A Review of Known and Hypothetical Transmission Routes
Elisabeth Mathijs•Ambroos Stals•Leen Baert•Nadine Botteldoorn•Sarah Denayer•
Axel Mauroy•Alexandra Scipioni•Georges Daube•Katelijne Dierick•Lieve Herman•
Els Van Coillie•Mieke Uyttendaele•Etienne Thiry
Received: 21 February 2012/Accepted: 6 October 2012/Published online: 3 November 2012
? Springer Science+Business Media New York 2012
worldwide leading cause of acute non-bacterial gastroen-
teritis. Due to a combination of prolonged shedding of high
virus levels in feces, virus particle shedding during
asymptomatic infections, and a high environmental per-
sistence, NoVs are easily transmitted pathogens. Norovirus
(NoV) outbreaks have often been reported and tend to
affect a lot of people. NoV is spread via feces and vomit,
but this NoV spread can occur through several transmission
routes. While person-to-person transmission is without a
doubt the dominant transmission route, human infective
Human noroviruses (NoVs) are considered a
NoV outbreaks are often initiated by contaminated food or
water. Zoonotic transmission of NoV has been investi-
gated, but has thus far not been demonstrated. The pre-
sented review aims to give an overview of these NoV
transmission routes. Regarding NoV person-to-person
transmission, the NoV GII.4 genotype is discussed in the
current review as it has been very successful for several
decades but reasons for its success have only recently been
suggested. Both pre-harvest and post-harvest contamina-
tion of food products can lead to NoV food borne illness.
Pre-harvest contamination of food products mainly occurs
via contact with polluted irrigation water in case of fresh
produce or with contaminated harvesting water in case of
bivalve molluscan shellfish. On the other hand, an infected
food handler is considered as a major cause of post-harvest
contamination of food products. Both transmission routes
are reviewed by a summary of described NoV food borne
outbreaks between 2000 and 2010. A third NoV trans-
mission route occurs via water and the spread of NoV via
river water, ground water, and surface water is reviewed.
Finally, although zoonotic transmission remains hypothet-
ical, a summary on the bovine and porcine NoV presence
observed in animals is given and the presence of human
infective NoV in animals is discussed.
person ? Food ? Water ? Zoonotic
Norovirus ? Transmission route ? Person-to-
Noroviruses (NoVs) were discovered in 1972 by immune
electron microscopy analysis of fecal samples of volunteers
challenged with fecal filtrates from a group of elementary
school students affected by an outbreak of gastroenteritis in
Elisabeth Mathijs and Ambroos Stals contributed equally to this work.
E. Mathijs ? A. Mauroy ? A. Scipioni ? E. Thiry
Department of Infectious and Parasitic diseases, Virology
and Viral diseases, Faculty of Veterinary Medicine, University
of Lie `ge, Boulevard du Colonster 20, 4000 Lie `ge, Belgium
E. Mathijs ? G. Daube
Food Science Department, Food Microbiology, Faculty
of Veterinary Medicine, University of Lie `ge, Boulevard du
Colonster 20, 4000 Lie `ge, Belgium
A. Stals (&) ? L. Baert ? M. Uyttendaele
Laboratory of Food Microbiology and Food Preservation,
Department of Food Safety and Food Quality, Faculty
of Bioscience Engineering, Ghent University, Coupure Links
653, 9000 Ghent, Belgium
A. Stals ? L. Herman ? E. Van Coillie
Technology and Food Science Unit, Institute for Agricultural
and Fisheries Research (ILVO), Brusselsesteenweg 370, 9090
N. Botteldoorn ? S. Denayer ? K. Dierick
Division of Bacteriology, Department of Microbiology, Belgian
Scientific Institute of Public Health, Juliette Wytsmanstraat 14,
1050 Brussels, Belgium
Food Environ Virol (2012) 4:131–152
1968 in Norwalk, Ohio (Kapikian et al. 1972). The
27–32 nm viral agent was originally named Norwalk virus
and was later recognized as the type agent of the genus
Norovirus (previously denoted as ‘‘Norwalk-like viruses’’
or ‘‘small round structured viruses’’). Similar to human
infective NoVs, animal infective NoVs were discovered by
electron microscopy of stool samples of domestic animal
species (calves and pigs) suffering from gastroenteritis
(Bridger 1980; Saif et al. 1980; Woode and Bridger 1978).
Together with the genera Sapovirus (previously called
‘‘Sapporo-like viruses’’), Lagovirus, Vesivirus, and Nebo-
virus, the Norovirus genus forms the Caliciviridae family
(Green et al. 2000). The Norovirus genus comprises five
genogroups (GI to GV) each containing several NoV
genotypes (Zheng et al. 2006). Genogroups I and II (GI and
GII) consist of 8 and 17—extended to 19 by Wang et al.
(2007)—–NoV genotypes, respectively. These genogroups
comprise the human infective NoV genotypes, together
with the Alphatron and Ft. Lauerdale genotypes in geno-
group IV (GIV). The latter genogroup also contains a
number of NoV genotypes infecting carnivores such as
dogs, lions, and cats (Martella et al. 2007; Martella et al.
2008; Pinto et al. 2012). Bovine and murine NoV are
classified in genogroup III (GIII) and V (GV), respectively,
while porcine NoV is also classified in GII. Human
infective NoVs are among the most important causes of
gastroenteritis in adults worldwide and NoV infections
often occur as outbreaks (Koopmans and Duizer 2004). On
the other hand, the true extent of the host range of animal
NoVs remains unknown although it is known that a large
number of animal species can be infected with NoVs
(Scipioni et al. 2008).
Human and animal infective NoVs are spread via feces
and vomit through different transmission routes. Due to the
development of sensitive methods for molecular detection
of NoVs, knowledge on these NoV transmission routes has
increased substantially. The current review, therefore,
aimed to provide an overview of known transmission
routes, specifically of human infective NoVs. Furthermore,
the presence of animal infective NoVs in bovine and por-
cine animals and the possibility of zoonotic transmission of
NoVs were discussed.
Transmission Routes of NoV
Described transmission routes of human infective NoVs
include person-to-person transmission (chapter 3.1), food
borne transmission (chapter 3.2), and water borne trans-
mission (chapter 3.3) while zoonotic transmission (chapter
3.4) has been considered a hypothetical—yet unproved—
route for NoV transmission.
A schematic overview of proven and hypothetical
transmission routes for human and animal infective NoVs
is shown in Fig. 1. Transmission of human infective NoVs
is facilitated by a number of factors such as (i) prolonged
duration of viral shedding, even after resolving of the
symptoms (Aoki et al. 2010; Atmar et al. 2008; Lee et al.
2007), (ii) fecal shedding during asymptomatic NoV
infections (Gallimore et al. 2004b; Ozawa et al. 2007;
Phillips et al. 2010), and (iii) NoV persistence on envi-
ronmental surfaces and in water and foods (Escudero et al.
2012; Lamhoujeb et al. 2009; Liu et al. 2009b; Ueki et al.
Although human infective NoVs can be transmitted
through several routes, person-to-person transmission is
considered to be the dominant NoV transmission route
(Fig. 1) (Kroneman et al. 2008). NoV outbreaks related to
this transmission route have extensively been documented
in semi-closed community settings such as hospitals, cruise
ships, day-care centers, and military settings and can affect
a few to a lot of people (Gallimore et al. 2004a, b; Grotto
et al. 2004; Takkinen 2006; Wick 2012). Recently, NoV
outbreaks between 2002 and 2006 were investigated using
data collected by 11 surveillance systems of the Food borne
Viruses in Europe (FBVE) network (Verhoef et al. 2010).
Out of 886 confirmed norovirus outbreaks with known
transmission route, 654 outbreaks (74 %) involved person-
to-person contamination. Similarly, Lopman et al. (2003)
and Siebenga et al. (2007) found that person-to-person
spread was the transmission route in 85 % and 82 % of
NoV outbreaks with a known mode of transmission in the
UK and in The Netherlands, respectively.
The NoV genotype most commonly identified in person-
to-person NoV gastroenteritis outbreaks is the NoV GII.4
genotype (Kroneman et al. 2008; Verhoef et al. 2010,
2009). Therefore, its epochal evolution has been docu-
mented thoroughly between 1974 and 2007. In the USA,
only 2 major NoV GII.4 strains were observed between
1974 and 1994 (a NoV GII.4 ancestor strain and GII.4
Camberwell). In the 7 year period between 1995 and 2002
a single major NoV GII.4 strain was considered dominant
(NoV GII.4 Grimsby) both in Europe and in the USA.
Subsequently, NoV GII.4 Farmington Hills and Hunter
(also named NoV GII.4 2002 and NoV GII.4 2004,
respectively, in Europe) caused 2 NoV epidemic seasons in
2002–2003 and 2004–2005. Finally, NoV GII.4 Laurens
and NoV GII.4 Den Haag (also named GII.4 2006a and
GII.4 2006b in Europe) have caused NoV epidemics since
2006 (Bok et al. 2009; Siebenga et al. 2009; Zheng et al.
2009). Bull and White (2011) recently reviewed reasons for
the success of the NoV GII.4 genotype and they concluded
132Food Environ Virol (2012) 4:131–152
that a synergism of multiple factors could be responsible
for its success. First of all, NoV GII.4 has a mutation rate
that is approximately 2-fold higher compared to other NoV
genotypes (Bok et al. 2009; Bull et al. 2010; Siebenga et al.
2010). This could in part be caused by the NoV GII.4 RNA
dependent RNA polymerase which has shown a lower
fidelity compared to some other NoV genotypes, enabling
the more prevalent viruses to avoid immune recognition by
rapidly altering their antigenic properties (Bull et al. 2010;
Bull and White 2011). Second, NoV GII.4 can bind more
histo-blood group antigen (HBGA) types than any other
NoV genotype, which could be a major contributing factor
to the NoV GII.4 dominance (Bull and White 2011). Third,
while long-term immunity may be possible for some NoV
genotypes (e.g., GII.3), it is possible that this is not the case
for GII.4 NoV (Bull and White 2011; Siebenga et al. 2009;
Yang et al. 2010). However, only limited research has been
performed on each factor and further study is needed.
Food Borne Transmission
Person-to-person transmission is without a doubt the
dominant transmission route for NoV, but the primary
cases in NoV outbreaks often have a food or water borne
cause (Fig. 1). Person-to-person transmission among con-
tacts of primary cases can further propagate the epidemic
(Becker et al. 2000; Patel et al. 2009). Food products can
be contaminated with NoV by contact with fecal material
or vomit, which can occur during any stage of the food
production (Baert et al. 2011). In essence, NoV contami-
nation of foods can occur during at a pre-harvest level, e.g.,
by irrigation of fresh produce with NoV contaminated
water or by use of contaminated manure, or at a (post-)
harvest level, e.g., by manual picking, processing, and
preparation of foods such as strawberries and raspberries
(Wei and Kniel 2010; Zainazor et al. 2010).
The current paragraph will go more into detail regarding
these transmission routes by a literature review of studies
investigating individual NoV food borne outbreaks. In
total, 51 studies describing 58 outbreaks that occurred
between 2000 and 2010 were reviewed (Table 1). The
number of described NoV food borne outbreaks is con-
sidered as a serious underestimation of the actual number
and is probably biased because peer-reviewed publications
of food borne outbreaks merely report large, well-
documented, unusual, or novel events (Baert et al. 2009b;
Kroneman et al. 2008; O’Brien et al. 2006). Furthermore,
NoV illness is normally self-limiting and complications are
not common which could lead to a further underestimation
of NoV food borne gastroenteritis outbreaks (Greening
2006; Lopman et al. 2002).
A food borne outbreak has been defined by multiple
official authorities such as the European Food Safety
Authority (EFSA), the World Health Organization (WHO),
and the Centers for Disease Control and Prevention (CDC).
However, all definitions include the occurrence of two or
more human cases of a same/similar disease resulting from
the same food source(s) (Anonymous 2000, 2010; World
Health Organization 2008). All reviewed outbreaks com-
plied with these definitions and the NoV food borne out-
break data were categorized in Table 1 per transmission
route: by pre-harvest contamination or by (post-) harvest
contamination. Regarding the latter transmission route,
focus was set on infected food handlers, either confirmed or
Fig. 1 Schematic overview of
the transmission routes of
human and animal infective
NoVs. Solid and dashed arrows
indicate proven and
routes, respectively. The
thickness of the arrows is
related to the likeliness of the
Food Environ Virol (2012) 4:131–152133
Table 1 Overview of NoV food borne outbreaks between 2000 and 2010
Attack rate (%)
NV in Food/food
Virus extraction (food)
method (food ? clinical)
5/9 stool: GI
(Le Guyader et al.
1043 people (6
Stool: GII.7, GII.4, GIIb
(Falkenhorst et al.
74/270 (27 %)
5/6 stool: GI.5
(Cotterelle et al.
43/74 (58 %)
5/5 stool: NV
(Hjertqvist et al.
2/2 stool: GI.4
3/5 raspberries: GI.4
(Maunula et al.
11/11 stool: GII.I
(Makary et al.
25/26 stool: GII.4
1 salad vegetable:
(Oogane et al.
Stool 2/25: GI, 12/25:
GII, GI ? GII: 9/25
1/2 lettuce heads:
(Ethelberg et al.
30/100 (30 %)
1/1 stool: GI.I
3/5 oysters: GI.I,
Direct RNA extraction
(Nenonen et al.
83/106 (78 %)
8/8 stool: GI.2/4,GII.5/6/
Proteinase K treatment
(Webby et al.
9/12 stool: GI.I/2,GII.4/7
62 Oysters: 25 GI,
Proteinase K treatment
(Le Guyader et al.
