, a number of studies have been carried out to develop methods to control pre- and post-production
contamination of shrimp. These methods are listed in Table 11
and summarized in the following section. They are sub-divided
into physical or chemical approaches.
4.1. Physical approaches

4.1.1. Cooking
Application of heat is one of the simplest and most effective
methods of eliminating pathogens from food. Boiling shrimp at
100 C for 1, 3, or 5 min has been shown to eliminate 103105 Listeria cells/g from naturally contaminated shrimp (McCarthy,
Motes, & McPhearson, 1990). However, boiling is not able to completely eliminate Listeria in articially inoculated (105 cells/g)
shrimp even after boiling for up to 5 min. The authors assumed
that either the naturally contaminated shrimps were externally
contaminated or naturally occurring Listeria were less heat-resistant in their natural environment. In addition, no L. monocytogenes
survived a cook-freeze-thaw process implying that freezing and
heating had an additive effect on lethality for L. monocytogenes.
Cooking in a microwave oven is also effective in eliminating Listeria
on shrimp. Gundavarapu, Hung, Brackett, and Mallikarjunan
(1995) investigated the effect of different microwave power levels
(240, 400, 560 and 800 Watt) on the survival of L. monocytogenes in
inoculated (5 105 cfu/g) shrimp. Their results show that Listeria
can be completely inactivated with 2 min holding after microwaving for 168, 84, 62, and 48 s at 240, 400, 560, and 800 Watt,
respectively. Recently Paranjpye, Peterson, Poysky, and Eklund
(2008) used a steam pasteurization method to eliminate naturally
contaminated L. monocytogenes in cooked-peeled shrimp. They exposed shrimp that were naturally contaminated with L. monocytogenes at 16 cfu/25 g to continuous steam cooking for 45, 60, and
90 s. The shrimps were then conveyed to normal shrimp processing lines and random samples taken to detect L. monocytogenes.
None of the steam-treated samples contained viable Listeria cells.
However, the product suffered a minor loss in avour, was slightly
tougher and weighed up to 25% less. It should be noted that the
heat resistance of L. monocytogenes seems to vary considerably
with the intrinsic properties, such as the lipid content, of the seafood. For instance, higher D60 (4.234.48 min) values were observed for salmon llets which have a higher lipid content than
cod (1.951.98 min) Ben Embarek & Huss, 1993). Thus, applying
heat resistance results from one product to another product may
not be valid.
In spite of numerous reports on the inactivation of Salmonella in
poultry, beef, and pork using different cooking methods, there is
very limited thermal inactivation data on Salmonella for seafood
in general and shrimp in particular. Doyle and Mazzotta (2000)
in their comprehensive review on thermal resistance of Salmonella
in food listed only one study on seafood (oysters) and none on
shrimp.
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

Table 11
Studies on Salmonella and Listeria control in shrimp.
Technology
Materials/chemicals/dose/
temperature/time
Test microorganisms
Type of shrimp (species)
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)
Fresh and frozen shrimp (n.s.)

Frozen shrimp
Frozen peeled, de-headed and
blanched shrimp (P. monodon)
Nerkar and Bandekar (1989)

Rashid et al. (1992)
Brandao-Areal et al. (1995)
High-pressure CO2
13.7 MPa/35 C/2 h
L. monocytogenes (ATCC 15313)
Fresh shrimp (pink shrimp)
Wei et al. (1991)
Steam pasteurization
Steam cooker/45, 60, 90 s
L. monocytogenes
Paranjpye et al. (2008)
Ozone
5 ppm ozone gas atmosphere and

ozonated water/20, 60, 120 min
5.2 mg ozone L 1/5 C/30 min
L. monocytogenes
Cooked and peeled cold-water

shrimp (Pandalus jordani)
shrimp (P. jordani)
Shrimp meat
Packaging
saran wrap, O2 non barrier type

skin packaging lm, vacuum pack
with an O2 barrier lm, EVA pouch
and Cryovac
1. MAP
2. Previous frozen storage
Air, vacuum and 100% CO2
modied atmosphere/3 C, 7 C,
12 C
L. monocytogenes
Fresh shrimp (brown and white

shrimp, Penaeus sp.)
Harrison et al. (1991)
L. monocytogenes (4 strains)
L. monocytogenes (5 strains)
Pandalus borealis
RTE shrimp
Mejholm et al. (2005)

