**3.** *Salmonella* **in foods**

*Salmonella* spp. are the most common pathogenic bacteria associated with a variety of foods. Although myriad foods can serve as *Salmonella* sources, meat and meat products, poultry and poultry products, and dairy products are significant sources of foodborne pathogen infections in humans. Presence of *Salmonella* spp. in fresh raw products can vary widely (Harris et al., 2003). Frequency usually ranges from 1 to 10 %, depending on a range of factors including organism, farming and/or food production practices, and geographical factors (Harris et al., 2003). Research on *Salmonella* frequency in different countries is extensive, and *Salmonella* serotypes have been isolated in a variety of foods (Table 1). Poultry and egg products have long been recognized as an important *Salmonella* source (Skov et al., 1999); in fact, contaminated poultry, eggs and dairy products are probably the most common cause of human Salmonellosis worldwide (Herikstad et al., 2002). *Salmonella* can contaminate eggs on the shell or internally, and egg shells are much more frequently contaminated than the white/yolk. Furthermore, egg surface contamination is associated with many different serotypes, while infection of the white/yolk is primarily associated with *S*. Enteritidis (Table 1).

Poultry and poultry products are a common foodborne illness vector. Poultry can carry some *Salmonella* serovars without any outwards signs or symptoms of disease. *Salmonella*  can be introduced to a flock via multiple environmental sources, such as feed, water, rodents or contact with other poultry. The gastrointestinal tract of one or more birds may harbor *Salmonella*-and, if damaged during slaughter, may contaminate other carcasses. Crosscontamination can also occur from a *Salmonella*-positive flock or contaminated slaughter equipment to the carcasses of a *Salmonella*-free flock, as well as via handling of raw poultry during food preparation. Sufficient heating will eliminate *Salmonella* from contaminated poultry and poultry products.

Pasteurization effectively kills *Salmonella* in milk, but consumption of unpasteurized milk and milk products is a well documented risk factor for salmonellosis in humans.

The Role of Foods in *Salmonella* Infections 25

Country Food Serotypes Reference

Infantis

Bongor

Japan Imported Seafood Weltevreden Asai et al., 2008 Iran Raw poultry Enteritidis, Baibouknown Jalali et al., 2008

monophasic

Australia Retail Raw Meats Typhimuriuam, Infantis Phillips et al.,

Turkey Chicken Infantis Cetinkaya et al.,

Hadar,

Brazil Poultry meat ND Reiter et al.,

Ireland Retail pork Typhimurium Prendergast

Kentucky, Heidelberg,

Typhimurium, Choleraesuis, Gallinarum, Anatum , Agona, Edinburg,

Enteritidis, Typhi, Pullorum,

Typhimurium, Agona, Thompson, Montevideo, C1

bars and retailers ND Atanassova

Albany, Typhimurium

Infantis, Typhimurium, Enteritidis, Brandenberg, 4,5,12:-:-, 4,12:-:-, 4:-:2, 6,7:k:-

Kentucky, Hadar, Indiana, Infantis, Enteritidis,

Heidelberg, Orion,

Mbandaka,

London, Havana, Anatum,

Berrang et al.,

et al., 2009

Quiroz-Santiago et al, 2009

Orozco et al.,

2008

2008

2008

2007

2007

et al., 2008

Van et al., 2007

Wong et al., 2007

Bucher et al.,

2009

Typhimurium, Typhimurium var. 5-; 4,5,12:I: -; Schwarzengrund, Montevideo, Ohio, Kiambu, Betha, Thompson; 4,12:I: -; Senftenberg, Enteritidis, Worthington, Hadar; 8,(20): - :z6; Mbandaka; 8,(20):I: -;

United States Broiler carcasses

Parsley, coriander, cauliflower, lettuce,

spinach

Tomatoes

Mexico Hydroponic

Germany Sushi from sushi

Vietnam Pork, beef, chicken, Shellfish

New Zealand Uncooked retail meats

Canada Chicken nuggets

and strips

Republic of

Mexico


Inadequately pasteurized milk as well as post-pasteurization contamination of milk and milk products are recognized sources of human disease.

Inadequately pasteurized milk as well as post-pasteurization contamination of milk and

Country Food Serotypes Reference United States Papaya Agona CDC, 2011 United States Cantaloupe Panama CDC, 2011

Muenster

Mexico Chili peppers ND Castro-Rosas

China Beef Enteritidis, Typhimurium Yang et al., 2010 Iran Chicken Thompson Dallal et al.,

Brazil Poultry carcass Enteritidis Freitas et al.,

Mexico Zucchini squash ND Castro-Rosas

Bangladesh Chick egg Typhimurium Hasan et al.,

Typhimurium,

*diarizonae*

*S. bongori*, S. *enterica* subsp.