2/4 stool: GI.I
5/6 oysters: GI.I
Proteinase K treatment
(Le Guyader et al.
15/22 (68 %)
11/11 stool: GI and GII
(Gallimore et al.
26/53 stool: GI.2
(David et al. 2007)
29/53 stool: GI.4/6,GII.4/
3/3 shellfish: GI.4,
Proteinase K treatment
(Le Guyader et al.
Oysters (frozen half
4/5 stool: GII
6/11 oysters: GII
(Ng et al. 2005)
24/24 stool: GI and GII
6/11 mussels: GI
(Prato et al. 2004)
18/20 stool: GII
(Rizzo et al. 2007)
no stool samples
59 pooled clams:
(Kingsley et al.
134Food Environ Virol (2012) 4:131–152
Table 1 continued
Attack rate (%)
NV in Food/food
Virus extraction (food)
method (food ? clinical)
15/16 stool: NV
5/8 food handlers:
(de Coster et al.
38/57 (67 %)
12/14 stool: NV
2/4 food handlers:
(Godoy et al. 2005)
24/27 stool: GII
(De Wit et al.
34/427 (1 %)
12/14 stool: GI.3 Desert
(Sala et al. 2005)
87/142 (61 %)
21/21 stool: NV
Food handler: NoV
(Payne et al. 2006)
23/32 stool: GII.4
15/23 Food handler:
(Ohwaki et al.
87/124 stool and vomit:
5/10 food handlers:
(Hirakata et al.
14/14 stool: GI.4 Chiba
Food handler: NoV
(Bohm et al. 2008)
19/19 stool: NV
handler ? cook:
(Lederer et al.
3/9 stool: GII.4
Food handler: GII.4
(Showell et al.
32/59 stool: GII
2/15 food handlers:
Direct RNA extraction
(Anderson et al.
5/6 stool: GII.7 Leeds
4/5 kitchen staff:
(Schmid et al.
60/106 (57 %)
6/13 stool: GII.6 Seacroft
Real-time RT-PCR ? EIA
(Vivancos et al.
8/28: GI.3 Desert Shield
Food handler: GI.3
(Zomer et al. 2009)
12/53 stool: GII.4 2006b
(Wadl et al. 2010)
35/61 (57 %)
24/31: GII.4 Terneuzen
5 food handlers:
RT-PCR ? EM
(Medici et al. 2008)
21/63 (33 %)
(Kuo et al. 2009)
4/4 stool: NV
Food handler: NoV
(Friedman et al.
Food Environ Virol (2012) 4:131–152 135
Table 1 continued
Attack rate (%)
NV in Food/food
Virus extraction (food)
method (food ? clinical)
45/83 (54 %)
31/36 stool: NV
(Kiehl et al. 2001)
63/85 (74 %)
5/5 stool: GII
(Parasidis et al.
28/48 (58 %)
12/13 stool: GII.4
(Glasscock et al.
7/8 stool: GI
RT-PCR ? EM
(Johansson et al.
33/83 (40 %)
4/4 stool: GI.3
(Nordgren et al.
21/25 (84 %)
2/2 stool: GI
(Fretz et al. 2005)
Buffet food (catered
4/4 stool samples: GIIb
Ham, salami: GIIb
Direct RNA extraction
(Boxman et al.
Buffet food (private
12/21 (57 %)
no stool samples
Ham off the bone:
Direct RNA extraction
(Boxman et al.
85/106 (80 %)
4/6 stool: GII
(Morioka et al.
6/6 (100 %)
no stool samples
Direct RNA extraction
(Boxman et al.
2/4 stool: NV
(Costas et al. 2007)
21/23 stool: GI.12
(Sakon et al. 2005)
64/113 (57 %)
3/3 stool: GI
(Dippold et al.
Canteen food (salad)
4/24 stool: GII
(Grotto et al. 2004)
Lettuce salad and
16/22 (73 %)
2/2 stool, 1/1 emesis:
Raspberries ? water
48/137 (35 %)
6/17 stool: GII.4 2006b
Direct RNA extraction
(Verhoef et al.
ns not specified, ab antibodies, EIA enzyme immuno assay
136Food Environ Virol (2012) 4:131–152
suspected (Table 1). The involvement of a NoV infected
food handler in a NoV food borne outbreak was considered
confirmed if (i) epidemiological analysis showed that the
food handler was infected before the food borne outbreak
and could be linked to manipulation of the involved food
products and if (ii) laboratory analysis showed identical
NoV genogroups or genotypes in the clinical samples from
both patients and food handler. For every reviewed NoV
food borne outbreak in Table 1, the attack rate (the number
of exposed individuals infected with NoV divided by the
number of exposed individuals in a NoV food borne out-
break), and/or the number of affected people and the lab-
oratory confirmation of the NoV presence in human and/or
food samples were described. Regardless of the transmis-
sion route, some trends were clearly noticeable. Overall,
RT-PCR was the most used NoV detection method as it
was used in 47 of 51 (92 %) studies. Extraction of virus
particles or viral genomic material from the food samples
was performed by various methods. Of the 23 studies
(45 %) that tested the NoV presence on food products, 14
studies (61 %) used elution-concentration extraction, pro-
teinase K treatment, and direct RNA extraction to extract
NoV from food, while 9 (39 %) studies did not specify the
used virus extraction method (Table 1). In general, all but
two studies (Boxman et al. 2007; Kingsley et al. 2002)
combined epidemiological investigations with molecular
detection of NoVs in clinical samples. A smaller fraction of
studies (29 %) was able to demonstrate the NoV presence
in the suspected food products (Table 1).
Pre-Harvest Contamination of Food Products
In general, food products most at risk for pre-harvest NoV
contamination include fresh produce and shellfish (Baert
et al. 2011; Lowther et al. 2012; Mattison et al. 2010; Stals
et al. 2011b). NoV contamination of fresh produce at a pre-
harvest stage can result from contact with polluted irriga-
tion water or contaminated manure (Wei and Kniel 2010),
while shellfish can be contaminated if grown in NoV
contaminated harvesting areas (Lowther et al. 2008).
Table 1 showed that 24 out of 58 (41.4 %) NoV food borne
outbreaks could be related to consumption of pre-harvest
contaminated fresh produce and shellfish and that mainly
raspberries and oysters were involved in these outbreaks.
An average attack rate of 51 % was observed with an
average of 145 people exposed per outbreak. The most
observed NoV genotype in clinical and food samples was
GII.4, although NoV genotypes GI.1, GI.2, GI.4, and GII.7
were frequently detected in food and clinical samples as
In 42 % (10 out of 24) of these outbreaks, identical
genogroups or genotypes were found in clinical and food
samples. In an additional 8 % (2 out of 24) of these NoV
food borne outbreaks, different NoV genotypes were
detected in clinical and food samples. Noteworthy, NoV
could be detected in shellfish samples in 9 of 11 (82 %)
studies, which could be explained by the higher levels of
NoV found in shellfish compared to other food products
due to their filter feeding capacity (Meyers 1984).
NoV and other viral pathogens have been observed in
shellfish by several screening studies. A 3 year survey
between 2005 and 2008 investigating 116 retail shellfish
samples (mussels, clams, and oysters) showed a confirmed
(sequenced) detection of NoV genotypes GII.4 2004 and
GIIb in 10.3 % of all tested samples (Terio et al. 2010).
Likewise, GII.4 and GIIb genotypes were found in 16.7 %
of oyster and mussel samples (n = 42) during a 2 year
survey for the NoV presence in Dutch shellfish (Boxman
et al. 2006) while a 1 year survey in 235 Italian shellfish
samples showed the presence of NoV and HAV in 13.2 %
and 2.2 % of all tested samples, respectively (Croci et al.
2007). Although some studies found NoV GII.4 in shellfish
samples related to NoV food borne outbreaks, the GIIb
genotype was not encountered in any of these studies
(Table 1). A lower NoV presence was observed when 1512
Japanese oysters were screened for the NoV presence as a
broad range of GI and GII NoV genotypes were found in
4.9 % of all tested oyster samples (Nishida et al. 2007).
NoV have been detected in sewage with high concentra-
tions (339 to 106NoV genomic copies per liter) and
treatment of the sewage caused only a minor reduction of
0.7–2.7 logs NoV genomic copies per liter (Lodder and de
Roda Husman 2005; van den Berg et al. 2005). A Japanese
study has shown that very similar NoV genotypes can be
detected in human feces, domestic sewage, treated waste-
water, river water, and in cultivated oysters (Ueki et al.
2005), demonstrating that transmission of NoV from con-
taminated harvesting water to bivalve filter feeding shell-
fish such as mussels or oysters is possible. Although
numerous studies using PCR have demonstrated the NoV
presence in various shellfish and shellfish harvesting areas,
the number of epidemiologically confirmed shellfish-asso-
ciated outbreaks is relatively low. Lowther et al. (2012)
found that the number of genomic copies detected in
shellfish samples was significantly higher in outbreak
related samples (mean level of 2148 NoV genomic copies/
g) compared to non-outbreak related samples (mean level
of 682 NoV genomic copies/g). Although more data is
needed, a critical level may aid NoV risk management in
shellfish. As critical limits of 100, 200, 500, 1000, or
10.000 NoV genomic copies would result in the rejection
of 33.6 to 88.9, 24.4 to 83.3, 10.0 to 72.2, 7.7 to 44.4, or 0
to 11.1 % of batches, respectively (Anonymous 2012),
careful consideration of a possible NoV critical limit in
oysters and other shellfish is needed.
Food Environ Virol (2012) 4:131–152 137
Regarding the NoV food borne outbreaks related to
consumption of pre-harvest contaminated raspberries, two
out of five studies were able to recover NoV from this food
matrix (Le Guyader et al. 2004; Maunula et al. 2009).
Multiple authors have stated that detection of NoVs in
raspberries can be challenging, especially if the NoV levels
are lower than 104genomic copies per 10–15 g (Stals et al.
2011c; Summa et al. 2012a). However, as a quantitative
method was not applied in both outbreak studies, the NoV
levels on the raspberries could not be determined. Only a
limited number of studies have investigated the pre-harvest
presence of enteric viruses on fresh produce. NoV and
adenovirus have been detected in a single spinach sample
when screening 30 produce samples for the enteric virus
presence (Cheong et al. 2009). A recent review by Baert
et al. (2011) summarized a Belgian, a Canadian, and a
French study screening the NoV presence on fresh produce
(Mattison et al. 2010; Stals et al. 2011b). NoV was detected
by real-time RT-PCR in 28 % (n = 641), 33 % (n = 6),
and 50 % (n = 6) of leafy greens tested in Canada, Bel-
gium, and France, respectively. Soft red fruits were found
positive in 35 % (n = 29) and 7 % (n = 150) of the
samples tested in Belgium and France, respectively.
However, subsequent sequencing of a conventional RT-
PCR amplicon was successful in merely 7 % of all positive
results. The latter finding gave rise to questions regarding
the interpretation of NoV-positive real-time RT-PCR
results in the light of the increase in sensitivity of the NoV
detection methodology. The authors suggested that strate-
gies to confirm the results by real-time RT-PCR should be
developed in analogy with the detection of microbial
pathogens in foods (Baert et al. 2011). Although a critical
limit for food products such as raspberries and other fresh
produce–similar to shellfish–is an option for risk manage-
ment, further research is needed regarding a potential link
between NoV levels on fresh produce and related food
(Post-) Harvest Contamination of Food Products
Contamination of food products at post-harvest stage can
occur at any point during harvesting, processing, preparing,
and packing of the food (Moe 2008; Todd et al. 2009). The
current review focussed on the transmission of NoV by
infected food handlers, as they have been confirmed to play
a major role in NoV transmission (Baert et al. 2009b;
Widdowson et al. 2005b). Table 1 showed that food han-
dlers were involved in 34 out of 58 (58 %) NoV food borne
outbreaks, either suspected (16 out of 34 outbreaks) or
confirmed (18 out of 34 outbreaks). Deli sandwiches were
the most frequent implicated foods in these food borne
outbreaks, but as expected, a wide range of food products
including catered meals, buffet foods, and prepared salads
have been involved. An average attack rate of 34 % was
observed with 120 people averagely exposed per outbreak,
which was comparable to the NoV food borne outbreaks
caused by pre-harvest contaminated foods. Remarkably,
NoV could be detected in food samples in merely 12 % (4
out of 34) of studies investigating NoV food borne out-
breaks related to infected food handlers, while this was
possible in 50 % (12 out of 24) of food samples in studies
investigating NoV food borne outbreaks related to pre-
harvest contamination of foods. This difference can be
explained by the fact that NoV detection in ready-to-eat
foods such as catered foods and deli sandwiches is sub-
stantially more difficult compared to fresh produce and
shellfish (Stals et al. 2011a, c). The main reason for this is
the composition of the food products; while fresh produce
is largely composed of carbohydrates and water, ready-to-
eat foods contain a lot of fat and proteins (Baert et al.
2008). As expected, the most frequently detected NoV
genotype in clinical samples was the GII.4 genotype,
although NoV GI.3 was detected in some outbreaks as well
The role of the food handler is considered an important
factor for food borne transmission of NoVs due to several
factors. First of all, it has been stated that an apparent NoV
infection of a food handler should always be reported to
avoid NoV food borne outbreaks and that an infected food
handler should not be at a work place where foods are
manipulated (Joint FAO/WHO Codex Alimentarius Com-
mission and Joint FAO/WHO Food Standards Program
2003; Moe 2008; Vivancos et al. 2009). Since food han-
dlers are often related to large catering establishments,
outbreaks related to this transmission route tend to affect a
lot of people at once (Noda et al. 2008). However, food
handlers returning to work after recovering from a NoV
infection can still shed considerable NoV levels and can
cause NoV food borne outbreaks (Atmar et al. 2008; Malek
et al. 2009). Second, food handlers carrying an asymp-
tomatic NoV infection can easily cause food borne out-
breaks since they can shed similarly high NoV levels
(Ozawa et al. 2007; Phillips et al. 2010). Asymptomatic
NoV infected food handlers manipulating deli sandwiches,
prepared meals, and salad vegetables have caused NoV
food borne outbreaks (Godoy et al. 2005; Ohwaki et al.
