**2.** *Salmonella* **contamination sources in foods**

*Salmonella* is found in the environment and the gastrointestinal tract of wild and farmed animals. Animals may become infected with *Salmonella* through environmental contamination, other animals or contaminated feed. Both animals and humans can function as *Salmonella* reservoirs. In addition to sheep, goats, cattle, chickens and pigs, other animals which can become infected with *Salmonella* include geese and other birds, lizards and other reptiles, shellfish, and amphibians such as turtles. Indeed, most *Salmonella* contamination is of animal origin.

Among livestock production systems, *Salmonella* is more frequently isolated from poultry (chicken, turkey, duck, and pheasants) than from other animals (Freitas et al., 2010).

<sup>\*</sup> Corresponding Author

The Role of Foods in *Salmonella* Infections 23

Contamination with *Salmonella* strains from fresh produce apparently stems mainly from horticultural products. The principal contamination routes are probably use of animalsource organic fertilizers, irrigation with wastewater, humans and other animals (Islam et al., 2004; Natvig et al., 2002)*.* Presence of *Salmonella* in the environment may also lead to contamination in fruits and vegetables because *Salmonella* can survive for long periods in the environment. Multiple pathogenic microorganism sources occur during food packaging,

Studies of environmental sources of *Salmonella* contamination indicate that water is an important source, particularly irrigation water containing manure, wildlife feces or sewage effluents *(*Islam et al., 2004; Reilly et al., 1981*).* Insects or birds may also transmit *Salmonella*  to different foods. Flies are a known *Salmonella* carrier (Greenberg & Klowden, 1972), and can transmit various pathogenic microorganisms, as well as viruses such as polioviruses, coxsackie viruses, infectious hepatitis and anthrax (Ugbogu et al., 2006). Moore *et al.* (2003) mentioned the possibility that *Chironomus* genus insects were direct or indirect vectors of

In general, non-typhoid *Salmonella* is a persistent contamination hazard in all raw foods, including animals, poultry, wild birds, eggs, fruit, vegetables, dairy products, fish and

*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

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

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

distribution and marketing.

shellfish and cereals.

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

with *S*. Enteritidis (Table 1).

poultry and poultry products.

enteric bacteria contamination in water and food.

*Salmonella*-infected animals shed the microorganism in the feces from where it can spread into soil, water, crops and/or other animals. All *Salmonella* serotypes can be harbored in the gastrointestinal tract of livestock. The most common chain of events leading to this foodborne illness involves healthy carrier animals which subsequently transfer the pathogen to humans during production, handling and/or consumption.

*Salmonella* transmission to food processing plants and food production equipment is a serious public health issue. *Salmonella* can enter the food chain at any point: crop, farm, livestock feed, food manufacturing, processing and retailing (Wong et al., 2002). A number of workers handle animals during slaughter and processing, and contamination is possible when *Salmonella* or any other pathogen is present on the equipment or the workers' hands or clothing. Contamination most often occurs during specific slaughter stages: bleeding, skinning (or defeathering in poultry), evisceration (removal of chest and abdomen contents, also known as gutting) and pre-processing carcass handling. Cattle may be asymptomatically infected with *Salmonella* and beef can be contaminated during slaughter and processing via gastrointestinal content, and by milk during milking. *Salmonella* Dublin which is highly pathogenic to humans, is strongly associated with cattle (host-adapted). This makes cattle an important target for *Salmonella* control efforts.

*Salmonella* can frequently be isolated from most species of live poultry, such as broilers, turkeys, ducks and geese. Levels in poultry can vary depending on country, production system and the specific control measures in place. Contamination in poultry products can occur at several stages in the slaughter process, be it feces during evisceration or crosscontamination from contaminated products or surfaces on the production line. Particular contamination 'hot spots' in the poultry slaughter process include defeathering, evisceration and cutting; chilling in a water bath reduces the *Salmonella* load but may in turn facilitate cross-contamination (Corry *et al*., 2002; Fluckey *et al*., 2003; Northcutt *et al*., 2003).

Pork and pork products are increasingly recognized as important sources of human salmonellosis (Nielsen and Wegener, 1997). *Salmonella* colonizes pigs on the farm, and pork is then contaminated during slaughter or subsequent processing. Control of *Salmonella* in pork can be implemented on the farm, at slaughter and during processing. Pre-harvest control consists of monitoring *Salmonella* at the herd level, and implementing *Salmonella*  reduction measures in infected herds through hygiene, animal separation, feeding strategy and strict control of *Salmonella* in the breeder and growing-finishing pig supply chain.

