Food Research International 45 (2012) 587–602

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Food Research International
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / f o o d r e s


Salmonella in surface and drinking water: Occurrence and water-mediated transmission
Caterina Levantesi a,⁎, Lucia Bonadonna b, Rossella Briancesco b, Elisabeth Grohmann c, Simon Toze d, Valter Tandoi a

Water Research Institute, CNR, via Salaria km 29, 300-00015 Monterotondo, Rome, Italy Department of Environment and Primary Prevention, Hygiene of Internal Water Unit, ISS, viale Regina Elena 299-00161, Rome, Italy Department of Infectious Diseases, University Medical Center Freiburg, Hugstetter Strasse 55, 79106 Freiburg, Germany d CSIRO EcoSciences Precinct, Dutton Park 41 Boggo Road, Dutton Park, QLD 4102, Australia
b c

a r t i c l e

i n f o

a b s t r a c t
Salmonella is one of the leading causes of intestinal illness all over the world as well as the etiological agent of more severe systemic diseases such as typhoid and paratyphoid fevers. While water is known to be a common vehicle for the transmission of typhoidal Salmonella serovars, non-typhoidal salmonellae are mainly known as foodborne pathogens. This paper provides a brief review of the last ten years of peer reviewed publications on the prevalence of Salmonella in natural freshwaters and drinking waters, and on the relevance of these sources for Salmonella dissemination. In industrialized countries, Salmonella was rarely reported in water-borne outbreaks despite it being frequently detected in surface waters including recreational waters and waters used for irrigation or as a drinking water source. Consistent contamination with irrigation waters has been shown to be a common route of crop contamination in produces related Salmonella outbreaks. Multiple drug resistant (MDR) Salmonella strains, that represent an increased hazard for human health and that may contribute to the dissemination of drug resistances were also detected in surface water in developed countries. Surface runoff was shown to play a main role as driver of Salmonella load in surface waters. Accordingly, analysis of serovars indicated a mixed human and animal origin of Salmonella contribution to surface waters, emphasizing the role of wild life animals in water contamination. Data relating to Salmonella prevalence in surface and drinking water in developing countries are quite rare. Nevertheless, data on waterborne outbreaks as well as case control studies investigating the risk factors for endemic typhoid fever confirmed the relevance of water as source for the transmission of this disease. In addition epidemiological studies and Salmonella surveys, consistently provided an undeniable evidence of the relevance of MDR Salmonella Typhi strains in water-borne typhoid fever in developing countries. © 2011 Elsevier Ltd. All rights reserved.

Article history: Received 16 March 2011 Accepted 23 June 2011 Keywords: Water-borne outbreaks Salmonella Typhoid fever Surface water Multiple drug resistance Drinking water

Contents 1. 2. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Water-borne Salmonella infections and control strategies . . . . . . . . . . . . . . 2.1. Developing countries . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Developed countries . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Control strategies to prevent Salmonella drinking water related transmission . Role of contaminated waters in Salmonella foodborne outbreaks . . . . . . . . . . Salmonella prevalence, diversity in surface, drinking water and groundwater . . . . 4.1. Surface waters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Diversity of Salmonella strains isolated from surface waters . . . . . . . . . 4.3. Drinking water and groundwater . . . . . . . . . . . . . . . . . . . . . Salmonella survival and monitoring in water environment . . . . . . . . . . . . . 5.1. Salmonella survival . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Conventional and alternative microbial indicators for Salmonella monitoring in . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . aquatic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 588 589 589 590 591 592 593 593 595 597 597 597 598

3. 4.


⁎ Corresponding author. Tel.: + 39 06 90672781; fax: + 39 06 90672787. E-mail address: (C. Levantesi). 0963-9969/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodres.2011.06.037

& Lipp. . Salmonella serovars have different host specificity. van Iersel. Tsuchihashi. Differently from other Salmonella serovars. diversity and survival of this enteric bacterium in the environment. . 2011. . . and subspecies can be found in a large variety of vertebrates. Liebana. due to its ability to colonize surfaces and replicate in biofilms of distribution system pipes (Jones & Bradshaw. . They are usually present in large numbers in raw sewage (10 3–10 4 CFU/L) and can still be present in wastewater effluent after advanced secondary treatment including coagulation. 2004. Kohoutová.588 C. . Cole. 2002. . . . Guo. enterica subspecies enterica is mainly associated to human and other warm blooded vertebrates. . . In some patients. .. . e. insects and algae were also found capable of harboring Salmonella and might be implicated in the transmission of this enteric pathogen (Byappanahalli et al. Martinez-Urtaza. Smith. Burton. non-typhoidal salmonellae. Wilkes et al. . . & Gerba. Currently over 2400 Salmonella serovars have been described but only about 50 serovars. 2005). the above reported characteristics suggest that water might be an important source for the transmission of all salmonellae. . . . are more frequently associated to foodborne than to waterborne transmission. . Natvig. . Garcia-Migura. . Traditionally members of the genus Salmonella are clustered in serovars according to their flagellar (h) and somatic (o) antigens. This issue is of particular concern in developing countries where the common use of untreated. Even though not common in developed countries. An increased knowledge on the prevalence. Enteric fevers. . sheep as well as wild birds (sea gull. calves. . . Gorski et al. 2009. . . 2010. . . & Roper. trough effective . 2009). . Schwartzbrod. . . 2003). 2002) and immune compromised HIV infected adults (Gordon. Cooperband. . . . As a consequence. standard disinfection procedures used in drinking water treatment processes are active against salmonellae (Cicmanec. 2005). Lhoutellier. . . Overall Salmonella spp. Literák.. Overall. Severe and invasive presentations of non-typhoidal salmonellosis in Africa are common in children with co-morbidities (Graham. . Plants. These zoonotic Salmonella serovars tend to cause acute but usually self-limiting gastroenteritis. . . . Martinez-Urtaza et al.. just like other enteric bacteria. 2011). enteric fevers remain an important and persistent health problem in less industrialized nations. these same serovars can cause severe systemic diseases such as osteomyelitis. . 1996). . Notably the emergence of MDR strains of Salmonella Enteriditis and Typhimurium was associated to the observed incidence of invasive salmonellosis (Gordon & Graham. . .. Overall. The growth of Salmonella in non-host environments such as wastewater sludge and compost has also been reported (Zaleski. However. & Pepper. elevated survival capacities in non-host environment have been reported for Salmonella (Winfield & Groisman. Salmonella is a ubiquitous enteric pathogen with a worldwide distribution that comprises a large number of serovars characterized by different host specificity and distribution. Lightfoot. Leclerc. Taxonomically the genus Salmonella comprises two species namely S. . . . 2002). . Bierosová. Ingham. . 2002). 1999. Ducray. pneumonia and meningitis (Pond. are common causes of infections in humans and warm blooded animals (Popoff. Levantesi et al. . Perez-Piñeiro. . estuarine as well as contaminated ground water (Haley. . the ubiquitous subtypes found in a number of animal species. pigeon) and reptiles can all be reservoirs of Salmonella (Dolejská. Levantesi et al. Zoonotic salmonellae are commonly described as foodborne pathogens. both typhoidal and non-typhoidal.. The increased frequency of MDR Salmonella strains in human infections is an emerging issue of major health concern (Lightfoot. 2008). 2004. . Introduction One third of the world's population live in countries with some level of water stress and water scarcity is expected to increase in the next few years due to increases in human population. filtration and disinfection (Maier. . . . contagious systemic diseases caused by the infection of the serovars Typhi and Paratyphi. 2004. all within the subspecies enterica. & Saco. . pigs. 1994) and sediment particles are believed to function as a micro ecological niche enhancing salmonellae survival in lakes (Chandran et al. Josephson. . poultry. 2004. 2008). & Odeyemi. . . Srikantiah et al. . . . . . . 1990. Salmonellae are frequently found in environmental samples. The species S. . . per capita consumption and the resulting impacts of human activity on the environment (Asano. In the aquatic environment this pathogen has been repeatedly detected in various types of natural waters such as rivers. . Wray & Wray. & Dei-Cas. . 2000. The availability of good quality water sources is therefore getting more and more limited and the impact of water-borne pathogens in human health is expected to be significant (Suresh & Smith. . arizonae. . 2006. & Beuchat. stools of infected persons are therefore the original source of contaminations for these pathogens. This microorganism can enter the aquatic environment directly with feces of infected humans or animals or indirectly. Ishii et al. . & Carr. . low quality water as drinking water sources together with inappropriate use and self-prescribing of antibiotics increase the risk of drug resistance and the probability of wide dissemination of resistant strains of high human health concern (Oluyege. together with a proper assessment. . . and cause different syndromes.g. . 2005). 2004. . the possible role of fecally contaminated waters in the dissemination of MDR Salmonella. . . . 2005) and the growth of Salmonella in water supplies is also considered possible. as well as antibiotic resistance genes though horizontal gene transfer is of great interest. 2009. . . . . diarizonae. . . . typhoid and paratyphoid fever are severe. Conclusions . 2005). On the basis of the clinical syndromes caused Salmonella are divided in to two distinct groups namely the typhoidal and nontyphoidal Salmonella serovars (Pond.. Tobias & Heinemeyer.. Dada. Typhi and Paratyphi are host adapted and can only infect humans. Chenn. . & Tchobanoglous. . drinking water as well as natural waters are known to be an important source for the transmission of these enteric microorganisms (Ashbolt. lakes. 2007). . . Salmonella. . 2004). Delgenès. 2003). 2004). 2009.. . . . . Beside humans. . Lynch et al. 2009. Brackett. Differently from typhoidal Salmonella strains. . . . enterica is further differentiated in to six subspecies (enterica. & Cízek. . . . . not only for the typhoid serovars. animal sources of Salmonella include pets. however.. 2008). is spread by the fecal–oral route of contamination. . . . / Food Research International 45 (2012) 587–602 6. Gerba. . farm animals and wild animals. . . Water contaminated with feces of human cases and carriers is one of the main vehicles of typhoid fever infections. Soil and sediment were also found to harbor salmonellae (Abdel-Monem & Dowidar. This microorganism is one of the leading causes of intestinal illness through the world as well as the etiological agent of more severe systemic diseases such as typhoid and paratyphoid fever (Pond. Leverenz. References . 2009. It is therefore critical to understand the relevance of natural and drinking water contribution to transmission of pathogenic microorganisms. . 2000). . . coastal waters. indica and houtenae) among which the S.. . . . salamae. however. 598 599 1. In addition to its widespread occurrence. 2001). Polo et al. enterica. . bongori and S. . Ingham. 2007). . via sewage discharge or agricultural land run off. . in 2003 an annual incidence of approximately 17 million cases of typhoid and paratyphoid fevers was reported worldwide (Kindhauser. Wéry. & Godon.. . . Pepper. . diverse geographic distribution. . Pond.

