Cross-contamination and recontamination by Salmonella in foods: A review

Contents

. . . .n and reination. . . .. . . .. . . .. . . .. . . .cts . .. . . .

Food Research International 45 (2012) 545556

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Food Research

e ls6. Modeling Salmonella transfer in foods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 551Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 553References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 553

1. Introduction is variable and may also be affected by human lifestyle and behavior,changes in industry, technology, commerce and travel (Foley, Lynne,Salmonellosis represents an importantcontinues to pose a major and unacceptablehealth in both developed and developing coSafety Authority (EFSA), 2010). The dynamic

Corresponding author. Tel.: +34 957218516; fax: +E-mail address: bt2cajie@uco.es (E. Carrasco).

0963-9969/$ see front matter 2011 Elsevier Ltd. Alldoi:10.1016/j.foodres.2011.11.004. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 550narios and retail points . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 550es . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5514. Cross-contamination in food-handling sce5. Biolm formation and food contact surfac1. Introduction . . . . . . . . . .2. Importance of cross-contaminatio3. Cross-contamination and recontam

3.1. Poultry meat . . . . . .3.2. Other meats . . . . . .3.3. Eggs and egg products . .3.4. Low-moisture foods . . .3.5. Fresh produce and spices3.6. Milk, dairy and milk produ3.7. Seafood . . . . . . . .review on cross-contamination models of Salmonella spp. is presented. 2011 Elsevier Ltd. All rights reserved.

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 545contamination events . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 546routes and sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 547. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 547. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 547. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 548. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 549. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 549. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 549consumer awareness of the risks of cross-contamination in the home and their role in its prevention. Finally, a

Also, at consumer level, Pub

the need to reinforce indusElena Carrasco , Andrs Morales-Rueda, Rosa Mara Garca-GimenoDepartment of Food Science and Technology, University of Crdoba, Campus de Excelencia International Agroalimentario ceiA3, Edicio Darwin, Anexo, 14010, Crdoba, Spain

a b s t r a c ta r t i c l e i n f o

Article history:Received 26 September 2011Accepted 10 November 2011

Keywords:SalmonellaCross-contaminationRecontaminationFood safetyModeling

The presence of Salmonella in foodstuffs represents an internationally accepted human health concern. AlthoughSalmonella causesmany foodborne disease outbreaks, there is little evidence to support cross-contamination as amajor contributing factor. However, the paramount importance of preventing cross-contamination and reconta-mination in assuring the safety of foodstuffs is well known. Sources and factors linked to cross-contaminationand recontamination of Salmonella in foods are reviewed in detail. Those foods which are not submitted to lethaltreatment at the end of processing orwhich do not receive further treatment in the home deserves special atten-tion. Salmonella cross-contamination and recontamination episodes have been connected to the following fac-tors: poor sanitation practices, poor equipment design, and decient control of ingredients. We also examinepotential cross-contamination in the home. Cross-contamination and recontamination events at factory level ev-idence the difculty encountered for eradicating this pathogen from the environment and facilities, highlighting

try preventive control measures such as appropriate and standardized sanitation.lic Health Authorities should install hygiene education programs in order to raiseReview

j ourna l homepage: www.foodborne disease thatthreat to human publicuntries (European Foods of Salmonella infection

34 957212000.

rights reserved.International

ev ie r .com/ locate / foodres& Nayak, 2008). Salmonella serovars are widespread in nature and canbe found in the intestinal tract of all animals species, both domesticandwild (Allerberger et al., 2002)which result in a variety of Salmonellainfection sources.

Currently, Salmonella spp. remains a serious foodborne illness riskworldwide according to data (European Food Safety Authority (EFSA),2010; FAO/WHO, 2002). Salmonellosis accounted for 131,468 conrmed

546 E. Carrasco et al. / Food Research International 45 (2012) 545556human cases in the European Union (EU) in 2008, representing the sec-ondmost often reported zoonotic disease in humans following campylo-bacteriosis. Human salmonellosis cases reported in 2008 show a 13.5%decrease from 2007 in the EU. However, several European countriesstill show a signicant increasing trend, proving that continuous effortsfor prevention and control are still necessary.

In the EU, serotypes Salmonella Enteritidis and Salmonella Typhimur-ium are reported as the twomajor etiologic agents of salmonellosis thathave adapted to humans. In the US, Salmonella Enteritidis and Typhi-murium represent the two most frequently reported serotypes accord-ing to Centers for Disease Control and Prevention (Centers for DiseaseControl, 2006). The distribution of Salmonella serotypes in Australia var-ies geographically. Thus, while S. Typhimuriumwas themost commonlyreported serovar in 2008, S. Enteritidis was frequently reported as causeof human disease, despite it is not endemic in Australia (Yates, 2011).While S. Enteritidis is mostly implicated in the consumption of poultryand eggs, S. Typhimurium is linked to a range of food-producing animalssuch as poultry, swine, cattle and sheep. S. Enteritidis was a rare serovaruntil the mid-late 1980s when it emerged as a frequent cause of salmo-nellosis in European countries and across the globe (Cogan&Humphrey,2003; Poppe, 1999). By the 1990s, S. Enteritidis replaced S. Typhimuriumas the most common serotype of salmonellosis isolated from humans inmany countries (Angulo & Swerdlow, 1999; Cogan & Humphrey, 2003;Tschape et al., 1999). Australia and New Zealand, however, experienceda relatively higher number of outbreaks due to S. Typhimurium com-pared to Canada, the US and theEU (Dalton et al., 2004). Previous salmo-nellosis outbreaks in Canada and theUS have been linked to S. Enteritidis(Centers for Disease Control, 2004). The global distribution of food andthe continuous movement of people around the world facilitate thespread of this agent, allowing the introduction of emerging Salmonellaserotypes into importing countries.

In general, salmonellosis is transmitted when Salmonella cells areintroduced in food preparation areas. Several factors such as multipli-cation in food due to inadequate storage temperature, insufcientcooking or cross-contamination are often implicated in salmonellosisoutbreaks (Ryan, Wall, & Gilbert, 1996; Todd, 1997). The main trans-mission routes of this pathogen are foods of animal origin contami-nated with fecal matter (Haeghebaert et al., 2003; Swartz, 2002).However, consumption of meat from infected animals may also occa-sionally be a source (Benenson, 1995; Tauxe, 1991).

Some investigations highlight the frequent occurrence of Salmonella inmeats and meat products (Mead et al., 1999) Overall, meat, poultry andeggs are acknowledged as constant vehicles of Salmonella serovars andgenerally involved in the infectious disease (Capita, Alvarez-Astorga,Alonso-Calleja, Moreno, & Garca-Fernndez, 2003; Wilson, 2002).However, a wide range of other foodstuffs such as milk, dairy products,fruits, vegetables, and shery products can be sources of Salmonellainfection (Todd, 1997). The incidence of Salmonella has been studied inpoultry meat in many countries such as the United Kingdom(Plummer & Dodd, 1995), Australia (Fearnley, Raupach, Lagala, &Cameron, 2011), Malaysia (Rusul, Khair, Radu, Cheah, & Yassin, 1996),Greece (Arvanitidou, Tsakris, Soanou, & Katsouyannopoulos, 1998),Spain (Domnguez, Gmez, & Zumalacrregui, 2001) and Italy (Busaniet al., 2005). High prevalence rates have been found in these countriesand the serotypes isolated vary geographically with predomination ofS. Enteritidis, S. Thyphimurium, S. Hadar, S. Newport, S. Virchow andS. Heidelberg. All these studies emphasize the fact that poultry meatrepresents amajor source of this pathogen and therefore, recontamina-tion of cooked poultry should be considered as amajor risk factor. How-ever, the importance and the impact of recontamination events arenot frequently well-documented in reports and scientic literature.This lack of supporting evidence may be explained by several rea-sons, such as incomplete insight in to the causes of foodborne diseases,underreporting cases or lack of outbreak investigation (Reij, DenAantrekker, & ILSI Europe Risk Analysis in Microbiology Task Force,

2004).The objective of this review is to examine the role of cross-contamination and recontamination of foods by Salmonella, the prin-cipal factors involved, and the strategies developed for prevention ofcross-contamination and recontamination.