Rutherford et al. (2007)
Microwave
240, 400, 560, 800 Watt
Frozen shrimp (n.s.)
Gundavarapu et al. (1995)
Chemicals
TSP (10% and 20%)
Five strains of L. monocytogenes

(Scott A, LCDC, V7, Brie-1, shrimp
isolate)
Four strains of L. monocytogenes
(Scott A, LCDC, V7 and Brie)
L. monocytogenes
Fresh shrimp (Penaeus sp)
Mu et al. (1997)
Cooked shrimp (n.s.)
Wang and Johnson (1997)
Frozen shrimp (Farfantepenaeus

aztecus)
Loi-Braden et al. (2005)
Cooked, peeled RTE shrimp (n.s.)
Kim (2007)
Raw shell-on, raw peeled and

cooked shell-on (P. aztecus)
Raw peeled shrimp (n.s.)
shrimp (P. jordani)
Dupard et al. (2006)
MC12 in combination with propyl

gallate
Electrolysed oxidizing (EO) water
CPC (0%, 0.1%, 0.3%, 0.5%, 0.7%, and

1.0%) and lactic acid (1%)
CPC (0.05%, 0.1%, 0.2%, 0.4%, 0.6%,
0.8%, and 1.0%)
Cranberry juice (27%)
ClO2 (5 ppm/10, 20, and 30 min)
S. typhimurium
Three Salmonella serotypes

mixture (S. enteritidis, S.
typhimurium, S. mission)
S. typhimurium (ATCC 14028,
A9589, 23564)
L. monocytogenes V7 (1/2 a)
L. monocytogenes
L. monocytogenes

Chen et al. (1992)
Beverly (2004)
n.s. not specied.
storage will remain contaminated after thawing for sale and

consumption.
(Johnson & Moser, 1967) and producing rancidity and off-odours

(Kanatt, Chander, & Sharma, 2005).
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
4.1.4. Modied atmosphere packaging (MAP)

Modied atmosphere packaging facilitates the distribution of
seafood and extends the shelf-life of raw and lightly preserved
shrimp products (Dalsgaard & Jorgensen, 2000; Lopez-Caballero,
Goncalves, & Nunes, 2002a). Limited studies have been carried
out on the survival of Salmonella and Listeria on chilled or frozen
RTE MAP shrimp products. Harrison et al. (1991) noted that vacuum packaging of shrimp did not enhance the conditions for
growth of L. monocytogenes (Scott A). Mejlholm et al. (2005) evaluated the growth of L. monocytogenes in cooked and peeled MAP
shrimp. They observed that L. monocytogenes grew at all storage
temperatures studied (2, 5, and 8 C) and growth at 5 and 8 C resulted in a 1000-fold increase, before the product became spoiled
as determined by sensory evaluation. In conclusion, they suggested
that to prevent L. monocytogenes becoming a safety problem,
cooked and peeled MAP shrimp should be distributed at 2 C and
with shelf-life of 2021 days. Recently Rutherford et al. (2007)
investigated the survival of L. monocytogens in RTE shrimp packed
under different conditions and stored at 3, 7, and 12 C. Their ndings indicate that regardless of temperature, MAP packaging incorporating CO2 is the most effective in controlling the growth of L.
monocytogenes, followed by vacuum and lastly air packaging.
356
4.1.5. High-pressure processing (HPP)

