**1. Introduction**

72 Salmonella – A Dangerous Foodborne Pathogen

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The occurrence and survival of enteric bacteria in marine ecosystems has been of interest to microbial ecology, sustainable usage of aquatic products, and the health of humans and the ecosystem (Barcina et al., 1986; Borrego and Figueras, 1997; Dionisio et al., 2000). Therefore, it is interesting to know and evaluate environmental factors that influence the occurrence of indicator bacteria and *Salmonella* spp. regarding sustainable and economical usage of aquatic products, ecosystem and human health.

The majority of bacteria present in domestic wastewater are comprised of saprophyte bacteria of faecal or terrestrial origin and pathogen bacteria such as *Salmonella, Shigella, Brucella*, *Mycobacterium*, *Escherichia coli*, *Leptospira, Campylobacter* and *Vibrio*. Furthermore, *Adenovirüs, Reovirüs, Rotavirüs* and *Hepatit* viruses as well as prozoons such as *Entamoeba histolytica, Giardia lamblia,* and *Cryptosporidium* may contaminate the sea by means of wastewater (Lynch and Hobbie 1988, Westwood 1994, Black 1996.)

*Salmonella* spp., one of the pathogenic bacteria which enter the sea environment as a result of anthropologic influences and particularly recreational use in coastal areas, continues to be a problem with regard to public health.

In order to define the source of *Salmonella* spp.*,* contamination strains isolated from seawater and rivers were studied by molecular marker methods. Their properties were compared with those of strains originating from possible sources of contamination such as sewage from humans, cattle, and treated sewage water used in watering plants (Graeber et al., 1995).

The perforation of *Salmonella* spp. into sea water is not only from terrestrial originated wastewater but also from ships' ballast water which is imported to and exported from ships to maintain their balance.

The movements of ballast waters, from one continent to another by ships, create a global distribution mechanism for pathogenic and antibiotic-resistant forms and it may be significant in the worldwide distribution of microorganisms, as well as for the epidemiology of waterborne diseases affecting plants and animals (Ruiz et al., 2000). At the same time, most of the pathogens sourcing from sewage have been found to be present in shellfish. Particularly in production areas which are under the heavy influence of contamination, the most frequently found pathogen in shellfish is *Salmonella* spp.

The Occurrence of Salmonella in Various Marine Environments in Turkey 75

the advances in technology, changes in food processing and packaging (Fedhusen 2000,

Because of their better survival in saline waters enterococci have been suggested to be better indicators of microbial risk in coastal and estuarine environments (Dionisio et al., 2000; Kamizoulis and Saliba, 2004; Noble et al., 2003; Polo et al., 1998; Prüss, 1998). Lemarchand and Lebaron (2003) have reported that considering the occurrence of *Salmonella* spp*.*, besides *Giardia* sp. and *Cryptosporidium* sp. and using changes of the levels of indicator organisms, ''higher microbiological risk'' and ''lower microbiological risk'' areas can be defined. Additionally, it was reported that fecal indicators do not exactly reflect the presence of pathogens such as *Salmonella* spp. in natural waters and that pathogens and indicators may have different behaviors in the aquatic environment (Lemarchand and Lebaron 2003).

Beta-lactam antibiotics are widely used for treatment of infections in the world. Domestic waste waters might be an important source of antibiotic-resistant *Enterobacteriaceae*. Resistances to clinically relevant antibiotics are widespread in aquatic bacteria, including potential human pathogens. Since antibiotic resistance related to domestic wastewaters is important for the ecosystem and also for human heath in the aquatic environments, the resistance frequency of some beta-lactam antibiotics to *Salmonella* spp. isolates were

In this study, the presence of *Salmonella* spp. and its relationship with primary hydrographic parameters and indicator organisms of bacterial pollution (total coliform, feacal coliforms) were investigated in the various marine areas of Turkey. The results were evaluated regarding sustainable and economical usage of aquatic products, the ecosystem and human

**1.3 The presence of** *Salmonella* **spp. and its relationship with indicator bacteria**  The presence of *Salmonella* spp. and its relationship with indicator bacteria can be variable according to the hydrodynamic characteristics and environmental factors of the studied areas. Some studies have reported that a relation between *Salmonella* spp. and faecal

bacterial-indicators was observed only rarely (Polo et al., 1998, 1999).

**1.4 Antibiotic resistance of** *Salmonella* **spp. in seawater** 

Fig. 1. Location of sampling sites in various marine areas of Turkey

Huss, et al., 2000, Egli et al., 2002).

investigated in this study.

#### **1.1 The presence of** *Salmonella* **spp. and its relationship with primary hydrographic parameters**

The presence of *Salmonella* and its relationship with primary hydrographic parameters (temperature, salinity, and dissolved oxygen) and indicator organisms in various marine environments were previously partly documented. It is known that the results of microbiological analysis were influenced by the dynamic structure of the aquatic environments. For instance, estuaries, lagoons, coastal and offshore environments are under variable environmental influences from each other. The hydrodynamic parameters of the estuary, in particular the flow rate, salinity gradient, and tidal cycles, were reported to be possible different relations between faecal-bacterial indicators and pathogens (Mill et al., 2006). Water temperature was positively associated with total *Salmonella* spp. levels. Bradd et. all (2009) reported that the levels of *Salmonella* spp. were correlated with average daily watershed rainfall for the 1 and 2 days preceding each sample collection. Similarly, environmental factors such as seasonal rainfall, salinity, and temperature were also correlated with *Salmonella* spp. abundance and diversity in the environment. (Bradd et. all 2009, Dionisio et al., 2000, Lemarchand and Lebaron, 2003; Martinez-Urtaza et al., 2004).

