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Salmonella in surface and drinking water: Occurrence andwater-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, Italyb Department of Environment and Primary Prevention, Hygiene of Internal Water Unit, ISS, viale Regina Elena 299-00161, Rome, Italyc Department of Infectious Diseases, University Medical Center Freiburg, Hugstetter Strasse 55, 79106 Freiburg, Germanyd CSIRO EcoSciences Precinct, Dutton Park 41 Boggo Road, Dutton Park, QLD 4102, Australia

⁎ Corresponding author. Tel.: +39 06 90672781; fax:E-mail address: [email protected] (C. Levantesi).

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Article history:Received 16 March 2011Accepted 23 June 2011Available online xxxx

Keywords:Water-borne outbreaksSalmonellaTyphoid feverSurface waterMultiple drug resistanceDrinking water

Salmonella is one of the leading causes of intestinal illness all over the world as well as the etiological agent ofmore severe systemic diseases such as typhoid and paratyphoid fevers. While water is known to be a commonvehicle for the transmission of typhoidal Salmonella serovars, non-typhoidal salmonellae are mainly known asfoodborne pathogens. This paper provides a brief review of the last ten years of peer reviewed publications onthe prevalence of Salmonella in natural freshwaters and drinkingwaters, and on the relevance of these sourcesfor Salmonella dissemination. In industrialized countries, Salmonella was rarely reported in water-borneoutbreaks despite it being frequently detected in surface waters including recreational waters and watersused for irrigation or as a drinking water source. Consistent contamination with irrigation waters has beenshown to be a common route of crop contamination in produces related Salmonella outbreaks. Multiple drugresistant (MDR) Salmonella strains, that represent an increased hazard for human health and that maycontribute to the dissemination of drug resistances were also detected in surface water in developedcountries. 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 tosurface waters, emphasizing the role of wild life animals in water contamination. Data relating to Salmonellaprevalence in surface and drinking water in developing countries are quite rare. Nevertheless, data on water-borne outbreaks as well as case control studies investigating the risk factors for endemic typhoid feverconfirmed the relevance of water as source for the transmission of this disease. In addition epidemiologicalstudies and Salmonella surveys, consistently provided an undeniable evidence of the relevance of MDRSalmonella Typhi strains in water-borne typhoid fever in developing countries.

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Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 02. Water-borne Salmonella infections and control strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

2.1. Developing countries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 02.2. Developed countries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 02.3. Control strategies to prevent Salmonella drinking water related transmission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

3. Role of contaminated waters in Salmonella foodborne outbreaks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 04. Salmonella prevalence, diversity in surface, drinking water and groundwater . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

4.1. Surface waters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 04.2. Diversity of Salmonella strains isolated from surface waters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 04.3. Drinking water and groundwater . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

5. Salmonella survival and monitoring in water environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 05.1. Salmonella survival . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 05.2. Conventional and alternative microbial indicators for Salmonella monitoring in aquatic environment . . . . . . . . . . . . . . . . . . 0

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6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

1. Introduction

One third of the world's population live in countries with somelevel of water stress and water scarcity is expected to increase in thenext few years due to increases in human population, per capitaconsumption and the resulting impacts of human activity on theenvironment (Asano, Burton, Leverenz, Tsuchihashi, & Tchobanoglous,2007). The availability of good quality water sources is thereforegetting more and more limited and the impact of water-bornepathogens in human health is expected to be significant (Suresh &Smith, 2004). It is therefore critical to understand the relevance ofnatural and drinkingwater contribution to transmission of pathogenicmicroorganisms.

Salmonella is a ubiquitous enteric pathogen with a worldwidedistribution that comprises a large number of serovars characterizedby different host specificity and distribution. This microorganism isone of the leading causes of intestinal illness through the world aswell as the etiological agent of more severe systemic diseases such astyphoid and paratyphoid fever (Pond, 2005). Zoonotic salmonellae arecommonly described as foodborne pathogens, however, drinkingwater as well as natural waters are known to be an important sourcefor the transmission of these enteric microorganisms (Ashbolt, 2004;Leclerc, Schwartzbrod, & Dei-Cas, 2002). Salmonella, just like otherenteric bacteria, is spread by the fecal–oral route of contamination.This microorganism can enter the aquatic environment directly withfeces of infected humans or animals or indirectly, e.g., via sewagedischarge or agricultural land run off. Overall Salmonella spp. andsubspecies can be found in a large variety of vertebrates. Besidehumans, animal sources of Salmonella include pets, farm animals andwild animals; calves, poultry, pigs, sheep as well as wild birds (seagull, pigeon) and reptiles can all be reservoirs of Salmonella (Dolejská,Bierosová, Kohoutová, Literák, & Cízek, 2009; Lightfoot, 2004; Wray &Wray, 2000). Plants, insects and algae were also found capable ofharboring Salmonella and might be implicated in the transmission ofthis 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. Theyare usually present in large numbers in raw sewage (103–104 CFU/L)and can still be present in wastewater effluent after advancedsecondary treatment including coagulation, filtration and disinfection(Maier, Pepper, & Gerba, 2000; Wéry, Lhoutellier, Ducray, Delgenès, &Godon, 2008). Soil and sediment were also found to harborsalmonellae (Abdel-Monem & Dowidar, 1990; Gorski et al., 2011;Tobias & Heinemeyer, 1994) and sediment particles are believed tofunction as a micro ecological niche enhancing salmonellae survival inlakes (Chandran et al., 2011). In the aquatic environment thispathogen has been repeatedly detected in various types of naturalwaters such as rivers, lakes, coastal waters, estuarine as well ascontaminated ground water (Haley, Cole, & Lipp, 2009; Levantesiet al., 2010; Martinez-Urtaza et al., 2004; Martinez-Urtaza, Liebana,Garcia-Migura, Perez-Piñeiro, & Saco, 2004; Polo et al., 1999; Wilkeset al., 2009).

In addition to its widespread occurrence, elevated survivalcapacities in non-host environment have been reported for Salmonella(Winfield & Groisman, 2003). The growth of Salmonella in non-hostenvironments such as wastewater sludge and compost has also beenreported (Zaleski, Josephson, Gerba, & Pepper, 2005) and the growthof Salmonella in water supplies is also considered possible, due to itsability to colonize surfaces and replicate in biofilms of distribution

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

system pipes (Jones & Bradshaw, 1996). However, standard disinfec-tion procedures used in drinking water treatment processes are activeagainst salmonellae (Cicmanec, Smith, & Carr, 2004).

Taxonomically the genus Salmonella comprises two speciesnamely S. bongori and S. enterica. The species S. enterica is furtherdifferentiated in to six subspecies (enterica, salamae, arizonae,diarizonae, indica and houtenae) among which the S. entericasubspecies enterica is mainly associated to human and other warmblooded vertebrates. Traditionally members of the genus Salmonellaare clustered in serovars according to their flagellar (h) and somatic(o) antigens. Currently over 2400 Salmonella serovars have beendescribed but only about 50 serovars, all within the subspeciesenterica, are common causes of infections in humans and warmblooded animals (Popoff, 2001). Salmonella serovars have differenthost specificity, diverse geographic distribution, and cause differentsyndromes. On the basis of the clinical syndromes caused Salmonellaare divided in to two distinct groups namely the typhoidal and non-typhoidal Salmonella serovars (Pond, 2005).

Enteric fevers, typhoid and paratyphoid fever are severe, conta-gious systemic diseases caused by the infection of the serovars Typhiand Paratyphi. Even though not common in developed countries,enteric fevers remain an important and persistent health problem inless industrialized nations. Overall, in 2003 an annual incidence ofapproximately 17 million cases of typhoid and paratyphoid fevers wasreported worldwide (Kindhauser, 2003). Differently from otherSalmonella serovars, Typhi and Paratyphi are host adapted and canonly infect humans; stools of infected persons are therefore theoriginal source of contaminations for these pathogens. Watercontaminated with feces of human cases and carriers is one of themain vehicles of typhoid fever infections.

Differently from typhoidal Salmonella strains, non-typhoidalsalmonellae, the ubiquitous subtypes found in a number of animalspecies, are more frequently associated to foodborne than to water-borne transmission. These zoonotic Salmonella serovars tend to causeacute but usually self-limiting gastroenteritis. In some patients,however, these same serovars can cause severe systemic diseasessuch as osteomyelitis, pneumonia and meningitis (Pond, 2005).Severe and invasive presentations of non-typhoidal salmonellosis inAfrica 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 andTyphimurium was associated to the observed incidence of invasivesalmonellosis (Gordon & Graham, 2008).

The increased frequency of MDR Salmonella strains in humaninfections is an emerging issue of major health concern (Lightfoot,2004; Lynch et al., 2009; Pond, 2005). As a consequence, the possiblerole of fecally contaminated waters in the dissemination of MDRSalmonella, both typhoidal and non-typhoidal, as well as antibioticresistance genes though horizontal gene transfer is of great interest.This issue is of particular concern in developing countries where thecommon use of untreated, low quality water as drinking watersources together with inappropriate use and self-prescribing ofantibiotics increase the risk of drug resistance and the probability ofwide dissemination of resistant strains of high human health concern(Oluyege, Dada, & Odeyemi, 2009; Srikantiah et al., 2007).

Overall, the above reported characteristics suggest that watermight be an important source for the transmission of all salmonellae,not only for the typhoid serovars. An increased knowledge on theprevalence, diversity and survival of this enteric bacterium in theenvironment, together with a proper assessment, trough effective

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surveillance and epidemiological studies, of the relevance of the waterenvironment in the transmission of Salmonella disease is desirable. Inthis respect the possible involvement of water in food contaminationis also of great interest.