High-pressure processing is an emerging non-thermal process
that can be used to destroy pathogenic microorganisms in seafood
without greatly affecting the quality of the product. In addition to
improving the safety of shrimp, HPP has also been demonstrated to
extend shrimp shelf-life (Lpez-Caballero, Perez-Mateos, Borderias, & Montero, 2000b; Montero, Lopez-Caballero, & Perez-Mateos,
2001). Shrimp are generally spoiled by Gram-negative bacteria,
which tend to be relatively pressure sensitive due to their cell wall
structure (Gram & Huss, 2000) and HPP may therefore prove to be
a valuable processing technology for shrimp. Although research
has demonstrated the benet of using HPP on shrimp and shrimp
products, limited studies have been carried out specically to eliminate or reduce Salmonella or Listeria in shrimp using this
technology.
4.1.6. High-pressure carbon dioxide (CO2)
The feasibility of using high-pressure CO2 to reduce the number
of Listeria in spiked (approximately 106 cfu/g) peeled shrimp has
been investigated by Wei, Balaban, Fernando, and Peplow (1991).
They found that treatment at 13.7 MPa for 2 h reduced 99% of L.
monocytogenes on shrimp.
4.2. Chemical approaches
4.2.1. The use of chlorine
Chlorine is the decontaminating agent most widely used to kill
pathogenic microorganisms in the seafood industry (WHO, 1984).
It is used to disinfect water used in the process (such as thawing
frozen products), washing raw materials and in making ice for
chilling shrimp. Commonly used chlorine compounds are liquid
chlorine solution (HOCl) and hypochlorite (OCl ). More recently
chlorine dioxide (ClO2) and electrolyzed oxidizing (EO) water have
also been used for this purpose. Specically, ClO2 has been recognized as a bactericidal, viricidal and fungicidal agent and is widely
used in Europe and US as an alternative to chlorine and hypochlorite. In addition, EO water has also been shown to possess strong
bactericidal activity against various foodborne pathogens (Kim,
Hung, & Brackett, 2000).
Although widely used in the seafood industry, there are only a
handful of published articles on the effectiveness of chlorine in
reducing the number of spoilage or pathogenic bacteria in shrimp
and even fewer have focused on Salmonella and Listeria. For instance, the effect of chlorine on Vibrio cells on shrimp has been reported by Chaiyakosa, Charernjiratragul, Umsakul, and Vuddhakul
(2007) and Sousa, Vieira, Patel, Hofer, and Mesquita (2001). Kim,
Huang, Marshall, and Wei (1999) demonstrated the effectiveness
of ClO2 in reducing the bacterial load (aerobic plate count) of
brown shrimp stored at 4 and 20 C for 3 and 7 days. In another
investigation ClO2 was reported to reduce the aerobic and psychrotrophic bacterial counts on shrimp stored at 5 C for 21 days (Andrews, Key, Martin, Grodner, & Park, 2002).
There has been a reported attempt to reduce Salmonella spp. on
inoculated fresh shrimp using EO water (Loi-Braden, Huang, Kim,
Wei, & Weese, 2005). The EO water is generated from a very dilute
sodium chloride (NaCl) solution by using a commercial electrolytic
cell containing a positively charged anode and negatively charged
cathode separated by a membrane. The NaCl undergoes electrolysis to produce hypochlorus acid (HOCl) and sodium hydroxide
(NaOH). The nding of this study indicated that acidic EO at
40 ppm free available chlorine is as effective as aqueous chlorine
of the same concentration. Furthermore, the EO was signicantly
more effective (p < 0.05) than tap water in reducing Salmonella load
on the inoculated shrimp. It was noted that reduction of pathogen
numbers was also observed after a period of frozen storage. Work
by Paranjpye et al. (2008) demonstrated that immersion of natu-
rally contaminated L. monocytogenes on IQF shrimp in a water tank

