Food Research International 45 (2012) 587602

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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

Review

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
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 conrmed 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.

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

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6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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1. 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, per capita consumption and the resulting impacts of human activity on the environment (Asano, Burton, Leverenz, Tsuchihashi, & Tchobanoglous, 2007). 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 signicant (Suresh & Smith, 2004). It is therefore critical to understand the relevance of natural and drinking water contribution to transmission of pathogenic microorganisms. Salmonella is a ubiquitous enteric pathogen with a worldwide distribution that comprises a large number of serovars characterized by different host specicity and distribution. 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, 2005). Zoonotic salmonellae are commonly described as foodborne pathogens, however, drinking water as well as natural waters are known to be an important source for the transmission of these enteric microorganisms (Ashbolt, 2004; Leclerc, Schwartzbrod, & Dei-Cas, 2002). Salmonella, just like other enteric bacteria, is spread by the fecaloral route of contamination. This microorganism can enter the aquatic environment directly with feces of infected humans or animals or indirectly, e.g., via sewage discharge or agricultural land run off. Overall Salmonella spp. and subspecies can be found in a large variety of vertebrates. Beside humans, animal sources of Salmonella include pets, farm animals and wild animals; calves, poultry, pigs, sheep as well as wild birds (sea gull, pigeon) and reptiles can all be reservoirs of Salmonella (Dolejsk, Bierosov, Kohoutov, Literk, & Czek, 2009; Lightfoot, 2004; Wray & Wray, 2000). Plants, insects and algae were also found capable of harboring Salmonella and might be implicated in the transmission of this enteric pathogen (Byappanahalli et al., 2009; Guo, van Iersel, Chenn, Brackett, & Beuchat, 2002; Ishii et al., 2006; Natvig, Ingham, Ingham, Cooperband, & Roper, 2002). Salmonellae are frequently found in environmental samples. They are usually present in large numbers in raw sewage (10 310 4 CFU/L) and can still be present in wastewater efuent after advanced secondary treatment including coagulation, ltration and disinfection (Maier, Pepper, & Gerba, 2000; Wry, Lhoutellier, Ducray, Delgens, & Godon, 2008). Soil and sediment were also found to harbor salmonellae (Abdel-Monem & Dowidar, 1990; Gorski et al., 2011; Tobias & Heinemeyer, 1994) and sediment particles are believed to function as a micro ecological niche enhancing salmonellae survival in lakes (Chandran et al., 2011). In the aquatic environment this pathogen has been repeatedly detected in various types of natural waters such as rivers, lakes, coastal waters, estuarine as well as contaminated ground water (Haley, Cole, & Lipp, 2009; Levantesi et al., 2010; Martinez-Urtaza et al., 2004; Martinez-Urtaza, Liebana, Garcia-Migura, Perez-Pieiro, & Saco, 2004; Polo et al., 1999; Wilkes et al., 2009). In addition to its widespread occurrence, elevated survival capacities in non-host environment have been reported for Salmonella (Wineld & Groisman, 2003). The growth of Salmonella in non-host environments such as wastewater sludge and compost has also been reported (Zaleski, Josephson, Gerba, & Pepper, 2005) and the growth of Salmonella in water supplies is also considered possible, due to its ability to colonize surfaces and replicate in biolms of distribution

system pipes (Jones & Bradshaw, 1996). However, standard disinfection procedures used in drinking water treatment processes are active against salmonellae (Cicmanec, Smith, & Carr, 2004). Taxonomically the genus Salmonella comprises two species namely S. bongori and S. enterica. The species S. enterica is further differentiated in to six subspecies (enterica, salamae, arizonae, diarizonae, indica and houtenae) among which the S. enterica subspecies enterica is mainly associated to human and other warm blooded vertebrates. Traditionally members of the genus Salmonella are clustered in serovars according to their agellar (h) and somatic (o) antigens. Currently over 2400 Salmonella serovars have been described but only about 50 serovars, all within the subspecies enterica, are common causes of infections in humans and warm blooded animals (Popoff, 2001). Salmonella serovars have different host specicity, diverse geographic distribution, and cause different syndromes. On the basis of the clinical syndromes caused Salmonella are divided in to two distinct groups namely the typhoidal and nontyphoidal Salmonella serovars (Pond, 2005). Enteric fevers, typhoid and paratyphoid fever are severe, contagious systemic diseases caused by the infection of the serovars Typhi and Paratyphi. Even though not common in developed countries, enteric fevers remain an important and persistent health problem in less industrialized nations. Overall, in 2003 an annual incidence of approximately 17 million cases of typhoid and paratyphoid fevers was reported worldwide (Kindhauser, 2003). Differently from other Salmonella serovars, Typhi and Paratyphi are host adapted and can only infect humans; stools of infected persons are therefore the original source of contaminations for these pathogens. Water contaminated with feces of human cases and carriers is one of the main vehicles of typhoid fever infections. Differently from typhoidal Salmonella strains, non-typhoidal salmonellae, the ubiquitous subtypes found in a number of animal species, are more frequently associated to foodborne than to waterborne transmission. These zoonotic Salmonella serovars tend to cause acute but usually self-limiting gastroenteritis. In some patients, however, these same serovars can cause severe systemic diseases such as osteomyelitis, pneumonia and meningitis (Pond, 2005). Severe and invasive presentations of non-typhoidal salmonellosis in Africa are common in children with co-morbidities (Graham, 2002) and immune compromised HIV infected adults (Gordon, 2008). Notably the emergence of MDR strains of Salmonella Enteriditis and Typhimurium was associated to the observed incidence of invasive salmonellosis (Gordon & Graham, 2008). The increased frequency of MDR Salmonella strains in human infections is an emerging issue of major health concern (Lightfoot, 2004; Lynch et al., 2009; Pond, 2005). As a consequence, the possible role of fecally contaminated waters in the dissemination of MDR Salmonella, both typhoidal and non-typhoidal, as well as antibiotic resistance genes though horizontal gene transfer is of great interest. This issue is of particular concern in developing countries where the common use of untreated, 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, Dada, & Odeyemi, 2009; Srikantiah et al., 2007). Overall, the above reported characteristics suggest that water might be an important source for the transmission of all salmonellae, not only for the typhoid serovars. An increased knowledge on the prevalence, diversity and survival of this enteric bacterium in the environment, together with a proper assessment, trough effective

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surveillance and epidemiological studies, of the relevance of the water environment in the transmission of Salmonella disease is desirable. In this respect the possible involvement of water in food contamination is also of great interest. 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. Initially epidemiological data on the watermediated transmission of Salmonella infections and on the possible strategies to control these diseases are described. Successively recent literature relating to Salmonella prevalence, diversity, and survival in surface water and drinking water is summarized. Finally, a short overview of the most relevant emerging issues which the scientic community is actually addressing in relation to Salmonella in water environments is given. 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. Furthermore the use and the evaluation of alternative fecal indicators of water contamination for Salmonella monitoring in aquatic environment is reported. Considering that limited scientic publications exist that report the presence of Salmonella in water when compared to reports of Salmonella in food, peer reviewed scientic publications of the last ten years were reviewed. 2. 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, 2008; Bhunia et al., 2009; Farooqui, Khan, & Kazmi, 2009; Franklin et al., 2009; Kozlica, Claudet, Solomon, Dunn, & Carpenter, 2010; Swaddiwudhipong & Kanlayanaphotporn, 2001; Taylor, Sloan, Cooper, Morton, & Hunter, 2000) and the analysis of risk factors associated with endemic or sporadic Salmonella infections (Denno et al., 2009; Gasem, Dolmans, Keuter, & Djokomoeljanto, 2001; Sharma, Ramakrishnan, Hutin, Manickam, & Gupte, 2009; Srikantiah et al., 2007; Tran et al., 2005; Vollaard et al., 2004). Beside scientic publications, reports of national surveillance systems, such as Communicable Disease Surveillance Centre (CDSC, United Kingdom) and Centers for Disease Control and Prevention and Environmental Protection Agency (CDC/EPA USA), provide useful data on salmonellae water-borne disease outbreaks (Craun et al., 2010; Dale, Kirk, Sinclair, Hall, & Leder, 2007; Smith et al., 2006). The level and quality of water-borne disease surveillance data, however, varies in different countries. In particular the situation in developing countries is problematic due to the lack of laboratory facilities and the scarcity of economic resources, however surveillance systems in many European countries have also been judged incapable of detecting water-borne disease (Blasi, Carere, Pompa, Rizzuto, & Funari, 2008; Hunter, 2003; Stanwell-Smith, Andersson, & Levy, 2003). 2.1. Developing countries Literature data related to water-borne salmonellae in developing countries relate mostly the typhoid Salmonella serovars. In the less industrialized area of the world, in particular in the Indian subcontinent and South East Asia, typhoid and paratyphoid fevers occur both in epidemic and endemic form, and remain a major public health problem (DeRoeck, Jodar, & Clements, 2007). The burden of typhoid fever worldwide is further compounded by the spread of multiple drug resistant S. Typhi (Kim, 2010; Lynch et al., 2009; Srikantiah et al., 2006; Swaddiwudhipong & Kanlayanaphotporn, 2001). Most of the recent publications on typhoid and paratyphoid fever water-borne infections in developing countries are from the Asian continent (Bhunia et al., 2009; Farooqui et al., 2009; Gasem et al., 2001; Kim et al., 2003; Lewis et al., 2005; Luxemburger et al., 2001; Mermin, Villar, & Carpenter, 1999; Sharma et al., 2009; Srikantiah et al., 2007;

Swaddiwudhipong & Kanlayanaphotporn, 2001; Tran et al., 2005; Vollaard et al., 2004). Very few or no publication from Africa and Central/Latin America, respectively, addressed the role of water as vehicle of Salmonella transmission in the last ten years. Reports on typhoid and paratyphoid fever epidemics in Asia consistently indicate that contamination of drinking water, sourced from well water (Farooqui et al., 2009), piped municipal drinking water (Bhunia et al., 2009; Kim et al., 2003; Lewis et al., 2005; Mermin et al., 1999) and unboiled spring water (Swaddiwudhipong & Kanlayanaphotporn, 2001) was the main source of outbreaks. In addition to this, most of the papers (Kim, 2010; Lewis et al., 2005; Mermin et al., 1999; Swaddiwudhipong & Kanlayanaphotporn, 2001) clearly show the involvement of MDR typhoid strains in water-borne epidemics. Mermin et al. (1999) reported a massive epidemic of MDR typhoid fever in Dushanbe, Tajikistan, associated with the consumption of municipal water. In the rst half of the year 1997, 8901 cases of typhoid fever and 95 associated deaths were reported in Dushanbe. A casecontrol study demonstrated that Salmonella Typhi infection was associated with drinking unboiled water or obtaining water from sources outside the house. Lack of chlorination, equipment failure, and back-siphonage in the water distribution system led to contamination of the drinking water (Mermin et al., 1999). Of 29 Salmonella serovar Typhi isolates tested, 27 were resistant to seven antibiotics, namely to ampicillin, chloramphenicol, nalidixic acid, streptomycin, sulsoxazole, tetracycline, and trimethoprim-sulfamethoxazole. Although 93% of the tested Salmonella serovar Typhi isolates from Dushanbe were resistant to antimicrobials commonly used for typhoid fever, the case mortality rate of 1.0% was rather low (Mermin et al., 1999). Farooqui et al. (2009) reported the study of a community outbreak of typhoid fever associated with drinking water in a village close to Karachi, Pakistan. This outbreak claimed three human lives and left more than 300 people infected within a one week. The infected people consumed water from a well that was the only available source of drinking water in the village. Epidemiological investigations revealed the gross contamination of the well with dead and decaying animal bodies, their fecal material and garbage. Microbiological testing conrmed 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., 2009). In the summer of 2002 during a 7week period, 5963 cases of typhoid fever were reported in Bharatpur, a town in Nepal with a population of 92,214 inhabitants (Lewis et al., 2005). This outbreak was the largest single-point source outbreak of MDR typhoid fever reported so far. The outbreak was traced with molecular epidemiological methods to a single sourcethe sole municipal water supply. A total of 90% of the isolates were resistant to more than one antibiotic. MDR S. 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, 2001). In agreement with the studies relating to typhoid fever outbreaks, epidemiological studies on the risk factors for endemic and sporadic typhoid fevers in Asia conrmed the association between this disease and the use of poor quality water (Gasem et al., 2001; Sharma et al., 2009; Srikantiah et al., 2007; Tran et al., 2005). Srikantiah et al. (2007) and Tran et al. (2005) indicated the use of untreated drinking water in Uzbekistan and unboiled surface water in Vietnam, respectively, as a major risk factor for typhoid fever. Srikantiah et al. (2007) also showed that MDR Salmonella Typhi strains were important in endemic typhoid fever in the Samarkand region of Uzbekistan. They found that multiple antimicrobial resistance to ampicillin, chloramphenicol, and trimethoprim-sulfamethoxazole, were in 6 (15%) of 41 Salmonella serovar Typhi isolates from patients. Furthermore recent consumption of antimicrobials (two weeks preceding illness) additionally increased the risk of infection (Srikantiah et al., 2007). In Seramang city and the surrounding area (Indonesia), typhoid fever

