Cross - Contamination and Recontamination by Salmonella in Foods: A Review

Food Research International 45 (2012) 545556
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Food Research International

journal homepage: www.elsevier.com/locate/foodres
Review
Cross-contamination and recontamination by Salmonella in foods: A review

Elena Carrasco , Andrs Morales-Rueda, Rosa Mara Garca-Gimeno
Department of Food Science and Technology, University of Crdoba, Campus de Excelencia International Agroalimentario ceiA3, Edicio Darwin, Anexo, 14010, Crdoba, Spain
a r t i c l e
i n f o
Article history:
Received 26 September 2011
Accepted 10 November 2011
Keywords:
Salmonella
Cross-contamination
Recontamination
Food safety
Modeling
a b s t r a c t
The presence of Salmonella in foodstuffs represents an internationally accepted human health concern. Although
Salmonella causes many foodborne disease outbreaks, there is little evidence to support cross-contamination as a
major contributing factor. However, the paramount importance of preventing cross-contamination and recontamination in assuring the safety of foodstuffs is well known. Sources and factors linked to cross-contamination
and recontamination of Salmonella in foods are reviewed in detail. Those foods which are not submitted to lethal
treatment at the end of processing or which do not receive further treatment in the home deserves special attention. Salmonella cross-contamination and recontamination episodes have been connected to the following factors: poor sanitation practices, poor equipment design, and decient control of ingredients. We also examine
potential cross-contamination in the home. Cross-contamination and recontamination events at factory level evidence the difculty encountered for eradicating this pathogen from the environment and facilities, highlighting
the need to reinforce industry preventive control measures such as appropriate and standardized sanitation.
Also, at consumer level, Public Health Authorities should install hygiene education programs in order to raise
consumer awareness of the risks of cross-contamination in the home and their role in its prevention. Finally, a
review on cross-contamination models of Salmonella spp. is presented.
2011 Elsevier Ltd. All rights reserved.
Contents
1.
2.
3.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . .
Importance of cross-contamination and recontamination events
Cross-contamination and recontamination routes and sources .
3.1.
Poultry meat . . . . . . . . . . . . . . . . . . . . .
3.2.
Other meats . . . . . . . . . . . . . . . . . . . . .
3.3.
Eggs and egg products . . . . . . . . . . . . . . . . .
3.4.
Low-moisture foods . . . . . . . . . . . . . . . . . .
3.5.
Fresh produce and spices . . . . . . . . . . . . . . .
3.6.
Milk, dairy and milk products . . . . . . . . . . . . .
3.7.
Seafood . . . . . . . . . . . . . . . . . . . . . . .
4.
Cross-contamination in food-handling scenarios and retail points
5.
Biolm formation and food contact surfaces . . . . . . . . . .
6.
Modeling Salmonella transfer in foods . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction
Salmonellosis represents an important foodborne disease that
continues to pose a major and unacceptable threat to human public
health in both developed and developing countries (European Food
Safety Authority (EFSA), 2010). The dynamics of Salmonella infection
Corresponding author. Tel.: + 34 957218516; fax: + 34 957212000.
E-mail address: bt2cajie@uco.es (E. Carrasco).
0963-9969/$ see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodres.2011.11.004
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is variable and may also be affected by human lifestyle and behavior,