2009; Vivancos et al. 2009). Third, poor personal hygiene
has been reported as well (Rizzo et al. 2007; Schmid et al.
2007), often in combination with food handlers suffering
from NoV illness still coming to work (Grotto et al. 2004).
Fourth, lack of respect to hygienic working circumstances
can contribute to NoV food borne outbreaks (Friedman
et al. 2005; Schmid et al. 2007). For example, sinks used
for both washing hands and washing lettuce have been
related to a NoV food borne outbreak (Payne et al. 2006).
Another study reported vomiting of an ill baker in a sink in
138Food Environ Virol (2012) 4:131–152
Table 2 Overview of bovine NoVs detected worldwide
Analysis and results
Age of positive
10 (7.5 %)
(Mauroy et al.
28 (9.3 %)
(Mauroy et al.
25 (18.4 %)
(Zakhour et al.
34 (8.9 %)
(Deng et al.
2 (4.9 %)
(Ike et al. 2007)
4 (8.5 %)
\9 days (3)
(Reuter et al.
6–7 months (1)
1 (3.8 %)
77 (31.6 %)
(van der Poel
et al. 2003)
(D ? N)
13 (4.2 %)
25 (20.8 %)
(van der Poel
et al. 2000)
(D ? N)
208 (49.6 %)
(Jor et al. 2010)
(mean 42 days)
2 (1.9 %)
(Mijovski et al.
38 (8.0 %)
(Oliver et al.
4 months (1)2 cows
Dairy (35 %)
44 (11.1 %)
(Milnes et al.
Beef (65 %)
Food Environ Virol (2012) 4:131–152139
the food preparation area which resulted in NoV contam-
ination of deli sandwiches (De Wit et al. 2007). Finally, an
underestimated factor may be the presence of ill children
and other family members in the food handler’s home
environment. Nevertheless, a few studies have mentioned
this as a risk factor for NoV food borne outbreaks (Boxman
et al. 2007; Daniels et al. 2000).
Food Borne Norovirus Outbreaks in Belgium (2004–2009)
As the current review has been a cooperation between dif-
ferent Belgian laboratories, we were able to review Belgian
NoV food borne outbreaks more into detail with regards to
the possible NoV transmission routes. In Belgium, a con-
vention between the Flemish Community and the National
Reference Laboratory for Food borne Outbreaks (NRL-
FBO) allowed analysis by the latter laboratory of human
samples in suspected NoV food borne outbreaks.
In Belgium, it has been observed that in 20–50 % of the
reported food borne outbreaks the causative agent remains
unknown and it is suspected that NoV could be partially
responsible for these unknown cases. Reasons for this
include a low reporting rate as NoV illness is normally
self-limiting and complications are rare (Greening 2006;
Lopman et al. 2002). Furthermore, analysis of clinical
samples of patients is not reimbursed in Belgium. A NoV
extraction and detection protocol as described by Baert
et al. (2008) and Stals et al. (2011a) was introduced in the
NRL-FBO in 2006. While only six NoV food borne out-
breaks were altogether observed in 2004, 2005, and 2006,
this number increased in 2007 to ten while seven NoV food
borne outbreaks were reported in 2008 and in 2009.
In 2006, two subsequent NoV food borne outbreaks in a
care center for disabled persons were investigated. During
the first episode, 12 persons became ill and NoV GII was
found in a ‘‘witness meal,’’ a food sample that is explicitly
stored for a certain time (usually 72 h to 1 week at 4 ?C or
at -20 ?C) to allow analysis of the food in case of a food
borne outbreak. Four months later, 50 people became ill in
the same institute and a mixture of NoV GI and GII was
found in one of the witness meals analyzed. These sub-
sequent outbreaks are an example of recurring NoV out-
breaks in health care facilities such as nursing homes and
hospitals (Cieslak et al. 2009; Koopmans 2009; Rosenthal
et al. 2011). A third outbreak took place in a hospital where
17 out of 400 people became ill. NoV GII was detected in
the soup and also in five out of six fecal samples and
epidemiological data indicated that an infected food han-
dler distributing the soup could have been at the origin of
this infection. Although soup is not commonly associated
with NoV outbreaks, it has been pointed out as a vehicle
for NoV transmission in a NoV outbreak in a residential-
care facility for the elderly (Medici et al. 2008).
Table 2 continued
Analysis and results
Age of positive
3 (1.6 %)
(Mattison et al.
48 (80.0 %)
(Wise et al.
4 (28.6 %)
258 (72.1 %)
(Smiley et al.
1 (0.9 %)
(Alcala ´ et al.
18 (2.8 %)
(Park et al.
60 (9.3 %)
\365 up to
15 (5.6 %)
(Wolf et al.
Ns not specified, nd not determined, N non diarrheic, D diarrheic
140 Food Environ Virol (2012) 4:131–152
In ten out of the 75 food borne outbreaks reported to the
NRL-FBO during 2007, NoV was confirmed as causative
agent and in total 392 persons were affected. The majority
of outbreaks occurred at work (30 %), camp sites (20 %),
and nursing homes (20 %), and the involvement of a food
handler was suspected in eight outbreaks. Noteworthy, the
NoV presence could be shown in food samples in five out
of ten (50 %) NoV food borne outbreaks demonstrating the
effectiveness of the NoV detection method described by
Baert et al. (2008) and Stals et al. (2011a) on naturally NoV
contaminated food samples such as soup, chicken and rice,
mashed potatoes, meat stew, and a composite meal. The
most important vehicles for NoV transmission were deli
sandwiches as they were involved in four out of ten NoV
food borne outbreaks.
NoV caused seven food borne outbreaks in 2008. In two
outbreaks, deli sandwiches were indicated as vehicles for
NoV transmission. While only fecal samples showed the
NoV presence in a first outbreak affecting 200 people, three
deli sandwich fillings (meatball, cheese, and chicken curry)
and food handler’s fecal sample were found NoV positive
in a second outbreak affecting 15 people. A third outbreak
resulted in NoV illness of 80 people participating at dif-
ferent barbecues. Fecal samples from ill persons in the
latter outbreak tested positive for the NoV presence, but
NoV could not be found in the food. Interestingly, in the
food handler’s family there was a history of gastroenteritis
a week before the barbecues took place, which confirms the
importance of NoV infections in the food handler’s envi-
ronment (Boxman et al. 2007; Daniels et al. 2000).
Finally, in five out of seven NoV food borne outbreaks
in 2009, the NoV presence could only be confirmed in fecal
samples of patients and/or of food handlers. In two out of
seven outbreaks, foods were confirmed as vehicle for NoV
The NoV food borne outbreaks in Belgium confirm
trends that have been observed worldwide. Most impor-
tantly, the majority of NoV food borne outbreaks were
related to infected food handlers, which confirms their
important role in NoV transmission (Moe 2008).
Water Borne Transmission
Transmission of NoV via water can occur by several
routes, although initial contamination is always caused by
discharge of human fecal material (Bosch 1998). NoVs and
NoV surrogate viruses can efficiently attach to lettuce veins
and can internalize lettuce leafs during irrigation. The latter
can lead to NoV contamination of the fresh produce
(Gandhi et al. 2010; Li et al. 2012; Vega et al. 2005, 2008;
Wei et al. 2010, 2011). River water, surface water, and
ground water are frequently used for irrigation of crops
(Knoxet al. 2011;Steeleand Odumeru2004).
Furthermore, people can be infected with NoV via con-
sumption of drinking water or via contact with recreational
surface water (Bosch 1998; Moe et al. 2007). As a thor-
ough overview of water related transmission routes for
NoV and other viral pathogens has been described by
Bosch et al. (1998), the current review will focus specifi-
cally on NoV transmission via river water, ground water,
and surface water. It should be noted that direct compari-
son of studies investigating the NoV presence in water is
difficult, as most studies use different NoV detection
River water is likely to be contaminated with NoV as rivers
are continuously fed with effluents of wastewater treatment
plants, which are optimized for the removal of bacteria
while removal viral pathogens could be less efficient (da
Silva et al. 2007; Hewitt et al. 2011; Maunula et al. 2012;
Ueki et al. 2005). The NoV presence in river water used for
irrigation and used as drinking water has extensively been
investigated in numerous screening worldwide and except
for a single study (La Rosa et al. 2007), the NoV presence
has been shown in all tested rivers (Haramoto et al. 2005;
Jurzik et al. 2010; Laverick et al. 2004; Lee and Kim 2008;
Lodder et al. 2010; Mans et al. 2012; Schets et al. 2008;
Westrell et al. 2006). In some cases, other enteric viruses
such as rotaviruses, enteroviruses, and adenoviruses have
been detected simultaneously (Haramoto et al. 2005; He
et al. 2011; Jurzik et al. 2010; Kishida et al. 2012; Kiulia
et al. 2010; Lodder et al. 2010; Schets et al. 2008).
Regarding the NoV concentrations found in river water
used for irrigation, a broad range of NoV levels can be
present, fluctuating between 12 NoV genomic copies/l and
6.4 9 104NoV genomic copies/l, although most studies
only indicated the presence/absence of NoV in water
(Haramoto et al. 2005; Jurzik et al. 2010; Laverick et al.
2004; Lodder et al. 2010; Westrell et al. 2006). Overall, a
broad range of NoV genotypes have been detected in river
water. While some studies have shown the dominant
presence of the GII.4 genotype (Blanco Fernandez et al.
2011; Lodder et al. 2010), most studies demonstrate the
simultaneous presence of various NoV genotypes such as
GI.4 and GI.5 alongside other less frequently observed
NoV genotypes (La Rosa et al. 2007; Lee and Kim 2008;
Mans et al. 2012). NoV levels in river water depend on
whether sewage and other sources containing human fecal
material is discharged and whether or not the sewage has
been treated (Lodder et al. 2010; Teunis et al. 2009).
Noteworthy, a seasonal variation in NoV levels has been
observed in long-term studies as NoVs were in generally
more frequently observed in winter and early spring (He
et al. 2011; Kishida et al. 2012; Kitajima et al. 2009, 2011;
Food Environ Virol (2012) 4:131–152 141
Pe ´rez-Sautu et al. 2012; Westrell et al. 2006). This sea-
sonality is most likely related to a combination of (i) the
fact that low temperatures are considered a good conser-
vation method for viruses (Baert et al. 2009a) and (ii)
higher prevalence of NoVs in the human population during
winter (Ahmed 2012; Rohayem 2009).
The microbial quality of ground water is in general con-
sidered very good as this water type tends to be cooler, is
protected from sunlight, and has less microbiological and
biological activity (Feachem et al. 1983; Steele and
Odumeru 2004). Nevertheless, several studies have inves-
tigated the presence of NoV and other enteric viruses in
this water type (Barthe et al. 2007; Cheong et al. 2009;
Gabrieli et al. 2009; Jung et al. 2011; Lee et al. 2011; Locas
et al. 2008). Although some studies did not find NoV in
well water, (Cheong et al. 2009; Locas et al. 2008), most
studies did demonstrate the NoV presence in various
ground water sources. A study investigating Italian ground
water sources found 15 % of sources positive (Gabrieli
et al. 2009), while 18–42 % of samples from Korean
ground water wells tested positive for NoV (Jung et al.
2011; Lee et al. 2011). Similar to the NoV screenings in
river water, a broad range of NoV genotypes has been
found in ground water screenings (Gabrieli et al. 2009; Lee
et al. 2011). Seasonality of the NoV presence and NoV
levels in ground water is not a thoroughly investigated
topic, although Westrell et al. (2006) demonstrated a clear
absence and the presence of NoV in summer and winter
months, respectively. On the other hand, another long-term
study did not find such an explicit seasonality (Lee et al.
2011). Further research is, therefore, needed to see whether
NoVs display a similar seasonal pattern as enteroviruses,
rotaviruses, and hepatitis A virus in ground water (Abba-
szadegan et al. 2003). Regarding the use of fecal indicator
organisms, no significant correlation could be shown in any
study investigating the NoV presence in ground water.
While some studies found the NoV presence despite the
absence of indicator organisms (Barthe et al. 2007; Gabrieli
et al. 2009), other studies did find indicator organisms such
as E. coli and coliphages but they were not related to the
NoV presence (Cheong et al. 2009; Jung et al. 2011).
However, a recent study showed that a combination of
different fecal indicators may be helpful, but that further
research is needed to support this observation (Lee et al.
Several NoV outbreaks have been related to contami-
nated ground water. NoV GI.3 has been found in fecal
samples and in ground water related to a NoV water borne
outbreak affecting at least 84 people in Wyoming, USA
(Parshionikar et al. 2003). In a water borne gastroenteritis
outbreak involving bacterial and viral pathogens, 21 % of
all fecal samples tested NoV positive, although ground
water as cause of the outbreak could only be determined by
epidemiological data (Gallay et al. 2006).
