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 Advances in
FOOD AND
NUTRITION
RESEARCH
VOLUME
62
ADVISORY BOARDS
KEN BUCKLE
University of New South Wales, Australia

MARY ELLEN CAMIRE

University of Maine, USA

ROGER CLEMENS
University of Southern California, USA

HILDEGARDE HEYMANN
University of California, Davis, USA

ROBERT HUTKINS
University of Nebraska, USA

RONALD JACKSON
Quebec, Canada

HUUB LELIEVELD
Global Harmonization Initiative, The Netherlands

DARYL B. LUND
University of Wisconsin, USA

CONNIE WEAVER
Purdue University, USA

RONALD WROLSTAD
Oregon State University, USA

SERIES EDITORS
GEORGE F. STEWART (1948–1982)
EMIL M. MRAK (1948–1987)
C. O. CHICHESTER (1959–1988)
BERNARD S. SCHWEIGERT (1984–1988)
JOHN E. KINSELLA (1989–1993)
STEVE L. TAYLOR (1995– )
 Advances in
FOOD AND
NUTRITION
RESEARCH
VOLUME
62
Edited by

STEVE L. TAYLOR
University of Nebraska, Lincoln

AMSTERDAM • BOSTON • HEIDELBERG • LONDON

NEW YORK • OXFORD • PARIS • SAN DIEGO
SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO
Academic Press is an imprint of Elsevier
Academic Press is an imprint of Elsevier
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ISBN: 978-0-12-385989-1
ISSN: 1043-4526

For information on all Academic Press publications

visit our website at elsevierdirect.com

Printed and bound in USA

11 12 13 10 9 8 7 6 5 4 3 2 1
 CONTENTS

Contributors vii

1. Norovirus as a Foodborne Disease Hazard 1

Kirsten Mattison
I. Introduction to Norovirus 2
II. Norovirus Genetic Types and Outbreak Association 3
III. Norovirus Outbreaks Spread Person to Person 7
IV. Norovirus Outbreaks Spread by Fomite Contamination 10
V. Norovirus Outbreaks Spread by Food Handlers 15
VI. Norovirus Outbreaks Attributed to Water and Food 16
VII. Conclusions 20
References 21

2. Mitigation of Greenhouse Gas Emissions in the

Production of Fluid Milk 41
Peggy M. Tomasula and Darin W. Nutter
I. Introduction 42
II. Sustainable Development and the Pillars of Sustainability 44
III. Life Cycle Assessment Methodology 45
IV. LCA of the Fluid Milk Supply Chain 46
V. On-farm GHG Emission Mitigation Strategies 62
VI. Mitigation Strategies for GHG Emissions in Processing Plants 70
VII. Conclusions and Future Prospects 79
References 80

3. Chemical Composition, Characterization, and Differentiation

of Honey Botanical and Geographical Origins 89
Jun Wang and Qing X. Li
I. Introduction 90
II. Authenticity Issues 93
III. Chemical Composition and Analytical Methods for Discrimination
of the Botanical and Geographical Origins of Honeys 98
IV. Special Marker Compounds 121

v
vi Contents

V. Conclusions 122
References 122

4. Japan Food Allergen Labeling Regulation—History and Evaluation 139

Hiroshi Akiyama, Takanori Imai, and Motohiro Ebisawa
I. Assessment of Immediate-type Food Allergies in Japan 140
II. Japanese Food Allergy-labeling System 144
III. Regulation of Detection Methods for Food Allergenic Ingredients 147
IV. Patient Evaluation of Allergy Food Labeling 167
Acknowledgments 169
References 169

5. Extrusion Texturized Dairy Proteins: Processing and Application 173

Charles I. Onwulata, Michael H. Tunick, and Phoebe X. Qi
I. Dairy Proteins 174
II. Processing 179
III. Development 188
IV. Applications 192
V. Conclusions 194
References 195

6. A Review of the Application of Atomic Force Microscopy (AFM)

in Food Science and Technology 201
Shaoyang Liu and Yifen Wang
I. Introduction 202
II. Principles of AFM 202
III. Representative Applications 206
IV. Conclusions 237
References 238

Index 241
 CONTRIBUTORS

Numbers in parentheses indicate the pages on which the authors’ contributions begin.