changes in industry, technology, commerce and travel (Foley, Lynne,
& Nayak, 2008). Salmonella serovars are widespread in nature and can
be found in the intestinal tract of all animals species, both domestic
and wild (Allerberger et al., 2002) which result in a variety of Salmonella
infection sources.
Currently, Salmonella spp. remains a serious foodborne illness risk
worldwide 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) 545556
human cases in the European Union (EU) in 2008, representing the second most often reported zoonotic disease in humans following campylobacteriosis. Human salmonellosis cases reported in 2008 show a 13.5%
decrease from 2007 in the EU. However, several European countries
still show a signicant increasing trend, proving that continuous efforts
for prevention and control are still necessary.
In the EU, serotypes Salmonella Enteritidis and Salmonella Typhimurium are reported as the two major etiologic agents of salmonellosis that
have adapted to humans. In the US, Salmonella Enteritidis and Typhimurium represent the two most frequently reported serotypes according to Centers for Disease Control and Prevention (Centers for Disease
Control, 2006). The distribution of Salmonella serotypes in Australia varies geographically. Thus, while S. Typhimurium was the most commonly
reported serovar in 2008, S. Enteritidis was frequently reported as cause
of human disease, despite it is not endemic in Australia (Yates, 2011).
While S. Enteritidis is mostly implicated in the consumption of poultry
and eggs, S. Typhimurium is linked to a range of food-producing animals
such as poultry, swine, cattle and sheep. S. Enteritidis was a rare serovar
until the mid-late 1980s when it emerged as a frequent cause of salmonellosis in European countries and across the globe (Cogan & Humphrey,
2003; Poppe, 1999). By the 1990s, S. Enteritidis replaced S. Typhimurium
as the most common serotype of salmonellosis isolated from humans in
many countries (Angulo & Swerdlow, 1999; Cogan & Humphrey, 2003;
Tschape et al., 1999). Australia and New Zealand, however, experienced
a relatively higher number of outbreaks due to S. Typhimurium compared to Canada, the US and the EU (Dalton et al., 2004). Previous salmonellosis outbreaks in Canada and the US have been linked to S. Enteritidis
(Centers for Disease Control, 2004). The global distribution of food and
the continuous movement of people around the world facilitate the
spread of this agent, allowing the introduction of emerging Salmonella
serotypes into importing countries.
In general, salmonellosis is transmitted when Salmonella cells are
introduced in food preparation areas. Several factors such as multiplication in food due to inadequate storage temperature, insufcient
cooking or cross-contamination are often implicated in salmonellosis
outbreaks (Ryan, Wall, & Gilbert, 1996; Todd, 1997). The main transmission routes of this pathogen are foods of animal origin contaminated with fecal matter (Haeghebaert et al., 2003; Swartz, 2002).
However, consumption of meat from infected animals may also occasionally be a source (Benenson, 1995; Tauxe, 1991).
Some investigations highlight the frequent occurrence of Salmonella in
meats and meat products (Mead et al., 1999) Overall, meat, poultry and
eggs are acknowledged as constant vehicles of Salmonella serovars and
generally 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 Salmonella
infection (Todd, 1997). The incidence of Salmonella has been studied in
poultry 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 (Busani
et al., 2005). High prevalence rates have been found in these countries
and the serotypes isolated vary geographically with predomination of
S. Enteritidis, S. Thyphimurium, S. Hadar, S. Newport, S. Virchow and
S. Heidelberg. All these studies emphasize the fact that poultry meat
represents a major source of this pathogen and therefore, recontamination of cooked poultry should be considered as a major risk factor. However, the importance and the impact of recontamination events are
not frequently well-documented in reports and scientic literature.
This lack of supporting evidence may be explained by several reasons, such as incomplete insight in to the causes of foodborne diseases,
underreporting cases or lack of outbreak investigation (Reij, Den
Aantrekker, & ILSI Europe Risk Analysis in Microbiology Task Force,
2004).
The objective of this review is to examine the role of crosscontamination and recontamination of foods by Salmonella, the principal factors involved, and the strategies developed for prevention of
cross-contamination and recontamination.
2. Importance of cross-contamination and recontamination
events
In accordance to Prez-Rodrguez, Valero, Carrasco, Garca-Gimeno,
and Zurera (2008), who reviewed bacterial transfer modeling in
foods, dened cross-contamination as a general term which refers to
the transfer, direct or indirect, of bacteria or virus from a contaminated
product to a non-contaminated product. Similarly, other terms have
been used to describe bacterial transfer, but not in a general sense,
such as recontamination, which is dened as contamination of food
after it has been submitted to an inactivation process.
According to the World Health Organization (WHO) (1992), 25% of
foodborne outbreaks are closely associated with cross-contamination
events involving decient hygiene practices, contaminated equipment,
contamination via food handlers, processing, or inadequate storage.
Identifying sources of infection frequently proves complicated as accurate data is often difcult to obtain from governments, industries, and
also incomplete investigations.
Salmonellosis outbreaks linked to cross-contamination processes
have highlighted the importance of these events to identify high-risk
foods and practices. Given the high percentage of foodborne outbreaks
linked to cross-contamination events, future investigations will suggest
possible cross-contamination routes when a Salmonella outbreak occurs. Cross-contamination and recontamination information on outbreaks in scientic literature is scant. Review papers on outbreaks
remain frequently unpublished as they do not completely fulll prerequisites such as high number of patients affected, emerging pathogen,
unusual serotypes or new food matrices. Outbreaks source attribution
cannot be regularly conrmed by food sample investigation due to
lack of leftover food matter.
When Salmonella survival is allowed under cross-contamination
and recontamination conditions, several factors such as inadequate
temperatures during food preparation as well as survival through
undercooking or food handling scenarios become critical.
The potential risk of Salmonella spp. to contaminate sites and surfaces in the household has been studied (Gorman, Bloomeld, &
Adley, 2002). These authors emphasize how the preparation of raw
food such as fresh chicken may magnify the dissemination of Salmonella
to hands and food contact surfaces. A signicant proportion of crosscontamination scenarios occur in domestic kitchens. In fact, in the Netherlands, Germany, and Spain, more than 50% of reported foodborne outbreaks were observed in the home (Beumer, Bloomeld, Exner, Fara, &
Scott, 1998; Scott, 1996). Several authors have demonstrated that Salmonella cells from frozen broiler chicken were able to contaminate
food 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 salmonellas
can be transferred from chicken to utensils, a variety of kitchen surfaces,
hands and other foods; from those, Salmonella cells were recovered
from surfaces up to 6 h after contamination. Bradford, Humphrey, and
Lappin-Scott (1997) examined the ability of S. Enteritidis, under sterile
and non-sterile conditions, to be cross-contaminated from inoculated
eggs droplets to melon and beef and grow on these products at ambient
temperature. Consumer awareness of the need to implement Good Hygiene Practices (GHP) is of paramount importance in order to prevent
the spread of Salmonella cells in food preparation areas.
Researchers are increasingly studying the ability of Salmonella to colonize different inert food contact surfaces to form biolm (Bonafonte
et 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
give insight in to the mechanisms underlying biolm formation, suggesting different strategies for prevention.
3. Cross-contamination and recontamination routes and sources
Cross-contamination and recontamination events linked to Salmonella
during food processing are reported in literature. Below is a review of
sources and routes of potential cross-contamination and recontamination
episodes by Salmonella spp. linked to different food categories.
3.1. Poultry meat
The association between poultry and Salmonella genus has long
since been recognized. It was not until the 1960s when the poultry industry started to grow thanks to the application of control measures
of pullorum disease and fowl typhoid (Poppe, 2000). Subsequently,
an increasing isolation of non-host specic Salmonella from poultry
products and human cases meant a challenge to identify the origin
of the strain involved in human cases. Currently consumption of poultry products remains as a well documented major source of salmonellosis, being undercooking and cross-contamination appointed as
recognizable 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 is
around 50%. When poultry ocks are infected at farms, Salmonella is
carried asymptomatically in the gastrointestinal tract and can be
readily transferred to carcasses through fecal contamination in the
abattoir. Further spread of cells may occur easily during processing
if carcasses become cross-contaminated. Also, the role of feed ingredients as a source of Salmonella in the poultry industry has received
great attention (Bailey et al., 2001). Feed products may constitute a
risk factor for introducing Salmonella since they are made from a wide
variety 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 recognized 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 feathers
for subsequent defeathering. Once carcasses have begun the scalding
process, great numbers of microbes from skin, feathers and involuntary
defecations, are released to the scald water. Although survival of these
bacteria depends on temperature, even high temperatures used in
hard scalding (5863 C) may have a slight effect on organisms attached to skin. Slavik, Kim, and Walker (1995) observed that Salmonella
was not signicantly reduced after hard scalding. The mechanisms
that might result in cross-contamination during defeathering include
aerosols (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 the
picker machine (Allen, Hinton, et al., 2003a; Allen, Tinker, Hinton, &
Wather, 2003b; Berrang, Buhr, Cason, & Dickens, 2001; Campbell et
al., 1984; Clouser, Doores, Mast, & Knabel, 1995a; Clouser, Knabel,
Mast, & Doores, 1995b). In this line, Nde, McEvoy, Sherwood, and
Logue (2007) appointed the ngers of the picker machine as well as
scald water as sources of cross-contamination during defeathering. A
better understanding of cross-contamination mechanisms during
processing has been studied by authors through the use of molecular
typing (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 prevalence (Sarlin et al., 1998). During evisceration, carcasses are sprayed
with water in order to remove organic remains and reduce microbial contamination by about 1 log unit. However, the removal of microorganisms
547
from carcasses in the spray process can be insufcient if bacteria are