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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., 2001). Finally, Sharma et al. (2009) showed that the unsafe use of water, namely scooping out water from containers instead of using piped water or water stored in a narrow mounted container at home, was associated with typhoid fever. Using GIS to explore the epidemiological pattern across Vietnam by investigating the risk factors associated with shigellosis, typhoid, and cholera, Kelly-Hope et al. (2007) revealed that typhoid fever prevailed in the Mekong River Delta. They observed that typhoid fever was mostly associated with high vapor pressure and the use of river and streams as drinking water. On the contrary, forested regions and public tap drinking water were found to be negatively associated with typhoid fever. In contrast to this, Vollaard et al. (2004) showed that fecally contaminated drinking water was not associated with typhoid and paratyphoid fevers in Jakarta Indonesia. However, in this study, the habit of boiling water before consumption was declared by all the people surveyed, both test cases and control sources, possibly explaining the lack of association between microbiological contamination of drinking water and typhoid fever. Vollaard et al. (2004) also showed that typhoid fever was signicantly associated with consuming ice cubes and iced drinks highlighting this as a likely water mediated route of transmission. 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., 2001), avored ice drinks (Black et al., 1985) and ice creams (Luby et al., 1998) are risk factors for this disease. In agreement with these observations was the report that prolonged survival of Salmonella in ice (Butler, Mahmoud, & Warren, 1977; Dickens, DuPont, & Johnson, 1985). 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., 2001; Sharma et al., 2009; Vollaard et al., 2004). Interestingly, Vollaard et al. (2004) showed that in Jakarta typhoid and paratyphoid fevers are associated with different routes of transmission. Risk factors for typhoid and paratyphoid fevers, respectively, were mainly within and outside the household. As in other developing countries, in Africa, Salmonella Typhi is a major cause of enteric disease, particularly in children (Crump, Luby, & Mintz, 2004). 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. However, a mean incidence of 50 cases per 100,000 persons per year has been estimated for the whole continent with a highest value in South Africa (N 100/100,000 cases/year) (Crump et al., 2004). 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. In Nigeria, Oguntoke, Aboderin, and Bankole (2009) investigated relationships between water-borne diseases, morbidity patterns, drinking water source quality and water handling practices in Ibadan City. Oguntoke et al. found that typhoid fever was the most common water-borne disease (39.3%) in the area followed by bacillary dysentery and cholera. 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., 2009). 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. Additionally multivariate regression analysis showed that the percentage of residents applying inadequate domestic water treatment (mostly potash alum addition) explained 68.6% (P b 0.04) of the pattern of waterborne diseases morbidity in the area (Oguntoke et al., 2009). 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, Odiyo, Musekene, & Tessema, 2009). The Venda region, a rural area, is characterized by the lack of clean potable water and the inadequacy of sanitation (Obi et al., 2004; Potgieter et al., 2005). Using a stratied random-sampling approach, the study identied a signicant 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., 2009). In many African countries MDR non-typhoidal salmonellae are reported to be the commonest cause of bacteraemia in children under 5 years (Gordon & Graham, 2008). Life-threatening invasive disease outbreaks in children caused by MDR non-typhoidal salmonellae have been reported in several African countries (e.g. Graham, 2002; Kariuki et al., 2006). Nevertheless the sources and mode of transmission of non-typhoidal salmonellae in Africa are still unknown. In a prospective study in Kenya, Kariuki et al. (2006) compared the serovars and genotypes of non-typhoidal salmonellae isolates from children with bacteraemia, from family contacts, and from home environmental samples. 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, 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, 2004). 2.2. Developed countries In contrast to what has been observed for the less industrialized nations, most of the data on water-borne salmonellae in developed countries involve non-typhoidal Salmonella serovars. In many industrialized countries, 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., 2009; Smith et al., 2006). Even if they remain endemic in a few geographic regions (Rizzo et al., 2008), typhoid and paratyphoid fever are now rare diseases, mainly associated with people returning from foreign travel to regions where these diseases are still much more common (Lynch et al., 2009). In the USA since 1971, the CDC, in collaboration with the EPA and with the Council of State and Territorial Epidemiologists, began a surveillance program to collect and report data of water-borne outbreaks. According to the CDC data from 1971 to 2000, 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, Calderon, & Craun, 2004). As revised by these authors, most of these salmonellae outbreaks (11/15) were associated with community water systems and groundwater instead of surface water. In the same period, the use of untreated groundwater along with inadequate treatment of collected groundwater and distribution systems contamination were the most important deciencies identied for causing outbreaks of enteric bacteria. Further analysis has shown that various Salmonella subspecies, comprising Typhimurium, Enteriditis, Bareilly, Javiana, Newport and Weltervreden, were the causes of water associated Salmonella outbreaks in the USA (Craun et al., 2004). From 2000 to 2006 salmonellae were found very rarely or not at all in drinking waterborne outbreaks in USA (Blackburn et al., 2004; Liang et al., 2006; Yoder et al., 2008). Nevertheless, two recent outbreaks indicated that water-borne salmonellae are still of health concern in cases of deciency of water treatment or inadequate water supply systems in the USA (Berg, 2008; Kozlica et al., 2010). In August 2008, the health department and regulatory ofcials identied an outbreak of

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Salmonella I 4,[5],12:i: involving ve persons in a rural community in Tennessee. An untreated water supply was recognized as the source of infection. It was found that the water, which had been collected from a spring, had been stored in a small unprotected reservoir subject to contamination from runoff and wildlife (Kozlica et al., 2010). In the second reported case during March and April 2008, an outbreak of water-borne disease associated with Salmonella struck the city of Alamosa in Colorado. Salmonellae were found to have contaminated the public water system that supplies drinking water to the community. The outbreak resulted in 442 reported illnesses, 122 of which were laboratory-conrmed, and one death. Epidemiological estimates suggested that up to 1300 people may have been ill (Berg, 2008). Alamosa's drinking water comes from deep artesian wells in an aquifer considered to be a protected groundwater source. Prior to the outbreak, the city's drinking water was not chlorinated for disinfection but was historically in compliance with all health-based drinking water standards. 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. The reservoir was found to have several small cracks and holes that likely allowed the contamination source to enter. Only one Salmonella water-borne outbreak related to recreational water exposure was recorded by the CDC between 1995 and 2005 (Levy, Bens, Craun, Calderon, & Herwaldt, 1998; Pond, 2005). On the contrary, recreational aquatic environments, both salt and fresh waters, were indicated as the most important risk factor for sporadic childhood Salmonella infections at three Washington state county health departments (Denno et al., 2009). Denno et al. (2009) conducted a prospective case control study to investigate the possible association between sporadic childhood reportable enteric infections and different plausible exposures. Infection with Salmonella was found to be strongly related to playing or swimming in natural water sources. In addition, 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. In Australia, salmonellae were found to be the most common pathogen in drinking water-borne outbreaks from 2001 to 2007 (Dale et al., 2007). Salmonella spp. were implicated in ve of 10 observed drinking water-borne outbreaks and in an outbreak derived from a contaminated aquarium. The serovars Saintpaul, Typhimurium, subsp IIIb 61:i:z35, Muenchen and Para B bv java, were identied as outbreak causes. Differently from what has been observed in the USA where Salmonella outbreaks were mostly related to contaminated community water systems, in Australia contaminated tank and bore waters were identied as the origin of outbreaks. 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. These authors also highlighted that most of the exposures to untreated drinking water were recorded as exposure to water collected in rainwater collection tanks. Roof collected rain water were involved in several other water-borne outbreaks by Salmonella in Australia (Franklin et al., 2009; Taylor et al., 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., 2009). In Europe, monographic water-borne outbreaks reports such as those of CDC/EPA, are not available because drinking water is dened as food and thus included in foodborne outbreaks reporting. Country specic review of water-borne outbreaks in Italy (Blasi et al., 2008) and the UK (Smith et al., 2006) were recently published. According to the complete surveillance data of Communicable Disease Surveillance Centre (CDSC), Salmonella was never associated to water-borne outbreaks in England and Wales from 1992 to 2003 (Smith et al., 2006). In contrast, salmonellae were implicated in outbreaks that

occurred in Italy from 1998 to 2005. However because the surveillance system on communicable diseases in Italy is not planned to efciently identify water-borne outbreaks, the number of reported cases do not represent an accurate clear estimation of the real situation (Blasi et al., 2008). 2.3. Control strategies to prevent Salmonella drinking water related transmission As for other water-borne pathogens, different measures can be adopted to hinder the spread of Salmonella in water environment, and consequently reduce human risk of infection. Regarding the measures to reduce the occurrence of Salmonella in drinking water, 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. For this purpose, the World Health Organization has developed Guidelines for Drinking Water Quality, which provides an internationally harmonized support to help countries develop rules and standards that are suitable to national and local circumstances (WHO, 2008). In developing countries, commonly lacking piped water supply, self-sustaining decentralized approaches including point of use chemical and solar disinfection, 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, Bartram, Lochery, & Wegelin, 2001). In this respect, 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 efciently reduced diarrhea incidence, with respect to water source interventions (Arnold & Colford, 2007; Clasen, Schmidt, Rabie, Roberts, & Cairncross, 2007; Fewtrell et al., 2005). Studies of the risk factors for typhoid and paratyphoid endemics and epidemics infections conrm that simple decentralized control strategies might be effective in the control of these diseases (Sharma et al., 2009; Srikantiah et al., 2007). According to the ndings of Sharma et al. (2009) home chlorination of drinking water, the use of narrow-mounted containers for safe water storage, 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. Farooqui et al. (2009) reported measures recently introduced by WHO that include solar disinfection, bleach addition, boiling, and use of low cost ceramic lters, which are well suited to prevent typhoid fever outbreaks due to the consumption of contaminated surface or drinking water. Education regarding the risk of drinking untreated surface water as well as promoting the use of boiled drinking water carried from home, was indicated by Srikantiah et al. (2007) as practical intervention measures to reduce water related transmission of typhoid fever in Samarkand (Uzbekistan). Srikantiah et al. (2007) also suggested specic intervention strategies to reduce the increased risk linked to MDR typhoid strains. According to their results the use of antimicrobials two weeks before onset of typhoid fever was independently associated to this disease; hence the development of primary care clinical treatment guidelines to reduce unnecessary antimicrobial exposure may efciently decrease the risk of typhoid fever. In many industrialized countries, the success of applied control strategies is conrmed by the small number of water-borne outbreaks caused by salmonellae. Nevertheless, outbreaks caused by microbial contamination of drinking water still result in substantial human and economic costs in these countries (Berg, 2008; Risebro et al., 2007). The identication 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. Causes of water-borne outbreaks in developed countries have been extensively reviewed in recent publications (Craun et al., 2010; Craun,

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Calderon, & Craun, 2005; Dale et al., 2007; Risebro et al., 2007; Schuster et al., 2005). Unfortunately most of these reviews consider the enteric bacteria as a whole and specic deciencies associated to salmonellae water-borne outbreaks could not be extrapolated. Schuster et al. (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. Analyzing water-borne outbreaks of enteric diseases associated with EU public drinking water supplies (19902005), Risebro et al. (2007) found that contamination of source water and failure of water treatment accounted for more than 50% of the recorded outbreaks. In particular they found that disinfection deciencies were associated with 75% of outbreaks due to bacterial, viral and mixed pathogen contamination (Risebro et al., 2007). In their complete review of drinking water associated outbreaks in USA (19712006) Craun et al. (2010) showed, inter alias, that greater attention is needed to address and reduce the risk of outbreaks in groundwater supplied systems and in private water systems. Overall it is apparent that the diversity of causative factors of outbreaks in different countries requires different specic control actions. The control is essentially carried out through application of process control measures, which are provided by the WHO Guidelines (WHO, 2008). The approach that has been proposed is the Hazard Analysis Critical Control Points (HACCP) approach, which prioritizes the identication of key potential contamination or control points in the treatment and distribution system. This approach has already been successfully used by the food and beverage industry, 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. Another successful approach, which is combined with HACCP principles, is the multi-barriers approach. Different steps are selected in the treatment process in order to increase removal capability and normal uctuations in performance can be compensated. In this way the likelihood that pathogens can enter the distribution system and reach consumers is minimized. The two approaches together constitute a water safety framework that is a basic structure to develop supply-specic water safety plans to ensure the production of high quality drinking water. In agreement with this, the EPA's Ground Water Rule (USEPA, 2006) establishes a risk targeted approach to identify those systems that may be most susceptible to fecal contamination and species corrective actions (Craun et al., 2010).

3. Role of contaminated waters in Salmonella foodborne outbreaks In recent years, reports of Salmonella outbreaks related to fresh produce consumption have illustrated the likely relationships between salmonellae, water and ultimately foodborne Salmonella infections (CDC, 2002, 2008; Greene et al., 2008; Mohle-Boetani et al., 2009; Sivapalasingam et al., 2003). It is now commonly accepted that fruit and vegetable consumption is a risk factor for infections with enteric pathogens (Heaton & Jones, 2007). 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., 2010; Heaton & Jones, 2007), and in particular of Salmonella (Hanning, Nutt, & Ricke, 2009). Salmonella is the most common aetiological agents associated to fresh produce related infections (Heaton & Jones, 2007; Sivapalasingam, Friedman, Cohen, & Tauxe, 2004). A wide spectrum of produce have been associated with salmonellae infections including tomatoes (Greene et al., 2008; Sivapalasingam et al., 2004), serrano peppers (CDC, 2008), cantaloupe (CDC, 2002; Sivapalasingam et al., 2004), lettuce (Takkinen et al., 2005), basil (Pezzoli et al., 2008), and mango (Sivapalasingam et al., 2003).