provide useful data on salmonellae water-borne disease outbreaks (Craun et al... varies in different countries. Ramakrishnan. Farooqui. Dale. MDR S. Tran et al. a short overview of the most relevant emerging issues which the scientific community is actually addressing in relation to Salmonella in water environments is given. Pakistan. Tran et al. 2009. 2009. Finally. Kirk. sourced from well water (Farooqui et al. 2004). 2007. Srikantiah et al. Dolmans. & Hunter. In the summer of 2002 during a 7week period. respectively.. Srikantiah et al. Initially epidemiological data on the watermediated transmission of Salmonella infections and on the possible strategies to control these diseases are described. (2009) reported the study of a community outbreak of typhoid fever associated with drinking water in a village close to Karachi. Villar. Lewis et al. 1999).. piped municipal drinking water (Bhunia et al. & Clements. 2001) clearly show the involvement of MDR typhoid strains in water-borne epidemics. 2003. 2009.. such as Communicable Disease Surveillance Centre (CDSC.. were in 6 (15%) of 41 Salmonella serovar Typhi isolates from patients.. In particular the importance of water environment in the transmission of drug resistant Salmonella strains and the possible role of water in fresh food contamination are described. typhoid fever . streptomycin. Sloan. Gasem. 2001.. sulfisoxazole. nalidixic acid. Typhi (Kim. Farooqui et al. Sharma. Dunn. 2001). 2005. 2009. 2005). Lewis et al. & Carpenter. 2009). and trimethoprim-sulfamethoxazole. 2005. Hutin. 2. Srikantiah et al.C. Smith et al.. 2007). Claudet. 2001.. Carere.. 2003. Farooqui et al. In the less industrialized area of the world. 1999). Microbiological testing confirmed the presence of MDR strains of Salmonella serovar Typhi in 100% of the well water samples and 65% of household water samples (Farooqui et al. chloramphenicol. Jodar.. (2007) and Tran et al. 1999) and unboiled spring water (Swaddiwudhipong & Kanlayanaphotporn. 2. 2009. 2007. 2006. 2009. Kim et al. 1999. Tran et al. In this respect the possible involvement of water in food contamination is also of great interest. Sharma et al.. and trimethoprim-sulfamethoxazole.. 2005. They found that multiple antimicrobial resistance to ampicillin. however surveillance systems in many European countries have also been judged incapable of detecting water-borne disease (Blasi. This paper provides a brief review of our understanding of the contribution of natural fresh water and drinking water as a route of Salmonella contamination. their fecal material and garbage. and survival in surface water and drinking water is summarized. Reports on typhoid and paratyphoid fever epidemics in Asia consistently indicate that contamination of drinking water.1.. 2008. associated with the consumption of municipal water. & Levy. This outbreak claimed three human lives and left more than 300 people infected within a one week. 2007. 2001. In Seramang city and the surrounding area (Indonesia).. Tajikistan. 2009. 2009). 2005. Beside scientific publications. Furthermore the use and the evaluation of alternative fecal indicators of water contamination for Salmonella monitoring in aquatic environment is reported... Very few or no publication from Africa and Central/Latin America. Sinclair. In the first half of the year 1997. typhoid and paratyphoid fevers occur both in epidemic and endemic form. Srikantiah et al. most of the papers (Kim. the case mortality rate of 1. (2005) indicated the use of untreated drinking water in Uzbekistan and unboiled surface water in Vietnam. Vollaard et al. Mermin et al. & Leder. 8901 cases of typhoid fever and 95 associated deaths were reported in Dushanbe. In particular the situation in developing countries is problematic due to the lack of laboratory facilities and the scarcity of economic resources. Swaddiwudhipong & Kanlayanaphotporn. 2003. Stanwell-Smith. The level and quality of water-borne disease surveillance data... A case–control study demonstrated that Salmonella Typhi infection was associated with drinking unboiled water or obtaining water from sources outside the house. In agreement with the studies relating to typhoid fever outbreaks.. 2010. Swaddiwudhipong & Kanlayanaphotporn. Pompa. reports of national surveillance systems.. 2010. Developing countries Literature data related to water-borne salmonellae in developing countries relate mostly the typhoid Salmonella serovars. Hall. peer reviewed scientific publications of the last ten years were reviewed. tetracycline. Most of the recent publications on typhoid and paratyphoid fever water-borne infections in developing countries are from the Asian continent (Bhunia et al. & Djokomoeljanto. Successively recent literature relating to Salmonella prevalence. Srikantiah et al. 2008. Swaddiwudhipong & Kanlayanaphotporn... Levantesi et al. diversity. Although 93% of the tested Salmonella serovar Typhi isolates from Dushanbe were resistant to antimicrobials commonly used for typhoid fever. United Kingdom) and Centers for Disease Control and Prevention and Environmental Protection Agency (CDC/EPA USA). Solomon. Hunter. 2007.. Mermin. 2003). 2001.214 inhabitants (Lewis et al. 2005). 2009. 27 were resistant to seven antibiotics. 2001. and remain a major public health problem (DeRoeck. Rizzuto. 2010. Andersson.. a town in Nepal with a population of 92. The infected people consumed water from a well that was the only available source of drinking water in the village. 2004).. In addition to this. equipment failure. Sharma et al. Lewis et al. Considering that limited scientific publications exist that report the presence of Salmonella in water when compared to reports of Salmonella in food. 2000) and the analysis of risk factors associated with endemic or sporadic Salmonella infections (Denno et al. 2009. Mermin et al.. / Food Research International 45 (2012) 587–602 589 surveillance and epidemiological studies. 2009. Bhunia et al.0% was rather low (Mermin et al. A total of 90% of the isolates were resistant to more than one antibiotic. & Gupte. (2007) also showed that MDR Salmonella Typhi strains were important in endemic typhoid fever in the Samarkand region of Uzbekistan.. Mermin et al. Keuter. Typhi were also found to be the etiological agent in a water-borne outbreak in a nonendemic community with otherwise good sanitation in Thailand (Swaddiwudhipong & Kanlayanaphotporn. and back-siphonage in the water distribution system led to contamination of the drinking water (Mermin et al. (1999) reported a massive epidemic of MDR typhoid fever in Dushanbe. 5963 cases of typhoid fever were reported in Bharatpur.. Vollaard et al. Kim et al.. Manickam. Furthermore recent consumption of antimicrobials (two weeks preceding illness) additionally increased the risk of infection (Srikantiah et al. Swaddiwudhipong & Kanlayanaphotporn. Epidemiological investigations revealed the gross contamination of the well with dead and decaying animal bodies. Morton. as a major risk factor for typhoid fever. & Kazmi. 2001) was the main source of outbreaks. Luxemburger et al. Kozlica. Gasem et al. however.. addressed the role of water as vehicle of Salmonella transmission in the last ten years. 2001). namely to ampicillin. This outbreak was the largest single-point source outbreak of MDR typhoid fever reported so far. The burden of typhoid fever worldwide is further compounded by the spread of multiple drug resistant S. 2007). 2005.. 2010. Srikantiah et al. Khan. & Funari. Water-borne Salmonella infections and control strategies Two different types of data are the most common available in respect to Salmonella water-mediated infections: the description of water-borne salmonella outbreaks (Berg. 2006). 2009. Cooper.. respectively. Lack of chlorination. Lynch et al.. in particular in the Indian subcontinent and South East Asia. of the relevance of the water environment in the transmission of Salmonella disease is desirable.. Taylor. 1999. The outbreak was traced with molecular epidemiological methods to a single source—the sole municipal water supply. Of 29 Salmonella serovar Typhi isolates tested. chloramphenicol. epidemiological studies on the risk factors for endemic and sporadic typhoid fevers in Asia confirmed the association between this disease and the use of poor quality water (Gasem et al. 2001. & Carpenter. Franklin et al.