Surface waters (e.g., lakes, bays, and recreational water)
are a known transmission route for NoV, as an overview of
water borne outbreaks between 2001 and 2004 associated
with surface water showed that NoV was the responsible
pathogen in 39.2 % of outbreaks with a confirmed etiology
(Dziuban et al. 2006; Yoder et al. 2004). Overall, only a
limited number of studies have investigated the NoV
presence in surface water. A Finnish study found 1 out of 7
investigated lakes positive for NoV between 2000 and
2001, while 50 % of samples from an estuarine bay in
Singapore tested positive for NoV (Aw et al. 2009; Horman
et al. 2004). Similar to drinking water and ground water,
fecal and chemical indicators have not been related to NoV
contamination of surface water (Horman et al. 2004).
The existence of a zoonotic reservoir for human infective
NoV has been investigated, but zoonotic transmission of
human infective NoV has thus far never been proven (Li
2012). Nevertheless, the detection of human infective NoV
in animal species in close contact with human beings raises
suspicion for cross-species or zoonotic transmission and for
the existence of an animal reservoir for human infective
NoV (Mattison et al. 2007; Scipioni et al. 2008). Therefore,
the animal and human infective NoV presence studies have
been performed in different animals and an overview of
these studies, based on the molecular detection of NoVs in
feces from cattle and pigs, is presented in Tables 2 and 3,
respectively. As the current review involved cooperation of
a number of Belgian laboratories investigating animal
NoV, we were able to compare Belgian data to worldwide
observations. For the Belgian perspective, diarrheic fecal
samples from domestic animals were screened for the NoV
presence between 2007 and 2008. NoV sequences were
detected in various animal types. While animal NoV were
found in cattle and pigs, all other domestic animal samples
(poultry, sheep, equine, cats, and dogs) tested negative
(Axel Mauroy, personal communication).
In Belgium, 7.5 % (in 2007) and 9.3 % (in 2008) of
feces samples coming from diarrheic calves and young
stock tested positive for the presence of bovine NoVs, with
NoV GIII.2 being by far the most prevalent genotype in
both studies (Mauroy et al. 2009a, b).
This data were in accordance with previously published
studies from the United Kingdom, Hungary, Germany, and
142Food Environ Virol (2012) 4:131–152
Table 3 Overview of porcine NoVs detected worldwide
Age of positive
43 (D ? N)
2 (4.6 %)
(Mauroy et al. 2008)
17 (D ? N)
1 (5.9 %)
(Reuter et al. 2007)
2 (2.0 %)
(van der Poel et al. 2000)
\21 up to
5 (1.2 %)
1 nursery3 finisher
(Mijovski et al. 2010)
96 (D ? N)
1 (1.1 %)
(Cunha et al. 2010)
30 (25.0 %)
(Mattison et al. 2007)
\28 up to
5/20 (20.0 %)
(L’Homme et al. 2009)
3/66 (4.5 %)
2 abattoirs [84
70 up to
19 (6.9 %)
(Wang et al. 2005b)
6 (2.2 %)
621 (D ? N)
64 (10.3 %)
(Wang et al. 2006)
20 % of finishers
\30 up to
2 (0.2 %)2
(Shen et al. 2009)
4 (0.4 %)
(Sugieda et al. 1998)
24 (D ? N)
1 (4.2 %)
(Yin et al. 2006)
42 (17.5 %)
(Nakamura et al. 2010)
10 (1.9 %)
(Keum et al. 2009)
2 (8.7 %)
(Wolf et al. 2009)
Ns not specified, nd not determined, N non diarrheic, D diarrheic
Food Environ Virol (2012) 4:131–152143
South Korea (Table 2) although other epidemiological data
available from calf farms in industrialized countries indi-
cated NoV prevalence ranging from 1.6 to 72 %. Similar to
the Belgian results, a majority of NoV GIII.2 was also
observed in most studies which may support the idea of the
existence of predominating NoV genotypes that dispose of
advantages upon other genotypes similar to what has been
observed for GII.4 NoVs in humans (Kroneman et al. 2008;
Siebenga et al. 2007; Verhoef et al. 2010, 2009). Interest-
ingly, a single Belgian cattle sample showed a GIII.1/
GIII.2 co-infection while a potential recombinant strain
between NoV GIII.1 and NoV GIII.2 was found in another
sample. This recombinant strain was closely related to a
previously described strain NoV GIII Thirsk in British and
Norwegian cattle (Jor et al. 2010; Oliver et al. 2004).
A 3 month survey found 4.6 % of Belgian pigs positive
for porcine NoVs in 2007 (Mauroy et al. 2008). Although
studies conducted in other industrialized countries found
the NoV presence in pigs ranging between 0.2 and 25 %,
Belgian results are congruent with data from Hungarian,
Canadian, and Japanese pigs. Both NoV strains detected in
Belgium clustered within the NoV GII.19 genotype. To
date, porcine NoVs cluster into three GII genotypes and all
three genotypes have been detected in Europe, America,
and Asia (Wang et al. 2005b).
Worldwide and in Belgium, bovine and porcine NoV are
widely endemic in their respective hosts, although data
diverges greatly between studies (Tables 2, 3). These dis-
parities observed could be explained by the use of different
detection methods, the use of internal amplification con-
trols for the detection of false negative results and different
The clinical impact of bovine NoVs included watery
often causes an asymptomatic infection (Scipioni et al.
2008). Porcine NoV has exclusively been detected in fecal
2008; Sugieda et al. 1998; van der Poel et al. 2000; Wang
et al. 2005a). Finally, murine NoVs cause a mild gastroen-
teritis in mice (Liu et al. 2009a; Thackray et al. 2007).
Noteworthy, multiple studies have already carefully sug-
gested that recombination of porcine and human infective
could be a hypothetical zoonotic transmission route (Bull
et al. 2007; Phan et al. 2007; Wang et al. 2005a). Similarly,
recombination between canine and human infective GIV
needed to confirm whether this could lead to zoonotic
transmission of NoV. Interestingly, recombination on the
ORF1/ORF2junction hasalso been observedamongmurine
NoVs (Matthijs et al. 2010).
Regarding the infection of animals with human infective
NoV, several studies have demonstrated that this is
possible in non-human primates, pigs, and pet dogs,
resulting in no clinical symptoms to very mild gastroen-
teritis (Bok et al. 2011; Rockx et al. 2005; Summa et al.
2012b; Takanashi et al. 2011). On the other hand, anti-
bodies for bovine NoVs have been detected in veterinarians
and in the general population (Widdowson et al. 2005a).
However, the number of studies investigating cross infec-
tion of animal and human infective NoV are limited and
further research is needed to see whether human infective
NoV can indeed be spread via animals.
Development of methods for molecular detection of human
and animal infective NoVs has confirmed NoV transmis-
sion routes that were suspected by investigating NoV
outbreaks before sequencing of the NoV genome (Green-
berg et al. 1979; Gunn et al. 1982; Koopman et al. 1982;
Sekla et al. 1989; White et al. 1986). Person-to-person
transmission of NoVs is by far the dominant transmission
route, but food and water borne transmission are also fre-
quently observed transmission routes. A strategy to reduce
or even prevent person-to-person transmission (and NoV
transmission in general) could be the development of a
NoV vaccine, based on the use of virus-like particles
containing capsid antigens. Some hurdles such as long-
term immunity and the need for immunity against multiple
NoV genotypes exist, but comprehensive strain surveil-
lance e.g., via web-based open-access genotyping tools
www.noronet.nl/noronet) and the use of multivalent vac-
cines may be a suitable approach for a vaccine develop-
ment (Atmar et al. 2011; LoBue et al. 2006; Vinje 2010).
Transmission of NoV by food handlers can easily lead to a
NoV gastroenteritis outbreak. Both the Codex Alimentarius
(2003) and the Food Code (2009) state that food handlers
suffering from NoV gastroenteritis should not be allowed
on the food preparation and handling areas. However,
transmission of NoV via asymptomatic infected food
handlers or via food handlers recovering from NoV gas-
troenteritis could be severely reduced by applying and
respecting intervention measures (Mokhtari and Jaykus
2009). Regarding an approach to prevent NoV food borne
outbreaks caused by pre-harvest contamination of bivalve
molluscan shellfish, a critical limit has been suggested
(Lowther et al. 2012), although both economical and public
health aspects should be kept in mind (Anonymous 2012).
The use of sensitive molecular NoV detection methods has
shown that a substantial fraction of fresh produce can be
contaminated with NoV while no associated NoV illness
was reported (Baert et al. 2011). A possible solution could
be confirmation of real-time PCR results using a different
suchas Noronet (http://
144Food Environ Virol (2012) 4:131–152
molecular detection assay (e.g., different primers and
probes) (Baert et al. 2011). Furthermore, NoV can effec-
tively be spread via water and has resulted in several NoV
water borne outbreaks (Maunula 2006). As most water
treatment plants are designed for removal of bacterial
pathogens, NoV can still be present in treated wastewater
(Katayama et al. 2008; Laverick et al. 2004; Rodriguez-
Lazaro et al. 2011; van den Berg et al. 2005). However,
further research is needed to determine whether novel
methods can sufficiently reduce the NoV presence in dif-
ferent water types (Springthorpe and Sattar 2007).
Regarding the role of animal NoVs, molecular detection
coupled with DNA sequencing has allowed numerous
molecular epidemiological studies of NoVs in humans and
in animals (Tables 2, 3). These studies have led to the
conclusion that NoV zoonotic transmission is unlikely to
happen although it cannot be excluded.
ject, funded by the Belgian policy ‘‘Science for a Sustainable
Development’’ (contract SD/AF/01). Furthermore, this work was
supported by the Federal Public Service for Health, Food chain and
Environment, Grant RT 10/6 (TRAVIFOOD), and by the Special
Research Fund of the Ghent University.
The authors are partners of the NORISK pro-
Abbaszadegan, M., LeChevallier, M., & Gerba, C. (2003). Occur-
rence of viruses IN US groundwaters. American Water Works
Journal, 95(9), 107–120.
Ahmed, S. M. (2012). The global seasonality of norovirus gastroen-
teritis. Master’s thesis.
Alcala ´, A. C., Hidalgo, M. A., Obando, C., Vizzi, E., Liprandi, F., &
Ludert, J. E. (2003). Molecular identification of bovine enteric
caliciviruses in Venezuela. Acta Cientifica Venezolana, 54(2),
Anderson, A. D., Garrett, V. D., Sobel, J., Monroe, S. S., Fankhauser,
R. L., Schwab, K. J., et al. (2001). Multistate outbreak of
Norwalk-like virus gastroenteritis associated with a common
Anonymous. (2000). Appendix B guidelines for confirmation of
foodborne-disease outbreaks. Morbidity and Mortality Weekly
Report, 49(SS01), 54–62.
Anonymous. (2009). FDA: Food code 2009. U.S. Public Health
Service FDA, http://www.fda.gov/downloads/Food/FoodSafety/
Anonymous. (2010). Manual for the reporting of food-borne
outbreaks in the framework of directive 2003/99/EC from the
reporting year 2009. EFSA Journal, 8(4), 1578.
Anonymous. (2012). Scientific opinion on norovirus (NoV) in oysters:
methods, limits and control options. EFSA Journal, 10(1), 2500.
Aoki, Y., Suto, A., Mizuta, K., Ahiko, T., Osaka, K., & Matsuzaki, Y.
(2010). Duration of norovirus excretion and the longitudinal
course of viral load in norovirus-infected elderly patients.
Journal of Hospital Infection, 75(1), 42–46.
Atmar, R. L., Bernstein, D. I., Harro, C. D., Al-Ibrahim, M. S., Chen,
W. H., Ferreira, J., et al. (2011). Norovirus vaccine against
experimental human Norwalk virus illness. New England
Journal of Medicine, 365(23), 2178–2187.
Atmar, R. L., Opekun, A. R., Gilger, M. A., Estes, M. K., Crawford,
S. E., Neill, F. H., et al. (2008). Norwalk virus shedding after
experimental human infection. Emerging Infectious Diseases,
Aw, T. G., Gin, K. Y.-H., Ean Oon, L. L., Chen, E. X., & Woo, C. H.
(2009). Prevalence and genotypes of human noroviruses in
tropical urban surface waters and clinical samples in Singapore.
Applied and Environmental Microbiology, 75(15), 4984–4992.
Baert, L., Debevere, J., & Uyttendaele, M. (2009a). The efficacy of
preservation methods to inactivate foodborne viruses. Interna-
tional Journal of Food Microbiology, 131(2–3), 83–94.
Baert, L., Mattison, K., Loisy-Hamon, F., Harlow, J., Martyres, A.,
Lebeau, B., et al. (2011). Review: Norovirus prevalence in
Belgian, Canadian and French fresh produce: A threat to human
health? International Journal of Food Microbiology, 151(3),
Baert, L., Uyttendaele, M., & Debevere, J. (2008). Evaluation of viral
extraction methods on a broad range of Ready-To-Eat foods with
conventional and real-time RT-PCR for Norovirus GII detection.
International Journal of Food Microbiology, 123(1–2), 101–108.
Baert, L., Uyttendaele, M., Stals, A., Van Coillie, E., Dierick, K.,
Debevere, J., et al. (2009b). Reported foodborne outbreaks due
to noroviruses in Belgium: The link between food and patient
investigations in an international context. Epidemiology and
Infection, 137(3), 316–325.
Barthe, C., Locas, A., Barbeau, B., Carriere, A., & Payment, P.
(2007). Virus occurrence in municipal groundwater sources in
Quebec, Canada. Canadian Journal of Microbiology, 53(6),
Becker, K. M., Moe, C. L., Southwick, K. L., & MacCormack, J. N.
(2000). Transmission of Norwalk virus during a football game.
New England Journal of Medicine, 343(17), 1223–1227.