Salmonellae are often isolated from produce samples in routine surveys (Thunberg, Tran, Bennett, & Matthews, 2002). Additionally some S. enterica strains have the ability to adhere to plant surfaces where they are able to survive for long periods and then grow (Gandhi, Golding, Yaron, & Matthews, 2001; Islam et al., 2004). The capacity of this pathogen to become endophytic, thus to invade internal plant parts has also been reported (e.g. Deering, Pruitt, Mauer, & Reuhs, 2011; Klerks, Franz, van Gent-Pelzer, Zijlstra, & van Bruggen, 2007; Lapidot & Yaron, 2009; Schikora, Carreri, Charpentier, & Hirt, 2008). Among others Lapidot and Yaron (2009) demonstrated the ability of S. enterica serovar Typhimurium to transfer from contaminated irrigation water in plant roots and then into the edible parts of mature parsley. However the transfer of S. enterica serovar Typhimurium from water to plants was shown only to occur with highly contaminated irrigation water (Lapidot & Yaron, 2009). Water is likely to be an important source of produce contamination in the eld as well as in post harvested processing (Berger et al., 2010). Water sources of varying microbiological quality are used for irrigation of produce worldwide. For example, in the UK, 71% of irrigation water is obtained from surface waters which receive treated sewage efuent (Tyrrel, Knox, & Weatherhead, 2006) and in developing countries untreated wastewater is also commonly used to irrigate crops, thus increasing the risk of microbial contamination (Ashbolt, 2004). Gagliardi, Millner, Lester, 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. Contaminated irrigation and processing waters were indicated as possible sources of Salmonella contamination in several fresh produce outbreaks (CDC, 2002, 2008; Greene et al., 2008; Sivapalasingam et al., 2003). In 2002 and 2005 two multistate outbreaks of S. Newport in USA, caused by the same rare S. Newport strain, were associated with eating tomatoes (Greene et al., 2008). Tomatoes causing of the outbreak were traced back to the eastern shore of Virginia where the S. Newport outbreak strain was isolated. Notably this outbreak strain was isolated from the pond water used to irrigate tomato elds both in 2002 and 2005 (Greene et al., 2008). The presence of the S. Newport outbreak strain, two years apart, in the irrigation pond demonstrate that if not properly addressed, the source of contamination can persist and cause continuous outbreaks (Greene et al., 2008). Salmonella serovar Newport was also the etiological agent in a multistate outbreak linked to mango consumption in USA (Sivapalasingam et al., 2003). The implicated mangoes were traced back to a single Brazilian farm where mangoes were washed with contaminated water (Sivapalasingam et al., 2003). Analysis of the irrigation and processing water at this farm indicated the presence of Salmonella spp. in the water. Sivapalasingam 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. The S. Newport outbreak strain was no actually isolated from the Brazilian water samples however, the farm investigation took place many months after the outbreak had occurred (Sivapalasingam et al., 2003). In 2008, 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, 2008). Jalapeno and serrano peppers imported from Mexico were identied as the major sources of this outbreak. The S. 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, 2008). Irrigation of elds with sewage contaminated waters and processing produce with Salmonella contaminated waters were also indicated as possible sources of contamination in an outbreak of S. Poona infections in the USA associated with eating imported cantaloupe (CDC, 2002).

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Several studies have investigated the potential source of produce contamination in the supply chain both at the pre-harvested and postharvested stages. According to the epidemiological data, surveys of Salmonella contamination in water used for fresh produce irrigation and in food processing identied the possible involvement of these waters in fresh vegetable and fruit contamination (Castillo et al., 2004; Duffy et al., 2005; Espinoza-Medina et al., 2006; Lpez Cuevas, Len Flix, Jimnez Edeza, & Chaidez Quiroz, 2009). Salmonella was detected in irrigation waters used for different type of fresh produces items, such as tomatoes, peppers and cantaloupes (Castillo et al., 2004; Duffy et al., 2005; Espinoza-Medina et al., 2006; Lpez Cuevas et al., 2009). Espinoza-Medina et al. (2006) evaluated the incidence of Salmonella contamination during cantaloupe production and processing, in ve farms in Sonora (Mexico) showing that irrigation water (23% of positive samples) and hands of workers packing cantaloupe (16.7% of positive samples) were the most likely sources of Salmonella contamination. Similarly, Castillo et al. (2004) described an extensive survey of Salmonella contamination at cantaloupe production farms in South Texas (USA) and Colima State (Mexico). By repetitive sequence based PCR analysis Castillo et al. (2004) identied the irrigation water source as a possible source of cantaloupe contamination. Similar levels of Salmonella contamination were found in the cantaloupe from USA and from Mexico (Castillo et al., 2004). Duffy et al. (2005) analyzed samples from fresh produce (orange, parsley and cantaloupe) and environmental samples (water, soil, equipment) at a produce production farm in Texas. Salmonella was only isolated from the irrigation water (16/25 isolates), equipment (6/25 isolates) and washed cantaloupe (3/25 isolates). 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., 2005). Finally Lpez Cuevas et al. (2009) recovered Salmonella in 39% of irrigation water samples in four different regions of the Culiacan valley (Sinaloa Mexico), an important area for the production of crops exported in the USA. Notably, 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 (Lpez Cuevas et al., 2009; Lugo-Melchor et al., 2010). 4. Salmonella prevalence, diversity in surface, 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. Salmonella prevalence in surface water and drinking water has not been uniformly investigated in different countries in recent papers. Surveys of Salmonella in fresh surface water environment were mainly performed in industrialized nations, in particular in Canada and North America. Reports of Salmonella prevalence in drinking water were instead more frequently from developing nations reecting the higher concern relating to the use of low quality drinking water in these countries. Overall, the scientic community has mainly recently focused on the prevalence of this microorganism in impacted and non-impacted watersheds (Haley et al., 2009; Jokinen et al., 2011; Patchanee, Molla, White, Line, & Gebreyes, 2010), on the identication of the routes of salmonellae contamination (Gorski et al., 2011; Jokinen et al., 2010, 2011; Obi et al., 2004; Patchanee et al., 2010), and on the inuence of environmental factors on the spread of Salmonella in water (Haley et al., 2009; Jokinen et al., 2010; Meinersmann et al., 2008; Wilkes et al., 2009). Particular attention was also addressed to the evaluation of available and new approaches to monitor sources of Salmonella contamination, and to predict its presence in different aquatic environments (Savichtcheva, Okayama, & Okabe, 2007; Schriewer et al., 2010; Walters, Gannon, & Field, 2007; Wilkes et al., 2009). Additionally, the recently available data on the prevalence of

antibiotic resistant Salmonella strains in surface and drinking water (Bhatta et al., 2007; Dolejsk et al., 2009; Meinersmann et al., 2008; Oluyege et al., 2009; Patchanee et al., 2010) consistently indicate that these aquatic environments are a reservoir of MDR strains, which might contribute to the dissemination of these MDR strains through susceptible populations. 4.1. Surface waters A survey of recent studies showed an increasing interest over the last two years on the role of non-host habitats, such as surface water environments as natural reservoir and in the transmission of Salmonella and other enteric pathogens (Ahmed, Sawant, Huygens, Goonetilleke, & Gardner, 2009; Byappanahalli et al., 2009; Dolejsk et al., 2009; Haley et al., 2009; Jokinen et al., 2010, 2011; Patchanee et al., 2010; Schriewer et al., 2010; Wilkes et al., 2009). A summary of the available data on Salmonella prevalence in surface fresh waters sources is shown in Table 1. The data provided in Table 1 conrms the ubiquitous nature of this enteric pathogen. Salmonellae were detected in different countries and in very diverse water sources, ranging from pristine (e.g. Patchanee et al., 2010; Till, McBride, Ball, Taylor, & Pyle, 2008) and low impacted water (e.g. Jokinen et al., 2010; Meinersmann et al., 2008; Patchanee et al., 2010) to heavily impacted water sources (e.g. Bonadonna, Filetici, Nusca, & Paradiso, 2006; Jyoti et al., 2010). Salmonella contamination occurred in surface water used for recreational purposes (Till et al., 2008); as source of drinking water (Till et al., 2008); and for irrigation (e.g. Gannon et al., 2004). This demonstrated wide distribution of salmonellae underlines that there is the potential for inadvertently using water contaminated with Salmonella, with associated potential health risks. As shown in Table 1, the Salmonella detection frequencies were extremely variable in the investigated surface waters with detection rates ranging from 3 to 100%. In general, the highest frequencies were reported in watersheds that had been highly impacted by human activities (Bonadonna et al., 2006; Jyoti et al., 2010) or in geographical areas with a history of high salmonellosis cases (Haley et al., 2009). However, Patchanee et al. (2010) showed that elevated frequencies of Salmonella were also found in a forestry watershed not inuenced by human activities. Notably, these authors observed similar prevalence of salmonellae in watersheds with diverse potential contamination sources, namely residential industrial (58.8%), forestry (57.1%), crop/agriculture (50%), and swine production (41.7%). Also of all the studies listed in Table 1, despite the importance of the knowledge of Salmonella concentrations in water to evaluate the risk of water related infection, only a few performed a quantitative assessment of Salmonella in environmental waters (Bonadonna et al., 2003, 2006; Byappanahalli et al., 2009; Haley et al., 2009; Jyoti et al., 2010; Lemarchand & Lebaron, 2003). Temporal and spatial variation of Salmonella frequencies were commonly observed in surface water (Bonadonna et al., 2006; Byappanahalli et al., 2009; Haley et al., 2009; Jokinen et al., 2010; Lemarchand & Lebaron, 2003; Meinersmann et al., 2008; Till et al., 2008; Wilkes et al., 2009). It is possible that variations in the occurrence of Salmonella in ambient water may be governed, in part, by environmental parameters such as temperature, water chemistry, and solar radiation that inuence survival and transport of the microorganism. Other possible reasons include changes in pathogen loading due to enhanced shedding from human and animal host, or from enhanced ow of water from contaminated sources. Positive correlations between rainfall events and Salmonella prevalence and/or diversity have been reported by many authors (Baudart, Lemarchand, Brisabois, & Lebaron, 2000; Haley et al., 2009; Jokinen et al., 2010; Polo et al., 1999; Schets, van Wijnen, Schijven, Schoon, & de RodaHusman, 2008; Wilkes et al., 2009). These results, which are supported by similar observations with respect to Salmonella contamination in

594 Table 1 Salmonella occurrence in surface waters. Level and frequency positive Surface water samples % (total samples) 8.5% (342) 13% (186) 10 10 CFU/100 mL 87% (8) 54% (86) 7% (143) 3% (32) 0.0020.017 MPN/mL 42% (19) 16% (87) 2.536.3 MPN/L 79% (72) 415% (1600)c 75% (83) 3.8% (79) 10.6% (216) 17.6% (17) 10% (725)e 53% (30) 1010 MPN/100 mL 100% (N 300) 75% (375)g 5.4% (802) 102105 MPN/100 mL 100% (10) 57% (14) 0.0642.4 CFU/L 100% (8)
a b c d e f g 4 b 4 6 a

C. Levantesi et al. / Food Research International 45 (2012) 587602

Dominant impact in the analyzed water Mainly inuenced 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 efuents, surface runoff, agricultural Not described

Country Canada

Survey extent

References Jokinen et al. (2011) Jokinen et al. (2010) Jyoti et al. (2010) Patchanee et al. (2010) Schriewer et al. (2010) Ahmed et al. (2009) Byappanahalli et al. (2009) Dolejsk et al. (2009) Haley et al. (2009) Wilkes et al. (2009) Meinersmann et al. (2008) Schets et al. (2008) Simental and MartinezUrtaza (2008) Till et al. (2008) Savichtcheva et al. (2007) Bonadonna et al. (2006) Obi et al. (2004) Gannon et al. (2004) Bonadonna et al. (2003) Obi, Potgieter, Bessong, 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, 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, dairy farming, municipal, sheep/pastoral, forestry undeveloped Mixed: WWTPs efuents, urban sewage, cow and pig farms Mixed: Urban/industrial comprising direct sewage discharge Animal and human activities, human and animal feces

9 sampling sites, 2 year Canada 4 sampling sites, 2 years India 8 sampling sites, 1 day USA 4 sampling sites, 2 years USA 10 sampling sites, 14 month Australia 8 sampling sites, 2 months USA numerous sampling sites, 2 years Czech 2 sampling sites, Republic 1 year USA 6 sampling sites, 12 months Canada 24 sampling sites, 3 years USA 82 sampling sites, 1 day Netherlands 8 sampling sites, 1 year Mexico Random sampling, 2 years New Zeland 25 sampling sites, 15 month Japan 5 sampling sites, 3 months Italy 8 sampling sites, 2 years South Africa 8 sampling sites Canada 1621 sampling sites, 2 years 1 sampling site, 1 year Weekly sampling, 5 months

Mixed: Urban/industrial, WWTP discharge agricultural Runoff from agricultural land and pastures, human and animal feces Mixed

Italy Africa France

qPCR quantication. Range of average monthly density. Different percentage in different seasons. Only found in canals and river. 15% of river sample used for drinking water supply. Highly contaminated area at environmental risk. Environmental samples including water and sediments (89%) and food (11%).

