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 b 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 article info Article history: Received 2 February 2009 Received in revised form 17 June 2009 Accepted 19 June 2009 Keywords: Salmonella Listeria Shrimp Prawns abstract Shrimp are an important commodity in the international fisheries 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 prod- ucts, indicates that the existing practices used by the manufacturers or processors are insufficient 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. Ó 2009 Elsevier Ltd. All rights reserved. Contents 1. Introduction ........................................................................................................ 344 1.1. Shrimp production ............................................................................................. 344 1.2. Shrimp trade .................................................................................................. 344 1.3. Shrimp consumption ............................................................................................ 344 1.4. Problems faced by the shrimp industry ............................................................................. 345 1.4.1. Shrimp safety from a regulatory perspective ................................................................. 345 1.4.2. Shrimp safety from a public health perspective ............................................................... 347 2. Prevalence of pathogens in the shrimp production chain .................................................................... 348 2.1. Salmonella .................................................................................................... 348 2.1.1. Characteristics and importance of Salmonella ................................................................. 348 2.1.2. Prevalence of Salmonella in the shrimp production chain ....................................................... 348 2.1.3. Growth and survival of Salmonella in shrimp and shrimp products ............................................... 351 2.2. Listeria ....................................................................................................... 351 2.2.1. Characteristics and importance of Listeria .................................................................... 351 2.2.2. Prevalence of Listeria in the shrimp production chain .......................................................... 351 2.2.3. Growth and survival of Listeria in shrimp and shrimp products .................................................. 353 3. Attachment and persistence of Salmonella and Listeria on shrimp ............................................................. 353 4. Control of Salmonella and Listeria in shrimp............................................................................... 354 4.1. Physical approaches ............................................................................................ 354 4.1.1. Cooking ............................................................................................... 354 4.1.2. Refrigeration ........................................................................................... 354 4.1.3. Irradiation ............................................................................................. 355 4.1.4. Modified atmosphere packaging (MAP) ...................................................................... 355 0956-7135/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2009.06.020 * 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: [email protected](G.A. Dykes). Food Control 21 (2010) 343–361 Contents lists available at ScienceDirect Food Control journal homepage: www.elsevier.com/locate/foodcont
Prevalence, persistence and control of Salmonella and Listeria in shrimp andshrimp 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, Australiab Fisheries Research Institute, 11960, Batu Maung, Penang, Malaysiac Department of Primary Industries and Fisheries, Hamilton, 4007 Queensland, Australiad Food Science Australia, Brisbane, 4173 Queensland, Australia
a r t i c l e i n f o
Article history:Received 2 February 2009Received in revised form 17 June 2009Accepted 19 June 2009
Keywords:SalmonellaListeriaShrimpPrawns
0956-7135/$ - see front matter � 2009 Elsevier Ltd. Adoi:10.1016/j.foodcont.2009.06.020
Shrimp are an important commodity in the international fisheries trade and there is an indication of anincrease in worldwide consumption of this crustacean. Salmonella and Listeria have been isolated fromshrimps and shrimp products on a regular basis since the 1980s. The continued reporting of the presenceof these pathogens in fresh and frozen shrimps, and even in the lightly preserved and ready-to-eat prod-ucts, indicates that the existing practices used by the manufacturers or processors are insufficient toeliminate these pathogens. This paper reviews the information available on Salmonella and Listeria inshrimp and makes recommendations on control options and avenues for future research in order toimprove shrimp safety and quality.
According to the United Nations Food and Agricultural Organi-sation (FAO) glossary for aquaculture, a shrimp is a decapod crus-tacean of the suborder Natantia, in the largest phylum in theanimal kingdom, the Arthropoda, and is characterized by jointedappendages and a periodically molted exoskeleton (FAO, 2008).The terms ‘‘shrimp” and ‘‘prawn” are used interchangeably for dif-ferent species in different parts of the world; however the FAO con-vention is to call the marine and brackish-water forms of thesedecapods ‘‘shrimps” and the freshwater forms ‘‘prawns”. For thepurpose of this review, the term ‘‘shrimp” is used to refer to all spe-cies of shrimp and prawns.
1.1. Shrimp production
Recent statistical data on shrimp production from both wildharvest and farm culture estimate levels at approximately 6624million metric tonnes totalling a value of more than US$ 23 billion.Wild harvest shrimp had traditionally been the major source forthe world shrimp market but as the levels from this source are sea-sonal and fluctuate, production from it has remained more or lessconstant over the years (Table 1). In 2000, for example, productionof wild harvest shrimp was estimated at around 3000 million met-ric tonnes, followed by a slight dip in 2001 and 2002 beforeremaining almost constant at 3.5 million tonnes from 2003 to2006 (FAO, 2009). Due to the inconsistency of the natural supply,increased efforts have been directed towards the production ofshrimp through aquaculture. In the year 2000, cultured shrimponly represented slightly more than a quarter (27.3%) of the totalshrimp production but it had increased to almost half (48.0%) bythe year 2006 (Table 1).
shrimp production from 2000 to 2006 (FAO, 2009).
Value 2000 2001
e 1000 tonnes 3087 2955US$ million 11,175 10,411
lture 1000 tonnes 1162 1347US$ million 7310 7492
1000 tonnes 4249 4302US$ million 18,485 17,893
tional exports of shrimp by FAO ISSCAAP (International Standard Statistical Classifi
There is a strong market demand for shrimp. World exports offresh and frozen shrimp (two major trade categories) have showna remarkable increase over the last 10 years (Table 2). In 1986,world shrimp exports totalled about 1.4 million metric tonnesbut tripled to almost 4.5 million tonnes in 2006 fuelled by in-creased world production, primarily from farming activities andfavourable economic conditions. Shrimp remains as one of themost popular seafood throughout the world and in 2006 contrib-uted 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 commercialvalue product in seafood trade (FAO, 2009).
1.3. Shrimp consumption
The increase in consumption of shrimp has been specifically re-ported in several countries. The United States (US) National MarineFisheries Services (NMFS) reports that shrimp consumption per ca-pita has increased steadily over the years from an average of 1.0 kgper year in 1989 to a record high of 1.8 kg in 2005 (NMFS, 2007).For the first time in 2001, shrimp surpassed canned tuna as themost consumed seafood in the US and has continued to grow inmore recent years (Hanson, House, Sureshwaran, G., & S., 2006).Similarly in the European Union (EU) the appetite for shrimp hascontinued to expand, evidenced by growth in most key marketsduring 2005. Figures for 2006 indicate new import levels especiallyfor Spain and France (O’Sullivan, 2006). Consumption of shrimp in
Fig. 1. Share of FDA violations for Salmonella by seafood product in 2001 (fromAllshouse et al., 2004).
M.N. Wan Norhana et al. / Food Control 21 (2010) 343–361 345
Australia has always been popular. A survey of Sydney’s seafoodretailers (fishmongers, supermarkets and fish and chips outlets)in 1999 indicated that cooked farmed prawns, baby octopus andNile perch were the outstanding ‘new-stars’ among all the three re-tailer types (Anon., 2002a). Green (uncooked) prawns also enteredthe list of best-selling seafood for Sydney fishmongers and super-markets, whereas they had not rated a mention in a 1991 survey.A similar trend was also evident in other parts of Australia (Perthand Melbourne).
Shrimp is enjoyed for the uniqueness of its flavour and texture.It can be served as appetizers or easy snacks. More importantly, interms of human health, the high cholesterol content of shrimp iscompensated by the very low total lipid content and the predom-inance of polyunsaturated fatty acids, especially the n-3 fatty acids.Findings suggest that moderate shrimp consumption will not ad-versely affect the overall lipoprotein profile in humans and canbe 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 con-clusion after testing the effects of diets matched for macronutrientcomposition, but with different amounts and sources of cholesterol(i.e., shrimp and egg), in normolipidemic human subjects. Anotheradvantage of shrimp meat is that the mercury content is relativelylower than other seafood. The US National Health and Nutritionsurvey (1999–2002), which evaluated most commonly consumedseafood species as sources of methyl mercury (MeHg) and ome-ga-3 fatty acids, indicated that salmon followed by shrimp arethe principal sources of omega-3 fatty acids and are lesser sourcesof MeHg compared to tuna which provides omega-3 fatty acids butalso considerably higher levels of MeHg (Mahaffey, Clickner, & Jef-fries, 2008).
1.4. Problems faced by the shrimp industry
One of the major problems faced by the shrimp industry, be-sides insufficient production and disease outbreaks, is shrimpproduct safety. A substantial proportion of shrimp product origi-nates from developing countries and there is therefore a possibilityof spreading pathogens between countries with an associated riskof foodborne illness. This concern has contributed to the enforce-ment of standards and regulatory procedures for shrimp products.The US Food and Drug Administration (FDA), for example, mayplace individual shrimp processing facilities or entire countrieswith a history of Salmonella-positive products on a list for ‘‘deten-tion without physical examination”. This means that every ship-ment of shrimp will be detained automatically and denied entryinto the US unless evidence is provided that the shipment is freeof Salmonella (FDA, 2004a). Due to these, as well as to ensure goodeconomic returns, shrimp quality and safety improvement are al-ways at the forefront of concerns by processing companies andexporting countries. Shrimp are important with respect from twoperspectives: regulatory and public health.
