Salmonella in Surface and Ddwringking Water Occurance and Water Mediated Transmission Levantesi - FoodResInter - 2011

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Salmonella in surface and drinking water:

Occurrence and water-mediated transmission
ARTICLE in FOOD RESEARCH INTERNATIONAL MARCH 2012
Impact Factor: 3.05 DOI: 10.1016/j.foodres.2011.06.037
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FRIN-03779; No of Pages 16
Food Research International xxx (2011) xxxxxx
Contents lists available at ScienceDirect
Food Research International

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / f o o d r e s
Review
Salmonella in surface and drinking water: Occurrence and

water-mediated transmission
Caterina Levantesi a,, Lucia Bonadonna b, Rossella Briancesco b, Elisabeth Grohmann c,
Simon Toze d, Valter Tandoi a
a
Water Research Institute, CNR, via Salaria km 29, 300-00015 Monterotondo, Rome, Italy
Department of Environment and Primary Prevention, Hygiene of Internal Water Unit, ISS, viale Regina Elena 299-00161, Rome, Italy
Department of Infectious Diseases, University Medical Center Freiburg, Hugstetter Strasse 55, 79106 Freiburg, Germany
d
CSIRO EcoSciences Precinct, Dutton Park 41 Boggo Road, Dutton Park, QLD 4102, Australia
b
c
a r t i c l e
i n f o
Article history:
Received 16 March 2011
Accepted 23 June 2011
Available online xxxx
Keywords:
Water-borne outbreaks
Salmonella
Typhoid fever
Surface water
Multiple drug resistance
Drinking water
a b s t r a c t
Salmonella is one of the leading causes of intestinal illness all over the world as well as the etiological agent of
more severe systemic diseases such as typhoid and paratyphoid fevers. While water is known to be a common
vehicle for the transmission of typhoidal Salmonella serovars, non-typhoidal salmonellae are mainly known as
foodborne pathogens. This paper provides a brief review of the last ten years of peer reviewed publications on
the prevalence of Salmonella in natural freshwaters and drinking waters, and on the relevance of these sources
for Salmonella dissemination. In industrialized countries, Salmonella was rarely reported in water-borne
outbreaks despite it being frequently detected in surface waters including recreational waters and waters
used for irrigation or as a drinking water source. Consistent contamination with irrigation waters has been
shown to be a common route of crop contamination in produces related Salmonella outbreaks. Multiple drug
resistant (MDR) Salmonella strains, that represent an increased hazard for human health and that may
contribute to the dissemination of drug resistances were also detected in surface water in developed
countries. Surface runoff was shown to play a main role as driver of Salmonella load in surface waters.
Accordingly, analysis of serovars indicated a mixed human and animal origin of Salmonella contribution to
surface waters, emphasizing the role of wild life animals in water contamination. Data relating to Salmonella
prevalence in surface and drinking water in developing countries are quite rare. Nevertheless, data on waterborne outbreaks as well as case control studies investigating the risk factors for endemic typhoid fever
conrmed the relevance of water as source for the transmission of this disease. In addition epidemiological
studies and Salmonella surveys, consistently provided an undeniable evidence of the relevance of MDR
Salmonella Typhi strains in water-borne typhoid fever in developing countries.
2011 Elsevier Ltd. All rights reserved.
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Water-borne Salmonella infections and control strategies . . . . . . . . . . . . . .
2.1.
Developing countries . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Developed countries . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.
Control strategies to prevent Salmonella drinking water related transmission .
Role of contaminated waters in Salmonella foodborne outbreaks . . . . . . . . . .
Salmonella prevalence, diversity in surface, drinking water and groundwater . . . .
4.1.
Surface waters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.
Diversity of Salmonella strains isolated from surface waters . . . . . . . . .
4.3.
Drinking water and groundwater . . . . . . . . . . . . . . . . . . . . .
Salmonella survival and monitoring in water environment . . . . . . . . . . . . .
5.1.
Salmonella survival . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.2.
Conventional and alternative microbial indicators for Salmonella monitoring in
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environment .
Corresponding author. Tel.: + 39 06 90672781; fax: +39 06 90672787.

E-mail address: Levantesi@irsa.cnr.it (C. Levantesi).
0963-9969/$ see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodres.2011.06.037
Please cite this article as: Levantesi, C., et al., Salmonella in surface and drinking water: Occurrence and
water-mediated transmission, Food Research International (2011), doi:10.1016/j.foodres.2011.06.037
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C. Levantesi et al. / Food Research International xxx (2011) xxxxxx
6.
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
One third of the world's population live in countries with some
level of water stress and water scarcity is expected to increase in the
next few years due to increases in human population, per capita
consumption and the resulting impacts of human activity on the
environment (Asano, Burton, Leverenz, Tsuchihashi, & Tchobanoglous,
2007). The availability of good quality water sources is therefore
getting more and more limited and the impact of water-borne
pathogens in human health is expected to be signicant (Suresh &
Smith, 2004). It is therefore critical to understand the relevance of
natural and drinking water contribution to transmission of pathogenic
microorganisms.
Salmonella is a ubiquitous enteric pathogen with a worldwide
distribution that comprises a large number of serovars characterized
by different host specicity and distribution. This microorganism is
one of the leading causes of intestinal illness through the world as
well as the etiological agent of more severe systemic diseases such as
typhoid and paratyphoid fever (Pond, 2005). Zoonotic salmonellae are
commonly described as foodborne pathogens, however, drinking
water as well as natural waters are known to be an important source
for the transmission of these enteric microorganisms (Ashbolt, 2004;
Leclerc, Schwartzbrod, & Dei-Cas, 2002). Salmonella, just like other
enteric bacteria, is spread by the fecaloral route of contamination.
This microorganism can enter the aquatic environment directly with
feces of infected humans or animals or indirectly, e.g., via sewage
discharge or agricultural land run off. Overall Salmonella spp. and
subspecies can be found in a large variety of vertebrates. Beside
humans, animal sources of Salmonella include pets, farm animals and
wild animals; calves, poultry, pigs, sheep as well as wild birds (sea
gull, pigeon) and reptiles can all be reservoirs of Salmonella (Dolejsk,
Bierosov, Kohoutov, Literk, & Czek, 2009; Lightfoot, 2004; Wray &
Wray, 2000). Plants, insects and algae were also found capable of
harboring Salmonella and might be implicated in the transmission of
this enteric pathogen (Byappanahalli et al., 2009; Guo, van Iersel,
Chenn, Brackett, & Beuchat, 2002; Ishii et al., 2006; Natvig, Ingham,
Ingham, Cooperband, & Roper, 2002).
Salmonellae are frequently found in environmental samples. They
are usually present in large numbers in raw sewage (10 310 4 CFU/L)
and can still be present in wastewater efuent after advanced
secondary treatment including coagulation, ltration and disinfection
(Maier, Pepper, & Gerba, 2000; Wry, Lhoutellier, Ducray, Delgens, &
Godon, 2008). Soil and sediment were also found to harbor
salmonellae (Abdel-Monem & Dowidar, 1990; Gorski et al., 2011;
Tobias & Heinemeyer, 1994) and sediment particles are believed to
function as a micro ecological niche enhancing salmonellae survival in
lakes (Chandran et al., 2011). In the aquatic environment this
pathogen has been repeatedly detected in various types of natural
waters such as rivers, lakes, coastal waters, estuarine as well as
contaminated ground water (Haley, Cole, & Lipp, 2009; Levantesi
et al., 2010; Martinez-Urtaza et al., 2004; Martinez-Urtaza, Liebana,
Garcia-Migura, Perez-Pieiro, & Saco, 2004; Polo et al., 1999; Wilkes
et al., 2009).
In addition to its widespread occurrence, elevated survival
capacities in non-host environment have been reported for Salmonella
(Wineld & Groisman, 2003). The growth of Salmonella in non-host
environments such as wastewater sludge and compost has also been
reported (Zaleski, Josephson, Gerba, & Pepper, 2005) and the growth
of Salmonella in water supplies is also considered possible, due to its
ability to colonize surfaces and replicate in biolms of distribution
0
0
system pipes (Jones & Bradshaw, 1996). However, standard disinfection procedures used in drinking water treatment processes are active
against salmonellae (Cicmanec, Smith, & Carr, 2004).
Taxonomically the genus Salmonella comprises two species
namely S. bongori and S. enterica. The species S. enterica is further
differentiated in to six subspecies (enterica, salamae, arizonae,
diarizonae, indica and houtenae) among which the S. enterica
subspecies enterica is mainly associated to human and other warm
blooded vertebrates. Traditionally members of the genus Salmonella
are clustered in serovars according to their agellar (h) and somatic
(o) antigens. Currently over 2400 Salmonella serovars have been
described but only about 50 serovars, all within the subspecies
enterica, are common causes of infections in humans and warm
blooded animals (Popoff, 2001). Salmonella serovars have different
host specicity, diverse geographic distribution, and cause different
syndromes. On the basis of the clinical syndromes caused Salmonella
are divided in to two distinct groups namely the typhoidal and nontyphoidal Salmonella serovars (Pond, 2005).
Enteric fevers, typhoid and paratyphoid fever are severe, contagious systemic diseases caused by the infection of the serovars Typhi
and Paratyphi. Even though not common in developed countries,
enteric fevers remain an important and persistent health problem in
less industrialized nations. Overall, in 2003 an annual incidence of
approximately 17 million cases of typhoid and paratyphoid fevers was
reported worldwide (Kindhauser, 2003). Differently from other
Salmonella serovars, Typhi and Paratyphi are host adapted and can
only infect humans; stools of infected persons are therefore the
original source of contaminations for these pathogens. Water
contaminated with feces of human cases and carriers is one of the
main vehicles of typhoid fever infections.
Differently from typhoidal Salmonella strains, non-typhoidal
salmonellae, the ubiquitous subtypes found in a number of animal
species, are more frequently associated to foodborne than to waterborne transmission. These zoonotic Salmonella serovars tend to cause
acute but usually self-limiting gastroenteritis. In some patients,
however, these same serovars can cause severe systemic diseases
such as osteomyelitis, pneumonia and meningitis (Pond, 2005).
Severe and invasive presentations of non-typhoidal salmonellosis in
Africa are common in children with co-morbidities (Graham, 2002)
and immune compromised HIV infected adults (Gordon, 2008).
Notably the emergence of MDR strains of Salmonella Enteriditis and
Typhimurium was associated to the observed incidence of invasive
salmonellosis (Gordon & Graham, 2008).
The increased frequency of MDR Salmonella strains in human
infections is an emerging issue of major health concern (Lightfoot,
2004; Lynch et al., 2009; Pond, 2005). As a consequence, the possible
role of fecally contaminated waters in the dissemination of MDR
Salmonella, both typhoidal and non-typhoidal, as well as antibiotic
resistance genes though horizontal gene transfer is of great interest.
This issue is of particular concern in developing countries where the
common use of untreated, low quality water as drinking water
sources together with inappropriate use and self-prescribing of
antibiotics increase the risk of drug resistance and the probability of
wide dissemination of resistant strains of high human health concern
(Oluyege, Dada, & Odeyemi, 2009; Srikantiah et al., 2007).
Overall, the above reported characteristics suggest that water
might be an important source for the transmission of all salmonellae,
not only for the typhoid serovars. An increased knowledge on the
prevalence, diversity and survival of this enteric bacterium in the
environment, together with a proper assessment, trough effective
surveillance and epidemiological studies, of the relevance of the water