coastal area and marine environment (Baudart, Grabulos, Barrusseau, & Lebaron, 2000; Simental & Martinez-Urtaza, 2008), indicated that increased pathogen load could be associated with rainfall events as one major environmental driver of Salmonella contamination in surface water environment. In agreement with this a positive correlation was reported in the literature between rainfall events and the incidence of Salmonella water related infections (e.g. Haddock & Malilay, 1986; Suresh & Smith, 2004). In contrast, 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. Till et al. (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. In contrast, the seasonal peak of Salmonella incidence in a Canadian watershed was observed in the fall (Wilkes et al., 2009) potentially reecting

enhanced livestock based fecal input during this period. According to Wilkes et al. (2009) salmonellae's incidence was found to be positively correlated with tributary discharge values as well as with accumulative rainfall. Only Haley et al. (2009) in a study of a watershed in Georgia USA found that Salmonella incidence peaked in the summer period. Over the complete study period, the presence of this pathogen was positively correlated with water temperatures and rainfall events (1 or 2 days before sampling). According to these results, the authors concluded that multiple environmental factors, including enhanced pathogen loading during storm events, 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. Spatial differences in Salmonella prevalence in surface waters have also been reported in the recent literature (Bonadonna et al., 2006; Lemarchand & Lebaron, 2003; Meinersmann et al., 2008; Savichtcheva

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et al., 2007; Schriewer et al., 2010). Schriewer et al. (2010) reported a higher frequency of salmonellae in surface waters that have marine inuences while Bonadonna et al. (2006) and Lemarchand and Lebaron (2003), observed that the highest concentration of this pathogen was associated to sampling points in densely populated areas and/or downstream of sewage efuents discharge sites. MDR strains have been detected in surface water in developed countries (Dolejsk et al., 2009; Meinersmann et al., 2008; Patchanee et al., 2010). In particular, Patchanee et al. (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. In contrast, antibiotic resistant strains were not detected from watersheds impacted by forestry, crop agriculture, or a residential/industrial area (Patchanee et al., 2010). 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, black-headed gulls nesting in this pond (Dolejsk et al., 2009). A total of 16% of water and 24% of gull samples yielded Salmonella. Antibiotic resistance was found in 12% of salmonellae isolated from the water and 28% of gull salmonellae. Resistance to the quinolone nalidixic acid, streptomycin, and tetracycline was often detected in these Salmonella isolates. Dolejsk et al. (2009) concluded from these results that black-headed gulls can be important reservoirs of antibiotic resistant salmonellae. Meinersmann and co-workers investigated the prevalence of Salmonella and their antimicrobial resistance prole in a synoptic study of the Oconee River Basin, a small river in north-eastern Georgia, USA (Meinersmann et al., 2008). Water samples were obtained from 83 sites with Salmonella isolated from 62 of the samples, however, only seven of the isolates were resistant to any antimicrobials.

Table 2 Salmonella diversity in surface waters. Diversity Common serovars (percentage Serovar number/ of total isolates) total isolates 11/29 Rubislaw (72.4%)a I:11:r:a Derby Anatum (18.3%) Gaminara (18.3%) Inverness (18.3%) Muenchen (8.7%)b Newport (8.7%)b Bredeney (6.7%) S. enterica subsp arizona (40.6%) Muenchen (14.2%)c Rubislaw (13.2%)c Mikawasima (6.1%) Montevideoe Enteritidis (50%)d,e Muenchen (20%) Rubislaw Hartford Give Others serovars Country Reference

12/104

Givea, Heidelberga, Canada Typhimurium, Senftenberg, Mbandaka, Other Mbandaka, Bullbay, Give, USA Miami, Braenderup

Jokinen et al. (2011)

Patchanee et al. (2010)

13/197

Braenderup, Anatum, I47:z4z23, Gaminara, Liverpool, Bareilly, Saint Paul, I4,(5):b,

USA

Haley et al. (2009)

6/17 19/73

4.2. Diversity of Salmonella strains isolated from surface waters All Salmonella serovars are considered as potential pathogens. Only about 50 of these serovars, however, have been predominantly isolated from humans or animals (Popoff, 2001). 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. Furthermore, the identication of sourcespecic serovars might help future tracking of sources of Salmonella contamination events. The rst comprehensive studies describing the diversity of Salmonella serovars in the aquatic environment were presented by Polo et al. (1999) and Baudart, Lemarchand, et al. (2000). Both research groups analyzed a large number of isolates from different natural aquatic systems (river, wastewater and marine coastal areas) showing a great diversity of Salmonella serovars. Since then, several works have provided further data on the different serovars present and on the possible sources of Salmonella contamination in surface water. A summary of recent available data is reported in Table 2. With the exception of few studies that analyzed a limited number of isolates (Dolejsk et al., 2009; Schets et al., 2008) or monitored highly contaminated watersheds (Bonadonna et al., 2006), 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. In comparison to the results of the initial studies by Baudart, Lemarchand, et al. (2000) and Polo et al. (1999), these latter consistent gures found that there was a low diversity of Salmonella serovars in the non-host water environment (Table 2). This difference might be explained by the very long period (5 years) of Salmonella monitoring described by Polo et al. (1999) and the reported increase in the numbers of serovars during ood events (10 of the 35 serovars were only isolated during the ood by Baudart, Lemarchand, et al. (2000)).

Infantis, Derbyf, Indiana, Hadarg, Typhimurium Infantis, Kiambu, Livingstone, Iv40:z4,z32: Typhimurium, Paratyphi B, Newport, Oranieneburg, Ouakam, Mbandaka, Montevideo, Thompson, Gaminara, Heidelberg, Braenderup

Czech Republic USA

Dolejsk et al. (2009) Meinersmann et al. (2008)

11/23

45/92a

19/36

Newport Virchow Typhimurium Typhimurium (39%) Urbana Suberu Vejle Typhimurium (13.7%) Subsp. II (8.4%) Infantis (5.3%) Bredeney (4.2%) Stanley (4.2%) Derby (4.2%) Derby (16.6%) 03,10:r: Anatum Bardo Javiana

Netherlands Schets et al. (2008) Othmarschem, Soerenga, Augustenborg, Breda, Coeln, DJugu Mexico Simental and MartinezUrtaza (2008) Bonadonna et al. (2006)

Saint Paul, Bovismorbicants, Montevideo, Enteriditis, Give (only serotypes detected also by other authors)

Italy

03,10:vt, Subsp.III b, Subsp. IV, Stanley, Typhimurium, Tennessee, London, Bovismorbicants, Dessau, Paratyphi B, Schleissheim, Lexington, Mbandaka, Enteriditis

Vietnam

Phan et al. (2003)

35/413h

Typhimurium (31.1%) Virchow Panama Newport Hadar Grumpensis

France

Baudart, Lemarchand, et al. (2000)

(continued on next page)

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

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Country

Reference

Spain

Polo et al. (1999)

a b c d e f g h

Also isolated from human and/or animal feces. Among the 10 most frequent serovar reported in human salmonellosis in USA. Common clinical serotypes in the analyzed geographical area. Percentage of Salmonella-positive samples. Dominant cause of salmonellosis in human and animal in Czech Republic. Only found in pigs in Czech Republic. Only found in human in Czech Republic. Only the most common serovars isolated from fresh water samples are reported.

Contamination sources and environmental factors were also shown to in uence serovar abundance. Peaks of Salmonella diversity were observed to be associated to a specic locations (e.g. urban/industrial impacted watershed, Patchanee et al., 2010), and seasons (e.g. greater detections in the summer period, Haley et al., 2009). Typhoid Salmonella serovars Typhi and Paratyphi A were only detected in surface waters in developing countries where the disease is endemic (Bhatta et al., 2007; Oluyege et al., 2009). In contrary, Salmonella Paratyphi B, although very rare, has been detected in surface waters in France (Baudart, Lemarchand, et al., 2000) and Italy (Bonadonna et al., 2006). As shown in Table 2, S. enterica serovars of high public health concern (e.g. Montevideo Newport, Bredney, Enteriditis, Infantis, Muenchen, Typhimurium) were detected in all the reported studies. One relevant fact that can be noted is that the clinical serovars that were common or dominant in the studied geographic areas, were usually also detected in the surface water samples (Bonadonna et al., 2006; Dolejsk et al., 2009; Haley et al., 2009; Patchanee et al., 2010). This indicates that the Salmonella population in water environments is inuenced by the incidence of human infections in the local area. Clinical serovars were not always dominant isolates in the studies of aquatic environment, however (Haley et al., 2009; Jokinen et al., 2011; Patchanee et al., 2010) suggesting that human sewage was not the sole or main source of contamination in these habitats. In agreement with this, the spectra of Salmonella serovars observed by various authors in surface water showed a mixed human/animal origin (Dolejsk et al., 2009; Haley et al., 2009; Jokinen et al., 2011; Patchanee et al., 2010). 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 conrmed by recent literature data. According to the dominance of the S. enterica subspecies arizonae (40% of isolates) in the Little River rural watershed (Georgia, USA), Haley et al. (2009) suggested that local reptile population may be a signicant source of the total Salmonella in this surface water. Jokinen et al. (2011) could only detect the serovar Rubislaw in the Oldman river watershed (Alberta, Canada) and in the feces of wild birds, while it was neither detected in the analyzed sewage (human contamination source) nor in feces of domestic animals. High frequency of Salmonella (57.1% of samples) from a forestry watershed not impacted by livestock was described by Patchanee et al. (2010). Patchanee et al.

(2010) also showed that Salmonella serovar Gaminara, was dominant in this same water system. According to Gaertner, Hahn, Rose, and Forstner (2008) S. Gaminara is mostly associated to wild animals. As previously noted, black-headed gulls were identied as an important reservoir of antibiotic resistant Salmonella contamination in a pond in Czech Republic (Dolejsk et al., 2009). All of these results indicate that wild animals can be one of the major sources of Salmonella contamination in the environment. In agreement with this, wild birds and other wild life have been identied as source of Salmonella water-borne outbreaks in different countries (Angulo et al., 1997; Schuster et al., 2005; Taylor et al., 2000). Understanding the relative contribution of different possible contamination routes on Salmonella introduction in surface waters is a necessary precursor for the selection of specic control strategies. An increase of knowledge on how the Salmonella genotypes and phenotypes are related to different potential contamination sources is essential. In this context, valuable information has been generated by the comprehensive work of Jokinen et al. (2011), Patchanee et al. (2010), and Gorski et al. (2011) that can be used for the suggestion of appropriate control strategies in impacted catchments and water sheds. 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. Only four serovars isolated from water (Rubislaw, Heidelberg, Give and I:11:r:) were also detected in feces or sewage samples. However, most of these serovars spanned a broad host range and thus it was not possible to identify the single contamination sources. Salmonella Rubislaw, the most common serovar in the water samples, was only detected in wild bird feces, but, since a limited number of fecal samples of wild birds was analyzed, it was not possible to understand the real contribution of these birds on the water contamination with Salmonella. Nevertheless, 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., 2010). Patchanee et al. used pulsed-eld gel electrophoresis PFGE genotyping coupled with serotyping techniques for tracking Salmonella contamination in four watersheds in North Carolina (USA). Salmonella genotypic and phenotypic diversity was analyzed and compared in differently impacted watersheds: swine-production, residential/industrial, forestry and crop agriculture (Patchanee et al., 2010). The resulting Salmonella genotypic and phenotypic diversity in differently impacted watersheds: swine-production, residential/industrial, 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. This suggested that there was a specic source of contamination for this watershed. In particular the serovars Anatum and Bredney were only found in this watershed. 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. Gorski et al. (2011) investigated the incidence and diversity of salmonellae in a major produce region of California. As part of the study they also analyzed serovars and genotypes (PFGE) of Salmonella strains isolated from water, cattle and wildlife feces, soil/sediment and preharvested lettuce/spinach. The serovars detected in the water samples, S. Infantis, S. Give, S. Typhimurium and the monophasic types 6,8:d: and 6,8::e,n,z15, were also isolated from wildlife feces. According to PFGE patterns, however, all the strains isolated from wildlife were distinguishable from those isolated from water. Nevertheless, some near matches indicated that crow and coyotes were potential sources for water contamination. These authors conclude that source tracking may be possible in these environments;