Gallinarum, Panama

Brancaster, Goelzau, Kentucky, Hadar, Agona, Poona, Bandia, Bessi, Brunei, Hull, Istanbul, Javiana, Magherafelt, Molade, Oxford, Rubislaw, Tamale,

and Zanzibar

Kentucky, Hadar, Enteritidis, Braenderup, Montevideo, Thompson, Mbandaka, Agona

Anatum, Cerro, Dublin, Infantis, Kentucky, Mbdanka, Montevideo,

Newport, Mbandaka, Braenderup, Cerro, Muenchen, I:4,12:i:-

Amsterdam, Anatum, Montevideo, Brandenburg, Give, Kiambu, Nyborg, Bredeney, Typhimurium, Meleagridis, Kentucky

Van Kessel et al., 2011

Brillhart & Joens, 2011

et al., 2011

Torres-Vitela et al., 2011

2010

2010

2010

2009

Betancor et al., 2010

et al., 2010

Dione et al., 2009

Lestari et al.,

2009

Arslan & Eyi,

milk products are recognized sources of human disease.

United States Raw milk

Mexico Cheese

Turkey Retail Meat

Senegal

Products

Uruguay Poultry and Eggs Enteritidis, Derby,

Chicken Carcasses and Street-Vended Restaurants

from retail stores

United States Chicken carcasses

United States Oysters served raw

in restaurants


The Role of Foods in *Salmonella* Infections 27

We studied the frequencies of coliform bacteria (CB), thermotolerant coliforms (TC), *Escherichia coli* and *Salmonella* in zucchini squash (Castro-Rosas et al., 2010) and jalapeño and serrano peppers (Castro-Rosas et al., 2011). In zucchini squash, infection was detected in 100% of cases for CB, 70% for TC, 62% for *E. coli* and 10% for *Salmonella* spp. Concentration range was 3.8 to 7.4 log CFU/fruit for CB, and <3 to 1000 MPN/fruit for TC and *E. coli*. In serrano chili peppers infection was detected in 100% of cases for CB, 90% for TC, 50% for *E. coli* and 10% for *Salmonella* spp., while in jalapeño peppers frequencies were 100% for CB, 86% for TC, 32% for *E. coli* and 12% for *Salmonella* spp. All *Salmonella*-positive samples were also *E. coli*-positive. For CB, concentration range was 3.8 to 7.9 log CFU/serrano sample and 5.3 to 8.2 log CFU/jalapeño sample, whereas TC and *E. coli* concentrations ranged from <3 to 1100 MPN/serrano and jalapeño samples (Castro-Rosas, et al., 2010; 2011). As is the case with other vegetables consumed raw, zucchini squash, and jalapeño and serrano peppers are potential pathogen vehicles. Sources of pathogenic microorganisms in the field include soil, water, wild and domestic animals, drift and runoff from adjacent farms and manure (Beuchat, 2006; Natvig, 2002). Once harvested and used in food preparation, zucchini squash, jalapeño and serrano peppers are all potential sources of cross contamination with

Salmonellosis infection is an increasing problem and recent salmonellosis outbreaks have been associated with a wider variety of vegetables, even those that were not previously considered to imply a risk (e.g. jalapeño peppers; CDC, 2008a*)*. Data on frequency of incidence for pathogenic bacteria such as *Salmonella* are clearly needed for a wide variety of vegetables which are consumed raw. Preventing contamination is vital to avoiding salmonellosis outbreaks, but it is also important to understand the potential survival and growth rates of *Salmonella* on specific substrates such as zucchini, jalapeño and serrano peppers. Our results suggest that both chili peppers and zucchini squash may be significant

*Salmonella* has been isolated from fruits and vegetables such as cantaloupes, melons, tomatoes, lettuce, and especially alfalfa sprouts (Table 1). These products can become contaminated by several routes, therefore, consumers need to thoroughly wash all fresh foods before consumption to reduce risk of illness from fruits and vegetables. With alfalfa sprouts and lettuce, washing can merely drive bacteria deeper into the lower layers of lettuce leaves or sprouts, so the outside three layers of lettuce leaves need to be removed

Finally, consumer awareness needs to be promoted that many other foods may carry *Salmonella*, even those not normally thought to be contamination sources. Most users know to handle raw chicken properly and to cook chicken and eggs thoroughly to avoid *Salmonella* contamination. But foods such as almonds, pecans and chocolate can also harbor *Salmonella*. In addition, as the food chain becomes completely global and highly complex, and international trade continues to develop, new foods will surely be linked to

Disease surveillance reports frequently identify poultry, meat and milk products as the main vehicles in salmonellosis outbreaks. However, in recent years foodborne illness outbreaks have been increasingly associated with greater consumption of fresh fruits and vegetables (CDC, 2009). *Salmonella* is responsible for frequent foodborne illness outbreaks in the

factors contributing to the endemicity of *Salmonella* in Mexico.

and sprouts need to separated before careful washing.

pathogenic microorganisms.

salmonellosis outbreaks.

