**6. References**

86 Salmonella – A Dangerous Foodborne Pathogen

such as seawater temperature, pH, salinity and dissolved oxygen are significant factors associated with the presence of *Salmonella* spp. In this study, seawater temperature was the only variable showing a linear positive effect on the presence of *Salmonella* in the sea, while

There are many factors such as temperature, salinity, sunlight, grazing by heterotrophic microorganisms affecting the survival of enteric bacteria in marine areas (*Sinton et al 2007:*  Harm, 1980, Gameson & Gould 1985, Jagger 1985, Rozen and Belkin 2001, Sinton 2005) Temperature also seemed to affect efficiently the abundance of indicator bacteria and *Salmonella* spp. in the study areas. *Salmonella* spp. positive samples were mostly recorded in the summer seasons and the indicator bacteria level was also higher during these periods compared to the other sampling seasons in 1998-2010. This situation is directly related to the increase of human activity, especially in coastal areas in summer seasons. However it also shows that despite the salinity stress, occurrences of indicator bacteria and *Salmonella* spp.

*C. gallina* and *D. trunculus* are two most common and abundant species in Turkish clam resources. Especially *C. gallina* is very important and valuable species, due to its great export potential, *C. gallina*, which has begun to be gathered since 1986 via mechanical dredge in

The mean values of bacterial contamination found in the 75 *R. venosa* samples under bacteriological analysis were between 15x10 and 24x103 and above. It is concluded that the area is under the influence of the waste products of dwellings and naval transportation

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. Because antibiotic resistance related to domestic waste waters is important for the ecosystem and also for human health, the resistance frequency of *Salmonella* spp. isolates to some beta-lactam antibiotics was investigated in this study. The antibiotic derivates which were found to be resistant to bacteria were different in different regions. This situation shows that pollution input and the usage rate of antibiotics have differences related to geographic regions. Further research will help towards setting limits on the prevalence of antibiotic-resistant bacteria and supporting the effectiveness of

It was reported that *Salmonella* spp. presence in marine waters is adequately predicted by total coliforms or fecal coliforms (Efstratiou et al. 2009). In this study, positive correlations were found between the presence of coliform bacteria (especially >103 cfu/100 ml) and occurrences of *Salmonella* spp. positive isolates. Efstratiou et al.( 2009) reported that the *E. coli* limits set by the EU Directive for defining "good" coastal bathing water quality (500 CFU100 ml−1) are much higher than the fecal coliform concentration which would best

The percentage distribution of the ratio values of Fecal Coliform to Fecal Streptococci in the surface water of the Aegean Sea and the relation of this ratio with the occurrence of *Salmonella* spp. was also investigated (Altuğ et al., 2007). The percentages of *Salmonella* spp. among total enteric bacteria were between 25% and 37%. Positive correlations were observed between the level of indicator bacteria and the presence of *Salmonella,* implying that *Salmonella* spp. occurrence is a part of anthropological pollution input in the investigated areas. The presence of isolates of *Salmonella* spp. in the marine environment is

the other parameters showed more complex nonlinear effects in the studied areas.

were possible under these conditions in the seawater.

(Altuğ and Güler 2002).

antimicrobial agents.

predict the absence of *Salmonella* spp.

Turkey, has great importance in terms of economy (Altuğ et. al., 2008).


The Occurrence of Salmonella in Various Marine Environments in Turkey 89

Lemarchand, K., Lebaron P. (2003). Occurrence of Salmonella spp. and Cryptosporidium

Lynch, E., Hobbie, J.E. (1988). *Principles of microbial behaviour in ecosystems*, Blackwell,

Martinez-Urtaza, M. Saco, J. de Novoa, Perez-Pieiro, P., Peiteado, J., Lozano-Leon, A. (2004).

Martinez, M. E., Egea, F., Castro, D., Morinigo, M.A., Romero, P., Borrego, J.J. (1991).