This paper provides a brief review of our understanding of thecontribution of natural fresh water and drinking water as a route ofSalmonella contamination. Initially epidemiological data on thewater-mediated transmission of Salmonella infections and on the possiblestrategies to control these diseases are described. Successively recentliterature relating to Salmonella prevalence, diversity, and survival insurface water and drinking water is summarized. Finally, a shortoverview of the most relevant emerging issues which the scientificcommunity is actually addressing in relation to Salmonella in waterenvironments is given. In particular the importance of waterenvironment in the transmission of drug resistant Salmonella strainsand the possible role of water in fresh food contamination aredescribed. Furthermore the use and the evaluation of alternative fecalindicators of water contamination for Salmonella monitoring inaquatic environment is reported. Considering that limited scientificpublications exist that report the presence of Salmonella in waterwhen compared to reports of Salmonella in food, peer reviewedscientific 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 inrespect to Salmonella water-mediated infections: the description ofwater-borne salmonella outbreaks (Berg, 2008; Bhunia et al., 2009;Farooqui, Khan, & Kazmi, 2009; Franklin et al., 2009; Kozlica, Claudet,Solomon, Dunn, & Carpenter, 2010; Swaddiwudhipong & Kanlayana-photporn, 2001; Taylor, Sloan, Cooper, Morton, & Hunter, 2000) andthe analysis of risk factors associated with endemic or sporadicSalmonella 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 scientific publications, reports of national surveillancesystems, such as Communicable Disease Surveillance Centre (CDSC,United Kingdom) and Centers for Disease Control and Prevention andEnvironmental Protection Agency (CDC/EPA USA), provide useful dataon salmonellae water-borne disease outbreaks (Craun et al., 2010;Dale, Kirk, Sinclair, Hall, & Leder, 2007; Smith et al., 2006). The leveland quality of water-borne disease surveillance data, however, variesin different countries. In particular the situation in developingcountries is problematic due to the lack of laboratory facilities andthe scarcity of economic resources, however surveillance systems inmany European countries have also been judged incapable ofdetecting 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 developingcountries relate mostly the typhoid Salmonella serovars. In the lessindustrialized area of the world, in particular in the Indian sub-continent and South East Asia, typhoid and paratyphoid fevers occurboth in epidemic and endemic form, and remain a major public healthproblem (DeRoeck, Jodar, & Clements, 2007). The burden of typhoidfever worldwide is further compounded by the spread of multipledrug resistant S. Typhi (Kim, 2010; Lynch et al., 2009; Srikantiah et al.,2006; Swaddiwudhipong & Kanlayanaphotporn, 2001). Most of therecent publications on typhoid and paratyphoid fever water-borneinfections in developing countries are from the Asian continent(Bhunia et al., 2009; Farooqui et al., 2009; Gasem et al., 2001; Kimet al., 2003; Lewis et al., 2005; Luxemburger et al., 2001; Mermin,Villar, & Carpenter, 1999; Sharma et al., 2009; Srikantiah et al., 2007;

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

Swaddiwudhipong & Kanlayanaphotporn, 2001; Tran et al., 2005;Vollaard et al., 2004). Very few or no publication from Africa andCentral/Latin America, respectively, addressed the role of water asvehicle of Salmonella transmission in the last ten years.

Reports on typhoid and paratyphoid fever epidemics in Asiaconsistently indicate that contamination of drinking water, sourcedfrom well water (Farooqui et al., 2009), piped municipal drinkingwater (Bhunia et al., 2009; Kim et al., 2003; Lewis et al., 2005; Merminet al., 1999) and unboiled spring water (Swaddiwudhipong &Kanlayanaphotporn, 2001) was the main source of outbreaks. Inaddition 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-borneepidemics. Mermin et al. (1999) reported a massive epidemic of MDRtyphoid fever in Dushanbe, Tajikistan, associated with the consump-tion of municipal water. In the first half of the year 1997, 8901 cases oftyphoid fever and 95 associated deaths were reported in Dushanbe. Acase–control study demonstrated that Salmonella Typhi infection wasassociated with drinking unboiled water or obtaining water fromsources outside the house. Lack of chlorination, equipment failure,and back-siphonage in the water distribution system led to contam-ination of the drinking water (Mermin et al., 1999). Of 29 Salmonellaserovar Typhi isolates tested, 27 were resistant to seven antibiotics,namely to ampicillin, chloramphenicol, nalidixic acid, streptomycin,sulfisoxazole, tetracycline, and trimethoprim-sulfamethoxazole. Al-though 93% of the tested Salmonella serovar Typhi isolates fromDushanbe were resistant to antimicrobials commonly used fortyphoid fever, the case mortality rate of 1.0% was rather low (Merminet al., 1999).

Farooqui et al. (2009) reported the study of a community outbreakof typhoid fever associated with drinking water in a village close toKarachi, Pakistan. This outbreak claimed three human lives and leftmore than 300 people infectedwithin a oneweek. The infected peopleconsumed water from a well that was the only available source ofdrinking water in the village. Epidemiological investigations revealedthe gross contamination of the well with dead and decaying animalbodies, their fecal material and garbage. Microbiological testingconfirmed the presence of MDR strains of Salmonella serovar Typhiin 100% of the well water samples and 65% of household watersamples (Farooqui et al., 2009). In the summer of 2002 during a 7-week 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 ofMDR typhoid fever reported so far. The outbreak was traced withmolecular epidemiological methods to a single source—the solemunicipal water supply. A total of 90% of the isolates wereresistant to more than one antibiotic. MDR S. Typhi were also foundto be the etiological agent in a water-borne outbreak in a non-endemic 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 sporadictyphoid fevers in Asia confirmed the association between this diseaseand 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 inUzbekistan and unboiled surface water in Vietnam, respectively, as amajor risk factor for typhoid fever. Srikantiah et al. (2007) alsoshowed that MDR Salmonella Typhi strains were important inendemic typhoid fever in the Samarkand region of Uzbekistan. Theyfound that multiple antimicrobial resistance to ampicillin, chloram-phenicol, and trimethoprim-sulfamethoxazole, were in 6 (15%) of 41Salmonella serovar Typhi isolates from patients. Furthermore recentconsumption of antimicrobials (two weeks preceding illness) addi-tionally increased the risk of infection (Srikantiah et al., 2007). InSeramang city and the surrounding area (Indonesia), typhoid fever

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was associated with living in a house without water supply from themunicipal network along with the use of low quality water forwashing and drinking (Gasem et al., 2001). Finally, Sharma et al.(2009) showed that the unsafe use of water, namely scooping outwater from containers instead of using piped water or water stored ina narrow mounted container at home, was associated with typhoidfever. Using GIS to explore the epidemiological pattern acrossVietnam by investigating the risk factors associated with shigellosis,typhoid, and cholera, Kelly-Hope et al. (2007) revealed that typhoidfever prevailed in theMekong River Delta. They observed that typhoidfever was mostly associated with high vapor pressure and the use ofriver and streams as drinking water. On the contrary, forested regionsand public tap drinking water were found to be negatively associatedwith typhoid fever. In contrast to this, Vollaard et al. (2004) showedthat fecally contaminated drinking water was not associated withtyphoid and paratyphoid fevers in Jakarta Indonesia. However, in thisstudy, the habit of boiling water before consumption was declared byall the people surveyed, both test cases and control sources, possiblyexplaining the lack of association between microbiological contam-ination of drinking water and typhoid fever. Vollaard et al. (2004) alsoshowed that typhoid fever was significantly associated with consum-ing ice cubes and iced drinks highlighting this as a likely watermediated route of transmission. The importance of ice cubes as apotential source of typhoid infection is supported by other studies inwhich it was shown that consumption of ice cubes (Gasem et al.,2001), flavored ice drinks (Black et al., 1985) and ice creams (Lubyet al., 1998) are risk factors for this disease. In agreement with theseobservations was the report that prolonged survival of Salmonella inice (Butler, Mahmoud, & Warren, 1977; Dickens, DuPont, & Johnson,1985).

Nevertheless most of the recent risk factor studies showed that useof unsafe water was not the only risk factor associated withtyphoid/paratyphoid fever thus indicating multiple routes of trans-mission for these diseases (Gasem et al., 2001; Sharma et al., 2009;Vollaard et al., 2004). Interestingly, Vollaard et al. (2004) showed thatin Jakarta typhoid and paratyphoid fevers are associated withdifferent routes of transmission. Risk factors for typhoid andparatyphoid fevers, respectively, were mainly within and outsidethe household.

As in other developing countries, in Africa, Salmonella Typhi is amajor cause of enteric disease, particularly in children (Crump, Luby,& Mintz, 2004). The real burden of typhoid fever in Africa is largelyunknown because of the lack of comprehensive surveillance studiesand credible measures of the disease incidence. However, a meanincidence of 50 cases per 100,000 persons per year has been estimatedfor the whole continent with a highest value in South Africa(N100/100,000 cases/year) (Crump et al., 2004). Even if typhoidfever can be considered an endemic disease in Africa very few studiesrelating to Salmonella Typhi waterborne transmission in this conti-nent are available in the recent literature.

In Nigeria, Oguntoke, Aboderin, and Bankole (2009) investigatedrelationships between water-borne diseases, morbidity patterns,drinking water source quality and water handling practices in IbadanCity. Oguntoke et al. found that typhoid fever was the most commonwater-borne disease (39.3%) in the area followed by bacillarydysentery and cholera. In agreement with the hypothesized watermediated route of transmission about 50% of the analyzed water-borne diseases infections occurred in the heavy rain period (Oguntokeet al., 2009). In Ibadan City Salmonella Typhi and Paratyphi weredetected in the well waters and themicrobial water quality was foundto be positively correlated with the pattern of water-borne diseasewithin the selected areas. Additionally multivariate regressionanalysis showed that the percentage of residents applying inadequatedomestic water treatment (mostly potash alum addition) explained68.6% (Pb0.04) of the pattern of waterborne diseases morbidity in thearea (Oguntoke et al., 2009). The spatial distribution of diarrhea and

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

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, arural area, is characterized by the lack of clean potable water and theinadequacy of sanitation (Obi et al., 2004; Potgieter et al., 2005). Usinga stratified random-sampling approach, the study identified asignificant clustering of diarrhea cases to two water extraction pointswhich were of poor microbial quality and contained potentialdiarrhea-causing organisms including Salmonella (Bessong et al.,2009).