2. Importance of cross-contamination and recontaminationevents

In accordance to Prez-Rodrguez, Valero, Carrasco, Garca-Gimeno,and Zurera (2008), who reviewed bacterial transfer modeling infoods, dened cross-contamination as a general term which refers tothe transfer, direct or indirect, of bacteria or virus from a contaminatedproduct to a non-contaminated product. Similarly, other terms havebeen used to describe bacterial transfer, but not in a general sense,such as recontamination, which is dened as contamination of foodafter it has been submitted to an inactivation process.

According to the World Health Organization (WHO) (1992), 25% offoodborne outbreaks are closely associated with cross-contaminationevents involving decient hygiene practices, contaminated equipment,contamination via food handlers, processing, or inadequate storage.Identifying sources of infection frequently proves complicated as accu-rate data is often difcult to obtain from governments, industries, andalso incomplete investigations.

Salmonellosis outbreaks linked to cross-contamination processeshave highlighted the importance of these events to identify high-riskfoods and practices. Given the high percentage of foodborne outbreakslinked to cross-contamination events, future investigations will suggestpossible cross-contamination routes when a Salmonella outbreak oc-curs. Cross-contamination and recontamination information on out-breaks in scientic literature is scant. Review papers on outbreaksremain frequently unpublished as they do not completely fulll prereq-uisites such as high number of patients affected, emerging pathogen,unusual serotypes or new food matrices. Outbreaks source attributioncannot be regularly conrmed by food sample investigation due tolack of leftover food matter.

When Salmonella survival is allowed under cross-contaminationand recontamination conditions, several factors such as inadequatetemperatures during food preparation as well as survival throughundercooking or food handling scenarios become critical.

The potential risk of Salmonella spp. to contaminate sites and sur-faces in the household has been studied (Gorman, Bloomeld, &Adley, 2002). These authors emphasize how the preparation of rawfood such as fresh chickenmaymagnify the dissemination of Salmonellato hands and food contact surfaces. A signicant proportion of cross-contamination scenarios occur in domestic kitchens. In fact, in theNeth-erlands, Germany, and Spain,more than 50% of reported foodborne out-breaks were observed in the home (Beumer, Bloomeld, Exner, Fara, &Scott, 1998; Scott, 1996). Several authors have demonstrated that Sal-monella cells from frozen broiler chicken were able to contaminatefood preparation areas (De Wit, Brockhuizen, & Kampelmacher, 1979;Roberts, 1972; Van Schothorst, Huisman, & Van Os, 1978). Similarly,De Boer and Hahne (1990) showed the ease with which salmonellascan be transferred from chicken to utensils, a variety of kitchen surfaces,hands and other foods; from those, Salmonella cells were recoveredfrom surfaces up to 6 h after contamination. Bradford, Humphrey, andLappin-Scott (1997) examined the ability of S. Enteritidis, under sterileand non-sterile conditions, to be cross-contaminated from inoculatedeggs droplets tomelon and beef and grow on these products at ambienttemperature. Consumer awareness of the need to implement Good Hy-giene Practices (GHP) is of paramount importance in order to preventthe spread of Salmonella cells in food preparation areas.

Researchers are increasingly studying the ability of Salmonella to col-onize different inert food contact surfaces to form biolm (Bonafonteet al., 2000; Hood & Zottola, 1997; Joseph, Otta, & Karunasagar, 2001)and its potential to act as a continuous source of bacterial contamination,

which may cause post-processing contamination. These investigations

also reported that Salmonella is able to survive air drying in food for at

547E. Carrasco et al. / Food Research International 45 (2012) 545556give insight in to themechanisms underlying biolm formation, suggest-ing different strategies for prevention.

3. Cross-contamination and recontamination routes and sources

Cross-contamination and recontamination events linked to Salmonelladuring food processing are reported in literature. Below is a review ofsources and routes of potential cross-contamination and recontaminationepisodes by Salmonella spp. linked to different food categories.

3.1. Poultry meat

The association between poultry and Salmonella genus has longsince been recognized. It was not until the 1960s when the poultry in-dustry started to grow thanks to the application of control measuresof pullorum disease and fowl typhoid (Poppe, 2000). Subsequently,an increasing isolation of non-host specic Salmonella from poultryproducts and human cases meant a challenge to identify the originof the strain involved in human cases. Currently consumption of poul-try products remains as a well documented major source of salmonel-losis, being undercooking and cross-contamination appointed asrecognizable risk events (Palmer et al., 2000; Roberts, 1983).

In Canada, Arsenault, Letelier, Quessy, Normand, and Boulianne(2007) observed that the prevalence of Salmonella-positive ocks isaround 50%. When poultry ocks are infected at farms, Salmonella iscarried asymptomatically in the gastrointestinal tract and can bereadily transferred to carcasses through fecal contamination in theabattoir. Further spread of cells may occur easily during processingif carcasses become cross-contaminated. Also, the role of feed ingredi-ents as a source of Salmonella in the poultry industry has receivedgreat attention (Bailey et al., 2001). Feed products may constitute arisk factor for introducing Salmonella since they are made from a widevariety of potentially contaminated ingredients (Crump, Grifn, &Angulo, 2002; Ricke, 2005).

During processing, certain stages including scalding, plucking(defeathering), evisceration, and chilling of carcasses have been recog-nized as likely cross-contamination pathways (Hafez, Stadler, & Kosters,1997; James, Williams, Prucha, Johnston, & Christensen, 1992; Ono &Yamamoto, 1999). The objective of carcass scalding is to soften feathersfor subsequent defeathering. Once carcasses have begun the scaldingprocess, great numbers of microbes from skin, feathers and involuntarydefecations, are released to the scald water. Although survival of thesebacteria depends on temperature, even high temperatures used inhard scalding (5863 C) may have a slight effect on organisms at-tached to skin. Slavik, Kim, andWalker (1995) observed that Salmonellawas not signicantly reduced after hard scalding. The mechanismsthat might result in cross-contamination during defeathering includeaerosols (Allen, Tinker, Hinton, & Wather, 2003b; Allen et al., 2003a),direct contact between contaminated and uncontaminated carcasses(Mulder, Dorresteijn, & Van Der Broek, 1978), and the ngers of thepicker machine (Allen, Hinton, et al., 2003a; Allen, Tinker, Hinton, &Wather, 2003b; Berrang, Buhr, Cason, & Dickens, 2001; Campbell etal., 1984; Clouser, Doores, Mast, & Knabel, 1995a; Clouser, Knabel,Mast, & Doores, 1995b). In this line, Nde, McEvoy, Sherwood, andLogue (2007) appointed the ngers of the picker machine as well asscald water as sources of cross-contamination during defeathering. Abetter understanding of cross-contamination mechanisms duringprocessing has been studied by authors through the use of moleculartyping (Bailey, Cox, Craven, & Cosby, 2002; Crespo, Jeffrey, Chin,Senties-Cue, & Shivaprasad, 2004; De Cesare, Manfreda, Dambauh,Guerzoni, & Franchini, 2001; Liebana et al., 2002).