1.4.1. Shrimp safety from a regulatory perspectiveSeafood is among the most common product that causes notifi-
cation of import alerts in importing countries. The EU Committeeon Rapid Alert System for Food and Feed (RASFF) indicates thatseafood caused more notifications from 2001 to 2005 than otherproducts such as meats, herbs and spices, fruits, vegetables, andnuts. In the EU, shrimp constitutes about 30–40% of total seafoodalert notifications and 5–10% of alerts for all food imports (Anon.,2002b, 2003, 2005). Meanwhile import detentions by the FDA forseafood products accounted for almost 27% of the total detentionsin 2001, second only to the vegetable/vegetable products category.Again shrimp (wild-harvest plus aquaculture combined) consti-tuted by far the largest proportion of import items detained,
accounting for more than half of all detentions (Fig. 1) (Allshouse,Buzby, Harvey, & Zorn, 2004). Similarly, under the Imported FoodProgram (IFP) implemented by the Australian Quarantine andInspection Service (AQIS), seafood (smoked fish, crustaceans andmolluscs) 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 inter-national seafood trade based on the number of border cases in theEU, US, and Japan indicated that the presence of pathogenic bacte-ria 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 tradeflow. The main bacterial species that cause detention in the USare Salmonella (35.6%) and followed by Listeria (4.1%) (Table 3). Sal-monella was also the second main cause of shrimp rejection (undermicrobial 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 Liste-ria monocytogenes has also been reported (Table 4). Although theimpact of Salmonella and Listeria (through shrimp products deten-tion, rejection, and recalls) on shrimp trade has not been quanti-fied, it is believed to be substantial. Direct and indirect financiallosses can result from these events through re-inspection, analys-ing samples, reviewing records, expiry of shelf-life and the costof handling products.
Currently there is no international agreement on ‘acceptablelevels’ of Salmonella or L. monocytogenes on food, includingshrimps. While details on the policy for the presence of Salmonellaand L. monocytogenes in food from all countries are not available,examples from some individual countries and food authoritiesare listed in Table 5. A regulatory requirement for the absence ofSalmonella (sometimes referred to as a zero tolerance policy) hasbeen established for raw or cooked/ready-to-eat (RTE) shrimps inAustralia, New Zealand, the EU, Hong Kong and the US. The Inter-national Commission of Microbiological Specification for Food(ICMSF) also suggests that Salmonella should not be detected in25 g raw or cooked shrimp products. Some countries such as theUS, Austria, Australia, New Zealand, and Italy have requirementsfor the absence of L. monocytogenes in 25 g of foods (FAO, 1999).On the other hand, other European countries (Germany, Nether-land and France) have a regulatory tolerance of less than 100 cfu/g of this pathogen at the point of consumption. Others still (Canada
Table 3Seafood import refusals by US FDA from July 2001 to June 2003 (Ababouch et al., 2005).
Year Month No. of refusal cases Reasons for refusals
* Note that for some products several reasons, e.g., both ‘‘filthy” and ‘‘Salmonella” are given as reasons for rejection but computed as one border case only. This explains whynumber of border cases is not the total of causes presented horizontally.
Table 4Shrimp products recalled from the market due to contamination with pathogenic bacteria.
Year Product Type Quantity Reason
1987 Shrimp Class 1 >14,099.4 kg Contaminated with L. monocytogenes1988 Shrimp Class 1 41 cartons (6 � 5 pounds plastic bag/carton) Contaminated with L. monocytogenes1988 Cooked and peeled IQF shrimp Class 1 n.s. Contaminated with L. monocytogenes1993 Shrimp salad Class n.s. Contaminated with L. monocytogenes1993 IQF shrimp Class 1 n.s. Contaminated with L. monocytogenesMay 1993 IQF shrimp Class 1 280 kg (50,272 cases) Contaminated with L. monocytogenesJuly 1993 Cooked shrimp Class 11 1319 cases Contaminated with SalmonellaJanuary 1995 Breaded shrimp Class 11 6153 cases Bacterial and decompositionJuly 2000 Cooked-peeled shrimp (IQF) Class 1 1665 kg Contaminated with L. monocytogenes
n.s. – Not specified.Source: http://www.fda.gov.opacom/Enforce.html.
Table 5Microbiological criteria/guidelines for Salmonella and L. monocytogenes in shrimp and shrimp products.
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) Standard 1.6.1. Australia New ZealandFood Standards Code, (1995)
New Zealand Salmonella: nil in 25 g Salmonella: nil in 25 g New Zealand Food Safety AuthorityL. monocytogenes: nil in 25 g
EU Salmonella spp.: absent in 25 g (n = 5, c = 0) EC (1993)Austria, Italy L. monocytogenes: absent in 25 g FAO (1999)Hong Kong Salmonella: absent in 25 g Hong Kong Food and Environmental
Hygiene Department (2001)L. monocytogenes: absent in 25 gUS Salmonella: adulterant Salmonella: adulterant FDA (2004b)
L. monocytogenes: zero tolerance policy L. monocytogenes: zero tolerance policy FAO (1999)ICMSF Salmonella (n = 5, c = 0, m = 0, M = –) Salmonella (n = 10, c = 0, m = 0, M = –) ICMSF (1986)Woolworths L. monocytogenes: not detected in 25 g L. monocytogenes: not detected in 25 g Woolworths (2007)
Salmonella spp.: 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.
346 M.N. Wan Norhana et al. / Food Control 21 (2010) 343–361
M.N. Wan Norhana et al. / Food Control 21 (2010) 343–361 347
and Denmark) have a regulatory tolerance of less than 100 cfu/g forsome food, and a zero tolerance for other foods especially thosewith extended shelf-lives that can support the growth of L. mono-cytogenes. As indicated in Table 5, the criteria are differ substan-tially from country to country and between food authorities. It isdefensible to have a zero tolerance policy for cooked products,since they have extended shelf-lives that can support growth ofpathogens. However, a zero tolerance requirements for raw orfresh shrimp may be too stringent since these products are goingto be washed and cooked before consumption. In fact, from thelimited outbreak data available, there is little evidence that lownumber of L. monocytogenes in shrimp will cause listeriosis evenin susceptible individuals (FAO, 1999). Such requirements caneffectively limit, or even block, shrimp trade resulting in substan-tial economic losses to the exporting countries, manufacturersand producers. With a science based risk assessment approachmore countries, such as Australian and New Zealand (FSANZ,2002) and the EU (EC (European Commission), 2005), have startedto implement an action level of 100 cfu/g for L. monocytogenes incooked shrimp products. A risk based approach considers the po-tential for growth of L. monocytogenes in cooked shrimp based oncriteria such as pH, water activity and shelf-life of the product.As the minimum infectious dose for L. monocytogenes is low (basedon low number of listeriosis cases), therefore the likehood of anyfood contaminated with low number of L. monocytogenes is consid-ered remote (FAO, 1999). There therefore seems little justificationfor regulating against products in which the pathogen cannot growif the level is at or below 100 cfu/g. The regulatory criteria for Sal-monella in cooked and raw shrimp have still been maintained bymost countries. This is due to a strong opinion, that Salmonella isnot part of the natural flora of the shrimp culture environment,nor is it inherently present in shrimp grow-out ponds, and thattheir presence clearly indicates fecal contamination.
There is a possibility that contamination of imported cookedshrimp are partly due to the US policy on forcing importers to havecontaminated shrimp cooked before approving their entry into theUS. Studies have shown that there is an additional risk that crosscontamination between raw and cooked products will occur inprocessing plants. For instances public health authorities in theUK have found the same serotypes of Salmonella in cooked prawnsand those which have been isolated from ponds during their sur-vey (Communicable Disease Report 1989, 1990 as cited in Reilly& Twiddy, 1992). In addition, the attachment and colonization ofbacteria to surfaces increases their resistance to stress, especiallyif the surfaces have naturally protective microhabitats like shrimp
Table 6Main documented cases of outbreaks associated with crustacean (including shrimp).
Agent No. of outbreaks No. of cases Countries repo
a Crustacean (shrimp, lobster crab) associated outbreaks reported to CDC (1998–2004b Of the 119 crustacean-associated outbreaks of unknown etiology, five were suspect
three were suspected Salmonella, and one was suspected Shigella.
carapace. This adaptation could lead to increase tolerance to heattreatments.
1.4.2. Shrimp safety from a public health perspectiveFrom a public health point of view, shrimp safety is becoming
more of a concern. The expanded international seafood trade hasfacilitated the introduction of pathogens into new geographic areasand human communities. Meanwhile the extensive use of antibiot-ics in intensive aquaculture has increased the development of mul-tiple-resistant pathogenic bacteria. This concern has beenhighlighted by an elevated prevalence of antimicrobial-resistantSalmonella in shrimp (Wan Norhana, Johara, & Ramlah, 2001; Zhaoet al., 2003) and other claims that RTE shrimp is an internationalvehicle of antibiotic resistant bacteria (Duran & Marshall, 2005).Furthermore, global warming and climate change may also havea potential negative impact on water- and food-borne diseasescaused by microbiological agents (Rose et al., 2001). With shrimpalways being produced in and processed using water; thesechanges may affect shrimp safety. To make it worse, the expandingpopulation of highly susceptible people due to aging, malnutrition,immuno-compromisation (HIV/AIDS, transplant and cancer pa-tients) and illnesses such as diabetes will result in more peopleneeding protection from unsafe food.