In many African countries MDR non-typhoidal salmonellae arereported to be the commonest cause of bacteraemia in children under5 years (Gordon & Graham, 2008). Life-threatening invasive diseaseoutbreaks in children caused byMDR non-typhoidal salmonellae havebeen reported in several African countries (e.g. Graham, 2002; Kariukiet al., 2006). Nevertheless the sources and mode of transmission ofnon-typhoidal salmonellae in Africa are still unknown. In a prospec-tive study in Kenya, Kariuki et al. (2006) compared the serovars andgenotypes of non-typhoidal salmonellae isolates from children withbacteraemia, from family contacts, and from home environmentalsamples. Salmonella isolates from family contacts showed the highestsimilarity to those of clinical cases indicating that human-to-humantransmission route plays a major role in non-typhoidal salmonellaetransmission in the area. Nevertheless, clustering of non-typhoidalSalmonella bacteraemia in the rainy season in Africa suggests thatthere 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 industrializednations, most of the data on water-borne salmonellae in developedcountries involve non-typhoidal Salmonella serovars. In many indus-trialized countries, the widespread implementation of municipalwater and sewage treatment systems in the second half of the 20thcentury has resulted in a dramatic decline in the incidence of water-borne typhoid fever (Lynch et al., 2009; Smith et al., 2006). Even ifthey remain endemic in a few geographic regions (Rizzo et al., 2008),typhoid and paratyphoid fever are now rare diseases, mainlyassociated with people returning from foreign travel to regionswhere these diseases are still much more common (Lynch et al.,2009).

In the USA since 1971, the CDC, in collaboration with the EPA andwith the Council of State and Territorial Epidemiologists, began asurveillance program to collect and report data of water-borneoutbreaks. According to the CDC data from 1971 to 2000, non-typhoidal zoonotic Salmonella were the causes of 15 drinking-water-borne outbreaks which accounted for 6% of the total zoonotic water-borne outbreaks in the USA (Craun, Calderon, & Craun, 2004). Asrevised by these authors, most of these salmonellae outbreaks (11/15)were associated with community water systems and groundwaterinstead of surface water. In the same period, the use of untreatedgroundwater along with inadequate treatment of collected ground-water and distribution systems contamination were the mostimportant deficiencies identified for causing outbreaks of entericbacteria. Further analysis has shown that various Salmonella subspe-cies, comprising Typhimurium, Enteriditis, Bareilly, Javiana, Newportand Weltervreden, were the causes of water associated Salmonellaoutbreaks in the USA (Craun et al., 2004). From 2000 to 2006salmonellae were found very rarely or not at all in drinking water-borne outbreaks in USA (Blackburn et al., 2004; Liang et al., 2006;Yoder et al., 2008). Nevertheless, two recent outbreaks indicated thatwater-borne salmonellae are still of health concern in cases ofdeficiency of water treatment or inadequate water supply systems inthe USA (Berg, 2008; Kozlica et al., 2010). In August 2008, the healthdepartment and regulatory officials identified an outbreak of

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Salmonella I 4,[5],12:i:– involving five persons in a rural community inTennessee. An untreated water supply was recognized as the source ofinfection. It was found that thewater, which had been collected from aspring, had been stored in a small unprotected reservoir subject tocontamination from runoff and wildlife (Kozlica et al., 2010). In thesecond reported case during March and April 2008, an outbreak ofwater-borne disease associated with Salmonella struck the city ofAlamosa in Colorado. Salmonellae were found to have contaminatedthe public water system that supplies drinking water to thecommunity. The outbreak resulted in 442 reported illnesses, 122 ofwhich were laboratory-confirmed, and one death. Epidemiologicalestimates suggested that up to 1300 people may have been ill (Berg,2008). Alamosa's drinking water comes from deep artesianwells in anaquifer considered to be a protected groundwater source. Prior to theoutbreak, the city's drinking water was not chlorinated for disinfec-tion but was historically in compliance with all health-based drinkingwater standards. The most probable cause of the outbreak was acontamination of a ground-level water storage reservoir by animalfeces that successively spread throughout the entire system. Thereservoir was found to have several small cracks and holes that likelyallowed the contamination source to enter.

Only one Salmonella water-borne outbreak related to recreationalwater exposure was recorded by the CDC between 1995 and 2005(Levy, Bens, Craun, Calderon, & Herwaldt, 1998; Pond, 2005). On thecontrary, recreational aquatic environments, both salt and freshwaters, were indicated as the most important risk factor for sporadicchildhood Salmonella infections at three Washington state countyhealth departments (Denno et al., 2009). Denno et al. (2009)conducted a prospective case control study to investigate the possibleassociation between sporadic childhood reportable enteric infectionsand different plausible exposures. Infection with Salmonella wasfound to be strongly related to playing or swimming in natural watersources. In addition, associations between the use of private well ashome drinking water sources and the use of septic systems for homewastewater disposal were also observed as potential sources ofSalmonella infections.

In Australia, salmonellae were found to be the most commonpathogen in drinking water-borne outbreaks from 2001 to 2007 (Daleet al., 2007). Salmonella spp. were implicated in five of 10 observeddrinking water-borne outbreaks and in an outbreak derived from acontaminated aquarium. The serovars Saintpaul, Typhimurium, subspIIIb 61:i:z35, Muenchen and Para B bv java, were identified asoutbreak causes. Differently from what has been observed in the USAwhere Salmonella outbreaks were mostly related to contaminatedcommunity water systems, in Australia contaminated tank and borewaters were identified as the origin of outbreaks. Ashbolt and Kirk(2006) conducted a case control study to investigate risk factors forsporadic Salmonella Mississippi infections in Tasmania (Australia)showing that the exposure to untreated drinking water was a riskfactor for this disease. These authors also highlighted that most of theexposures to untreated drinking water were recorded as exposure towater collected in rainwater collection tanks. Roof collected rainwater were involved in several other water-borne outbreaks bySalmonella in Australia (Franklin et al., 2009; Taylor et al., 2000)suggesting that appropriate preventive measures must be undertakento avoid that the increased use of rainwater tanks may increase therisk of water-borne disease outbreaks (Franklin et al., 2009).

In Europe, monographic water-borne outbreaks reports such asthose of CDC/EPA, are not available because drinking water is definedas food and thus included in foodborne outbreaks reporting. Countryspecific review of water-borne outbreaks in Italy (Blasi et al., 2008)and the UK (Smith et al., 2006) were recently published. According tothe complete surveillance data of Communicable Disease SurveillanceCentre (CDSC), Salmonella was never associated to water-borneoutbreaks in England and Wales from 1992 to 2003 (Smith et al.,2006). In contrast, salmonellae were implicated in outbreaks that

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

occurred in Italy from 1998 to 2005. However because thesurveillance system on communicable diseases in Italy is not plannedto efficiently identify water-borne outbreaks, the number of reportedcases do not represent an accurate clear estimation of the realsituation (Blasi et al., 2008).

2.3. Control strategies to prevent Salmonella drinking water relatedtransmission

As for other water-borne pathogens, different measures can beadopted to hinder the spread of Salmonella in water environment, andconsequently reduce human risk of infection. Regarding the measuresto reduce the occurrence of Salmonella in drinking water, the controlstrategies have to be elaborated and adopted on the basis of the waterresource availability and the economic and developmental level of thecountry. For this purpose, the World Health Organization hasdeveloped Guidelines for Drinking Water Quality, which provides aninternationally harmonized support to help countries develop rulesand 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 usechemical and solar disinfection, safe water storage and behavioralchanges are indicated as reliable options to directly target the mostaffected population and reduce water-borne disease burden throughimproved drinking water quality (Mintz, Bartram, Lochery, &Wegelin, 2001). In this respect, three recent reviews that usedmeta-analysis to evaluate the effect of water treatment at point of useon water quality and diarrhea reduction showed that point of useinterventions more efficiently reduced diarrhea incidence, withrespect 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 endemicsand epidemics infections confirm that simple decentralized controlstrategies might be effective in the control of these diseases (Sharmaet al., 2009; Srikantiah et al., 2007). According to the findings ofSharma et al. (2009) home chlorination of drinking water, the use ofnarrow-mounted containers for safe water storage, and drawing outwater by tilting the container or using taps to avoid contaminationmay be effective practices to avoid spread of typhoid in west BengalIndia. Farooqui et al. (2009) reportedmeasures recently introduced byWHO that include solar disinfection, bleach addition, boiling, and useof low cost ceramic filters, which are well suited to prevent typhoidfever outbreaks due to the consumption of contaminated surface ordrinking water.

Education regarding the risk of drinking untreated surfacewater aswell as promoting the use of boiled drinkingwater carried from home,was indicated by Srikantiah et al. (2007) as practical interventionmeasures to reduce water related transmission of typhoid fever inSamarkand (Uzbekistan). Srikantiah et al. (2007) also suggestedspecific intervention strategies to reduce the increased risk linked toMDR typhoid strains. According to their results the use of antimicro-bials two weeks before onset of typhoid fever was independentlyassociated to this disease; hence the development of primary careclinical treatment guidelines to reduce unnecessary antimicrobialexposure may efficiently decrease the risk of typhoid fever.