In carcass evisceration, a series of automated machines are involved.This stage can contribute considerably to an increase in Salmonella prev-alence (Sarlin et al., 1998). During evisceration, carcasses are sprayedwithwater in order to remove organic remains and reducemicrobial con-

tamination by about 1 log unit. However, the removal of microorganismsleast 24 h and therefore, when cells are released from perishablefoods on cutting boards, they may be viable for long periods of time.Jimnez, Tiburzi, Salsi, Moguilevsky, and Pirovani (2008) studied refrig-eration conditions affecting the survival of Salmonella Hadar inoculatedon chicken skin and investigated the potential of transfer to a plasticcutting board. They dened two scenarioswhere carcasseswere treatedor untreatedwith a decontamination agent to assess the effectiveness ofthe decontamination process in regards to the reduction of S. Hadar atthree temperature levels (2 C, 6 C and 8 C) and the likelihood ofcross-contamination. They found that Salmonella was able to detachfrom chicken skin and be transferred to cutting board more readilywhen chicken was treated with acid. Similarly, Nissen, Maugesten,and Lea (2001) observed that growth of S. Enteritidis on untreatedchicken breasts was not signicantly different from the growth ondecontaminated chicken, except after 3 days when a considerablyhigher growth was found on untreated samples. The attachment abilityof Salmonella has also been associated with the moisture content ofmeat; when carcasses are still fresh and the moisture of the skin ishigh, the transference from carcasses to other surfaces is moremarked (De Boer & Hahne, 1990; Dickson, 1990; Jimnez et al., 2008;Kusumaningrum, Riboldi, Hazeleger, & Beumer, 2003).

3.2. Other meats

Poultry, pork, and beef have been identied as common sourcesfor salmonellosis (Bacon, Sofos, Belk, Hyatt, & Smith, 2002;Botteldoorn, Heyndrickx, Rijpens, Grijspeerdt, & Herman, 2003). InDenmark and Germany, the estimation of salmonellosis associatedwith consumption of pork has been linked to 1520% of humancases (Berends, Van Knapen, Mossel, Burt, & Snijders, 1998; Borch,Nesbakken, & Christensen, 1996).

At pre-harvest, contaminated feed, water, vectors and other environ-mental sources linked to swineproductionhavebeen suggested as poten-tial sources of Salmonella (Bailey, 1993; Nayak, Kenney, Keswani, & Ritz,2003). Pigs can be infected during transport or waiting period in lairagebefore slaughtering. It has been suggested that lairage and the slaughter-house environment are probably the major source for Salmonella infec-tions prior to slaughter (Hurd, McKean, Wesley, & Karriker, 2001;Swanenburg, Urlings, Keuzenkamp, & Snijders, 2001). Once Salmonellacolonizes the gastrointestinal tract of pigs, carcasses can become con-taminated at slaughter, and consequently contaminated raw or under-cooked red meats will act as transmission routes for salmonellosis.from carcasses in the spray process can be insufcient if bacteria arermly attached to the tissues (Lillard, 1993).

Chilling of poultry carcasses to 4 C is supposed to guaranteethat no Salmonella present will be able to multiply. This step includesimmersion in cold water or exposure to cold air either by passingcarcasses through an air blast system or holding them in a chillingroom. As chill water used for immersion of carcasses is usuallyreplaced, the accumulation of bacteria should be minimal. However,since large numbers of carcasses are packed together in water baths,the chances for cross-contamination are increased. In fact, waterchilling is considered a major factor in ock-to-ock transmission ofSalmonella (James et al., 1992; Lillard, 1990; Sarlin et al., 1998).Cross-contamination may still be possible via air currents and waterdroplets if carcasses are sprayed during chilling stage (Mead, Allen,Burton, & Corry, 2000).

According to Bloomeld and Scott (1997), cross-contamination risksassociated with different locations and surfaces depend not only on theoccurrence of likely harmful pathogens, but also on the probability oftransfer from those sites. As described by Jackson, Blair, McDowell,Kennedy, and Bolton (2007), food pathogens might survive on refriger-ated surfaces and pose a cross-contamination risk. Mattick et al. (2003)According to Borch et al. (1996), the main contamination sources of

548 E. Carrasco et al. / Food Research International 45 (2012) 545556pig carcasses are feces, pharynx and stomach, and environmental sourcessuch as contact surfaces and handling.

During slaughter, not only carcasses of infected pigs, but cross-contamination from the environment and other infected animals mayoccur. Botteldoorn et al. (2003) studied the prevalence of Salmonellain swine at the moment of slaughter and observed that the slaughter-house environment was highly contaminated. These authors estimatedthat cross-contamination accounted for 29% of the positive carcasses.These results agree with other studies (Berends, Van Knapen, Snijders,& Mossel, 1997; Borch et al., 1996) that observed that cross-contamination accounted for 30% of the entire pork carcass contamina-tion in slaughterhouses. Continuous environmental infection sourcesmay maintain Salmonella in slaughterhouses indicating inefcient orpoor hygiene practices (Botteldoorn et al., 2003). In regard to risk fac-tors at slaughter associated with the presence of Salmonella on hog car-casses, Letellier et al. (2009) underlined the importance of thepreslaughter and pre-evisceration environment on the nal contamina-tion status of carcasses. They observed that cleanliness of the hogs andstatus of scald water were signicant factors associatedwith Salmonellastatus of the carcasses at the end of the slaughtering process. Geneticcharacterization and serology used in this study highlighted that partic-ular attention should be paid to herd contamination levels of incominganimals and the pre-evisceration environment.

Once slaughtered, the next steps aremanufacturing and preparationand storage at retail. At these levels, three major factors such ashandling, time and temperature may signicantly inuence the micro-biological quality of pork meat (Lo Fo Wong et al., 2003). Special caremust be considered in order to avoid cross-contamination betweenproducts, as large quantities of rawmeat of different originmay be han-dled closely together.

Besides swine, cattle are also known reservoirs of Salmonella; groundbeef has been implicated in salmonellosis outbreaks (Centers for DiseaseControl, 2006). Despite Salmonella in ground beef has decreased with theimplementation of the HACCP system (Eblen, Barlo, & Naugle, 2006), therisk of transmitting this pathogen through the food chain cannot bedisregarded, especially in raw, smoked or lightly cooked meat products.Several investigations have studied the overall occurrence of Salmonella inbeef samples, showing prevalence rates of 1.1% (Little, Richardson, Owen,De Pinna, & Threlfall, 2008b), 4.2% (Bosilevac, Guerini, Kalchayanand, &Koohmaraie, 2009) and 6.0% (Gallegos-Robles et al., 2009). In the US, theFood Safety Inspection Service has suggested that the current prevalenceof ground beef is 2.4%. Since standard culturing techniques (which are themost popular) may have a lower level of sensitivity than others methodssuch as immunomagnetic separation (Barkocy-Gallagher et al., 2003), theprevalence of this pathogen in ground beef may be underestimated.