**4.** *Salmonella* **outbreaks** 


ND: not determined

Table 1. *Salmonella* serotypes identified in different foods and countries.

*Salmonella* spp. have been isolated from filter feeder seafood species such as oysters, clams and mussels (Table 1). These species acquire their food from the water flowing through their bodies, but also ingest anything else that happens to be in the water. If oceans, lakes and bays are contaminated with fecal matter, the shellfish living in them intake any waterborne pathogens and harbor them in their intestines. The highest potential infection risk is from oysters, since they are most often eaten raw on the half shell. A single raw oyster can contain enough bacteria to cause an infection in the human gut. Mussels and clams pose less of a risk because they are usually steamed, killing *Salmonella* and most other bacteria. The above constitute only a sampling of the principal ways in which animals and animal products cause lead to *Salmonella* infection.

Fresh produce as a possible disease vehicle has become the focus of increasing concern since contamination can occur at multiple steps along the food chain. *Salmonella* is among the most worrisome of the pathogenic microorganisms found in minimally-processed fresh produce (CDC, 2009; Heaton et al., 2008). Bacterial contamination of whole or minimallyprocessed fresh vegetables can occur at different processing stages (i.e. harvest, trimming, washing, slicing, soaking, dehydrating, blending and/or packaging) (Harris el al., 2003). Produce can also be contaminated with human or animal source pathogens (Beuchat, 2006; Natvig, 2002). *Salmonella* spp. are the most common etiological agent associated with fresh produce related infection in the United States (US). A range of fresh fruit and vegetable products have been implicated in *Salmonella* infection, most frequently lettuce, sprouted seeds, melons and tomatoes (Table 2). *Salmonella* spp. are often isolated during routine surveys of produce such as lettuce, cauliflower, sprouts, mustard cress, endive and spinach (Thunberg et al., 2002); mushrooms (Doran et al., 2005); bean sprouts, alfalfa sprouts, unpasteurized juices and fresh salad fruits and vegetables (CDC, 2009).

In Mexico, *Salmonella* has been isolated from raw vegetables such as alfalfa sprouts *(*Castro-Rosas and Escartín, 1999*)*, parsley, cilantro, cauliflower, lettuce and spinach (Quiroz-Santiago et al., 2009). It has also been identified from zucchini squash (*Cucurbita pepo*) (Castro-Rosas et al., 2010), and jalapeño and serrano chili peppers (Castro-Rosas et al., 2011). In 2008, 600,000 tons of zucchini were produced in Mexico: 419,768 tons for the domestic market (SAGARPA, 2010) and approximately 200,000 tons for the US market (USDA, 2010). This squash is most commonly consumed cooked in Mexico and other countries, but can be eaten raw (e.g. green salads). In 2009, over 1,981,500 tons of chili peppers were produced in Mexico; of these 613,308 tons were jalapeño peppers and 216,617 tons were serrano peppers *(*SAGARPA, 2010*).* These peppers are most commonly consumed raw [e.g. green salads or Mexican sauce (salsa)], both in Mexico and other countries.

Country Food Serotypes Reference

United States Almonds 35 different serotypes Danyluk et al.,

*Salmonella* spp. have been isolated from filter feeder seafood species such as oysters, clams and mussels (Table 1). These species acquire their food from the water flowing through their bodies, but also ingest anything else that happens to be in the water. If oceans, lakes and bays are contaminated with fecal matter, the shellfish living in them intake any waterborne pathogens and harbor them in their intestines. The highest potential infection risk is from oysters, since they are most often eaten raw on the half shell. A single raw oyster can contain enough bacteria to cause an infection in the human gut. Mussels and clams pose less of a risk because they are usually steamed, killing *Salmonella* and most other bacteria. The above constitute only a sampling of the principal ways in which animals and animal products

Fresh produce as a possible disease vehicle has become the focus of increasing concern since contamination can occur at multiple steps along the food chain. *Salmonella* is among the most worrisome of the pathogenic microorganisms found in minimally-processed fresh produce (CDC, 2009; Heaton et al., 2008). Bacterial contamination of whole or minimallyprocessed fresh vegetables can occur at different processing stages (i.e. harvest, trimming, washing, slicing, soaking, dehydrating, blending and/or packaging) (Harris el al., 2003). Produce can also be contaminated with human or animal source pathogens (Beuchat, 2006; Natvig, 2002). *Salmonella* spp. are the most common etiological agent associated with fresh produce related infection in the United States (US). A range of fresh fruit and vegetable products have been implicated in *Salmonella* infection, most frequently lettuce, sprouted seeds, melons and tomatoes (Table 2). *Salmonella* spp. are often isolated during routine surveys of produce such as lettuce, cauliflower, sprouts, mustard cress, endive and spinach (Thunberg et al., 2002); mushrooms (Doran et al., 2005); bean sprouts, alfalfa sprouts,