2. Smith et al. namely scooping out water from containers instead of using piped water or water stored in a narrow mounted container at home. 1998) are risk factors for this disease. Finally.. Dickens. in collaboration with the EPA and with the Council of State and Territorial Epidemiologists. found that typhoid fever was the most common water-borne disease (39. and cholera. Nevertheless most of the recent risk factor studies showed that use of unsafe water was not the only risk factor associated with typhoid/paratyphoid fever thus indicating multiple routes of transmission for these diseases (Gasem et al. 2004). They observed that typhoid fever was mostly associated with high vapor pressure and the use of river and streams as drinking water. and Bankole (2009) investigated relationships between water-borne diseases. clustering of non-typhoidal Salmonella bacteraemia in the rainy season in Africa suggests that there is also a water-borne/water-associated transmission route (Suresh & Smith.04) of the pattern of waterborne diseases morbidity in the area (Oguntoke et al.2. Salmonella Typhi is a major cause of enteric disease.. 2004). & Tessema. (2006) compared the serovars and genotypes of non-typhoidal salmonellae isolates from children with bacteraemia. As in other developing countries. 2008).3%) in the area followed by bacillary dysentery and cholera. Newport and Weltervreden.. was associated with typhoid fever. flavored ice drinks (Black et al. In agreement with these observations was the report that prolonged survival of Salmonella in ice (Butler.. The real burden of typhoid fever in Africa is largely unknown because of the lack of comprehensive surveillance studies and credible measures of the disease incidence. the CDC. Vollaard et al. typhoid. forested regions and public tap drinking water were found to be negatively associated with typhoid fever. the widespread implementation of municipal water and sewage treatment systems in the second half of the 20th century has resulted in a dramatic decline in the incidence of waterborne typhoid fever (Lynch et al. comprising Typhimurium. According to the CDC data from 1971 to 2000. respectively. the habit of boiling water before consumption was declared by all the people surveyed. the study identified a significant clustering of diarrhea cases to two water extraction points which were of poor microbial quality and contained potential diarrhea-causing organisms including Salmonella (Bessong et al. (2004) showed that in Jakarta typhoid and paratyphoid fevers are associated with different routes of transmission. were the causes of water associated Salmonella outbreaks in the USA (Craun et al. Sharma et al. The Venda region. Oguntoke et al. 2006). Calderon.6% (P b 0. 2009.. In the USA since 1971.g. mainly associated with people returning from foreign travel to regions where these diseases are still much more common (Lynch et al. & Mintz. 2004). The spatial distribution of diarrhea and microbial quality of water for domestic uses in the Venda region (South Africa) were analyzed by GIS during an outbreak of diarrhea (Bessong. Additionally multivariate regression analysis showed that the percentage of residents applying inadequate domestic water treatment (mostly potash alum addition) explained 68. a rural area. nontyphoidal zoonotic Salmonella were the causes of 15 drinking-waterborne outbreaks which accounted for 6% of the total zoonotic waterborne outbreaks in the USA (Craun. Developed countries In contrast to what has been observed for the less industrialized nations.000 persons per year has been estimated for the whole continent with a highest value in South Africa (N 100/100. DuPont. & Warren.. most of the data on water-borne salmonellae in developed countries involve non-typhoidal Salmonella serovars. Bareilly.. In many industrialized countries. 2009.. 2010). However. Kariuki et al.. 2008). / Food Research International 45 (2012) 587–602 was associated with living in a house without water supply from the municipal network along with the use of low quality water for washing and drinking (Gasem et al. Mahmoud. Luby. 2009). 2008).. Sharma et al. Musekene. (2007) revealed that typhoid fever prevailed in the Mekong River Delta.590 C.000 cases/year) (Crump et al. 2004). Graham. Vollaard et al. 2004. In agreement with the hypothesized water mediated route of transmission about 50% of the analyzed waterborne diseases infections occurred in the heavy rain period (Oguntoke et al. Kariuki et al.. began a surveillance program to collect and report data of water-borne outbreaks. 2001). a mean incidence of 50 cases per 100. Even if typhoid fever can be considered an endemic disease in Africa very few studies relating to Salmonella Typhi waterborne transmission in this continent are available in the recent literature. Yoder et al.. 2009). Interestingly. 2008. Odiyo.. 2009). 2004). Using a stratified random-sampling approach.. 2006. 2004). Kozlica et al. In Nigeria.. is characterized by the lack of clean potable water and the inadequacy of sanitation (Obi et al. possibly explaining the lack of association between microbiological contamination of drinking water and typhoid fever. Potgieter et al. 1985). As revised by these authors. (2004) showed that fecally contaminated drinking water was not associated with typhoid and paratyphoid fevers in Jakarta Indonesia. 2009). most of these salmonellae outbreaks (11/15) were associated with community water systems and groundwater instead of surface water. 2006). (2009) showed that the unsafe use of water. Further analysis has shown that various Salmonella subspecies. Nevertheless. (2004) also showed that typhoid fever was significantly associated with consuming ice cubes and iced drinks highlighting this as a likely water mediated route of transmission... particularly in children (Crump. The importance of ice cubes as a potential source of typhoid infection is supported by other studies in which it was shown that consumption of ice cubes (Gasem et al. 1977. & Johnson. were mainly within and outside the household. Enteriditis. Nevertheless the sources and mode of transmission of non-typhoidal salmonellae in Africa are still unknown.. Life-threatening invasive disease outbreaks in children caused by MDR non-typhoidal salmonellae have been reported in several African countries (e. the health department and regulatory officials identified an outbreak of . morbidity patterns. & Craun. Aboderin. In a prospective study in Kenya. In many African countries MDR non-typhoidal salmonellae are reported to be the commonest cause of bacteraemia in children under 5 years (Gordon & Graham.. However. 2001. Even if they remain endemic in a few geographic regions (Rizzo et al. From 2000 to 2006 salmonellae were found very rarely or not at all in drinking waterborne outbreaks in USA (Blackburn et al. Javiana.. 2004. in Africa. Vollaard et al. drinking water source quality and water handling practices in Ibadan City. In contrast to this. On the contrary. typhoid and paratyphoid fever are now rare diseases. Liang et al. In August 2008. 2005). Using GIS to explore the epidemiological pattern across Vietnam by investigating the risk factors associated with shigellosis. 2001). and from home environmental samples. Oguntoke. 2009). Risk factors for typhoid and paratyphoid fevers. from family contacts. 1985) and ice creams (Luby et al.. in this study. Kelly-Hope et al. the use of untreated groundwater along with inadequate treatment of collected groundwater and distribution systems contamination were the most important deficiencies identified for causing outbreaks of enteric bacteria. two recent outbreaks indicated that water-borne salmonellae are still of health concern in cases of deficiency of water treatment or inadequate water supply systems in the USA (Berg. Salmonella isolates from family contacts showed the highest similarity to those of clinical cases indicating that human-to-human transmission route plays a major role in non-typhoidal salmonellae transmission in the area. Nevertheless.. 2002. Levantesi et al.. both test cases and control sources. In the same period. Vollaard et al. In Ibadan City Salmonella Typhi and Paratyphi were detected in the well waters and the microbial water quality was found to be positively correlated with the pattern of water-borne disease within the selected areas.

2005). Country specific review of water-borne outbreaks in Italy (Blasi et al. According to the complete surveillance data of Communicable Disease Surveillance Centre (CDSC). Salmonellae were found to have contaminated the public water system that supplies drinking water to the community. 2010. 2008. Education regarding the risk of drinking untreated surface water as well as promoting the use of boiled drinking water carried from home. Only one Salmonella water-borne outbreak related to recreational water exposure was recorded by the CDC between 1995 and 2005 (Levy. Schmidt. with respect to water source interventions (Arnold & Colford. 122 of which were laboratory-confirmed.. & Cairncross. The serovars Saintpaul. and one death. Alamosa's drinking water comes from deep artesian wells in an aquifer considered to be a protected groundwater source. 2. (2007) as practical intervention measures to reduce water related transmission of typhoid fever in Samarkand (Uzbekistan). Pond. Bartram. & Herwaldt. Taylor et al. associations between the use of private well as home drinking water sources and the use of septic systems for home wastewater disposal were also observed as potential sources of Salmonella infections. monographic water-borne outbreaks reports such as those of CDC/EPA. Roof collected rain water were involved in several other water-borne outbreaks by Salmonella in Australia (Franklin et al. 2010). 2007). On the contrary. Studies of the risk factors for typhoid and paratyphoid endemics and epidemics infections confirm that simple decentralized control strategies might be effective in the control of these diseases (Sharma et al. In contrast. Lochery. hence the development of primary care clinical treatment guidelines to reduce unnecessary antimicrobial exposure may efficiently decrease the risk of typhoid fever.[5]. 2005). safe water storage and behavioral changes are indicated as reliable options to directly target the most affected population and reduce water-borne disease burden through improved drinking water quality (Mintz. and consequently reduce human risk of infection. 2007). salmonellae were found to be the most common pathogen in drinking water-borne outbreaks from 2001 to 2007 (Dale et al. (2009) home chlorination of drinking water. Calderon.. Epidemiological estimates suggested that up to 1300 people may have been ill (Berg.. and drawing out water by tilting the container or using taps to avoid contamination may be effective practices to avoid spread of typhoid in west Bengal India. Ashbolt and Kirk (2006) conducted a case control study to investigate risk factors for sporadic Salmonella Mississippi infections in Tasmania (Australia) showing that the exposure to untreated drinking water was a risk factor for this disease. 2008). Clasen.. (2009) conducted a prospective case control study to investigate the possible association between sporadic childhood reportable enteric infections and different plausible exposures. self-sustaining decentralized approaches including point of use chemical and solar disinfection. Craun. which are well suited to prevent typhoid fever outbreaks due to the consumption of contaminated surface or drinking water. Srikantiah et al. Control strategies to prevent Salmonella drinking water related transmission As for other water-borne pathogens. Rabie. (2007) also suggested specific intervention strategies to reduce the increased risk linked to MDR typhoid strains. The most probable cause of the outbreak was a contamination of a ground-level water storage reservoir by animal feces that successively spread throughout the entire system. However because the surveillance system on communicable diseases in Italy is not planned to efficiently identify water-borne outbreaks. In the second reported case during March and April 2008. 1998. Infection with Salmonella was found to be strongly related to playing or swimming in natural water sources. In this respect. the use of narrow-mounted containers for safe water storage. in Australia contaminated tank and bore waters were identified as the origin of outbreaks. An untreated water supply was recognized as the source of infection. 2007). the city's drinking water was not chlorinated for disinfection but was historically in compliance with all health-based drinking water standards. Farooqui et al.... Levantesi et al. In Europe. commonly lacking piped water supply. In many industrialized countries. In Australia. outbreaks caused by microbial contamination of drinking water still result in substantial human and economic costs in these countries (Berg. the control strategies have to be elaborated and adopted on the basis of the water resource availability and the economic and developmental level of the country. Risebro et al. The reservoir was found to have several small cracks and holes that likely allowed the contamination source to enter. The identification of the causes outbreaks and the potential threats to water quality is necessary to formulate effective prevention strategies that will minimize the further onset of outbreaks and related costs. (2009) reported measures recently introduced by WHO that include solar disinfection.. Denno et al. recreational aquatic environments. salmonellae were implicated in outbreaks that occurred in Italy from 1998 to 2005.. Salmonella spp. which provides an internationally harmonized support to help countries develop rules and standards that are suitable to national and local circumstances (WHO. were identified as outbreak causes.12:i:– involving five persons in a rural community in Tennessee. 2008). According to the findings of Sharma et al. Fewtrell et al.. . the success of applied control strategies is confirmed by the small number of water-borne outbreaks caused by salmonellae. & Wegelin. both salt and fresh waters.C. Salmonella was never associated to water-borne outbreaks in England and Wales from 1992 to 2003 (Smith et al. Prior to the outbreak. Causes of water-borne outbreaks in developed countries have been extensively reviewed in recent publications (Craun et al. It was found that the water. boiling. 2009. was indicated by Srikantiah et al. 2007. subsp IIIb 61:i:z35. The outbreak resulted in 442 reported illnesses. which had been collected from a spring. the World Health Organization has developed Guidelines for Drinking Water Quality. Craun. Srikantiah et al.. Nevertheless. three recent reviews that used meta-analysis to evaluate the effect of water treatment at point of use on water quality and diarrhea reduction showed that point of use interventions more efficiently reduced diarrhea incidence. According to their results the use of antimicrobials two weeks before onset of typhoid fever was independently associated to this disease. For this purpose. / Food Research International 45 (2012) 587–602 591 Salmonella I 4. bleach addition. In addition. 2006) were recently published. had been stored in a small unprotected reservoir subject to contamination from runoff and wildlife (Kozlica et al. 2009). Roberts.. 2000) suggesting that appropriate preventive measures must be undertaken to avoid that the increased use of rainwater tanks may increase the risk of water-borne disease outbreaks (Franklin et al. an outbreak of water-borne disease associated with Salmonella struck the city of Alamosa in Colorado. Differently from what has been observed in the USA where Salmonella outbreaks were mostly related to contaminated community water systems. In developing countries. are not available because drinking water is defined as food and thus included in foodborne outbreaks reporting. 2009). were indicated as the most important risk factor for sporadic childhood Salmonella infections at three Washington state county health departments (Denno et al. were implicated in five of 10 observed drinking water-borne outbreaks and in an outbreak derived from a contaminated aquarium. Regarding the measures to reduce the occurrence of Salmonella in drinking water. different measures can be adopted to hinder the spread of Salmonella in water environment. 2006). 2008) and the UK (Smith et al. Typhimurium.. Bens. the number of reported cases do not represent an accurate clear estimation of the real situation (Blasi et al. and use of low cost ceramic filters. 2001). 2008). Muenchen and Para B bv java.3. 2009. 2007... These authors also highlighted that most of the exposures to untreated drinking water were recorded as exposure to water collected in rainwater collection tanks.