Sporadic diseases outbreaks associated with crustacean (includ-ing shrimp) consumption have been reported (Table 6), however,the exact global incidence of disease from this source is not known.In the US, 10–19% of the estimated 76 million foodborne illnessesreported yearly involved seafood (Durborow, 1999). Mead et al.(1999) disagreed with this and stated that some unknown portionof the estimated 76 million is attributable to seafood. Furthermore,the data reported by Durborow (1999) also did not capture unre-ported outbreaks or sporadic cases of foodborne illnesses. Thisraises an important issue in that in some countries, although thereis some sort of reporting system, there is the likelihood of severeunder-reporting, whereas in other countries there is no obligationto report foodborne diseases to public health authorities. All ofthese scenarios illustrate why the global picture of outbreaks fromseafood in general and shrimp in particular is less than clear andcomplete.
Besides significant under-reporting, disease surveillance reportsfrom Europe and North America indicate that human infectionassociated with consumption of shrimp occurs very rarely as com-pared to pork, beef and poultry. This finding was based on theobservation that Salmonella strains isolated from most of theclinical cases appear to be different from those found in shrimp
rting outbreaks References
Riedo et al. (1994)Wallace, Guzewich, Cambridge, Altekruse, and Morse (1999)
Potasman, Paz, and Odeh (2002)NACMCF (2008)a
).ed S. aureus, two were suspected B. cereus, 10 were suspected V. parahaemolyticus,
348 M.N. Wan Norhana et al. / Food Control 21 (2010) 343–361
resulting in the conclusion that shrimp constitutes a very low riskto public health (Feldhusen, 2000). However this might not be truefor all countries. For example S. weltevreden which is a commonisolate from shrimp culture environments and shrimp products(Phan et al., 2005; Reilly & Twiddy, 1992; Shabarinath, Kumar,Khushiramani, Karunasagar, & Karunasagar, 2007; Wan Norhanaet al., 2001), is also the most common serotype involved in humaninfection in Thailand (Bangtrakulnonth et al., 2004), Vietnam (Phanet al., 2005) and Malaysia (Yassin, Tiew, & Jegathesan, 1995). Sta-tistics from the World Health Organization (WHO) also confirmthat S. weltevreden is gaining importance as the most significantcause of non-typhoidal disease in South East Asia and the WesternPacific, in sharp contrast to Western Europe and US, where it isinfrequently found (Aarestrup et al., 2003). The S. weltevredenserovar was also the most common Salmonella serovar found inseafood imported from Thailand and Malaysia (Heinitz, Ruble,Wagner, & Tatini, 2000). These observations could point to foodor waterborne reservoirs of S. weltevreden in countries with highlevels of this serovar which are not linked to seafood. This is prob-ably why although S. weltevreden has historically been a leadingisolate in shrimp coming to US there are not many cases of diseaseassociated with this serovar. In addition, countries in North Amer-ica and the EU that report a large number of salmonellosis cases todata-bank typically do not report rare serovars thus resulting inunder-reporting of these serovars in these countries (Galaniset al., 2006).
Although the number of outbreaks due to shrimp consumptionare low, they still present a potential risk to the public and espe-cially to those who eat raw (sashimi), lightly and partially cooked(seared on the outside and rare on the inside) shrimp. With wide-spread prevalence of Salmonella and Listeria in shrimp, this productshould be cooked sufficiently and handled properly so that inges-tion of viable pathogens that survive cooking processes and crosscontamination in the kitchen are avoided.
In addition to fresh and raw shrimp, cooked shrimp productsare also gaining an important place in the market resulting fromconsumer demand for RTE food. Certain features in cooked shrimpproduction, such as cooking on board fishing vessels, chilling withsea water, intensive handling and long transportation, make themsusceptible to microbial contamination. Furthermore, these prod-ucts are capable of supporting growth of microorganisms, includ-ing pathogenic bacteria. Worse still, they are often consumeddirectly without further heating or cooking thus making them apotentially high-risk food. Similarly organic shrimps, which areproduced with no disinfectants or antimicrobial agents, could rep-resent a serious health or economic threat if not handled and man-ufactured under stringent conditions.
2. Prevalence of pathogens in the shrimp production chain
Although many significant pathogens are associated with theshrimp production chain (Reilly & Kaferstein, 1997) only a few,for example Salmonella, Listeria, and Vibrio, have been thoroughlystudied with respect to their prevalence and impact on regulationand public health. This review discusses only Salmonella and Liste-
Table 7Growth limits for Salmonella (adapted from Jay, Diane, Dundas, Frankish, & Lightfoot, 200
Parameter (other conditions being optimal) Minimum
Temperature (�C) 5.2 (most serotypes wpH 3.8Salt tolerance (%) –*
Water activity (Aw) 0.94
* –: Not reported.
ria in the shrimp production chain with respect to their persistenceon shrimp and shrimp products, as well as strategies to controlthem.
2.1. Salmonella
2.1.1. Characteristics and importance of SalmonellaSalmonellae are Gram-negative, non-sporeforming rods (usually
0.7–1.5 � 2–5 lm in dimensions) and belong to the family Entero-bacteriaceae. They are facultative anaerobes, mostly motile andcan be present in various environmental conditions outside livinghosts including in a desiccated state. They are facultative anaer-obes, mostly motile and can be present in various environmentalconditions outside living hosts including in a desiccated state. Theyare, however, unable to grow under desiccated conditions. Table 7indicates the various factors, with upper, lower and optimal limits,that support the growth of this genus. Salmonella is frequentlyfound in the intestinal tract of numerous animals including birdsand man. There are more than 2500 serovars and are consideredpotential pathogens in animal and human.
Salmonellosis constitutes a major public health burden and rep-resents a significant cost to society in many countries. Very fewcountries report data on the economic cost of the disease. In theUSA, an estimated 1.4 million non-typhoidal Salmonella infectionsare 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$ 3billion (Economic Research Services (ERS), 2009). Salmonella wasthe most frequent cause of outbreaks of seafood illnesses in theUS from 1998 to 2004 (National Advisory Committee on Microbio-logical Criteria for Food (NACMCF), 2008).
2.1.2. Prevalence of Salmonella in the shrimp production chainSeveral researchers have studied Salmonella prevalence in
shrimp culture environments especially in the tropics (Table 8).Salmonellae have been isolated from shrimp pond water includingsource water and holding ponds (Bhaskar et al., 1995, 1998; Iyer &Varma, 1990; Koonse, Burkhardt, Chirtel & Hoskin, 2005; Leang-phibul, 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; WanNorhana et al., 2001), feed (Bhaskar et al., 1995; Bhaskar et al.,1998; Wan Norhana et al., 2001), manures used for the fertilizationof shrimp ponds (Llobrerra et al., 1990; Reilly, Twiddy, & Fuchs,1992) and in probiotics used to promote shrimp health (Koonseet al., 2005). These reported incidences indicate that Salmonellacan be found in shrimp farms irrespective of the culture methodsas 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 cultureenvironment, it is not surprising they are also detected in farmedshrimp species such as white shrimp (Penaeus merguensis) from
3).
Optimum Maximum
ill not grow at <7.0) 35–37 45–475.5–7.5 9.5–* 4–5–* >0.99
Table 8Prevalence of Salmonella in the shrimp production chain.