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

Vollaard et al., 2004). Very few or no publication from Africa and
Central/Latin America, respectively, addressed the role of water as
vehicle of Salmonella transmission in the last ten years.
Reports on typhoid and paratyphoid fever epidemics in Asia
consistently indicate that contamination of drinking water, sourced
from well water (Farooqui et al., 2009), piped municipal drinking
water (Bhunia et al., 2009; Kim et al., 2003; Lewis et al., 2005; Mermin
et al., 1999) and unboiled spring water (Swaddiwudhipong &
Kanlayanaphotporn, 2001) was the main source of outbreaks. In
addition to this, most of the papers (Kim, 2010; Lewis et al., 2005;
Mermin et al., 1999; Swaddiwudhipong & Kanlayanaphotporn, 2001)
clearly show the involvement of MDR typhoid strains in water-borne
epidemics. Mermin et al. (1999) reported a massive epidemic of MDR
typhoid fever in Dushanbe, Tajikistan, associated with the consumption of municipal water. In the rst half of the year 1997, 8901 cases of
typhoid fever and 95 associated deaths were reported in Dushanbe. A
casecontrol study demonstrated that Salmonella Typhi infection was
associated with drinking unboiled water or obtaining water from
sources outside the house. Lack of chlorination, equipment failure,
and back-siphonage in the water distribution system led to contamination of the drinking water (Mermin et al., 1999). Of 29 Salmonella
serovar Typhi isolates tested, 27 were resistant to seven antibiotics,
namely to ampicillin, chloramphenicol, nalidixic acid, streptomycin,
sulsoxazole, tetracycline, and trimethoprim-sulfamethoxazole. Although 93% of the tested Salmonella serovar Typhi isolates from
Dushanbe were resistant to antimicrobials commonly used for
typhoid fever, the case mortality rate of 1.0% was rather low (Mermin
et al., 1999).
Farooqui et al. (2009) reported the study of a community outbreak
of typhoid fever associated with drinking water in a village close to
Karachi, Pakistan. This outbreak claimed three human lives and left
more than 300 people infected within a one week. The infected people
consumed water from a well that was the only available source of
drinking water in the village. Epidemiological investigations revealed
the gross contamination of the well with dead and decaying animal
bodies, their fecal material and garbage. Microbiological testing
conrmed the presence of MDR strains of Salmonella serovar Typhi
in 100% of the well water samples and 65% of household water
samples (Farooqui et al., 2009). In the summer of 2002 during a 7week period, 5963 cases of typhoid fever were reported in Bharatpur,
a town in Nepal with a population of 92,214 inhabitants (Lewis et al.,
2005). This outbreak was the largest single-point source outbreak of
MDR typhoid fever reported so far. The outbreak was traced with
molecular epidemiological methods to a single sourcethe sole
municipal water supply. A total of 90% of the isolates were
resistant to more than one antibiotic. MDR S. Typhi were also found
to be the etiological agent in a water-borne outbreak in a nonendemic community with otherwise good sanitation in Thailand
(Swaddiwudhipong & Kanlayanaphotporn, 2001).
In agreement with the studies relating to typhoid fever outbreaks,
epidemiological studies on the risk factors for endemic and sporadic
typhoid fevers in Asia conrmed the association between this disease
and the use of poor quality water (Gasem et al., 2001; Sharma et al.,
2009; Srikantiah et al., 2007; Tran et al., 2005). Srikantiah et al. (2007)
and Tran et al. (2005) indicated the use of untreated drinking water in
Uzbekistan and unboiled surface water in Vietnam, respectively, as a
major risk factor for typhoid fever. Srikantiah et al. (2007) also
showed that MDR Salmonella Typhi strains were important in
endemic typhoid fever in the Samarkand region of Uzbekistan. They
found that multiple antimicrobial resistance to ampicillin, chloramphenicol, and trimethoprim-sulfamethoxazole, were in 6 (15%) of 41
Salmonella serovar Typhi isolates from patients. Furthermore recent
consumption of antimicrobials (two weeks preceding illness) additionally increased the risk of infection (Srikantiah et al., 2007). In
Seramang city and the surrounding area (Indonesia), typhoid fever
was associated with living in a house without water supply from the
municipal network along with the use of low quality water for
washing and drinking (Gasem et al., 2001). Finally, Sharma et al.
(2009) showed that the unsafe use of water, namely scooping out
water from containers instead of using piped water or water stored in
a narrow mounted container at home, was associated with typhoid
fever. Using GIS to explore the epidemiological pattern across
Vietnam by investigating the risk factors associated with shigellosis,
typhoid, and cholera, Kelly-Hope et al. (2007) revealed that typhoid
fever prevailed in the Mekong River Delta. They observed that typhoid
fever was mostly associated with high vapor pressure and the use of
river and streams as drinking water. On the contrary, forested regions
and public tap drinking water were found to be negatively associated
with typhoid fever. In contrast to this, Vollaard et al. (2004) showed
that fecally contaminated drinking water was not associated with
typhoid and paratyphoid fevers in Jakarta Indonesia. However, in this
study, the habit of boiling water before consumption was declared by
all the people surveyed, both test cases and control sources, possibly
explaining the lack of association between microbiological contamination of drinking water and typhoid fever. Vollaard et al. (2004) also
showed that typhoid fever was signicantly associated with consuming ice cubes and iced drinks highlighting this as a likely water
mediated route of transmission. The importance of ice cubes as a
potential source of typhoid infection is supported by other studies in
which it was shown that consumption of ice cubes (Gasem et al.,
2001), avored ice drinks (Black et al., 1985) and ice creams (Luby
et al., 1998) are risk factors for this disease. In agreement with these
observations was the report that prolonged survival of Salmonella in
ice (Butler, Mahmoud, & Warren, 1977; Dickens, DuPont, & Johnson,
1985).
Nevertheless most of the recent risk factor studies showed that use
of unsafe water was not the only risk factor associated with
typhoid/paratyphoid fever thus indicating multiple routes of transmission for these diseases (Gasem et al., 2001; Sharma et al., 2009;
Vollaard et al., 2004). Interestingly, Vollaard et al. (2004) showed that
in Jakarta typhoid and paratyphoid fevers are associated with
different routes of transmission. Risk factors for typhoid and
paratyphoid fevers, respectively, were mainly within and outside
the household.
As in other developing countries, in Africa, Salmonella Typhi is a
major cause of enteric disease, particularly in children (Crump, Luby,
& Mintz, 2004). The real burden of typhoid fever in Africa is largely
unknown because of the lack of comprehensive surveillance studies
and credible measures of the disease incidence. However, a mean
incidence of 50 cases per 100,000 persons per year has been estimated
for the whole continent with a highest value in South Africa
(N100/100,000 cases/year) (Crump et al., 2004). Even if typhoid
fever can be considered an endemic disease in Africa very few studies
relating to Salmonella Typhi waterborne transmission in this continent are available in the recent literature.
In Nigeria, Oguntoke, Aboderin, and Bankole (2009) investigated
relationships between water-borne diseases, morbidity patterns,
drinking water source quality and water handling practices in Ibadan
City. Oguntoke et al. found that typhoid fever was the most common
water-borne disease (39.3%) in the area followed by bacillary
dysentery and cholera. In agreement with the hypothesized water
mediated route of transmission about 50% of the analyzed waterborne diseases infections occurred in the heavy rain period (Oguntoke
et al., 2009). In Ibadan City Salmonella Typhi and Paratyphi were
detected in the well waters and the microbial water quality was found
to be positively correlated with the pattern of water-borne disease
within the selected areas. Additionally multivariate regression
analysis showed that the percentage of residents applying inadequate
domestic water treatment (mostly potash alum addition) explained
68.6% (P b 0.04) of the pattern of waterborne diseases morbidity in the
area (Oguntoke et al., 2009). The spatial distribution of diarrhea and
microbial quality of water for domestic uses in the Venda region

(South Africa) were analyzed by GIS during an outbreak of diarrhea
(Bessong, Odiyo, Musekene, & Tessema, 2009). The Venda region, a
rural area, is characterized by the lack of clean potable water and the
inadequacy of sanitation (Obi et al., 2004; Potgieter et al., 2005). Using
a stratied random-sampling approach, the study identied a
signicant clustering of diarrhea cases to two water extraction points
which were of poor microbial quality and contained potential
diarrhea-causing organisms including Salmonella (Bessong et al.,
2009).
In many African countries MDR non-typhoidal salmonellae are
reported to be the commonest cause of bacteraemia in children under
5 years (Gordon & Graham, 2008). Life-threatening invasive disease
outbreaks in children caused by MDR non-typhoidal salmonellae have
been reported in several African countries (e.g. Graham, 2002; Kariuki
et al., 2006). Nevertheless the sources and mode of transmission of
non-typhoidal salmonellae in Africa are still unknown. In a prospective study in Kenya, Kariuki et al. (2006) compared the serovars and
genotypes of non-typhoidal salmonellae isolates from children with
bacteraemia, from family contacts, and from home environmental
samples. Salmonella isolates from family contacts showed the highest
similarity to those of clinical cases indicating that human-to-human
transmission route plays a major role in non-typhoidal salmonellae
transmission in the area. Nevertheless, clustering of non-typhoidal
Salmonella bacteraemia in the rainy season in Africa suggests that
there is also a water-borne/water-associated transmission route
(Suresh & Smith, 2004).
2.2. Developed countries
In contrast to what has been observed for the less industrialized
nations, most of the data on water-borne salmonellae in developed
countries involve non-typhoidal Salmonella serovars. In many industrialized countries, the widespread implementation of municipal
water and sewage treatment systems in the second half of the 20th
century has resulted in a dramatic decline in the incidence of waterborne typhoid fever (Lynch et al., 2009; Smith et al., 2006). Even if
they remain endemic in a few geographic regions (Rizzo et al., 2008),
typhoid and paratyphoid fever are now rare diseases, mainly
associated with people returning from foreign travel to regions
where these diseases are still much more common (Lynch et al.,
2009).
In the USA since 1971, the CDC, in collaboration with the EPA and
with the Council of State and Territorial Epidemiologists, began a
surveillance program to collect and report data of water-borne
outbreaks. According to the CDC data from 1971 to 2000, nontyphoidal zoonotic Salmonella were the causes of 15 drinking-waterborne outbreaks which accounted for 6% of the total zoonotic waterborne outbreaks in the USA (Craun, Calderon, & Craun, 2004). As
revised by these authors, most of these salmonellae outbreaks (11/15)
were associated with community water systems and groundwater
instead of surface water. In the same period, the use of untreated
groundwater along with inadequate treatment of collected groundwater and distribution systems contamination were the most
important deciencies identied for causing outbreaks of enteric
bacteria. Further analysis has shown that various Salmonella subspecies, comprising Typhimurium, Enteriditis, Bareilly, Javiana, Newport
and Weltervreden, were the causes of water associated Salmonella
outbreaks in the USA (Craun et al., 2004). From 2000 to 2006
salmonellae were found very rarely or not at all in drinking waterborne outbreaks in USA (Blackburn et al., 2004; Liang et al., 2006;
Yoder et al., 2008). Nevertheless, two recent outbreaks indicated that
water-borne salmonellae are still of health concern in cases of
deciency of water treatment or inadequate water supply systems in
the USA (Berg, 2008; Kozlica et al., 2010). In August 2008, the health
department and regulatory ofcials identied an outbreak of
Salmonella I 4,[5],12:i: involving ve persons in a rural community in

Tennessee. An untreated water supply was recognized as the source of
infection. It was found that the water, which had been collected from a
spring, had been stored in a small unprotected reservoir subject to
contamination from runoff and wildlife (Kozlica et al., 2010). In the
second reported case during March and April 2008, an outbreak of
water-borne disease associated with Salmonella struck the city of
Alamosa in Colorado. Salmonellae were found to have contaminated
the public water system that supplies drinking water to the
community. The outbreak resulted in 442 reported illnesses, 122 of
which were laboratory-conrmed, and one death. Epidemiological
estimates suggested that up to 1300 people may have been ill (Berg,
2008). Alamosa's drinking water comes from deep artesian wells in an
aquifer considered to be a protected groundwater source. Prior to the
outbreak, the city's drinking water was not chlorinated for disinfection but was historically in compliance with all health-based drinking
water standards. The most probable cause of the outbreak was a
contamination of a ground-level water storage reservoir by animal
feces that successively spread throughout the entire system. The
reservoir was found to have several small cracks and holes that likely
allowed the contamination source to enter.
Only one Salmonella water-borne outbreak related to recreational
water exposure was recorded by the CDC between 1995 and 2005
(Levy, Bens, Craun, Calderon, & Herwaldt, 1998; Pond, 2005). On the
contrary, recreational aquatic environments, both salt and fresh
waters, were indicated as the most important risk factor for sporadic
childhood Salmonella infections at three Washington state county
health departments (Denno et al., 2009). Denno et al. (2009)
conducted a prospective case control study to investigate the possible
association between sporadic childhood reportable enteric infections
and different plausible exposures. Infection with Salmonella was
found to be strongly related to playing or swimming in natural water
sources. In addition, associations between the use of private well as
home drinking water sources and the use of septic systems for home
wastewater disposal were also observed as potential sources of
Salmonella infections.
In Australia, salmonellae were found to be the most common
pathogen in drinking water-borne outbreaks from 2001 to 2007 (Dale
et al., 2007). Salmonella spp. were implicated in ve of 10 observed
drinking water-borne outbreaks and in an outbreak derived from a
contaminated aquarium. The serovars Saintpaul, Typhimurium, subsp
IIIb 61:i:z35, Muenchen and Para B bv java, were identied as
outbreak causes. Differently from what has been observed in the USA
where Salmonella outbreaks were mostly related to contaminated
community water systems, in Australia contaminated tank and bore
waters were identied as the origin of outbreaks. Ashbolt and Kirk
(2006) conducted a case control study to investigate risk factors for
sporadic Salmonella Mississippi infections in Tasmania (Australia)
showing that the exposure to untreated drinking water was a risk
factor for this disease. These authors also highlighted that most of the
exposures to untreated drinking water were recorded as exposure to
water collected in rainwater collection tanks. Roof collected rain
water were involved in several other water-borne outbreaks by
Salmonella in Australia (Franklin et al., 2009; Taylor et al., 2000)
suggesting that appropriate preventive measures must be undertaken
to avoid that the increased use of rainwater tanks may increase the
risk of water-borne disease outbreaks (Franklin et al., 2009).
In Europe, monographic water-borne outbreaks reports such as
those of CDC/EPA, are not available because drinking water is dened
as food and thus included in foodborne outbreaks reporting. Country
specic review of water-borne outbreaks in Italy (Blasi et al., 2008)
and the UK (Smith et al., 2006) were recently published. According to
the complete surveillance data of Communicable Disease Surveillance
Centre (CDSC), Salmonella was never associated to water-borne
outbreaks in England and Wales from 1992 to 2003 (Smith et al.,
2006). In contrast, salmonellae were implicated in outbreaks that
occurred in Italy from 1998 to 2005. However because the