Blanco Fernandez, M. D., Torres, C., Martinez, L. C., Giordano,
M. O., Masachessi, G., Barril, P. A., et al. (2011). Genetic and
evolutionary characterization of norovirus from sewage and
surface waters in Cordoba City, Argentina. Infection, Genetics
and Evolution, 11(7), 1631–1637.
Bohm, S. R., Brennan, B. M., Schirmer, R., & Cabose, G. (2008).
Norovirus outbreak associated with ill food-service workers:
Michigan, January–February 2006 (Reprinted MMWR, vol 56,
pg 1212–1216, 2007). Journal of the American Medical
Association, 299(2), 164–166.
Bok, K., Abente, E. J., Realpe-Quintero, M., Mitra, T., Sosnovtsev,
S. V., Kapikian, A. Z., et al. (2009). Evolutionary dynamics of
GII. 4 Noroviruses over a thirty-four year period. Journal of
Virology, 83(22), 11890–11901.
Bok, K., Parra, G. I., Mitra, T., Abente, E., Shaver, C. K., Boon, D.,
et al. (2011). Chimpanzees as an animal model for human
norovirus infection and vaccine development. Proceedings of the
National Academy of Sciences, 108(1), 325–330.
Bosch, A. (1998). Human enteric viruses in the water environment: A
minireview. International Microbiology, 1(3), 191–196.
Boxman, I. L. A., Tilburg, J. J. H. C., Loeke, N. A. J. M., Vennema,
H., de Boer, E., & Koopmans, M. (2007). An efficient and rapid
method for recovery of norovirus from food associated with
outbreaks of gastroenteritis. Journal of Food Protection, 70(2),
Boxman, I. L. A., Tilburg, J. J. H. C., Te Loeke, N. A. J. M.,
Vennema, H., Jonker, K., de Boer, E., et al. (2006). Detection of
noroviruses in shellfish in the Netherlands. International Journal
of Food Microbiology, 108(3), 391–396.
Bridger, J. C. (1980). Detection by electron microscopy of caliciv-
iruses, astroviruses and rotavirus-like particles in the faeces of
Food Environ Virol (2012) 4:131–152 145
piglets with diarrhoea. The Veterinary Record, 107(23),
Bull, R. A., Eden, J. S., Rawlinson, W. D., White, P. A. (2010). Rapid
evolution of pandemic Noroviruses of the GII.4 Lineage. PLoS
Pathogens, 6(3), e-1000831.
Bull, R. A., Tanaka, M. M., & White, P. A. (2007). Norovirus
recombination. Journal of General Virology, 88(12), 3347–3359.
Bull, R. A., & White, P. A. (2011). Mechanisms of GII. 4 norovirus
evolution. Trends in Microbiology, 19(5), 233–240.
Cheong, S., Lee, C., Song, S. W., Choi, W. C., Lee, C. H., & Kim,
S. J. (2009). Enteric viruses in raw vegetables and groundwater
used for irrigation in South Korea. Applied and Environmental
Microbiology, 75(24), 7745–7751.
Cieslak, P. R., Lee, L. E., Papafragkou, E., & An, N. (2009).
Recurring norovirus outbreaks in a long-term residential treat-
ment facility-Oregon, 2007. Morbidity and Mortality Weekly
Report, 58(25), 694–698.
Costas, L., Vilella, A., Llupia, A., Bosch, J., de Jimenez Anta, M. T.,
& Trilla, A. (2007). Outbreak of norovirus gastroenteritis among
staff at a hospital in Barcelona, Spain, September 2007. Euro
Surveillance, 12(11), E071122.5.
Cotterelle, B., Drougard, C., Rolland, J., Becamel, M., Boudon, M.,
Pinede, S., et al. (2005). Outbreak of norovirus infection
associated with the consumption of frozen raspberries, France,
March 2005. Euro Surveillance, 10(17), E050428.1.
Croci, L., Losio, M. N., Suffredini, E., Pavoni, E., Di Pasquale, S.,
Fallacara, F., et al. (2007). Assessment of human enteric viruses
in shellfish from the northern Adriatic sea. International Journal
of Food Microbiology, 114(2), 252–257.
Cunha, J. B., De Mendonc ¸a, M. C. L., Miagostovich, M. P., & Leite,
J. P. G. (2010). Genetic diversity of porcine enteric caliciviruses
in pigs raised in Rio de Janeiro State, Brazil. Archives of
Virology, 155(8), 1301–1305.
da Silva, A. K., Le Saux, J. C., Parnaudeau, S., Pommepuy, M.,
Elimelech, M., & Le Guyader, F. S. (2007). Evaluation of
removal of noroviruses during wastewater treatment, using real-
time reverse transcription-PCR: Different behaviors of geno-
groups I and II. Applied and Environmental Microbiology,
Daniels, N. A., Bergmire-Sweat, D. A., Schwab, K. J., Hendricks,
K. A., Reddy, S., Rowe, S. H., et al. (2000). A foodborne outbreak
of gastroenteritis associated with Norwalk-like viruses: First
molecular traceback to deli sandwiches contaminated during
preparation. Journal of Infectious Diseases, 181(4), 1467–1470.
David, S. T., McIntyre, L., MacDougall, L., Kelly, D., Liem, S.,
Schallie, K., et al. (2007). An outbreak of norovirus caused by
consumption of oysters from geographically dispersed harvest
sites, British Columbia, Canada, 2004. Foodborne Pathogens
and Disease, 4(3), 349–358.
de Coster, E., de Wit, M., & Widdowson, M. (2001). Large outbreak
of Norwalk-like virus in ministry staff in the Netherlands. Euro
Surveillance, 5(1), 1–2.
De Wit, M. A. S., Widdowson, M. A., Vennema, H., de Bruin, E.,
Fernandes, T., & Koopmans, M. (2007). Large outbreak of
norovirus: The baker who should have known better. Journal of
Infection, 55(2), 188–193.
Deng, Y., Batten, C. A., Liu, B. L., Lambden, P. R., Elschner, M.,
Gu ¨nther, H., et al. (2003). Studies of epidemiology and
seroprevalence of bovine noroviruses in Germany. Journal of
Clinical Microbiology, 41(6), 2300–2305.
Dippold, L., Lee, R., Selman, C., Monroe, S., & Henry, C. (2003). A
gastroenteritis outbreak due to norovirus associated with a
Colorado hotel. Journal of Environmental Health, 66(5), 13–26.
Dziuban, E. J., Liang, J. L., Craun, G. F., Hill, V., Yu, P. A., Painter,
J., et al. (2006). Surveillance for waterborne disease and
outbreaks associated with recreational water—United States,
2003–2004. Morbidity and Mortality Weekly Report, 55(12),
Escudero, B. I., Rawsthorne, H., Gensel, C., & Jaykus, L. A. (2012).
Persistence and transferability of noroviruses on and between
common surfaces and foods. Journal of Food Protection, 75(5),
Ethelberg, S., Lisby, M., Bottiger, B., Schultz, A. C., Villif, A.,
Jensen, T., et al. (2010). Outbreaks of gastroenteritis linked to
lettuce, Denmark, January 2010. Eurosurveillance, 15(6), 2–4.
Falkenhorst, G., Krusell, L., Lisby, M., Madsen, S. B., Bottiger, B., &
Molbak, K. (2005). Imported frozen raspberries cause a series of
norovirus outbreaks in Denmark, 2005. Euro Surveillance, 10(9),
Feachem, R., Mara, D. D., & Bradley, D. J. (1983). Sanitation and
disease: Health aspects of excreta and wastewater management
(p. 294). Dorchester: Wiley.
Fretz, R., Svoboda, P., Luthi, T. M., Tanner, M., & Baumgartner, A.
(2005). Outbreaks of gastroenteritis due to infections with
Norovirus in Switzerland, 2001–2003. Epidemiology and Infec-
tion, 133(3), 429–437.
Friedman, D. S., Heisey-Grove, D., Argyros, F., Berl, E., Nsubuga, J.,
Stiles, T., et al. (2005). An outbreak of norovirus gastroenteritis
associated with wedding cakes. Epidemiology and Infection,
Gabrieli, R., Maccari, F., Ruta, A., Pana, A., & Divizia, M. (2009).
Norovirus detection in groundwater. Food and Environmental
Virology, 1(2), 92–96.
Gallay, A., De Valk, H., Cournot, M., Ladeuil, B., Hemery, C.,
Castor, C., et al. (2006). A large multi-pathogen waterborne
community outbreak linked to faecal contamination of a
groundwater system, France, 2000. Clinical Microbiology and
Infection, 12(6), 561–570.
Gallimore, C. I., Barreiros, M. A. B., Brown, D. W. G., Nascimento,
J. P., & Leite, J. P. G. (2004a). Noroviruses associated with acute
gastroenteritis in a children’s day care facility in Rio de Janeiro,
Brazil. Brazilian Journal of Medical and Biological Research,
Gallimore, C. I., Cheesbrough, J. S., Lamden, K., Bingham, C., Graya,
J. J., & Gray, J. J. (2005). Multiple norovirus genotypes character-
ised from an oyster-associated outbreak of gastroenteritis. Interna-
tional Journal of Food Microbiology, 103(3), 323–330.
Gallimore, C. I., Cubitt, D., Du Plessis, N., & Gray, J. J. (2004b).
Asymptomatic and symptomatic excretion of noroviruses during
a hospital outbreak of gastroenteritis. Journal of Clinical
Microbiology, 42(5), 2271–2274.
Gandhi, K. M., Mandrell, R. E., & Tian, P. (2010). Binding of virus-
like particles of Norwalk virus to romaine lettuce veins. Applied
and Environmental Microbiology, 76(24), 7997–8003.
Glasscock, S., Welch, J., Dailer, J., Elmer, W., Kline, K., del Rosario,
M., et al. (2007). Multistate outbreak of norovirus gastroenteritis
among attendees at a family reunion—Grant County, West
Virginia, October 2006. Morbidity and Mortality Weekly Report,
(2005). Outbreak of food-borne Norovirus associated with the
consumption of sandwiches. Medicina Clinica, 124(5), 161–164.
Green, K. Y., Ando, T., Balayan, M. S., Berke, T., Clarke, I. N., Estes,
M. K., et al. (2000). Taxonomy of the caliciviruses. Journal of
Infectious Diseases, 181, S322–S330.
Greenberg, H. R., Valdesuso, J., Yolken, R. H., Gangarosa, E., Gary,
W., Wyatt, R. G., et al. (1979). Role of Norwalk virus in
outbreaks of nonbacterial gastroenteritis. Journal of Infectious
Diseases, 139(5), 564–568.
Greening, G. E. (2006). Human and animal viruses in food (including
taxonomy of enteric viruses). In S. M. Goyal (Ed.), Viruses in
foods (p. 5). New York: Springer.
146Food Environ Virol (2012) 4:131–152
Grotto, I., Huerta, M., Balicer, R. D., Halperin, T., Cohen, D., Orr, N.,
et al. (2004). An outbreak of norovirus gastroenteritis on an
Israeli military base. Infection, 32(6), 339–343.
Gunn, R. A., Janowski, H. T., Lieb, S. P. E. N., Prather, E. C., &
Greenberg, H. B. (1982). Norwalk virus gastroenteritis following
raw oyster consumption. American Journal of Epidemiology,
Haramoto, E., Katayama, H., Oguma, K., & Ohgaki, S. (2005).
Application of cation-coated filter method to detection of
noroviruses, enteroviruses, adenoviruses, and torque teno viruses
in the Tamagawa River in Japan. Applied and Environmental
Microbiology, 71(5), 2403–2411.
He, X., Wei, Y., Cheng, L., Zhang, D., & Wang, Z. (2011). Molecular
detection of three gastroenteritis viruses in urban surface waters
in Beijing and correlation with levels of fecal indicator bacteria.
Environmental Monitoring and Assessment, 184(9), 5563–5570.
Hewitt, J., Leonard, M., Greening, G. E., & Lewis, G. D. (2011).
Influence of wastewater treatment process and the population
size on human virus profiles in wastewater. Water Research,
Hirakata, Y., Arisawa, K., Nishio, O., & Nakagomi, O. (2005).
Multiprefectural spread of gastroenteritis outbreaks attributable
to a single genogroup II norovirus strain from a tourist restaurant
in Nagasaki, Japan. Journal of Clinical Microbiology, 43(3),
Hjertqvist, M., Johansson, A., Svensson, N., Abom, P. E., Magnusson,
C., Olsson, M., et al. (2006). Four outbreaks of norovirus
gastroenteritis after consuming raspberries, Sweden, June–
August 2006. Euro Surveillance, 11(9), E060907.1.
Horman, A., Rimhanen-Finne, R., Maunula, L., von Bonsdorff, C. H.,
Torvela, N., Heikinheimo, A., et al. (2004). Campylobacter spp.,
Giardia spp., Cryptosporidium noroviruses and indicator organ-
isms in surface water in southwestern Finland, 2000–2001.
Applied and Environmental Microbiology, 70(1), 87–95.
Ike, A. C., Roth, B. N., Bo ¨hm, R., Pfitzner, A. J., & Marschang, R. E.
(2007). Identification of bovine enteric Caliciviruses (BEC) from
cattle in Baden-Wu ¨rttemberg. DTW. Deutsche Tierarztliche
Wochenschrift, 114(1), 12–15.
Johansson, P. J. H., Torven, M., Hammarlund, A. C., Bjorne, U.,
Hedlund, K. O., & Svensson, L. (2002). Food-borne outbreak of
gastroenteritis associated with genogroup I calicivirus. Journal
of Clinical Microbiology, 40(3), 794–798.