 Hiroshi Akiyama
National Institute of Health Sciences, Division of Novel Foods and
Immunochemistry, 1-18-1 Kamiyoga, Setagaya-ku, Tokyo, Japan (139)
 Motohiro Ebisawa
Clinical Research Center for Allergology and Rheumatology, National
Hospital Organization, Sagamihara National Hospital, 18-1 Sakuradai,
Minami-ku, Sagamihara, Kanagawa, Japan (139)
 Takanori Imai
Clinical Research Center for Allergology and Rheumatology, National
Hospital Organization, Sagamihara National Hospital, 18-1 Sakuradai,
Minami-ku, Sagamihara, Kanagawa, Japan (139)
 Qing X. Li
Department of Molecular Biosciences and Bioengineering, University of
Hawaii of Manoa, Honolulu, Hawaii, USA (89)
 Shaoyang Liu
Biosystems Engineering Department, Auburn University, Auburn,
Alabama, USA (201)
 Kirsten Mattison
Bureau of Microbial Hazards, Health Canada, PL2204E, Ottawa,
Ontario, Canada (1)
 Darin W. Nutter
Mechanical Engineering Department, University of Arkansas, Fayette-
ville, Arkansas, USA (41)
 Charles I. Onwulata
Center of Excellence in Extrusion and Polymer Rheology, Eastern
Regional Research Center, Agricultural Research Service, U.S.
Department of Agriculture, Wyndmoor, Pennsylvania, USA (173)
 Phoebe X. Qi
Center of Excellence in Extrusion and Polymer Rheology, Eastern
Regional Research Center, Agricultural Research Service, U.S.
Department of Agriculture, Wyndmoor, Pennsylvania, USA (173)

vii
viii Contributors

 Peggy M. Tomasula
United States Department of Agriculture, Agricultural Research Service,
Eastern Regional Research Center, Dairy and Functional Foods
Research Unit, Wyndmoor, Pennsylvania, USA (41)
 Michael H. Tunick
Center of Excellence in Extrusion and Polymer Rheology, Eastern
Regional Research Center, Agricultural Research Service, U.S.
Department of Agriculture, Wyndmoor, Pennsylvania, USA (173)
 Jun Wang
Department of Molecular Biosciences and Bioengineering, University of
Hawaii of Manoa, Honolulu, Hawaii, USA (89)
 Yifen Wang
Biosystems Engineering Department, Auburn University, Auburn,
Alabama, USA (201)
 CHAPTER 1
Norovirus as a Foodborne
Disease Hazard
Kirsten Mattison1

Contents I.Introduction to Norovirus 2

II.Norovirus Genetic Types and Outbreak Association 3
III.Norovirus Outbreaks Spread Person to Person 7
IV. Norovirus Outbreaks Spread by Fomite
Contamination 10
V. Norovirus Outbreaks Spread by Food Handlers 15
VI. Norovirus Outbreaks Attributed to Water and Food 16
VII. Conclusions 20
References 21

Abstract Norovirus (NoV) is the most common cause of infectious gastroen-

teritis in the world. Gastroenteritis caused by bacterial and parasitic
pathogens is commonly linked to food sources, but the link
between NoV and contaminated foods has been more difficult to
establish. Even when epidemiological information indicates that an
outbreak originated with food, the presence of NoV in the suspect
product may not be confirmed. If food is found to contain a
common strain of NoV that circulates widely in the community, it
is not possible to use strain typing to link the contamination to
patient cases. Although food is certainly implicated in NoV spread,
there are additional person-to-person and fomite transmission
routes that have been shown to be important. NoV has an
extremely low infectious dose, is stable in the environment, and
resists disinfection. Cell culture methods are not available, so
viability cannot be determined. Finally, many NoV outbreaks

Bureau of Microbial Hazards, Health Canada, PL2204E, Ottawa, Ontario, Canada

1
Corresponding author: Kirsten Mattison, E-mail address: [email protected]

Advances in Food and Nutrition Research, Volume 62

ISSN 1043-4526, DOI: 10.1016/B978-0-12-385989-1.00001-6

1
2 Kirsten Mattison

originate with when an infected food handler contaminates ready-

to-eat food, which can be interpreted as foodborne or person-to-
person transmission. This review will discuss both the physical
characteristics of NoVs and the available epidemiological informa-
tion with particular reference to the role of foods in NoV
transmission.

I. INTRODUCTION TO NOROVIRUS
Norovirus is a genus of the Caliciviridae family, named for the cup-shaped
depressions visible in the capsid by electron microscopy (Fauquet et al.,
2005). Other genera within Caliciviridae are Lagovirus that infects rabbits
and hares, Vesivirus, infecting multiple animal species including cats and
sea lions, and Sapovirus that infects humans.
The human caliciviruses, norovirus (NoV) and sapovirus, have also
been described as small round structured viruses, for their 27–30 nm
capsids. The NoV capsid consists of 180 copies of the VP1 major capsid
protein packed as an icosahedron (Prasad et al., 1999) and the VP2 minor
capsid protein, which may contribute to stability (Bertolotti-Ciarlet et al.,
2002). The S domain of VP1 forms the inner shell of the capsid, while the P
domain protrudes from the capsid surface and contributes to binding the
histoblood group antigen receptor (Cao et al., 2007) and antigenicity
(Donaldson et al., 2008; Lindesmith et al., 2010).
The NoV genome is approximately 7.5 kb in length and contains three
open reading frames ( Jiang et al., 1993). ORF1 codes for a polyprotein that
is cleaved by the viral protease into at least six nonstructural proteins
including the viral Vpg, protease, and RNA-dependent RNA polymerase
(Sosnovtsev et al., 2006). ORF2 codes for the major capsid protein VP1, and
ORF3 codes for the minor capsid protein VP2 (Green, 2007). The P domain
of VP1, in particular the P2 subdomain, is the most variable region of the
NoV genome, while the 50 untranslated region (UTR) and the junction
between ORF1 and ORF2 are the most highly conserved regions of the
genome (Kageyama et al., 2003). The P2 subdomain is associated with
NoV antigenic variation (Lindesmith et al., 2008; Siebenga et al., 2007b),
while the highly conserved regions are the sites of initiation for transcrip-
tion of the viral genomic and subgenomic RNAs (Asanaka et al., 2005; Bull
et al., 2005; Lambden et al., 1995).
Sequence analysis of the major capsid protein, VP1, groups NoV into
five genogroups that contain at least 29 genetic clusters (Zheng et al.,
2006). Most of the strains associated with human infection belong to
genogroup I (GI) or GII, while GIII viruses infect cattle, GIV viruses infect
humans and canines, and GV viruses infect mice.
 Norovirus as a Foodborne Disease Hazard 3