Additionally, cross-contamination in the kitchen can contributesignicantly to salmonellosis incidence. Iordache and Tofan (2008)demonstrated the ease with which two strains of Salmonella Enteriti-dis were able to cross-contaminate beef surfaces from inoculated eggdroplets.

The role of cross-contamination in RTEmeats should also be regarded.On a global scale, RTE meat products may act as vehicles for foodbornepathogens. Some RTE meat products such as biltong (traditional SouthAfrican dried and spiced meat made from beef, wild game, or chicken)or jerky (American dried meat product from domestic andwild animals)have been involved in salmonellosis outbreaks (Bokkenheuser, 1963;Centers forDisease Control, 1995;Neser, Louw, Klein, & Sacks, 1957). Pre-vious studies conducted on other RTE products revealed that factors suchas food handlers, aprons, utensils, and work surfaces are potential sitesfor bacterial contamination (Christison, Lindsay, & von Holy, 2007,2008; Lues & Van Tonder, 2007). Naidoo and Lindsay (2010) evaluatedhygiene of surfaces that come into direct contact with an RTE driedmeat product, biltong, and highlighted the importance of such surfacesas potential sites contributing to cross-contamination of the nal productat the point of sale. With the aid of molecular DNA sequencing methods

the study demonstrated that bacterial strains isolated from biltong and,correspondingly, from cutting utensils were 100% genetically identical.Several studies have linked cutting utensils as sources of contaminationof RTE products (Lunden, Autio, & Korkeala, 2002; Pal, Labuza, & Diez-Gonzalez, 2008). Cutting during RTEmeat slicing have a signicant inu-ence in cross-contamination scenarios since blades are capable of dissem-inating high numbers of microbial populations with every slice whichmay include foodborne pathogens such as Staphylococcus aureus, Escher-ichia coli or Salmonella (Fernane, Morales, Carrasco, & Garca-Gimeno,2010; Prez-Rodrguez et al., 2007).

In the production of meat andmeat products, numerous attempts tomitigate the risk of salmonellosis have been made. At the farm, AIAO(all-inall-out) system has been proposed to reduce the risk of cross-contamination between groups of animals; AIAO swine productionsconsist of keeping animals together in groups where pigs fromdifferentgroups are not mixed during their stay on the farm. Lo Fo Wong et al.(2003) has reported the importance of controlling feed (e.g. acidica-tion of feed) to reduce or remove Salmonella from a herd. During trans-portation to the abattoir, animals are subjected to stress factors such asovercrowding, long duration of transport, unfamiliar pigs, noises,etc., which may result in an increase of number of animals excretingSalmonella until arrival at the slaughterhouse (Berends et al., 1997).To reduce the spread of infection during transport, it has been pro-posed not to mix unfamiliar animals and handle them as quietlyand gently as possible (Warriss, Brown, Edwards, Anil, & Fordham,1992). Also, trucks should be thoroughly cleaned and disinfected be-tween transports (Rajkowski, Eblen, & Laubach, 1998). In the slaugh-terhouse, Olsen, Brown, Madsen, and Bisgaard (2003) emphasizedthe importance of the segregation of clean and dirty processes to re-duce the likelihood of cross-contamination and the need to improve thehygiene of the equipment used. During processing, Cason and Hinton(2006) concluded that multistage scalding reduced the likelihood forcross-contamination of Salmonella, when compared with a single-tanksystem. Also, scalding temperature should be set, at least, at 62 C(Hald, Wingstrand, Swanenburg, von Altrock, & Thorberg, 2003). Waterchilling of carcasses is considered a major factor in ock-to-ock trans-mission of Salmonella (Lillard, 1990); a total residual chlorine of 45 to50 mg/l to keepwater free from viable vegetative bacteria has been sug-gested (Lillard, 1989).

3.3. Eggs and egg products

Salmonella Enteritidis is primarily linked to consumption of poul-try, eggs, and egg-derived products (Hayes, Nylen, Smith, Salmon, &Palmer, 1999; Schmid, Burnens, Baumgartner, & Oberreich, 1996).According to Gast and Beard (1992), fresh laid eggs naturally maycontain no more than a few hundred Salmonella cells. Prompt refrig-eration procedures can prevent the growth of these small populationsduring storage (Gast, Guraya, Guard, & Holt, 2010). This study dem-onstrates that once Salmonella Enteritidis is introduced into the albu-men, it can reach the yolk and multiply during unrefrigerated storage.Eggs infected with Salmonella represent a serious threat to con-sumers. Further investigation of handling of contaminated eggs isnecessary to understand their role in kitchens, even if they are notpurposed for raw consumption. For instance, kitchen surfaces andutensils may become contaminated by raw infected eggs and serveas an infection medium to other foodstuffs. In fact, research data hasshown that cross-contamination events linked to eggs have resultedin outbreaks. Slinko et al. (2009) described an outbreak (SalmonellaTyphimuriumphage type 197) in a series of restaurants across Brisbane,Australia, in a two-month period. Investigation of these restaurantsidentied a lack of food hygiene and potential cross-contamination is-sues. The outbreakwas traced back to cracked and dirty eggs. In Austra-lia, Food Safety Standards (Food Standards Code) were developed toprovide more effective and nationally uniform food safety legislation.Despite national code prohibit the sale of cracked and dirty eggs for re-

tail or catering, the Food Standards Code did not appear to have

Salmonella because of the nature of cultivation and/or harvesting pro-cesses. A great number of nut and seed products have been recalled due

549E. Carrasco et al. / Food Research International 45 (2012) 545556to Salmonella contamination (Podolak et al., 2010). Cross-contaminationand recontamination due to poor sanitary design andmachinerymainte-nance in peanut products may contribute to Salmonella contamination.Also, if ingredients are not adequately handled and/or stored and becomecontaminatedwith Salmonella, they potentially act as a source of contam-ination for processed nished products. During a salmonellosis outbreakinvestigation in US, the FDA declared that raw peanut storage was unsui-table (U.S. Food & Drug Administration, 2009a) and cross-contaminationopportunities were plausible. In 2007, investigations of an outbreak ofsalmonellosis linked to peanut butter, the roof of the factory leaked andproperly protected public health as it allowed the sale of contaminated,cracked, and dirty eggs to restaurants where foods and surfaces werecross-contaminated through food handling. Likewise, a survey con-ducted after an unusual number of Salmonella Enteritidis outbreaks as-sociated with the use of eggs in food service in England and Wales(Little et al., 2008) revealed evidence of inadequate eggs storage andhandling practices. The food service sector should be aware of salmo-nellosis hazards and receive proper training on hygiene practices suchas the usage of raw shell eggs, in order to avoid cross-contamination ep-isodes and reduce the risk of salmonellosis.