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however, they stressed that the use of genotyping methods with higher resolution than PGFE would be necessary to determine the relatedness of very clonal serovars. 4.3. Drinking water and groundwater A summary of recent available publications on Salmonella occurrence in groundwater and drinking water, from a combination of water either treated or untreated prior to use as public drinking water untreated is provided in Table 3. As shown in Table 3, Salmonella was detected with varying frequencies in the analyzed water. Several studies describe Salmonella prevalence in drinking water in African countries, mainly South Africa and Nigeria (Akinyemi, Oyefolu, Salu, Adewale, & Fasure, 2006; Momba, Malakate, & Theron, 2006; Oguntoke et al., 2009; Oluyege et al., 2009; Potgieter et al., 2005). Momba et al. (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. Similarly in the Limpopo Province (South Africa), 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., 2005). As shown in Table 3 lower frequencies of Salmonella in drinking water samples were reported from Nigeria compared to South Africa (Akinyemi et al., 2006; Oguntoke et al., 2009; Oluyege et al., 2009) (Table 3). Nevertheless, Nigeria surface and groundwater used as drinking water sources in rural communities were also shown to be reservoirs of Salmonella (Akinyemi et al., 2006; Oguntoke et al., 2009; Oluyege et al., 2009). In addition, the surveys of Salmonella prevalence in drinking water in Nigeria undertaken by Oluyege et al. (2009) showed that all the Salmonella strains isolated were resistant to several antibiotics. Furthermore, MDR resistance to more than 4 antibiotics was observed in most of these isolates (Oluyege et al., 2009). It should be noted, however, that in contrast to what was observed in surface waters studies from other countries, most of these African publications relied on very few data points to link the water as reservoirs of salmonellae. A notable comparison is the comprehensive study of Bhatta et al. (2007), which provided undeniable evidence of the poor microbiological quality of the public drinking water supplied in urban Nepal. Bhatta et al. (2007) clearly showed the importance of the
Table 3 Salmonella occurrence in drinking water. Level and frequency % Water source positive sample (total samples) 6 1013.8 102 gc/L 10.7% (214) 104106 CFU/100 mLb 50% (4) 23.6% 13.3%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. (2010) India Jyoti et al. (2010) Nigeria Oguntoke et al. (2009) Nigeria Oluyege et al. (2009) Nepal Bhatta et al. (2007) South Momba et al. Africa (2006) Nigeria Akinyemi et al. (2006) South Potgieter et al. Africa (2005)

human host-specic strains Typhi and Paratyphi A, indicating the impact of human source contamination on the overall Salmonella input in the analyzed water source. Furthermore, they highlighted the common occurrence of MDR Salmonella strains which increased the risk connected to the use of these water supply systems. The literature demonstrate that a lack of hygienic conditions, non-appropriate water supply structures, and improper disinfection were consistently identied as the main cause of water contamination in developing countries (Akinyemi et al., 2006; Bhatta et al., 2007; Momba et al., 2006; Oluyege et al., 2009). 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. Contamination of groundwater by microbial pathogens has been documented also in developed countries due to failures in well head protection, inadequate off-set and diffuse contamination sources (Bockelmann et al., 2009; Borchardt, Haas, & Hunt, 2004; Goss & Richards, 2008). Groundwater can be contaminated by a wide range of pathogens, but like for most water sources, enteric pathogens remain the greatest risk. Despite the common assumptions that all enteric pathogens are a contamination risk for groundwater (e.g. John & Rose, 2005) the majority of studies of pathogens in groundwater has focused on the presence of indicator microorganisms (e.g. Emmanuel, Pierre, & Perrodin, 2009; Wall, Pang, Sinton, & Close, 2008), risks posed by enteric viruses (e.g. Borchardt et al., 2004; Locas, Barthe, Margolin, & Payment, 2008), or protozoa (e.g. Boyer, Kuczynska, & Fayer, 2009). In contrast, the information on the presence of Salmonella spp. in groundwater is limited. In one of the few studies reported on Salmonella in groundwater, Li et al. (2009) determined that the consumption of groundwater was an independent risk factor for a number of conrmed cases of Salmonella choleraesuis in Taiwan. In another study of groundwater quality in Turkey, Ozler and Aydin (2008) detected Salmonella in 15% of the groundwater samples tested. 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). Levantesi et al. (2010) were able to occasionally detect Salmonella in two aquifers used as MAR sites receiving recycled water, however, they detected Salmonella much less frequently than other pathogens such as Cryptosporidium and Giardia. In Australia, where the issue of water scarcity has resulted in the promotion of the use of roof harvested rain water for drinking or other purposes, several studies have been undertaken investigating the microbiological quality of the collected rain waters. Ahmed, Huygens, Goonetilleke and Gardner (2008) and Ahmed, Vieritz, 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. 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 10,000 persons a year suggesting that roof harvested rainwater should be disinfected if used for potable water purposes (Ahmed et al., 2010). Another study also linked roof harvested rain water with Salmonella water-borne infection in Australia (Ashbolt & Kirk, 2006; Franklin et al., 2009) further highlighting the risks from Salmonella in roof harvested rain water.

5. Salmonella survival and monitoring in water environment 5.1. Salmonella survival The majority of research on Salmonella survival in aquatic environment has been done in the last decades of the 20th century. Overall, these older studies investigated the physicochemical and biological factors inuencing Salmonella survival in various water

gc: gene copies. a 35% for indoor use including drinking, showering and kitchen use. b Presumptive Salmonella identication. c Used untreated for drinking purpose. d Percentage of the Gram negative isolates from water samples. e Determined by qPCR but reported as CFU/100 mL. f % of positive sampling sites. g Salmonella was only detected in well water.

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environments and compared the survival capacity of different enteric bacteria (e.g. Salmonella and E. coli). In the last ten years this topic has been less frequently addressed. Chandran and Hatha (2005) described a microcosm study that investigated the relative survival of E. coli and Salmonella Typhimurium in estuary waters focusing on the effect of biological factors, dissolved organic and inorganic substances, and sunlight on the inactivation of these bacteria. The results showed that sunlight was the most important factor for inactivation, followed by biotic factors. The biotic factors were determined to comprise of a combination of predation by protozoa and bacteria, bacteriophage lysis, and competition with autochthonous microbes. They also found that dissolved organic substances present in the estuarine water, in the absence of the native biota, promoted survival and growth of these enteric bacteria. In contrast to what has been previously described in other studies (Mezrioui, Baleux, & Trousselier, 1995; Rhodes & Karton, 1988; Wineld & Groisman, 2003), E. coli cells showed a better survival capacity when compared to S. Typhimurium under all tested conditions. In another microcosm study by the same research group, an enhanced survival capacity of Salmonella in lake sediment with respect to the overlaying water was observed (Chandran et al., 2011). According to these results, the lake sediment offered some sort of protection for this enteric pathogen and, thus, potentially act as a reservoir of Salmonella. The effect of sunlight on the persistence of S. enterica, E. coli and Campylobacter jejuni in river and seawater was also investigated by Sinton, Hall, and Braithwaite (2007). 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. Furthermore, in agreement to Chandran and Hatha (2005) they showed that S. enterica was inactivated up to 1.6 times faster than E. coli. Pathogens have been documented to decay when introduced into aquifers and this information can be used for Managed Aquifer Recharge sites (Gordon & Toze, 2003; Toze, 2004). As with the detection of pathogens in groundwater, most information available focuses on the survival of enteric viruses (Nasser, Glozman, & Nitzan, 2002; Toze, Hanna, Smith, Edmonds, & McCrow, 2004) and there is limited information specically on the survival of Salmonella. Despite this, inactivation of Salmonella in groundwater has been noted in one study of pathogen decay at a Managed Aquifer Recharge site. Toze, Bekele, Page, Sidhu, and Shackleton (2010) observed that Salmonella had a 1 log reduction time in groundwater of 1 day. This is similar to decay times observed in groundwater for other bacteria such as coliforms (Gordon & Toze, 2003) but less than observed for enteric viruses or protozoa (Toze et al., 2010). Recent studies indicate that secondary habitat may provide the required conditions to promote survival and replication of enteric microorganisms including Salmonella. In particular, Ishii et al. (2006) and Byappanahalli et al. (2009) showed that the lamentous green alga Chladophora in Michigan lake, could arbor salmonellae at much higher concentrations compared to the numbers in the surrounding water. 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, Shively, Nevers, Sadowsky, & Whitman, 2003), Byappanahalli et al. (2009) hypothesize that Salmonella is likely to multiply on Chladophora in the water column. 5.2. 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, 2007; Savichtcheva & Okabe, 2006). The efciency 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., 2009; Savichtcheva et al., 2007; Schriewer et al., 2010; Wilkes et al., 2009). Despite this, in a comprehensive study describing the occurrence of enteric pathogens in a Canadian watershed and their relationships with environmental parameters and FIB, Wilkes et al. (2009) showed that a good prediction of Salmonella presence can be obtained by FIB determination. In particular, they indicated that E. coli and fecal coliforms were the most appropriate indicators of Salmonella presence compared to Clostridium perfringens, enterococci and total coliforms. The identied E. coli threshold level that gave the greater probability of pathogen detection was N E. coli 89 CFU/100 mL. This E. coli threshold was determined to correlate with the identication of 89% of Salmonella positive samples. Schriewer et al. (2010) also observed that at a specic threshold level fecal coliforms as well as enterococci and total coliforms were good predictors of Salmonella presence in Californian rivers with sea intrusion. They also found, however, that these microbial indicators did not efciently predict Salmonella in rivers that were not inuenced by sea intrusion. In contrast with these results, no correlation were observed between FIB and Salmonella presence/absence in ponds and creeks in the Brisbane city area in Australia (Ahmed et al., 2009), or in the Small River basin in Georgia, USA (Meinersmann et al., 2008). Another potential indicator are the Bacteroidales. Bacteroidales are fecal anaerobes that are present in feces in much higher densities than conventional FIB and have different host specicities (Field & Samadpour, 2007). Feces from different sources such as human, horse, pigs, dogs, and ruminant can be identied by Bacteroidales host specic PCR primers which can allow source tracking of fecal contamination. Favorable results were obtained using this method in comparison to other source tracking approaches (Grifth, Weisburg, & McGee, 2003). Furthermore, due to their host specic distribution, these markers might predict the presence of certain pathogens associated to specic 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., 2007; Schriewer et al., 2010; Walters et al., 2007). According to Savichtcheva et al. (2007), 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. They found that the probability of its occurrence became signicantly high (N 7080%) when the concentration of human Bacteroides genetic markers exceeded 10 6 copies/100 mL. No correlations were found with cow and pig Bacteroides 16S rRNA genetic markers in the same study. Differently from the results from Savichtcheva et al. (2007), two recent studies analyzing river and estuarine water environments showed no predictive value for various Bacteroidales host specic markers in association with Salmonella detection (Schriewer et al., 2010; Walters et al., 2007). Nevertheless, Walters and colleagues showed that ruminant specic Bacteroidales markers were more frequently detected in Salmonella positive samples (36%) compared to human specic markers (2.6%) (Walters et al., 2007). 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. 6. 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. Salmonella has been detected in sources as diverse as rivers, lakes, pond, groundwater and drinking water, while sources of the bacterium have been like to sources that include inputs from human, domestic animals and wild life.

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Extensive surveys of Salmonella spp. occurrence in surface waters in industrialized countries con rmed the ubiquitous nature of this enteric pathogen. Moreover, 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. Analysis of isolated serovars consistently showed a mixed human and animal origin of Salmonella in surface water environments. This emphasizing the role of wild life animals in water contamination along with the more accepted livestock and human sources. Overall, a great complexity was observed in the structure of Salmonella populations in surface water environments. Studies revealed large serovars diversity, both in water and in likely sources of contamination as well as spatial and temporal variation in the detection of Salmonella types and frequencies. In spite of the recognized potential of microbial source tracking, these methods have not been extensively used to investigate the sources of Salmonella contamination in the surface water environments. Nevertheless, 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 specic transmission routes. Salmonella serovars of human health concern were shown to be widespread in natural fresh waters although more rare environmental serovars were also frequently detected. At present little is known about the pathogenicity of these rarer serovars isolated from the environment and further research is required to understand the role of these serovars in water-borne disease dissemination. Regardless, human infections have been reported for most of the serovars detected in surface water including those usually associated with wild animals. A number of studies in developed countries detected clinically relevant Salmonella serovars in water utilized for indoor uses, irrigation and recreational uses, and of further concern, also detected MDR Salmonella strains in natural freshwaters. Overall, these results proposed that there was the likelihood of surface watermediated Salmonella infections. This conclusion, however, is not supported by epidemiological water-borne outbreaks data showing rare involvement of surface waters, both as drinking water sources and for recreational use, in Salmonella outbreaks. Nevertheless, 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. Salmonella was not one of the leading causes of reported waterborne outbreaks in developed countries, being usually reported less frequently than other pathogens as agent of water mediated epidemics (e.g. Cryptosporidium, Giardia, E. coli 0157:H7; norovirus, Shigella, and Campylobacter). Detected Salmonella outbreaks were mostly linked to contaminated drinking waters. Different types of drinking water (municipal water system, well, tank water) were indicated as sources of outbreaks, however, all the outbreaks were consistently associated with the use of untreated or inadequately treated water. Studies have shown that Salmonella is efciently removed by conventional disinfection procedures utilized in water treatment processes and thus is of little risk in adequately treated water sources. Despite this, the true incidence of Salmonella waterborne diseases might be greater than is reected in the reported outbreaks statistics as not all water-borne disease outbreaks are recognized or reported, especially in countries with a low level of water-borne outbreaks surveillance. In addition, 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.

The data on water-borne outbreaks in developing countries are not complete as national outbreaks surveillance systems are usually limited and in spite of the likely large number of studies performed in the eld, the data produced have rarely been published. The data available in the scientic 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. The scientic data, overall, conrms that water is a common source for the transmission of this disease, but also highlight that other risk factors are associated with typhoid fever indicating multiple routes of transmission. 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. The risk of MDR strains dissemination is further exacerbated in less industrialized countries through the customs of inappropriate use and self-prescribing antibiotics. The efciency of conventional and alternative microbial indicators of fecal contamination to monitor Salmonella in water environments is still a matter requiring further study due to the need for rapid, specic and reliable methods that can be used for the control of environmental water quality. 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. Additionally, no signicant improvements were achieved by applying alternative indicators to the Salmonella presence in surface waters. Bacteroidales were found to perform equally or slightly better than FIB in a direct comparison of their capacity to predict Salmonella presence. However the relationship between Bacteroidales and Salmonella were found to not be constant in surface water as inconsistent results were obtained in different studies. This review has shown that there are still limitations on the understanding of Salmonella in water and their potential sources. Salmonella remain a signicant 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. Of particular concern is the rise in the presence of multi-drug resistance in Salmonella and the causes of this drug resistance.