. 2009). & Matthews. inter alias. 2008... Different steps are selected in the treatment process in order to increase removal capability and normal fluctuations in performance can be compensated. In particular they found that disinfection deficiencies were associated with 75% of outbreaks due to bacterial. 2007). Risebro et al. 2008). which prioritizes the identification of key potential contamination or control points in the treatment and distribution system. Charpentier. 2007. 2008. Newport strain. and Ingram (2003) showed an increased count of microbial indicators on cantaloupe rinds after fruit washing and cooling in hydrocooler indicating that inadequately decontaminated water used in post harvesting produce processing can also be a sources of microbial contamination. Friedman. A wide spectrum of produce have been associated with salmonellae infections including tomatoes (Greene et al. which is combined with HACCP principles. & Reuhs. Yaron. Role of contaminated waters in Salmonella foodborne outbreaks In recent years.. 2002). The approach that has been proposed is the “Hazard Analysis Critical Control Points” (HACCP) approach. Gagliardi. The two approaches together constitute a water safety framework that is a basic structure to develop supply-specific water safety plans to ensure the production of high quality drinking water. 2011. In this way the likelihood that pathogens can enter the distribution system and reach consumers is minimized. that greater attention is needed to address and reduce the risk of outbreaks in groundwater supplied systems and in private water systems. 2006) establishes a risk targeted approach to identify those systems that may be most susceptible to fecal contamination and specifies corrective actions (Craun et al.. 2008). Franz.. (2007) found that contamination of source water and failure of water treatment accounted for more than 50% of the recorded outbreaks. Sivapalasingam et al. in the UK. Irrigation of fields with sewage contaminated waters and processing produce with Salmonella contaminated waters were also indicated as possible sources of contamination in an outbreak of S.. water and ultimately foodborne Salmonella infections (CDC. 2006) and in developing countries untreated wastewater is also commonly used to irrigate crops. 2009. were associated with eating tomatoes (Greene et al. in the irrigation pond demonstrate that if not properly addressed. the source of contamination can persist and cause continuous outbreaks (Greene et al. 2004). enterica strains have the ability to adhere to plant surfaces where they are able to survive for long periods and then grow (Gandhi. The S. serrano peppers (CDC. Nutt.. Mohle-Boetani et al.. two years apart. Unfortunately most of these reviews consider the enteric bacteria as a whole and specific deficiencies associated to salmonellae water-borne outbreaks could not be extrapolated. cantaloupe (CDC. Levantesi et al. (2003) suggested that hot and cool water treatment which allowed the internalization of Salmonella in the mangoes was the most likely source of contamination. (2010) showed. 2008). Sivapalasingam. 2002). The control is essentially carried out through application of process control measures.592 C. Islam et al.. in the water. & Craun. is the multi-barriers approach. 2004). 2010. Knox. & Weatherhead. Analyzing water-borne outbreaks of enteric diseases associated with EU public drinking water supplies (1990–2005). Golding. 2005). 2002. Newport outbreak strain was isolated. it allows operators and authorities to focus their resources on monitoring crucial points to detect and quickly correct any deviation from a correctly operating system.g... Contaminated irrigation and processing waters were indicated as possible sources of Salmonella contamination in several fresh produce outbreaks (CDC.. 2008. 2003). & Hirt. 2002. 2007. 2005). 2008). . the EPA's Ground Water Rule (USEPA. In their complete review of drinking water associated outbreaks in USA (1971–2006) Craun et al. 2010). Jalapeno and serrano peppers imported from Mexico were identified as the major sources of this outbreak. 2008. Zijlstra. the farm investigation took place many months after the outbreak had occurred (Sivapalasingam et al. This approach has already been successfully used by the food and beverage industry.. Schikora. In 2002 and 2005 two multistate outbreaks of S. Salmonella is the most common aetiological agents associated to fresh produce related infections (Heaton & Jones. & Ricke. Risebro et al. enterica serovar Typhimurium from water to plants was shown only to occur with highly contaminated irrigation water (Lapidot & Yaron.. Salmonella serovar Newport was also the etiological agent in a multistate outbreak linked to mango consumption in USA (Sivapalasingam et al. reports of Salmonella outbreaks related to fresh produce consumption have illustrated the likely relationships between salmonellae. Tran. Sivapalasingam et al. Among others Lapidot and Yaron (2009) demonstrated the ability of S. 2003). Pruitt. Additionally some S. 2004). 2008). Deering. 2004). Carreri.. van Gent-Pelzer. 2008). Newport outbreak strain. 3. Tomatoes causing of the outbreak were traced back to the eastern shore of Virginia where the S. 2007). For example. 2003).. (2005) analyzed 288 cases of drinking water related outbreaks in Canada from 1974 to 2001 showing that water treatment failure and contamination from wildlife were the causative factors most often cited in outbreak reports. 71% of irrigation water is obtained from surface waters which receive treated sewage effluent (Tyrrel.. Klerks. Millner. 2007. and in particular of Salmonella (Hanning. which are provided by the WHO Guidelines (WHO.. viral and mixed pathogen contamination (Risebro et al. & Tauxe. In agreement with this. caused by the same rare S. 2007... Notably this outbreak strain was isolated from the pond water used to irrigate tomato fields both in 2002 and 2005 (Greene et al. Cohen. 2003). 2008). Greene et al. Overall it is apparent that the diversity of causative factors of outbreaks in different countries requires different specific control actions. The implicated mangoes were traced back to a single Brazilian farm where mangoes were washed with contaminated water (Sivapalasingam et al. The capacity of this pathogen to become endophytic. Newport outbreak strain was no actually isolated from the Brazilian water samples however. 2007). 2008. 2008). thus increasing the risk of microbial contamination (Ashbolt. Mauer. 2005. Water is likely to be an important source of produce contamination in the field as well as in post harvested processing (Berger et al. Dale et al. The S.. lettuce (Takkinen et al. thus to invade internal plant parts has also been reported (e. enterica serovar Typhimurium to transfer from contaminated irrigation water in plant roots and then into the edible parts of mature parsley. Greene et al. Schuster et al. Sivapalasingam et al.. Water sources of varying microbiological quality are used for irrigation of produce worldwide. Poona infections in the USA associated with eating imported cantaloupe (CDC. 2009).. 2008). 2010). & Matthews. Another successful approach. and mango (Sivapalasingam et al. 2001. In 2008. Bennett. 2002. basil (Pezzoli et al. Three recently published reviews clearly summarized the current knowledge on the role of fresh produces as source for the transmission of human enteric pathogens (Berger et al. 2003). Schuster et al. Salmonellae are often isolated from produce samples in routine surveys (Thunberg. & van Bruggen. Heaton & Jones. Newport in USA. 2003). a large multistate outbreak of Salmonella Saintpaul associated with multiple raw produce items infected a total of 1442 people in the USA and Canada (CDC. However the transfer of S. / Food Research International 45 (2012) 587–602 Calderon. 2009. Sivapalasingam et al. It is now commonly accepted that fruit and vegetable consumption is a risk factor for infections with enteric pathogens (Heaton & Jones. Sivapalasingam et al. Analysis of the irrigation and processing water at this farm indicated the presence of Salmonella spp. The presence of the S. 2004).. Lapidot & Yaron. Saintpaul outbreak strain was isolated from samples of jalapeno pepper as well as of irrigation water at a Mexican farm suggesting a possible route of Salmonella contamination (CDC. Lester.