Point of sampling Type of sample Origin of sample No. ofsamples
Positive(%)
Common serotypeisolated
References
Shrimp culture environment Pond water Thailand 139 0.5 n.s. Leangphibul et al. (1986)Sediment 144 0.1Freshly harvested shrimp 23 n.dPond water India n.s. n.s. S. weltevreden Iyer and Varma (1990)Mud S. farmsen
S. newportMud/water Major aquaculture
region22.1 S. weltevreden Reilly and Twiddy (1992)
Freshly harvested shrimp 16.0Pond water Indonesia n.s. n.s. Putro et al. (1990)Sediment One
sampleFreshly harvested shrimp One
sampleManure Philippines 0–23.0 n.s. Llobrerra et al. (1990)Freshly harvested shrimp 3.0Shrimp heads and gut 11.0Farmed P. merguiensis Thailand n.s. S. weltevreden Rattagool et al. (1990)During Farming India Bhaskar et al. (1998)Pond water 30 37.4 n.s.Sediment 30 28.8Shrimp 18 37.5Clam meat 30 31.2Formulated feed 30 25.6At harvestPond water 6 54.5Sediment 6 16.7Shrimp 18 12.5Pond water Malaysia 280 67.0 S. weltevreden Wan Norhana et al. (2001)Sediment 40 5.0Freshly harvested shrimp 340 23.0Feed 25 5.0Freshwater shrimp India n.s. n.s. n.s. Jeyasekaran and Ayyappan
(2002)(Machrobrachium rosenbergii)Feces 103 farms from six
countries65 9.2 S. weltevreden Koonse et al. (2005)
Pond water 145 8.2Source water 120 5.0Holding pond water 40 2.5Pond grow-out water 261 3.5Waste water 3 33.0Processing water 22 13.6Pond sediment 225 1.0Source sediment 25 24.0Probiotic samples n.s. 25 4.0Feeds 63 0Shrimps 247 1.6
Wholesale market/distributors/importers
Fresh and frozen shrimp US 211 8.1 n.s. Gecan et al. (1994)Imported raw shrimp US 3683 4.3 S. weltevreden Heinitz et al. (2000)Imported RTE cooked seafooda 1766 2.0 S. senftenbergFresh shrimp Hydrebad, India 35 11.0 n.s. Jonnalagadda and Bhat (2004)
Retailers Dried shrimp Bombay, India 25 4.0 n.s. Iyer and Shrivastava (1989)Raw shrimp Malaysia 16 25.0 S. blockley Arumugaswamy et al. (1995)
S. weltevredenS. agona
Shrimp paste 19 10.5 S. chincolS. newportS. kentucky
Fresh raw shrimp Coimbatore, India S. senftenberg Hatha andLakshmanaperumalsamy(1997)
M. rosenbergii 30 20.0 S. typhimuriumParapenaeopsis stylifera 32 6.3 S. weltevredenP. indicus 85 21.2 S. paratyphi BP. monodon 90 11.1 S. typhiFresh shrimp Mangalore, India 20 5.0 n.s. Kumar et al. (2003)Fresh shrimp Hydrebad, India 35 11.0 n.s. Jonnalagadda and Bhat (2004)Shrimp Vietnam 110 24.5 S. weltevreden Phan et al. (2005)
S. tennesseS. dessau
Fresh shrimp Dhaka 11.0 n.s. Pinu et al. (2007)Fresh shrimp Mangalore, India 27 59.0 S. weltevreden Shabarinath et al. (2007)
(continued on next page)
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Table 8 (continued)
Point of sampling Type of sample Origin of sample No. ofsamples
Positive(%)
Common serotypeisolated
References
Fresh White shrimp, Tigershrimp
Japan 212 2.4 S. weltevreden Asai et al. (2008)
Frozen shrimp sushi Germany 16 18.8 n.s. Atanassova et al. (2008)Fresh shrimp Cochin, India 58 18.9–34.4 n.s. Kumar et al. (2008)Captured shrimp Sri Lanka 180 14.4 S. newport Ubeyratne et al. (2008)Cultured 11.1 S. weltevreden
Manufacturers/processors/exporters
Process water, ice, floor utensil,table top, animal droppings
India n.s. n.s. S. weltevreden Iyer and Varma (1990)
S. bareillyS. typhimurium
Peeled and deveined shrimp India 150 12.0 n.s. Iyer and Shrivastava (1989)Headless shell-on shrimp 130 10.0Peeled undeveined shrimp 100 14.0Cooked and peeled shrimp 180 0.0Dried non-penaeid shrimp 25 4.0Utensils 150 2.0Floor 50 4.0Water 120 1.0Processed shrimp products South East Asia n.s. 0.5–2.8 n.s. Reilly et al. (1992)IQF and cooked shrimp India 2178 1 sample S. typhimurium Hatha et al. (1998)IQF and cooked shrimp India 2390 1 sample S. typhimurium Hatha et al. (2003)
n.s. – not specified; n.d – not detected.a Includes cooked shrimp, breaded shrimp and shrimp balls.
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Thailand (Rattagool, Wongchida, & Sanghtong, 1990), freshwaterprawn (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 majorshrimp producing countries (Koonse et al., 2005; Reilly & Twiddy,1992; Reilly et al., 1992). The percentage of occurrence of Salmo-nella in pond water is higher (0.5–67.0%) than in shrimp (1.6–37.5%), feed (fresh and formulated) (5.0–31.2%) and sediment/mud (0.1–28.8%). It should be noted that there are also reportsindicating the absence of Salmonella in shrimp culture environ-ments (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 sce-nario as in some of these studies the numbers of samples taken andponds examined were low and no repeated testing was performed.
Based on their studies Bhaskar et al. (1995, 1998), Iyer andVarma (1990), Reilly and Twiddy (1992) and Wan Norhana et al.(2001) concluded that Salmonella was a part of the natural floraof the shrimp culture environment. This conclusion is supportedby the WHO declaration which recognized Salmonella as ‘‘geonotic”disease, as well as the fact that foodborne zoonoses that are noteasily eliminated from the food chain. However, Dalsgaard et al.(1995) strongly maintained that Salmonella did not appear to con-stitute a normal part of the microflora in tropical brackish-waterenvironment, a point of view supported by the low occurrence ofSalmonella in some studies (Leangphibul et al., 1986; Putro et al.,1990). The latter suggestion was strongly backed up by the find-ings from a comprehensive study of 103 shrimp aquaculture farmsin six countries (two from Southeast Asia, one in central Asia, onein Central America and one in North America). A significant rela-tionship was found between the log number of fecal bacteria andthe probability that any given sample would contain Salmonella.There also was a clear connection between Salmonella serotypesin source water and grow-out pond water and in other samples.The study concluded that Salmonella was not part of the naturalflora of the shrimp culture environment, but that its occurrencewas significantly related to the concentration of fecal bacteria inthe source and grow-out pond water (Koonse et al., 2005).
The sources of Salmonella introduction into the shrimp cultureenvironment have been investigated. Some studies suggest thatanimal manure and contaminated feeds added to grow-out pondsare possible sources of Salmonella (Bhaskar et al., 1995; Bhaskaret al., 1998; Llobrerra et al., 1990; Reilly & Twiddy, 1992), whileothers claim that sediment (Iyer & Varma, 1990; Reilly et al.,1992) and water (Bhaskar et al., 1995) are possible sources ofcontamination.
In addition to shrimp culture environments, there are reports ofSalmonella in fresh and frozen shrimp collected from landing cen-tres, 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), In-dia (Hatha & Lakshamanaperumalsamy, 1997; Jonnalagadda &Bhatt, 2004; Kumar, Sunil, Venugopal, Karunasagar, & Karunasagar,2003; Kumar, Surendran, & Thampuran, 2008), Malaysia (Arumu-gaswamy, Rusul, Abdul Hamid, & Cheah, 1995), Sri Lanka (Ube-yratne et al., 2008), and Vietnam (Phan et al., 2005). There arealso 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 processingenvironments. Iyer and Shrivastava (1989) reported on the inci-dence of Salmonella on processed shrimps, utensils and floor andin water used in a processing plant. The incidence was highest infresh shrimp products (10–14%), followed by floor swab samples(4%), utensils (2%) and processing water (1%). Salmonella howeverwas not detected in cooked shrimp products. Subsequently, withthe implementation of HACCP in shrimp processing plants in India,much lower occurrences were observed (Hatha, Maqbool, & Ku-mar, 2003; Hatha, Paul, & Rao, 1998).
Generally, the prevalence of Salmonella in fresh shrimp andshrimp products isolated from processing plants is comparable(10.0–14.0%) to that from the wholesalers/importers (4.3–11.0%)but much lower than that from retailers (2.4–59.0%). This may bedue to temperature abuse and cross contamination that couldeasily occur at retail level as compared to the controlled environ-ment of the shrimp processing plant. In addition to fresh and fro-zen shrimp, Salmonella has also been shown to be present in
Table 9Growth conditions for Listeria (adapted from Sutherland, Miles, & Laboyrie, 2003).
Parameter (other conditions being optimal) Minimum Optimum Maximum
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preserved shrimp products such as dried shrimp (4%) (Iyer & Shriv-astava, 1989) and shrimp paste (10.5%) (Arumugaswamy et al.,1995). Furthermore, its occurrence has also been reported in pre-pared RTE items such as cooked shrimp (0.1–2.0%) (Hatha et al.,1998; Hatha et al., 2003; Heinitz et al., 2000) and frozen Nigirishrimp sushi (18.8%) (Atanassova, Reich, & Klein, 2008). The pres-ence of Salmonella in the latter products is alarming as they areusually 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 theshrimp anatomy harbour the most contamination. Rattagool et al.(1990) indicated that Salmonella might be located both internallyand externally. This is in agreement with Hatha and Lakshmanape-rumalsamy’s (1997) observation which indicated 33.8% of Salmo-nella occurred on the shrimp body surface, 35.1% in the gills and31.2% in the alimentary canal. However, Venkateshwaran, Manava-lan, and Natarajan (1985) and Llobrerra et al. (1990) claim that thecephalic region tends to harbour more Salmonella than other bodyparts.
As indicated in Table 8, the most frequently isolated Salmonellaserotypes from shrimp and shrimp products are S. weltevreden andS. typhimurium. The prevalence of S. typhi in Hatha and Lakshman-aperumalsamy’s (1997) study led to speculation that some con-tamination 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 tobe the most frequently isolated serovars from Asian and central Pa-cific seafood products.
2.1.3. Growth and survival of Salmonella in shrimp and shrimpproducts
Although specific studies on the growth rate or survival of Sal-monella in shrimp and shrimp products are limited, a few authorshave indirectly showed that some Salmonella serotypes might havethe ability to survive refrigeration and freezing temperatures (Gec-an et al., 1994; Hatha et al., 1998; Iyer & Shrivastava, 1989). Iyerand Shrivastava (1989) investigated the viability of Salmonella incooked shrimp homogenates at frozen temperatures (�20 �C and�40 �C). All ten serotypes studied were demonstrated to be resis-tant to freezing (�40 �C). However, some differences were ob-served among serotypes during subsequent storage at �20 �C.S. paratyphi B was the most resistant strain and managed tosurvive storage for up to 9 months, while the S. saintpaul wasthe least resistant (up to 5 months). In addition, the ability ofSalmonella to survive a relatively high salt condition has also beendemonstrated (Arumugaswamy et al., 1995).