containing 5 ppm ClO2 for 10, 20, and 30 min is not effective in
inactivating L. monocytogenes on cooked shrimp meat.
4.2.2. The use of ozone
Both gaseous and dissolved forms of ozone are approved to be
used as antimicrobial agents by the food industry, including the
seafood industry (FDA, 1982). The application of ozone has an
advantage over processes such as cooking, as there is less weight
loss and toughening associated with this technology. Ozone may,
however, result in the development of undesirable compounds in
foods through the oxidation of proteins and unsaturated fatty acids
(Menzel, 1984). Chen, Huang, Moody, and Jiang (1992) investigated
the effect of 2% ozonated saline (5.2 mg ozone/L, 5 C) on the inactivation of nine bacterial strains (including S. typhimurium) in
shrimp meat. Their ndings showed that S. typhimurium was the
most resistant of the species tested, with only 0.1 log cycle reductions. Other authors (Chawla, Bell, & Janes, 2007) studied the optimization of ozonated water to reduce total bacterial counts in
white shrimp (Litoenaeus setiferus). They found that soaking
shrimps in 3 ppm dissolved ozone for 40 and 60 s caused the greatest reduction of total aerobic counts on the shrimp meat. Paranjpye
et al. (2008), on the other hand, specically investigated the effect
of washing and soaking of naturally contaminated L. monocytogenes on IQF shrimp in 5 ppm ozonated water and ozone gas. They
found that regardless of whether shrimp were washed or soaked
with ozonated water for 20 or 60 min, or exposed to ozone gas
for similar durations, the treatment was ineffective in inactivating
L. monocytogenes. Ozone also seemed to have a deleterious effect
on the physical appearance of the shrimp after prolonged treatment (120 min) resulting in the distinctive pink tones of the esh
fading to white.
4.2.3. The use of phosphates
Some studies have sought to eliminate or reduce L. monocytogenes on shrimp using food additives. For example, Mu, Huang,
Gates, and Wu (1997) investigated the efcacy of using trisodium
phosphate (TSP) at 10% and 20% concentration to reduce L. monocytogenes on fresh shrimp. No signicant reduction in L. monocytogenes was apparent in this study regardless of the concentration
of TSP used. These authors suggested that cells of L. monocytogenes
might have formed strong attachment to the shrimps shell, or become physically entrapped, and were thus not readily affected by
TSP. In addition, the alkaline pH range resulting from TSP treatment might actually enhance the attachment of L. monocytogenes
to the shrimps surface as observed by Herald and Zottola (1988).
These authors found greater attachment of L. monocytogenes to
stainless steel surfaces at pH 8.0 than 5.0 or 7.0.
4.2.4. The use of quaternary ammonia compounds
Previously Dupard, Janes, Beverly, and Bell (2006) investigated
the efcacy of cetylpyridinium chloride (CPC) in a soaking treatment to reduce L. monocytogenes V7 on the surface of raw and
cooked shrimp. The largest reduction of 7.0 logs was observed from
cooked shell-on shrimp treated with 1.0% CPC, whereas only 4.5
log reductions were observed in raw shell-on shrimp. Recently
Kim (2007) studied the effect of lactic acid and CPC individually
and in combination in reducing the S. typhimurium population
on RTE shrimp. A single intervention of CPC (up to 1.34 log cfu/g
reduction) was more effective than lactic acid used alone (0.9 log
cfu/g reduction) or in combination (0.83 log cfu/g reduction).
4.2.5. Others
The efciency of monoglycerides (glycerol mono-esters of fatty
acids) in reducing L. monocytogenes in cooked shrimp was investigated by Wang and Johnson (1997). These authors found that
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
of illness from seafood (from US data), there is a need to determine