In many industrialized countries, the success of applied controlstrategies is confirmed by the small number of water-borne outbreakscaused by salmonellae. Nevertheless, outbreaks caused by microbialcontamination of drinking water still result in substantial human andeconomic costs in these countries (Berg, 2008; Risebro et al., 2007).The identification of the causes outbreaks and the potential threats towater quality is necessary to formulate effective prevention strategiesthat will minimize the further onset of outbreaks and related costs.Causes of water-borne outbreaks in developed countries have beenextensively 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 considerthe enteric bacteria as a whole and specific deficiencies associated tosalmonellae water-borne outbreaks could not be extrapolated.Schuster et al. (2005) analyzed 288 cases of drinking water relatedoutbreaks in Canada from 1974 to 2001 showing that water treatmentfailure and contamination from wildlife were the causative factorsmost often cited in outbreak reports. Analyzing water-borne out-breaks of enteric diseases associated with EU public drinking watersupplies (1990–2005), Risebro et al. (2007) found that contaminationof source water and failure of water treatment accounted for morethan 50% of the recorded outbreaks. In particular they found thatdisinfection deficiencies were associated with 75% of outbreaks due tobacterial, viral and mixed pathogen contamination (Risebro et al.,2007). In their complete review of drinking water associatedoutbreaks in USA (1971–2006) Craun et al. (2010) showed, interalias, that greater attention is needed to address and reduce the risk ofoutbreaks in groundwater supplied systems and in private watersystems. Overall it is apparent that the diversity of causative factors ofoutbreaks in different countries requires different specific controlactions. The control is essentially carried out through application ofprocess control measures, which are provided by theWHO Guidelines(WHO, 2008). The approach that has been proposed is the “HazardAnalysis Critical Control Points” (HACCP) approach, which prioritizesthe identification of key potential contamination or control points inthe treatment and distribution system. This approach has alreadybeen successfully used by the food and beverage industry, it allowsoperators and authorities to focus their resources on monitoringcrucial points to detect and quickly correct any deviation from acorrectly operating system. Another successful approach, which iscombined with HACCP principles, is the multi-barriers approach.Different steps are selected in the treatment process in order toincrease removal capability and normal fluctuations in performancecan be compensated. In this way the likelihood that pathogens canenter the distribution system and reach consumers is minimized. Thetwo approaches together constitute a water safety framework that is abasic structure to develop supply-specific water safety plans to ensurethe production of high quality drinking water. In agreement with this,the EPA's Ground Water Rule (USEPA, 2006) establishes a risktargeted approach to identify those systems that may be mostsusceptible to fecal contamination and specifies corrective actions(Craun et al., 2010).

3. Role of contaminated waters in Salmonella foodborneoutbreaks

In recent years, reports of Salmonella outbreaks related to freshproduce consumption have illustrated the likely relationshipsbetween salmonellae, water and ultimately foodborne Salmonellainfections (CDC, 2002, 2008; Greene et al., 2008; Mohle-Boetani et al.,2009; Sivapalasingam et al., 2003). It is now commonly accepted thatfruit and vegetable consumption is a risk factor for infections withenteric pathogens (Heaton & Jones, 2007). Three recently publishedreviews clearly summarized the current knowledge on the role offresh produces as source for the transmission of human entericpathogens (Berger et al., 2010; Heaton & Jones, 2007), and inparticular of Salmonella (Hanning, Nutt, & Ricke, 2009). Salmonella isthe most common aetiological agents associated to fresh producerelated infections (Heaton & Jones, 2007; Sivapalasingam, Friedman,Cohen, & Tauxe, 2004). A wide spectrum of produce have beenassociated with salmonellae infections including tomatoes (Greeneet 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).

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

Salmonellae are often isolated from produce samples in routinesurveys (Thunberg, Tran, Bennett, & Matthews, 2002). Additionallysome S. enterica strains have the ability to adhere to plant surfaceswhere they are able to survive for long periods and then grow(Gandhi, Golding, Yaron, & Matthews, 2001; Islam et al., 2004). Thecapacity of this pathogen to become endophytic, thus to invadeinternal plant parts has also been reported (e.g. Deering, Pruitt,Mauer, & Reuhs, 2011; Klerks, Franz, van Gent-Pelzer, Zijlstra, & vanBruggen, 2007; Lapidot & Yaron, 2009; Schikora, Carreri, Charpentier,& Hirt, 2008). Among others Lapidot and Yaron (2009) demonstratedthe ability of S. enterica serovar Typhimurium to transfer fromcontaminated irrigation water in plant roots and then into the edibleparts of mature parsley. However the transfer of S. enterica serovarTyphimurium from water to plants was shown only to occur withhighly contaminated irrigation water (Lapidot & Yaron, 2009).

Water is likely to be an important source of produce contam-ination in the field as well as in post harvested processing (Berger etal., 2010). Water sources of varying microbiological quality areused for irrigation of produce worldwide. For example, in the UK,71% of irrigation water is obtained from surface waters whichreceive treated sewage effluent (Tyrrel, Knox, & Weatherhead,2006) and in developing countries untreated wastewater is alsocommonly used to irrigate crops, thus increasing the risk ofmicrobial contamination (Ashbolt, 2004). Gagliardi, Millner, Lester,and Ingram (2003) showed an increased count of microbialindicators on cantaloupe rinds after fruit washing and cooling inhydrocooler indicating that inadequately decontaminated waterused in post harvesting produce processing can also be a sources ofmicrobial contamination.

Contaminated irrigation and processing waters were indicated aspossible sources of Salmonella contamination in several fresh produceoutbreaks (CDC, 2002, 2008; Greene et al., 2008; Sivapalasingam et al.,2003). In 2002 and 2005 two multistate outbreaks of S. Newport inUSA, caused by the same rare S. Newport strain, were associated witheating tomatoes (Greene et al., 2008). Tomatoes causing of theoutbreak were traced back to the eastern shore of Virginia where theS. Newport outbreak strain was isolated. Notably this outbreak strainwas isolated from the pond water used to irrigate tomato fields bothin 2002 and 2005 (Greene et al., 2008). The presence of the S.Newportoutbreak strain, two years apart, in the irrigation pond demonstratethat if not properly addressed, the source of contamination can persistand cause continuous outbreaks (Greene et al., 2008).

Salmonella serovar Newport was also the etiological agent in amultistate outbreak linked to mango consumption in USA(Sivapalasingam et al., 2003). The implicated mangoes were tracedback to a single Brazilian farm where mangoes were washed withcontaminated water (Sivapalasingam et al., 2003). Analysis of theirrigation and processing water at this farm indicated the presence ofSalmonella spp. in the water. Sivapalasingam et al. (2003) suggestedthat hot and cool water treatment which allowed the internalizationof Salmonella in the mangoes was the most likely source ofcontamination. The S. Newport outbreak strain was no actuallyisolated from the Brazilian water samples however, the farminvestigation took place many months after the outbreak hadoccurred (Sivapalasingam et al., 2003). In 2008, a large multistateoutbreak of Salmonella Saintpaul associated with multiple rawproduce items infected a total of 1442 people in the USA and Canada(CDC, 2008). Jalapeno and serrano peppers imported from Mexicowere identified as the major sources of this outbreak. The S. Saintpauloutbreak strain was isolated from samples of jalapeno pepper as wellas of irrigation water at a Mexican farm suggesting a possible route ofSalmonella contamination (CDC, 2008). Irrigation of fields withsewage contaminated waters and processing produce with Salmonellacontaminated waters were also indicated as possible sources ofcontamination in an outbreak of S. Poona infections in the USAassociated with eating imported cantaloupe (CDC, 2002).

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Several studies have investigated the potential source of producecontamination in the supply chain both at the pre-harvested and post-harvested stages. According to the epidemiological data, surveys ofSalmonella contamination in water used for fresh produce irrigationand in food processing identified the possible involvement of thesewaters in fresh vegetable and fruit contamination (Castillo et al.,2004; Duffy et al., 2005; Espinoza-Medina et al., 2006; López Cuevas,León Félix, Jiménez Edeza, & Chaidez Quiroz, 2009). Salmonella wasdetected in irrigation waters used for different type of fresh producesitems, such as tomatoes, peppers and cantaloupes (Castillo et al.,2004; Duffy et al., 2005; Espinoza-Medina et al., 2006; López Cuevaset al., 2009).

Espinoza-Medina et al. (2006) evaluated the incidence ofSalmonella contamination during cantaloupe production and proces-sing, in five 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 Salmonellacontamination. Similarly, Castillo et al. (2004) described an extensivesurvey of Salmonella contamination at cantaloupe production farms inSouth Texas (USA) and Colima State (Mexico). By repetitive sequencebased PCR analysis Castillo et al. (2004) identified the irrigation watersource as a possible source of cantaloupe contamination. Similar levelsof Salmonella contamination were found in the cantaloupe from USAand from Mexico (Castillo et al., 2004). Duffy et al. (2005) analyzedsamples from fresh produce (orange, parsley and cantaloupe) andenvironmental samples (water, soil, equipment) at a produceproduction farm in Texas. Salmonella was only isolated from theirrigation water (16/25 isolates), equipment (6/25 isolates) andwashed cantaloupe (3/25 isolates). However by PFGE the Salmonellastrains isolates from the irrigation water and equipment were shownto be different from the cantaloupe isolates (Duffy et al., 2005). FinallyLópez Cuevas et al. (2009) recovered Salmonella in 39% of irrigationwater samples in four different regions of the Culiacan valley (SinaloaMexico), an important area for the production of crops exported in theUSA. Notably, resistance to tetracyclines was observed in many of theSalmonella strains isolated which correlated with the use of theseantibiotics to treat and control plant pathogens infections (LópezCuevas et al., 2009; Lugo-Melchor et al., 2010).