rmly attached to the tissues (Lillard, 1993).
Chilling of poultry carcasses to 4 C is supposed to guarantee
that no Salmonella present will be able to multiply. This step includes
immersion in cold water or exposure to cold air either by passing
carcasses through an air blast system or holding them in a chilling
room. As chill water used for immersion of carcasses is usually
replaced, 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, water
chilling is considered a major factor in ock-to-ock transmission of
Salmonella (James et al., 1992; Lillard, 1990; Sarlin et al., 1998).
Cross-contamination may still be possible via air currents and water
droplets if carcasses are sprayed during chilling stage (Mead, Allen,
Burton, & Corry, 2000).
According to Bloomeld and Scott (1997), cross-contamination risks
associated with different locations and surfaces depend not only on the
occurrence of likely harmful pathogens, but also on the probability of
transfer from those sites. As described by Jackson, Blair, McDowell,
Kennedy, and Bolton (2007), food pathogens might survive on refrigerated surfaces and pose a cross-contamination risk. Mattick et al. (2003)
also reported that Salmonella is able to survive air drying in food for at
least 24 h and therefore, when cells are released from perishable
foods on cutting boards, they may be viable for long periods of time.
Jimnez, Tiburzi, Salsi, Moguilevsky, and Pirovani (2008) studied refrigeration conditions affecting the survival of Salmonella Hadar inoculated
on chicken skin and investigated the potential of transfer to a plastic
cutting board. They dened two scenarios where carcasses were treated
or untreated with a decontamination agent to assess the effectiveness of
the decontamination process in regards to the reduction of S. Hadar at
three temperature levels (2 C, 6 C and 8 C) and the likelihood of
cross-contamination. They found that Salmonella was able to detach
from chicken skin and be transferred to cutting board more readily
when chicken was treated with acid. Similarly, Nissen, Maugesten,
and Lea (2001) observed that growth of S. Enteritidis on untreated
chicken breasts was not signicantly different from the growth on
decontaminated chicken, except after 3 days when a considerably
higher growth was found on untreated samples. The attachment ability
of Salmonella has also been associated with the moisture content of
meat; when carcasses are still fresh and the moisture of the skin is
high, the transference from carcasses to other surfaces is more
marked (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 sources
for salmonellosis (Bacon, Sofos, Belk, Hyatt, & Smith, 2002;
Botteldoorn, Heyndrickx, Rijpens, Grijspeerdt, & Herman, 2003). In
Denmark and Germany, the estimation of salmonellosis associated
with consumption of pork has been linked to 1520% of human
cases (Berends, Van Knapen, Mossel, Burt, & Snijders, 1998; Borch,
Nesbakken, & Christensen, 1996).
At pre-harvest, contaminated feed, water, vectors and other environmental sources linked to swine production have been suggested as potential sources of Salmonella (Bailey, 1993; Nayak, Kenney, Keswani, & Ritz,
2003). Pigs can be infected during transport or waiting period in lairage
before slaughtering. It has been suggested that lairage and the slaughterhouse environment are probably the major source for Salmonella infections prior to slaughter (Hurd, McKean, Wesley, & Karriker, 2001;
Swanenburg, Urlings, Keuzenkamp, & Snijders, 2001). Once Salmonella
colonizes the gastrointestinal tract of pigs, carcasses can become contaminated at slaughter, and consequently contaminated raw or undercooked red meats will act as transmission routes for salmonellosis.
According to Borch et al. (1996), the main contamination sources of
548
pig carcasses are feces, pharynx and stomach, and environmental sources
such as contact surfaces and handling.
During slaughter, not only carcasses of infected pigs, but crosscontamination from the environment and other infected animals may
occur. Botteldoorn et al. (2003) studied the prevalence of Salmonella
in swine at the moment of slaughter and observed that the slaughterhouse environment was highly contaminated. These authors estimated
that 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 crosscontamination accounted for 30% of the entire pork carcass contamination in slaughterhouses. Continuous environmental infection sources
may maintain Salmonella in slaughterhouses indicating inefcient or
poor hygiene practices (Botteldoorn et al., 2003). In regard to risk factors at slaughter associated with the presence of Salmonella on hog carcasses, Letellier et al. (2009) underlined the importance of the
preslaughter and pre-evisceration environment on the nal contamination status of carcasses. They observed that cleanliness of the hogs and
status of scald water were signicant factors associated with Salmonella
status of the carcasses at the end of the slaughtering process. Genetic
characterization and serology used in this study highlighted that particular attention should be paid to herd contamination levels of incoming
animals and the pre-evisceration environment.
Once slaughtered, the next steps are manufacturing and preparation
and storage at retail. At these levels, three major factors such as
handling, time and temperature may signicantly inuence the microbiological quality of pork meat (Lo Fo Wong et al., 2003). Special care
must be considered in order to avoid cross-contamination between
products, as large quantities of raw meat of different origin may be handled closely together.
Besides swine, cattle are also known reservoirs of Salmonella; ground
beef has been implicated in salmonellosis outbreaks (Centers for Disease
Control, 2006). Despite Salmonella in ground beef has decreased with the
implementation of the HACCP system (Eblen, Barlo, & Naugle, 2006), the
risk of transmitting this pathogen through the food chain cannot be
disregarded, especially in raw, smoked or lightly cooked meat products.
Several investigations have studied the overall occurrence of Salmonella in
beef 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, the
Food Safety Inspection Service has suggested that the current prevalence
of ground beef is 2.4%. Since standard culturing techniques (which are the
most popular) may have a lower level of sensitivity than others methods
such as immunomagnetic separation (Barkocy-Gallagher et al., 2003), the
prevalence of this pathogen in ground beef may be underestimated.
Additionally, cross-contamination in the kitchen can contribute
signicantly to salmonellosis incidence. Iordache and Tofan (2008)
demonstrated the ease with which two strains of Salmonella Enteritidis were able to cross-contaminate beef surfaces from inoculated egg
droplets.
The role of cross-contamination in RTE meats should also be regarded.
On a global scale, RTE meat products may act as vehicles for foodborne
pathogens. Some RTE meat products such as biltong (traditional South
African dried and spiced meat made from beef, wild game, or chicken)
or jerky (American dried meat product from domestic and wild animals)
have been involved in salmonellosis outbreaks (Bokkenheuser, 1963;
Centers for Disease Control, 1995; Neser, Louw, Klein, & Sacks, 1957). Previous studies conducted on other RTE products revealed that factors such
as food handlers, aprons, utensils, and work surfaces are potential sites
for bacterial contamination (Christison, Lindsay, & von Holy, 2007,
2008; Lues & Van Tonder, 2007). Naidoo and Lindsay (2010) evaluated
hygiene of surfaces that come into direct contact with an RTE dried
meat product, biltong, and highlighted the importance of such surfaces
as potential sites contributing to cross-contamination of the nal product
at 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 contamination
of RTE products (Lunden, Autio, & Korkeala, 2002; Pal, Labuza, & DiezGonzalez, 2008). Cutting during RTE meat slicing have a signicant inuence in cross-contamination scenarios since blades are capable of disseminating high numbers of microbial populations with every slice which
may include foodborne pathogens such as Staphylococcus aureus, Escherichia coli or Salmonella (Fernane, Morales, Carrasco, & Garca-Gimeno,
2010; Prez-Rodrguez et al., 2007).
In the production of meat and meat products, numerous attempts to
mitigate the risk of salmonellosis have been made. At the farm, AIAO
(all-inall-out) system has been proposed to reduce the risk of crosscontamination between groups of animals; AIAO swine productions
consist of keeping animals together in groups where pigs from different
groups are not mixed during their stay on the farm. Lo Fo Wong et al.
(2003) has reported the importance of controlling feed (e.g. acidication of feed) to reduce or remove Salmonella from a herd. During transportation to the abattoir, animals are subjected to stress factors such as
overcrowding, long duration of transport, unfamiliar pigs, noises,
etc., which may result in an increase of number of animals excreting
Salmonella until arrival at the slaughterhouse (Berends et al., 1997).
To reduce the spread of infection during transport, it has been proposed not to mix unfamiliar animals and handle them as quietly
and gently as possible (Warriss, Brown, Edwards, Anil, & Fordham,
1992). Also, trucks should be thoroughly cleaned and disinfected between transports (Rajkowski, Eblen, & Laubach, 1998). In the slaughterhouse, Olsen, Brown, Madsen, and Bisgaard (2003) emphasized
the importance of the segregation of clean and dirty processes to reduce the likelihood of cross-contamination and the need to improve the
hygiene of the equipment used. During processing, Cason and Hinton
(2006) concluded that multistage scalding reduced the likelihood for
cross-contamination of Salmonella, when compared with a single-tank
system. Also, scalding temperature should be set, at least, at 62 C
(Hald, Wingstrand, Swanenburg, von Altrock, & Thorberg, 2003). Water
chilling of carcasses is considered a major factor in ock-to-ock transmission of Salmonella (Lillard, 1990); a total residual chlorine of 45 to
50 mg/l to keep water free from viable vegetative bacteria has been suggested (Lillard, 1989).
3.3. Eggs and egg products
Salmonella Enteritidis is primarily linked to consumption of poultry, 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 may
contain no more than a few hundred Salmonella cells. Prompt refrigeration procedures can prevent the growth of these small populations
during storage (Gast, Guraya, Guard, & Holt, 2010). This study demonstrates that once Salmonella Enteritidis is introduced into the albumen, it can reach the yolk and multiply during unrefrigerated storage.
Eggs infected with Salmonella represent a serious threat to consumers. Further investigation of handling of contaminated eggs is
necessary to understand their role in kitchens, even if they are not
purposed for raw consumption. For instance, kitchen surfaces and
utensils may become contaminated by raw infected eggs and serve
as an infection medium to other foodstuffs. In fact, research data has
shown that cross-contamination events linked to eggs have resulted
in outbreaks. Slinko et al. (2009) described an outbreak (Salmonella
Typhimurium phage type 197) in a series of restaurants across Brisbane,
Australia, in a two-month period. Investigation of these restaurants
identied a lack of food hygiene and potential cross-contamination issues. The outbreak was traced back to cracked and dirty eggs. In Australia, Food Safety Standards (Food Standards Code) were developed to
provide more effective and nationally uniform food safety legislation.
Despite national code prohibit the sale of cracked and dirty eggs for retail or catering, the Food Standards Code did not appear to have
properly protected public health as it allowed the sale of contaminated,