References
Abdel-Monem, M. H. A. A., & Dowidar, A. (1990). Recoveries of Salmonella from soil in eastern region of Saudi Arabia Kingdom. The Journal of the Egyptian Public Health Association, 65, 6175. Ahmed, W., Huygens, F., Goonetilleke, A., & Gardner, T. (2008). Real-time PCR detection of pathogenic microorganisms in roof-harvested rainwater in Southeast Queensland, Australia. Applied and Environmental Microbiology, 74, 5490 5496. Ahmed, W., Sawant, S., Huygens, F., Goonetilleke, A., & Gardner, T. (2009). Prevalence and occurrence of zoonotic bacterial pathogens in surface waters determined by quantitative PCR. Water Research, 43, 49184928. Ahmed, W., Vieritz, A., Goonetillek, A., & Gardner, T. (2010). Health risk from the use of roof-harvested rainwater in southeast Queensland, Australia, as potable and non-potable water, determined using Quantitative Microbial Risk Assessment. Applied and Environmental Microbiology, 76, 73827391. Akinyemi, K. O., Oyefolu, A. O. B., Salu, O. B., Adewale, O. A., & Fasure, A. K. (2006). Bacterial pathogens associated with tap and well waters in Lagos, Nigeria. East and Central African Journal of Surgery, 11(1), 110117. Angulo, F. J., Tippen, S., Sharp, D. J., Payne, B. J., Collier, C., Hill, J. E., et al. (1997). A community water-borne outbreak of salmonellosis and the effectiveness of a boil water order. American Journal of Public Health, 87(4), 580584. Arnold, B. F., & Colford, J. M. (2007). 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. The American Journal of Tropical Medicine and Hygiene, 76, 354364. Asano, T., Burton, F. L., Leverenz, H. L., Tsuchihashi, R., & Tchobanoglous, G. (2007). Water reuse Issues, technologies and applications (1st edn.). New York, USA: McGraw-Hill. Ashbolt, N. J. (2004). Microbial contamination of drinking water and disease outcomes in developing regions. Toxicology, 198, 229238. Ashbolt, R., & Kirk, M. D. (2006). Salmonella Mississippi infections in Tasmania: The role of native Australian animals and untreated drinking water. Epidemiology and Infection, 134, 12571265.

600

C. Levantesi et al. / Food Research International 45 (2012) 587602 Craun, G. F., Brunkard, J. M., Yoder, J. S., Roberts, V. A., Carpenter, J., Wade, T., et al. (2010). Causes of outbreaks associated with drinking water in the United States from 19712006. Clinical Microbiology Reviews, 23(3), 507528. Craun, G. F., Calderon, R. L., & Craun, M. F. (2004). Water-borne outbreaks caused by zoonotic pathogens in the USA. In J. A. Cotruvo, A. Dufour, G. Rees, J. Bartram, R. Carr, D. O. Cliver, G. F. Craun, R. Fayer, & V. P. J. Gannon (Eds.), Water-borne zoonoses identication, causes, and control (pp. 120135). London: IWA Publishing, World Health Organization. Craun, G. F., Calderon, R. L., & Craun, M. F. (2005). Outbreaks associated with recreational water in the United States. International Journal of Environmental Health Research, 15(4), 243262. Crump, J. A., Luby, S. P., & Mintz, E. D. (2004). The global burden of typhoid fever. Bulletin of the World Health Organization, 82(5), 346352. Dale, K., Kirk, M., Sinclair, M., Hall, R., & Leder, K. (2007). Reported outbreaks of gastrointestinal disease in Australia are predominantly associated with recreational exposure. Australian and New Zealand Journal of Public Health, 10(34), 527530. Deering, A. J., Pruitt, R. E., Mauer, L. J., & Reuhs, B. L. (2011). Examination of the internalization of Salmonella serovar Typhimurium in peanut, Arachis Hypogaea, using immunocytochemical techniques. Food Research International , doi: 10.1016/j.foodres.2011.01.061. Denno, D. M., William, E., Keene, C. M., Hutter, J. K., Koepsell, M., Patnode, D., et al. (2009). Tri-county comprehensive assessment of risk factors for sporadic reportable bacterial enteric infection in children. The Journal of Infectious Diseases, 199, 467476. DeRoeck, D., Jodar, L., & Clements, J. (2007). Putting typhoid vaccination on the global health agenda. The New England Journal of Medicine, 357(11), 10691071. Dickens, D. L., DuPont, H. L., & Johnson, P. C. (1985). Survival of bacterial enteropathogens in the ice of popular drinks. Journal of the American Medical Association, 253, 31413143. Dolejsk, M., Bierosov, B., Kohoutov, L., Literk, I., & Czek, A. (2009). Antibioticresistant Salmonella and Escherichia coli isolates with integrons and extendedspectrum beta-lactamases in surface water and sympatric black-headed gulls. Journal of Applied Microbiology, 106(6), 19411950. Duffy, E. A., Lucia, L. M., Kells, J. M., Castillo, A., Pillai, S. D., & Acuff, G. R. (2005). Concentrations of Escherichia coli and genetic diversity and antibiotic resistance proling of Salmonella isolated from irrigation water, packing shed equipment, and fresh produce in Texas. Journal of Food Protection, 68(1), 7079. Emmanuel, E., Pierre, M. G., & Perrodin, Y. (2009). Groundwater contamination by microbiological and chemical substances released from hospital wastewater: Health risk assessment for drinking water consumers. Environment International, 35, 718726. U.S. Environmental Protection Agency (2006). National primary drinking water regulations: Ground water rule; Final rule. 40 CFR parts 9, 141 and 142 Fed. Regist. 71, 6557465660. . Espinoza-Medina, I. E., Rodrguez-Leyva, F. J., Vargas-Arispuro, I., Islas-Osuna, M. A., Acedo-Flix, E., & Martnez-Tllez, M. A. (2006). PCR identi cation of Salmonella: Potential contamination sources from production and postharvest handling of cantaloupes. Journal of Food Protection, 69(6), 14221425. Farooqui, A., Khan, A., & Kazmi, S. U. (2009). Investigation of a community outbreak of typhoid fever associated with drinking water. BMC Public Health, 9(476), doi: 10.1186/1471-2458-9-476. Fewtrell, L., Kaufmann, R. B., Kay, D., Enanoria, W., Haller, L., & Colford, J. M., Jr. (2005). Water, sanitation, and hygiene interventions to reduce diarrhoea in less developed countries: a systematic review and meta-analysis. The Lancet Infectious Diseases, 5, 4252. Field, K. G., & Samadpour, M. (2007). Fecal source tracking, the indicator paradigm, and managing water quality. Water Research, 41, 35173538. Franklin, L. J., Fielding, J. E., Gregory, J., Gullan, L., Lightfoot, D., Poznanski, S. Y., et al. (2009). An outbreak of Salmonella Typhimurium 9 at a school camp linked to contamination of rainwater tanks. Epidemiology and Infection, 137(3), 434440. Gaertner, J. P., Hahn, D., Rose, F. L., & Forstner, M. R. J. (2008). Detection of salmonellae in different turtle species within the headwater spring ecosystem. Journal of Wildlife Diseases, 44, 519526. Gagliardi, J. V., Millner, P. D., Lester, G., & Ingram, D. (2003). On-farm and postharvest processing sources of bacterial contamination to melon rinds. Journal of Food Protection, 66, 8287. Gandhi, M., Golding, S., Yaron, S., & Matthews, K. R. (2001). Use of green uorescent protein expressing Salmonella Stanley to investigate survival, spatial location, and control on alfalfa sprouts. Journal of Food Protection, 64, 18911898. Gannon, V. P., Graham, T. A., Read, S., Ziebell, K., Muckle, A., Mori, J., et al. (2004). Bacterial pathogens in rural water supplies in Southern Alberta, Canada. Journal of Toxicology and Environmental Health, 67(2022), 16431653. Gasem, M. H., Dolmans, W. M., Keuter, M. M., & Djokomoeljanto, R. R. (2001). Poor food hygiene and housing as risk factors for typhoid fever in Semarang, Indonesia. Tropical Medicine & International Health, 6, 484490. Gordon, M. A. (2008). Salmonella infections in immunocompromised adults. The Journal of Infection, 56, 413422. Gordon, M. A., & Graham, S. M. (2008). Invasive salmonellosis in Malawi. The Journal of Infection in Developing Countries, 2(6), 438442. Gordon, C., & Toze, S. (2003). In uence of groundwater characteristics on the survival of enteric viruses. Journal of Applied Microbiology, 95, 536544. Gorski, L., Parker, C. T., Liang, A., Cooley, M. B., Jay-Russell, M. T., Gordus, A. G., et al. (2011). Prevalence, distribution and diversity of Salmonella enterica in a major produce region of California. Applied and Environmental Microbiology, doi: 10.1128/AEM.02321-10.

Baudart, J., Grabulos, J., Barrusseau, J. P., & Lebaron, P. (2000). Salmonella spp. and fecal coliform load in coastal waters from a point vs. nonpoint source of pollution. Journal of Environmental Quality, 29, 241250. Baudart, J., Lemarchand, K., Brisabois, A., & Lebaron, P. (2000). Diversity of Salmonella strains isolated from the aquatic environment as determined by serotyping and amplication of the ribosomal DNA spacer regions. Applied and Environmental Microbiology, 66, 15441552. Berg, R. (2008). The Alamosa Salmonella outbreak: A gumshoe investigation. Journal of Environmental Health, 71(2), 5458. Berger, C. N., Sodha, S. V., Shaw, R. K., Grifn, P. M., Pink, D., Hand, P., et al. (2010). Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environmental Microbiology, 12(9), 23852397. Bessong, P. O., Odiyo, J. O., Musekene, J. N., & Tessema, A. (2009). Spatial distribution of diarrhoea and microbial quality of domestic water during an outbreak of diarrhoea in the Tshikuwi community in Venda, South Africa. Journal of Health, Population and Nutrition, 27(5), 652659. Bhatta, D. R., Bangtrakulnonth, A., Tishyadhigama, T., Saroj, S. D., Bandekar, J. R., Hendriksen, R. S., et al. (2007). Serotyping, PCR, phage-typing and antibiotic sensitivity testing of Salmonella serovars isolated from urban drinking water supply systems of Nepal. Letters in Applied Microbiology, 44, 588594. Bhunia, R., Hutin, Y., Ramakrishnan, R., Pal, N., Sen, T., & Murhekar, M. (2009). A typhoid fever outbreak in a slum of South Dumdum municipality, West Bengal, India, 2007: Evidence for foodborne and water-borne transmission. BMC Public Health, 9, 115, doi:10.1186/1471-2458-9-115471-2458-9-115. Black, R. E., Cisneros, L., Levine, M. M., Ban, A., Lobos, H., & Rodriguez, H. (1985). Case control study to identify risk factors for paediatric endemic typhoid fever in Santiago, Chile. Bulletin of the World Health Organization, 63, 899904. Blackburn, B. G., Craun, G. F., Yoder, J. S., Hill, V., Calderon, R. L., Chen, N., et al. (2004). Surveillance for water-borne disease outbreaks associated with drinking water United States, 20012002. MMWR Morbidity and Mortality Weekly Report, 53, 2345. Blasi, M. F., Carere, M., Pompa, M. G., Rizzuto, E., & Funari, E. (2008). Water related diseases outbreaks reported in Italy. Journal of Water and Health, 423432. Bockelmann, U., Dorries, H. H., Ayuso-Gabella, M. N., de Marcay, M. S., Tandoi, V., Levantesi, C., et al. (2009). Quantitative PCR monitoring of antibiotic resistance genes and bacterial pathogens in three European articial groundwater recharge systems. Applied and Environmental Microbiology, 75, 154163. Bonadonna, L., Briancesco, R., Donia, D., Ottaviani, M., Veschetti, E., & Divizia, M. (2003). Aspetti igienico-sanitari delle acque del ume Tevere: presenza di protozoi patogeni e rapporti di correlazione con parametri microbiologici e chimico-sici. Annali di Igiene: Medicina Preventiva e di Comunit, 16, 273280. Bonadonna, L., Filetici, E., Nusca, A., & Paradiso, R. (2006). Controlli ambientali sulla diffusione di sierotipi di Salmonella spp in acque uviali. Microbiologia Medica, 21(4), 311315. Borchardt, M. A., Haas, N. L., & Hunt, R. J. (2004). Vulnerability of drinking-water wells in La Crosse, Wisconsin, to enteric-virus contamination from surface water contributions. Applied and Environmental Microbiology, 70, 59375946. Boyer, D. G., Kuczynska, E., & Fayer, R. (2009). Transport, fate, and infectivity of Cryptosporidium parvum oocysts released from manure and leached through macroporous soil. Environmental Geology, 58, 10111019. Butler, T., Mahmoud, A. A. F., & Warren, K. S. (1977). Algorithms in the diagnosis and management of exotic diseases. XIII Typhoid fever. The Journal of Infectious Diseases, 135, 10171020. Byappanahalli, M. N., Sawdey, R., Ishii, S., Shively, D. A., Ferguson, J. A., Whitman, R. L., et al. (2009). Seasonal stability of Cladophora-associated Salmonella in Lake Michigan watersheds. Water Research, 43, 806814. Byappanahalli, M. N., Shively, D. A., Nevers, M. B., Sadowsky, M. J., & Whitman, R. L. (2003). Growth and survival of Escherichia coli and enterococci populations in the macro-alga Cladophora (Chlorophyta). FEMS Microbiology Ecology , 46 (2), 203 211. Castillo, A., Mercado, I., Lucia, L. M., Martnez-Ruiz, Y., Ponce de Len, J., Murano, E. A., et al. (2004). Salmonella contamination during production of cantaloupe: A binational study. Journal of Food Protection, 67(4), 713720. Centers for Disease Control and Prevention (2002). Multistate outbreaks of Salmonella serotype Poona infections associated with eating cantaloupe from Mexico United States and Canada, 20002002. MMWR. Morbidity and Mortality Weeekly Repor, 51(46), 10441047. Centers for Disease Control and Prevention (2008). Outbreak of Salmonella serotype Saintpaul infections associated with multiple raw produce items United States, 2008. MMWR. Morbidity and Mortality Weeekly Report, 57(34), 929934. Chandran, A., & Hatha, A. A. M. (2005). Relative survival of Escherichia coli and Salmonella Typhimurium in a tropical estuary. Water Research, 39, 13971403. Chandran, A., Varghese, S., Kandeler, E., Thomas, A., Hatha, M., & Mazumder, A. (2011). An assessment of potential public health risk associated with the extended survival of indicator and pathogenic bacteria in freshwater lake sediments. International Journal of Hygiene and Environmental Health, doi: 10.1016/j.ijheh.2011.01.002 Accepted. Cicmanec, J. L., Smith, J. E., & Carr, R. (2004). Control of zoonotic diseases in drinking-water. In J. A. Cotruvo, A. Dufour, G. Rees, J. Bartram, R. Carr, D. O. Cliver, G. F. Craun, R. Fayer, & V. P. J. Gannon (Eds.), Water-borne zoonoses identication, causes, and control (pp. 426436). London: IWA Publishing, World Health Organization. Clasen, T., Schmidt, W. P., Rabie, T., Roberts, I., & Cairncross, S. (2007). Interventions to improve water quality for preventing diarrhoea: Systematic review and metaanalysis. British Medical Journal, 334(7597), 782, doi:10.1136/bmj.39118.489931.BE BMJ.