4. Salmonella prevalence, diversity in surface, drinking water andgroundwater

Salmonella contaminated waters might contribute through directingestion of the water or via indirect contamination of fresh food tothe transmission of this microorganism. Salmonella prevalence insurface water and drinking water has not been uniformly investigatedin different countries in recent papers. Surveys of Salmonella in freshsurface water environment were mainly performed in industrializednations, in particular in Canada and North America. Reports ofSalmonella prevalence in drinking water were instead more frequent-ly from developing nations reflecting the higher concern relating tothe use of low quality drinking water in these countries. Overall, thescientific community hasmainly recently focused on the prevalence ofthis microorganism in impacted and non-impacted watersheds(Haley et al., 2009; Jokinen et al., 2011; Patchanee, Molla, White,Line, & Gebreyes, 2010), on the identification of the routes ofsalmonellae contamination (Gorski et al., 2011; Jokinen et al., 2010,2011; Obi et al., 2004; Patchanee et al., 2010), and on the influence ofenvironmental factors on the spread of Salmonella in water (Haleyet al., 2009; Jokinen et al., 2010; Meinersmann et al., 2008; Wilkeset al., 2009). Particular attention was also addressed to the evaluationof available and new approaches to monitor sources of Salmonellacontamination, and to predict its presence in different aquaticenvironments (Savichtcheva, Okayama, & Okabe, 2007; Schrieweret al., 2010; Walters, Gannon, & Field, 2007; Wilkes et al., 2009).Additionally, the recently available data on the prevalence of

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

antibiotic resistant Salmonella strains in surface and drinking water(Bhatta et al., 2007; Dolejská et al., 2009; Meinersmann et al., 2008;Oluyege et al., 2009; Patchanee et al., 2010) consistently indicate thatthese aquatic environments are a reservoir of MDR strains, whichmight contribute to the dissemination of these MDR strains throughsusceptible populations.

4.1. Surface waters

A survey of recent studies showed an increasing interest over thelast two years on the role of non-host habitats, such as surface waterenvironments as natural reservoir and in the transmission ofSalmonella and other enteric pathogens (Ahmed, Sawant, Huygens,Goonetilleke, & Gardner, 2009; Byappanahalli et al., 2009; Dolejskáet al., 2009; Haley et al., 2009; Jokinen et al., 2010, 2011; Patchaneeet al., 2010; Schriewer et al., 2010; Wilkes et al., 2009). A summary ofthe available data on Salmonella prevalence in surface fresh waterssources is shown in Table 1.

The data provided in Table 1 confirms the ubiquitous nature of thisenteric pathogen. Salmonellae were detected in different countriesand in very diverse water sources, ranging from pristine (e.g.Patchanee et al., 2010; Till, McBride, Ball, Taylor, & Pyle, 2008) andlow 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 forrecreational purposes (Till et al., 2008); as source of drinking water(Till et al., 2008); and for irrigation (e.g. Gannon et al., 2004). Thisdemonstrated wide distribution of salmonellae underlines that thereis the potential for inadvertently using water contaminated withSalmonella, with associated potential health risks. As shown in Table 1,the Salmonella detection frequencies were extremely variable in theinvestigated surface waters with detection rates ranging from 3 to100%. In general, the highest frequencies were reported in watershedsthat had been highly impacted by human activities (Bonadonna et al.,2006; Jyoti et al., 2010) or in geographical areas with a history of highsalmonellosis cases (Haley et al., 2009). However, Patchanee et al.(2010) showed that elevated frequencies of Salmonella were alsofound in a forestry watershed not influenced by human activities.Notably, these authors observed similar prevalence of salmonellae inwatersheds with diverse potential contamination sources, namelyresidential 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 ofthe knowledge of Salmonella concentrations in water to evaluate therisk of water related infection, only a few performed a quantitativeassessment 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 werecommonly 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 theoccurrence of Salmonella in ambient water may be governed, in part,by environmental parameters such as temperature, water chemistry,and solar radiation that influence survival and transport of themicroorganism. Other possible reasons include changes in pathogenloading due to enhanced shedding from human and animal host, orfrom enhanced flow of water from contaminated sources. Positivecorrelations between rainfall events and Salmonella prevalence and/ordiversity have been reported by many authors (Baudart, Lemarchand,Brisabois, & Lebaron, 2000; Haley et al., 2009; Jokinen et al., 2010; Poloet al., 1999; Schets, van Wijnen, Schijven, Schoon, & de RodaHusman,2008; Wilkes et al., 2009). These results, which are supported bysimilar observations with respect to Salmonella contamination in

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Table 1Salmonella occurrence in surface waters.

Level and frequency positivesamples % (total samples)

Surface water Dominant impact in the analyzed water Country Survey extent References

8.5% (342) River water Mainly influenced by rainfall runoff anddrainage from agricultural land

Canada 9 sampling sites,2 year

Jokinen et al. (2011)

13% (186) River water Mixed Canada 4 sampling sites,2 years

Jokinen et al. (2010)

104–106 CFU/100 mLa River water Mixed comprising untreated sewage ofresidential setup

India 8 sampling sites,1 day

Jyoti et al. (2010)87% (8)54% (86) Four differently impacted

watersheds systemsSwine production Residential/industrialForestry Crop agriculture

USA 4 sampling sites,2 years

Patchanee et al. (2010)

7% (143) River and estuaries Not described USA 10 sampling sites,14 month

Schriewer et al. (2010)

3% (32) Urban pond and tidal creeks Mixed: WWTPs effluents, surface runoff,agricultural

Australia 8 sampling sites,2 months

Ahmed et al. (2009)

0.002–0.017 MPN/mL Lake and river water Not described USA numeroussampling sites,2 years

Byappanahalli et al.(2009)42% (19)

16% (87) Pond Urban CzechRepublic

2 sampling sites,1 year

Dolejská et al. (2009)

2.5–36.3 MPN/Lb River watershed Mixed: mainly forested and agricultural in aarea with high incidence of salmonellosi

USA 6 sampling sites,12 months

Haley et al. (2009)79% (72)4–15% (1600)c River and streams mixed Canada 24 sampling sites,

3 yearsWilkes et al. (2009)

75% (83) Small river Mainly rural area USA 82 sampling sites,1 day

Meinersmann et al.(2008)

3.8% (79) Urban canals/river andrecreational lakesd

Not described Netherlands 8 sampling sites,1 year

Schets et al. (2008)

10.6% (216) Stream water Puddles Mixed comprising WWTP discharge Mexico Randomsampling, 2 years

Simental and Martinez-Urtaza (2008)17.6% (17)

10% (725)e Rivers and lakes Fresh waterrecreational and water supply sites

Mixed: birds, dairy farming, municipal,sheep/pastoral, forestry undeveloped

New Zeland 25 sampling sites,15 month

Till et al. (2008)

53% (30) River and pond around Sapporocity

Mixed: WWTPs effluents, urban sewage, cowand pig farms

Japan 5 sampling sites,3 months

Savichtcheva et al.(2007)

10–104 MPN/100 mL Riverf Mixed: Urban/industrial comprising directsewage discharge

Italy 8 sampling sites,2 years

Bonadonna et al. (2006)100% (N300)75% (375)g River, borehole Animal and human activities, human and

animal fecesSouth Africa 8 sampling sites Obi et al. (2004)

5.4% (802) River and irrigation water Canada 16–21 samplingsites, 2 years

Gannon et al. (2004)

102–105 MPN/100 mL River Mixed: Urban/industrial, WWTP dischargeagricultural

Italy 1 sampling site,1 year

Bonadonna et al. (2003)100% (10)57% (14) River water Runoff from agricultural land and pastures,

human and animal fecesAfrica Weekly sampling,

5 monthsObi, Potgieter, Bessong,and Matsaung (2003)

0.06–42.4 CFU/L River Mixed France Lemarchand andLebaron (2003)100% (8)

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

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coastal area and marine environment (Baudart, Grabulos, Barrusseau,& Lebaron, 2000; Simental & Martinez-Urtaza, 2008), indicated thatincreased pathogen load could be associated with rainfall events asone major environmental driver of Salmonella contamination insurface water environment. In agreement with this a positivecorrelation was reported in the literature between rainfall eventsand the incidence of Salmonellawater related infections (e.g. Haddock& Malilay, 1986; Suresh & Smith, 2004). In contrast, the variableseasonal occurrence of Salmonella in aquatic environments reportedin the recent literature was not consistent with the summer peakhuman and animal salmonellosis infection observed worldwide. Tillet al. (2008) reported an increase of the concentration of Salmonelladuring late winter in New Zealand at a site where birds and sheepwere the major potential contamination source. In contrast, theseasonal peak of Salmonella incidence in a Canadian watershed wasobserved in the fall (Wilkes et al., 2009) potentially reflecting

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

enhanced livestock based fecal input during this period. Accordingto Wilkes et al. (2009) salmonellae's incidence was found to bepositively correlated with tributary discharge values as well as withaccumulative rainfall. Only Haley et al. (2009) in a study of awatershed in Georgia USA found that Salmonella incidence peaked inthe summer period. Over the complete study period, the presence ofthis pathogen was positively correlated with water temperatures andrainfall events (1 or 2 days before sampling). According to theseresults, the authors concluded that multiple environmental factors,including enhanced pathogen loading during storm events, increasedsurvival in the water environment at warm temperatures andincreased host shedding in the warmer season might explain theSalmonella peak during the summer months.

Spatial differences in Salmonella prevalence in surface waters havealso been reported in the recent literature (Bonadonna et al., 2006;Lemarchand & Lebaron, 2003; Meinersmann et al., 2008; Savichtcheva

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Table 2Salmonella diversity in surface waters.

Diversity Commonserovars

Others serovars Country Reference

Serovarnumber/totalisolates

(percentageof totalisolates)

11/29 Rubislaw(72.4%)a

Givea, Heidelberga,Typhimurium,Senftenberg, Mbandaka,Other

Canada Jokinen et al.(2011)

I:11:r:–a

Derby12/104 Anatum

(18.3%)Mbandaka, Bullbay, Give,Miami, Braenderup

USA Patchanee etal. (2010)

Gaminara(18.3%)Inverness(18.3%)Muenchen(8.7%)b

Newport(8.7%)b

Bredeney(6.7%)

13/197 S. entericasubsp arizona(40.6%)

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

USA Haley et al.(2009)

Muenchen(14.2%)c

Rubislaw(13.2%)c

Mikawasima(6.1%)Montevideoe

6/17 Enteritidisd,e

Infantis, Derbyf, Indiana,g

Czech Dolejská et al.