cracked, and dirty eggs to restaurants where foods and surfaces were
cross-contaminated through food handling. Likewise, a survey conducted after an unusual number of Salmonella Enteritidis outbreaks associated with the use of eggs in food service in England and Wales
(Little et al., 2008) revealed evidence of inadequate eggs storage and
handling practices. The food service sector should be aware of salmonellosis hazards and receive proper training on hygiene practices such
as the usage of raw shell eggs, in order to avoid cross-contamination episodes and reduce the risk of salmonellosis.
3.4. Low-moisture foods

Salmonella spp. is expected to be present in any raw food product
since this pathogen is widely disseminated in nature (e.g., water, soil,
plants, and animals). Salmonella spp. is able to survive for weeks in
water and for years in soil if environmental conditions such as temperature, humidity, and pH are favorable (Todar, 2008). Low water
activity (aw) represents a barrier to growth for many vegetative pathogens, including Salmonella spp. (Betts, 2007). Processed foods such
as powdered milk, chocolate, peanut butter, infant food, and bakery
products are characteristically low-aw food products. Epidemiological
and environmental data investigations have indicated that crosscontamination plays a major role in the contamination of these products (Smith, Daifas, El-Khry, Koukoutsis, & El-Khry, 2004). Salmonella
spp. has the capacity to survive in dry foods and feeds for long periods
of time (Hiramatsu, Matsumoto, Sakae, & Miyazaki, 2005; Janning, in't
Veld, Notermans, & Kramer, 1994; Juven et al., 1984). Furthermore, it
has been reported that the combination of low aw and high fat content 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 lowmoisture products. Poor sanitation practices, substandard facilities,
equipment design, and improper maintenance remain the main
causes of Salmonella contamination in low-moisture foods. Lowmoisture products contaminated by Salmonella where recontamination and cross-contamination events have been mostly reported are
presented.
Chocolate presents a very low moisture content (b8%) and high fat
levels. Several potential sources of Salmonella like raw cocoa beans or
powdered milk may carry Salmonella cells. Although Salmonella is not capable of growing in nished chocolate, it is able to survive for long periods
of time, representing a signicant risk even at low levels in the product.
Cross-contamination and recontamination events involving chocolate
have been reported. Craven, Mackel, Baine, Barker, and Gangarosa
(1975) reported an international outbreak by Salmonella Eastbourne
linked to contaminated chocolate where cross-contamination by airborne
dust was a plausible cause. In 2006, a Salmonella Montevideo outbreak
linked to chocolate products was attributed to a leaking episode (Food
Standards Agency, 2006).
Nut and seed products may be naturally contaminated with
Salmonella because of the nature of cultivation and/or harvesting processes. A great number of nut and seed products have been recalled due
to Salmonella contamination (Podolak et al., 2010). Cross-contamination
and recontamination due to poor sanitary design and machinery maintenance in peanut products may contribute to Salmonella contamination.
Also, if ingredients are not adequately handled and/or stored and become
contaminated with Salmonella, they potentially act as a source of contamination for processed nished products. During a salmonellosis outbreak
investigation in US, the FDA declared that raw peanut storage was unsuitable (U.S. Food & Drug Administration, 2009a) and cross-contamination
opportunities were plausible. In 2007, investigations of an outbreak of
salmonellosis linked to peanut butter, the roof of the factory leaked and
the sprinkler system broke down (Funk, 2007).
549
Spray drying is a method of producing a dry powder from a liquid