3.4. Low-moisture foods

Salmonella spp. is expected to be present in any raw food productsince this pathogen is widely disseminated in nature (e.g., water, soil,plants, and animals). Salmonella spp. is able to survive for weeks inwater and for years in soil if environmental conditions such as tem-perature, humidity, and pH are favorable (Todar, 2008). Low wateractivity (aw) represents a barrier to growth for many vegetative path-ogens, including Salmonella spp. (Betts, 2007). Processed foods suchas powdered milk, chocolate, peanut butter, infant food, and bakeryproducts are characteristically low-aw food products. Epidemiologicaland environmental data investigations have indicated that cross-contamination plays a major role in the contamination of these prod-ucts (Smith, Daifas, El-Khry, Koukoutsis, & El-Khry, 2004). Salmonellaspp. has the capacity to survive in dry foods and feeds for long periodsof time (Hiramatsu, Matsumoto, Sakae, &Miyazaki, 2005; Janning, in'tVeld, Notermans, & Kramer, 1994; Juven et al., 1984). Furthermore, ithas been reported that the combination of low aw and high fat con-tent of foods might have a synergistic effect on Salmonella survival(Shachar & Yaron, 2006). Podolak, Enache, Stone, Black, and Elliott(2010) reviewed several sources and risk factors for contamination,survival, persistence, and heat resistance by Salmonella in low-moisture products. Poor sanitation practices, substandard facilities,equipment design, and improper maintenance remain the maincauses of Salmonella contamination in low-moisture foods. Low-moisture products contaminated by Salmonella where recontamina-tion and cross-contamination events have been mostly reported arepresented.

Chocolate presents a very low moisture content (b8%) and high fatlevels. Several potential sources of Salmonella like raw cocoa beans orpowderedmilkmay carry Salmonella cells. Although Salmonella is not ca-pable of growing innished chocolate, it is able to survive for long periodsof time, representing a signicant risk even at low levels in the product.Cross-contamination and recontamination events involving chocolatehave been reported. Craven, Mackel, Baine, Barker, and Gangarosa(1975) reported an international outbreak by Salmonella Eastbournelinked to contaminated chocolatewhere cross-contamination by airbornedust was a plausible cause. In 2006, a Salmonella Montevideo outbreaklinked to chocolate products was attributed to a leaking episode (FoodStandards Agency, 2006).

Nut and seed products may be naturally contaminated withthe sprinkler system broke down (Funk, 2007).Spray drying is a method of producing a dry powder from a liquidby rapidly drying by hot gas. Spray drying food applications includemilk powder, coffee, tea, eggs, cereal, avorings, etc. The mostimportant factors that inuence the survival of Salmonella in spray-dried products are temperature during processing, particle density, fatcontent and strain variation (Miller, Goepfert, & Amundson, 1972).While spray drying foods, the equipment may inuence Salmonellacontamination as Rowe et al. (1987) indicated in a Salmonella Ealingoutbreak.

Salmonella contamination of oilmeal has been a matter of concernfor many years (Sato, 2003). The eradication of Salmonella in oilmealplants is a difcult task since a high probability of spreading contam-ination from manufacturing to storage areas has been observed andhence, cross-contamination is plausible (Morita, Kitazawa, Iida, &Kamata, 2006).

Control of Salmonella in low-moisture foods presents several chal-lenges to manufacturers. The Grocery Manufacturers Association (2008)published a guidance document, establishing seven control elementsagainst Salmonella contamination: 1) prevent entrance and spread ofSalmonella in processing facilities; 2) increase the stringency of hygienepractices and controls in the Primary Salmonella Control Area; 3) appli-cation of hygienic principles to building an equipment design; 4) pre-vent or reduce growth of Salmonella in the facility; 5) establish a rawmaterials/ingredients control program; 6) validate control measuresto inactivate Salmonella; and 7) establish procedures for verication ofSalmonella controls and corrective actions.

3.5. Fresh produce and spices

Vegetables, including cilantro, broccoli, cauliower, lettuce, and spin-ach, have also been reported as vehicles of Salmonella (Quiroz-Santiagoet al., 2009). Fresh tomatoes have been commonly linked to salmonello-sis outbreaks in the US (U.S. Food & Drug Administration, 2009b). Ranaet al. (2010) examined Salmonella cross-contamination during posthar-vest washing of tomatoes and observed that Salmonella could spreadfrom contaminated to uninoculated tomatoes during washing proce-dures. Fresh herbs and spices are classied into the RTE category(Regulation EC No. 2073/2005). Spices such as clove, oregano, blackpepper, and paprika among others, may be exposed to great microbi-al contamination during harvesting and processing and they are soldwithout any treatment to reduce contamination. Data from literatureshows that Salmonella has been isolated in spices (Moreira,Lourencao, Pinto, & Rall, 2009; Pafumi, 1986). Despite the industryhaving more and more sophisticated control mechanisms available,well-designed equipment systems are not able to combat cross-contamination from poor sourcing, choice, and control of raw mate-rials and ingredients.

Fresh produce may be contaminated during production, harvest,processing, at retail levels or in the kitchen at home. Washing proce-dure is one of the most studied measures to reduce the level of con-tamination. Pao, Kelsey, and Long (2009) examined the efcacy ofchlorine dioxide during spray washing of tomatoes for preventingSalmonella enterica transfer from inoculated roller brushes to fruitand wash runoff, reporting an important reduction of the pathogen(5.00.3 log). Rana et al. (2010) designed a washing system oftomatoes to simulate a commercial postharvest washing, showingthat the use of higher temperatures (37 C) during washing lead tolower Salmonella uptakes than those observed at 20 C.

3.6. Milk, dairy and milk products

Several foodborne pathogens have usually been detected in rawmilk, including Salmonella spp., Campylobacter spp., E. coli, Listeriamonocytogenes, and S. aureus (Oliver, Jayarao, & Almeida, 2005). Fecalcontamination duringmilking constitutes a primary route for pathogen

transmission. The consumption of raw milk represents a well-

550 E. Carrasco et al. / Food Research International 45 (2012) 545556documented issue for human health (Headrick et al., 1998; LeJeune &Rajala-Schultz, 2009). However, increasing number of consumers de-mand rawmilk and/or products made from rawmilk and other unpro-cessed products. According to epidemiological data, it is necessary toconsider not only the risk of raw milk consumption, but also the likelyepisodes of recontamination and cross-contamination that can takeplace at the industry or home kitchens if milk is not pasteurized orheat-treated. However, pasteurized milk has also been involved in sal-monellosis infections and outbreaks, as reported by Olsen et al.(2004). According to these authors, pasteurization was adequate.Nevertheless, microbial testing demonstrated that coliform countswere higher (>100 cfu/mL) than those recommended by PasteurizedMilk Ordinance (10 cfu/mL). Cross-contamination episodes were notidentied though they should not be ruled out.

Cheese has been characterized as one of the safest food products bysome experts (Johnson, Nelson, & Johnson, 1990); however, sincecheese is considered an RTE food product and does not undergo any fur-ther treatment before consumption, contamination episodes should beconsidered. Contaminated raw milk as well as cross-contaminationwith pathogens such as Salmonella, can be introduced into dairy proces-sing plants and represents a human health risk if unpasteurized milk isused for cheese production (Kousta, Mataragas, Skandamis, & Drosinos,2010). Cross-contamination of cheese may be originated from starterculture, brine, oor, packaging material, cheese vat, cheese cloth, curdcutting knife, cold room, and production room air (Temelli, Anar, Sen,& Akyuva, 2006). Domnguez et al. (2009) reported a Salmonella out-break caused by raw-milk cheese containing low contamination levelswhich had not been detected. Despite there are not reported outbreakswhere cheeses cross-contamination is linked to salmonellosis outbreaks,these data suggests that contamination and cross-contamination ofcheese may occur, and if ignored or underestimated, the risk of salmo-nellosis could increase.