surveillance system on communicable diseases in Italy is not planned
to efciently identify water-borne outbreaks, the number of reported
cases do not represent an accurate clear estimation of the real
situation (Blasi et al., 2008).
2.3. Control strategies to prevent Salmonella drinking water related
transmission
As for other water-borne pathogens, different measures can be
adopted to hinder the spread of Salmonella in water environment, and
consequently reduce human risk of infection. Regarding the measures
to reduce the occurrence of Salmonella in drinking water, the control
strategies have to be elaborated and adopted on the basis of the water
resource availability and the economic and developmental level of the
country. For this purpose, the World Health Organization has
developed Guidelines for Drinking Water Quality, which provides an
internationally harmonized support to help countries develop rules
and standards that are suitable to national and local circumstances
(WHO, 2008).
In developing countries, commonly lacking piped water supply,
self-sustaining decentralized approaches including point of use
chemical and solar disinfection, safe water storage and behavioral
changes are indicated as reliable options to directly target the most
affected population and reduce water-borne disease burden through
improved drinking water quality (Mintz, Bartram, Lochery, &
Wegelin, 2001). In this respect, three recent reviews that used
meta-analysis to evaluate the effect of water treatment at point of use
on water quality and diarrhea reduction showed that point of use
interventions more efciently reduced diarrhea incidence, with
respect to water source interventions (Arnold & Colford, 2007; Clasen,
Schmidt, Rabie, Roberts, & Cairncross, 2007; Fewtrell et al., 2005).
Studies of the risk factors for typhoid and paratyphoid endemics
and epidemics infections conrm that simple decentralized control
strategies might be effective in the control of these diseases (Sharma
et al., 2009; Srikantiah et al., 2007). According to the ndings of
Sharma et al. (2009) home chlorination of drinking water, the use of
narrow-mounted containers for safe water storage, and drawing out
water by tilting the container or using taps to avoid contamination
may be effective practices to avoid spread of typhoid in west Bengal
India. Farooqui et al. (2009) reported measures recently introduced by
WHO that include solar disinfection, bleach addition, boiling, and use
of low cost ceramic lters, which are well suited to prevent typhoid
fever outbreaks due to the consumption of contaminated surface or
drinking water.
Education regarding the risk of drinking untreated surface water as
well as promoting the use of boiled drinking water carried from home,
was indicated by Srikantiah et al. (2007) as practical intervention
measures to reduce water related transmission of typhoid fever in
Samarkand (Uzbekistan). Srikantiah et al. (2007) also suggested
specic intervention strategies to reduce the increased risk linked to
MDR typhoid strains. According to their results the use of antimicrobials two weeks before onset of typhoid fever was independently
associated to this disease; hence the development of primary care
clinical treatment guidelines to reduce unnecessary antimicrobial
exposure may efciently decrease the risk of typhoid fever.
In many industrialized countries, the success of applied control
strategies is conrmed by the small number of water-borne outbreaks
caused by salmonellae. Nevertheless, outbreaks caused by microbial
contamination of drinking water still result in substantial human and
economic costs in these countries (Berg, 2008; Risebro et al., 2007).
The identication of the causes outbreaks and the potential threats to
water quality is necessary to formulate effective prevention strategies
that will minimize the further onset of outbreaks and related costs.
Causes of water-borne outbreaks in developed countries have been
extensively reviewed in recent publications (Craun et al., 2010; Craun,
Calderon, & Craun, 2005; Dale et al., 2007; Risebro et al., 2007;
Schuster et al., 2005). Unfortunately most of these reviews consider
the enteric bacteria as a whole and specic deciencies associated to
salmonellae water-borne outbreaks could not be extrapolated.
Schuster et al. (2005) analyzed 288 cases of drinking water related
outbreaks in Canada from 1974 to 2001 showing that water treatment
failure and contamination from wildlife were the causative factors
most often cited in outbreak reports. Analyzing water-borne outbreaks of enteric diseases associated with EU public drinking water
supplies (19902005), Risebro et al. (2007) found that contamination
of source water and failure of water treatment accounted for more
than 50% of the recorded outbreaks. In particular they found that
disinfection deciencies were associated with 75% of outbreaks due to
bacterial, viral and mixed pathogen contamination (Risebro et al.,
2007). In their complete review of drinking water associated
outbreaks in USA (19712006) Craun et al. (2010) showed, inter
alias, that greater attention is needed to address and reduce the risk of
outbreaks in groundwater supplied systems and in private water
systems. Overall it is apparent that the diversity of causative factors of
outbreaks in different countries requires different specic control
actions. The control is essentially carried out through application of
process control measures, which are provided by the WHO Guidelines
(WHO, 2008). The approach that has been proposed is the Hazard
Analysis Critical Control Points (HACCP) approach, which prioritizes
the identication of key potential contamination or control points in
the treatment and distribution system. This approach has already
been successfully used by the food and beverage industry, it allows
operators and authorities to focus their resources on monitoring
crucial points to detect and quickly correct any deviation from a
correctly operating system. Another successful approach, which is
combined with HACCP principles, is the multi-barriers approach.
Different steps are selected in the treatment process in order to
increase removal capability and normal uctuations in performance
can be compensated. In this way the likelihood that pathogens can
enter the distribution system and reach consumers is minimized. The
two approaches together constitute a water safety framework that is a
basic structure to develop supply-specic water safety plans to ensure
the production of high quality drinking water. In agreement with this,
the EPA's Ground Water Rule (USEPA, 2006) establishes a risk
targeted approach to identify those systems that may be most
susceptible to fecal contamination and species corrective actions
(Craun et al., 2010).
3. Role of contaminated waters in Salmonella foodborne

outbreaks
In recent years, reports of Salmonella outbreaks related to fresh
produce consumption have illustrated the likely relationships
between salmonellae, water and ultimately foodborne Salmonella
infections (CDC, 2002, 2008; Greene et al., 2008; Mohle-Boetani et al.,
2009; Sivapalasingam et al., 2003). It is now commonly accepted that
fruit and vegetable consumption is a risk factor for infections with
enteric pathogens (Heaton & Jones, 2007). Three recently published
reviews clearly summarized the current knowledge on the role of
fresh produces as source for the transmission of human enteric
pathogens (Berger et al., 2010; Heaton & Jones, 2007), and in
particular of Salmonella (Hanning, Nutt, & Ricke, 2009). Salmonella is
the most common aetiological agents associated to fresh produce
related infections (Heaton & Jones, 2007; Sivapalasingam, Friedman,
Cohen, & Tauxe, 2004). A wide spectrum of produce have been
associated with salmonellae infections including tomatoes (Greene
et al., 2008; Sivapalasingam et al., 2004), serrano peppers (CDC,
2008), cantaloupe (CDC, 2002; Sivapalasingam et al., 2004), lettuce
(Takkinen et al., 2005), basil (Pezzoli et al., 2008), and mango
(Sivapalasingam et al., 2003).
Salmonellae are often isolated from produce samples in routine

surveys (Thunberg, Tran, Bennett, & Matthews, 2002). Additionally
some S. enterica strains have the ability to adhere to plant surfaces
where they are able to survive for long periods and then grow
(Gandhi, Golding, Yaron, & Matthews, 2001; Islam et al., 2004). The
capacity of this pathogen to become endophytic, thus to invade
internal plant parts has also been reported (e.g. Deering, Pruitt,
Mauer, & Reuhs, 2011; Klerks, Franz, van Gent-Pelzer, Zijlstra, & van
Bruggen, 2007; Lapidot & Yaron, 2009; Schikora, Carreri, Charpentier,
& Hirt, 2008). Among others Lapidot and Yaron (2009) demonstrated
the ability of S. enterica serovar Typhimurium to transfer from
contaminated irrigation water in plant roots and then into the edible
parts of mature parsley. However the transfer of S. enterica serovar
Typhimurium from water to plants was shown only to occur with
highly contaminated irrigation water (Lapidot & Yaron, 2009).
Water is likely to be an important source of produce contamination in the eld as well as in post harvested processing (Berger et
al., 2010). Water sources of varying microbiological quality are
used for irrigation of produce worldwide. For example, in the UK,
71% of irrigation water is obtained from surface waters which
receive treated sewage efuent (Tyrrel, Knox, & Weatherhead,
2006) and in developing countries untreated wastewater is also
commonly used to irrigate crops, thus increasing the risk of
microbial contamination (Ashbolt, 2004). Gagliardi, Millner, Lester,
and Ingram (2003) showed an increased count of microbial
indicators on cantaloupe rinds after fruit washing and cooling in
hydrocooler indicating that inadequately decontaminated water
used in post harvesting produce processing can also be a sources of
microbial contamination.
Contaminated irrigation and processing waters were indicated as
possible sources of Salmonella contamination in several fresh produce
outbreaks (CDC, 2002, 2008; Greene et al., 2008; Sivapalasingam et al.,
2003). In 2002 and 2005 two multistate outbreaks of S. Newport in
USA, caused by the same rare S. Newport strain, were associated with
eating tomatoes (Greene et al., 2008). Tomatoes causing of the
outbreak were traced back to the eastern shore of Virginia where the
S. Newport outbreak strain was isolated. Notably this outbreak strain
was isolated from the pond water used to irrigate tomato elds both
in 2002 and 2005 (Greene et al., 2008). The presence of the S. Newport
outbreak strain, two years apart, in the irrigation pond demonstrate
that if not properly addressed, the source of contamination can persist
and cause continuous outbreaks (Greene et al., 2008).
Salmonella serovar Newport was also the etiological agent in a
multistate outbreak linked to mango consumption in USA
(Sivapalasingam et al., 2003). The implicated mangoes were traced
back to a single Brazilian farm where mangoes were washed with
contaminated water (Sivapalasingam et al., 2003). Analysis of the
irrigation and processing water at this farm indicated the presence of
Salmonella spp. in the water. Sivapalasingam et al. (2003) suggested
that hot and cool water treatment which allowed the internalization
of Salmonella in the mangoes was the most likely source of
contamination. The S. Newport outbreak strain was no actually
isolated from the Brazilian water samples however, the farm
investigation took place many months after the outbreak had
occurred (Sivapalasingam et al., 2003). In 2008, a large multistate
outbreak of Salmonella Saintpaul associated with multiple raw
produce items infected a total of 1442 people in the USA and Canada
(CDC, 2008). Jalapeno and serrano peppers imported from Mexico
were identied as the major sources of this outbreak. The S. Saintpaul
outbreak strain was isolated from samples of jalapeno pepper as well
as of irrigation water at a Mexican farm suggesting a possible route of
Salmonella contamination (CDC, 2008). Irrigation of elds with
sewage contaminated waters and processing produce with Salmonella
contaminated waters were also indicated as possible sources of
contamination in an outbreak of S. Poona infections in the USA
associated with eating imported cantaloupe (CDC, 2002).
Several studies have investigated the potential source of produce

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

(Bhatta et al., 2007; Dolejsk et al., 2009; Meinersmann et al., 2008;
Oluyege et al., 2009; Patchanee et al., 2010) consistently indicate that
these aquatic environments are a reservoir of MDR strains, which
might contribute to the dissemination of these MDR strains through
susceptible populations.
4.1. Surface waters
A survey of recent studies showed an increasing interest over the
last two years on the role of non-host habitats, such as surface water
environments as natural reservoir and in the transmission of
Salmonella and other enteric pathogens (Ahmed, Sawant, Huygens,
Goonetilleke, & Gardner, 2009; Byappanahalli et al., 2009; Dolejsk
et al., 2009; Haley et al., 2009; Jokinen et al., 2010, 2011; Patchanee
et al., 2010; Schriewer et al., 2010; Wilkes et al., 2009). A summary of
the available data on Salmonella prevalence in surface fresh waters
sources is shown in Table 1.
The data provided in Table 1 conrms the ubiquitous nature of this
enteric pathogen. Salmonellae were detected in different countries
and in very diverse water sources, ranging from pristine (e.g.
Patchanee et al., 2010; Till, McBride, Ball, Taylor, & Pyle, 2008) and
low impacted water (e.g. Jokinen et al., 2010; Meinersmann et al.,
2008; Patchanee et al., 2010) to heavily impacted water sources (e.g.
Bonadonna, Filetici, Nusca, & Paradiso, 2006; Jyoti et al., 2010).
Salmonella contamination occurred in surface water used for
recreational purposes (Till et al., 2008); as source of drinking water
(Till et al., 2008); and for irrigation (e.g. Gannon et al., 2004). This
demonstrated wide distribution of salmonellae underlines that there
is the potential for inadvertently using water contaminated with
Salmonella, with associated potential health risks. As shown in Table 1,
the Salmonella detection frequencies were extremely variable in the
investigated surface waters with detection rates ranging from 3 to
100%. In general, the highest frequencies were reported in watersheds
that had been highly impacted by human activities (Bonadonna et al.,
2006; Jyoti et al., 2010) or in geographical areas with a history of high
salmonellosis cases (Haley et al., 2009). However, Patchanee et al.
(2010) showed that elevated frequencies of Salmonella were also
found in a forestry watershed not inuenced by human activities.
Notably, these authors observed similar prevalence of salmonellae in
watersheds with diverse potential contamination sources, namely
residential industrial (58.8%), forestry (57.1%), crop/agriculture
(50%), and swine production (41.7%).
Also of all the studies listed in Table 1, despite the importance of
the knowledge of Salmonella concentrations in water to evaluate the
risk of water related infection, only a few performed a quantitative
assessment of Salmonella in environmental waters (Bonadonna et al.,
2003, 2006; Byappanahalli et al., 2009; Haley et al., 2009; Jyoti et al.,
2010; Lemarchand & Lebaron, 2003).
Temporal and spatial variation of Salmonella frequencies were
commonly observed in surface water (Bonadonna et al., 2006;
Byappanahalli et al., 2009; Haley et al., 2009; Jokinen et al., 2010;
Lemarchand & Lebaron, 2003; Meinersmann et al., 2008; Till et al.,
2008; Wilkes et al., 2009). It is possible that variations in the
occurrence of Salmonella in ambient water may be governed, in part,
by environmental parameters such as temperature, water chemistry,
and solar radiation that inuence survival and transport of the
microorganism. Other possible reasons include changes in pathogen
loading due to enhanced shedding from human and animal host, or
from enhanced ow of water from contaminated sources. Positive
correlations between rainfall events and Salmonella prevalence and/or
diversity have been reported by many authors (Baudart, Lemarchand,
Brisabois, & Lebaron, 2000; Haley et al., 2009; Jokinen et al., 2010; Polo
et al., 1999; Schets, van Wijnen, Schijven, Schoon, & de RodaHusman,
2008; Wilkes et al., 2009). These results, which are supported by
similar observations with respect to Salmonella contamination in
Table 1
Salmonella occurrence in surface waters.
Level and frequency positive Surface water
samples % (total samples)
Dominant impact in the analyzed water
Country
8.5% (342)
Mainly inuenced by rainfall runoff and

drainage from agricultural land
Mixed
Canada
River water
13% (186)
4
River water
10 10 CFU/100 mL
87% (8)
54% (86)
River water
Mixed comprising untreated sewage of

residential setup
Swine production Residential/industrial
Forestry Crop agriculture
Not described
7% (143)
Four differently impacted

watersheds systems
River and estuaries
3% (32)
Urban pond and tidal creeks
0.0020.017 MPN/mL
42% (19)
Lake and river water
Mixed: WWTPs efuents, surface runoff,

agricultural
Not described
16% (87)
Pond
Urban
River watershed
River and streams
Mixed: mainly forested and agricultural in a

area with high incidence of salmonellosi
mixed
75% (83)
Small river
Mainly rural area
3.8% (79)
Urban canals/river and

recreational lakesd
Stream water Puddles
Not described
Rivers and lakes Fresh water

recreational and water supply sites
River and pond around Sapporo
city
Riverf
Mixed: birds, dairy farming, municipal,

sheep/pastoral, forestry undeveloped
Mixed: WWTPs efuents, urban sewage, cow
and pig farms
Mixed: Urban/industrial comprising direct
sewage discharge
Animal and human activities, human and
animal feces
2.536.3 MPN/L
79% (72)
415% (1600)c
10.6% (216)
17.6% (17)
10% (725)e
53% (30)
4
1010 MPN/100 mL
100% (N 300)
75% (375)g
River, borehole
5.4% (802)
River and irrigation water
102105 MPN/100 mL
100% (10)
57% (14)
River
0.0642.4 CFU/L
100% (8)
River
a
b
c
d
e
f
g
River water
Mixed comprising WWTP discharge
9 sampling sites,
2 year
Canada
4 sampling sites,
2 years
India
8 sampling sites,
1 day
USA
4 sampling sites,
2 years
USA
10 sampling sites,
14 month
Australia
8 sampling sites,
2 months
USA
numerous
sampling sites,
2 years
2 sampling sites,
Czech
Republic
1 year
USA
6 sampling sites,
12 months
Canada
24 sampling sites,
3 years
USA
82 sampling sites,
1 day
Netherlands 8 sampling sites,
1 year
Mexico
Random
sampling, 2 years
New Zeland 25 sampling sites,
15 month
Japan
5 sampling sites,
3 months
Italy
8 sampling sites,
2 years
South Africa 8 sampling sites
Canada
Mixed: Urban/industrial, WWTP discharge

agricultural
Runoff from agricultural land and pastures,
human and animal feces
Mixed
Survey extent
Italy
Africa
1621 sampling
sites, 2 years
1 sampling site,
1 year
Weekly sampling,
5 months
France
References
Jokinen et al. (2011)
Jokinen et al. (2010)
Jyoti et al. (2010)
Patchanee et al. (2010)
Schriewer et al. (2010)
Ahmed et al. (2009)
Byappanahalli et al.
(2009)
Dolejsk et al. (2009)
Haley et al. (2009)
Wilkes et al. (2009)
Meinersmann et al.
(2008)
Schets et al. (2008)
Simental and MartinezUrtaza (2008)
Till et al. (2008)
Savichtcheva et al.
(2007)
Bonadonna et al. (2006)
Obi et al. (2004)
Gannon et al. (2004)
Bonadonna et al. (2003)
Obi, Potgieter, Bessong,
and Matsaung (2003)
Lemarchand and
Lebaron (2003)
qPCR quantication.
Range of average monthly density.
Different percentage in different seasons.
Only found in canals and river.
15% of river sample used for drinking water supply.
Highly contaminated area at environmental risk.
Environmental samples including water and sediments (89%) and food (11%).
coastal area and marine environment (Baudart, Grabulos, Barrusseau,