by rapidly drying by hot gas. Spray drying food applications include
milk powder, coffee, tea, eggs, cereal, avorings, etc. The most
important factors that inuence the survival of Salmonella in spraydried products are temperature during processing, particle density, fat
content and strain variation (Miller, Goepfert, & Amundson, 1972).
While spray drying foods, the equipment may inuence Salmonella
contamination as Rowe et al. (1987) indicated in a Salmonella Ealing
outbreak.
Salmonella contamination of oilmeal has been a matter of concern
for many years (Sato, 2003). The eradication of Salmonella in oilmeal
plants is a difcult task since a high probability of spreading contamination from manufacturing to storage areas has been observed and
hence, cross-contamination is plausible (Morita, Kitazawa, Iida, &
Kamata, 2006).
Control of Salmonella in low-moisture foods presents several challenges to manufacturers. The Grocery Manufacturers Association (2008)
published a guidance document, establishing seven control elements
against Salmonella contamination: 1) prevent entrance and spread of
Salmonella in processing facilities; 2) increase the stringency of hygiene
practices and controls in the Primary Salmonella Control Area; 3) application of hygienic principles to building an equipment design; 4) prevent or reduce growth of Salmonella in the facility; 5) establish a raw
materials/ingredients control program; 6) validate control measures
to inactivate Salmonella; and 7) establish procedures for verication of
Salmonella controls and corrective actions.
3.5. Fresh produce and spices
Vegetables, including cilantro, broccoli, cauliower, lettuce, and spinach, have also been reported as vehicles of Salmonella (Quiroz-Santiago
et al., 2009). Fresh tomatoes have been commonly linked to salmonellosis outbreaks in the US (U.S. Food & Drug Administration, 2009b). Rana
et al. (2010) examined Salmonella cross-contamination during postharvest washing of tomatoes and observed that Salmonella could spread
from contaminated to uninoculated tomatoes during washing procedures. Fresh herbs and spices are classied into the RTE category
(Regulation EC No. 2073/2005). Spices such as clove, oregano, black
pepper, and paprika among others, may be exposed to great microbial contamination during harvesting and processing and they are sold
without any treatment to reduce contamination. Data from literature
shows that Salmonella has been isolated in spices (Moreira,
Lourencao, Pinto, & Rall, 2009; Pafumi, 1986). Despite the industry
having more and more sophisticated control mechanisms available,
well-designed equipment systems are not able to combat crosscontamination from poor sourcing, choice, and control of raw materials and ingredients.
Fresh produce may be contaminated during production, harvest,
processing, at retail levels or in the kitchen at home. Washing procedure is one of the most studied measures to reduce the level of contamination. Pao, Kelsey, and Long (2009) examined the efcacy of
chlorine dioxide during spray washing of tomatoes for preventing
Salmonella enterica transfer from inoculated roller brushes to fruit
and wash runoff, reporting an important reduction of the pathogen
(5.0 0.3 log). Rana et al. (2010) designed a washing system of
tomatoes to simulate a commercial postharvest washing, showing
that the use of higher temperatures (37 C) during washing lead to
lower Salmonella uptakes than those observed at 20 C.
3.6. Milk, dairy and milk products
Several foodborne pathogens have usually been detected in raw
milk, including Salmonella spp., Campylobacter spp., E. coli, Listeria
monocytogenes, and S. aureus (Oliver, Jayarao, & Almeida, 2005). Fecal
contamination during milking constitutes a primary route for pathogen
transmission. The consumption of raw milk represents a well-
550
documented issue for human health (Headrick et al., 1998; LeJeune &
Rajala-Schultz, 2009). However, increasing number of consumers demand raw milk and/or products made from raw milk and other unprocessed products. According to epidemiological data, it is necessary to
consider not only the risk of raw milk consumption, but also the likely
episodes of recontamination and cross-contamination that can take
place at the industry or home kitchens if milk is not pasteurized or
heat-treated. However, pasteurized milk has also been involved in salmonellosis infections and outbreaks, as reported by Olsen et al.
(2004). According to these authors, pasteurization was adequate.
Nevertheless, microbial testing demonstrated that coliform counts
were higher (>100 cfu/mL) than those recommended by Pasteurized
Milk Ordinance (10 cfu/mL). Cross-contamination episodes were not
identied though they should not be ruled out.
Cheese has been characterized as one of the safest food products by
some experts (Johnson, Nelson, & Johnson, 1990); however, since
cheese is considered an RTE food product and does not undergo any further treatment before consumption, contamination episodes should be
considered. Contaminated raw milk as well as cross-contamination
with pathogens such as Salmonella, can be introduced into dairy processing plants and represents a human health risk if unpasteurized milk is
used for cheese production (Kousta, Mataragas, Skandamis, & Drosinos,
2010). Cross-contamination of cheese may be originated from starter
culture, brine, oor, packaging material, cheese vat, cheese cloth, curd
cutting knife, cold room, and production room air (Temelli, Anar, Sen,
& Akyuva, 2006). Domnguez et al. (2009) reported a Salmonella outbreak caused by raw-milk cheese containing low contamination levels
which had not been detected. Despite there are not reported outbreaks
where cheeses cross-contamination is linked to salmonellosis outbreaks,
these data suggests that contamination and cross-contamination of
cheese may occur, and if ignored or underestimated, the risk of salmonellosis could increase.
3.7. Seafood
Seafood is responsible for a signicant amount of foodborne diseases and represents a great concern from a public health perspective.
Salmonella is not a component of the normal ora of sea animals, thus
contamination of seafood is a result of fecal contamination through
polluted water, infected food handlers or cross-contamination during
production or transport (Lunestad & Borlaug, 2009). High prevalence
is frequently attributed to poor hygienic practices during handling
and transportation from landing centers to sh markets. Shrimp is
one of the most reported seafoods associated with salmonellosis
(Wan Norhana et al., 2010). Certain aspects of cooked shrimp production like cooking procedures aboard shing vessels, chilling with seawater, and intensive handling and transportation make them
susceptible to be contaminated.
Data gathered from studies involving Salmonella contamination in
prawns (Hatha, Maqbool, & Kumar, 2003; Heinitz, Ruble, Wagner, &
Tatini, 2000; Reilly & Twiddy, 1992) have suggested the likelihood of
cross-contamination between raw and cooked products. Wan Norhana,
Poole, Deeth, and Dykes (2010) reported various physical control
measures, including cooking, refrigeration, irradiation, modied atmosphere packaging (MAP), high-pressure processing (HPP) and highpressure carbon dioxide.
4. Cross-contamination in food-handling scenarios and retail points
Salmonella can remain viable on food contact surfaces for signicant
periods, increasing the risk of cross-contamination events between food
handlers, food products, and food contact surfaces (De Cesare, Sheldon,
Smith, & Jaykus, 2003; Humphrey, Martin, & Whitehead, 1994). The role
of food workers in foodborne outbreaks have been clearly demonstrated by several authors (Todd, Greig, Bartleson, & Michaels, 2009). Thus,
the transmission and survival of enteric pathogens such as Salmonella
in the food processing and preparation environment through humans