2.2. Listeria
2.2.1. Characteristics and importance of ListeriaListeria are Gram-positive, non-sporing short rods (0.4–0.5 lm)
that are ubiquitous in nature. They are motile by means of peritri-chous flagella that give a tumbling form of motility (Seeliger &Jones, 1986). They are facultatively anaerobic bacteria with psy-chotropic and mesophilic features. The genus contains six species:L. monocytogenes, Listeria innocua, Listeria seeligeri, Listeria welshi-meri, Listeria ivanovii, and Listeria grayi. Table 9 shows limits andoptimal factors that support the growth of Listeria. L. monocytoge-nes is widely recognized as the principal human pathogen of theListeria genus. Annually listeriosis accounts for about 2500 casesof illness at a cost of approximately US$ 200 million in the US(CCCDC, 2002). Although rare as compared to salmonellosis, liste-riosis manifests as a severe illness with an exceptionally high levelof mortality (20–40%), particularly of those who are most vulnera-ble, for both epidemic and sporadic cases (Slutsker & Schuchat,
1999). Listeriosis is mainly reported from industrialized countrieswith few or no reports from Africa, Asia and South America. Thisobservation may reflect different consumption patterns, dietaryhabits, host susceptibility and lack of testing facilities (Rocourt, Jac-quet, & Bille, 1997), or alternatively a lack of reporting in non-industrialized countries.
2.2.2. Prevalence of Listeria in the shrimp production chainUnlike Salmonella, Listeria spp. are indigenous to the marine
and estuarine environments (Reilly & Kaferstein, 1997) and theirassociation with shrimp is therefore to be expected. Table 10 listsstudies reporting the prevalence of Listeria in the shrimp produc-tion chain. Compared to Salmonella, there are limited studies onthe occurrence of Listeria in the shrimp culture environment.Bhaskar et al. (1995) and (1998) investigated the prevalence ofListeria spp. during the course of shrimp culture and found thatL. monocytogenes was absent from all samples. Of the samplesanalyzed during farming, only feed (clam meat) showed thepresence of L. innocua and L. seeligeri in 10.0% of the samplestested whereas at harvest 50.0% of sediments samples containedL. seeligeri, L. innocua and Listeria murrayii. The L. seeligeri specieswas also detected in 16.6% of shrimp samples at harvest. Thesefindings 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. monocytoge-nes appear to be common in tropical areas. Similarly, Ben Embarek(1994) reported a higher prevalence of L. monocytogenes in shrimpfrom temperate (4–12%) than tropical countries (0–2%). Neverthe-less, some studies conducted after 1994 demonstrated that theprevalence of L. monocytogenes in tropical shrimp equal to thatin temperate shrimp, thus refuting the initial hypothesis.Jeyasekaran, Karunasagar, and Karunasagar (1996) claimed thatthe absence of L. monocytogenes in earlier reports could be dueto inadequate methodology used. These authors demonstratedthat both L. monocytogenes and other Listeria spp. could be foundsimultaneously in shrimp and other seafood tested, and this find-ing indicates that these species might share the same ecologicalniche. This is very significant because the presence of L. innocuaand other non-pathogenic species of Listeria may serve as indica-tors of the presence of L. monocytogenes. A relatively high preva-lence of L. monocytogenes was later reported in other tropicalareas such as Brazil (17.4–18.0%) (Destro, Leitao, & Farber,1996), Costa Rica (33.0–50.0%) (Ellner, Utzinger, & Garcia, 1991as 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 detectL. monocytogenes in fresh and dried shrimp in India. The findingsof the latter study could be due to the limited number of samplestested.
The occurrence of L. monocytogenes in shrimp and shrimp prod-ucts has been well demonstrated (Table 10). The presence of thisgenus in fresh and frozen raw shrimp at retailers, wholesalersand importers is quite common and prevalence varies from verylow to almost 50.0% (Adesiyun, 1993; Berry, Park, & Lightner,
Table 10Prevalence of Listeria in the shrimp production chain.
Point of sampling Type of sample Origin of sample No. ofsamples
Positive for (%) References
Listeria spp. L. monocytogenes
Shrimp pond During farmingSediment India 30 0 0 Bhaskar et al. (1998)Water 30 0 0Fresh raw shrimp 18 0 0Clam meat 30 10.0 0Formulated feed 30 0 0At harvestSediment 6 50.0 0Water 6 0 0Shrimp 18 16.6 0
Wholesalers/distributors/importers
Raw shrimp Imported products(US)
7 n.s. 28.5 Weagant et al. (1988)
Cooked and peeled shrimp 8 25.0Frozen shrimp (for export) Brazil 45 6.6 8.8 Hofer and Ribeiro (1990)a
Raw shrimp US 49 n.s. 9.0 Farber (1991)Frozen raw shrimp Imported products
to US30 16.7 6.7 Berry et al. (1994)
Fresh and frozen shrimp Imported into US 205 6.8 n.s. Gecan et al. (1994)Frozen raw shrimp Imported into US 74 20.0 5.0 Jinneman et al. (1999)Cooked shrimp Imported into Canada 274 n.s. 1.5 Farber (2000)Peeled shrimp 4
Retailers Fresh raw (Metapenaeus sp.) Cochin, India 5 40.0 n.d Fuchs and Surendran (1989)Frozen peeled prawn 4 50.0Fresh and frozen shrimp US 4 25.0 0 Buchanan, Stahl, Bencivengo,
and Dell Corral (1989)b
Fresh shrimp Costa Rica 12 n.s. 33.0 Ellner et al. (1991)a
Frozen shrimp 2 n.s. 50Cooked shrimp n.s. 20 n.s. 20.0 Farber (1991)Frozen semi-ready foodsc Taiwan 68 n.s. 34.0 Wong et al. (1990)Shrimp salad Iceland 13 23.0 23.0 Hartemink and Georgsson (1991)Fresh raw 11 9.0 9.0Fresh and frozen shrimp India 19 10.5 0 Manoj et al. (1991)Freshly caught shrimp US Gulf Coast 74 n.s. 11.0 Motes (1991)Raw seafoodd US 59 28.8–44.1 n.s. Noah et al. (1991)Peeled shrimp in brine Norway 16 n.s. 18.0 Rørvik and Yndestad (1991)Frozen shrimp Japan 70 8.6 1.4 Masuda et al. (1992)b
Raw shrimp Japan 38 n.s. 15.8 2.6 Ryu et al. (1992)Fresh seafoode Trinidad 102 n.s. 10.8 2.0 Adesiyun (1993)Fresh raw shrimp France 17 23.5 11.8 Ravomanana et al. (1993)b
Cooked shrimp 35 54.3 11.4Fresh raw shrimp Malaysia 16 n.s. 44.0 Arumugaswamy et al. (1994)RTE foodf 27 n.s. 22.0Cooked, peeled, frozen shrimp England 30 n.s. 6.0 McLauchlin and Nichols (1994)Fresh raw shrimp Mangalore, India 28 3.6–46.4 10.7 Jeyasekaran et al. (1996)Cured seafoodg Denmark 191 n.s. 4.0 Jørgenson and Huss (1998)Fresh shrimp Chile 59 n.s. 28.8 Cordano and Rocourt (2001)Cooked-peeled and shell-on Australia 380 n.s. 3.0 Anon. (2002c)Fresh shrimp India 11 9.1 n.d Dhanashree et al. (2003)Dried shrimp 27 11.1Fresh shrimp (P. monodon) India 30 73.3 6.7 Moharem et al. (2007)Fresh shrimp and frozen Iran 12 8.3 n.d Jalali and Abedi (2008)Fresh shrimp Goa, India 10 30.0 n.d Parihar et al. (2008)
Manufacturer/processors Frozen shrimp (P. brasiliensis) Brazil 178 47.2 18.0 Destro, Piva, Leitao, and Landgraf(1994)a
Processed seafoodd US 152 5.9–18.4 n.s. Noah et al. (1991)Plant environment Brazil 56 n.s. 25.0 Destro et al. (1996)Water 21 23.8Utensils 33 24.2Shrimp 178 17.4Cooked-peeled shrimp Iceland 3331 8.1 26.5h Valdimarsson et al. (1998)Raw material (fresh shrimp) Iceland 43 23.2 20.9 Gudmundsdottir et al. (2006)Shrimp shell 18 16.7 16.7Plant environment 552 13.4 12.0Cooked-peeled shrimp(end product)
82 n.d n.d
n.s. – not specified 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 identification was done on 49 of the 270 (8.1%) positive samples.
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1994; Buchanan, Stahl, Bencivengo, & Dell Corral, 1989 as reportedin Ben Embarek, 1994; Cordano & Rocourt, 2001; Farber, 1991;Hartemink & Georgsson, 1991; Hofer & Ribeiro, 1990 as reportedin 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 productsdo not pose a threat to the majority of people as they undergosome processing before being eaten. However, they still pose somerisk to susceptible populations when consumed raw or lightlycooked. In addition, the possibility of cross contamination in theprocessing plant, kitchen or food service establishment is also ofconcern.
Of greater consequence is that L. monocytogenes has been iso-lated from RTE shrimp products such as cooked shrimp (Anon,2002c; Farber, 1991, 2000; Ravomanana et al., 1993 as reportedin Ben Embarek, 1994; McLauchlin & Nichols, 1994; Weagantet 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 commercialcooking process. Furthermore, the occurrence of L. monocytogeneshas also been documented in frozen semi-ready foods such asshrimp dumplings (Wong, Chao, & Lee, 1990) and lightly preservedshrimp products such as brined shrimp and oil-marinated shrimp(Jorgensen & Huss, 1998; Rorvik & Yndestad, 1991).