& Lebaron, 2000; Simental & Martinez-Urtaza, 2008), indicated that
increased pathogen load could be associated with rainfall events as
one major environmental driver of Salmonella contamination in
surface water environment. In agreement with this a positive
correlation was reported in the literature between rainfall events
and the incidence of Salmonella water related infections (e.g. Haddock
& Malilay, 1986; Suresh & Smith, 2004). In contrast, the variable
seasonal occurrence of Salmonella in aquatic environments reported
in the recent literature was not consistent with the summer peak
human and animal salmonellosis infection observed worldwide. Till
et al. (2008) reported an increase of the concentration of Salmonella
during late winter in New Zealand at a site where birds and sheep
were the major potential contamination source. In contrast, the
seasonal peak of Salmonella incidence in a Canadian watershed was
observed in the fall (Wilkes et al., 2009) potentially reecting
enhanced livestock based fecal input during this period. According

to Wilkes et al. (2009) salmonellae's incidence was found to be
positively correlated with tributary discharge values as well as with
accumulative rainfall. Only Haley et al. (2009) in a study of a
watershed in Georgia USA found that Salmonella incidence peaked in
the summer period. Over the complete study period, the presence of
this pathogen was positively correlated with water temperatures and
rainfall events (1 or 2 days before sampling). According to these
results, the authors concluded that multiple environmental factors,
including enhanced pathogen loading during storm events, increased
survival in the water environment at warm temperatures and
increased host shedding in the warmer season might explain the
Salmonella peak during the summer months.
Spatial differences in Salmonella prevalence in surface waters have
also been reported in the recent literature (Bonadonna et al., 2006;
Lemarchand & Lebaron, 2003; Meinersmann et al., 2008; Savichtcheva
et al., 2007; Schriewer et al., 2010). Schriewer et al. (2010) reported a

higher frequency of salmonellae in surface waters that have marine
inuences while Bonadonna et al. (2006) and Lemarchand and
Lebaron (2003), observed that the highest concentration of this
pathogen was associated to sampling points in densely populated
areas and/or downstream of sewage efuents discharge sites.
MDR strains have been detected in surface water in developed
countries (Dolejsk et al., 2009; Meinersmann et al., 2008; Patchanee
et al., 2010). In particular, Patchanee et al. (2010) showed that swine
production was a major source of antibiotic resistant Salmonella in
water environments as all the Salmonella isolates from a swine
production watershed had multiple resistances to antibiotics. In
contrast, antibiotic resistant strains were not detected from watersheds impacted by forestry, crop agriculture, or a residential/industrial
area (Patchanee et al., 2010). Antibiotic resistant Salmonella have also
been detected in surface water from a pond in the north-eastern part of
the Czech Republic as well as in birds, black-headed gulls nesting in
this pond (Dolejsk et al., 2009). A total of 16% of water and 24% of gull
samples yielded Salmonella. Antibiotic resistance was found in 12% of
salmonellae isolated from the water and 28% of gull salmonellae.
Resistance to the quinolone nalidixic acid, streptomycin, and tetracycline was often detected in these Salmonella isolates. Dolejsk et al.
(2009) concluded from these results that black-headed gulls can be
important reservoirs of antibiotic resistant salmonellae. Meinersmann
and co-workers investigated the prevalence of Salmonella and their
antimicrobial resistance prole in a synoptic study of the Oconee River
Basin, a small river in north-eastern Georgia, USA (Meinersmann et al.,
2008). Water samples were obtained from 83 sites with Salmonella
isolated from 62 of the samples, however, only seven of the isolates
were resistant to any antimicrobials.
Table 2
Salmonella diversity in surface waters.
Diversity Common
serovars
Serovar
(percentage
number/ of total
total
isolates)
isolates
Others serovars
11/29
Givea, Heidelberga,
Canada
Typhimurium,
Senftenberg, Mbandaka,
Other
Mbandaka, Bullbay, Give, USA
Miami, Braenderup
Jokinen et al.
(2011)
Braenderup, Anatum,
I47:z4z23, Gaminara,
Liverpool, Bareilly, Saint
Paul, I4,(5):b,
USA
Haley et al.
(2009)
Infantis, Derbyf, Indiana,

Hadarg, Typhimurium
Infantis, Kiambu,
Livingstone, Iv40:z4,z32:
Typhimurium, Paratyphi
B, Newport,
Oranieneburg, Ouakam,
Mbandaka, Montevideo,
Thompson, Gaminara,
Heidelberg, Braenderup
Czech
Republic
USA
Dolejsk et al.
(2009)
Meinersmann
et al. (2008)
12/104
13/197
6/17
19/73
4.2. Diversity of Salmonella strains isolated from surface waters

All Salmonella serovars are considered as potential pathogens. Only
about 50 of these serovars, however, have been predominantly
isolated from humans or animals (Popoff, 2001). Information
regarding the distribution and characteristics of Salmonella serovars
present in the environment are essential in assessing the role of nonhost aquatic habitats in the diffusion of Salmonella subtypes of high
human health concern. Furthermore, the identication of sourcespecic serovars might help future tracking of sources of Salmonella
contamination events.
The rst comprehensive studies describing the diversity of
Salmonella serovars in the aquatic environment were presented by
Polo et al. (1999) and Baudart, Lemarchand, et al. (2000). Both
research groups analyzed a large number of isolates from different
natural aquatic systems (river, wastewater and marine coastal areas)
showing a great diversity of Salmonella serovars. Since then, several
works have provided further data on the different serovars present
and on the possible sources of Salmonella contamination in surface
water. A summary of recent available data is reported in Table 2.
With the exception of few studies that analyzed a limited number
of isolates (Dolejsk et al., 2009; Schets et al., 2008) or monitored
highly contaminated watersheds (Bonadonna et al., 2006), the total
number of serovars detected in the investigated aquatic environments
ranged from 10 to 20 independently of the number of isolates or
samples analyzed in the different studies. In comparison to the results
of the initial studies by Baudart, Lemarchand, et al. (2000) and Polo
et al. (1999), these latter consistent gures found that there was a low
diversity of Salmonella serovars in the non-host water environment
(Table 2). This difference might be explained by the very long period
(5 years) of Salmonella monitoring described by Polo et al. (1999) and
the reported increase in the numbers of serovars during ood events
(10 of the 35 serovars were only isolated during the ood by Baudart,
Lemarchand, et al. (2000)).
11/23
45/92a
19/36
35/413h
Rubislaw
(72.4%)a
I:11:r:a
Derby
Anatum
(18.3%)
Gaminara
(18.3%)
Inverness
(18.3%)
Muenchen
(8.7%)b
Newport
(8.7%)b
Bredeney
(6.7%)
S. enterica
subsp arizona
(40.6%)
Muenchen
(14.2%)c
Rubislaw
(13.2%)c
Mikawasima
(6.1%)
Montevideoe
Enteritidis
(50%)d,e
Muenchen
(20%)
Rubislaw
Hartford
Give
Newport
Virchow
Typhimurium
Typhimurium
(39%)
Urbana
Suberu
Vejle
Typhimurium
(13.7%)
Subsp. II
(8.4%)
Infantis
(5.3%)
Bredeney
(4.2%)
Stanley
(4.2%)
Derby (4.2%)
Derby
(16.6%)
03,10:r:
Anatum
Bardo
Javiana
Country
Reference
Patchanee et
al. (2010)
Netherlands Schets et al.

(2008)
Othmarschem, Soerenga,
Augustenborg, Breda,
Coeln, DJugu
Mexico
Simental and
MartinezUrtaza
(2008)
Saint Paul,
Bovismorbicants,
Montevideo, Enteriditis,
Give (only serotypes
detected also by other
authors)
Italy
Bonadonna et
al. (2006)
03,10:vt, Subsp.III b,
Subsp. IV, Stanley,
Typhimurium,
Tennessee, London,
Bovismorbicants,
Dessau, Paratyphi B,
Schleissheim, Lexington,
Mbandaka, Enteriditis
Vietnam
Phan et al.
(2003)
France
Baudart,
Lemarchand,
et al. (2000)
Typhimurium
(31.1%)
Virchow
Panama
Newport
Hadar
Grumpensis
(continued on next page)
10
Table 2 (continued)
Diversity Common
serovars
Serovar
(percentage
number/ of total
total
isolates)
isolates
44/316h
a
b
c
d
e
f
g
h
Enteriditis
Virchow
Hadar
Infantis
Typhimurium
Goldcoast
Ohio
Others serovars
Country
Reference
Spain
Polo et al.
(1999)
Also isolated from human and/or animal feces.

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

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

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

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

10.7% (214)
104106 CFU/100 mLb
50% (4)
23.6%
Drinking water supply
13.3%d
Surface waterc
14% (300)
Tap water of urban water

supply system
Borehole standpipes water
and surface waterc
Well and tap waterg
Australia Ahmed et al.

(2010)
India
Jyoti et al.
(2010)
Nigeria
Oguntoke et
al. (2009)
Nigeria
Oluyege et al.
(2009)
Nepal
Bhatta et al.
(2007)
South
Momba et al.
Africa
(2006)
Nigeria
Akinyemi et al.
(2006)
South
Potgieter et al.
Africa
(2005)
100%(8)e
16% (18)f
100%
Roof harvested rainwatera
Well and borehole waterc
Borehole standpipes water

and surface waterc
Reference
gc: gene copies.

a
35% for indoor use including drinking, showering and kitchen use.
b
Presumptive Salmonella identication.
c
Used untreated for drinking purpose.
d
Percentage of the Gram negative isolates from water samples.
e
Determined by qPCR but reported as CFU/100 mL.
f
% of positive sampling sites.
g
Salmonella was only detected in well water.
11
human host-specic strains Typhi and Paratyphi A, indicating the

impact of human source contamination on the overall Salmonella input
in the analyzed water source. Furthermore, they highlighted the
common occurrence of MDR Salmonella strains which increased the
risk connected to the use of these water supply systems. The literature
demonstrate that a lack of hygienic conditions, non-appropriate water
supply structures, and improper disinfection were consistently identied as the main cause of water contamination in developing countries
(Akinyemi et al., 2006; Bhatta et al., 2007; Momba et al., 2006; Oluyege
et al., 2009).
Groundwater is becoming increasingly relied upon as a major
source of water and the security of water quality for groundwater in
developing nations is a major issue. Contamination of groundwater by
microbial pathogens has been documented also in developed
countries due to failures in well head protection, inadequate off-set
and diffuse contamination sources (Bockelmann et al., 2009;
Borchardt, Haas, & Hunt, 2004; Goss & Richards, 2008). Groundwater
can be contaminated by a wide range of pathogens, but like for most
water sources, enteric pathogens remain the greatest risk. Despite the
common assumptions that all enteric pathogens are a contamination
risk for groundwater (e.g. John & Rose, 2005) the majority of studies of
pathogens in groundwater has focused on the presence of indicator
microorganisms (e.g. Emmanuel, Pierre, & Perrodin, 2009; Wall, Pang,
Sinton, & Close, 2008), risks posed by enteric viruses (e.g. Borchardt
et al., 2004; Locas, Barthe, Margolin, & Payment, 2008), or protozoa
(e.g. Boyer, Kuczynska, & Fayer, 2009). In contrast, the information on
the presence of Salmonella spp. in groundwater is limited. In one of the
few studies reported on Salmonella in groundwater, Li et al. (2009)
determined that the consumption of groundwater was an independent risk factor for a number of conrmed cases of Salmonella
choleraesuis in Taiwan. In another study of groundwater quality in
Turkey, Ozler and Aydin (2008) detected Salmonella in 15% of the
groundwater samples tested.
There is also information about Salmonella detection and behavior
in groundwater from a study where recycled water has been
intentionally recharged to aquifers during Managed Aquifer Recharge
(MAR). Levantesi et al. (2010) were able to occasionally detect
Salmonella in two aquifers used as MAR sites receiving recycled water,
however, they detected Salmonella much less frequently than other
pathogens such as Cryptosporidium and Giardia.
In Australia, where the issue of water scarcity has resulted in the
promotion of the use of roof harvested rain water for drinking or other
purposes, several studies have been undertaken investigating the
microbiological quality of the collected rain waters. Ahmed, Huygens,
Goonetilleke and Gardner (2008) and Ahmed, Vieritz, Goonetillek and
Gardner (2010) detected Salmonella in tanks collecting roof harvested
rain water for indoor and outdoor use and indicated wild birds or
animal feces as likely source of contaminations. A risk assessment
study using these results indicated that there was a risk of infection
for Salmonella ingestion that exceeded the threshold value of 1 extra
infection for 10,000 persons a year suggesting that roof harvested
rainwater should be disinfected if used for potable water purposes
(Ahmed et al., 2010). Another study also linked roof harvested rain
water with Salmonella water-borne infection in Australia (Ashbolt &
Kirk, 2006; Franklin et al., 2009) further highlighting the risks from
Salmonella in roof harvested rain water.
5. Salmonella survival and monitoring in water environment