C. Levantesi et al. / Food Research International 45 (2012) 587602 Goss, M., & Richards, C. (2008). Development of a risk-based index for source water protection planning, which supports the reduction of pathogens from agricultural activity entering water resources. Journal of Environmental Management, 87, 623632. Graham, S. M. (2002). Salmonellosis in children in developing and developed countries and populations. Current Opinion in Infectious Diseases, 15, 507512. Greene, S. K., Daly, E. R., Talbot, E. A., Demma, L. J., Holzbauer, S., Patel, N. J., et al. (2008). Recurrent multistate outbreak of Salmonella Newport associated with tomatoes from contaminated elds, 2005. Epidemiology and Infection, 136(2), 157165. Grifth, J. F., Weisburg, S. B., & McGee, C. D. (2003). Evaluation of microbial source tracking methods using mixed fecal sources in aqueous test samples. Journal of Water and Health, 1, 141152. Guo, X., van Iersel, M. W., Chenn, J., Brackett, R. E., & Beuchat, L. R. (2002). Evidence of association of salmonellae with tomato plants grown hydroponically in inoculated nutrient solution. Applied and Environmental Microbiology, 68, 36393643. Haddock, R. L., & Malilay, J. (1986). The possible role of rainfall in spreading Salmonella on Guam. Journal of Diarrhoeal Diseases Research, 4(4), 229232. Haley, B. J., Cole, D. J., & Lipp, E. K. (2009). Distribution, diversity and seasonality of water-borne Salmonella in a rural watershed. Applied and Environmental Microbiology, 75, 12481255. Hanning, I. B., Nutt, J. D., & Ricke, S. C. (2009). Salmonellosis outbreaks in the United States due to fresh produce: Sources and potential intervention measures. Foodborne Pathogens and Disease, 6(6), 635648. Heaton, J. C., & Jones, K. (2007). Microbial contamination of fruit and vegetables and the behavior of enteropathogens in the phyllosphere: A review. Journal of Applied Microbiology, 104(3), 613626. Hunter, P. R. (2003). Principles and components of surveillance systems. In P. R. Hunter, M. Waite, & E. Ronchi (Eds.), Drinking water and infectious disease: Establishing the links. Boca Raton, FL: CRC Press. Ishii, S., Yan, T., Shively, D. A., Byappanahalli, M. N., Whitman, R. L., & Sadowsky, M. J. (2006). Cladophora (Chlorophyta) spp. harbour human bacterial pathogens in near shore water of Lake Michigan. Applied and Environmental Microbiology, 72, 45454553. Islam, M., Morgan, J., Doyle, M. P., Phatak, S. C., Millner, P., & Jiang, X. (2004). Fate of Salmonella enterica serovar Typhimurium on carrots and radishes grown in elds treated with contaminated manure composts or irrigation water. Applied and Environmental Microbiology, 70, 24972502. John, D. E., & Rose, J. B. (2005). Review of factors affecting microbial survival in groundwater. Environmental Science & Technology, 39, 73457356. Jokinen, C., Edge, T. A., Ho, S., Koning, W., Laing, C., Mauro, W., et al. (2011). Molecular subtypes of Campylobacter spp., Salmonella enterica, and Escherichia coli O157:H7 isolated from fecal and surface water samples in the Oldman River watershed, Alberta, Canada. Water Research, 45, 12471257. Jokinen, C. C., Schreier, H., Mauro, W., Taboada, E., Isaac-Renton, J. L., Topp, E., et al. (2010). The occurrence and sources of Campylobacter spp., Salmonella enterica and Escherichia coli O157:H7 in the Salmon River, British Columbia, Canada. Journal of Water and Health, 8, 374386. Jones, K., & Bradshaw, S. B. (1996). Biolm formation by the enterobacteriaceae: A comparison between Salmonella enteritidis, Escherichia coli and a nitrogen-xing strain of Klebsiella pneumoniae. The Journal of Applied Bacteriology, 80(4), 458464. Jyoti, A., Ram, S., Vajpayee, P., Singh, G., Dwivedi, P. D., Jain, S. K., et al. (2010). Contamination of surface and potable water in South Asia by salmonellae: Culture-independent quantication with molecular beacon real-time PCR. The Science of the Total Environment, 408(6), 12561263. Kariuki, S., Revathi, G., Kariuki, N., Kiiru, J., Mwituria, J., Muyodi, J., et al. (2006). Invasive multidrug-resistant non-typhoidal Salmonella infections in Africa: Zoonotic or anthroponotic transmission? Journal of Medical Microbiology, 55, 585591. Kelly-Hope, L. A., Alonso, W. J., Thiem, V. D., Anh, D. D., Canh, D. G., Lee, H., et al. (2007). Geographical distribution and risk factors associated with enteric diseases in Vietnam. The American Journal of Tropical Medicine and Hygiene, 76, 706712. Kim, S. (2010). Salmonella serovars from foodborne and water-borne diseases in Korea, 19982007: Total isolates decreasing versus rare serovars emerging. Journal of Korean Medical Science, 25, 16931699. Kim, S., Lim, O. Y., Kim, S. H., Kim, J. Y., Kang, Y. H., & Lee, B. K. (2003). Pulsed-eld gel electrophoresis and mutation typing of gyrA gene of quinolone-resistant Salmonella enterica serovar Paratyphi A isolated from outbreak and sporadic cases, 19982002, Korea. Journal of Microbiology and Biotechnology, 13, 155158. Kindhauser, M. K. (2003). Communicable diseases 2002: Global defence against the infectious disease threat. Geneva: World Health Organization. Klerks, M. M., Franz, E., van Gent-Pelzer, M., Zijlstra, C., & van Bruggen, A. H. (2007). Differential interaction of Salmonella enterica serovars with lettuce cultivars and plantmicrobe factors inuencing the colonization efciency. The ISME Journal, 1, 620631. Kozlica, J., Claudet, A. L., Solomon, D., Dunn, J. R., & Carpenter, L. R. (2010). Waterborne outbreak of Salmonella I 4,[5],12:i:. Foodborne Pathogens and Disease, 7(11), 14311433. Lapidot, A., & Yaron, S. (2009). Transfer of Salmonella enterica serovar Typhimurium from contaminated irrigation water to parsley is dependent on curli and cellulose, the biolm matrix components. Journal of Food Protection, 72(3), 618623. Leclerc, H., Schwartzbrod, L., & Dei-Cas, E. (2002). Microbial agents associated with water-borne diseases. Critical Reviews in Microbiology, 28(4), 371409.

601

Lemarchand, K., & Lebaron, P. (2003). Occurrence of Salmonella spp. and Cryptosporidium spp. in a French coastal watershed: Relationship with faecal indicators. FEMS Microbiology Letters, 218(1), 203209. Levantesi, C., La Mantia, R., Masciopinto, C., Bckelmann, U., Ayuso-Gabella, M. N., Salgot, M., et al. (2010). Quantication of pathogenic microorganisms and microbial indicators in three wastewater reclamation and managed aquifer recharge facilities in Europe. The Science of the Total Environment, 408(21), 49234930. Levy, D., Bens, M. S., Craun, G. F., Calderon, R. L., & Herwaldt, B. L. (1998). Surveillance for water-borne disease outbreaks United States, 19951996. MMWR. Morbidity and Mortality Weekly Report, 47(SS05), 134. Lewis, M. D., Serichantalergs, O., Pitarangsi, C., Chuanak, N., Mason, C. J., Regmi, L. R., et al. (2005). Typhoid fever: A massive, single-point source, multidrug-resistant outbreak in Nepal. Clinical Infectious Diseases, 40(4), 554561. Li, T. H., Chiu, C. H., Chen, W. C., Chen, C. M., Hsu, Y. M., Chiou, S. S., et al. (2009). Consumption of groundwater as an independent risk factor of Salmonella Choleraesuis infection: A casecontrol study in Taiwan. Journal of Environmental Health, 72, 2831. Liang, J. L., Dziuban, E. J., Craun, G. F., Hill, V., Moore, M. R., Gelting, R. J., et al. (2006). Surveillance for water-borne disease and outbreaks associated with drinking water and water not intended for drinkingUnited States, 20032004. MMWR. Surveillance Summaries, 55(12), 3165. Lightfoot, D. (2004). Salmonella and other enteric organisms. In J. A. Cotruvo, A. Dufour, G. Rees, J. Bartram, R. Carr, D. O. Cliver, G. F. Craun, R. Fayer, & V. P. J. Gannon (Eds.), Water-borne zoonoses identication, causes, and control (pp. 228241). London: IWA Publishing, World Health Organization. Locas, A., Barthe, C., Margolin, A. B., & Payment, P. (2008). Groundwater microbiological quality in Canadian drinking water municipal wells. Canadian Journal of Microbiology, 54, 472478. Lpez Cuevas, O., Len Flix, J., Jimnez Edeza, M., & Chaidez Quiroz, C. (2009). Detection and antibiotic resistance of Escherichia coli and Salmonella in water and agricultural soil. Revista Fitotecnia Mexicana, 32(2), 119126. Luby, S. P., Faizan, M. K., Fisher-Hoch, S. P., Syed, A., Mintz, E. D., Bhutta, Z. A., et al. (1998). Risk factors for typhoid fever in an endemic setting, Karachi, Pakistan. Epidemiology and Infection, 120, 129138. Lugo-Melchor, Y., Quiones, B., Amzquita-Lpez, B. A., Len-Flix, J., Garca-Estrada, R., & Chaidez, C. (2010). Characterization of tetracycline resistance in Salmonella enterica strains recovered from irrigation water in the Culiacan Valley, Mexico. Microbial Drug Resistance, 16(3), 185190. Luxemburger, C., Duc, C. M., Lanh, M. N., Wain, J., Hien, T. T., Simpson, J., et al. (2001). Risk factors for typhoid fever in Mekong delta, southern Vietnam: A casecontrol study. Transactions of the Royal Society of Tropical Medicine and Hygiene, 95(1), 1923. Lynch, M. F., Blanton, E. M., Bulens, S., Polyak, C., Vojdani, J., Stevenson, J., et al. (2009). Typhoid fever in the United States, 19992006. Journal of the American Medical Association, 302(8), 852869. Maier, R., Pepper, I., & Gerba, C. (2000). Environmental microbiology. Orlando, Florida: Academic Press. Martinez-Urtaza, J., Liebana, E., Garcia-Migura, L., Perez-Pieiro, P., & Saco, M. (2004). Characterization of Salmonella enterica serovar Typhimurium from marine environments in coastal waters of Galicia (Spain). Applied and Environmental Microbiology, 70, 40304034. Martinez-Urtaza, J., Saco, M., de Novoa, J., Perez-Pieiro, P., Peiteado, J., Lozano-Leon, A., et al. (2004). Inuence of environmental factors and human activity on the presence of Salmonella serovars in a marine environment. Applied and Environmental Microbiology, 70, 20892097. Meinersmann, R. J., Berrang, M. E., Jackson, C. R., Fedorka-Cray, P., Ladely, S., Little, E., et al. (2008). Salmonella, Campylobacter and Enterococcus spp.: Their antimicrobial resistance proles and their spatial relationships in a synoptic study of the Upper Oconee River basin. Microbial Ecology, 55(3), 444452. Mermin, J. H., Villar, R., & Carpenter, J. (1999). A massive epidemic of multidrugresistant typhoid fever in Tajikistan associated with consumption of municipal water. The Journal of Infectious Diseases, 179, 14161422. Mezrioui, N., Baleux, B., & Trousselier, M. (1995). A microcosm study of the survival of Escherichia coli and Salmonella Typhimurium in brackish water. Water Research, 29, 459465. Mintz, E., Bartram, J., Lochery, P., & Wegelin, M. (2001). Not just a drop in the bucket: Expanding access to point-of-use water treatment systems. American Journal of Public Health, 91, 15651570. Mohle-Boetani, J. C., Farrar, J., Bradley, P., Barak, J. D., Miller, M., Mandrell, R., et al. (2009). Salmonella infections associated with mung bean sprouts: Epidemiological and environmental investigations. Epidemiology and Infection , 137, 57 366. Momba, M. N., Malakate, V. K., & Theron, J. (2006). Abundance of pathogenic Escherichia coli, Salmonella Typhimurium and Vibrio cholerae in Nkonkobe drinking water sources. Journal of Water and Health, 4(3), 289296. Nasser, A. M., Glozman, R., & Nitzan, Y. (2002). Contribution of microbial activity to virus reduction in saturated soil. Water Research, 36, 25892595. Natvig, E. E., Ingham, S. C., Ingham, B. H., Cooperband, L. R., & Roper, T. R. (2002). Salmonella enterica serovar Typhimurium and Escherichia coli contamination of root and leaf vegetables grown in soils with incorporated bovine manure. Applied and Environmental Microbiology, 68, 27372744. Obi, C. L., Potgieter, N., Bessong, P. O., & Matsaung, G. (2003). Scope of potential bacterial agents of diarrhoea and microbial assessment of quality of river water sources in rural Venda communities in South Africa. Water Science and Technology, 47(3), 5964.