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et al., 2007; Schriewer et al., 2010). Schriewer et al. (2010) reported ahigher frequency of salmonellae in surface waters that have marineinfluences while Bonadonna et al. (2006) and Lemarchand andLebaron (2003), observed that the highest concentration of thispathogen was associated to sampling points in densely populatedareas and/or downstream of sewage effluents discharge sites.

MDR strains have been detected in surface water in developedcountries (Dolejská et al., 2009; Meinersmann et al., 2008; Patchaneeet al., 2010). In particular, Patchanee et al. (2010) showed that swineproduction was a major source of antibiotic resistant Salmonella inwater environments as all the Salmonella isolates from a swineproduction watershed had multiple resistances to antibiotics. Incontrast, antibiotic resistant strains were not detected from water-sheds impacted by forestry, crop agriculture, or a residential/industrialarea (Patchanee et al., 2010). Antibiotic resistant Salmonella have alsobeendetected in surfacewater fromapond in the north-eastern part ofthe Czech Republic as well as in birds, black-headed gulls nesting inthis pond (Dolejská et al., 2009). A total of 16% of water and 24% of gullsamples yielded Salmonella. Antibiotic resistance was found in 12% ofsalmonellae isolated from the water and 28% of gull salmonellae.Resistance to the quinolone nalidixic acid, streptomycin, and tetracy-cline was often detected in these Salmonella isolates. Dolejská et al.(2009) concluded from these results that black-headed gulls can beimportant reservoirs of antibiotic resistant salmonellae. Meinersmannand co-workers investigated the prevalence of Salmonella and theirantimicrobial resistance profile in a synoptic study of the Oconee RiverBasin, a small river in north-eastern Georgia, USA (Meinersmann et al.,2008). Water samples were obtained from 83 sites with Salmonellaisolated from 62 of the samples, however, only seven of the isolateswere resistant to any antimicrobials.

(50%) Hadar , Typhimurium Republic (2009)19/73 Muenchen

(20%)Infantis, Kiambu,Livingstone, Iv40:z4,z32:–

USA Meinersmannet al. (2008)

Rubislaw Typhimurium, ParatyphiB, Newport,Oranieneburg, Ouakam,Mbandaka, Montevideo,Thompson, Gaminara,Heidelberg, Braenderup

HartfordGive

3 Newport Netherlands Schets et al.(2008)Virchow

Typhimurium11/23 Typhimurium

(39%)Othmarschem, Soerenga,Augustenborg, Breda,Coeln, DJugu

Mexico Simental andMartinez-Urtaza(2008)

UrbanaSuberuVejle

45/92a Typhimurium(13.7%)

Saint Paul,Bovismorbificants,Montevideo, Enteriditis,Give (only serotypesdetected also by otherauthors)

Italy Bonadonna etal. (2006)

Subsp. II(8.4%)Infantis(5.3%)Bredeney(4.2%)Stanley(4.2%)Derby (4.2%)

19/36 Derby(16.6%)

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

Vietnam Phan et al.(2003)

03,10:r:–AnatumBardoJaviana

35/413h Typhimurium(31.1%)

France Baudart,Lemarchand,et al. (2000)Virchow

PanamaNewportHadarGrumpensis

(continued on next page)

4.2. Diversity of Salmonella strains isolated from surface waters

All Salmonella serovars are considered as potential pathogens. Onlyabout 50 of these serovars, however, have been predominantlyisolated from humans or animals (Popoff, 2001). Informationregarding the distribution and characteristics of Salmonella serovarspresent in the environment are essential in assessing the role of non-host aquatic habitats in the diffusion of Salmonella subtypes of highhuman health concern. Furthermore, the identification of source-specific serovars might help future tracking of sources of Salmonellacontamination events.

The first comprehensive studies describing the diversity ofSalmonella serovars in the aquatic environment were presented byPolo et al. (1999) and Baudart, Lemarchand, et al. (2000). Bothresearch groups analyzed a large number of isolates from differentnatural aquatic systems (river, wastewater and marine coastal areas)showing a great diversity of Salmonella serovars. Since then, severalworks have provided further data on the different serovars presentand on the possible sources of Salmonella contamination in surfacewater. A summary of recent available data is reported in Table 2.

With the exception of few studies that analyzed a limited numberof isolates (Dolejská et al., 2009; Schets et al., 2008) or monitoredhighly contaminated watersheds (Bonadonna et al., 2006), the totalnumber of serovars detected in the investigated aquatic environmentsranged from 10 to 20 independently of the number of isolates orsamples analyzed in the different studies. In comparison to the resultsof the initial studies by Baudart, Lemarchand, et al. (2000) and Poloet al. (1999), these latter consistent figures found that there was a lowdiversity of Salmonella serovars in the non-host water environment(Table 2). This difference might be explained by the very long period(5 years) of Salmonellamonitoring described by Polo et al. (1999) andthe reported increase in the numbers of serovars during flood events(10 of the 35 serovars were only isolated during the flood by Baudart,Lemarchand, et al. (2000)).

Please cite this article as: Levantesi, C., et al., Salmonella in surface and drinking water: Occurrence andwater-mediated transmission, Food Research International (2011), doi:10.1016/j.foodres.2011.06.037

Table 2 (continued)

Diversity Commonserovars

Others serovars Country Reference

Serovarnumber/totalisolates

(percentageof totalisolates)

44/316h Enteriditis Spain Polo et al.(1999)Virchow

HadarInfantisTyphimuriumGoldcoastOhio

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

10 C. Levantesi et al. / Food Research International xxx (2011) xxx–xxx

Contamination sources and environmental factors were alsoshown to influence serovar abundance. Peaks of Salmonelladiversity were observed to be associated to a specific locations(e.g. urban/industrial impacted watershed, Patchanee et al., 2010),and seasons (e.g. greater detections in the summer period, Haley etal., 2009).

Typhoid Salmonella serovars Typhi and Paratyphi A were onlydetected in surface waters in developing countries where the diseaseis endemic (Bhatta et al., 2007; Oluyege et al., 2009). In contrary,Salmonella Paratyphi B, although very rare, has been detected insurface waters in France (Baudart, Lemarchand, et al., 2000) and Italy(Bonadonna et al., 2006). As shown in Table 2, S. enterica serovars ofhigh public health concern (e.g. Montevideo Newport, Bredney,Enteriditis, Infantis, Muenchen, Typhimurium) were detected in allthe reported studies.

One relevant fact that can be noted is that the clinical serovars thatwere common or dominant in the studied geographic areas, wereusually also detected in the surface water samples (Bonadonna et al.,2006; Dolejská et al., 2009; Haley et al., 2009; Patchanee et al., 2010).This indicates that the Salmonella population in water environments isinfluenced by the incidence of human infections in the local area.Clinical serovars were not always dominant isolates in the studies ofaquatic environment, however (Haley et al., 2009; Jokinen et al., 2011;Patchanee et al., 2010) suggesting that human sewage was not thesole or main source of contamination in these habitats. In agreementwith this, the spectra of Salmonella serovars observed by variousauthors in surface water showed a mixed human/animal origin(Dolejská et al., 2009; Haley et al., 2009; Jokinen et al., 2011;Patchanee et al., 2010).

The common assumption that livestock production is one of themain sources of surface water contamination by enteric bacteria suchas Salmonella has not been fully confirmed 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), Haleyet al. (2009) suggested that local reptile population may be asignificant source of the total Salmonella in this surface water. Jokinenet al. (2011) could only detect the serovar Rubislaw in the Oldmanriver watershed (Alberta, Canada) and in the feces of wild birds, whileit was neither detected in the analyzed sewage (human contamina-tion source) nor in feces of domestic animals. High frequency ofSalmonella (57.1% of samples) from a forestry watershed not impactedby livestock was described by Patchanee et al. (2010). Patchanee et al.

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

(2010) also showed that Salmonella serovar Gaminara, was dominantin this same water system. According to Gaertner, Hahn, Rose, andForstner (2008) S. Gaminara is mostly associated to wild animals. Aspreviously noted, black-headed gulls were identified as an importantreservoir of antibiotic resistant Salmonella contamination in a pond inCzech Republic (Dolejská et al., 2009). All of these results indicate thatwild animals can be one of the major sources of Salmonellacontamination in the environment. In agreement with this, wildbirds and other wild life have been identified as source of Salmonellawater-borne outbreaks in different countries (Angulo et al., 1997;Schuster et al., 2005; Taylor et al., 2000).

Understanding the relative contribution of different possiblecontamination routes on Salmonella introduction in surface watersis a necessary precursor for the selection of specific control strategies.An increase of knowledge on how the Salmonella genotypes andphenotypes are related to different potential contamination sources isessential. In this context, valuable information has been generated bythe comprehensive work of Jokinen et al. (2011), Patchanee et al.(2010), and Gorski et al. (2011) that can be used for the suggestion ofappropriate control strategies in impacted catchments and watersheds.

Jokinen et al. (2011) compared the serovars detected in theOldman river watershed with those present in sewage (humansource) and in animal feces as potential source of Salmonellacontamination in the investigated area. Only four serovars isolatedfrom water (Rubislaw, Heidelberg, Give and I:11:r:–) were alsodetected in feces or sewage samples. However, most of these serovarsspanned a broad host range and thus it was not possible to identify thesingle contamination sources. Salmonella Rubislaw, the most commonserovar in thewater samples, was only detected inwild bird feces, but,since a limited number of fecal samples of wild birds was analyzed, itwas not possible to understand the real contribution of these birds onthe water contamination with Salmonella. Nevertheless, serovarscomparison in feces and water samples indicated that other animalsfound in the watershed were not contributing to the Salmonellacontamination in the Oldmann river watershed (Jokinen et al., 2010).