MacDonell, M.T., Singleton, F. L., Hood, M.A. (1982). Diluent composition for use of API

MacFaddin, J.F. (1980). Biochemical Tests for Identification of Medical Bacteria, 2nd ed.,

Mill, A., Schlacher, T., Katouli, M. (2006). Tidal and longitudinal variation of faecal indicator

Munro, P.M., Gauthier, M.J., Breittmayer, V.A., Bongiovanni, J. (1989). Influence of some

National Comittee for Clinical Laboratory Standards. (1999). (NCCLS) Performance

Noble, R.T., Moore, D.F., Leecaster, M.K., McGee, M.K., Weisberg, S.B. (2003). Comparison

Pincus, D. H. (2005). Encyclopedia of Rapid Microbiological Methods Volume 1. Ed. Miller,

Polo, F., Figueras, M., Inza, I., Sala, J., Fleisher, J., Guarro, J. (1998). Relationship between

Prüss, A. (1998). Review of epidemiological studies on health effects from exposure to

Rozen, Y., Belkin, S. (2001). Survival of enteric bacteria in seawater. *FEMS Microbiology* 

Ruiz, G. M., Rawlings, T. K., Dobbs, F. C., Drake, L. A., Mullady T., Huq, A., Colwell, R. R. (2000). Global spread of microorganisms by ships. *Nature*, 408, 49-50.

ocean recreational water quality testing, *Water Research*, 37, 1637–1643. Nunes, A.J.P., Parsons, G. J. (1998). Dynamics of tropical coastal aquaculture systems and

*Biomérieux*, Inc. Hazelwood, MO USA PDA/DHI 1-32.

recreational water, *International Journal of Epidemiology,* 27, 1.

*Microbiology Letters.* 218, 203-209.

*Microbiology* 70, 2089–2097.

*Microbiology,* 44, 423–427.

*Bulletin*, 52, 881–891.

M100-S9, Wayne.

27–37.

Williams and Wilkins, Baltimore MD. 249-260.

*enviromental microbiology*, 55, 2017- 2014.

*Microbiology Letters,* 160, 253–256.

*Reviews,* 25, 513–529.

*USA* 54, 612–618.

Oxford,

spp. in a French coastal watershed: relationship with fecal indicators. *FEMS* 

Influence of environmental factors and human activity on the presence of *Salmonella* serovars in a marine environment. *Journal of Applied and Environmental* 

Accumulation and depuration of pathogenic and indicator microorganisms by the bivalve mollusc, Chamelea gallina L, under laboratory. *Journal of Food Protection.* 

20E in characterizing marine and estuarine bacteria. *Applied Environmental* 

bacteria in an estuarine creek in southeast Queensland, Australia. *Marine Pollution* 

osmoregulaiton processes on starvation of *Escherichia coli* in seawater. *Applied and* 

standards for antimicrobial susceptibility testing, Ninth Informational Supplement,

of total coliform, fecal coliform, and enterococcus bacterial indicator response for

the consequences to waste production. *Journal of the World Aquaculture Society*, 29,

M. J. Chapter 1 *Microbial Identification using the Biomérieux VITEK*® *2 System* 

presence of *Salmonella* and indicators of faecal pollution in aquatic habitats, *FEMS* 


Borrego, J.J., Figueras, M.J. (1997). Microbiological quality of natural waters. *Microbiol. SEM*

Bradd J. Haley Dana J. Cole, Erin K. Lipp. (2009). Distribution, Diversity, and Seasonality of

Carlucci, A. F., Scarpino, P. V., Pramer, D. (1960). Evaluation of factors affecting survival of

Cook, D. W., Burkhardt, W. III, A. DePaola, S. A., McCarthy K., Calci, R. (2001). *Molluscan* 

Dionisio, L.P.C., Joao, M., Ferreiro, V.S., Fidalgo, M.L., Garcia Rosado, M.E., Borrego, J.J.

Efstratiou, M.A., Mavridou, A., Richardson, C. (2009). Prediction of Salmonella in seawater

EPA, (1986*). U.S.Environmental Protection Agency. Ambient Water Quality Criteria for* 

FDA. (1998). *Bacterial analytical manual*, 8th ed. Revision A. AOAC International,

Feldhusen, F. (2000). The role of seafood in bacterial foodborne diseases. *Microbes Infection,* 2,

Gameson, A. L. H., Gould, D. J. (1985). Bacterial mortality, Part 2. In Investigations of

Graeber, I., Montenegro, M.A., Bunge, C., Boettcher, U. (1995). Molecular marker analysis of

Harm, W. (1980). Biological Effects of Ultraviolet Radiation. Cambridge University Press,

Huss, H. H., Reilly, A., Embarek, P.K.B. (2000). Prevention and control of hazards in

Inal, T., Bese, M., Ugur, M., Tantas, A. (1979). Izmir seaport waters and Salmonella

José,V.F. (1996). Bivalves e a segurança do consumidor. Dissertação de Mestrado. Ciência

Kamizoulis, G., Saliba, L. (2004). Development of coastal recreational water quality standards in the Mediterranean, *Environment International,* 30, 841–854.

contamination. *Research Bulletin TUBITAK,* Ankara 293, 20. Jagger, J. (1985). Solar-UV Actions on Living Cells. Praeger, New York, USA.

changes and challenges. *FEMS Microbiology Reviews* 26, 111– 112.