5.1. Salmonella survival
The majority of research on Salmonella survival in aquatic
environment has been done in the last decades of the 20th century.
Overall, these older studies investigated the physicochemical and
biological factors inuencing Salmonella survival in various water
12
environments and compared the survival capacity of different enteric

bacteria (e.g. Salmonella and E. coli).
In the last ten years this topic has been less frequently addressed.
Chandran and Hatha (2005) described a microcosm study that
investigated the relative survival of E. coli and Salmonella Typhimurium
in estuary waters focusing on the effect of biological factors, dissolved
organic and inorganic substances, and sunlight on the inactivation of
these bacteria. The results showed that sunlight was the most important
factor for inactivation, followed by biotic factors. The biotic factors were
determined to comprise of a combination of predation by protozoa and
bacteria, bacteriophage lysis, and competition with autochthonous
microbes. They also found that dissolved organic substances present in
the estuarine water, in the absence of the native biota, promoted
survival and growth of these enteric bacteria. In contrast to what has
been previously described in other studies (Mezrioui, Baleux, &
Trousselier, 1995; Rhodes & Karton, 1988; Wineld & Groisman,
2003), E. coli cells showed a better survival capacity when compared
to S. Typhimurium under all tested conditions. In another microcosm
study by the same research group, an enhanced survival capacity of
Salmonella in lake sediment with respect to the overlaying water was
observed (Chandran et al., 2011). According to these results, the lake
sediment offered some sort of protection for this enteric pathogen and,
thus, potentially act as a reservoir of Salmonella.
The effect of sunlight on the persistence of S. enterica, E. coli and
Campylobacter jejuni in river and seawater was also investigated by
Sinton, Hall, and Braithwaite (2007). They showed that inactivation
rates in sunlight were clearly higher than in the dark and that the
extent of inactivation was directly related to the amount of insolation.
Furthermore, in agreement to Chandran and Hatha (2005) they
showed that S. enterica was inactivated up to 1.6 times faster than E.
coli.
Pathogens have been documented to decay when introduced into
aquifers and this information can be used for Managed Aquifer
Recharge sites (Gordon & Toze, 2003; Toze, 2004). As with the
detection of pathogens in groundwater, most information available
focuses on the survival of enteric viruses (Nasser, Glozman, & Nitzan,
2002; Toze, Hanna, Smith, Edmonds, & McCrow, 2004) and there is
limited information specically on the survival of Salmonella. Despite
this, inactivation of Salmonella in groundwater has been noted in one
study of pathogen decay at a Managed Aquifer Recharge site. Toze,
Bekele, Page, Sidhu, and Shackleton (2010) observed that Salmonella
had a 1 log reduction time in groundwater of 1 day. This is similar to
decay times observed in groundwater for other bacteria such as
coliforms (Gordon & Toze, 2003) but less than observed for enteric
viruses or protozoa (Toze et al., 2010).
Recent studies indicate that secondary habitat may provide the
required conditions to promote survival and replication of enteric
microorganisms including Salmonella. In particular, Ishii et al. (2006)
and Byappanahalli et al. (2009) showed that the lamentous green
alga Chladophora in Michigan lake, could arbor salmonellae at much
higher concentrations compared to the numbers in the surrounding
water. According to these observations and to previous results
showing that this alga can support the growth of enteric bacteria by
providing nutrients in the algal excretions (Byappanahalli, Shively,
Nevers, Sadowsky, & Whitman, 2003), Byappanahalli et al. (2009)
hypothesize that Salmonella is likely to multiply on Chladophora in the
water column.
Salmonella in aquatic environment remains a matter of debate in

recent papers (Ahmed et al., 2009; Savichtcheva et al., 2007;
Schriewer et al., 2010; Wilkes et al., 2009). Despite this, in a
comprehensive study describing the occurrence of enteric pathogens
in a Canadian watershed and their relationships with environmental
parameters and FIB, Wilkes et al. (2009) showed that a good
prediction of Salmonella presence can be obtained by FIB determination. In particular, they indicated that E. coli and fecal coliforms were
the most appropriate indicators of Salmonella presence compared to
Clostridium perfringens, enterococci and total coliforms. The identied
E. coli threshold level that gave the greater probability of pathogen
detection was NE. coli 89 CFU/100 mL. This E. coli threshold was
determined to correlate with the identication of 89% of Salmonella
positive samples. Schriewer et al. (2010) also observed that at a
specic threshold level fecal coliforms as well as enterococci and total
coliforms were good predictors of Salmonella presence in Californian
rivers with sea intrusion. They also found, however, that these
microbial indicators did not efciently predict Salmonella in rivers that
were not inuenced by sea intrusion. In contrast with these results, no
correlation were observed between FIB and Salmonella presence/absence in ponds and creeks in the Brisbane city area in Australia
(Ahmed et al., 2009), or in the Small River basin in Georgia, USA
(Meinersmann et al., 2008).
Another potential indicator are the Bacteroidales. Bacteroidales are
fecal anaerobes that are present in feces in much higher densities than
conventional FIB and have different host specicities (Field &
Samadpour, 2007). Feces from different sources such as human,
horse, pigs, dogs, and ruminant can be identied by Bacteroidales host
specic PCR primers which can allow source tracking of fecal
contamination. Favorable results were obtained using this
method in comparison to other source tracking approaches (Grifth,
Weisburg, & McGee, 2003). Furthermore, due to their host specic
distribution, these markers might predict the presence of certain
pathogens associated to specic source of pollution.
The relationship between Bacteroides 16S rRNA genetic markers
and Salmonella in aquatic environment has been addressed in a few
papers (Savichtcheva et al., 2007; Schriewer et al., 2010; Walters et al.,
2007). According to Savichtcheva et al. (2007), human and total
Bacteroides 16S rRNA genetic markers in wastewater and river
samples were positively correlated with the presence of Salmonella
and showed a good predictive value for the presence of this pathogen.
They found that the probability of its occurrence became signicantly
high (N7080%) when the concentration of human Bacteroides genetic
markers exceeded 10 6 copies/100 mL. No correlations were found
with cow and pig Bacteroides 16S rRNA genetic markers in the same
study. Differently from the results from Savichtcheva et al. (2007),
two recent studies analyzing river and estuarine water environments
showed no predictive value for various Bacteroidales host specic
markers in association with Salmonella detection (Schriewer et al.,
2010; Walters et al., 2007). Nevertheless, Walters and colleagues
showed that ruminant specic Bacteroidales markers were more
frequently detected in Salmonella positive samples (36%) compared to
human specic markers (2.6%) (Walters et al., 2007). They concluded
that agricultural runoff were a major contribution to the Salmonella
contamination in the analyzed watershed while contamination from
human sources was only a minor contribution.
6. Conclusions
5.2. Conventional and alternative microbial indicators for Salmonella

monitoring in aquatic environment
The limits and advantages of conventional and alternative indicators of fecal contamination for pathogen monitoring in aquatic
environment have been recently extensively reviewed (Field &
Samadpour, 2007; Savichtcheva & Okabe, 2006). The efciency of
fecal indicator bacteria (FIB) to predict the presence/absence of
This review on the occurrence and risk of Salmonella in water has

demonstrated that Salmonella can be present in a variety of aquatic
environments and that contamination can come from a range of
sources. Salmonella has been detected in sources as diverse as rivers,
lakes, pond, groundwater and drinking water, while sources of the
bacterium have been like to sources that include inputs from human,
domestic animals and wild life.
Extensive surveys of Salmonella spp. occurrence in surface

waters in industrialized countries conrmed the ubiquitous nature
of this enteric pathogen. Moreover, the positive correlations
between Salmonella frequencies and rainfall events observed in
many of the studies indicated that surface runoff plays a main role
as driver of Salmonella load in aquatic environments. Analysis of
isolated serovars consistently showed a mixed human and animal
origin of Salmonella in surface water environments. This emphasizing the role of wild life animals in water contamination along
with the more accepted livestock and human sources. Overall, a
great complexity was observed in the structure of Salmonella
populations in surface water environments. Studies revealed large
serovars diversity, both in water and in likely sources of contamination as well as spatial and temporal variation in the detection of
Salmonella types and frequencies.
In spite of the recognized potential of microbial source tracking,
these methods have not been extensively used to investigate the
sources of Salmonella contamination in the surface water environments. Nevertheless, the results obtained to-date suggest that
microbial source tracking by genotyping methods in these environments may be possible and may be extremely useful to identify
related strains in complex environmental Salmonella populations and
to highlight specic transmission routes.
Salmonella serovars of human health concern were shown to be
widespread in natural fresh waters although more rare environmental
serovars were also frequently detected. At present little is known
about the pathogenicity of these rarer serovars isolated from the
environment and further research is required to understand the role
of these serovars in water-borne disease dissemination. Regardless,
human infections have been reported for most of the serovars
detected in surface water including those usually associated with
wild animals. A number of studies in developed countries detected
clinically relevant Salmonella serovars in water utilized for indoor
uses, irrigation and recreational uses, and of further concern, also
detected MDR Salmonella strains in natural freshwaters. Overall, these
results proposed that there was the likelihood of surface watermediated Salmonella infections. This conclusion, however, is not
supported by epidemiological water-borne outbreaks data showing
rare involvement of surface waters, both as drinking water sources
and for recreational use, in Salmonella outbreaks. Nevertheless,
exposure to recreational water was indicated as the most important
risk factor for childhood Salmonella infections indicating that different
transmission routes may be implicated in the transmission of sporadic
and epidemic diseases.
Salmonella was not one of the leading causes of reported waterborne outbreaks in developed countries, being usually reported less
frequently than other pathogens as agent of water mediated
epidemics (e.g. Cryptosporidium, Giardia, E. coli 0157:H7; norovirus,
Shigella, and Campylobacter). Detected Salmonella outbreaks were
mostly linked to contaminated drinking waters. Different types of
drinking water (municipal water system, well, tank water) were
indicated as sources of outbreaks, however, all the outbreaks were
consistently associated with the use of untreated or inadequately
treated water. Studies have shown that Salmonella is efciently
removed by conventional disinfection procedures utilized in water
treatment processes and thus is of little risk in adequately treated
water sources. Despite this, the true incidence of Salmonella waterborne diseases might be greater than is reected in the reported
outbreaks statistics as not all water-borne disease outbreaks are
recognized or reported, especially in countries with a low level of
water-borne outbreaks surveillance. In addition, Salmonella contaminated waters used to irrigate and wash produce crops have been
implicated in a large number of food-borne outbreaks demonstrating
that additional indirect routes of transmissions should be considered
to correctly evaluate the role of water in Salmonella diseases
dissemination.
13
The data on water-borne outbreaks in developing countries are