L. monocytogenes occurs in shrimp processing plant environ-ments (25%), water used in processing (23.8%), utensils (24.2%)and on shrimp products (17.4–26.5%) (Destro et al., 1996; Gudm-undsdottir, Gudbjornsdottir, Einarsson, Kristinsson, & Kristjansson,2006; Valdimarsson, Einarsson, Gudbjornsdottir, & Magnusson,1998). The sources of L. monocytogenes introduction into theshrimp processing environment have been investigated. Somestudies have demonstrated that persistent ‘‘in-house” strains of L.monocytogenes may contaminate seafood during processing (Autioet al., 1999; Fonnesbech Vogel, Huss, Ojeniyi, Ahrens, & Gram,2001). Other studies have suggested that transient L. monocytoge-nes from raw seafood contaminate the final products (Gudmunds-dottir et al., 2006; Markkula, Autio, Lunden, & Korkeala, 2005).Regardless of the source, some authors have hypothesized thatthe presence of Listeria in cooked products is due to undercookingof the product (Budu-Amoako, Toora, Walton, Ablett, & Smith,1992; Fuchs & Reilly, 1992).
2.2.3. Growth and survival of Listeria in shrimp and shrimp productsThe growth of Listeria in shrimp may be influenced by factors
including the availability of essential nutrient, pH, temperature,water activity, competitive microflora and the presence of foodadditives that enhance or inhibit growth (Lovett, Francis, & Brad-shaw, 1990). L. monocytogenes can grow at salt concentrations of13–14% and survive in salt at concentrations of up to 30% (Farber,Coates, & Daley, 1992; Fuchs & Reilly, 1992). Salt alone is thereforeunlikely to be a control measure for the growth of L. monocytogenesin processed seafood. L. monocytogenes has also been observed tosurvive for long periods in processing plants, household refrigera-tors and freezers (FDA, 1999). Packaging methods do not affect thegrowth of L. monocytogenes (Harrison, Huang, Chao, & Shineman,1991), although some of the latest packaging technologies, suchas antimicrobial films/wraps or ‘smart packaging’, may be effectivein reducing the growth of Listeria and provide essential protectionduring storage and transportation.
Quantification of the growth and survival of L. monocytogenesin shrimp and shrimp products have been reported. Dorsa, Mar-shall, Moody, and Hackney (1993) reported that L. monocytogeneshas a shorter generation time in seafood products than in other
protein meats. This observation is in agreement with Shinemanand Harrison (1994) who observed that regardless of whetherthe shrimp are cooked or left raw, L. monocytogenes has a signif-icantly (p < 0.01) greater ability to grow on them compared tobeef or chicken stored aerobically at 4 �C. Similarly, the growthrate of L. monocytogenes in cooked crustaceans (including shrimp)(0.38 logs/day at 5 �C) is reported to be higher that most RTE foodsuch as smoked seafood (0.155) and soft cheeses (0.105), but sim-ilar to liquid milk (0.262) and deli meats (0.244) (FSANZ, 2002).Ideal growth conditions, such as pH range (6.8–7.0), water activ-ity (0.99) and salt content (1–2%), may be among the factors thatpromote growth of L. monocytogenes in cooked shrimp (FSANZ,2002). Lovett et al. (1990) specifically examined Listeria growthin refrigerated shrimps and found that after storage for 1–2 weeksat 7 �C the number of L. monocytogenes increased from 103 to106�8 cfu/g. Similarly Farber (1991) noted a 2–3 log increase ofL. monocytogenes in cooked shrimp after storage for 1 week at4 �C. He also observed that L. monocytogenes appeared to growslowly at 4 �C in naturally contaminated shrimp but better in arti-ficially inoculated cooked shrimp. This could mean that naturallyoccurring Listeria are more susceptible to cold. More importantlythis finding suggests that if L. monocytogenes is present in cookedshrimp, even in low numbers, significant levels may be reached ifthe products are stored at temperatures commonly encounteredin chilled display cabinets at retail outlets. Even higher numberscould be rapidly reached in the case of temperature abuse ofproduct.
The growth and survival of L. monocytogenes in lightly preservedproducts, such as brined shrimp, have also been explored. Brinedshrimp is a popular product consisting of cooked and peeledshrimp in brine, which contains salt and combinations of benzoic,citric and sorbic acids. L. monocytogenes have been demonstratedto grow in cold and warm water brined shrimp at temperaturesof 8–25 �C (Dalsgaard & Jorgensen, 2000). In cold-water shrimpwith 3.3% water-phase salt (WPS), growth was observed at 15�and 25 �C, and in warm water shrimp (2.3% WPS) an increase inL. 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 asdetermined by sensory evaluation. In addition, Burnet, Mertz, Ben-nie, Ford, and Starobin (2005) investigated the growth of L. mono-cytogenes in shrimp salad and found that it did not support thegrowth of L. monocytogenes, with the overall population decliningthroughout the 14-days storage period at 5, 7 and 10 �C. The lowpH (4.8 and 4.5) of the shrimp salad used in the study may contrib-ute to the reduction in the L. monocytogenes populations. On theother hand, Hwang and Tamplin (2005) observed L. monocytogenesgrowth in salads (imitation-shrimp crabmeat mixture) regardlessof 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 Lis-teria in other shrimp products is limited.
3. Attachment and persistence of Salmonella and Listeria onshrimp
Bacterial attachment to food production surfaces is regarded asone of the first steps in the contamination of food. It is widely ac-cepted to occur in two stages, reversible and irreversible (Marshall,Stout, & Mitchell, 1971). The former involves the bacteria being inclose enough proximity to allow initial attachment to take place,and this is governed by van der Waals forces, electrostatic forcesand hydrophobic interactions (Gilbert, Evans, Evans, Duguid, &Brown, 1991; Vanloosdrecht, Lyklema, Norde, & Zehnder, 1989).This process is instantaneous and during initial contact bacteriastill show Brownian motion and can be easily removed by shear
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fluid forces e.g., rinsing. The second stage occurs as the bacteria arelocked onto the surface with the help of exo-polysaccharides orspecific structures such as pili or fimbrae. Here, much strongerphysical or chemical forces are required to remove the bacteriae.g., scraping, scrubbing, or chemical cleaners.
With the widespread prevalence of Salmonella and Listeria inshrimp production chains, surprisingly little is known about theirattachment and persistence on shrimp and shrimp products. Bycontrast, studies on Salmonella and Listeria attachment to animal(chicken, beef, pork) food surfaces (Benedict, Schultz, & Jones,1991; Chung, Dickson, & Crouse, 1989; Notermans & Kampelmach-er, 1974; Dickson & Macneil, 1991) have been conducted since the1970s. More recently studies on the attachment of these bacteriato fruits (Pao & Davis, 2001), vegetables (Barak, Whitehand, &Charkowski, 2002; Ells & Hansen, 2006; Garrood, Wilson, & Broc-klehurst, 2004; Gorski, Palumbo, & Mandrell, 2003; Iturriaga,Escartin, Beuchat, & Martinez-Peniche, 2003) and fish (Kim & Mar-shall, 2001; Kim & Marshall, 2002; Verhaegh, Marshall, & Oh, 1996)have been reported. Although information on the attachment ofSalmonella and Listeria to shrimp is very limited, we speculate thatthe process is similar to that associated with meat and plant prod-ucts. It is not known whether Salmonella and Listeria are able to at-tach to and hence externally colonize shrimp carapace and tissue,although some strains of L. monocytogenes have been demon-strated to possess chitinolytic activity (Leisner et al., 2008) andprevious work has suggested chitin particles enhances the attach-ment of L. monocytogenes (McCarthy, 1992). Our recent investiga-tion on the relationship between the physicochemicalcharacteristics of non-chitinolytic Salmonella (S. typhimuriumand S. senftenberg) and Listeria (L. monocytogenes (Scott A andV7) and attachment to shrimp carapace suggested that the chitin-olytic activity of Salmonella and Listeria might not play a major rolein initial attachment to and colonization on the carapace. On theother hand, the bacterial cell surface charges, hydrophobicity, elec-tron donor/acceptor potential as well as the carapace roughnessare significantly related to attachment capabilities of these bacteriato carapaces. Nevertheless, the same properties could not be re-lated to subsequent colonization on the carapace (Wan Norhana,Goulter, Poole, Deeth, & Dykes, 2009). The attachment of bacteriato surfaces increases their resistance to stress, especially if the sur-faces have naturally protective microhabitats (Watnick & Kolter,1999). This adaptation could have important consequences, suchas extended survival periods in the environment and increased tol-erance to treatments that would otherwise be lethal during thepreparation of shrimp in the home, food service establishmentsor processing plants. Currently, there is limited information onthe increase of tolerance observed in Salmonella or Listeria due toattachment to shrimp carapace. There is however a study relatedto this topic by McCarthy (1992) who investigated the effects ofsanitizers on L. monocytogenes cells attached to chitin and observedmore than 10-fold increase in resistance to chlorine, iodine, andquaternary ammonium compound sanitizers compared to sus-pended cells. This author concluded that the recommended con-centrations and time of exposure for disinfectants might noteffectively eliminate Listeria attached to porous surfaces such aschitin.
4. Control of Salmonella and Listeria in shrimp
Owing to the common occurrence of Salmonella and Listeria inshrimp and shrimp products, a number of studies have been car-ried out to develop methods to control pre- and post-productioncontamination of shrimp. These methods are listed in Table 11and summarized in the following section. They are sub-dividedinto physical or chemical approaches.