Patchanee et al. used pulsed-field gel electrophoresis PFGEgenotyping coupled with serotyping techniques for trackingSalmonella contamination in four watersheds in North Carolina(USA). Salmonella genotypic and phenotypic diversity was analyzedand compared in differently impacted watersheds: swine-produc-tion, residential/industrial, forestry and crop agriculture (Patchaneeet al., 2010). The resulting Salmonella genotypic and phenotypicdiversity in differently impacted watersheds: swine-production,residential/industrial, forestry and crop agriculture was comparedshowing that isolates from the swine-production watershed weredistinctly different from other isolates both in their genotypes andserovars. This suggested that there was a specific source ofcontamination for this watershed. In particular the serovarsAnatum and Bredney were only found in this watershed. Theauthors also showed that Salmonella strains isolated from residen-tial/industrial and forestry were genotypically related and sug-gested that there was a potential cross contamination betweenthese watersheds.

Gorski et al. (2011) investigated the incidence and diversity ofsalmonellae in a major produce region of California. As part of thestudy they also analyzed serovars and genotypes (PFGE) of Salmonellastrains isolated from water, cattle and wildlife feces, soil/sedimentand preharvested lettuce/spinach. The serovars detected in the watersamples, S. Infantis, S.Give, S. Typhimurium and themonophasic types6,8:d:– and 6,8:–:e,n,z15, were also isolated from wildlife feces.According to PFGE patterns, however, all the strains isolated fromwildlife were distinguishable from those isolated from water.Nevertheless, some near matches indicated that crow and coyoteswere potential sources for water contamination. These authorsconclude that source tracking may be possible in these environments;

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however, they stressed that the use of genotyping methods withhigher resolution than PGFE would be necessary to determine therelatedness of very clonal serovars.

4.3. Drinking water and groundwater

A summary of recent available publications on Salmonellaoccurrence in groundwater and drinking water, from a combinationof water either treated or untreated prior to use as public drinkingwater untreated is provided in Table 3. As shown in Table 3, Salmonellawas detected with varying frequencies in the analyzed water. Severalstudies describe Salmonella prevalence in drinking water in Africancountries, mainly South Africa and Nigeria (Akinyemi, Oyefolu, Salu,Adewale, & Fasure, 2006; Momba, Malakate, & Theron, 2006; Oguntokeet al., 2009; Oluyege et al., 2009; Potgieter et al., 2005). Momba et al.(2006) reportedpoormicrobiological quality of drinkingwater in a ruralarea of the Eastern Cape Province (South Africa) where Salmonellaarizonae was detected in 100% of municipal drinking water samples.Similarly in the Limpopo Province (South Africa), samples watercollected from standpipes of boreholes and from surface water used asdrinking water source were always found to be positive for Salmonella(Potgieter et al., 2005). As shown in Table 3 lower frequencies ofSalmonella in drinking water samples were reported from Nigeriacompared to South Africa (Akinyemi et al., 2006; Oguntoke et al., 2009;Oluyege et al., 2009) (Table 3). Nevertheless, Nigeria surface andgroundwater used as drinkingwater sources in rural communitieswerealso shown to be reservoirs of Salmonella (Akinyemi et al., 2006;Oguntoke et al., 2009; Oluyege et al., 2009). In addition, the surveys ofSalmonella prevalence in drinking water in Nigeria undertaken byOluyege et al. (2009) showed that all the Salmonella strains isolatedwere resistant to several antibiotics. Furthermore, MDR resistance tomore than 4 antibiotics was observed inmost of these isolates (Oluyegeet al., 2009). It should be noted, however, that in contrast to what wasobserved in surface waters studies from other countries, most of theseAfrican publications relied on very few data points to link the water asreservoirs of salmonellae. A notable comparison is the comprehensivestudy of Bhatta et al. (2007),whichprovidedundeniable evidence of thepoor microbiological quality of the public drinking water supplied inurban Nepal. Bhatta et al. (2007) clearly showed the importance of the

Table 3Salmonella occurrence in drinking water.

Level and frequency %positive sample (totalsamples)

Water source Country Reference

6·101–3.8·102 gc/L Roof harvested rainwatera Australia Ahmed et al.(2010)10.7% (214)

104–106 CFU/100 mLb Drinking water supply India Jyoti et al.(2010)50% (4)

23.6% Well and borehole waterc Nigeria Oguntoke etal. (2009)

13.3%d Surface waterc Nigeria Oluyege et al.(2009)

14% (300) Tap water of urban watersupply system

Nepal Bhatta et al.(2007)

100%(8)e Borehole standpipes waterand surface waterc

SouthAfrica

Momba et al.(2006)

16% (18)f Well and tap waterg Nigeria Akinyemi et al.(2006)

100% Borehole standpipes waterand surface waterc

SouthAfrica

Potgieter et al.(2005)

gc: gene copies.a 35% for indoor use including drinking, showering and kitchen use.b Presumptive Salmonella identification.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.

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

human host-specific strains Typhi and Paratyphi A, indicating theimpact of human source contamination on the overall Salmonella inputin the analyzed water source. Furthermore, they highlighted thecommon occurrence of MDR Salmonella strains which increased therisk connected to the use of these water supply systems. The literaturedemonstrate that a lack of hygienic conditions, non-appropriate watersupply structures, and improper disinfection were consistently identi-fied as the main cause of water contamination in developing countries(Akinyemi et al., 2006; Bhatta et al., 2007; Momba et al., 2006; Oluyegeet al., 2009).

Groundwater is becoming increasingly relied upon as a majorsource of water and the security of water quality for groundwater indeveloping nations is a major issue. Contamination of groundwater bymicrobial pathogens has been documented also in developedcountries due to failures in well head protection, inadequate off-setand diffuse contamination sources (Bockelmann et al., 2009;Borchardt, Haas, & Hunt, 2004; Goss & Richards, 2008). Groundwatercan be contaminated by a wide range of pathogens, but like for mostwater sources, enteric pathogens remain the greatest risk. Despite thecommon assumptions that all enteric pathogens are a contaminationrisk for groundwater (e.g. John & Rose, 2005) themajority of studies ofpathogens in groundwater has focused on the presence of indicatormicroorganisms (e.g. Emmanuel, Pierre, & Perrodin, 2009; Wall, Pang,Sinton, & Close, 2008), risks posed by enteric viruses (e.g. Borchardtet al., 2004; Locas, Barthe, Margolin, & Payment, 2008), or protozoa(e.g. Boyer, Kuczynska, & Fayer, 2009). In contrast, the information onthe presence of Salmonella spp. in groundwater is limited. In one of thefew studies reported on Salmonella in groundwater, Li et al. (2009)determined that the consumption of groundwater was an indepen-dent risk factor for a number of confirmed cases of Salmonellacholeraesuis in Taiwan. In another study of groundwater quality inTurkey, Ozler and Aydin (2008) detected Salmonella in 15% of thegroundwater samples tested.

There is also information about Salmonella detection and behaviorin groundwater from a study where recycled water has beenintentionally recharged to aquifers during Managed Aquifer Recharge(MAR). Levantesi et al. (2010) were able to occasionally detectSalmonella in two aquifers used as MAR sites receiving recycled water,however, they detected Salmonella much less frequently than otherpathogens such as Cryptosporidium and Giardia.

In Australia, where the issue of water scarcity has resulted in thepromotion of the use of roof harvested rainwater for drinking or otherpurposes, several studies have been undertaken investigating themicrobiological quality of the collected rain waters. Ahmed, Huygens,Goonetilleke and Gardner (2008) and Ahmed, Vieritz, Goonetillek andGardner (2010) detected Salmonella in tanks collecting roof harvestedrain water for indoor and outdoor use and indicated wild birds oranimal feces as likely source of contaminations. A risk assessmentstudy using these results indicated that there was a risk of infectionfor Salmonella ingestion that exceeded the threshold value of 1 extrainfection for 10,000 persons a year suggesting that roof harvestedrainwater should be disinfected if used for potable water purposes(Ahmed et al., 2010). Another study also linked roof harvested rainwater with Salmonella water-borne infection in Australia (Ashbolt &Kirk, 2006; Franklin et al., 2009) further highlighting the risks fromSalmonella 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 aquaticenvironment has been done in the last decades of the 20th century.Overall, these older studies investigated the physicochemical andbiological factors influencing Salmonella survival in various water

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environments and compared the survival capacity of different entericbacteria (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 thatinvestigated the relative survival of E. coli and Salmonella Typhimuriumin estuary waters focusing on the effect of biological factors, dissolvedorganic and inorganic substances, and sunlight on the inactivation ofthese bacteria. The results showed that sunlightwas themost importantfactor for inactivation, followed by biotic factors. The biotic factors weredetermined to comprise of a combination of predation by protozoa andbacteria, bacteriophage lysis, and competition with autochthonousmicrobes. They also found that dissolved organic substances present inthe estuarine water, in the absence of the native biota, promotedsurvival and growth of these enteric bacteria. In contrast to what hasbeen previously described in other studies (Mezrioui, Baleux, &Trousselier, 1995; Rhodes & Karton, 1988; Winfield & Groisman,2003), E. coli cells showed a better survival capacity when comparedto S. Typhimurium under all tested conditions. In another microcosmstudy by the same research group, an enhanced survival capacity ofSalmonella in lake sediment with respect to the overlaying water wasobserved (Chandran et al., 2011). According to these results, the lakesediment 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 andCampylobacter jejuni in river and seawater was also investigated bySinton, Hall, and Braithwaite (2007). They showed that inactivationrates in sunlight were clearly higher than in the dark and that theextent of inactivation was directly related to the amount of insolation.Furthermore, in agreement to Chandran and Hatha (2005) theyshowed that S. enterica was inactivated up to 1.6 times faster than E.coli.