Sawant.. Finally López Cuevas et al. Schoon. Schets. Jokinen et al. and swine production (41.1%). 2010. Wilkes et al. Temporal and spatial variation of Salmonella frequencies were commonly observed in surface water (Bonadonna et al. 2004. 2007. crop/agriculture (50%). by environmental parameters such as temperature. 2011. / Food Research International 45 (2012) 587–602 593 Several studies have investigated the potential source of produce contamination in the supply chain both at the pre-harvested and postharvested stages.. 2010. & Paradiso. A summary of the available data on Salmonella prevalence in surface fresh waters sources is shown in Table 1. According to the epidemiological data. 2004. Salmonella prevalence in surface water and drinking water has not been uniformly investigated in different countries in recent papers. Espinoza-Medina et al. 2008. & Field. equipment) at a produce production farm in Texas... Surface waters A survey of recent studies showed an increasing interest over the last two years on the role of non-host habitats.. the highest frequencies were reported in watersheds that had been highly impacted by human activities (Bonadonna et al. The data provided in Table 1 confirms the ubiquitous nature of this enteric pathogen. 2009.. and for irrigation (e. 4. Surveys of Salmonella in fresh surface water environment were mainly performed in industrialized nations. Duffy et al. White. 2008. Wilkes et al.. & Lebaron. such as tomatoes. López Cuevas et al. 2010. & Gardner. 2010. 2009. 2009). in five farms in Sonora (Mexico) showing that irrigation water (23% of positive samples) and hands of workers packing cantaloupe (16.. 2005.. Walters. Castillo et al. Brisabois. Duffy et al. Goonetilleke.. 2009. 4.. Dolejská et al. 2010.. 2005). an important area for the production of crops exported in the USA. 2009). with associated potential health risks. the recently available data on the prevalence of antibiotic resistant Salmonella strains in surface and drinking water (Bhatta et al. Schriewer et al. 2009).. which might contribute to the dissemination of these MDR strains through susceptible populations. Meinersmann et al. 2010). in part. surveys of Salmonella contamination in water used for fresh produce irrigation and in food processing identified the possible involvement of these waters in fresh vegetable and fruit contamination (Castillo et al. (2009) recovered Salmonella in 39% of irrigation water samples in four different regions of the Culiacan valley (Sinaloa Mexico). (2004) identified the irrigation water source as a possible source of cantaloupe contamination. Jokinen et al. Till. diversity in surface. Jokinen et al.. Polo et al.. as source of drinking water (Till et al. 2010). water chemistry. (2006) evaluated the incidence of Salmonella contamination during cantaloupe production and processing. resistance to tetracyclines was observed in many of the Salmonella strains isolated which correlated with the use of these antibiotics to treat and control plant pathogens infections (López Cuevas et al. Also of all the studies listed in Table 1.. 2009.. & Pyle. Similar levels of Salmonella contamination were found in the cantaloupe from USA and from Mexico (Castillo et al. Lemarchand & Lebaron. These results.. Reports of Salmonella prevalence in drinking water were instead more frequently from developing nations reflecting the higher concern relating to the use of low quality drinking water in these countries. 2009. Patchanee et al. López Cuevas. 2010).g. 2011. Filetici.. 2009. Jyoti et al. 2006. 2010. However. & Chaidez Quiroz. Obi et al. Jyoti et al. Byappanahalli et al. 2010.. Gannon et al. 2010.7% of positive samples) were the most likely sources of Salmonella contamination. 2009). Positive correlations between rainfall events and Salmonella prevalence and/or diversity have been reported by many authors (Baudart.. and to predict its presence in different aquatic environments (Savichtcheva... Dolejská et al. Additionally. Salmonella contamination occurred in surface water used for recreational purposes (Till et al. Schriewer et al. van Wijnen. 2005. 2009. Gannon. 2010) to heavily impacted water sources (e. León Félix. peppers and cantaloupes (Castillo et al. Salmonellae were detected in different countries and in very diverse water sources. Levantesi et al. Wilkes et al. Huygens. McBride. Nusca. & de RodaHusman.. Espinoza-Medina et al. 2010). Bonadonna. Jokinen et al.. drinking water and groundwater Salmonella contaminated waters might contribute through direct ingestion of the water or via indirect contamination of fresh food to the transmission of this microorganism. 2008). Patchanee et al.. 2009).. parsley and cantaloupe) and environmental samples (water. Patchanee et al. Salmonella prevalence. 2008.. 2009.. 2007. 2003. ranging from pristine (e. in particular in Canada and North America. 2010. Particular attention was also addressed to the evaluation of available and new approaches to monitor sources of Salmonella contamination. the scientific community has mainly recently focused on the prevalence of this microorganism in impacted and non-impacted watersheds (Haley et al. 2008). 2006. 2009. Espinoza-Medina et al. Line. namely residential industrial (58. 2010.... Wilkes et al. Similarly. these authors observed similar prevalence of salmonellae in watersheds with diverse potential contamination sources. Ball.. 2004). Salmonella was only isolated from the irrigation water (16/25 isolates). Jyoti et al. (2010) showed that elevated frequencies of Salmonella were also found in a forestry watershed not influenced by human activities. 2010. such as surface water environments as natural reservoir and in the transmission of Salmonella and other enteric pathogens (Ahmed. Patchanee. Haley et al. which are supported by similar observations with respect to Salmonella contamination in . Molla. Patchanee et al. Lemarchand.. and solar radiation that influence survival and transport of the microorganism.. Other possible reasons include changes in pathogen loading due to enhanced shedding from human and animal host.. Okayama.. Meinersmann et al.. Notably. soil.. Jokinen et al..g. forestry (57... 2009.1.. 1999. Jokinen et al. Schijven...8%). 2004.. & Okabe... 2008. Jiménez Edeza. 2009). Patchanee et al. Meinersmann et al. 2009. 2010) or in geographical areas with a history of high salmonellosis cases (Haley et al. Taylor. 2009). Jokinen et al.. 2000.. Patchanee et al.. (2004) described an extensive survey of Salmonella contamination at cantaloupe production farms in South Texas (USA) and Colima State (Mexico)... 2004). 2007. 2003). 2010) consistently indicate that these aquatic environments are a reservoir of MDR strains. However by PFGE the Salmonella strains isolates from the irrigation water and equipment were shown to be different from the cantaloupe isolates (Duffy et al.. 2006. Meinersmann et al.. Till et al. or from enhanced flow of water from contaminated sources. 2008.C. As shown in Table 1.g. 2008) and low impacted water (e.. 2003. 2006.. This demonstrated wide distribution of salmonellae underlines that there is the potential for inadvertently using water contaminated with Salmonella. Wilkes et al... (2005) analyzed samples from fresh produce (orange. Salmonella was detected in irrigation waters used for different type of fresh produces items. only a few performed a quantitative assessment of Salmonella in environmental waters (Bonadonna et al. Duffy et al. 2009. Lugo-Melchor et al.7%). Notably. 2006.g. & Gebreyes. 2009). 2011. 2011. Byappanahalli et al. on the identification of the routes of salmonellae contamination (Gorski et al. Haley et al. 2006. despite the importance of the knowledge of Salmonella concentrations in water to evaluate the risk of water related infection. Lemarchand & Lebaron. Byappanahalli et al. the Salmonella detection frequencies were extremely variable in the investigated surface waters with detection rates ranging from 3 to 100%.. Overall. Haley et al. 2008. It is possible that variations in the occurrence of Salmonella in ambient water may be governed.. By repetitive sequence based PCR analysis Castillo et al. and on the influence of environmental factors on the spread of Salmonella in water (Haley et al. Oluyege et al. 2009. 2009. Haley et al. equipment (6/25 isolates) and washed cantaloupe (3/25 isolates). In general.

(2009) salmonellae's incidence was found to be positively correlated with tributary discharge values as well as with accumulative rainfall. In contrast. 2003. (2006) Obi et al. 2 years Czech 2 sampling sites. 14 month Australia 8 sampling sites. municipal.6% (216) 17. 12 months Canada 24 sampling sites. 2 year Canada 4 sampling sites. According to these results. Simental & Martinez-Urtaza. 2 years South Africa 8 sampling sites Canada 16–21 sampling sites. Barrusseau. 1 year Weekly sampling. 1986.002–0. (2004) Gannon et al. 15 month Japan 5 sampling sites. (2009) Haley et al. cow and pig farms Mixed: Urban/industrial comprising direct sewage discharge Animal and human activities.5% (342) 13% (186) 10 –10 CFU/100 mL 87% (8) 54% (86) 7% (143) 3% (32) 0. In contrast. Highly contaminated area at environmental risk.06–42. 2000.594 Table 1 Salmonella occurrence in surface waters. (2009) Byappanahalli et al. (2008) Schets et al. 5 months Mixed: Urban/industrial. 2008). agricultural Not described Country Canada Survey extent References Jokinen et al.4% (802) 102–105 MPN/100 mL 100% (10) 57% (14) 0.6% (17) 10% (725)e 53% (30) 10–10 MPN/100 mL 100% (N 300) 75% (375)g 5. 15% of river sample used for drinking water supply. the variable seasonal occurrence of Salmonella in aquatic environments reported in the recent literature was not consistent with the summer peak human and animal salmonellosis infection observed worldwide.8% (79) 10. Spatial differences in Salmonella prevalence in surface waters have also been reported in the recent literature (Bonadonna et al. the presence of this pathogen was positively correlated with water temperatures and rainfall events (1 or 2 days before sampling). 2008. (2008) reported an increase of the concentration of Salmonella during late winter in New Zealand at a site where birds and sheep were the major potential contamination source. Savichtcheva . Environmental samples including water and sediments (89%) and food (11%). Suresh & Smith.017 MPN/mL 42% (19) 16% (87) 2. (2009) Wilkes et al. Over the complete study period. 2006. surface runoff. Range of average monthly density. 1 day USA 4 sampling sites. Potgieter. (2010) Patchanee et al. Levantesi et al. (2009) Dolejská et al. Grabulos. 1 year Mexico Random sampling. including enhanced pathogen loading during storm events. dairy farming. (2008) Simental and MartinezUrtaza (2008) Till et al. Republic 1 year USA 6 sampling sites.3 MPN/L 79% (72) 4–15% (1600)c 75% (83) 3. indicated that increased pathogen load could be associated with rainfall events as one major environmental driver of Salmonella contamination in surface water environment.. 2 years New Zeland 25 sampling sites. the seasonal peak of Salmonella incidence in a Canadian watershed was observed in the fall (Wilkes et al. & Lebaron.g. (2003) Obi. (2010) Schriewer et al.. human and animal feces 9 sampling sites. 2 years India 8 sampling sites. sheep/pastoral. Only Haley et al. forestry undeveloped Mixed: WWTPs effluents. increased survival in the water environment at warm temperatures and increased host shedding in the warmer season might explain the Salmonella peak during the summer months. (2008) Savichtcheva et al. Till et al. coastal area and marine environment (Baudart. / Food Research International 45 (2012) 587–602 Dominant impact in the analyzed water Mainly influenced by rainfall runoff and drainage from agricultural land Mixed Mixed comprising untreated sewage of residential setup Swine production Residential/industrial Forestry Crop agriculture Not described Mixed: WWTPs effluents. According to Wilkes et al. 3 months Italy 8 sampling sites. Only found in canals and river. In agreement with this a positive correlation was reported in the literature between rainfall events and the incidence of Salmonella water related infections (e. 2 months USA numerous sampling sites. WWTP discharge agricultural Runoff from agricultural land and pastures. borehole River and irrigation water River River water River Urban Mixed: mainly forested and agricultural in a area with high incidence of salmonellosi mixed Mainly rural area Not described Mixed comprising WWTP discharge Mixed: birds. 2009) potentially reflecting enhanced livestock based fecal input during this period. Bessong. (2009) in a study of a watershed in Georgia USA found that Salmonella incidence peaked in the summer period. (2004) Bonadonna et al. the authors concluded that multiple environmental factors. 2004). Different percentage in different seasons. human and animal feces Mixed Italy Africa France qPCR quantification.5–36. Level and frequency positive Surface water samples % (total samples) 8. and Matsaung (2003) Lemarchand and Lebaron (2003) River water River water River water Four differently impacted watersheds systems River and estuaries Urban pond and tidal creeks Lake and river water Pond River watershed River and streams Small river Urban canals/river and recreational lakesd Stream water Puddles Rivers and lakes Fresh water recreational and water supply sites River and pond around Sapporo city Riverf River. (2010) Ahmed et al. (2010) Jyoti et al. urban sewage.. Lemarchand & Lebaron.4 CFU/L 100% (8) a b c d e f g 4 b 4 6 a C. 2 years USA 10 sampling sites. (2009) Meinersmann et al. Haddock & Malilay. 2 years 1 sampling site. (2011) Jokinen et al. Meinersmann et al. (2007) Bonadonna et al. 1 day Netherlands 8 sampling sites. 3 years USA 82 sampling sites.