In Mexico, *Salmonella* has been isolated from raw vegetables such as alfalfa sprouts *(*Castro-Rosas and Escartín, 1999*)*, parsley, cilantro, cauliflower, lettuce and spinach (Quiroz-Santiago et al., 2009). It has also been identified from zucchini squash (*Cucurbita pepo*) (Castro-Rosas et al., 2010), and jalapeño and serrano chili peppers (Castro-Rosas et al., 2011). In 2008, 600,000 tons of zucchini were produced in Mexico: 419,768 tons for the domestic market (SAGARPA, 2010) and approximately 200,000 tons for the US market (USDA, 2010). This squash is most commonly consumed cooked in Mexico and other countries, but can be eaten raw (e.g. green salads). In 2009, over 1,981,500 tons of chili peppers were produced in Mexico; of these 613,308 tons were jalapeño peppers and 216,617 tons were serrano peppers *(*SAGARPA, 2010*).* These peppers are most commonly consumed raw [e.g. green salads or

Table 1. *Salmonella* serotypes identified in different foods and countries.

unpasteurized juices and fresh salad fruits and vegetables (CDC, 2009).

Mexican sauce (salsa)], both in Mexico and other countries.

Biafra, Braenderup, Weltevreden

Tunung et al.,

2007

2007

Street food, fried chicken, kerabu jantung pisang, sambal fish, mix vegetables

Malaysia

ND: not determined

cause lead to *Salmonella* infection.

We studied the frequencies of coliform bacteria (CB), thermotolerant coliforms (TC), *Escherichia coli* and *Salmonella* in zucchini squash (Castro-Rosas et al., 2010) and jalapeño and serrano peppers (Castro-Rosas et al., 2011). In zucchini squash, infection was detected in 100% of cases for CB, 70% for TC, 62% for *E. coli* and 10% for *Salmonella* spp. Concentration range was 3.8 to 7.4 log CFU/fruit for CB, and <3 to 1000 MPN/fruit for TC and *E. coli*. In serrano chili peppers infection was detected in 100% of cases for CB, 90% for TC, 50% for *E. coli* and 10% for *Salmonella* spp., while in jalapeño peppers frequencies were 100% for CB, 86% for TC, 32% for *E. coli* and 12% for *Salmonella* spp. All *Salmonella*-positive samples were also *E. coli*-positive. For CB, concentration range was 3.8 to 7.9 log CFU/serrano sample and 5.3 to 8.2 log CFU/jalapeño sample, whereas TC and *E. coli* concentrations ranged from <3 to 1100 MPN/serrano and jalapeño samples (Castro-Rosas, et al., 2010; 2011). As is the case with other vegetables consumed raw, zucchini squash, and jalapeño and serrano peppers are potential pathogen vehicles. Sources of pathogenic microorganisms in the field include soil, water, wild and domestic animals, drift and runoff from adjacent farms and manure (Beuchat, 2006; Natvig, 2002). Once harvested and used in food preparation, zucchini squash, jalapeño and serrano peppers are all potential sources of cross contamination with pathogenic microorganisms.

Salmonellosis infection is an increasing problem and recent salmonellosis outbreaks have been associated with a wider variety of vegetables, even those that were not previously considered to imply a risk (e.g. jalapeño peppers; CDC, 2008a*)*. Data on frequency of incidence for pathogenic bacteria such as *Salmonella* are clearly needed for a wide variety of vegetables which are consumed raw. Preventing contamination is vital to avoiding salmonellosis outbreaks, but it is also important to understand the potential survival and growth rates of *Salmonella* on specific substrates such as zucchini, jalapeño and serrano peppers. Our results suggest that both chili peppers and zucchini squash may be significant factors contributing to the endemicity of *Salmonella* in Mexico.

*Salmonella* has been isolated from fruits and vegetables such as cantaloupes, melons, tomatoes, lettuce, and especially alfalfa sprouts (Table 1). These products can become contaminated by several routes, therefore, consumers need to thoroughly wash all fresh foods before consumption to reduce risk of illness from fruits and vegetables. With alfalfa sprouts and lettuce, washing can merely drive bacteria deeper into the lower layers of lettuce leaves or sprouts, so the outside three layers of lettuce leaves need to be removed and sprouts need to separated before careful washing.

Finally, consumer awareness needs to be promoted that many other foods may carry *Salmonella*, even those not normally thought to be contamination sources. Most users know to handle raw chicken properly and to cook chicken and eggs thoroughly to avoid *Salmonella* contamination. But foods such as almonds, pecans and chocolate can also harbor *Salmonella*. In addition, as the food chain becomes completely global and highly complex, and international trade continues to develop, new foods will surely be linked to salmonellosis outbreaks.