3.7. Seafood

Seafood is responsible for a signicant amount of foodborne dis-eases and represents a great concern from a public health perspective.Salmonella is not a component of the normal ora of sea animals, thuscontamination of seafood is a result of fecal contamination throughpolluted water, infected food handlers or cross-contamination duringproduction or transport (Lunestad & Borlaug, 2009). High prevalenceis frequently attributed to poor hygienic practices during handlingand transportation from landing centers to sh markets. Shrimp isone of the most reported seafoods associated with salmonellosis(Wan Norhana et al., 2010). Certain aspects of cooked shrimp produc-tion like cooking procedures aboard shing vessels, chilling with sea-water, and intensive handling and transportation make themsusceptible to be contaminated.

Data gathered from studies involving Salmonella contamination inprawns (Hatha, Maqbool, & Kumar, 2003; Heinitz, Ruble, Wagner, &Tatini, 2000; Reilly & Twiddy, 1992) have suggested the likelihood ofcross-contamination between raw and cooked products. Wan Norhana,Poole, Deeth, and Dykes (2010) reported various physical controlmeasures, including cooking, refrigeration, irradiation, modied atmo-sphere packaging (MAP), high-pressure processing (HPP) and high-pressure carbon dioxide.

4. Cross-contamination in food-handling scenarios and retail points

Salmonella can remain viable on food contact surfaces for signicantperiods, increasing the risk of cross-contamination events between foodhandlers, food products, and food contact surfaces (De Cesare, Sheldon,Smith, & Jaykus, 2003; Humphrey,Martin, &Whitehead, 1994). The roleof food workers in foodborne outbreaks have been clearly demonstrat-ed by several authors (Todd, Greig, Bartleson, & Michaels, 2009). Thus,

the transmission and survival of enteric pathogens such as Salmonellain the food processing and preparation environment through humansrepresent an important risk. Among the different causes of foodborneoutbreaks, consumermishandling of food in household plays an impor-tant role. Anderson, Shuster, Hansen, Levy, and Volk (2004) indicatedthat 25% of reported outbreaks are caused by inadequate consumerhandling and food preparation at home. In fact, epidemiological studieshave revealed that a signicant number of consumers followunsafe andrisky practices duringmeal preparation (Redmond&Grifth, 2003) anddo not implement proper hygienic measures to prevent cross-contamination events (Fischer et al., 2007; Jay, Comar, & Govenlock,1999). In a survey performed by Klontz, Timbo, Fein, and Levy (1995)about hygiene practices, 25% of respondents were reported to reutilizecutting boards without cleaning after cutting raw meat or chicken.Therefore, it is reasonable to expect a reduction of salmonellosis andother foodborne diseases if consumers would apply safe food-handling practices. Cross-contamination and transfer rates of Salmonel-la enterica from chicken to lettuce were assessed by Ravishankar, Zhu,and Jaroni (2010) under different food-handling scenarios, with andwithout washing procedures. The study showed that washing usingonly water is not enough to remove S. enterica while washing proce-dures including soap, hot water, and vigorous mechanical scrubbingare suitable to reduce cross-contamination.

Retail point scenarios must be addressed since a wide variety ofspecialist foods such as RTE products are frequently sold in delicates-sen and fast food restaurants, where stainless steel blade retail slicersare commonly used in meal preparations. Most likely underreportedat retail levels, cross-contamination scenarios involving equipmentand utensils such as boards, knives, and slicers are likely to occurwhen good hygiene practices are not applied by personnel. Slicingof foodstuffs such as RTE meat products can enhance the risk ofcross-contamination by contact with contaminated surfaces. Indeednot only slicing, but also cutting operations, handling or packagingcontributes to increase the risk of cross-contamination. Investigationsduring a salmonellosis outbreak in 1963 conrmed that the vehicle ofinfection was a tin of corned beef (Ash, McKendrick, Robertson, &Hughes, 1964). The tin was originally contaminated during processing,but it also contaminated slicing machine and spread the contaminationto other RTEmeats. The potential risk of transfer of Salmonella in slicingscenarios has not been well assessed thus far. However, the study ofthese scenarios would provide empirical data to develop guides tar-geted at retailers and industry on proper slicing practices and cleaningand disinfection procedures to prevent transfer and survival ofSalmonella.

The role of shopping bags in cross-contamination events has alsobeen discussed. If not adequately washed between uses, reusablebags create the potential for cross-contamination of foods. Forinstance, when raw meat products and nished foods are carried inthe same bag, either together or between uses, the opportunities forcross-contamination increase. Gerba, Williams, and Sinclair (2010)studied the potential for cross-contamination of various food prod-ucts by reusable shopping bags and observed that great numbers ofbacteria were found in almost all bags and coliform bacteria in half.The study suggested that raw meats or other uncooked food productscontaminated bags. E. coliwas detected in 12% of bags, demonstratingthat reusable bags can be contaminated by enteric microorganismsand they constitute a potential hazard, especially if growth were tobe proven in plastic bags. Although Salmonella and other pathogenssuch as Listeria spp. were not isolated from bags, the risk of ndingthese organisms in reusable shopping bags should not be ignored. Infact, some studies have demonstrated that children have an increasedrisk of salmonellosis if they ride in a shopping cart carrying meat prod-ucts and eating other foods such as fruits or vegetables previously pre-pared at home (Fulterton et al., 2007; Jones et al., 2006). Handling rawfood products during shopping and transport to the home is a route forthe transmission of these bacteria. Packaged meats might contaminate

the bag since they can leak during transport. Harrison, Grifth,

551E. Carrasco et al. / Food Research International 45 (2012) 545556Tennant, and Peters (2001) declared that chicken and chicken packag-ing is a potential vehicle for the introduction of pathogens in retailand domestic kitchens and, in particular, for the cross-contaminationof Salmonella and Campylobacter. The study highlighted that food indus-try and consumers should be concerned about the potential risk of sal-monellosis and campylobacteriosis from contamination of both theexternal and internal packaging surfaces in addition to the chickenitself. It should also be noted that, once contaminated, bags are fre-quently assigned to purposes others than carrying groceries, and then,the risk of cross-contamination increases. The study also revealed thatconsumers rarely wash reusable bags, and bacteria were able to growwhen stored in the car trunks. This suggests that it is necessary to makerecommendations targeted at consumers in order to reduce the risk ofcross-contamination by using reusable shopping bags.