4.1. Physical approaches
4.1.1. CookingApplication of heat is one of the simplest and most effective
methods of eliminating pathogens from food. Boiling shrimp at100 �C for 1, 3, or 5 min has been shown to eliminate 103–105 Lis-teria cells/g from naturally contaminated shrimp (McCarthy,Motes, & McPhearson, 1990). However, boiling is not able to com-pletely eliminate Listeria in artificially inoculated (105 cells/g)shrimp even after boiling for up to 5 min. The authors assumedthat either the naturally contaminated shrimps were externallycontaminated or naturally occurring Listeria were less heat-resis-tant in their natural environment. In addition, no L. monocytogenessurvived a cook-freeze-thaw process implying that freezing andheating had an additive effect on lethality for L. monocytogenes.Cooking in a microwave oven is also effective in eliminating Listeriaon 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 ininoculated (5 � 105 cfu/g) shrimp. Their results show that Listeriacan be completely inactivated with 2 min holding after microwa-ving 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 naturallycontaminated L. monocytogenes in cooked-peeled shrimp. They ex-posed shrimp that were naturally contaminated with L. monocytog-enes at 16 cfu/25 g to continuous steam cooking for 45, 60, and90 s. The shrimps were then conveyed to normal shrimp process-ing 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 flavour, was slightlytougher and weighed up to 25% less. It should be noted that theheat resistance of L. monocytogenes seems to vary considerablywith the intrinsic properties, such as the lipid content, of the sea-food. For instance, higher D60 (4.23–4.48 min) values were ob-served for salmon fillets which have a higher lipid content thancod (1.95–1.98 min) Ben Embarek & Huss, 1993). Thus, applyingheat resistance results from one product to another product maynot be valid.
In spite of numerous reports on the inactivation of Salmonella inpoultry, beef, and pork using different cooking methods, there isvery limited thermal inactivation data on Salmonella for seafoodin general and shrimp in particular. Doyle and Mazzotta (2000)in their comprehensive review on thermal resistance of Salmonellain food listed only one study on seafood (oysters) and none onshrimp.
4.1.2. RefrigerationRefrigeration and freezing are well-known techniques for
extending the shelf-life of food products. These processes lowerthe temperature to levels at which bacterial metabolic processesare stopped and the rates of chemical and biochemical reactionsreduced. Listeria is known to have the capability to grow at refrig-eration temperatures on shrimp and this has been established byseveral authors (Table 10). A study examining the effect of refrig-erating and freezing L. monocytogenes on shrimp established thatthis pathogen could survive both processes with little increasein numbers on iced shrimp and a slight decrease (less than 1.0log) on frozen product (Harrison et al., 1991). Similarly, Mejlholm,Boknaes, and Dalgaard (2005) demonstrated that L. monocytogenesincreased by 1000-fold at 5� and 8 �C before shrimp, which wasstored under a modified atmosphere, was determined to bespoiled by sensory evaluation. However, in the same productstored at 2 �C, spoilage was not detected. It can be concluded fromthese studies that cooked shrimp contaminated prior to frozen
Table 11Studies on Salmonella and Listeria control in shrimp.
Test microorganisms Type of shrimp (species) References
Irradiation 0.1–4.0 kGy S. enteritidis, S. typhimurium Fresh and frozen shrimp (n.s.) Nerkar and Bandekar (1989)0.5–4.0 kGy L. monocytogenes Frozen shrimp Rashid et al. (1992)2.5–5.0 kGy (cobalt-60irradiation)/2 �C
CPC (0.05%, 0.1%, 0.2%, 0.4%, 0.6%,0.8%, and 1.0%)
L. monocytogenes V7 (1/2 a) Raw shell-on, raw peeled andcooked shell-on (P. aztecus)
Dupard et al. (2006)
Cranberry juice (27%) L. monocytogenes Raw peeled shrimp (n.s.) Beverly (2004)ClO2 (5 ppm/10, 20, and 30 min) L. monocytogenes Cooked and peeled cold-water
shrimp (P. jordani)Paranjpye et al. (2008)
n.s. – not specified.
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storage will remain contaminated after thawing for sale andconsumption.
4.1.3. IrradiationIrradiation 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 effectivemethods for decontaminating both the surface and deep muscleof fresh meat and poultry. There is substantial literature on the ef-fects of irradiation in reducing Salmonella and Listeria on shrimp. Astudy by Nerkar and Bandekar (1989), for example, showed com-plete elimination of Salmonella on frozen shrimp when irradiatedat 4.0 kGy. Similarly Ito, Adulyatham, Sangthong, and Ishigaki(1989) reported that doses of 4.0–5.0 kGy were required to reducethe numbers of S. typhimurium on shrimp by 6.0 log cycles. Inaddition, a slightly lower dose (3.0 kGy) was reported to reduceL. monocytogenes inoculated at a level of 104/g in frozen shrimp(Rashid, Ito, & Ishigaki, 1992). However, irradiation at 5.0 kGywas found to be insufficient to totally eliminate L. monocytogenesin frozen shrimp (Brandao-Areal, Charbonneau, & Thibault, 1995).
Although irradiation appears to be effective in eliminatingpathogens in shrimp, there is an unsubstantiated view amongstthe public that food irradiation is unsafe and undesirable. Thereis also evidence some that irradiation may reduce the nutritionalvalue of some foods by the destruction of aromatic amino acids
(Johnson & Moser, 1967) and producing rancidity and off-odours(Kanatt, Chander, & Sharma, 2005).
4.1.4. Modified atmosphere packaging (MAP)Modified atmosphere packaging facilitates the distribution of
seafood and extends the shelf-life of raw and lightly preservedshrimp products (Dalsgaard & Jorgensen, 2000; Lopez-Caballero,Goncalves, & Nunes, 2002a). Limited studies have been carriedout on the survival of Salmonella and Listeria on chilled or frozenRTE MAP shrimp products. Harrison et al. (1991) noted that vac-uum packaging of shrimp did not enhance the conditions forgrowth of L. monocytogenes (Scott A). Mejlholm et al. (2005) eval-uated the growth of L. monocytogenes in cooked and peeled MAPshrimp. They observed that L. monocytogenes grew at all storagetemperatures studied (2, 5, and 8 �C) and growth at 5 and 8 �C re-sulted in a 1000-fold increase, before the product became spoiledas determined by sensory evaluation. In conclusion, they suggestedthat to prevent L. monocytogenes becoming a safety problem,cooked and peeled MAP shrimp should be distributed at 2 �C andwith shelf-life of 20–21 days. Recently Rutherford et al. (2007)investigated the survival of L. monocytogens in RTE shrimp packedunder different conditions and stored at 3, 7, and 12 �C. Their find-ings indicate that regardless of temperature, MAP packaging incor-porating CO2 is the most effective in controlling the growth of L.monocytogenes, followed by vacuum and lastly air packaging.
356 M.N. Wan Norhana et al. / Food Control 21 (2010) 343–361
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 seafoodwithout greatly affecting the quality of the product. In addition toimproving the safety of shrimp, HPP has also been demonstrated toextend shrimp shelf-life (López-Caballero, Perez-Mateos, Borde-rias, & 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 wallstructure (Gram & Huss, 2000) and HPP may therefore prove to bea valuable processing technology for shrimp. Although researchhas demonstrated the benefit of using HPP on shrimp and shrimpproducts, limited studies have been carried out specifically to elim-inate or reduce Salmonella or Listeria in shrimp using thistechnology.
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 hasbeen 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 chlorineChlorine 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 thawingfrozen products), washing raw materials and in making ice forchilling shrimp. Commonly used chlorine compounds are liquidchlorine solution (HOCl) and hypochlorite (OCl�). More recentlychlorine dioxide (ClO2) and electrolyzed oxidizing (EO) water havealso been used for this purpose. Specifically, ClO2 has been recog-nized as a bactericidal, viricidal and fungicidal agent and is widelyused in Europe and US as an alternative to chlorine and hypochlo-rite. In addition, EO water has also been shown to possess strongbactericidal activity against various foodborne pathogens (Kim,Hung, & Brackett, 2000).
Although widely used in the seafood industry, there are only ahandful of published articles on the effectiveness of chlorine inreducing the number of spoilage or pathogenic bacteria in shrimpand even fewer have focused on Salmonella and Listeria. For in-stance, the effect of chlorine on Vibrio cells on shrimp has been re-ported by Chaiyakosa, Charernjiratragul, Umsakul, and Vuddhakul(2007) and Sousa, Vieira, Patel, Hofer, and Mesquita (2001). Kim,Huang, Marshall, and Wei (1999) demonstrated the effectivenessof ClO2 in reducing the bacterial load (aerobic plate count) ofbrown shrimp stored at 4� and �20 �C for 3 and 7 days. In anotherinvestigation ClO2 was reported to reduce the aerobic and psychro-trophic bacterial counts on shrimp stored at 5 �C for 21 days (An-drews, Key, Martin, Grodner, & Park, 2002).