Joint FAO/WHO Codex Alimentarius Commission, & Joint FAO/
WHO Food Standards Program. (2003). Codex alimentarius:
Food hygiene, basic texts.
Jor, E., Myrmel, M., & Jonassen, C. M. (2010). SYBR Green based
real-time RT-PCR assay for detection and genotype prediction of
bovine noroviruses and assessment of clinical significance in
Norway. Journal of Virological Methods, 169(1), 1–7.
Jung, J. H., Yoo, C. H., Koo, E. S., Kim, H. M., Na, Y., Jheong,
W. H., et al. (2011). Occurrence of norovirus and other enteric
viruses in untreated groundwaters of Korea. Journal of Water
and Health, 9(3), 544–555.
Jurzik, L., Hamza, I. A., Puchert, W., U¨berla, K., & Wilhelm, M.
(2010). Chemical and microbiological parameters as possible
indicators for human enteric viruses in surface water. Interna-
tional Journal of Hygiene and Environmental Health, 213(3),
Kapikian, A. Z., Wyatt, R. G., Dolin, R., Thornhill, T. S., Kalica,
A. R., & Chanock, R. M. (1972). Visualization by immune
electron microscopy of a 27-nm particle associated with acute
infectious nonbacterial gastroenteritis. Journal of Virology,
Katayama, H., Haramoto, E., Oguma, K., Yamashita, H., Tajima, A.,
Nakajima, H., et al. (2008). One-year monthly quantitative
survey of noroviruses, enteroviruses, and adenoviruses in
wastewater collected from six plants in Japan. Water Research,
Keum, H., Moon, H., Park, S., Kim, H., Rho, S., & Park, B. (2009).
Porcine noroviruses and sapoviruses on Korean swine farms.
Archives of Virology, 154(11), 1765–1774.
Kiehl, W., Schreier, E., Twisselman, B., & Wunderle, W. (2001).
Outbreak of Norwalk-like infection in Germany. Eurosurveil-
lance, 5(15), 1.
Kingsley, D. H., Meade, G. K., & Richards, G. P. (2002). Detection of
both hepatitis A virus and Norwalk-like virus in imported clams
associated with food-borne illness. Applied and Environmental
Microbiology, 68(8), 3914–3918.
Kishida, N., Morita, H., Haramoto, E., Asami, M., & Akiba, M.
(2012). One-year weekly survey of noroviruses and enteric
adenoviruses in the Tone River water in Tokyo metropolitan
area, Japan. Water Research, 46(9), 2905–2910.
Kitajima, M., Haramoto, E., Phanuwan, C., Katayama, H., & Ohgaki,
S. (2009). Detection of genogroup IV norovirus in wastewater
and river water in Japan. Letters in Applied Microbiology, 49(5),
Kitajima, M., Oka, T., Haramoto, E., Phanuwan, C., Takeda, N.,
Katayama, K., et al. (2011). Genetic diversity of genogroup IV
noroviruses in wastewater in Japan. Letters in Applied Micro-
biology, 52(2), 181–184.
Kiulia, N. M., Netshikweta, R., Page, N. A., van Zyl, W. B., Kiraithe,
M. M., Nyachieo, A., et al. (2010). The detection of enteric
viruses in selected urban and rural river water and sewage in
Kenya, with special reference to rotaviruses. Journal of Applied
Microbiology, 109(3), 818–828.
Knox, J. W., Tyrrel, S. F., Daccache, A., & Weatherhead, E. K.
(2011). A geospatial approach to assessing microbiological
water quality risks associated with irrigation abstraction. Water
and Environment Journal, 25(2), 282–289.
Koopman, J. S., Eckert, E. A., Greenberg, H. B., Strohm, B. C.,
Isaacson, R. E., & Monto, A. S. (1982). Norwalk virus enteric
illness acquired by swimming exposure. American Journal of
Epidemiology, 115(2), 173–177.
Koopmans, M. (2009). Noroviruses in healthcare settings: A
challenging problem. Journal of Hospital Infection, 73(4),
Koopmans, M., & Duizer, E. (2004). Foodborne viruses: An emerging
problem. International Journal of Food Microbiology, 90(1),
Kroneman, A., Vennema, H., Deforche, K., Avoort, H. V. D.,
Penaranda, S., Oberste, M. S., et al. (2011). An automated
genotyping tool for enteroviruses and noroviruses. Journal of
Clinical Virology, 51(2), 121–125.
Kroneman, A., Verhoef, L., Harris, J., Vennema, H., Duizer, E., van
Duynhoven, Y., et al. (2008). Analysis of integrated virological
and epidemiological reports of norovirus outbreaks collected
within the Foodborne Viruses in Europe Network from 1 July
2001 to 30 June 2006. Journal of Clinical Microbiology, 46(9),
Kuo, H. W., Schmid, D., Jelovcan, S., Pichler, A. M., Magnet, E.,
Reichart, S., et al. (2009). A foodborne outbreak due to
Norovirus in Austria, 2007. Journal of Food Protection, 72(1),
La Rosa, G., Fontana, S., Di Grazia, A., Iaconelli, M., Pourshaban,
M., & Muscillo, M. (2007). Molecular identification and genetic
analysis of norovirus genogroups I and II in water environments:
Comparative analysis of different reverse transcription-PCR
assays (vol 73, pg 4152). Applied and Environmental Microbi-
ology, 73(19), 6329.
Lamhoujeb, S., Fliss, I., Ngazoa, S. E., & Jean, J. (2009). Molecular
study of the persistence of infectious human Norovirus on food-
contact surfaces. Food and Environmental Virology, 1(2), 51–56.
Food Environ Virol (2012) 4:131–152147
Laverick, M. A., Wyn-Jones, A. P., & Carter, M. J. (2004).
Quantitative RT-PCR for the enumeration of noroviruses
(Norwalk-like viruses) in water and sewage. Letters in Applied
Microbiology, 39(2), 127–136.
Le Guyader, F. S., Bon, F., DeMedici, D., Parnaudeau, S., Bertone,
A., Crudeli, S., et al. (2006). Detection of multiple noroviruses
associated with an international gastroenteritis outbreak linked to
oyster consumption. Journal of Clinical Microbiology, 44(11),
Le Guyader, F. S., Le Saux, J. C., Ambert-Balay, K., Krol, J., Serais,
O., Parnaudeau, S., et al. (2008). Aichi virus, norovirus,
astrovirus, enterovirus, and rotavirus involved in clinical cases
from a French oyster-related gastroenteritis outbreak. Journal of
Clinical Microbiology, 46(12), 4011–4017.
Le Guyader, F. S., Mittelholzer, C., Haugarreau, L., Hedlund, K. O.,
Alsterlund, R., Pommepuy, M., et al. (2004). Detection of norovi-
ruses in raspberries associated with a gastroenteritis outbreak.
International Journal of Food Microbiology, 97(2), 179–186.
Le Guyader, F. S., Neill, F. H., Dubois, E., Bon, F., Loisy, F., Kohli,
E., et al. (2003). A semiquantitative approach to estimate
Norwalk-like virus contamination of oysters implicated in an
outbreak. International Journal of Food Microbiology, 87(1–2),
Lederer, I., Schmid, D., Pichler, A. M., Dapra, R., Kraler, P.,
Blassnig, A., et al. (2005). Outbreak of norovirus infections
associated with consuming food from a catering company,
Austria, September 2005. Euro Surveillance, 10(10), E051020.7.
Lee, N., Chan, M. C. W., Wong, B., Choi, K. W., Sin, W., Lui, G.,
et al. (2007). Fecal viral concentration and diarrhea in norovirus
gastroenteritis. Emerging Infectious Diseases, 13(9), 1399–1401.
Lee, C., & Kim, S. J. (2008). The genetic diversity of human
noroviruses detected in river water in Korea. Water Research,
Lee, H., Kim, M., Lee, J. E., Lim, M. Y., Kim, M. J., Kim, J. M., et al.
(2011). Investigation of norovirus occurrence in groundwater in
metropolitan Seoul, Korea. Science of the Total Environment,
L’Homme, Y., Sansregret, R., Plante-Fortier, E., Lamontagne, A. M.,
Ouardani, M., Lacroix, G., et al. (2009). Genomic characteriza-
tion of swine caliciviruses representing a new genus of
Caliciviridae. Virus Genes, 39(1), 66–75.
Li, J. (2012). New interventions against human Norovirus: Pro-
gresses, challenges, and opportunities. Annual Review of Food
Science and Technology, 3(1), 331–352.
Li, D., Baert, L., Xia, M., Zhong, W., Jiang, X., & Uyttendaele, M.
(2012). Effects of a variety of food extracts and juices on the
specific binding ability of Norovirus GII. 4 P particles. Journal
of Food Protection, 75(7), 1350–1354.
Liu, P. B., Chien, Y. W., Papafragkou, E., Hsiao, H. M., Jaykus, L.
A., & Moe, C. (2009a). Persistence of human noroviruses on
food preparation surfaces and human hands. Food and Environ-
mental Virology, 1(3–4), 141–147.
Liu, G., Kahan, S. M., Jia, Y., & Karst, S. M. (2009b). Primary high-
dose murine norovirus 1 infection fails to protect from secondary
challenge with homologous virus. Journal of Virology, 83(13),
LoBue, A. D., Lindesmith, L., Yount, B., Harrington, P. R.,
Thompson, J. M., Johnston, R. E., et al. (2006). Multivalent
norovirus vaccines induce strong mucosal and systemic blocking
antibodies against multiple strains. Vaccine, 24(24), 5220–5234.
Locas, A., Barthe, C., Margolin, A. B., & Payment, P. (2008).
Groundwater microbiological quality in Canadian drinking water
municipal wells. Canadian Journal of Microbiology, 54(6),
Lodder, W. J., & de Roda Husman, A. M. (2005). Presence of
noroviruses and other enteric viruses in sewage and surface
waters in The Netherlands. Applied and Environmental Micro-
biology, 71(3), 1453–1461.
Lodder, W. J., van den Berg, H., Rutjes, S. A., & de Roda Husman,
A. M. (2010). Presence of enteric viruses in source waters for
drinking water production in The Netherlands. Applied and
Environmental Microbiology, 76(17), 5965–5971.
Lopman, B. A., Adak, G. K., Reacher, M. H., & Brown, D. W. G.
(2003). Two epidemiologic patterns of Norovirus outbreaks:
Surveillance in England and Wales, 1992–2000. Emerging
Infectious Diseases, 9(1), 71–77.
Lopman, B. A., Brown, D. W., & Koopmans, M. (2002). Human
caliciviruses in Europe. Journal of Clinical Virology, 24(3),
Lowther, J. A., Gustar, N. E., Hartnell, R. E., & Lees, D. N. (2012).
Comparison of norovirus RNA levels in outbreak-related oysters
with background environmental levels. Journal of Food Protec-
tion, 75(2), 389–393.
Lowther, J. A., Henshilwood, K., & Lees, D. N. (2008). Determination of
norovirus contamination in oysters from two commercial harvesting
areas over an extended period, using semiquantitative real-time
reverse transcription PCR. Journal of Food Protection, 71(7),
Makary, P., Maunula, L., Niskanen, T., Kuusi, M., Virtanen, M.,
Pajunen, S., et al. (2009). Multiple norovirus outbreaks among
workplace canteen users in Finland, July 2006. Epidemiology
and Infection, 137(3), 402–407.
Abarca, B., et al. (2009). Outbreak of norovirus infection among
river rafters associated with packaged delicatessen meat, Grand
Canyon, 2005. Clinical Infectious Diseases, 48(1), 31–37.
Mans, J., Netshikweta, R., Magwalivha, M., van Zyl, W. B., Taylor,
M. B. (2012). Diverse norovirus genotypes identified in sewage-
polluted river water in South Africa. Epidemiology and Infec-
tion, 1–11 (Epub ahead of print).
Martella, V., Campolo, M., Lorusso, E., Cavicchio, P., Camero, M.,
Bellacicco, A. L., et al. (2007). Norovirus in captive lion cub
(Panthera leo). Emerging Infectious Diseases, 13, 1071–1073.
Martella, V., Decaro, N., Lorusso, E., Radogna, A., Moschidou, P.,
Amorisco, F., et al. (2009). Genetic heterogeneity and recom-
bination in canine noroviruses. Journal of Virology, 83(21),
Martella, V., Lorusso, E., Decaro, N., Elia, G., Radogna, A.,
D’Abramo, M., et al. (2008). Detection and molecular charac-
terization of a canine norovirus. Emerging Infectious Diseases,
Matthijs, E., Muylkens, B., Mauroy, A., Ziant, D., Delwiche, T., &
Thiry, E. (2010). Experimental evidence of recombination in
murine noroviruses. Journal of General Virology, 91(11),
Mattison, K., Harlow, J., Morton, V., Cook, A., Pollari, F., &
Bidawid, S. (2010). Enteric viruses in ready-to-eat packaged
leafy greens. Emerging Infectious Diseases, 16(11), 1815–1817.
Mattison, K., Shukla, A., Cook, A., Pollari, F., Friendship, R., Kelton,
D., et al. (2007). Human noroviruses in swine and cattle.
Emerging Infectious Diseases, 13(8), 1184–1188.
Maunula, L. (2006). Waterborne norovirus outbreaks. Future Virol-
ogy, 2(1), 101–112.
Maunula, L., Roivainen, M., Keranen, M., Makela, S., Soderberg, K.,
Summa, M., et al. (2009). Detection of human norovirus from
frozen raspberries in a cluster of gastroenteritis outbreaks.
Eurosurveillance, 14(49), 16–18.