Kitchen surfaces also represent a signicant risk of cross-contamination and recontamination events (Redmond & Grifth,2003). Domestic food contact surfaces appear to play an importantrole in the transmission of foodborne agents such as Salmonella spp. Re-searchers currently debate which surface materials pose the greatestrisk to consumer health in terms of cross-contamination during foodpreparation. Accordingly, some studies have underlined the essentialparadox of choosing food contact surfaces, i.e. those characteristicsthat make a surface easy to clean may also more likely release food-borne pathogens during common food preparation practices (Moore,Blair, & McDowell, 2007). For instance, cutting boards are commonlyperceived as signicant fomites in cross-contamination of foodstuffswith foodborne agents. Wooden cutting boards and utensils havebeen banned for a long time in production sites of meat and poultryfoods. Still today, opposition is present in respect to the use of wood in-stead of plastic during food processing despite the lack of evidence ofthe presumed better sanitation properties of plastic utensils (Ak,Cliver, & Kaspar, 1994; Carpentier, 1997). In contrast, to date, severalpublications are in favor of wood, demonstrating that plastic is not em-pirically better (Boursillon & Riethmller, 2005; Prechter, Betz, Cerny,Wegener, & Windeisen, 2002;). Nevertheless, it is generally recognizedthat bacteria are able to penetrate the pores of wood where they arethen trapped. While plastic cutting boards can be cleaned in a dish-washer (as well as some specially treated wooden boards), this opera-tion may distribute the pathogen onto other food contact surfaces; incontrast, most small wooden boards can be sterilized in a microwaveoven. Cliver (2006) stated that epidemiological studies seem to showthat cutting board cleaning habits have a slight inuence on the inci-dence of salmonellosis. Therefore, the use of wooden cutting boards isstill controversial. Even though the choice of plasticmight improve safe-ty due to better cleaning properties of plastic cutting boards, they arenot as signicant as often stated.

Klontz et al. (1995) reported that 25% of their respondents reusedcutting boards after cutting rawmeat or chicken without proper clean-ing procedures. Redmond and Grifth (2003) observed that 81% of con-sumers used the same utensils and cutting boards for preparation ofboth raw and RTE products. Deciencies in food preparation hygienesuch as inadequate cleaning of cutting boards after cutting raw meatand poultry likely play a signicant role in contamination by pathogens(De Boer &Hahne, 1990). Cross-contamination and transfer rates of Sal-monella enterica from chicken to lettuce under three different food-handling scenarios were evaluated by Ravishankar et al. (2010). Theirstudy revealed that Salmonella was easily transferred from cuttingboards and knives to lettuce if utensils were not carefully washedwith soap and hotwater after cutting chicken andbefore cutting lettuce.Furthermore, this study showed that merely washing contaminatedkitchens utensils was not enough to remove S. enterica. The transferrate obtained in the scenario 1 of this study was 45%, where cuttingboard and knife were unwashed after cutting the chicken. Similar re-sults were found by Moore, Sheldon, and Jaykus (2003) who foundtransfer rates of 3666% for S. Typhimurium from stainless steel sur-

faces to lettuce. Although signicant amounts of Salmonella cells canbe removed during washing, diminishing transfer rates, it may not beeffective at eliminating the risk of transfer since current infective dose es-timates are as low as 10 cells (Cogan, Slader, Bloomeld, & Humphrey,2002). Kusumaningrum, Van Asselt, Beumer, and Zwietering (2004)studied cross-contamination of various foodborne pathogens includingSalmonella spp. As transfer rates can vary according to the organism,the type of surface and food product, cross-contamination should beassessed on a case-by-case basis.

Therefore, cross-contamination in the home kitchen is particularlyimportant and probably, underestimated. The risk of unsafe food-handling practices and poor hygiene is relatively high, and impossibleto control. Consumer food safety education is a key issue for ensuringfood safety, despite little attention has been paid to this importantlast step of the farm to fork chain. According to FAO/WHO (2002),undercooking and cross-contamination in the homes represent twogeneral pathways for Salmonella spp. contamination.

5. Biolm formation and food contact surfaces

Biolm formation is awell-known bacterialmode of growth and sur-vival which protects bacteria from stressful environmental conditionssuch as drying and cleaning procedures of food surfaces and environ-ment (Reuter, Mallet, Bruce, & van Vliet, 2010). Cross-contaminationlinked to raw and processed foods by food contact surfaces has beenidentied as a potential hazardous event (Barners, Lo, Adams, &Chamberlain, 1999). Salmonella spp. has been recovered from a widerange of food contact surfaces; as commented previously, Salmonella isable to attach to inert surfaces in the food processing environment(Hood & Zottola, 1997; Joseph et al., 2001) and consequently form bio-lms (Stepanovic, Circovik, Ranin, & Svabic-Vlahovic, 2004). Once a bio-lm is formed, it becomes a source of food contamination in processinglines, representing a serious concern for the food industry.

Most of the food processing industry's surfaces such as machin-ery, pipelines, and working surfaces are made of stainless steel. Thismaterial is traditionally selected in the kitchen for food preparationbecause of its mechanical strength, corrosion resistance, and lon-gevity (Holah & Thorpe, 1990). Food particles are frequently re-moved from these surfaces when good hygiene practices areapplied, although microorganisms might not be removed if appro-priate disinfection procedures are not implemented. Some authorshave reported the presence of viable Salmonella spp. on stainlesssteel surfaces (Kusumaningrum et al., 2003) and other materialscommonly found in processing plants such as rubber and polyure-thane (Chia, Goulter, McMeekin, Dykes, & Fegan, 2009). Goughand Dodd (1998) showed that Salmonella survived when RTEcame into contact with raw contaminated vegetables through cut-ting boards and stainless steel utensils. Different factors inuencingthe attachment capacity of Salmonella spp. have been studied.Oliveira, Oliveira, Teixeira, Azeredo, and Oliveira (2007) suggestedthat attachment is strongly strain dependent and the importanceof other factors such as production of polysaccharides should beevaluated. Giaouris and Nychas (2006) demonstrated that increasingthe levels of appropriate nutrients also provides the most optimal envi-ronment for S. Enteritidis PT 4 to adhere, and subsequently, enhancebiolm formation on stainless steel surfaces.

Slicing has been shown to be a risky factor in cross-contaminationevents, especially if RTE products are sliced, as blades are able to dis-seminate high numbers of Salmonella (Fernane et al., 2010). In thissense, improving cleaning and disinfection procedures through handwashing, changing of gloves, and daily sanitation of cutting utensilsand display cabinets is essential (Naidoo & Lindsay, 2010).

6. Modeling Salmonella transfer in foods

Cross-contamination and recontamination models have experi-

enced a great development in the last years. Zhao, Zhao, Doyle,

552 E. Carrasco et al. / Food Research International 45 (2012) 545556Rubino, and Meng (1998) proposed a model of cross-contaminationof Enterobacter aerogenes (with attachment characteristics similar tothose of Salmonella spp.) from raw chicken to cutting board, andfrom cutting board to vegetables, revealing that from 106 cfu/g of E.aerogenes inoculated on the chicken, approximately 105 cfu/cm2

was transferred to the cutting board, and approximately 103104 ofE. aerogenes to the vegetables. However, this experience was notmodeled mathematically. From now on, by model we will meanmathematical model.

Prez-Rodrguez et al. (2008) published the state-of-the-art ofbacterial transfer phenomenon, including a review of the transfermodels developed so far. The most popular models are based ontransfer rates, which involve the application of Eq. (1).

Nr TR=100 Nd 1

where Nr is the quantity of cells transferred to the receptor surface; TRis transfer rate, i.e. the percentage of cells transferred from one sur-face (donor) to another surface (receptor), and Nd is the quantity ofcells contaminating the donor surface.

Often, transfer rates (TRs) show a large variation as a consequenceof the large number of factors involved as well as the errors inherentto microbial collection from surfaces and enumeration techniques. Tocapture the uncertainty and variability of TR data, normal distributionhas been proposed as the most appropriate to describe the log-transformed TR data (Montville, Chen, & Schaffner, 2001; Schaffner,2003).