Diversity of Salmonella strains isolated from surface waters All Salmonella serovars are considered as potential pathogens. MDR strains have been detected in surface water in developed countries (Dolejská et al. Diversity Common serovars (percentage Serovar number/ of total isolates) total isolates 11/29 Rubislaw (72. Soerenga. 2009. wastewater and marine coastal areas) showing a great diversity of Salmonella serovars. (2003) 35/413h Typhimurium (31.. Montevideo. et al. Tennessee. Resistance to the quinolone nalidixic acid. only seven of the isolates were resistant to any antimicrobials. Montevideo. Infantis. Newport. Antibiotic resistant Salmonella have also been detected in surface water from a pond in the north-eastern part of the Czech Republic as well as in birds. Oranieneburg. This difference might be explained by the very long period (5 years) of Salmonella monitoring described by Polo et al.4%) Infantis (5. (2006) Saint Paul. et al. Braenderup Czech Republic USA Dolejská et al. Liverpool. (2010) reported a higher frequency of salmonellae in surface waters that have marine influences while Bonadonna et al. II (8. Bullbay. Typhimurium Infantis.2.. Indiana. Schriewer et al. 2009). streptomycin. (2010) showed that swine production was a major source of antibiotic resistant Salmonella in water environments as all the Salmonella isolates from a swine production watershed had multiple resistances to antibiotics.. have been predominantly isolated from humans or animals (Popoff. A summary of recent available data is reported in Table 2. USA Haley et al. (2011) Patchanee et al. (2008) 3 11/23 45/92a 19/36 Newport Virchow Typhimurium Typhimurium (39%) Urbana Suberu Vejle Typhimurium (13. Enteriditis Vietnam Phan et al.z32:– Typhimurium. Typhimurium. 2008) or monitored highly contaminated watersheds (Bonadonna et al. et al. enterica subsp arizona (40. however. 2008). / Food Research International 45 (2012) 587–602 595 et al. Heidelberg..7%)b Newport (8. (2000) and Polo et al.. Coeln. The first comprehensive studies describing the diversity of Salmonella serovars in the aquatic environment were presented by Polo et al. Since then. Saint Paul. Antibiotic resistance was found in 12% of salmonellae isolated from the water and 28% of gull salmonellae. Canada Typhimurium.6%) Muenchen (14. Lexington. In particular. Kiambu.. Gaminara.3%) Bredeney (4. Schleissheim. Thompson. Meinersmann and co-workers investigated the prevalence of Salmonella and their antimicrobial resistance profile in a synoptic study of the Oconee River Basin. (1999). Table 2 Salmonella diversity in surface waters. the total number of serovars detected in the investigated aquatic environments ranged from 10 to 20 independently of the number of isolates or samples analyzed in the different studies. Iv40:z4.C. Dessau. observed that the highest concentration of this pathogen was associated to sampling points in densely populated areas and/or downstream of sewage effluents discharge sites. Livingstone. several works have provided further data on the different serovars present and on the possible sources of Salmonella contamination in surface water. Mbandaka. USA (Meinersmann et al.3%) Gaminara (18. and tetracycline was often detected in these Salmonella isolates. Lemarchand.. (2010) 13/197 Braenderup. Senftenberg.2%)c Rubislaw (13. 2007. Lemarchand..1%) Virchow Panama Newport Hadar Grumpensis France Baudart. (2009) concluded from these results that black-headed gulls can be important reservoirs of antibiotic resistant salmonellae.3%) Muenchen (8. I47:z4z23.III b. In contrast. Breda. (2009) 6/17 19/73 4. crop agriculture. et al. 2010). Augustenborg. Subsp. Furthermore. Water samples were obtained from 83 sites with Salmonella isolated from 62 of the samples.7%)b Bredeney (6. however. Paratyphi B. Mbandaka. Bareilly. Enteriditis.10:r:– Anatum Bardo Javiana Netherlands Schets et al. In comparison to the results of the initial studies by Baudart. Subsp.e Muenchen (20%) Rubislaw Hartford Give Others serovars Country Reference 12/104 Givea. Paratyphi B. a small river in north-eastern Georgia. or a residential/industrial area (Patchanee et al. Dolejská et al. black-headed gulls nesting in this pond (Dolejská et al. Schets et al. Only about 50 of these serovars. Patchanee et al.10:vt. Give.6%) 03. Lemarchand.2%) Derby (4. Mbandaka. Anatum. IV. (2000)). With the exception of few studies that analyzed a limited number of isolates (Dolejská et al. Information regarding the distribution and characteristics of Salmonella serovars present in the environment are essential in assessing the role of nonhost aquatic habitats in the diffusion of Salmonella subtypes of high human health concern. the identification of sourcespecific serovars might help future tracking of sources of Salmonella contamination events. Gaminara. USA Miami.1%) Montevideoe Enteritidis (50%)d. London. (1999) and Baudart. 2006). 2008. Derbyf..7%) Subsp.3%) Inverness (18. (2006) and Lemarchand and Lebaron (2003).4%)a I:11:r:–a Derby Anatum (18. Give (only serotypes detected also by other authors) Italy 03. (1999) and the reported increase in the numbers of serovars during flood events (10 of the 35 serovars were only isolated during the flood by Baudart. A total of 16% of water and 24% of gull samples yielded Salmonella.. Heidelberga. I4.7%) S. Both research groups analyzed a large number of isolates from different natural aquatic systems (river. Stanley. Lemarchand. Meinersmann et al. 2001). these latter consistent figures found that there was a low diversity of Salmonella serovars in the non-host water environment (Table 2).(5):b.. (2009) Meinersmann et al. (2008) Othmarschem. Other Mbandaka. Braenderup Jokinen et al. Ouakam. (2000).2%) Stanley (4. DJugu Mexico Simental and MartinezUrtaza (2008) Bonadonna et al. (2000) (continued on next page) . Patchanee et al.2%)c Mikawasima (6. 2010). Hadarg. Bovismorbificants. 2010). Bovismorbificants. 2009. antibiotic resistant strains were not detected from watersheds impacted by forestry. Schriewer et al.2%) Derby (16. Levantesi et al.

Among the 10 most frequent serovar reported in human salmonellosis in USA. All of these results indicate that wild animals can be one of the major sources of Salmonella contamination in the environment. 2009. 2009).. As shown in Table 2. 2009. serovars comparison in feces and water samples indicated that other animals found in the watershed were not contributing to the Salmonella contamination in the Oldmann river watershed (Jokinen et al. (2011) compared the serovars detected in the Oldman river watershed with those present in sewage (human source) and in animal feces as potential source of Salmonella contamination in the investigated area. was dominant in this same water system. et al. Bredney. (2011) could only detect the serovar Rubislaw in the Oldman river watershed (Alberta. S. An increase of knowledge on how the Salmonella genotypes and phenotypes are related to different potential contamination sources is essential. enterica subspecies arizonae (40% of isolates) in the Little River rural watershed (Georgia. One relevant fact that can be noted is that the clinical serovars that were common or dominant in the studied geographic areas. (2010). Typhimurium and the monophasic types 6. Typhoid Salmonella serovars Typhi and Paratyphi A were only detected in surface waters in developing countries where the disease is endemic (Bhatta et al.g. enterica serovars of high public health concern (e. 2010). Hahn.. The serovars detected in the water samples.g. Patchanee et al. USA).. greater detections in the summer period.z15. but. This indicates that the Salmonella population in water environments is influenced by the incidence of human infections in the local area.. Infantis. Peaks of Salmonella diversity were observed to be associated to a specific locations (e. wild birds and other wild life have been identified as source of Salmonella water-borne outbreaks in different countries (Angulo et al. 2010) suggesting that human sewage was not the sole or main source of contamination in these habitats. Schuster et al. .8:–:e. 2009. Jokinen et al. Levantesi et al. Nevertheless. Patchanee et al. since a limited number of fecal samples of wild birds was analyzed. was only detected in wild bird feces. Montevideo Newport. Salmonella genotypic and phenotypic diversity was analyzed and compared in differently impacted watersheds: swine-production. residential/industrial. Patchanee et al. (2010).596 Table 2 (continued) Diversity Common serovars (percentage Serovar number/ of total isolates) total isolates 44/316h Enteriditis Virchow Hadar Infantis Typhimurium Goldcoast Ohio Others serovars C. 2011. In contrary. 2005. S. Contamination sources and environmental factors were also shown to in fl uence serovar abundance.g. As previously noted.. Oluyege et al. Gaminara is mostly associated to wild animals. These authors conclude that source tracking may be possible in these environments. 2006. The common assumption that livestock production is one of the main sources of surface water contamination by enteric bacteria such as Salmonella has not been fully confirmed by recent literature data.. Give. 2000) and Italy (Bonadonna et al. Patchanee et al. Salmonella Rubislaw. 2009.. Typhimurium) were detected in all the reported studies. black-headed gulls were identified as an important reservoir of antibiotic resistant Salmonella contamination in a pond in Czech Republic (Dolejská et al. (2010) also showed that Salmonella serovar Gaminara. and seasons (e. used pulsed-field gel electrophoresis PFGE genotyping coupled with serotyping techniques for tracking Salmonella contamination in four watersheds in North Carolina (USA). 2009).n. (2011) that can be used for the suggestion of appropriate control strategies in impacted catchments and water sheds. Give and I:11:r:–) were also detected in feces or sewage samples. Patchanee et al. were also isolated from wildlife feces. Only found in pigs in Czech Republic. Dominant cause of salmonellosis in human and animal in Czech Republic.... and Gorski et al. valuable information has been generated by the comprehensive work of Jokinen et al. and Forstner (2008) S. (2011).1% of samples) from a forestry watershed not impacted by livestock was described by Patchanee et al. 1997. 2010). has been detected in surface waters in France (Baudart.. residential/industrial. 2007. although very rare. In agreement with this. Jokinen et al. 2011. however (Haley et al. Common clinical serotypes in the analyzed geographical area. Muenchen... Enteriditis. Only four serovars isolated from water (Rubislaw... Lemarchand. Dolejská et al. (1999) a b c d e f g h Also isolated from human and/or animal feces. Percentage of Salmonella-positive samples. Haley et al. In agreement with this. however. urban/industrial impacted watershed. Understanding the relative contribution of different possible contamination routes on Salmonella introduction in surface waters is a necessary precursor for the selection of specific control strategies. 2009. S. (2011) investigated the incidence and diversity of salmonellae in a major produce region of California. Haley et al. Gorski et al. According to the dominance of the S. Rose. forestry and crop agriculture was compared showing that isolates from the swine-production watershed were distinctly different from other isolates both in their genotypes and serovars. Only found in human in Czech Republic. This suggested that there was a specific source of contamination for this watershed. 2010). Haley et al. 2000).. However. Canada) and in the feces of wild birds.. 2006). Jokinen et al. High frequency of Salmonella (57. In this context. / Food Research International 45 (2012) 587–602 Country Reference Spain Polo et al. all the strains isolated from wildlife were distinguishable from those isolated from water. 2010). Heidelberg.. The resulting Salmonella genotypic and phenotypic diversity in differently impacted watersheds: swine-production. cattle and wildlife feces.. As part of the study they also analyzed serovars and genotypes (PFGE) of Salmonella strains isolated from water. In particular the serovars Anatum and Bredney were only found in this watershed. 2009). 2010). According to Gaertner. Haley et al. Jokinen et al. the most common serovar in the water samples. Nevertheless. Patchanee et al. Clinical serovars were not always dominant isolates in the studies of aquatic environment. most of these serovars spanned a broad host range and thus it was not possible to identify the single contamination sources. Taylor et al.8:d:– and 6.. forestry and crop agriculture (Patchanee et al. Salmonella Paratyphi B.. According to PFGE patterns. The authors also showed that Salmonella strains isolated from residential/industrial and forestry were genotypically related and suggested that there was a potential cross contamination between these watersheds. it was not possible to understand the real contribution of these birds on the water contamination with Salmonella. while it was neither detected in the analyzed sewage (human contamination source) nor in feces of domestic animals. some near matches indicated that crow and coyotes were potential sources for water contamination.. the spectra of Salmonella serovars observed by various authors in surface water showed a mixed human/animal origin (Dolejská et al. were usually also detected in the surface water samples (Bonadonna et al. soil/sediment and preharvested lettuce/spinach. (2009) suggested that local reptile population may be a significant source of the total Salmonella in this surface water.. Infantis. Only the most common serovars isolated from fresh water samples are reported. S. Patchanee et al.