602

C. Levantesi et al. / Food Research International 45 (2012) 587602 Smith, A., Reacher, M., Smerdon, W., Adak, G. K., Nichols, G., & Chalmers, R. M. (2006). Outbreaks of water-borne infectious intestinal disease in England and Wales, 19922003. Epidemiology and Infection, 134(6), 11411149. Srikantiah, P., Girgis, F. Y., Luby, S. P., Jennings, G., Wasfy, M. O., Crump, J. A., et al. (2006). Population-based surveillance of typhoid fever in Egypt. The American Journal of Tropical Medicine and Hygiene, 74, 114119. Srikantiah, P., Vafokulov, S., Luby, S. P., Ishmail, T., Earhart, K., Khodjaev, N., et al. (2007). Epidemiology and risk factors for endemic typhoid fever in Uzbekistan. Tropical Medicine & International Health, 12(7), 838847. Stanwell-Smith, R., Andersson, Y., & Levy, D. A. (2003). National surveillance systems. In P. R. Hunter, M. Waite, & E. Ronchi (Eds.), Drinking water and infectious disease: Establishing the links. Boca Raton, FL: CRC Press. Suresh, K., & Smith, H. V. (2004). Tropical organisms in Asia/Africa/South America. In J. A. Cotruvo, A. Dufour, G. Rees, J. Bartram, R. Carr, D. O. Cliver, G. F. Craun, R. Fayer, & V. P. J. Gannon (Eds.), Water-borne zoonoses identication, causes, and control (pp. 93112). London: IWA Publishing, World Health Organization. Swaddiwudhipong, W., & Kanlayanaphotporn, J. (2001). A common-source waterborne outbreak of multidrug resistant typhoid fever in a rural Thai community. Journal of the Medical Association of Thailand, 84, 15131517. Takkinen, J., Nakari, U. M., Johansson, T., Niskanen, T., Siitonen, A., & Kuusi, M. (2005). A nationwide outbreak of multiresistant Salmonella Typhimurium var. Copenhagen DT104B infection in Finland due to contaminated lettuce from Spain, May 2005. Eurosurveillance Weekly 10 http://www.eurosurveillance.org/ew/2005/050630.asp accessed on 27/5/2011 Taylor, R., Sloan, D., Cooper, T., Morton, B., & Hunter, I. (2000). A water-borne outbreak of Salmonella Saintpaul. Communicable Diseases Intelligence, 24, 336340. Thunberg, R. L., Tran, T. T., Bennett, R. W., & Matthews, R. N. (2002). Research note: Microbial evaluation of selected fresh produce obtained at retail markets. Journal of Food Protection, 65, 677682. Till, D., McBride, G., Ball, A., Taylor, K., & Pyle, E. (2008). Large-scale freshwater microbiological study: Rationale, results and risks. Journal of Water and Health, 6(4), 443460. Tobias, H., & Heinemeyer, E. A. (1994). Occurrence of Salmonella in coastal North Sea water and their hygienic relation to indicator bacteria and sources of contamination. Zentralblatt fr Hygiene und Umweltmedizin, 195(56), 495508. Toze, S. (2004). Pathogen survival in groundwater during articial recharge. In J. Steenvoorden, & T. Endreny (Eds.), Wastewater re-use and groundwater quality (pp. 7084). Wallingford: Int Assoc Hydrological Sciences. Toze, S., Bekele, E., Page, D., Sidhu, J., & Shackleton, M. (2010). Use of static quantitative microbial risk assessment to determine pathogen risks in an unconned carbonate aquifer used for managed aquifer recharge. Water Research, 44, 10381049. Toze, S., Hanna, J., Smith, T., Edmonds, L., & McCrow, A. (2004). Determination of water quality improvements due to the articial recharge of treated efuent. In J. Steenvoorden, & T. Endreny (Eds.), Wastewater re-use and groundwater quality (pp. 5360). Wallingford: Int Assoc Hydrological Sciences. Tran, H. H., Bjune, G., Nguyen, B. M., Rottingen, J. A., Grais, R. F., & Guerin, P. J. (2005). Risk factors associated with typhoid fever in Son La province, northern Vietnam. Transactions of the Royal Society of Tropical Medicine and Hygiene, 99, 819826. Tyrrel, S. F., Knox, J. W., & Weatherhead, E. K. (2006). Microbiological water quality requirements for salad irrigation in the United Kingdom. Journal of Food Protection, 69, 20292035. Vollaard, A. M., Ali, S., Van Asten, H. A., Widjaja, S., Visser, L. G., & Surjadi, C. (2004). Risk factors for typhoid and paratyphoid fever in Jakarta, Indonesia. Journal of the American Medical Association, 291, 26072615. Wall, K., Pang, L., Sinton, L., & Close, M. (2008). Transport and attenuation of microbial tracers and efuent microorganisms in saturated pumice sand aquifer material. Water, Air, and Soil Pollution, 188, 213224. Walters, S. P., Gannon, V. P., & Field, K. G. (2007). Detection of Bacteroidales fecal indicators and the zoonotic pathogens E. coli 0157:H7, Salmonella, and Campylobacter in river water. Environmental Science & Technology , 41 , 18561862. Wry, N., Lhoutellier, C., Ducray, F., Delgens, J. P., & Godon, J. J. (2008). Behaviour of pathogenic and indicator bacteria during urban wastewater treatment and sludge composting, as revealed by quantitative PCR. Water Research, 42, 5362. WHO (2008). Guidelines for drinking-water quality: Third edition incorporating the rst and second addenda. Recommendations, Vol. 1., Geneva: IWA Publishing, World Health Organization. Wilkes, G., Edge, T., Gannon, V., Jokinen, C., Lyautey, E., Medeiros, D., et al. (2009). Seasonal relationships among indicator bacteria, pathogenic bacteria, Cryptosporidium oocysts, Giardia cysts, and hydrological indices for surface waters within an agricultural landscape. Water Research, 43, 22092223. Wineld, M. D., & Groisman, E. A. (2003). Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli . Applied and Environmental Microbiology, 69(7), 36873694. Wray, C., & Wray, K. A. (2000). Salmonella in domestic animals. Oxon, UK: CABI Publishing. Yoder, J., Roberts, V., Craun, G. F., Hill, V., Hicks, L. A., Alexander, N. T., et al. (2008). Surveillance for water-borne disease and outbreaks associated with drinking water and water not intended for drinkingUnited States, 20052006. MMWR Surveillance Summary, 57(9), 3962. Zaleski, K. J., Josephson, K. L., Gerba, C. P., & Pepper, I. L. (2005). Potential regrowth and recolonization of salmonellae and indicators in biosolids and biosolid-amended soil. Applied and Environmental Microbiology, 71, 37013708.

Obi, C. L., Potgieter, N., Musie, E. M., Igumbor, E. O., Bessong, P. O., Samie, A., et al. (2004). Human and environmental-associated non-typhoidal Salmonella isolates from different sources in the Venda region of South Africa. Proceedings of the 2004 Water Institute of Southern Africa (WISA), Biennial Conference, May 2004. Oguntoke, O., Aboderin, O. J., & Bankole, A. M. (2009). Association of water-borne diseases morbidity pattern and water quality in parts of Ibadan City, Nigeria. Tanzania Journal of Health Research, 11(4), 189195. Oluyege, J. O., Dada, A. C., & Odeyemi, A. T. (2009). Incidence of multiple antibiotic resistant Gram-negative bacteria isolated from surface and underground water sources in south western region of Nigeria. Water Science and Technology, 59(10), 19291936. Ozler, H. M., & Aydin, A. (2008). Hydrochemical and microbiological quality of groundwater in West Thrace Region of Turkey. Environmental Geology, 54, 355363. Patchanee, P., Molla, B., White, N., Line, D. E., & Gebreyes, W. A. (2010). Tracking Salmonella contamination in various watersheds and phenotypic and genotypic diversity. Foodborne Pathogens and Disease, 7, 11131120. Pezzoli, L., Elson, R., Little, C. L., Yip, H., Fisher, I., Yishai, R., et al. (2008). Packed with Salmonella Investigation of an international outbreak of Salmonella Senftenberg infection linked to contamination of prepacked basil in 2007. Foodborne Pathogen Disease, 5, 661668. Phan, T. T., Khai, L. T. L., Loc, C. B., Hayashidani, H., Sameshima, T., Watanabe, T., et al. (2003). Isolation of Salmonella strains from the aquatic environment and comparison with those of animal origin in Tan PhuThanh village, Mekong Delta, Vietnam. Japan Agricultural Research Quarterly, 37(4), 237241. Polo, F., Figueras, M. J., Inza, I., Sala, J., Fleisher, J. M., & Guarro, J. (1999). Prevalence of Salmonella serotypes in environmental waters and their relationships with indicator organisms. Antonie Van Leeuwenhoek, 75, 285292. Pond, K. (2005). Water recreation and disease infections: Plausibility of associated acute effects, sequelae and mortality. London: IWA Publishing, World Health Organization. Popoff, M. Y. (2001). Antigenic formulas of the Salmonella serovars (8th ed.). Paris, Institut Pasteur: WHO Collaborating Centre for Reference and Research on Salmonella. Potgieter, N., Obi, C. L., Bessong, P. O., Igumbor, E. O., Samie, A., & Nengobela, R. (2005). Bacterial contamination of VhuswaA local weaning food and stored drinkingwater in impoverished households in the Venda Region of South Africa. Journal of Health, Population and Nutrition, 23(2), 150155. Rhodes, M. W., & Karton, H. (1988). Survival of E. coli and Salmonella spp. in estuarine environments. Applied and Environmental Microbiology, 54, 29022907. Risebro, H. L., Doria, M. F., Andersson, Y., Medema, G., Osborn, K., Schlosser, O., et al. (2007). Fault tree analysis of the causes of water-borne outbreaks. Journal of Water and Health, 5(1), 118. Rizzo, C., Santantonio, M., Coscia, M. F., Monno, R., De Vito, D., & Rizzo, G. (2008). Typhoid fever in Italy, 20002006. Journal of Infection in Developing Countries, 2(6), 466468. Savichtcheva, O., & Okabe, S. (2006). Alternative indicators of fecal pollution: Relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Research, 40, 24632476. Savichtcheva, O., Okayama, N., & Okabe, S. (2007). Relationships between Bacteroides 16S rRNA genetic markers and presence of bacterial enteric pathogens and conventional fecal indicators. Water Research, 41, 36153628. Schets, F. M., van Wijnen, J. H., Schijven, J. F., Schoon, H., & de RodaHusman, A. M. (2008). Monitoring of water-borne pathogens in surface waters in Amsterdam, the Netherlands, and the potential health risk associated with exposure to Cryptosporidium and Giardia in these waters. Applied and Environmental Microbiology, 74, 20692078. Schikora, A., Carreri, A., Charpentier, E., & Hirt, H. (2008). The dark side of the salad: Salmonella typhimurium overcomes the innate immune response of Arabidopsis thaliana and shows an endopathogenic lifestyle. PloS One, 3(5), e2279. Schriewer, A., Miller, W. A., Byrne, B. A., Miller, M. A., Oates, S., Conrad, P. A., et al. (2010). Presence of Bacteroidales as a predictor of pathogens in surface waters of the central California coast. Applied and Environmental Microbiology , 76, 58025814. Schuster, C. J., Ellis, A. G., Robertson, W. J., Charron, D. F., Aramini, J. J., Marshall, B. J., et al. (2005). Infectious disease outbreaks related to drinking water in Canada, 1974 2001. Canadian Journal of Public Health, 96(4), 254258. Sharma, P. K., Ramakrishnan, R., Hutin, Y., Manickam, P., & Gupte, M. D. (2009). Risk factors for typhoid in Darjeeling, West Bengal, India: Evidence for practical action. Tropical Medicine & International Health, 14(6), 696702. Simental, L., & Martinez-Urtaza, J. (2008). Climate patterns governing the presence and permanence of Salmonella in coastal area of Bahia de Todos Santos Mexico. Applied and Environmental Microbiology, 74, 58185924. Sinton, L., Hall, C., & Braithwaite, R. (2007). Sunlight inactivation of Campylobacter jejuni and Salmonella enterica, compared with Escherichia coli, in seawater and river water. Journal of Water and Health, 5(3), 357365. Sivapalasingam, S., Barrett, E., Kimura, A., Van Duyne, S., De Witt, W., Ying, M., et al. (2003). A multistate outbreak of Salmonella enterica Serotype Newport infection linked to mango consumption: Impact of water-dip disinfestation technology. Clinical Infectious Diseases, 37(12), 15851590. Sivapalasingam, S., Friedman, C. R., Cohen, L., & Tauxe, R. V. (2004). Fresh produce: A growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. Journal of Food Protection, 67(10), 23422353.