Maunula, L., So ¨derberg, K., Vahtera, H., Vuorilehto, V. P., von
Bonsdorff, C. H., Valtari, M., et al. (2012). Presence of human
noro-and adenoviruses in river and treated wastewater, a
longitudinal study and method comparison. Journal of Water
and Health, 10(1), 87–99.
148Food Environ Virol (2012) 4:131–152
Mauroy, A., Scipioni, A., Mathijs, E., Saegerman, C., Mast, J.,
Bridger, J. C., et al. (2009a). Epidemiological study of bovine
norovirus infection by RT-PCR and a VLP-based antibody
ELISA. Veterinary Microbiology, 137(3–4), 243–251.
Mauroy, A., Scipioni, A., Mathijs, E., Thys, C., & Thiry, E. (2009b).
Molecular detection of kobuviruses and recombinant noroviruses
in cattle in continental Europe. Archives of Virology, 154(11),
Mauroy, A., Scipioni, A., Matthijs, E., Miry, C., Ziant, D., Thys, C.,
et al. (2008). Noroviruses and sapoviruses in pigs in Belgium.
Archives of Virology, 153(10), 1927–1931.
Medici, M. C., Morelli, A., Arcangeletti, M. C., Calderaro, A., De
Conto, F., Martinelli, M., et al. (2008). An outbreak of norovirus
infection in an Italian residential-care facility for the elderly.
Clinical Microbiology and Infection: The Official Publication of
the European Society of Clinical Microbiology and Infections
Diseases, 15(1), 97–100.
Portugal, December 2008. Eurosurveillance, 14(41), 19–21.
Meyers, T. R. (1984). Marine bivalve mollusks as reservoirs of viral
finfish pathogens: Significance to marine and anadromous finfish
aquaculture. Marine Fisheries Review, 46(3), 14–17.
Mijovski, J. Z., Poljsak-Prijatelj, M., Steyer, A., Barlic-Maganja, D.,
& Koren, S. (2010). Detection and molecular characterisation of
noroviruses and sapoviruses in asymptomatic swine and cattle in
Slovenian farms. Infection, Genetics and Evolution, 10(3),
Milnes, A. S., Binns, S. H., Oliver, S. L., & Bridger, J. C. (2007).
Retrospective study of noroviruses in samples of diarrhoea from
cattle, using the Veterinary Laboratories Agency’s Farmfile
database. Veterinary Record, 160(10), 326–330.
Moe, C. L. (2007). Waterborne transmission of infectious agents. In
C. J. Hurst, R. L. Crawford, J. L. Garland, D. A. Lipson,
A. L. Mills, & L. D. Stetzenbach (Eds.), Manual of environmental
microbiology (pp. 222–248). Washington, DC: ASM Press.
Moe, C. L. (2008). Preventing norovirus transmission: How should
we handle food handlers? Clinical Infectious Diseases, 48(1),
Mokhtari, A., & Jaykus, L. A. (2009). Quantitative exposure model
for the transmission of norovirus in retail food preparation.
International Journal of Food Microbiology, 133(1–2), 38–47.
Morioka, S., Sakata, T., Tamaki, A., Shioji, T., Funaki, A.,
Yamamoto, Y., et al. (2006). A food-borne norovirus outbreak
at a primary school in Wakayama Prefecture. Japanese Journal
of Infectious Diseases, 59(3), 205–207.
Nakamura, K., Saga, Y., Iwai, M., Obara, M., Horimoto, E.,
Hasegawa, S., et al. (2010). Frequent detection of noroviruses
and sapoviruses in swine population and high genetic diversity of
porcine sapovirus in Japan, during fiscal year 2008. Journal of
Clinical Microbiology, 48(4), 1215–1222.
Nenonen, N. P., Hannoun, C., Olsson, M. B., & Bergstrom, T. (2009).
Molecular analysis of an oyster-related norovirus outbreak.
Journal of Clinical Virology, 45(2), 105–108.
Ng, T. L., Chan, P. P., Phua, T. H., Loh, J. P., Yip, R., Wong, C., et al.
(2005). Oyster-associated outbreaks of Norovirus gastroenteritis
in Singapore. Journal of Infection, 51(5), 413–418.
Nishida, T., Nishio, O., Kato, M., Chuma, T., Kato, H., Iwata, H.,
et al. (2007). Genotyping and quantitation of noroviruses in
oysters from Two Distinct Sea areas in Japan. Microbiology and
Immunology, 51(2), 177–184.
Noda, M., Fukuda, S., & Nishio, O. (2008). Statistical analysis of
attack rate in norovirus foodborne outbreaks. International
Journal of Food Microbiology, 122(1–2), 216–220.
Nordgren, J., Kindberg, E., Lindgren, P. E., Matussek, A., &
Svensson, L. (2010). Norovirus gastroenteritis outbreak with a
secretor-independent susceptibility pattern, Sweden. Emerging
Infectious Diseases, 16(1), 81–87.
O’Brien, S. J., Gillespie, I. A., Sivanesan, M. A., Elson, R., Hughes,
C., & Adak, G. K. (2006). Publication bias in foodborne
outbreaks of infectious intestinal disease and its implications for
evidence-based food policy. England and Wales 1992–2003.
Epidemiology and Infection, 134(04), 667–674.
Ohwaki, K., Nagashima, H., Aoki, M., Aoki, H., & Yano, E. (2009).
A foodborne norovirus outbreak at a hospital and an attached
long-term care facility. Japanese Journal of Infectious Diseases,
Oliver, S. L., Brown, D. W. G., Green, J., & Bridger, J. C. (2004). A
chimeric bovine enteric calicivirus: Evidence for genomic
recombination in genogroup III of the Norovirus genus of the
Caliciviridae. Virology, 326(2), 231–239.
Oliver, S. L., Dastjerdi, A. M., Wong, S., El-Attar, L., Gallimore, C.,
Brown, D. W. G., et al. (2003). Molecular characterization of
bovine enteric caliciviruses: a distinct third genogroup of
noroviruses (Norwalk-like viruses) unlikely to be of risk to
humans. Journal of Virology, 77(4), 2789–2798.
Oogane, T., Hirata, A., Funatogawa, K., Kobayashi, K., Sato, T., &
Kimura, H. (2008). Food poisoning outbreak caused by norovi-
rus GII/4 in school lunch, Tochigi Prefecture, Japan. Japanese
Journal of Infectious Diseases, 61(5), 423–424.
Otto, P. H., Clarke, I. N., Lambden, P. R., Salim, O., Reetz, J., &
Liebler-Tenorio, E. M. (2011). Infection of calves with bovine
norovirus GIII. 1 strain jena virus: an experimental model to
study the pathogenesis of norovirus infection. Journal of
Virology, 85(22), 12013–12021.
Ozawa, K., Oka, T., Takeda, N., & Hansman, G. S. (2007). Norovirus
infections in symptomatic and asymptomatic food handlers in
Japan. Journal of Clinical Microbiology, 45(12), 3996–4005.
Parasidis, T., Divari, E., Fatouros, N., & Vantarakis, A. (2007).
Outbreak of acute gastroenteritis in Greece during a school
excursion, April 2007. Euro Surveillance, 12(7), E0705–E0707.
Park, S. I., Jeong, C., Kim, H. H., Park, S. H., Park, S. J., Hyun, B. H.,
et al. (2007). Molecular epidemiology of bovine noroviruses in
South Korea. Veterinary Microbiology, 124(1–2), 125–133.
Parshionikar, S. U., Willian-True, S., Fout, G. S., Robbins, D. E.,
Seys, S. A., Cassady, J. D., et al. (2003). Waterborne outbreak of
gastroenteritis associated with a norovirus. Applied and Envi-
ronmental Microbiology, 69(9), 5263–5268.
Patel, M. M., Hall, A. J., Vinje, J., & Parashar, U. D. (2009).
Noroviruses: A comprehensive review. Journal of Clinical
Virology: The Official Publication of the Pan American Society
for Clinical Virology, 44(1), 1–8.
Payne, K., Hall, M., Lutzke, M., Armstrong, C., & King, J. (2006).
Multisite outbreak of norovirus associated with a franchise
restaurant—Kent County, Michigan, May 2005. Morbidity and
Mortality Weekly Report, 55(14), 395–397.
Pe ´rez-Sautu, U., Sano, D., Guix, S., Kasimir, G., Pinto, R. M., &
Bosch, A. (2012). Human norovirus occurrence and diversity in
the Llobregat river catchment, Spain. Environmental Microbiol-
ogy, 14(2), 494–502.
Phan, T. G., Kaneshi, K., Ueda, Y., Nakaya, S., Nishimura, S.,
Yamamoto, A., et al. (2007). Genetic heterogeneity, evolution,
and recombination in noroviruses. Journal of Medical Virology,
Phillips, G., Tam, C. C., Rodrigues, L. C., & Lopman, B. (2010).
Prevalence and characteristics of asymptomatic norovirus infec-
tion in the community in England. Epidemiology and Infection,
Pinto, P., Wang, Q., Chen, N., Dubovi, E. J., Daniels, J. B., Millward,
L. M., et al. (2012). Discovery and genomic characterization of
noroviruses from a gastroenteritis outbreak in domestic cats in
the US. PLoS One, 7(2), e-32739.
Food Environ Virol (2012) 4:131–152 149
Prato, R., Lopalco, P. L., Chironna, M., Barbuti, G., Germinario, C.,
& Quarto, M. (2004). Norovirus gastroenteritis general outbreak
associated with raw shellfish consumption in south Italy. BMC
Infectious Disease, 6(37), 1–6.
Reuter, G., Biro, H., & Szucs, G. (2007). Enteric caliciviruses in
domestic pigs in Hungary. Archives of Virology, 152(3),
Reuter, G., Pankovics, P., & Egyed, L. (2009). Detection of genotype
1 and 2 bovine noroviruses in Hungary. Veterinary Record,
Rizzo, C., Di Bartolo, I., Santantonio, M., Coscia, M. F., Monno, R.,
De Vito, D., et al. (2007). Epidemiological and virological
investigation of a Norovirus outbreak in a resort in Puglia, Italy.
BMC Infectious Diseases, 7, 135.
Rockx, B. H. G., Bogers, W., Heeney, J. L., van Amerongen, G., &
Koopmans, M. P. G. (2005). Experimental norovirus infections
in non-human primates. Journal of Medical Virology, 75(2),
Rodriguez-Lazaro, D., Cook, N., Ruggeri, F. M., Sellwood, J., Nasser,
A., Nascimento, M. S. J., et al. (2011). Virus hazards from food,
water and other contaminated environments. FEMS Microbiol-
ogy Reviews, 36(4), 786–814.
Rohayem, J. (2009). Norovirus seasonality and the potential impact of
climate change. Clinical Microbiology & Infection, 15(6),
Rosenthal, N. A., LE Lee, Vermeulen, B. A. J., Hedberg, K., Keene,
W. E., Widdowson, M. A., et al. (2011). Epidemiological and
genetic characteristics of norovirus outbreaks in long-term care
facilities, 2003–2006. Epidemiology and Infection, 139(2),
Saif, L. J., Bohl, E. H., Theil, K. W., Cross, R. F., & House, J. A.
(1980). Rotavirus-like, calicivirus-like, and 23-nm virus-like
particles associated with diarrhea in young pigs. Journal of
Clinical Microbiology, 12(1), 105–111.
Sakon, N., Yamazaki, K., Yoda, T., Kanki, M., Otake, T., &
Tsukamoto, T. (2005). A norovirus outbreak of gastroenteritis
linked to packed lunches. Japanese Journal of Infectious
Diseases, 58(4), 253.
Sala, M. R., Cardenosa, N., Arias, C., Llovet, T., Recasens, A.,
Dominguez, A., et al. (2005). An outbreak of food poisoning due
to a genogroup I norovirus. Epidemiology and Infection, 133(1),
Schets, F. M., Van Wijnen, J. H., Schijven, J. F., Schoon, H., & de
Roda Husman, A. M. (2008). Monitoring of waterborne patho-
gens in surface waters in Amsterdam, The Netherlands, and the
potential health risk associated with exposure to Cryptosporidi-
um and Giardia in these waters. Applied and Environmental
Microbiology, 74(7), 2069–2078.
Schmid, D., Stuger, H. P., Lederer, I., Pichler, A. M., Kainz-
Arnfelser, G., Schreier, E., et al. (2007). A foodborne norovirus
outbreak due to manually prepared salad, Austria 2006. Infec-
tion, 35(4), 232–239.
Scipioni, A., Mauroy, A., Vinje, J., & Thiry, E. (2008). Animal
noroviruses. The Veterinary Journal, 178(1), 32–45.
Sekla, L., Stackiw, W., Dzogan, S., & Sargeant, D. (1989). Foodborne
gastroenteritis due to Norwalk virus in a Winnipeg hotel. CMAJ:
Canadian Medical Association Journal, 140(12), 1461–1464.
Shen, Q., Zhang, W., Yang, S., Chen, Y., Ning, H., Shan, T., et al.
(2009). Molecular detection and prevalence of porcine caliciv-
iruses in eastern China from 2008 to 2009. Archives of Virology,
Showell, D., Sundkvist, T., Reacher, M., & Gray, J. (2007). Norovirus
outbreak associated with canteen salad in Suffolk, United
Kingdom. Euro Surveillance, 12(11), E071129.6.
Siebenga, J. J., Lemey, P., Pond, S. L. K., Rambaut, A., Vennema, H.,
& Koopmans, M. (2010). Phylodynamic reconstruction reveals
norovirus GII. 4 epidemic expansions and their molecular
determinants. PLoS Pathogens, 6(5), e-1000884.
Siebenga, J. J., Vennema, H., Duizer, E., & Koopmans, M. P. G.