represent an important risk. Among the different causes of foodborne
outbreaks, consumer mishandling of food in household plays an important role. Anderson, Shuster, Hansen, Levy, and Volk (2004) indicated
that 25% of reported outbreaks are caused by inadequate consumer
handling and food preparation at home. In fact, epidemiological studies
have revealed that a signicant number of consumers follow unsafe and
risky practices during meal preparation (Redmond & Grifth, 2003) and
do not implement proper hygienic measures to prevent crosscontamination 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 reutilize
cutting boards without cleaning after cutting raw meat or chicken.
Therefore, it is reasonable to expect a reduction of salmonellosis and
other foodborne diseases if consumers would apply safe foodhandling practices. Cross-contamination and transfer rates of Salmonella enterica from chicken to lettuce were assessed by Ravishankar, Zhu,
and Jaroni (2010) under different food-handling scenarios, with and
without washing procedures. The study showed that washing using
only water is not enough to remove S. enterica while washing procedures including soap, hot water, and vigorous mechanical scrubbing
are suitable to reduce cross-contamination.
Retail point scenarios must be addressed since a wide variety of
specialist foods such as RTE products are frequently sold in delicatessen and fast food restaurants, where stainless steel blade retail slicers
are commonly used in meal preparations. Most likely underreported
at retail levels, cross-contamination scenarios involving equipment
and utensils such as boards, knives, and slicers are likely to occur
when good hygiene practices are not applied by personnel. Slicing
of foodstuffs such as RTE meat products can enhance the risk of
cross-contamination by contact with contaminated surfaces. Indeed
not only slicing, but also cutting operations, handling or packaging
contributes to increase the risk of cross-contamination. Investigations
during a salmonellosis outbreak in 1963 conrmed that the vehicle of
infection 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 contamination
to other RTE meats. The potential risk of transfer of Salmonella in slicing
scenarios has not been well assessed thus far. However, the study of
these scenarios would provide empirical data to develop guides targeted at retailers and industry on proper slicing practices and cleaning
and disinfection procedures to prevent transfer and survival of
Salmonella.
The role of shopping bags in cross-contamination events has also
been discussed. If not adequately washed between uses, reusable
bags create the potential for cross-contamination of foods. For
instance, when raw meat products and nished foods are carried in
the same bag, either together or between uses, the opportunities for
cross-contamination increase. Gerba, Williams, and Sinclair (2010)
studied the potential for cross-contamination of various food products by reusable shopping bags and observed that great numbers of
bacteria were found in almost all bags and coliform bacteria in half.
The study suggested that raw meats or other uncooked food products
contaminated bags. E. coli was detected in 12% of bags, demonstrating
that reusable bags can be contaminated by enteric microorganisms
and they constitute a potential hazard, especially if growth were to
be proven in plastic bags. Although Salmonella and other pathogens
such as Listeria spp. were not isolated from bags, the risk of nding
these organisms in reusable shopping bags should not be ignored. In
fact, some studies have demonstrated that children have an increased
risk of salmonellosis if they ride in a shopping cart carrying meat products and eating other foods such as fruits or vegetables previously prepared at home (Fulterton et al., 2007; Jones et al., 2006). Handling raw
food products during shopping and transport to the home is a route for
the transmission of these bacteria. Packaged meats might contaminate
the bag since they can leak during transport. Harrison, Grifth,
Tennant, and Peters (2001) declared that chicken and chicken packaging is a potential vehicle for the introduction of pathogens in retail
and domestic kitchens and, in particular, for the cross-contamination
of Salmonella and Campylobacter. The study highlighted that food industry and consumers should be concerned about the potential risk of salmonellosis and campylobacteriosis from contamination of both the
external and internal packaging surfaces in addition to the chicken
itself. It should also be noted that, once contaminated, bags are frequently assigned to purposes others than carrying groceries, and then,
the risk of cross-contamination increases. The study also revealed that
consumers rarely wash reusable bags, and bacteria were able to grow
when stored in the car trunks. This suggests that it is necessary to make
recommendations targeted at consumers in order to reduce the risk of
cross-contamination by using reusable shopping bags.
Kitchen surfaces also represent a signicant risk of crosscontamination and recontamination events (Redmond & Grifth,
2003). Domestic food contact surfaces appear to play an important
role in the transmission of foodborne agents such as Salmonella spp. Researchers currently debate which surface materials pose the greatest
risk to consumer health in terms of cross-contamination during food
preparation. Accordingly, some studies have underlined the essential
paradox of choosing food contact surfaces, i.e. those characteristics
that make a surface easy to clean may also more likely release foodborne pathogens during common food preparation practices (Moore,
Blair, & McDowell, 2007). For instance, cutting boards are commonly
perceived as signicant fomites in cross-contamination of foodstuffs
with foodborne agents. Wooden cutting boards and utensils have
been banned for a long time in production sites of meat and poultry
foods. Still today, opposition is present in respect to the use of wood instead of plastic during food processing despite the lack of evidence of
the presumed better sanitation properties of plastic utensils (Ak,
Cliver, & Kaspar, 1994; Carpentier, 1997). In contrast, to date, several
publications are in favor of wood, demonstrating that plastic is not empirically better (Boursillon & Riethmller, 2005; Prechter, Betz, Cerny,
Wegener, & Windeisen, 2002;). Nevertheless, it is generally recognized
that bacteria are able to penetrate the pores of wood where they are
then trapped. While plastic cutting boards can be cleaned in a dishwasher (as well as some specially treated wooden boards), this operation may distribute the pathogen onto other food contact surfaces; in
contrast, most small wooden boards can be sterilized in a microwave
oven. Cliver (2006) stated that epidemiological studies seem to show
that cutting board cleaning habits have a slight inuence on the incidence of salmonellosis. Therefore, the use of wooden cutting boards is
still controversial. Even though the choice of plastic might improve safety due to better cleaning properties of plastic cutting boards, they are
not as signicant as often stated.
Klontz et al. (1995) reported that 25% of their respondents reused
cutting boards after cutting raw meat or chicken without proper cleaning procedures. Redmond and Grifth (2003) observed that 81% of consumers used the same utensils and cutting boards for preparation of
both raw and RTE products. Deciencies in food preparation hygiene
such as inadequate cleaning of cutting boards after cutting raw meat
and poultry likely play a signicant role in contamination by pathogens
(De Boer & Hahne, 1990). Cross-contamination and transfer rates of Salmonella enterica from chicken to lettuce under three different foodhandling scenarios were evaluated by Ravishankar et al. (2010). Their
study revealed that Salmonella was easily transferred from cutting
boards and knives to lettuce if utensils were not carefully washed
with soap and hot water after cutting chicken and before cutting lettuce.
Furthermore, this study showed that merely washing contaminated
kitchens utensils was not enough to remove S. enterica. The transfer
rate obtained in the scenario 1 of this study was 45%, where cutting
board and knife were unwashed after cutting the chicken. Similar results were found by Moore, Sheldon, and Jaykus (2003) who found
transfer rates of 3666% for S. Typhimurium from stainless steel surfaces to lettuce. Although signicant amounts of Salmonella cells can
551
be removed during washing, diminishing transfer rates, it may not be