In one of the few studies reported on Salmonella in groundwater. 2009) further highlighting the risks from Salmonella in roof harvested rain water. Drinking water and groundwater A summary of recent available publications on Salmonella occurrence in groundwater and drinking water. (2010) India Jyoti et al.g. It should be noted. & Fayer. (2006) South Potgieter et al. samples water collected from standpipes of boreholes and from surface water used as drinking water source were always found to be positive for Salmonella (Potgieter et al. (2007). Africa (2005) human host-specific strains Typhi and Paratyphi A. 4.. MDR resistance to more than 4 antibiotics was observed in most of these isolates (Oluyege et al. Groundwater can be contaminated by a wide range of pathogens. f % of positive sampling sites.C. (2009) Nepal Bhatta et al.. In addition. risks posed by enteric viruses (e.3%d 14% (300) 100%(8)e 16% (18)f 100% Roof harvested rainwatera Drinking water supply Well and borehole waterc Surface waterc Tap water of urban water supply system Borehole standpipes water and surface waterc Well and tap waterg Borehole standpipes water and surface waterc Country Reference Australia Ahmed et al. mainly South Africa and Nigeria (Akinyemi. 2004. Contamination of groundwater by microbial pathogens has been documented also in developed countries due to failures in well head protection.. Salu. Barthe. Oluyege et al.3. 2006. 2005) the majority of studies of pathogens in groundwater has focused on the presence of indicator microorganisms (e. Momba et al. Salmonella was detected with varying frequencies in the analyzed water. Ahmed. the surveys of Salmonella prevalence in drinking water in Nigeria undertaken by Oluyege et al. As shown in Table 3 lower frequencies of Salmonella in drinking water samples were reported from Nigeria compared to South Africa (Akinyemi et al.. d Percentage of the Gram negative isolates from water samples.. non-appropriate water supply structures. 2004.1. 2005). Adewale.8 · 102 gc/L 10. 2006. that in contrast to what was observed in surface waters studies from other countries. Furthermore. c Used untreated for drinking purpose. Oluyege et al. Wall. 2009. Overall. 2006. several studies have been undertaken investigating the microbiological quality of the collected rain waters. Vieritz.. . Levantesi et al. Another study also linked roof harvested rain water with Salmonella water-borne infection in Australia (Ashbolt & Kirk. Oguntoke et al. & Theron. & Perrodin. In another study of groundwater quality in Turkey. John & Rose. from a combination of water either treated or untreated prior to use as public drinking water untreated is provided in Table 3. but like for most water sources. Several studies describe Salmonella prevalence in drinking water in African countries. Pierre. most of these African publications relied on very few data points to link the water as reservoirs of salmonellae... inadequate off-set and diffuse contamination sources (Bockelmann et al. 5. or protozoa (e. 2009) (Table 3). Goss & Richards. / Food Research International 45 (2012) 587–602 597 however. and improper disinfection were consistently identified as the main cause of water contamination in developing countries (Akinyemi et al. these older studies investigated the physicochemical and biological factors influencing Salmonella survival in various water gc: gene copies.7% (214) 104–106 CFU/100 mLb 50% (4) 23. 2009. In contrast.. As shown in Table 3.g. Borchardt et al. (2007) clearly showed the importance of the Table 3 Salmonella occurrence in drinking water. The literature demonstrate that a lack of hygienic conditions. which provided undeniable evidence of the poor microbiological quality of the public drinking water supplied in urban Nepal. Goonetillek and Gardner (2010) detected Salmonella in tanks collecting roof harvested rain water for indoor and outdoor use and indicated wild birds or animal feces as likely source of contaminations. Oguntoke et al. In Australia.. 2006. indicating the impact of human source contamination on the overall Salmonella input in the analyzed water source. (2006) reported poor microbiological quality of drinking water in a rural area of the Eastern Cape Province (South Africa) where Salmonella arizonae was detected in 100% of municipal drinking water samples. Furthermore. however. Momba. There is also information about Salmonella detection and behavior in groundwater from a study where recycled water has been intentionally recharged to aquifers during Managed Aquifer Recharge (MAR).. 2008). g Salmonella was only detected in well water. Kuczynska. A notable comparison is the comprehensive study of Bhatta et al. Salmonella survival and monitoring in water environment 5. 2009. showering and kitchen use..000 persons a year suggesting that roof harvested rainwater should be disinfected if used for potable water purposes (Ahmed et al.. b Presumptive Salmonella identification. Boyer. Potgieter et al. Locas. Bhatta et al. Borchardt. Nigeria surface and groundwater used as drinking water sources in rural communities were also shown to be reservoirs of Salmonella (Akinyemi et al. Momba et al. Similarly in the Limpopo Province (South Africa). 2009). 2009). Huygens. the information on the presence of Salmonella spp. Africa (2006) Nigeria Akinyemi et al. (2009) Nigeria Oluyege et al. Level and frequency % Water source positive sample (total samples) 6 · 101–3. where the issue of water scarcity has resulted in the promotion of the use of roof harvested rain water for drinking or other purposes. 2006. A risk assessment study using these results indicated that there was a risk of infection for Salmonella ingestion that exceeded the threshold value of 1 extra infection for 10. (2009) determined that the consumption of groundwater was an independent risk factor for a number of confirmed cases of Salmonella choleraesuis in Taiwan. however. 2006. they highlighted the common occurrence of MDR Salmonella strains which increased the risk connected to the use of these water supply systems.. 2005). they detected Salmonella much less frequently than other pathogens such as Cryptosporidium and Giardia.. & Close. 2009.6% 13. (2009) showed that all the Salmonella strains isolated were resistant to several antibiotics.. Pang. 2009. Despite the common assumptions that all enteric pathogens are a contamination risk for groundwater (e. 2010). Levantesi et al.. Goonetilleke and Gardner (2008) and Ahmed. Haas.g. a 35% for indoor use including drinking. Malakate. Li et al. Groundwater is becoming increasingly relied upon as a major source of water and the security of water quality for groundwater in developing nations is a major issue. Oluyege et al. (2010) were able to occasionally detect Salmonella in two aquifers used as MAR sites receiving recycled water.. Margolin. Franklin et al. Ozler and Aydin (2008) detected Salmonella in 15% of the groundwater samples tested. 2008). & Payment. Emmanuel. e Determined by qPCR but reported as CFU/100 mL. in groundwater is limited. 2009). Oluyege et al. 2009.. & Hunt. Oyefolu. (2007) South Momba et al. 2006. 2007. Oguntoke et al.g. enteric pathogens remain the greatest risk. Bhatta et al. (2010) Nigeria Oguntoke et al. Salmonella survival The majority of research on Salmonella survival in aquatic environment has been done in the last decades of the 20th century. 2009). they stressed that the use of genotyping methods with higher resolution than PGFE would be necessary to determine the relatedness of very clonal serovars. 2008). Sinton. & Fasure. Nevertheless.