Until recently, most human *Salmonellosis* cases have been caused by contaminated food animals, but in recent years an array of new food vehicles in foodborne disease transmission has been identified. Foods previously thought to be safe are now considered to be hazardous. These new food vehicles share several features. Contamination typically occurs early in the production process, rather than just before consumption. Consumer preferences and the globalized food market result in ingredients from many countries being combined in a single product, making it difficult to trace the specific contamination source. Many foods also have fewer barriers to microbial growth, such as added salt, sugar or preservatives. Their consequent short shelf life means they are often eaten or discarded by the time an outbreak is recognized. Under these circumstances, efforts to prevent contamination at the source are very important. Fresh produce such as fruits and vegetables have gained attention as transmission vehicles since contamination can occur at any one of the multiple steps in the processing chain (Bouchrif et al., 2009). Factors influencing the rise in salmonellosis outbreaks linked to vegetables include changes in agricultural practices and eating habits, as well as greater worldwide commerce in fresh produce (Collins, 1997)*.*

*Salmonella*-infected animals shed the microorganism in the feces from where it can spread into soil, water, crops and/or other animals. All *Salmonella* serotypes can be harbored in the gastrointestinal tract of livestock. The most common chain of events leading to this foodborne illness involves healthy carrier animals which subsequently transfer the pathogen

*Salmonella* transmission to food processing plants and food production equipment is a serious public health issue. *Salmonella* can enter the food chain at any point: crop, farm, livestock feed, food manufacturing, processing and retailing (Wong et al., 2002). A number of workers handle animals during slaughter and processing, and contamination is possible when *Salmonella* or any other pathogen is present on the equipment or the workers' hands or clothing. Contamination most often occurs during specific slaughter stages: bleeding, skinning (or defeathering in poultry), evisceration (removal of chest and abdomen contents, also known as gutting) and pre-processing carcass handling. Cattle may be asymptomatically infected with *Salmonella* and beef can be contaminated during slaughter and processing via gastrointestinal content, and by milk during milking. *Salmonella* Dublin which is highly pathogenic to humans, is strongly associated with cattle (host-adapted). This

*Salmonella* can frequently be isolated from most species of live poultry, such as broilers, turkeys, ducks and geese. Levels in poultry can vary depending on country, production system and the specific control measures in place. Contamination in poultry products can occur at several stages in the slaughter process, be it feces during evisceration or crosscontamination from contaminated products or surfaces on the production line. Particular contamination 'hot spots' in the poultry slaughter process include defeathering, evisceration and cutting; chilling in a water bath reduces the *Salmonella* load but may in turn facilitate

Pork and pork products are increasingly recognized as important sources of human salmonellosis (Nielsen and Wegener, 1997). *Salmonella* colonizes pigs on the farm, and pork is then contaminated during slaughter or subsequent processing. Control of *Salmonella* in pork can be implemented on the farm, at slaughter and during processing. Pre-harvest control consists of monitoring *Salmonella* at the herd level, and implementing *Salmonella*  reduction measures in infected herds through hygiene, animal separation, feeding strategy and strict control of *Salmonella* in the breeder and growing-finishing pig supply chain. Until recently, most human *Salmonellosis* cases have been caused by contaminated food animals, but in recent years an array of new food vehicles in foodborne disease transmission has been identified. Foods previously thought to be safe are now considered to be hazardous. These new food vehicles share several features. Contamination typically occurs early in the production process, rather than just before consumption. Consumer preferences and the globalized food market result in ingredients from many countries being combined in a single product, making it difficult to trace the specific contamination source. Many foods also have fewer barriers to microbial growth, such as added salt, sugar or preservatives. Their consequent short shelf life means they are often eaten or discarded by the time an outbreak is recognized. Under these circumstances, efforts to prevent contamination at the source are very important. Fresh produce such as fruits and vegetables have gained attention as transmission vehicles since contamination can occur at any one of the multiple steps in the processing chain (Bouchrif et al., 2009). Factors influencing the rise in salmonellosis outbreaks linked to vegetables include changes in agricultural practices and eating habits, as well as greater worldwide commerce in fresh produce (Collins, 1997)*.*

cross-contamination (Corry *et al*., 2002; Fluckey *et al*., 2003; Northcutt *et al*., 2003).

to humans during production, handling and/or consumption.

makes cattle an important target for *Salmonella* control efforts.

Contamination with *Salmonella* strains from fresh produce apparently stems mainly from horticultural products. The principal contamination routes are probably use of animalsource organic fertilizers, irrigation with wastewater, humans and other animals (Islam et al., 2004; Natvig et al., 2002)*.* Presence of *Salmonella* in the environment may also lead to contamination in fruits and vegetables because *Salmonella* can survive for long periods in the environment. Multiple pathogenic microorganism sources occur during food packaging, distribution and marketing.

Studies of environmental sources of *Salmonella* contamination indicate that water is an important source, particularly irrigation water containing manure, wildlife feces or sewage effluents *(*Islam et al., 2004; Reilly et al., 1981*).* Insects or birds may also transmit *Salmonella*  to different foods. Flies are a known *Salmonella* carrier (Greenberg & Klowden, 1972), and can transmit various pathogenic microorganisms, as well as viruses such as polioviruses, coxsackie viruses, infectious hepatitis and anthrax (Ugbogu et al., 2006). Moore *et al.* (2003) mentioned the possibility that *Chironomus* genus insects were direct or indirect vectors of enteric bacteria contamination in water and food.

In general, non-typhoid *Salmonella* is a persistent contamination hazard in all raw foods, including animals, poultry, wild birds, eggs, fruit, vegetables, dairy products, fish and shellfish and cereals.