Waterborne Salmonellae in a Rural Watershed. *Applied and Environmental* 

*Escherichia coli* in sea water studies with heat and filter-sterilized sea water. *Applied* 

*shellfish: oyster, mussels and clams.* In: F. P. Downes & K. Ito, editors. Compendium of methods for the microbiological examination of foods. 4th ed. APHA,

(2000). Occurrence of Salmonella spp in estuarine and coastal waters of Portugal.

by total an faecal coliforms and Enterococci. *Marine Pollution Bulletin*, 58, 201- 205.Egli, T., Koster, W., Meile, L. (2002). Pathogenic microbes in water and food:

*Bacteria-1986*. U.S.Environmental Protection Agency, EPA-440/5-84-002,

sewage discharges to some British coastal waters. WRc Techn. Rep. TR 222. WRc

*Salmonella typhimurium* from surface water, humans, and animals. *Europan Journal* 

13, 413–426.

Washington.

Washington, D.C

Washington, DC.

1651–1660.

*Microbiology*, 75, 5, 1248–1255.

*Antonie van Leewenhoek*. 78, 99–106.

Environment, Medmenham, UK.

seafood. *Food Control,* 11, 149–156.

Ambiental, São Paulo, USP.

*Epidemioogy.* 11, 325-33.

London, England.

*Microbiology.* 5, 9, 400–404.


**5** 

*Turkey* 

İlkan Ali Olgunoğlu *University of Adiyaman Vocational School of Kahta* 

*Salmonella* **in Fish and Fishery Products** 

With more than 30.000 known species, sh form the biggest group in the animal kingdom that is used for the production of animal-based foods. About 700 of these species are commercially shed and used for food production. Further, some 100 crustacean and 100 molluscan species (for example mussels, snails and cephalopods) are processed as food for humans in fish industry (Oehlenschläger & Rehbein, 2009). However, some fishery product is processed in a modern fish industry which is a technologically advanced and complicated industry in line with any other food industry, and with the same risk of product being

The vast majority of outbreaks of food-related illness are due to pathogenic microorganisms, rather than to chemical or physical contaminants. As they are generally undetectable by the unaided human senses (i.e.they do not usually cause colour changes or produce off-flavours or taints in the food) and they are capable of rapid growth under favourable storage conditions (Lelieveld et al. 2003). The United States Centers for Disease Control and Prevention reported that fish and shellfish account for 5% of the individual cases and 10% of all foodborne illness outbreaks, with most of the outbreaks resulting from the consumption

*Salmonella* is responsible for more than 40.000 cases of food-borne illness every year. The incidence of *Salmonella* infections has risen dramatically since the 1980s, leading to high medical costs, a loss of wages for workers who become ill, and a loss of productivity for the companies whose workers do become ill. In all, these financial losses can cost more than \$3.6 billion each year. *Salmonella* infections have long been a concern to scientists, doctors, and the U.S. Food and Drug Administration (FDA) (Brands, 2006). *Salmonella* is causing a public health problem associated with fish and fishery products. A monitoring of *Salmonella* has been suggested as a measure of fish quality. Also, risk management decisions should take into account the whole food chain from primary production to consumption, and should be implemented in the context of appropriate food safety infrastructures, for instance regulatory enforcement, food product tracing and traceability systems. In the fish processing chain managing risks should be based on scientific knowledge of the microbiological hazards and the understanding of the primary production, processing and manufacturing technologies and handling during food preparation, storage and transport, retail and catering (Popovic et al., 2010). Their presence in fish and fishery product is therefore seen as

a sign of poor standards of process hygiene and sanitation (Dalsgaard, 1998).

contaminated with pathogenic organisms (Huss, 1994).

of raw molluscan shellfish (Flick, 2008).

**1. Introduction** 