coli and fecal coliforms were the most appropriate indicators of Salmonella presence compared to Clostridium perfringens. 2003). Sadowsky. 2007). 2004). They showed that inactivation rates in sunlight were clearly higher than in the dark and that the extent of inactivation was directly related to the amount of insolation. 2002. the lake sediment offered some sort of protection for this enteric pathogen and. Wilkes et al. Byappanahalli et al. coli cells showed a better survival capacity when compared to S. Recent studies indicate that secondary habitat may provide the required conditions to promote survival and replication of enteric microorganisms including Salmonella. Schriewer et al.. dissolved organic and inorganic substances. USA (Meinersmann et al. and Shackleton (2010) observed that Salmonella had a 1 log reduction time in groundwater of 1 day. Despite this. Smith. Bacteroidales are fecal anaerobes that are present in feces in much higher densities than conventional FIB and have different host specificities (Field & Samadpour. Furthermore.. Rhodes & Karton. 2003) but less than observed for enteric viruses or protozoa (Toze et al. No correlations were found with cow and pig Bacteroides 16S rRNA genetic markers in the same study. 1995. 2007). Pathogens have been documented to decay when introduced into aquifers and this information can be used for Managed Aquifer Recharge sites (Gordon & Toze. 2003. Despite this.6 times faster than E. Differently from the results from Savichtcheva et al. Baleux. Ishii et al. 2007). lakes. 2010. 5. 2006). The results showed that sunlight was the most important factor for inactivation. According to these observations and to previous results showing that this alga can support the growth of enteric bacteria by providing nutrients in the algal excretions (Byappanahalli. in agreement to Chandran and Hatha (2005) they showed that S. 2009). Schriewer et al. In contrast to what has been previously described in other studies (Mezrioui. 2010. pond. an enhanced survival capacity of Salmonella in lake sediment with respect to the overlaying water was observed (Chandran et al. They also found that dissolved organic substances present in the estuarine water. coli. Wilkes et al. / Food Research International 45 (2012) 587–602 environments and compared the survival capacity of different enteric bacteria (e. could arbor salmonellae at much higher concentrations compared to the numbers in the surrounding water. 2010). and ruminant can be identified by Bacteroidales host specific PCR primers which can allow source tracking of fecal contamination. & Nitzan. Savichtcheva et al. (2010) also observed that at a specific threshold level fecal coliforms as well as enterococci and total coliforms were good predictors of Salmonella presence in Californian rivers with sea intrusion. & McCrow. 2009. 6. 2007). Edmonds. inactivation of Salmonella in groundwater has been noted in one study of pathogen decay at a Managed Aquifer Recharge site. In contrast with these results. enterococci and total coliforms. Favorable results were obtained using this method in comparison to other source tracking approaches (Griffith. no correlation were observed between FIB and Salmonella presence/absence in ponds and creeks in the Brisbane city area in Australia (Ahmed et al.. Levantesi et al. 2007. (2009) showed that a good prediction of Salmonella presence can be obtained by FIB determination. Savichtcheva & Okabe. Feces from different sources such as human. Hall. 2008). Weisburg. 2007. 2003). groundwater and drinking water.. that these microbial indicators did not efficiently predict Salmonella in rivers that were not influenced by sea intrusion.2. . coli). and sunlight on the inactivation of these bacteria. and competition with autochthonous microbes. Page. Furthermore. Nevers.... The effect of sunlight on the persistence of S. however. enterica. Walters et al. In another microcosm study by the same research group. Glozman.. and Braithwaite (2007). coli threshold level that gave the greater probability of pathogen detection was N E. 2007. promoted survival and growth of these enteric bacteria. 2010..6%) (Walters et al. domestic animals and wild life.. Shively. potentially act as a reservoir of Salmonella. (2007). followed by biotic factors. 1988. most information available focuses on the survival of enteric viruses (Nasser. The identified E. Bekele. This is similar to decay times observed in groundwater for other bacteria such as coliforms (Gordon & Toze.. Hanna. In particular.. 2003). This E. (2006) and Byappanahalli et al. coli 89 CFU/100 mL. Nevertheless. (2007). in a comprehensive study describing the occurrence of enteric pathogens in a Canadian watershed and their relationships with environmental parameters and FIB. The biotic factors were determined to comprise of a combination of predation by protozoa and bacteria. They also found. The efficiency of fecal indicator bacteria (FIB) to predict the presence/absence of Salmonella in aquatic environment remains a matter of debate in recent papers (Ahmed et al. coli and Salmonella Typhimurium in estuary waters focusing on the effect of biological factors. In the last ten years this topic has been less frequently addressed. & Whitman. They concluded that agricultural runoff were a major contribution to the Salmonella contamination in the analyzed watershed while contamination from human sources was only a minor contribution. pigs. Walters and colleagues showed that ruminant specific Bacteroidales markers were more frequently detected in Salmonella positive samples (36%) compared to human specific markers (2. Salmonella and E. they indicated that E. & McGee. Conventional and alternative microbial indicators for Salmonella monitoring in aquatic environment The limits and advantages of conventional and alternative indicators of fecal contamination for pathogen monitoring in aquatic environment have been recently extensively reviewed (Field & Samadpour. According to these results.. (2009) hypothesize that Salmonella is likely to multiply on Chladophora in the water column. thus..598 C. two recent studies analyzing river and estuarine water environments showed no predictive value for various Bacteroidales host specific markers in association with Salmonella detection (Schriewer et al. Schriewer et al. Conclusions This review on the occurrence and risk of Salmonella in water has demonstrated that Salmonella can be present in a variety of aquatic environments and that contamination can come from a range of sources. Walters et al. Winfield & Groisman. According to Savichtcheva et al. 2004) and there is limited information specifically on the survival of Salmonella. Toze. coli and Campylobacter jejuni in river and seawater was also investigated by Sinton. Chandran and Hatha (2005) described a microcosm study that investigated the relative survival of E. 2009). & Trousselier. As with the detection of pathogens in groundwater. bacteriophage lysis. in the absence of the native biota. or in the Small River basin in Georgia. coli threshold was determined to correlate with the identification of 89% of Salmonella positive samples. Another potential indicator are the Bacteroidales. horse. Toze. dogs. Salmonella has been detected in sources as diverse as rivers. these markers might predict the presence of certain pathogens associated to specific source of pollution. The relationship between Bacteroides 16S rRNA genetic markers and Salmonella in aquatic environment has been addressed in a few papers (Savichtcheva et al. Typhimurium under all tested conditions. human and total Bacteroides 16S rRNA genetic markers in wastewater and river samples were positively correlated with the presence of Salmonella and showed a good predictive value for the presence of this pathogen. (2009) showed that the filamentous green alga Chladophora in Michigan lake.g. enterica was inactivated up to 1. In particular. Toze. Sidhu. They found that the probability of its occurrence became significantly high (N 70–80%) when the concentration of human Bacteroides genetic markers exceeded 10 6 copies/100 mL. while sources of the bacterium have been like to sources that include inputs from human. due to their host specific distribution. E. E. 2011).

Epidemiology and Infection. (1990). (2006). determined using Quantitative Microbial Risk Assessment. Water Research. 198.. 1257–1265. N. In spite of the recognized potential of microbial source tracking. Studies revealed large serovars diversity. Toxicology. Asano. Ahmed. coli 0157:H7. Adewale. F. Overall. Despite this. Microbial contamination of drinking water and disease outcomes in developing regions.). Collier. J. Bacterial pathogens associated with tap and well waters in Lagos. Nevertheless. 7382–7391. Bacteroidales were found to perform equally or slightly better than FIB in a direct comparison of their capacity to predict Salmonella presence. A.. T.C. B. Detected Salmonella outbreaks were mostly linked to contaminated drinking waters. S. Australia..g. D. 354–364. A. Treating water with chlorine at point-of-use to improve water quality and reduce child diarrhea in developing countries: A systematic review and meta-analysis. A. J. USA: McGraw-Hill. A. B. Ahmed.. This conclusion. Salmonella Mississippi infections in Tasmania: The role of native Australian animals and untreated drinking water. the true incidence of Salmonella waterborne diseases might be greater than is reflected in the reported outbreaks statistics as not all water-borne disease outbreaks are recognized or reported. F. O. confirms that water is a common source for the transmission of this disease. A. and Campylobacter). (2006). A community water-borne outbreak of salmonellosis and the effectiveness of a boil water order. A number of studies in developed countries detected clinically relevant Salmonella serovars in water utilized for indoor uses. O. A. (2007). Shigella. Of particular concern is the rise in the presence of multi-drug resistance in Salmonella and the causes of this drug resistance. K. Recoveries of Salmonella from soil in eastern region of Saudi Arabia Kingdom. all the outbreaks were consistently associated with the use of untreated or inadequately treated water. The risk of MDR strains dissemination is further exacerbated in less industrialized countries through the customs of inappropriate use and self-prescribing antibiotics. M. irrigation and recreational uses. human infections have been reported for most of the serovars detected in surface water including those usually associated with wild animals. being usually reported less frequently than other pathogens as agent of water mediated epidemics (e. 76. Prevalence and occurrence of zoonotic bacterial pathogens in surface waters determined by quantitative PCR. Additionally. (2007). Payne. (2010). However the relationship between Bacteroidales and Salmonella were found to not be constant in surface water as inconsistent results were obtained in different studies.. & Dowidar. B. Cryptosporidium. Oyefolu. Huygens. L. Real-time PCR detection of pathogenic microorganisms in roof-harvested rainwater in Southeast Queensland. American Journal of Public Health. Hill. these results proposed that there was the likelihood of surface watermediated Salmonella infections. & Gardner. 43. (1997). 5490 – 5496. In addition. the data produced have rarely been published. East and Central African Journal of Surgery. T. these methods have not been extensively used to investigate the sources of Salmonella contamination in the surface water environments. A. 134. J. Analysis of isolated serovars consistently showed a mixed human and animal origin of Salmonella in surface water environments. Sawant. however. New York. Tsuchihashi. J. This review has shown that there are still limitations on the understanding of Salmonella in water and their potential sources. 76. however. G. both as drinking water sources and for recreational use. technologies and applications (1st edn. Leverenz. in Salmonella outbreaks. & Colford.... 229–238. Regardless. The data available in the scientific literature related to water-borne transmission of Salmonella in developing countries are mainly case control studies that have analyzed the risk for endemic typhoid Salmonella. R. Reports of massive water-borne Salmonella outbreaks as well as epidemiological studies on endemic typhoid and paratyphoid fevers underlined the relevance of MDR Salmonella strains in these countries. Salmonella serovars of human health concern were shown to be widespread in natural fresh waters although more rare environmental serovars were also frequently detected. (2004). 11(1). A.. a great complexity was observed in the structure of Salmonella populations in surface water environments. Salmonella contaminated waters used to irrigate and wash produce crops have been implicated in a large number of food-borne outbreaks demonstrating that additional indirect routes of transmissions should be considered to correctly evaluate the role of water in Salmonella diseases dissemination. & Fasure. Most of the studies that looked for a link between indicators and Salmonella found inconsistent results on the relationship between the occurrence of FIB and Salmonella. the results obtained to-date suggest that microbial source tracking by genotyping methods in these environments may be possible and may be extremely useful to identify related strains in complex environmental Salmonella populations and to highlight specific transmission routes. O.. Giardia. Overall. E. W. especially in countries with a low level of water-borne outbreaks surveillance.. R. exposure to recreational water was indicated as the most important risk factor for childhood Salmonella infections indicating that different transmission routes may be implicated in the transmission of sporadic and epidemic diseases. et al. This emphasizing the role of wild life animals in water contamination along with the more accepted livestock and human sources. Angulo. Studies have shown that Salmonella is efficiently removed by conventional disinfection procedures utilized in water treatment processes and thus is of little risk in adequately treated water sources. J. / Food Research International 45 (2012) 587–602 599 Extensive surveys of Salmonella spp. (2009). both in water and in likely sources of contamination as well as spatial and temporal variation in the detection of Salmonella types and frequencies. the positive correlations between Salmonella frequencies and rainfall events observed in many of the studies indicated that surface runoff plays a main role as driver of Salmonella load in aquatic environments. Levantesi et al. 110–117. S. W.. & Gardner. Australia. T.. Arnold.. Applied and Environmental Microbiology. Salmonella was not one of the leading causes of reported waterborne outbreaks in developed countries. (2008).. norovirus. F. Huygens. Sharp. is not supported by epidemiological water-borne outbreaks data showing rare involvement of surface waters. D. & Tchobanoglous. The scientific data. A. Ashbolt. Goonetillek. Salu. no significant improvements were achieved by applying alternative indicators to the Salmonella presence in surface waters. B. but also highlight that other risk factors are associated with typhoid fever indicating multiple routes of transmission. A. 65.. E. Water reuse — Issues. Salmonella remain a significant health risk in developing nations and improved understanding of the role of water in the dissemination of Salmonella in these countries and on how to manage the risks. Nevertheless. 4918–4928. Ahmed. 580–584. H. Ashbolt. Burton. Tippen. K. Different types of drinking water (municipal water system. Goonetilleke. also detected MDR Salmonella strains in natural freshwaters. as potable and non-potable water. The American Journal of Tropical Medicine and Hygiene.. Akinyemi. F. Health risk from the use of roof-harvested rainwater in southeast Queensland. F. T.. overall. tank water) were indicated as sources of outbreaks.. 87(4)... References Abdel-Monem. J. well. 74.... W. 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