the thermal inactivation kinetics of this organism in seafood
(including shrimp). With more value-added shrimp products in
the market and given the fact that food components inuence
the heat resistance of Salmonella and Listeria, research also needs
to be carried out on the effect of different ingredients and the relative effects on survival and heat resistance of Salmonella and
Listeria.
Nowadays, marinated shrimps have become popular as they are
convenient to cook and come in various avours. Marinated
shrimps are also economically benecial because the product has
an extended shelf-life. Marinating technology in other meat and
poultry industries is well developed and research has demonstrated the antimicrobial properties of the marinades towards certain foodborne pathogens. However, similar effects of marinades
on pathogenic bacteria in shrimp are not well established.
Since the majority of foodborne illness cases reported occur at
home as a result of improper food handling (Knabel, 1995), more
research needs to be carried out in this area too. The rapid-paced
lives and lack of food safety knowledge indicate a need for additional approaches to decrease incidence of foodborne illnesses at
home. Furthermore the relatively recent trend in green consumerism has led to a renewal of scientic interest in ordinary household
items to be used as sanitizer (Smid & Gorris, 1999). However not
much research has been conducted on consumer use of easily
available compounds to rinse raw shrimp as a means of reducing
microbial or better pathogen loads prior to preparation.
6. Conclusions
This survey of the literature suggests that most investigations of
the interaction of Salmonella and Listeria with shrimp are surveys
studying the presence of these bacteria, studies determining the
growth of these pathogens on shrimp or studies testing various
chemicals or treatments for killing these bacteria on shrimp. There
are few studies investigating what initially allows bacteria to associate with shrimp and how they remain attached. By the factors involved in this process, we suggest that more effective strategies for
their control can be developed. In addition, further research needs
to be carried out on control of these pathogens at household or
food establishment levels. It is also apparent that there is a strong
need to develop cost effective minimal processing and chemicalfree technologies which can effectively eliminate pathogens and
simultaneously allow a shelf-stable and fresher product to be
produced.
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Food Control 21 (2010) 343361

Contents lists available at ScienceDirect

Prevalence, persistence and control of Salmonella and Listeria in shrimp and

M.N. Wan Norhana et al. / Food Control 21 (2010) 343361

1.2. Shrimp trade

There is a strong market demand for shrimp. World exports of

1.1. Shrimp production

1.3. Shrimp consumption

World export of shrimp

Share of total shery product exported (%)

M.N. Wan Norhana et al. / Food Control 21 (2010) 343361

Australia has always been popular. A survey of Sydneys seafood

accounting for more than half of all detentions (Fig. 1) (Allshouse,

M.N. Wan Norhana et al. / Food Control 21 (2010) 343361

No. of refusal cases

Reasons for refusals

Contaminated with L. monocytogenes

n.s. Not specied.

Microbiological criteria/guidelines/specication/maximum limits

RTE shrimp/cooked shrimp

M = acceptability limit beyond which the results are considered unsatisfactory.

Standard 1.6.1. Australia New Zealand

M.N. Wan Norhana et al. / Food Control 21 (2010) 343361

carapace. This adaptation could lead to increase tolerance to heat

Countries reporting outbreaks

Riedo et al. (1994)

Potasman, Paz, and Odeh (2002)

Crustacean (shrimp, lobster crab) associated outbreaks reported to CDC (19982004).

M.N. Wan Norhana et al. / Food Control 21 (2010) 343361

resulting in the conclusion that shrimp constitutes a very low risk

2. Prevalence of pathogens in the shrimp production chain

ria in the shrimp production chain with respect to their persistence

5.2 (most serotypes will not grow at <7.0)

M.N. Wan Norhana et al. / Food Control 21 (2010) 343361

Shrimp culture environment

Leangphibul et al. (1986)

Iyer and Varma (1990)

Freshly harvested shrimp

103 farms from six

Llobrerra et al. (1990)

Rattagool et al. (1990)

Jeyasekaran and Ayyappan

Koonse et al. (2005)

Gecan et al. (1994)

Iyer and Shrivastava (1989)

Putro et al. (1990)

Wan Norhana et al. (2001)

Fresh and frozen shrimp

Fresh raw shrimp

Reilly and Twiddy (1992)

Jonnalagadda and Bhat (2004)

Kumar et al. (2003)

Pinu et al. (2007)

M.N. Wan Norhana et al. / Food Control 21 (2010) 343361

Fresh White shrimp, Tiger

Asai et al. (2008)

Atanassova et al. (2008)

Process water, ice, oor utensil,

Iyer and Varma (1990)

Iyer and Shrivastava (1989)

Reilly et al. (1992)

Peeled and deveined shrimp

South East Asia

n.s. not specied; n.d not detected.