not complete as national outbreaks surveillance systems are usually
limited and in spite of the likely large number of studies performed
in the eld, the data produced have rarely been published. The data
available in the scientic literature related to water-borne transmission of Salmonella in developing countries are mainly case
control studies that have analyzed the risk for endemic typhoid
Salmonella. The scientic data, overall, conrms that water is a
common source for the transmission of this disease, but also
highlight that other risk factors are associated with typhoid fever
indicating multiple routes of transmission. Reports of massive
water-borne Salmonella outbreaks as well as epidemiological
studies on endemic typhoid and paratyphoid fevers underlined
the relevance of MDR Salmonella strains in these countries. The risk
of MDR strains dissemination is further exacerbated in less
industrialized countries through the customs of inappropriate use
and self-prescribing antibiotics.
The efciency of conventional and alternative microbial indicators
of fecal contamination to monitor Salmonella in water environments is
still a matter requiring further study due to the need for rapid, specic
and reliable methods that can be used for the control of environmental water quality. Most of the studies that looked for a link between
indicators and Salmonella found inconsistent results on the relationship between the occurrence of FIB and Salmonella. Additionally, no
signicant improvements were achieved by applying alternative
indicators to the Salmonella presence in surface waters. Bacteroidales
were found to perform equally or slightly better than FIB in a direct
comparison of their capacity to predict Salmonella presence. However
the relationship between Bacteroidales and Salmonella were found to
not be constant in surface water as inconsistent results were obtained
in different studies.
This review has shown that there are still limitations on the
understanding of Salmonella in water and their potential sources.
Salmonella remain a signicant health risk in developing nations and
improved understanding of the role of water in the dissemination of
Salmonella in these countries and on how to manage the risks. Of
particular concern is the rise in the presence of multi-drug resistance
in Salmonella and the causes of this drug resistance.
References
Abdel-Monem, M. H. A. A., & Dowidar, A. (1990). Recoveries of Salmonella from soil in
eastern region of Saudi Arabia Kingdom. The Journal of the Egyptian Public Health
Association, 65, 6175.
Ahmed, W., Huygens, F., Goonetilleke, A., & Gardner, T. (2008). Real-time PCR
detection of pathogenic microorganisms in roof-harvested rainwater in
Southeast Queensland, Australia. Applied and Environmental Microbiology, 74,
54905496.
Ahmed, W., Sawant, S., Huygens, F., Goonetilleke, A., & Gardner, T. (2009). Prevalence
and occurrence of zoonotic bacterial pathogens in surface waters determined by
quantitative PCR. Water Research, 43, 49184928.
Ahmed, W., Vieritz, A., Goonetillek, A., & Gardner, T. (2010). Health risk from the use
of roof-harvested rainwater in southeast Queensland, Australia, as potable and
non-potable water, determined using Quantitative Microbial Risk Assessment.
Applied and Environmental Microbiology, 76, 73827391.
Akinyemi, K. O., Oyefolu, A. O. B., Salu, O. B., Adewale, O. A., & Fasure, A. K. (2006).
Bacterial pathogens associated with tap and well waters in Lagos, Nigeria. East
and Central African Journal of Surgery, 11(1), 110117.
Angulo, F. J., Tippen, S., Sharp, D. J., Payne, B. J., Collier, C., Hill, J. E., et al. (1997). A
community water-borne outbreak of salmonellosis and the effectiveness of a boil
water order. American Journal of Public Health, 87(4), 580584.
Arnold, B. F., & Colford, J. M. (2007). Treating water with chlorine at point-of-use to
improve water quality and reduce child diarrhea in developing countries: A
systematic review and meta-analysis. The American Journal of Tropical Medicine
and Hygiene, 76, 354364.
Asano, T., Burton, F. L., Leverenz, H. L., Tsuchihashi, R., & Tchobanoglous, G. (2007).
Water reuse Issues, technologies and applications (1st edn.). New York, USA:
McGraw-Hill.
Ashbolt, N. J. (2004). Microbial contamination of drinking water and disease outcomes
in developing regions. Toxicology, 198, 229238.
Ashbolt, R., & Kirk, M. D. (2006). Salmonella Mississippi infections in Tasmania: The role
of native Australian animals and untreated drinking water. Epidemiology and
Infection, 134, 12571265.
14
Baudart, J., Grabulos, J., Barrusseau, J. P., & Lebaron, P. (2000). Salmonella spp. and fecal
coliform load in coastal waters from a point vs. nonpoint source of pollution. Journal
of Environmental Quality, 29, 241250.
Baudart, J., Lemarchand, K., Brisabois, A., & Lebaron, P. (2000). Diversity of Salmonella
strains isolated from the aquatic environment as determined by serotyping and
amplication of the ribosomal DNA spacer regions. Applied and Environmental
Microbiology, 66, 15441552.
Berg, R. (2008). The Alamosa Salmonella outbreak: A gumshoe investigation. Journal of
Environmental Health, 71(2), 5458.
Berger, C. N., Sodha, S. V., Shaw, R. K., Grifn, P. M., Pink, D., Hand, P., et al. (2010). Fresh
fruit and vegetables as vehicles for the transmission of human pathogens.
Environmental Microbiology, 12(9), 23852397.
Bessong, P. O., Odiyo, J. O., Musekene, J. N., & Tessema, A. (2009). Spatial distribution of
diarrhoea and microbial quality of domestic water during an outbreak of diarrhoea
in the Tshikuwi community in Venda, South Africa. Journal of Health, Population and
Nutrition, 27(5), 652659.
Bhatta, D. R., Bangtrakulnonth, A., Tishyadhigama, T., Saroj, S. D., Bandekar, J. R.,
Hendriksen, R. S., et al. (2007). Serotyping, PCR, phage-typing and antibiotic
sensitivity testing of Salmonella serovars isolated from urban drinking water supply
systems of Nepal. Letters in Applied Microbiology, 44, 588594.
Bhunia, R., Hutin, Y., Ramakrishnan, R., Pal, N., Sen, T., & Murhekar, M. (2009). A typhoid
fever outbreak in a slum of South Dumdum municipality, West Bengal, India, 2007:
Evidence for foodborne and water-borne transmission. BMC Public Health, 9, 115,
doi:10.1186/1471-2458-9-115471-2458-9-115.
Black, R. E., Cisneros, L., Levine, M. M., Ban, A., Lobos, H., & Rodriguez, H. (1985). Case
control study to identify risk factors for paediatric endemic typhoid fever in
Santiago, Chile. Bulletin of the World Health Organization, 63, 899904.
Blackburn, B. G., Craun, G. F., Yoder, J. S., Hill, V., Calderon, R. L., Chen, N., et al. (2004).
Surveillance for water-borne disease outbreaks associated with drinking water
United States, 20012002. MMWR Morbidity and Mortality Weekly Report, 53,
2345.
Blasi, M. F., Carere, M., Pompa, M. G., Rizzuto, E., & Funari, E. (2008). Water related
diseases outbreaks reported in Italy. Journal of Water and Health, 423432.
Bockelmann, U., Dorries, H. H., Ayuso-Gabella, M. N., de Marcay, M. S., Tandoi, V.,
Levantesi, C., et al. (2009). Quantitative PCR monitoring of antibiotic resistance
genes and bacterial pathogens in three European articial groundwater recharge
systems. Applied and Environmental Microbiology, 75, 154163.
Bonadonna, L., Briancesco, R., Donia, D., Ottaviani, M., Veschetti, E., & Divizia, M. (2003).
Aspetti igienico-sanitari delle acque del ume Tevere: presenza di protozoi
patogeni e rapporti di correlazione con parametri microbiologici e chimico-sici.
Annali di Igiene: Medicina Preventiva e di Comunit, 16, 273280.
Bonadonna, L., Filetici, E., Nusca, A., & Paradiso, R. (2006). Controlli ambientali sulla
diffusione di sierotipi di Salmonella spp in acque uviali. Microbiologia Medica, 21
(4), 311315.
Borchardt, M. A., Haas, N. L., & Hunt, R. J. (2004). Vulnerability of drinking-water wells
in La Crosse, Wisconsin, to enteric-virus contamination from surface water
contributions. Applied and Environmental Microbiology, 70, 59375946.
Boyer, D. G., Kuczynska, E., & Fayer, R. (2009). Transport, fate, and infectivity of
Cryptosporidium parvum oocysts released from manure and leached through
macroporous soil. Environmental Geology, 58, 10111019.
Butler, T., Mahmoud, A. A. F., & Warren, K. S. (1977). Algorithms in the diagnosis and
management of exotic diseases. XIII Typhoid fever. The Journal of Infectious Diseases,
135, 10171020.
Byappanahalli, M. N., Sawdey, R., Ishii, S., Shively, D. A., Ferguson, J. A., Whitman, R. L.,
et al. (2009). Seasonal stability of Cladophora-associated Salmonella in Lake
Michigan watersheds. Water Research, 43, 806814.
Byappanahalli, M. N., Shively, D. A., Nevers, M. B., Sadowsky, M. J., & Whitman, R. L.
(2003). Growth and survival of Escherichia coli and enterococci populations in
the macro-alga Cladophora (Chlorophyta). FEMS Microbiology Ecology, 46(2),
203211.
Castillo, A., Mercado, I., Lucia, L. M., Martnez-Ruiz, Y., Ponce de Len, J., Murano, E. A.,
et al. (2004). Salmonella contamination during production of cantaloupe: A
binational study. Journal of Food Protection, 67(4), 713720.
Centers for Disease Control and Prevention (2002). Multistate outbreaks of Salmonella
serotype Poona infections associated with eating cantaloupe from Mexico United
States and Canada, 20002002. MMWR. Morbidity and Mortality Weeekly Repor, 51
(46), 10441047.
Centers for Disease Control and Prevention (2008). Outbreak of Salmonella serotype
Saintpaul infections associated with multiple raw produce items United States,
2008. MMWR. Morbidity and Mortality Weeekly Report, 57(34), 929934.
Chandran, A., & Hatha, A. A. M. (2005). Relative survival of Escherichia coli and
Salmonella Typhimurium in a tropical estuary. Water Research, 39, 13971403.
Chandran, A., Varghese, S., Kandeler, E., Thomas, A., Hatha, M., & Mazumder, A.
(2011). An assessment of potential public health risk associated with the
extended survival of indicator and pathogenic bacteria in freshwater lake
sediments. International Journal of Hygiene and Environmental Health, doi:
10.1016/j.ijheh.2011.01.002 Accepted.
Cicmanec, J. L., Smith, J. E., & Carr, R. (2004). Control of zoonotic diseases in
drinking-water. In J. A. Cotruvo, A. Dufour, G. Rees, J. Bartram, R. Carr, D. O.
Cliver, G. F. Craun, R. Fayer, & V. P. J. Gannon (Eds.), Water-borne zoonoses
identication, causes, and control (pp. 426436). London: IWA Publishing, World
Health Organization.
Clasen, T., Schmidt, W. P., Rabie, T., Roberts, I., & Cairncross, S. (2007). Interventions to
improve water quality for preventing diarrhoea: Systematic review and metaanalysis. British Medical Journal, 334(7597), 782, doi:10.1136/bmj.39118.489931.BE
BMJ.
Craun, G. F., Brunkard, J. M., Yoder, J. S., Roberts, V. A., Carpenter, J., Wade, T., et al.
(2010). Causes of outbreaks associated with drinking water in the United States
from 19712006. Clinical Microbiology Reviews, 23(3), 507528.
Craun, G. F., Calderon, R. L., & Craun, M. F. (2004). Water-borne outbreaks caused by
zoonotic pathogens in the USA. In J. A. Cotruvo, A. Dufour, G. Rees, J. Bartram, R.
Carr, D. O. Cliver, G. F. Craun, R. Fayer, & V. P. J. Gannon (Eds.), Water-borne zoonoses
identication, causes, and control (pp. 120135). London: IWA Publishing, World
Health Organization.
Craun, G. F., Calderon, R. L., & Craun, M. F. (2005). Outbreaks associated with
recreational water in the United States. International Journal of Environmental
Health Research, 15(4), 243262.
Crump, J. A., Luby, S. P., & Mintz, E. D. (2004). The global burden of typhoid fever.
Bulletin of the World Health Organization, 82(5), 346352.
Dale, K., Kirk, M., Sinclair, M., Hall, R., & Leder, K. (2007). Reported outbreaks of
gastrointestinal disease in Australia are predominantly associated with
recreational exposure. Australian and New Zealand Journal of Public Health, 10
(34), 527530.
Deering, A. J., Pruitt, R. E., Mauer, L. J., & Reuhs, B. L. (2011). Examination of the
internalization of Salmonella serovar Typhimurium in peanut, Arachis Hypogaea,
using immunocytochemical techniques. Food Research International, doi:
10.1016/j.foodres.2011.01.061.
Denno, D. M., William, E., Keene, C. M., Hutter, J. K., Koepsell, M., Patnode, D., et al.
(2009). Tri-county comprehensive assessment of risk factors for sporadic
reportable bacterial enteric infection in children. The Journal of Infectious
Diseases, 199, 467476.
DeRoeck, D., Jodar, L., & Clements, J. (2007). Putting typhoid vaccination on the
global health agenda. The New England Journal of Medicine, 357(11), 10691071.
Dickens, D. L., DuPont, H. L., & Johnson, P. C. (1985). Survival of bacterial
enteropathogens in the ice of popular drinks. Journal of the American Medical
Association, 253, 31413143.
Dolejsk, M., Bierosov, B., Kohoutov, L., Literk, I., & Czek, A. (2009). Antibioticresistant Salmonella and Escherichia coli isolates with integrons and extendedspectrum beta-lactamases in surface water and sympatric black-headed gulls.
Journal of Applied Microbiology, 106(6), 19411950.
Duffy, E. A., Lucia, L. M., Kells, J. M., Castillo, A., Pillai, S. D., & Acuff, G. R. (2005).
Concentrations of Escherichia coli and genetic diversity and antibiotic resistance
proling of Salmonella isolated from irrigation water, packing shed equipment,
and fresh produce in Texas. Journal of Food Protection, 68(1), 7079.
Emmanuel, E., Pierre, M. G., & Perrodin, Y. (2009). Groundwater contamination by
microbiological and chemical substances released from hospital wastewater:
Health risk assessment for drinking water consumers. Environment International, 35, 718726.
U.S. Environmental Protection Agency (2006). National primary drinking water
regulations: Ground water rule; Final rule. 40 CFR parts 9, 141 and 142 Fed. Regist.
71, 6557465660. .
Espinoza-Medina, I. E., Rodrguez-Leyva, F. J., Vargas-Arispuro, I., Islas-Osuna, M. A.,
Acedo-Flix, E., & Martnez-Tllez, M. A. (2006). PCR identication of
Salmonella: Potential contamination sources from production and postharvest
handling of cantaloupes. Journal of Food Protection, 69(6), 14221425.
Farooqui, A., Khan, A., & Kazmi, S. U. (2009). Investigation of a community outbreak
of typhoid fever associated with drinking water. BMC Public Health, 9(476), doi:
10.1186/1471-2458-9-476.
Fewtrell, L., Kaufmann, R. B., Kay, D., Enanoria, W., Haller, L., & Colford, J. M., Jr.
(2005). Water, sanitation, and hygiene interventions to reduce diarrhoea in less
developed countries: a systematic review and meta-analysis. The Lancet
Infectious Diseases, 5, 4252.
Field, K. G., & Samadpour, M. (2007). Fecal source tracking, the indicator paradigm,
and managing water quality. Water Research, 41, 35173538.
Franklin, L. J., Fielding, J. E., Gregory, J., Gullan, L., Lightfoot, D., Poznanski, S. Y., et al.
(2009). An outbreak of Salmonella Typhimurium 9 at a school camp linked to
contamination of rainwater tanks. Epidemiology and Infection, 137(3), 434440.
Gaertner, J. P., Hahn, D., Rose, F. L., & Forstner, M. R. J. (2008). Detection of
salmonellae in different turtle species within the headwater spring ecosystem.
Journal of Wildlife Diseases, 44, 519526.
Gagliardi, J. V., Millner, P. D., Lester, G., & Ingram, D. (2003). On-farm and
postharvest processing sources of bacterial contamination to melon rinds.
Journal of Food Protection, 66, 8287.
Gandhi, M., Golding, S., Yaron, S., & Matthews, K. R. (2001). Use of green uorescent
protein expressing Salmonella Stanley to investigate survival, spatial location,
and control on alfalfa sprouts. Journal of Food Protection, 64, 18911898.
Gannon, V. P., Graham, T. A., Read, S., Ziebell, K., Muckle, A., Mori, J., et al. (2004).
Bacterial pathogens in rural water supplies in Southern Alberta, Canada. Journal
of Toxicology and Environmental Health, 67(2022), 16431653.
Gasem, M. H., Dolmans, W. M., Keuter, M. M., & Djokomoeljanto, R. R. (2001). Poor
food hygiene and housing as risk factors for typhoid fever in Semarang,
Indonesia. Tropical Medicine & International Health, 6, 484490.
Gordon, M. A. (2008). Salmonella infections in immunocompromised adults. The
Journal of Infection, 56, 413422.
Gordon, M. A., & Graham, S. M. (2008). Invasive salmonellosis in Malawi. The Journal
of Infection in Developing Countries, 2(6), 438442.
Gordon, C., & Toze, S. (2003). Inuence of groundwater characteristics on the
survival of enteric viruses. Journal of Applied Microbiology, 95, 536544.
Gorski, L., Parker, C. T., Liang, A., Cooley, M. B., Jay-Russell, M. T., Gordus, A. G., et al.
(2011). Prevalence, distribution and diversity of Salmonella enterica in a major
produce region of California. Applied and Environmental Microbiology, doi:
10.1128/AEM.02321-10.