Usually, the actual contamination level of surfaces is low, and transfernot necessarily occurs. However, articial contamination levels in exper-iments carried out to develop transfermodels is high to obtain countableconcentrations. Hence, transfer experiments are intended tomodel non-zero transfer rates, rather than modeling failed bacterial transfers, i.e. 0%transfer. Schaffner (2004) and Yang et al. (2006) applied cross contami-nation frequency values and TRs to describe microbial prevalence andconcentration changes, respectively. Ariza, Mettler, Daudin, and Sanaa(2006) based their compartmental and dynamic cross contaminationmodel on the binomial process of bacterial transfer. This is, assumingthatmicroorganisms are homogeneously distributed in foods, a binomialdistribution B(n, p) could be applied to describe bacterial transferbetween different compartments, p being the transfer probability of acell and n the number of bacteria in the compartment. The binomialmodel can also explain 0% transfer events (prevalence changes) whenp and/or n become very small.

Moore et al. (2003) approached the cross-contamination phenom-enon from stainless steel to lettuce in a similarway as Zhao et al. (1998),although they calculated the transfer rate of S. Typhimurium andCampylobacter jejuni, showing that S. Typhimuriumwas able to transferduring the rst 60 min of contact with a transfer rate (TR) of up to 66%.TR was calculated as follows:

% transf er CFULETCFULETCFUSST

100% 2

where CFULET is the number of colony forming units found in lettuce andCFUSST is the number of colony forming units found in stainless steelcoupons.

Other authors (Kusumaningrum et al., 2003) have calculated TRdifferently from Moore et al. (2003). As described above by Prez-Rodrguez et al. (2008), solving for TR in Eq. (1) we get:

% transf er rate Nf=Ns 100%

where Nf = CFU recovered from food; Ns = CFU on surfaces recov-ered by contact plate.

These authors calculated the TR for S. enteritidis, S. aureus and C. jejunifrom stainless steel surfaces to food (cucumber and chicken llet slices).

S. enteritidis TR data ranged from 10526% to 5018% in cucumberslices, and from 9442% to 329% in roasted chicken llets, dependingon the time of recovery of cells (just or 15 min after the cross-contamination event) and the application or not of pressure (the levelof pressure appliedwas 500 g per slice, approximately 20 g/cm2, compa-rable to the pressure applied during sampling with contact plates). In alater stage, Kusumaningrum et al. (2004) carried out a quantitative anal-ysis of cross-contamination of Salmonella and Campylobacter spp. via do-mestic kitchen surface, to nally estimate the risk of salmonellosis andcampylobacteriosis per serving of salad. In this analysis, they modeledthe transfer rate of bothmicroorganisms from chicken carcasses to kitch-en surfaces (TR1) and from kitchen surfaces to salad vegetables (TR2). Inthis way, the level of contamination of the pathogen in salad vegetableswas given by Eq. (3).

Cv N TR1=100 TR2=100 3

where Cv is the level of contamination on salads; N is the level of micro-organisms on contaminated chicken carcasses (CFU/cm2 carcass); andTR1 and TR2 are as above.

The authors found that, for Salmonella, the TR1 mean was 1.6%,while the TR2 mean was 34.8%. As their quantitative analysis was sto-chastic, the authors selected normal distributions to describe the log-transformed transfer rates from one surface to another.

Chen, Jackson, Chea, and Schaffner (2001) quantied bacterialcross-contamination rates during common food service tasks; forthis, they used E. aerogenes as surrogate for Salmonella. They calculat-ed TR in an appropriate manner depending on the task evaluated. Forinstance, to evaluate cross-contamination from chicken to hand, theycalculated TR as:

Transf er Rate % CFU on the Hand=CFU on the Chicken 100 4

where CFU=colony forming units.Then, with TR calculated for all replicate experiments of each task,

the authors adjusted probability distributions to TR data, nding othersthan normal distribution as best t in accordance to the KolmogorovSmirnov test. For example, transfer data from chicken to hand, from cut-ting board to lettuce and handwashing (reduction rate) obeyed to Betadistribution; Weibull distribution was more adequate for modelingtransfer from hand to lettuce and from hand to spigot; lastly, Gammadistribution was the best model for describing the transfer from spigotto clean hand.

Mller, Nauta, Christensen, Dalgaad, and Hansen (2011) pre-sented a cross contamination model of Salmonella in pork processingduring a small-scale grinding process. After evaluating three models,the goodness-of-t indices applied (Root Mean sum of Square Errorsand Akaike Information Criterion) as well as two validation factors(bias and accuracy factors) indicated that the best model was that as-suming two environments inside the grinder: in one of them, food ma-trix is relatively loosely attached and is responsible for the fast transferto the minced meat, while in the second matrix the transfer occurs at aslower rate. Fig. 1 is a graphic representation of the model. In this way,after passing ve contaminated pork slices (108 cfu/slice) throughthe grinder, the subsequent non-contaminated slices were contaminat-ed at a descending rate as they were being grinded, presenting a longtail region, similar to the thermal inactivation process.

The developed model satisfactorily predicted the observed behav-ior of Salmonella during its cross-contamination in the grinding of upto 110 pork slices. The proposed model is an important tool to exam-ine the effect of cross-contamination in quantitative microbial risk as-sessment investigations and might also be applied to various otherfood processes where cross-contamination is involved.

More research is needed in relation to cross-contamination model-ing. Identication and measurement of different factors affectingcross-contamination events are crucial. Different tasks and hygiene

practices during food serving operations should be described in detail

3620 from the Andalusia Government, the project AGL 2008-03298/

Allen, V. M., Hinton, M. H., Tinker, D. B., Gibson, C., Mead, G. C., & Wather, C. M. (2003).Microbial cross-contamination by airborne dispersion and contagion during

553E. Carrasco et al. / Food Research International 45 (2012) 545556defeathering of poultry. British Poultry Science, 44, 567576.Allen, V. M., Tinker, D. B., Hinton, M. H., & Wather, C. M. (2003). Dispersal of microor-

ganisms in commercial defeathering systems. British Poultry Science, 44, 5359.Allerberger, F., Liesegang, A., Grif, K., Prager, R., Danzl, J., Hck, F., et al. (2002). Occur-

rence of Salmonella enterica serovar Dublin in Austria. Euro Surveillance, 7, 325.Anderson, J. B., Shuster, T. A., Hansen, K. E., Levy, A. S., & Volk, A. (2004). A camera's

view of consumer food-handling behaviors. Journal of the American Dietetic Associ-ation, 104, 186191.ALI from the Spanish Science and Innovation Ministry, the Europeanproject FP7-KBBE-2007-2A n 222738 from the VII Framework Pro-gramme and ERDF funding. The authors would also like to thank thePlan Andaluz de Investigacin for a Research Staff Training grant.FEDER also provided additional funding.

References

Ak, N. O., Cliver, D. O., & Kaspar, C. W. (1994). Decontamination of plastic and woodencutting boards for kitchen use. Journal Food Protection, 57, 1622.for experimental studies in terms of environmental conditions andphysiological state of Salmonella spp. Variability of transfer rates shouldalso be characterized by probability distributions, as it has been widelyrecognized the great variability encountered during cross-contamination.As more cross-contamination models become available, more accurateexposure assessments and risk characterization will be developed.

Acknowledgments

This work was partly nanced by the Project of Excellence CTS-

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