effective at eliminating the risk of transfer since current infective dose estimates 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 including
Salmonella spp. As transfer rates can vary according to the organism,
the type of surface and food product, cross-contamination should be
assessed on a case-by-case basis.
Therefore, cross-contamination in the home kitchen is particularly
important and probably, underestimated. The risk of unsafe foodhandling practices and poor hygiene is relatively high, and impossible
to control. Consumer food safety education is a key issue for ensuring
food safety, despite little attention has been paid to this important
last step of the farm to fork chain. According to FAO/WHO (2002),
undercooking and cross-contamination in the homes represent two
general pathways for Salmonella spp. contamination.
5. Biolm formation and food contact surfaces
Biolm formation is a well-known bacterial mode of growth and survival which protects bacteria from stressful environmental conditions
such as drying and cleaning procedures of food surfaces and environment (Reuter, Mallet, Bruce, & van Vliet, 2010). Cross-contamination
linked to raw and processed foods by food contact surfaces has been
identied as a potential hazardous event (Barners, Lo, Adams, &
Chamberlain, 1999). Salmonella spp. has been recovered from a wide
range of food contact surfaces; as commented previously, Salmonella is
able to attach to inert surfaces in the food processing environment
(Hood & Zottola, 1997; Joseph et al., 2001) and consequently form biolms (Stepanovic, Circovik, Ranin, & Svabic-Vlahovic, 2004). Once a biolm is formed, it becomes a source of food contamination in processing
lines, representing a serious concern for the food industry.
Most of the food processing industry's surfaces such as machinery, pipelines, and working surfaces are made of stainless steel. This
material is traditionally selected in the kitchen for food preparation
because of its mechanical strength, corrosion resistance, and longevity (Holah & Thorpe, 1990). Food particles are frequently removed from these surfaces when good hygiene practices are
applied, although microorganisms might not be removed if appropriate disinfection procedures are not implemented. Some authors
have reported the presence of viable Salmonella spp. on stainless
steel surfaces (Kusumaningrum et al., 2003) and other materials
commonly found in processing plants such as rubber and polyurethane (Chia, Goulter, McMeekin, Dykes, & Fegan, 2009). Gough
and Dodd (1998) showed that Salmonella survived when RTE
came into contact with raw contaminated vegetables through cutting boards and stainless steel utensils. Different factors inuencing
the attachment capacity of Salmonella spp. have been studied.
Oliveira, Oliveira, Teixeira, Azeredo, and Oliveira (2007) suggested
that attachment is strongly strain dependent and the importance
of other factors such as production of polysaccharides should be
evaluated. Giaouris and Nychas (2006) demonstrated that increasing
the levels of appropriate nutrients also provides the most optimal environment for S. Enteritidis PT 4 to adhere, and subsequently, enhance
biolm formation on stainless steel surfaces.
Slicing has been shown to be a risky factor in cross-contamination
events, especially if RTE products are sliced, as blades are able to disseminate high numbers of Salmonella (Fernane et al., 2010). In this
sense, improving cleaning and disinfection procedures through hand
washing, changing of gloves, and daily sanitation of cutting utensils
and display cabinets is essential (Naidoo & Lindsay, 2010).
6. Modeling Salmonella transfer in foods
Cross-contamination and recontamination models have experienced a great development in the last years. Zhao, Zhao, Doyle,
552
Rubino, and Meng (1998) proposed a model of cross-contamination

of Enterobacter aerogenes (with attachment characteristics similar to
those of Salmonella spp.) from raw chicken to cutting board, and
from cutting board to vegetables, revealing that from 10 6 cfu/g of E.
aerogenes inoculated on the chicken, approximately 10 5 cfu/cm 2
was transferred to the cutting board, and approximately 10 310 4 of
E. aerogenes to the vegetables. However, this experience was not
modeled mathematically. From now on, by model we will mean
mathematical model.
Prez-Rodrguez et al. (2008) published the state-of-the-art of
bacterial transfer phenomenon, including a review of the transfer
models developed so far. The most popular models are based on
transfer rates, which involve the application of Eq. (1).
slices, and from 94 42% to 32 9% in roasted chicken llets, depending

on the time of recovery of cells (just or 15 min after the crosscontamination event) and the application or not of pressure (the level
of pressure applied was 500 g per slice, approximately 20 g/cm2, comparable to the pressure applied during sampling with contact plates). In a
later stage, Kusumaningrum et al. (2004) carried out a quantitative analysis of cross-contamination of Salmonella and Campylobacter spp. via domestic kitchen surface, to nally estimate the risk of salmonellosis and
campylobacteriosis per serving of salad. In this analysis, they modeled
the transfer rate of both microorganisms from chicken carcasses to kitchen surfaces (TR1) and from kitchen surfaces to salad vegetables (TR2). In
this way, the level of contamination of the pathogen in salad vegetables
was given by Eq. (3).
Nr TR=100 Nd
Cv N TR1 =100 TR2 =100
where Nr is the quantity of cells transferred to the receptor surface; TR