Pathogens have been documented to decay when introduced intoaquifers and this information can be used for Managed AquiferRecharge sites (Gordon & Toze, 2003; Toze, 2004). As with thedetection of pathogens in groundwater, most information availablefocuses on the survival of enteric viruses (Nasser, Glozman, & Nitzan,2002; Toze, Hanna, Smith, Edmonds, & McCrow, 2004) and there islimited information specifically on the survival of Salmonella. Despitethis, inactivation of Salmonella in groundwater has been noted in onestudy of pathogen decay at a Managed Aquifer Recharge site. Toze,Bekele, Page, Sidhu, and Shackleton (2010) observed that Salmonellahad a 1 log reduction time in groundwater of 1 day. This is similar todecay times observed in groundwater for other bacteria such ascoliforms (Gordon & Toze, 2003) but less than observed for entericviruses or protozoa (Toze et al., 2010).

Recent studies indicate that secondary habitat may provide therequired conditions to promote survival and replication of entericmicroorganisms including Salmonella. In particular, Ishii et al. (2006)and Byappanahalli et al. (2009) showed that the filamentous greenalga Chladophora in Michigan lake, could arbor salmonellae at muchhigher concentrations compared to the numbers in the surroundingwater. According to these observations and to previous resultsshowing that this alga can support the growth of enteric bacteria byproviding 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 thewater column.

5.2. Conventional and alternative microbial indicators for Salmonellamonitoring in aquatic environment

The limits and advantages of conventional and alternative in-dicators of fecal contamination for pathogen monitoring in aquaticenvironment have been recently extensively reviewed (Field &Samadpour, 2007; Savichtcheva & Okabe, 2006). The efficiency offecal indicator bacteria (FIB) to predict the presence/absence of

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

Salmonella in aquatic environment remains a matter of debate inrecent papers (Ahmed et al., 2009; Savichtcheva et al., 2007;Schriewer et al., 2010; Wilkes et al., 2009). Despite this, in acomprehensive study describing the occurrence of enteric pathogensin a Canadian watershed and their relationships with environmentalparameters and FIB, Wilkes et al. (2009) showed that a goodprediction of Salmonella presence can be obtained by FIB determina-tion. In particular, they indicated that E. coli and fecal coliforms werethe most appropriate indicators of Salmonella presence compared toClostridium perfringens, enterococci and total coliforms. The identifiedE. coli threshold level that gave the greater probability of pathogendetection was NE. coli 89 CFU/100 mL. This E. coli threshold wasdetermined to correlate with the identification of 89% of Salmonellapositive samples. Schriewer et al. (2010) also observed that at aspecific threshold level fecal coliforms as well as enterococci and totalcoliforms were good predictors of Salmonella presence in Californianrivers with sea intrusion. They also found, however, that thesemicrobial indicators did not efficiently predict Salmonella in rivers thatwere not influenced by sea intrusion. In contrast with these results, nocorrelation were observed between FIB and Salmonella presence/ab-sence 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 arefecal anaerobes that are present in feces in much higher densities thanconventional FIB and have different host specificities (Field &Samadpour, 2007). Feces from different sources such as human,horse, pigs, dogs, and ruminant can be identified by Bacteroidales hostspecific PCR primers which can allow source tracking of fecalcontamination. Favorable results were obtained using thismethod in comparison to other source tracking approaches (Griffith,Weisburg, & McGee, 2003). Furthermore, due to their host specificdistribution, these markers might predict the presence of certainpathogens associated to specific source of pollution.

The relationship between Bacteroides 16S rRNA genetic markersand Salmonella in aquatic environment has been addressed in a fewpapers (Savichtcheva et al., 2007; Schriewer et al., 2010;Walters et al.,2007). According to Savichtcheva et al. (2007), human and totalBacteroides 16S rRNA genetic markers in wastewater and riversamples were positively correlated with the presence of Salmonellaand showed a good predictive value for the presence of this pathogen.They found that the probability of its occurrence became significantlyhigh (N70–80%)when the concentration of human Bacteroides geneticmarkers exceeded 106 copies/100 mL. No correlations were foundwith cow and pig Bacteroides 16S rRNA genetic markers in the samestudy. Differently from the results from Savichtcheva et al. (2007),two recent studies analyzing river and estuarine water environmentsshowed no predictive value for various Bacteroidales host specificmarkers in association with Salmonella detection (Schriewer et al.,2010; Walters et al., 2007). Nevertheless, Walters and colleaguesshowed that ruminant specific Bacteroidales markers were morefrequently detected in Salmonella positive samples (36%) compared tohuman specific markers (2.6%) (Walters et al., 2007). They concludedthat agricultural runoff were a major contribution to the Salmonellacontamination in the analyzed watershed while contamination fromhuman sources was only a minor contribution.

6. Conclusions

This review on the occurrence and risk of Salmonella in water hasdemonstrated that Salmonella can be present in a variety of aquaticenvironments and that contamination can come from a range ofsources. Salmonella has been detected in sources as diverse as rivers,lakes, pond, groundwater and drinking water, while sources of thebacterium 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 surfacewaters in industrialized countries confirmed the ubiquitous natureof this enteric pathogen. Moreover, the positive correlationsbetween Salmonella frequencies and rainfall events observed inmany of the studies indicated that surface runoff plays a main roleas driver of Salmonella load in aquatic environments. Analysis ofisolated serovars consistently showed a mixed human and animalorigin of Salmonella in surface water environments. This empha-sizing the role of wild life animals in water contamination alongwith the more accepted livestock and human sources. Overall, agreat complexity was observed in the structure of Salmonellapopulations in surface water environments. Studies revealed largeserovars diversity, both in water and in likely sources of contam-ination as well as spatial and temporal variation in the detection ofSalmonella types and frequencies.

In spite of the recognized potential of microbial source tracking,these methods have not been extensively used to investigate thesources of Salmonella contamination in the surface water environ-ments. Nevertheless, the results obtained to-date suggest thatmicrobial source tracking by genotyping methods in these environ-ments may be possible and may be extremely useful to identifyrelated strains in complex environmental Salmonella populations andto highlight specific transmission routes.

Salmonella serovars of human health concern were shown to bewidespread in natural freshwaters althoughmore rare environmentalserovars were also frequently detected. At present little is knownabout the pathogenicity of these rarer serovars isolated from theenvironment and further research is required to understand the roleof these serovars in water-borne disease dissemination. Regardless,human infections have been reported for most of the serovarsdetected in surface water including those usually associated withwild animals. A number of studies in developed countries detectedclinically relevant Salmonella serovars in water utilized for indooruses, irrigation and recreational uses, and of further concern, alsodetected MDR Salmonella strains in natural freshwaters. Overall, theseresults proposed that there was the likelihood of surface water-mediated Salmonella infections. This conclusion, however, is notsupported by epidemiological water-borne outbreaks data showingrare involvement of surface waters, both as drinking water sourcesand for recreational use, in Salmonella outbreaks. Nevertheless,exposure to recreational water was indicated as the most importantrisk factor for childhood Salmonella infections indicating that differenttransmission routes may be implicated in the transmission of sporadicand epidemic diseases.

Salmonella was not one of the leading causes of reported water-borne outbreaks in developed countries, being usually reported lessfrequently than other pathogens as agent of water mediatedepidemics (e.g. Cryptosporidium, Giardia, E. coli 0157:H7; norovirus,Shigella, and Campylobacter). Detected Salmonella outbreaks weremostly linked to contaminated drinking waters. Different types ofdrinking water (municipal water system, well, tank water) wereindicated as sources of outbreaks, however, all the outbreaks wereconsistently associated with the use of untreated or inadequatelytreated water. Studies have shown that Salmonella is efficientlyremoved by conventional disinfection procedures utilized in watertreatment processes and thus is of little risk in adequately treatedwater sources. Despite this, the true incidence of Salmonella water-borne diseases might be greater than is reflected in the reportedoutbreaks statistics as not all water-borne disease outbreaks arerecognized or reported, especially in countries with a low level ofwater-borne outbreaks surveillance. In addition, Salmonella contam-inated waters used to irrigate and wash produce crops have beenimplicated in a large number of food-borne outbreaks demonstratingthat additional indirect routes of transmissions should be consideredto correctly evaluate the role of water in Salmonella diseasesdissemination.

Please cite this article as: Levantesi, C., et al., Salmonella in surface andwater-mediated transmission, Food Research International (2011), doi:1

The data on water-borne outbreaks in developing countries arenot complete as national outbreaks surveillance systems are usuallylimited and in spite of the likely large number of studies performedin the field, the data produced have rarely been published. The dataavailable in the scientific literature related to water-borne trans-mission of Salmonella in developing countries are mainly casecontrol studies that have analyzed the risk for endemic typhoidSalmonella. The scientific data, overall, confirms that water is acommon source for the transmission of this disease, but alsohighlight that other risk factors are associated with typhoid feverindicating multiple routes of transmission. Reports of massivewater-borne Salmonella outbreaks as well as epidemiologicalstudies on endemic typhoid and paratyphoid fevers underlinedthe relevance of MDR Salmonella strains in these countries. The riskof MDR strains dissemination is further exacerbated in lessindustrialized countries through the customs of inappropriate useand self-prescribing antibiotics.

The efficiency of conventional and alternative microbial indicatorsof fecal contamination tomonitor Salmonella in water environments isstill a matter requiring further study due to the need for rapid, specificand reliable methods that can be used for the control of environmen-tal water quality. Most of the studies that looked for a link betweenindicators and Salmonella found inconsistent results on the relation-ship between the occurrence of FIB and Salmonella. Additionally, nosignificant improvements were achieved by applying alternativeindicators to the Salmonella presence in surface waters. Bacteroidaleswere found to perform equally or slightly better than FIB in a directcomparison of their capacity to predict Salmonella presence. Howeverthe relationship between Bacteroidales and Salmonella were found tonot be constant in surface water as inconsistent results were obtainedin different studies.

This review has shown that there are still limitations on theunderstanding of Salmonella in water and their potential sources.Salmonella remain a significant health risk in developing nations andimproved understanding of the role of water in the dissemination ofSalmonella in these countries and on how to manage the risks. Ofparticular concern is the rise in the presence of multi-drug resistancein Salmonella and the causes of this drug resistance.

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