Goss, M., & Richards, C. (2008). Development of a risk-based index for source water
protection planning, which supports the reduction of pathogens from
agricultural activity entering water resources. Journal of Environmental Management, 87, 623632.
Graham, S. M. (2002). Salmonellosis in children in developing and developed
countries and populations. Current Opinion in Infectious Diseases, 15, 507512.
Greene, S. K., Daly, E. R., Talbot, E. A., Demma, L. J., Holzbauer, S., Patel, N. J., et al.
(2008). Recurrent multistate outbreak of Salmonella Newport associated with
tomatoes from contaminated elds, 2005. Epidemiology and Infection, 136(2),
157165.
Grifth, J. F., Weisburg, S. B., & McGee, C. D. (2003). Evaluation of microbial source
tracking methods using mixed fecal sources in aqueous test samples. Journal of
Water and Health, 1, 141152.
Guo, X., van Iersel, M. W., Chenn, J., Brackett, R. E., & Beuchat, L. R. (2002). Evidence
of association of salmonellae with tomato plants grown hydroponically in
inoculated nutrient solution. Applied and Environmental Microbiology, 68,
36393643.
Haddock, R. L., & Malilay, J. (1986). The possible role of rainfall in spreading Salmonella
on Guam. Journal of Diarrhoeal Diseases Research, 4(4), 229232.
Haley, B. J., Cole, D. J., & Lipp, E. K. (2009). Distribution, diversity and seasonality of
water-borne Salmonella in a rural watershed. Applied and Environmental Microbiology, 75, 12481255.
Hanning, I. B., Nutt, J. D., & Ricke, S. C. (2009). Salmonellosis outbreaks in the United
States due to fresh produce: Sources and potential intervention measures.
Foodborne Pathogens and Disease, 6(6), 635648.
Heaton, J. C., & Jones, K. (2007). Microbial contamination of fruit and vegetables and the
behavior of enteropathogens in the phyllosphere: A review. Journal of Applied
Microbiology, 104(3), 613626.
Hunter, P. R. (2003). Principles and components of surveillance systems. In P. R. Hunter,
M. Waite, & E. Ronchi (Eds.), Drinking water and infectious disease: Establishing the
links. Boca Raton, FL: CRC Press.
Ishii, S., Yan, T., Shively, D. A., Byappanahalli, M. N., Whitman, R. L., & Sadowsky, M. J.
(2006). Cladophora (Chlorophyta) spp. harbour human bacterial pathogens in near
shore water of Lake Michigan. Applied and Environmental Microbiology, 72,
45454553.
Islam, M., Morgan, J., Doyle, M. P., Phatak, S. C., Millner, P., & Jiang, X. (2004). Fate of
Salmonella enterica serovar Typhimurium on carrots and radishes grown in
elds treated with contaminated manure composts or irrigation water. Applied
and Environmental Microbiology, 70, 24972502.
John, D. E., & Rose, J. B. (2005). Review of factors affecting microbial survival in
groundwater. Environmental Science & Technology, 39, 73457356.
Jokinen, C., Edge, T. A., Ho, S., Koning, W., Laing, C., Mauro, W., et al. (2011).
Molecular subtypes of Campylobacter spp., Salmonella enterica, and Escherichia
coli O157:H7 isolated from fecal and surface water samples in the Oldman River
watershed, Alberta, Canada. Water Research, 45, 12471257.
Jokinen, C. C., Schreier, H., Mauro, W., Taboada, E., Isaac-Renton, J. L., Topp, E., et al.
(2010). The occurrence and sources of Campylobacter spp., Salmonella enterica
and Escherichia coli O157:H7 in the Salmon River, British Columbia, Canada.
Journal of Water and Health, 8, 374386.
Jones, K., & Bradshaw, S. B. (1996). Biolm formation by the enterobacteriaceae: A
comparison between Salmonella enteritidis, Escherichia coli and a nitrogen-xing
strain of Klebsiella pneumoniae. The Journal of Applied Bacteriology, 80(4),
458464.
Jyoti, A., Ram, S., Vajpayee, P., Singh, G., Dwivedi, P. D., Jain, S. K., et al. (2010).
Contamination of surface and potable water in South Asia by salmonellae:
Culture-independent quantication with molecular beacon real-time PCR. The
Science of the Total Environment, 408(6), 12561263.
Kariuki, S., Revathi, G., Kariuki, N., Kiiru, J., Mwituria, J., Muyodi, J., et al. (2006).
Invasive multidrug-resistant non-typhoidal Salmonella infections in Africa:
Zoonotic or anthroponotic transmission? Journal of Medical Microbiology, 55,
585591.
Kelly-Hope, L. A., Alonso, W. J., Thiem, V. D., Anh, D. D., Canh, D. G., Lee, H., et al.
(2007). Geographical distribution and risk factors associated with enteric
diseases in Vietnam. The American Journal of Tropical Medicine and Hygiene, 76,
706712.
Kim, S. (2010). Salmonella serovars from foodborne and water-borne diseases in Korea,
19982007: Total isolates decreasing versus rare serovars emerging. Journal of
Korean Medical Science, 25, 16931699.
Kim, S., Lim, O. Y., Kim, S. H., Kim, J. Y., Kang, Y. H., & Lee, B. K. (2003). Pulsed-eld gel
electrophoresis and mutation typing of gyrA gene of quinolone-resistant
Salmonella enterica serovar Paratyphi A isolated from outbreak and sporadic
cases, 19982002, Korea. Journal of Microbiology and Biotechnology, 13, 155158.
Kindhauser, M. K. (2003). Communicable diseases 2002: Global defence against the
infectious disease threat. Geneva: World Health Organization.
Klerks, M. M., Franz, E., van Gent-Pelzer, M., Zijlstra, C., & van Bruggen, A. H. (2007).
Differential interaction of Salmonella enterica serovars with lettuce cultivars and
plantmicrobe factors inuencing the colonization efciency. The ISME Journal, 1,
620631.
Kozlica, J., Claudet, A. L., Solomon, D., Dunn, J. R., & Carpenter, L. R. (2010). Waterborne outbreak of Salmonella I 4,[5],12:i:. Foodborne Pathogens and Disease, 7
(11), 14311433.
Lapidot, A., & Yaron, S. (2009). Transfer of Salmonella enterica serovar Typhimurium
from contaminated irrigation water to parsley is dependent on curli and cellulose,
the biolm matrix components. Journal of Food Protection, 72(3), 618623.
Leclerc, H., Schwartzbrod, L., & Dei-Cas, E. (2002). Microbial agents associated with
water-borne diseases. Critical Reviews in Microbiology, 28(4), 371409.
15
Lemarchand, K., & Lebaron, P. (2003). Occurrence of Salmonella spp. and Cryptosporidium spp. in a French coastal watershed: Relationship with faecal indicators. FEMS
Microbiology Letters, 218(1), 203209.
Levantesi, C., La Mantia, R., Masciopinto, C., Bckelmann, U., Ayuso-Gabella, M. N.,
Salgot, M., et al. (2010). Quantication of pathogenic microorganisms and
microbial indicators in three wastewater reclamation and managed aquifer
recharge facilities in Europe. The Science of the Total Environment, 408(21),
49234930.
Levy, D., Bens, M. S., Craun, G. F., Calderon, R. L., & Herwaldt, B. L. (1998). Surveillance for
water-borne disease outbreaks United States, 19951996. MMWR. Morbidity and
Mortality Weekly Report, 47(SS05), 134.
Lewis, M. D., Serichantalergs, O., Pitarangsi, C., Chuanak, N., Mason, C. J., Regmi, L. R.,
et al. (2005). Typhoid fever: A massive, single-point source, multidrug-resistant
outbreak in Nepal. Clinical Infectious Diseases, 40(4), 554561.
Li, T. H., Chiu, C. H., Chen, W. C., Chen, C. M., Hsu, Y. M., Chiou, S. S., et al. (2009).
Consumption of groundwater as an independent risk factor of Salmonella
Choleraesuis infection: A casecontrol study in Taiwan. Journal of Environmental
Health, 72, 2831.
Liang, J. L., Dziuban, E. J., Craun, G. F., Hill, V., Moore, M. R., Gelting, R. J., et al. (2006).
Surveillance for water-borne disease and outbreaks associated with drinking water
and water not intended for drinkingUnited States, 20032004. MMWR.
Surveillance Summaries, 55(12), 3165.
Lightfoot, D. (2004). Salmonella and other enteric organisms. In J. A. Cotruvo, A. Dufour,
G. Rees, J. Bartram, R. Carr, D. O. Cliver, G. F. Craun, R. Fayer, & V. P. J. Gannon (Eds.),
Water-borne zoonoses identication, causes, and control (pp. 228241). London: IWA
Publishing, World Health Organization.
Locas, A., Barthe, C., Margolin, A. B., & Payment, P. (2008). Groundwater microbiological
quality in Canadian drinking water municipal wells. Canadian Journal of
Lpez Cuevas, O., Len Flix, J., Jimnez Edeza, M., & Chaidez Quiroz, C. (2009).
Detection and antibiotic resistance of Escherichia coli and Salmonella in water and
agricultural soil. Revista Fitotecnia Mexicana, 32(2), 119126.
Luby, S. P., Faizan, M. K., Fisher-Hoch, S. P., Syed, A., Mintz, E. D., Bhutta, Z. A., et al.
(1998). Risk factors for typhoid fever in an endemic setting, Karachi, Pakistan.
Epidemiology and Infection, 120, 129138.
Lugo-Melchor, Y., Quiones, B., Amzquita-Lpez, B. A., Len-Flix, J., Garca-Estrada, R.,
& Chaidez, C. (2010). Characterization of tetracycline resistance in Salmonella
enterica strains recovered from irrigation water in the Culiacan Valley, Mexico.
Microbial Drug Resistance, 16(3), 185190.
Luxemburger, C., Duc, C. M., Lanh, M. N., Wain, J., Hien, T. T., Simpson, J., et al. (2001).
Risk factors for typhoid fever in Mekong delta, southern Vietnam: A casecontrol
study. Transactions of the Royal Society of Tropical Medicine and Hygiene, 95(1),
1923.
Lynch, M. F., Blanton, E. M., Bulens, S., Polyak, C., Vojdani, J., Stevenson, J., et al. (2009).
Typhoid fever in the United States, 19992006. Journal of the American Medical
Association, 302(8), 852869.
Maier, R., Pepper, I., & Gerba, C. (2000). Environmental microbiology. Orlando, Florida:
Academic Press.
Martinez-Urtaza, J., Liebana, E., Garcia-Migura, L., Perez-Pieiro, P., & Saco, M. (2004).
Characterization of Salmonella enterica serovar Typhimurium from marine
environments in coastal waters of Galicia (Spain). Applied and Environmental
Martinez-Urtaza, J., Saco, M., de Novoa, J., Perez-Pieiro, P., Peiteado, J., Lozano-Leon, A.,
et al. (2004). Inuence of environmental factors and human activity on the
presence of Salmonella serovars in a marine environment. Applied and Environmental Microbiology, 70, 20892097.
Meinersmann, R. J., Berrang, M. E., Jackson, C. R., Fedorka-Cray, P., Ladely, S., Little, E.,
et al. (2008). Salmonella, Campylobacter and Enterococcus spp.: Their antimicrobial
resistance proles and their spatial relationships in a synoptic study of the Upper
Oconee River basin. Microbial Ecology, 55(3), 444452.
Mermin, J. H., Villar, R., & Carpenter, J. (1999). A massive epidemic of multidrugresistant typhoid fever in Tajikistan associated with consumption of municipal
water. The Journal of Infectious Diseases, 179, 14161422.
Mezrioui, N., Baleux, B., & Trousselier, M. (1995). A microcosm study of the survival of
Escherichia coli and Salmonella Typhimurium in brackish water. Water Research, 29,
459465.
Mintz, E., Bartram, J., Lochery, P., & Wegelin, M. (2001). Not just a drop in the bucket:
Expanding access to point-of-use water treatment systems. American Journal of
Public Health, 91, 15651570.
Mohle-Boetani, J. C., Farrar, J., Bradley, P., Barak, J. D., Miller, M., Mandrell, R., et al.
(2009). Salmonella infections associated with mung bean sprouts: Epidemiological and environmental investigations. Epidemiology and Infection, 137,
57366.
Momba, M. N., Malakate, V. K., & Theron, J. (2006). Abundance of pathogenic Escherichia
coli, Salmonella Typhimurium and Vibrio cholerae in Nkonkobe drinking water
sources. Journal of Water and Health, 4(3), 289296.
Nasser, A. M., Glozman, R., & Nitzan, Y. (2002). Contribution of microbial activity to
virus reduction in saturated soil. Water Research, 36, 25892595.
Natvig, E. E., Ingham, S. C., Ingham, B. H., Cooperband, L. R., & Roper, T. R. (2002).
Salmonella enterica serovar Typhimurium and Escherichia coli contamination of root
and leaf vegetables grown in soils with incorporated bovine manure. Applied and
Environmental Microbiology, 68, 27372744.
Obi, C. L., Potgieter, N., Bessong, P. O., & Matsaung, G. (2003). Scope of potential bacterial
agents of diarrhoea and microbial assessment of quality of river water sources in
rural Venda communities in South Africa. Water Science and Technology, 47(3),
5964.
16
Obi, C. L., Potgieter, N., Musie, E. M., Igumbor, E. O., Bessong, P. O., Samie, A., et al.
(2004). Human and environmental-associated non-typhoidal Salmonella isolates from different sources in the Venda region of South Africa. Proceedings of
the 2004 Water Institute of Southern Africa (WISA), Biennial Conference, May
2004.
Oguntoke, O., Aboderin, O. J., & Bankole, A. M. (2009). Association of water-borne
diseases morbidity pattern and water quality in parts of Ibadan City, Nigeria.
Tanzania Journal of Health Research, 11(4), 189195.
Oluyege, J. O., Dada, A. C., & Odeyemi, A. T. (2009). Incidence of multiple antibiotic
resistant Gram-negative bacteria isolated from surface and underground water
sources in south western region of Nigeria. Water Science and Technology, 59(10),
19291936.
Ozler, H. M., & Aydin, A. (2008). Hydrochemical and microbiological quality of
groundwater in West Thrace Region of Turkey. Environmental Geology, 54, 355363.
Patchanee, P., Molla, B., White, N., Line, D. E., & Gebreyes, W. A. (2010). Tracking
Salmonella contamination in various watersheds and phenotypic and genotypic
diversity. Foodborne Pathogens and Disease, 7, 11131120.
Pezzoli, L., Elson, R., Little, C. L., Yip, H., Fisher, I., Yishai, R., et al. (2008). Packed with
Salmonella Investigation of an international outbreak of Salmonella Senftenberg
infection linked to contamination of prepacked basil in 2007. Foodborne Pathogen
Disease, 5, 661668.
Phan, T. T., Khai, L. T. L., Loc, C. B., Hayashidani, H., Sameshima, T., Watanabe, T., et al.
(2003). Isolation of Salmonella strains from the aquatic environment and
comparison with those of animal origin in Tan PhuThanh village, Mekong Delta,
Vietnam. Japan Agricultural Research Quarterly, 37(4), 237241.
Polo, F., Figueras, M. J., Inza, I., Sala, J., Fleisher, J. M., & Guarro, J. (1999). Prevalence of
Salmonella serotypes in environmental waters and their relationships with
indicator organisms. Antonie Van Leeuwenhoek, 75, 285292.
Pond, K. (2005). Water recreation and disease infections: Plausibility of associated acute
effects, sequelae and mortality. London: IWA Publishing, World Health Organization.
Popoff, M. Y. (2001). Antigenic formulas of the Salmonella serovars (8th ed.). Paris,
Institut Pasteur: WHO Collaborating Centre for Reference and Research on
Salmonella.
Potgieter, N., Obi, C. L., Bessong, P. O., Igumbor, E. O., Samie, A., & Nengobela, R. (2005).
Bacterial contamination of VhuswaA local weaning food and stored drinkingwater in impoverished households in the Venda Region of South Africa. Journal of
Health, Population and Nutrition, 23(2), 150155.
Rhodes, M. W., & Karton, H. (1988). Survival of E. coli and Salmonella spp. in estuarine
environments. Applied and Environmental Microbiology, 54, 29022907.
Risebro, H. L., Doria, M. F., Andersson, Y., Medema, G., Osborn, K., Schlosser, O., et al.
(2007). Fault tree analysis of the causes of water-borne outbreaks. Journal of Water
and Health, 5(1), 118.
Rizzo, C., Santantonio, M., Coscia, M. F., Monno, R., De Vito, D., & Rizzo, G. (2008).
Typhoid fever in Italy, 20002006. Journal of Infection in Developing Countries, 2(6),
466468.
Savichtcheva, O., & Okabe, S. (2006). Alternative indicators of fecal pollution: Relations
with pathogens and conventional indicators, current methodologies for direct
pathogen monitoring and future application perspectives. Water Research, 40,
24632476.
Savichtcheva, O., Okayama, N., & Okabe, S. (2007). Relationships between Bacteroides
16S rRNA genetic markers and presence of bacterial enteric pathogens and
conventional fecal indicators. Water Research, 41, 36153628.
Schets, F. M., van Wijnen, J. H., Schijven, J. F., Schoon, H., & de RodaHusman, A. M.
(2008). Monitoring of water-borne pathogens in surface waters in Amsterdam, the
Netherlands, and the potential health risk associated with exposure to Cryptosporidium and Giardia in these waters. Applied and Environmental Microbiology, 74,
20692078.
Schikora, A., Carreri, A., Charpentier, E., & Hirt, H. (2008). The dark side of the salad:
Salmonella typhimurium overcomes the innate immune response of Arabidopsis
thaliana and shows an endopathogenic lifestyle. PloS One, 3(5), e2279.
Schriewer, A., Miller, W. A., Byrne, B. A., Miller, M. A., Oates, S., Conrad, P. A., et al.
(2010). Presence of Bacteroidales as a predictor of pathogens in surface waters of
the central California coast. Applied and Environmental Microbiology, 76,
58025814.
Schuster, C. J., Ellis, A. G., Robertson, W. J., Charron, D. F., Aramini, J. J., Marshall, B. J., et al.
(2005). Infectious disease outbreaks related to drinking water in Canada, 1974
2001. Canadian Journal of Public Health, 96(4), 254258.
Sharma, P. K., Ramakrishnan, R., Hutin, Y., Manickam, P., & Gupte, M. D. (2009). Risk
factors for typhoid in Darjeeling, West Bengal, India: Evidence for practical action.
Tropical Medicine & International Health, 14(6), 696702.
Simental, L., & Martinez-Urtaza, J. (2008). Climate patterns governing the presence and
permanence of Salmonella in coastal area of Bahia de Todos Santos Mexico. Applied
and Environmental Microbiology, 74, 58185924.
Sinton, L., Hall, C., & Braithwaite, R. (2007). Sunlight inactivation of Campylobacter jejuni
and Salmonella enterica, compared with Escherichia coli, in seawater and river
water. Journal of Water and Health, 5(3), 357365.
Sivapalasingam, S., Barrett, E., Kimura, A., Van Duyne, S., De Witt, W., Ying, M., et al.
(2003). A multistate outbreak of Salmonella enterica Serotype Newport infection
linked to mango consumption: Impact of water-dip disinfestation technology.
Clinical Infectious Diseases, 37(12), 15851590.
Sivapalasingam, S., Friedman, C. R., Cohen, L., & Tauxe, R. V. (2004). Fresh produce: A
growing cause of outbreaks of foodborne illness in the United States, 1973 through
1997. Journal of Food Protection, 67(10), 23422353.
Smith, A., Reacher, M., Smerdon, W., Adak, G. K., Nichols, G., & Chalmers, R. M. (2006).
Outbreaks of water-borne infectious intestinal disease in England and Wales,
19922003. Epidemiology and Infection, 134(6), 11411149.
Srikantiah, P., Girgis, F. Y., Luby, S. P., Jennings, G., Wasfy, M. O., Crump, J. A., et al.
(2006). Population-based surveillance of typhoid fever in Egypt. The American
Journal of Tropical Medicine and Hygiene, 74, 114119.
Srikantiah, P., Vafokulov, S., Luby, S. P., Ishmail, T., Earhart, K., Khodjaev, N., et al. (2007).
Epidemiology and risk factors for endemic typhoid fever in Uzbekistan. Tropical
Medicine & International Health, 12(7), 838847.
Stanwell-Smith, R., Andersson, Y., & Levy, D. A. (2003). National surveillance systems. In
P. R. Hunter, M. Waite, & E. Ronchi (Eds.), Drinking water and infectious disease:
Establishing the links. Boca Raton, FL: CRC Press.
Suresh, K., & Smith, H. V. (2004). Tropical organisms in Asia/Africa/South America. In J.
A. Cotruvo, A. Dufour, G. Rees, J. Bartram, R. Carr, D. O. Cliver, G. F. Craun, R. Fayer, &
V. P. J. Gannon (Eds.), Water-borne zoonoses identication, causes, and control
(pp. 93112). London: IWA Publishing, World Health Organization.
Swaddiwudhipong, W., & Kanlayanaphotporn, J. (2001). A common-source waterborne outbreak of multidrug resistant typhoid fever in a rural Thai community.
Journal of the Medical Association of Thailand, 84, 15131517.
Takkinen, J., Nakari, U. M., Johansson, T., Niskanen, T., Siitonen, A., & Kuusi, M. (2005). A
nationwide outbreak of multiresistant Salmonella Typhimurium var. Copenhagen
DT104B infection in Finland due to contaminated lettuce from Spain, May 2005.
Eurosurveillance Weekly 10 http://www.eurosurveillance.org/ew/2005/050630.asp
accessed on 27/5/2011
Taylor, R., Sloan, D., Cooper, T., Morton, B., & Hunter, I. (2000). A water-borne outbreak
of Salmonella Saintpaul. Communicable Diseases Intelligence, 24, 336340.
Thunberg, R. L., Tran, T. T., Bennett, R. W., & Matthews, R. N. (2002). Research note:
Microbial evaluation of selected fresh produce obtained at retail markets. Journal of
Food Protection, 65, 677682.
Till, D., McBride, G., Ball, A., Taylor, K., & Pyle, E. (2008). Large-scale freshwater
microbiological study: Rationale, results and risks. Journal of Water and Health, 6(4),
443460.
Tobias, H., & Heinemeyer, E. A. (1994). Occurrence of Salmonella in coastal North Sea
water and their hygienic relation to indicator bacteria and sources of
contamination. Zentralblatt fr Hygiene und Umweltmedizin, 195(56), 495508.
Toze, S. (2004). Pathogen survival in groundwater during articial recharge. In J.
Steenvoorden, & T. Endreny (Eds.), Wastewater re-use and groundwater quality
(pp. 7084). Wallingford: Int Assoc Hydrological Sciences.
Toze, S., Bekele, E., Page, D., Sidhu, J., & Shackleton, M. (2010). Use of static quantitative
microbial risk assessment to determine pathogen risks in an unconned carbonate
aquifer used for managed aquifer recharge. Water Research, 44, 10381049.
Toze, S., Hanna, J., Smith, T., Edmonds, L., & McCrow, A. (2004). Determination of
water quality improvements due to the articial recharge of treated efuent. In
J. Steenvoorden, & T. Endreny (Eds.), Wastewater re-use and groundwater quality
(pp. 5360). Wallingford: Int Assoc Hydrological Sciences.
Tran, H. H., Bjune, G., Nguyen, B. M., Rottingen, J. A., Grais, R. F., & Guerin, P. J. (2005).
Risk factors associated with typhoid fever in Son La province, northern Vietnam.
Transactions of the Royal Society of Tropical Medicine and Hygiene, 99, 819826.
Tyrrel, S. F., Knox, J. W., & Weatherhead, E. K. (2006). Microbiological water quality
requirements for salad irrigation in the United Kingdom. Journal of Food Protection,
69, 20292035.
Vollaard, A. M., Ali, S., Van Asten, H. A., Widjaja, S., Visser, L. G., & Surjadi, C. (2004). Risk
factors for typhoid and paratyphoid fever in Jakarta, Indonesia. Journal of the
American Medical Association, 291, 26072615.
Wall, K., Pang, L., Sinton, L., & Close, M. (2008). Transport and attenuation of microbial
tracers and efuent microorganisms in saturated pumice sand aquifer material.
Water, Air, and Soil Pollution, 188, 213224.
Walters, S. P., Gannon, V. P., & Field, K. G. (2007). Detection of Bacteroidales fecal
indicators and the zoonotic pathogens E. coli 0157:H7, Salmonella, and
Campylobacter in river water. Environmental Science & Technology, 41,
18561862.
Wry, N., Lhoutellier, C., Ducray, F., Delgens, J. P., & Godon, J. J. (2008). Behaviour of
pathogenic and indicator bacteria during urban wastewater treatment and
sludge composting, as revealed by quantitative PCR. Water Research, 42, 5362.
WHO (2008). Guidelines for drinking-water quality: Third edition incorporating the
rst and second addenda. Recommendations, Vol. 1., Geneva: IWA Publishing,
World Health Organization.
Wilkes, G., Edge, T., Gannon, V., Jokinen, C., Lyautey, E., Medeiros, D., et al. (2009).
Seasonal relationships among indicator bacteria, pathogenic bacteria, Cryptosporidium oocysts, Giardia cysts, and hydrological indices for surface waters within an
agricultural landscape. Water Research, 43, 22092223.
Wineld, M. D., & Groisman, E. A. (2003). Role of nonhost environments in the
lifestyles of Salmonella and Escherichia coli. Applied and Environmental
Microbiology, 69(7), 36873694.
Wray, C., & Wray, K. A. (2000). Salmonella in domestic animals. Oxon, UK: CABI
Publishing.
Yoder, J., Roberts, V., Craun, G. F., Hill, V., Hicks, L. A., Alexander, N. T., et al. (2008).
Surveillance for water-borne disease and outbreaks associated with drinking
water and water not intended for drinkingUnited States, 20052006. MMWR
Surveillance Summary, 57(9), 3962.
Zaleski, K. J., Josephson, K. L., Gerba, C. P., & Pepper, I. L. (2005). Potential regrowth and
recolonization of salmonellae and indicators in biosolids and biosolid-amended
soil. Applied and Environmental Microbiology, 71, 37013708.