is transfer rate, i.e. the percentage of cells transferred from one surface (donor) to another surface (receptor), and Nd is the quantity of
cells contaminating the donor surface.
Often, transfer rates (TRs) show a large variation as a consequence
of the large number of factors involved as well as the errors inherent
to microbial collection from surfaces and enumeration techniques. To
capture the uncertainty and variability of TR data, normal distribution
has been proposed as the most appropriate to describe the logtransformed TR data (Montville, Chen, & Schaffner, 2001; Schaffner,
2003).
Usually, the actual contamination level of surfaces is low, and transfer
not necessarily occurs. However, articial contamination levels in experiments carried out to develop transfer models is high to obtain countable
concentrations. Hence, transfer experiments are intended to model nonzero transfer rates, rather than modeling failed bacterial transfers, i.e. 0%
transfer. Schaffner (2004) and Yang et al. (2006) applied cross contamination frequency values and TRs to describe microbial prevalence and
concentration changes, respectively. Ariza, Mettler, Daudin, and Sanaa
(2006) based their compartmental and dynamic cross contamination
model on the binomial process of bacterial transfer. This is, assuming
that microorganisms are homogeneously distributed in foods, a binomial
distribution B(n, p) could be applied to describe bacterial transfer
between different compartments, p being the transfer probability of a
cell and n the number of bacteria in the compartment. The binomial
model can also explain 0% transfer events (prevalence changes) when
p and/or n become very small.
Moore et al. (2003) approached the cross-contamination phenomenon from stainless steel to lettuce in a similar way as Zhao et al. (1998),
although they calculated the transfer rate of S. Typhimurium and
Campylobacter jejuni, showing that S. Typhimurium was able to transfer
during the rst 60 min of contact with a transfer rate (TR) of up to 66%.
TR was calculated as follows:
% transf er
CFU LET
100%
CFU LET CFU SST
where CFULET is the number of colony forming units found in lettuce and
CFUSST is the number of colony forming units found in stainless steel
coupons.
Other authors (Kusumaningrum et al., 2003) have calculated TR
differently from Moore et al. (2003). As described above by PrezRodrguez 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 recovered by contact plate.
These authors calculated the TR for S. enteritidis, S. aureus and C. jejuni
from stainless steel surfaces to food (cucumber and chicken llet slices).
S. enteritidis TR data ranged from 10526% to 5018% in cucumber
where Cv is the level of contamination on salads; N is the level of microorganisms on contaminated chicken carcasses (CFU/cm2 carcass); and
TR1 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 stochastic, the authors selected normal distributions to describe the logtransformed transfer rates from one surface to another.
Chen, Jackson, Chea, and Schaffner (2001) quantied bacterial
cross-contamination rates during common food service tasks; for
this, they used E. aerogenes as surrogate for Salmonella. They calculated TR in an appropriate manner depending on the task evaluated. For
instance, to evaluate cross-contamination from chicken to hand, they
calculated 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 others
than normal distribution as best t in accordance to the Kolmogorov
Smirnov test. For example, transfer data from chicken to hand, from cutting board to lettuce and hand washing (reduction rate) obeyed to Beta
distribution; Weibull distribution was more adequate for modeling
transfer from hand to lettuce and from hand to spigot; lastly, Gamma
distribution was the best model for describing the transfer from spigot
to clean hand.
Mller, Nauta, Christensen, Dalgaad, and Hansen (2011) presented a cross contamination model of Salmonella in pork processing
during a small-scale grinding process. After evaluating three models,
the goodness-of-t indices applied (Root Mean sum of Square Errors
and Akaike Information Criterion) as well as two validation factors
(bias and accuracy factors) indicated that the best model was that assuming two environments inside the grinder: in one of them, food matrix is relatively loosely attached and is responsible for the fast transfer
to the minced meat, while in the second matrix the transfer occurs at a
slower rate. Fig. 1 is a graphic representation of the model. In this way,
after passing ve contaminated pork slices (108 cfu/slice) through
the grinder, the subsequent non-contaminated slices were contaminated at a descending rate as they were being grinded, presenting a long
tail region, similar to the thermal inactivation process.
The developed model satisfactorily predicted the observed behavior of Salmonella during its cross-contamination in the grinding of up
to 110 pork slices. The proposed model is an important tool to examine the effect of cross-contamination in quantitative microbial risk assessment investigations and might also be applied to various other
food processes where cross-contamination is involved.
More research is needed in relation to cross-contamination modeling. Identication and measurement of different factors affecting
cross-contamination events are crucial. Different tasks and hygiene
practices during food serving operations should be described in detail
Salmonella counts (log cfu/portion)
8
7
6
5
4
3
2
1
0
0
20
40
60
80
100
120
Portion number
Fig. 1. Transfer model (5 parameters) of Salmonella Typhimurium DT104 during grinding

of pork slices.
for experimental studies in terms of environmental conditions and

physiological state of Salmonella spp. Variability of transfer rates should
also be characterized by probability distributions, as it has been widely
recognized the great variability encountered during cross-contamination.
As more cross-contamination models become available, more accurate
exposure assessments and risk characterization will be developed.
Acknowledgments
This work was partly nanced by the Project of Excellence CTS3620 from the Andalusia Government, the project AGL 2008-03298/
ALI from the Spanish Science and Innovation Ministry, the European
project FP7-KBBE-2007-2A n 222738 from the VII Framework Programme and ERDF funding. The authors would also like to thank the
Plan Andaluz de Investigacin for a Research Staff Training grant.
FEDER also provided additional funding.
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Contents lists available at SciVerse ScienceDirect

Food Research International

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

is variable and may also be affected by human lifestyle and behavior,

E. Carrasco et al. / Food Research International 45 (2012) 545556

E. Carrasco et al. / Food Research International 45 (2012) 545556

from carcasses in the spray process can be insufcient if bacteria are

3.2. Other meats

E. Carrasco et al. / Food Research International 45 (2012) 545556

correspondingly, from cutting utensils were 100% genetically identical.

E. Carrasco et al. / Food Research International 45 (2012) 545556

properly protected public health as it allowed the sale of contaminated,

3.4. Low-moisture foods

Spray drying is a method of producing a dry powder from a liquid

E. Carrasco et al. / Food Research International 45 (2012) 545556

in the food processing and preparation environment through humans

E. Carrasco et al. / Food Research International 45 (2012) 545556

be removed during washing, diminishing transfer rates, it may not be

E. Carrasco et al. / Food Research International 45 (2012) 545556

Rubino, and Meng (1998) proposed a model of cross-contamination

slices, and from 94 42% to 32 9% in roasted chicken llets, depending

Cv N TR1 =100 TR2 =100

where Nr is the quantity of cells transferred to the receptor surface; TR

Salmonella counts (log cfu/portion)

E. Carrasco et al. / Food Research International 45 (2012) 545556

Fig. 1. Transfer model (5 parameters) of Salmonella Typhimurium DT104 during grinding

for experimental studies in terms of environmental conditions and

E. Carrasco et al. / Food Research International 45 (2012) 545556

Cliver, D. O. (2006). Cutting boards in Salmonella cross-contamination. Journal of AOAC

E. Carrasco et al. / Food Research International 45 (2012) 545556

E. Carrasco et al. / Food Research International 45 (2012) 545556

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