(2007). Gastroenteritis caused by norovirus GGII.4, the Nether-
Siebenga, J. J., Vennema, H., Zheng, D. P., Vinje, J., Lee, B. E., Pang,
X. L., et al. (2009). Norovirus illness is a global problem:
Emergence and spread of norovirus GII.4 variants, 2001–2007.
Journal of Infectious Diseases, 200(5), 802–812.
Smiley, J. R., Hoet, A. E., Trave ´n, M., Tsunemitsu, H., & Saif, L. J.
(2003). Reverse transcription-PCR assays for detection of bovine
enteric caliciviruses (BEC) and analysis of the genetic relation-
ships among BEC and human caliciviruses. Journal of Clinical
Microbiology, 41(7), 3089–3099.
Springthorpe, S., & Sattar, S. A. (2007). Chapter 6 Virus removal
during drinking water treatment. vol. 17, 109–126.
Stals, A., Baert, L., De Keuckelaere, A., Van Coillie, E., &
Uyttendaele, M. (2011a). Evaluation of a norovirus detection
methodology for ready-to-eat foods. International Journal of
Food Microbiology, 145(2–3), 420–425.
Stals, A., Baert, L., Jasson, V., Van Coillie, E., & Uyttendaele, M.
(2011b). Screening of fruit products for norovirus and the
difficulty of interpreting positive PCR results. Journal of Food
Protection, 74(3), 425–431.
Stals, A., Baert, L., Van Coillie, E., & Uyttendaele, M. (2011c).
Evaluation of a norovirus detection methodology for soft red
fruits. Food Microbiology, 28(1), 52–58.
Steele, M., & Odumeru, J. (2004). Irrigation water as source of
foodborne pathogens on fruit and vegetables. Journal of Food
Protection, 67(12), 2839–2849.
Sugieda, M., Nagaoka, H., Kakishima, Y., Ohshita, T., Nakamura, S.,
& Nakajima, S. (1998). Detection of Norwalk-like virus genes in
the caecum contents of pigs. Archives of Virology, 143(6),
Summa, M., von Bonsdorff, C. H., & Maunula, L. (2012a).
Evaluation of four virus recovery methods for detecting noro-
viruses on fresh lettuce, sliced ham, and frozen raspberries.
Journal of Virological Methods, 183(2), 154–160.
Summa, M., von Bonsdorff, C. H., & Maunula, L. (2012b). Pet dogs,
a transmission route for human noroviruses? Journal of Clinical
Virology, 53(3), 244–247.
Takanashi, S., Wang, Q., Chen, N., Shen, Q., Jung, K., Zhang, Z.,
et al. (2011). Characterization of emerging GII. g/GII. 12
noroviruses from a gastroenteritis outbreak in the United States
in 2010. Journal of Clinical Microbiology, 49(9), 3234–3244.
Takkinen, J. (2006). Recent norovirus outbreaks on river and
seagoing cruise ships in Europe. Euro Surveillance, 11(6),
Terio, V., Martella, V., Moschidou, P., Di Pinto, P., Tantillo, G., &
Buonavoglia, C. (2010). Norovirus in retail shellfish. Food
Microbiology, 27(1), 29–32.
Teunis, P. F. M., Rutjes, S. A., Westrell, T., & de Roda Husman,
A. M. (2009). Characterization of drinking water treatment for
virus risk assessment. Water Research, 43(2), 395–404.
Thackray, L. B., Wobus, C. E., Chachu, K. A., Liu, B., Alegre, E. R.,
Henderson, K. S., et al. (2007). Murine noroviruses comprising a
single genogroup exhibit biological diversity despite limited
sequence divergence. Journal of Virology, 81(19), 10460–10473.
Todd, E. C. D., Greig, J. D., Bartleson, C. A., & Michaels, B. S.
(2009). Outbreaks where food workers have been implicated in
the spread of foodborne disease. Part 6. Transmission and
survival of pathogens in the food processing and preparation
environment. Journal of Food Protection, 72(1), 202–219.
Ueki, Y., Sano, D., Watanabe, T., Akiyama, K., & Omura, T. (2005).
Norovirus pathway in water environment estimated by genetic
150Food Environ Virol (2012) 4:131–152
analysis of strains from patients of gastroenteritis, sewage,
treated wastewater, river water and oysters. Water Research,
Ueki, Y., Shoji, M., Suto, A., Tanabe, T., Okimura, Y., Kikuchi, Y.,
et al. (2007). Persistence of caliciviruses in artificially contam-
inated oysters during depuration. Applied and Environmental
Microbiology, 73(17), 5698–5701.
van den Berg, H., Lodder, W., van der Poel, W., Vennema, H., & de
Roda Husman, A. M. (2005). Genetic diversity of noroviruses in
raw and treated sewage water. Research in Microbiology,
van der Poel, W. H., Van der Heide, H. R., Verschoor, F.,
Gelderblom, H., Vinje, J., & Koopmans, M. P. (2003). Epide-
miology of Norwalk-like virus infections in cattle in The
Netherlands. Veterinary Microbiology, 92(4), 297–309.
van der Poel, W. H., Vinje, J., van Der Heide, R., Herrera, M. I., Vivo,
A., & Koopmans, M. P. (2000). Norwalk-like calicivirus genes
in farm animals. Emerging Infectious Diseases, 6(1), 36–41.
Vega, E., Garland, J., & Pillai, S. D. (2008). Electrostatic forces
control nonspecific virus attachment to lettuce. Journal of Food
Protection, 71(3), 522–529.
Vega, E., Smith, J., Garland, J., Matos, A., & Pillai, S. D. (2005).
Variability of virus attachment patterns to butterhead lettuce.
Journal of Food Protection, 68(10), 2112–2117.
Verhoef, L., Boxman, I. L., Duizer, E., Rutjes, S. A., Vennema, H.,
Friesema, I. H. M., et al. (2008). Multiple exposures during a
norovirus outbreak on a river-cruise sailing through Europe,
2006. Euro Surveillance, 12(1), 246–252.
Verhoef, L. P. B., Kroneman, A., van Duynhoven, Y., Boshuizen, H.,
van Pelt, W., & Koopmans, M. (2009). Selection tool for
foodborne norovirus outbreaks. Emerging Infectious Diseases,
Verhoef, L., Vennema, H., van Pelt, W., Lees, D., Boshuizen, H.,
Henshilwood, K., et al. (2010). Use of norovirus genotype
profiles to differentiate origins of foodborne outbreaks. Emerg-
ing Infectious Diseases, 16(4), 617–621.
Vinje, J. (2010). A norovirus vaccine on the horizon? The Journal of
Infectious Diseases, 202(11), 1623–1625.
Vivancos, R., Shroufi, A., Sillis, M., Aird, H., Gallimore, C. I., Myers,
L., et al. (2009). Food-related norovirus outbreak among people
attending two barbeques: Epidemiological, virological, and
environmental investigation. International Journal of Infectious
Diseases, 13(5), 629–635.
Wadl, M., Scherer, K., Nielsen, S., Diedrich, S., Ellerbroek, L., Frank,
C., et al. (2010). Food-borne norovirus-outbreak at a military
base, Germany, 2009. BMC Infectious Diseases, 10, 30.
Wang, Q. H., Costantini, V., & Saif, L. J. (2007). Porcine enteric
caliciviruses: Genetic and antigenic relatedness to human
caliciviruses, diagnosis and epidemiology. Vaccine, 25(30),
Wang, Q. H., Han, M. G., Cheetham, S., Souza, M., Funk, J. A., &
Saif, L. J. (2005a). Porcine noroviruses related to human
noroviruses. Emerging Infectious Diseases, 11(12), 1874–1881.
L. J. (2005b). Genetic diversity and recombination of porcine
sapoviruses. Journal of Clinical Microbiology, 43(12), 5963–5972.
Wang, Q. H., Souza, M., Funk, J. A., Zhang, W., & Saif, L. J. (2006).
Prevalence of noroviruses and sapoviruses in swine of various
ages determined by reverse transcription-PCR and microwell
hybridization assays. Journal of Clinical Microbiology, 44(6),
Webby, R. J., Carville, K. S., Kirk, M. D., Greening, G., Ratcliff,
oyster meat causing multiple outbreaks of norovirus infection in
Australia. Clinical Infectious Diseases, 44(8), 1026–1031.
Wei, J., Jin, Y., Sims, T., & Kniel, K. E. (2010). Manure-and
biosolids-resident murine norovirus 1 attachment to and inter-
nalization by Romaine lettuce. Applied and Environmental
Microbiology, 76(2), 578–583.
Wei, J., Jin, Y., Sims, T., & Kniel, K. E. (2011). Internalization of
murine norovirus 1 into Lactuca sativa during irrigation. Applied
and Environmental Microbiology, 77(7), 2508–2512.
Wei, J., & Kniel, K. E. (2010). Pre-harvest viral contamination of
crops originating from fecal matter. Food and Environmental
Virology, 2(4), 195–206.
Westrell, T., Teunis, P., van den Berg, H., Lodder, W., Ketelaars, H.,
Stenstro ¨m, T. A., et al. (2006). Short-and long-term variations of
norovirus concentrations in the Meuse river during a 2-year
study period. Water Research, 40(14), 2613–2620.
White, K., Osterholm, M. T., Mariott, J., Lawrence, D. H., Ristinen,
T., & Greenberg, H. B. (1986). A foodborne outbreak of
Norwalk virus gastroenteritis evidence for post-recovery trans-
mission. American Journal of Epidemiology, 124(1), 120–126.
Wick, J. Y. (2012). Norovirus: Noxious in nursing facilities: Almost
unavoidable. The Consultant Pharmacist, 27(2), 98–104.
Widdowson, M. A., Rockx, B., Schepp, R., van der Poel, W. H. M.,
Vinje, J., van Duynhoven, Y. T., et al. (2005a). Detection of
serum antibodies to bovine norovirus in veterinarians and the
general population in the Netherlands. Journal of Medical
Virology, 76(1), 119–128.
Widdowson, M. A., Sulka, A., Bulens, S. N., Beard, R. S., Chaves,
S. S., Hammond, R., et al. (2005b). Norovirus and foodborne
disease, United States, 1991–2000. Emerging Infectious Dis-
eases, 11(1), 95–102.
Wise, A. G., Monroe, S. S., Hanson, L. E., Grooms, D. L., Sockett,
D., & Maes, R. K. (2004). Molecular characterization of
noroviruses detected in diarrheic stools of Michigan and
Wisconsin dairy calves: Circulation of two distinct subgroups.
Virus Research, 100(2), 165–177.
Wolf, S., Williamson, W., Hewitt, J., Lin, S., Rivera-Aban, M., Ball,
A., et al. (2009). Molecular detection of norovirus in sheep and
pigs in New Zealand farms. Veterinary Microbiology, 133(1–2),
Wolf, S., Williamson, W. M., Hewitt, J., Rivera-Aban, M., Lin, S.,
Ball, A., et al. (2007). Sensitive multiplex real-time reverse
transcription-PCR assay for the detection of human and animal
noroviruses in clinical and environmental samples. Applied and
Environmental Microbiology, 73(17), 5464–5470.
Woode, G. N., & Bridger, J. C. (1978). Isolation of small viruses
resembling astroviruses and caliciviruses from acute enteritis of
calves. Journal of Medical Microbiology, 11(4), 441–452.
World Health Organization (2008). Foodborne disease outbreaks:
guidelines for investigation and control.
Yang, Y., Xia, M., Tan, M., Huang, P., Zhong, W., Pang, X. L., et al.
(2010). Genetic and phenotypic characterization of GII-4
noroviruses that circulated during 1987 to 2008. Journal of
Virology, 84(18), 9595–9607.
Yin, Y., Tohya, Y., Ogawa, Y., Numazawa, D., Kato, K., & Akashi,
H. (2006). Genetic analysis of calicivirus genomes detected in
intestinal contents of piglets in Japan. Archives of Virology,
Yoder, J. S., Blackburn, B. G., Craun, G. F., Hill, V., Levy, D. A.,
Chen, N., et al. (2004). Surveillance for waterborne-disease
outbreaks associated with recreational water—United States,
2001–2002. Morbidity and Mortality Weekly Report, 53(8),
Zainazor, C. T., Hidayah, M. S. N., Chai, L. C., Tunung, R., Ghazali,
F. M., & Son, R. (2010). The scenario of norovirus contamina-
tion in food and food handlers. Journal of Microbiology and
Biotechnology, 20(2), 229–237.
Food Environ Virol (2012) 4:131–152 151
Zakhour, M., Maalouf, H., Di Bartolo, I., Haugarreau, L., Le Download full-text
Guyader, F. S., Ruvoen-Clouet, N., et al. (2010). Bovine
norovirus: Carbohydrate ligand, environmental contamination,
and potential cross-species transmission via oysters. Applied and
Environmental Microbiology, 76(19), 6404–6411.
Zheng, D. P., Ando, T., Fankhauser, R. L., Beard, R. S., Glass, R. I.,
& Monroe, S. S. (2006). Norovirus classification and proposed
strain nomenclature. Virology, 346(2), 312–323.
Zheng, D. P., Widdowson, M. A., Glass, R. I., & Vinje, J. (2009).
Molecular epidemiology of GII. 4 noroviruses in the US between
1994 and 2006. Journal of Clinical Microbiology, 48(1),
Zomer, T. P., De Jong, B., Ku ¨hlmann-Berenzon, S., Nyre ´n, O.,
Svenungsson, B., Hedlund, K. O., et al. (2009). A norovirus
outbreak at a manufacturing company. Epidemiology and
Infection, 138, 501–506.
152Food Environ Virol (2012) 4:131–152