There has been a reported attempt to reduce Salmonella spp. oninoculated fresh shrimp using EO water (Loi-Braden, Huang, Kim,Wei, & Weese, 2005). The EO water is generated from a very dilutesodium chloride (NaCl) solution by using a commercial electrolyticcell containing a positively charged anode and negatively chargedcathode separated by a membrane. The NaCl undergoes electroly-sis to produce hypochlorus acid (HOCl) and sodium hydroxide(NaOH). The finding of this study indicated that acidic EO at40 ppm free available chlorine is as effective as aqueous chlorineof the same concentration. Furthermore, the EO was significantlymore effective (p < 0.05) than tap water in reducing Salmonella loadon the inoculated shrimp. It was noted that reduction of pathogennumbers was also observed after a period of frozen storage. Workby Paranjpye et al. (2008) demonstrated that immersion of natu-
rally contaminated L. monocytogenes on IQF shrimp in a water tankcontaining 5 ppm ClO2 for 10, 20, and 30 min is not effective ininactivating L. monocytogenes on cooked shrimp meat.
4.2.2. The use of ozoneBoth gaseous and dissolved forms of ozone are approved to be
used as antimicrobial agents by the food industry, including theseafood industry (FDA, 1982). The application of ozone has anadvantage over processes such as cooking, as there is less weightloss and toughening associated with this technology. Ozone may,however, result in the development of undesirable compounds infoods through the oxidation of proteins and unsaturated fatty acids(Menzel, 1984). Chen, Huang, Moody, and Jiang (1992) investigatedthe effect of 2% ozonated saline (5.2 mg ozone/L, 5 �C) on the inac-tivation of nine bacterial strains (including S. typhimurium) inshrimp meat. Their findings showed that S. typhimurium was themost resistant of the species tested, with only 0.1 log cycle reduc-tions. Other authors (Chawla, Bell, & Janes, 2007) studied the opti-mization of ozonated water to reduce total bacterial counts inwhite shrimp (Litoenaeus setiferus). They found that soakingshrimps in 3 ppm dissolved ozone for 40 and 60 s caused the great-est reduction of total aerobic counts on the shrimp meat. Paranjpyeet al. (2008), on the other hand, specifically investigated the effectof washing and soaking of naturally contaminated L. monocytoge-nes on IQF shrimp in 5 ppm ozonated water and ozone gas. Theyfound that regardless of whether shrimp were washed or soakedwith ozonated water for 20 or 60 min, or exposed to ozone gasfor similar durations, the treatment was ineffective in inactivatingL. monocytogenes. Ozone also seemed to have a deleterious effecton the physical appearance of the shrimp after prolonged treat-ment (120 min) resulting in the distinctive pink tones of the fleshfading to white.
4.2.3. The use of phosphatesSome studies have sought to eliminate or reduce L. monocytog-
enes on shrimp using food additives. For example, Mu, Huang,Gates, and Wu (1997) investigated the efficacy of using trisodiumphosphate (TSP) at 10% and 20% concentration to reduce L. mono-cytogenes on fresh shrimp. No significant reduction in L. monocyt-ogenes was apparent in this study regardless of the concentrationof TSP used. These authors suggested that cells of L. monocytogenesmight have formed strong attachment to the shrimp’s shell, or be-come physically entrapped, and were thus not readily affected byTSP. In addition, the alkaline pH range resulting from TSP treat-ment might actually enhance the attachment of L. monocytogenesto the shrimp’s surface as observed by Herald and Zottola (1988).These authors found greater attachment of L. monocytogenes tostainless steel surfaces at pH 8.0 than 5.0 or 7.0.
4.2.4. The use of quaternary ammonia compoundsPreviously Dupard, Janes, Beverly, and Bell (2006) investigated
the efficacy of cetylpyridinium chloride (CPC) in a soaking treat-ment to reduce L. monocytogenes V7 on the surface of raw andcooked shrimp. The largest reduction of 7.0 logs was observed fromcooked shell-on shrimp treated with 1.0% CPC, whereas only 4.5log reductions were observed in raw shell-on shrimp. RecentlyKim (2007) studied the effect of lactic acid and CPC individuallyand in combination in reducing the S. typhimurium populationon RTE shrimp. A single intervention of CPC (up to 1.34 log cfu/greduction) was more effective than lactic acid used alone (0.9 logcfu/g reduction) or in combination (0.83 log cfu/g reduction).
4.2.5. OthersThe efficiency of monoglycerides (glycerol mono-esters of fatty
acids) in reducing L. monocytogenes in cooked shrimp was investi-gated by Wang and Johnson (1997). These authors found that
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monolaurin (MC12) (500 lg/g) was the most inhibitory monoglyc-eride, but was only bacteriostatic rather than bacteriocidal. Whencombined with propyl gallate (200 lg/g) the activity of MC12 im-proved, reducing levels of L. monocytogenes 10–100-fold in cookedshrimp after 2–4 weeks storage at 4 �C, as compared to untreatedcontrol samples.
In another investigation, Beverly (2004) examined the antimi-crobial effect of cranberry juice (27%) against L. monocytogeneson raw peeled shrimp. At 37 �C there were no significant differ-ences in L. monocytogenes population in the marinated shrimp after30 or 60 min. At 4 �C, however, there was a significant differencewhen the shrimp were marinated for 60 min. After 24 h marinatingthe L. monocytogenes counts were reduced by 1 log cfu/ml.
There is a paucity of data regarding the efficacy of novel meth-ods in achieving pathogen inactivation in shrimp products. Fromthe available literature, almost all control or intervention strategiesfocus on the elimination of Salmonella and Listeria in shrimp andshrimp products within the industrial processing environment.There are advantages and disadvantages of each of the control op-tions mentioned. Even though the current literature indicates thatSalmonella and L. monocytogenes can be reduced, but cannot alwaysbe eradicated from finished product or the plant environment, theindustry should work towards elimination of these pathogens.Combinations of natural antimicrobials and high-pressure treat-ment and high-pressure CO2 or vacuum packaging are probablythe most effective of the strategies available. With a 99% reductionof L. monocytogenes by using high-pressure CO2 (Wei et al., 1991)and substantial extension of shelf-life of shrimp using vacuumpackaging and high-pressure treatment (Lopez-Caballero, Perez-Mateos, Borderias, & Montero, 2000), these strategies could syner-gistically enhance the safety and quality of shrimp. In additionthere is no negative public perception of these types of treatmentas compared to irradiation and chemical applications. Otheremerging approaches that could be applied to shrimp are pulsedlight 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 dem-onstrated that the reduction of surface microorganisms is possible(Wong, Linton, & Gerrard, 1998). Pulse light technology was ap-proved by the US FDA in 2003 for application in food products afterbeing evaluated for both safety and effectiveness. However the costof these technologies is high thus limiting their use. In addition,there is a clear requirement for more information on control strat-egies that could be applied at home, in food service establishmentsor at retail level. Furthermore, while there is a larger body of liter-ature on L. monocytogenes; more studies investigating control ofSalmonella in shrimp are required.
5. Research needs
While research has assisted in understanding how and whereshrimp and shrimp products become contaminated with Salmo-nella and Listeria, a greater understanding of the mechanisms andfactors (physico-chemical and environmental) by which Salmonellaand Listeria attach to/colonize shrimp surfaces and how best to kill/remove attached/colonized cells is required. This may assist in thedevelopment of novel interventions to control these pathogens onshrimp. By the same token, more research is required to determinehow resistant are the attached/colonized cells of Salmonella andListeria on shrimp surfaces to environmental stresses, such as in-creases and decreases of temperature, low pH conditions and thebiocidal activity of disinfectant solutions.
There is limited thermal inactivation data for Salmonella in sea-food in general and shrimp and shrimp products in particular. AsSalmonella is the bacterial pathogen that causes the most outbreaks
of illness from seafood (from US data), there is a need to determinethe thermal inactivation kinetics of this organism in seafood(including shrimp). With more value-added shrimp products inthe market and given the fact that food components influencethe heat resistance of Salmonella and Listeria, research also needsto be carried out on the effect of different ingredients and the rel-ative effects on survival and heat resistance of Salmonella andListeria.
Nowadays, marinated shrimps have become popular as they areconvenient to cook and come in various flavours. Marinatedshrimps are also economically beneficial because the product hasan extended shelf-life. Marinating technology in other meat andpoultry industries is well developed and research has demon-strated the antimicrobial properties of the marinades towards cer-tain foodborne pathogens. However, similar effects of marinadeson pathogenic bacteria in shrimp are not well established.
Since the majority of foodborne illness cases reported occur athome as a result of improper food handling (Knabel, 1995), moreresearch needs to be carried out in this area too. The rapid-pacedlives and lack of food safety knowledge indicate a need for addi-tional approaches to decrease incidence of foodborne illnesses athome. Furthermore the relatively recent trend in ‘green’ consumer-ism has led to a renewal of scientific interest in ordinary householditems to be used as sanitizer (Smid & Gorris, 1999). However notmuch research has been conducted on consumer use of easilyavailable compounds to rinse raw shrimp as a means of reducingmicrobial or better pathogen loads prior to preparation.
6. Conclusions
This survey of the literature suggests that most investigations ofthe interaction of Salmonella and Listeria with shrimp are surveysstudying the presence of these bacteria, studies determining thegrowth of these pathogens on shrimp or studies testing variouschemicals or treatments for killing these bacteria on shrimp. Thereare few studies investigating what initially allows bacteria to asso-ciate with shrimp and how they remain attached. By the factors in-volved in this process, we suggest that more effective strategies fortheir control can be developed. In addition, further research needsto be carried out on control of these pathogens at household orfood establishment levels. It is also apparent that there is a strongneed to develop cost effective minimal processing and chemical-free technologies which can effectively eliminate pathogens andsimultaneously allow a shelf-stable and fresher product to beproduced.
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