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Salmonella in surface and drinking water: Occurrence and

Corresponding author. Tel.: + 39 06 90672781; fax: +39 06 90672787.

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

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

surveillance and epidemiological studies, of the relevance of the water

Swaddiwudhipong & Kanlayanaphotporn, 2001; Tran et al., 2005;

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

microbial quality of water for domestic uses in the Venda region

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

Salmonella I 4,[5],12:i: involving ve persons in a rural community in

occurred in Italy from 1998 to 2005. However because the

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

3. Role of contaminated waters in Salmonella foodborne

Salmonellae are often isolated from produce samples in routine

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

Several studies have investigated the potential source of produce

antibiotic resistant Salmonella strains in surface and drinking water

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

Dominant impact in the analyzed water

Mainly inuenced by rainfall runoff and

Mixed comprising untreated sewage of

Four differently impacted

Urban pond and tidal creeks

Lake and river water

Mixed: WWTPs efuents, surface runoff,

Mixed: mainly forested and agricultural in a

Mainly rural area

Urban canals/river and

Rivers and lakes Fresh water

Mixed: birds, dairy farming, municipal,

River and irrigation water

Mixed comprising WWTP discharge

Mixed: Urban/industrial, WWTP discharge

coastal area and marine environment (Baudart, Grabulos, Barrusseau,

enhanced livestock based fecal input during this period. According

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

et al., 2007; Schriewer et al., 2010). Schriewer et al. (2010) reported a

Infantis, Derbyf, Indiana,

4.2. Diversity of Salmonella strains isolated from surface waters

Netherlands Schets et al.

(continued on next page)

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

Also isolated from human and/or animal feces.

Contamination sources and environmental factors were also

(2010) also showed that Salmonella serovar Gaminara, was dominant

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

however, they stressed that the use of genotyping methods with

6 1013.8 102 gc/L

Drinking water supply

Tap water of urban water

Australia Ahmed et al.