## **1.2 The presence of** *Salmonella* **spp. and its relationship with economically important aquatic products**

The presence of *Salmonella* spp. and its relationship with aquatic products with respect to food health is one of the important headlines of this issue. Providing quality safety of aquatic products from their catching to their marketing to consumers has great importance in terms of human health as well as economical and ecological aspects.

Shellfish are filter-feeding organisms and because their power of movement is limited, they feed on the organic substances which the sea brings. They can reflect bacterial changes around them because they are capable of accumulating bacteria in high concentrations and the accumulation rate can change depending on microbial species. It was reported that *Chamalea gallina* can accumulate *S. typhimurium*, *E. coli, Vibrio parahaemolyticus, Aeromonas hydrophyla, Streptococcus faecalis,* and *Staphylococcus aureus* in the first six hours in laboratory conditions (Martinez et al., 1991)*.* Nunes and Parsons (1998) reported that feeding oysters filter the surrounding water at a rate of 2 to 5 liter/hour eventually assimilating all the biotic and abiotic contaminants present in their environment. Due to the sensitivity of organisms and accumulation of environmental contamination, more bacterial contamination can be found in mussels than in the sea samples surrounding them. Because of these characteristics, shellfish have been accepted as bioindicators for detecting bacterial contamination in marine environments.

*Salmonella* spp. infections are one of the primary illnesses caused by the consumption of mussels. Bacterial pollution levels, associated with anthropological factors, are related to the occurrence of pathogenic bacteria in marine environments. *S. typhi* was isolated frequently in bivalve molluscs which were caught from a contaminated sea region. *Salmonella* spp*.* is one of the most important causes of human gastrointestinal diseases worldwide. Inal et al. (1979) have isolated *S. typhi* in shellfish taken from regions contaminated by slaughterhouse wastewater on the coast of the Aegean Sea, Turkey.

For these reasons, the consumption of shellfish has been generally associated with foodrelated infective diseases (Cook et al., 2001, Jose 1996). Food borne hazards are still of great concern for human health. Particularly the risks connected with shellfish and seafood consumption continue to be important both in developing and developed countries despite

**1.1 The presence of** *Salmonella* **spp. and its relationship with primary hydrographic** 

The presence of *Salmonella* and its relationship with primary hydrographic parameters (temperature, salinity, and dissolved oxygen) and indicator organisms in various marine environments were previously partly documented. It is known that the results of microbiological analysis were influenced by the dynamic structure of the aquatic environments. For instance, estuaries, lagoons, coastal and offshore environments are under variable environmental influences from each other. The hydrodynamic parameters of the estuary, in particular the flow rate, salinity gradient, and tidal cycles, were reported to be possible different relations between faecal-bacterial indicators and pathogens (Mill et al., 2006). Water temperature was positively associated with total *Salmonella* spp. levels. Bradd et. all (2009) reported that the levels of *Salmonella* spp. were correlated with average daily watershed rainfall for the 1 and 2 days preceding each sample collection. Similarly, environmental factors such as seasonal rainfall, salinity, and temperature were also correlated with *Salmonella* spp. abundance and diversity in the environment. (Bradd et. all 2009, Dionisio et al., 2000, Lemarchand and Lebaron, 2003; Martinez-Urtaza et al., 2004).

**1.2 The presence of** *Salmonella* **spp. and its relationship with economically important** 

The presence of *Salmonella* spp. and its relationship with aquatic products with respect to food health is one of the important headlines of this issue. Providing quality safety of aquatic products from their catching to their marketing to consumers has great importance

Shellfish are filter-feeding organisms and because their power of movement is limited, they feed on the organic substances which the sea brings. They can reflect bacterial changes around them because they are capable of accumulating bacteria in high concentrations and the accumulation rate can change depending on microbial species. It was reported that *Chamalea gallina* can accumulate *S. typhimurium*, *E. coli, Vibrio parahaemolyticus, Aeromonas hydrophyla, Streptococcus faecalis,* and *Staphylococcus aureus* in the first six hours in laboratory conditions (Martinez et al., 1991)*.* Nunes and Parsons (1998) reported that feeding oysters filter the surrounding water at a rate of 2 to 5 liter/hour eventually assimilating all the biotic and abiotic contaminants present in their environment. Due to the sensitivity of organisms and accumulation of environmental contamination, more bacterial contamination can be found in mussels than in the sea samples surrounding them. Because of these characteristics, shellfish have been accepted

in terms of human health as well as economical and ecological aspects.

as bioindicators for detecting bacterial contamination in marine environments.

wastewater on the coast of the Aegean Sea, Turkey.

*Salmonella* spp. infections are one of the primary illnesses caused by the consumption of mussels. Bacterial pollution levels, associated with anthropological factors, are related to the occurrence of pathogenic bacteria in marine environments. *S. typhi* was isolated frequently in bivalve molluscs which were caught from a contaminated sea region. *Salmonella* spp*.* is one of the most important causes of human gastrointestinal diseases worldwide. Inal et al. (1979) have isolated *S. typhi* in shellfish taken from regions contaminated by slaughterhouse

For these reasons, the consumption of shellfish has been generally associated with foodrelated infective diseases (Cook et al., 2001, Jose 1996). Food borne hazards are still of great concern for human health. Particularly the risks connected with shellfish and seafood consumption continue to be important both in developing and developed countries despite

**parameters** 

**aquatic products** 

the advances in technology, changes in food processing and packaging (Fedhusen 2000, Huss, et al., 2000, Egli et al., 2002).