NoV infection causes acute vomiting, diarrhea, and abdominal cramps

(Koopmans, 2008). Fever is reported in approximately 40% of NoV cases
(Kaplan et al., 1982; Wyatt et al., 1974). Cases typically become symptom-
atic 24–48 h after infection, and the illness typically resolves after 48–72 h
(Teunis et al., 2008; Wyatt et al., 1974). Both symptomatic illness and
asymptomatic shedding have been shown to last longer in children, as
well as hospitalized or immunocompromised patients (Kirkwood and
Streitberg, 2008; Lopman et al., 2004; Rockx et al., 2002; Simon et al.,
2006). Attempts have been made to correlate levels of NoV shedding
with a particular genogroup or with disease severity, but to date, no
clear picture has emerged (Ajami et al., 2010; Barreira et al., 2010; Chan
et al., 2006; Lee et al., 2007). Deaths have been associated with NoV
infection due to severe dehydration in sensitive populations (Chadwick
et al., 2000; Dedman et al., 1998; Stuart et al., 2010).
NoVs infect all age groups and are the most common cause of infec-
tious gastroenteritis in both community and healthcare settings (de Wit
et al., 2001b; Estes et al., 2006; Green et al., 2002; Lopman et al., 2003, 2004).
See Table 1.1 for a summary of some published NoV outbreak reports.
Although outbreaks occur throughout the year (Alain and Denis, 2007),
there seems to be increased NoV activity in the colder months in temper-
ate climates (Dey et al., 2010; Greer et al., 2009; Lopman et al., 2009;
Rohayem, 2009). A precise description of NoV prevalence worldwide is
not possible, due to differences in surveillance systems and in detection
methods, but reports suggest that anywhere from 5% to 30% of tested
cases of gastroenteritis are caused by NoV (Amar et al., 2007; Bon et al.,
1999; de Wit et al., 2001a; Monica et al., 2007; Oh et al., 2003; O’Ryan et al.,
2000; Pang et al., 1999; Parashar et al., 2004). Repeated infection with the
same NoV strain is possible, as natural infection does not appear to confer
long-lasting immunity ( Johnson et al., 1990; Parrino et al., 1977).

II. NOROVIRUS GENETIC TYPES AND

OUTBREAK ASSOCIATION
Of all the NoV genetic clusters, the GII.4 cluster represents the majority of
NoV detected by public health testing laboratories (Adamson et al., 2007; Ho
et al., 2006; Ike et al., 2006; Kearney et al., 2007; Maunula and Von Bonsdorff,
2005; Park et al., 2010; Reuter et al., 2008; Siebenga et al., 2007a; Tu et al., 2007).
This cluster is identified around the world (Siebenga et al., 2009) and has
been circulating for at least 35 years (Bok et al., 2009). The GII.4 strains have
been shown to have a higher mutation rate than other clusters (Bull et al.,
2010), possibly associated with specific amino acid changes in the viral
polymerase (Bruggink and Marshall, 2008, 2009). Six major strain variants
of GII.4 NoV were identified between 1990 and 2006 (Lindesmith et al., 2008;
TABLE 1.1 Examples of norovirus outbreak reports published since 2005

Outbreak NoV
type Outbreak source Data available genotype Reference

Person to Contact among patients, Epidemiology and NoV NRa Grima et al. (2009), Grmek Kosnik
person relatives, and staff in a from cases et al. (2007), Leuenberger et al.
nursing home/hospital (2007), Simon et al. (2006),
Sommer et al. (2009)
Contact among patients, Epidemiology and NoV GII Calderon-Margalit et al. (2005)
relatives, and staff in from cases
multiple nursing homes
Contact among students at a Epidemiology and NoV NR Honish et al. (2008)
university residence from cases
Contact among guests at a Epidemiology and NoV NR Michel et al. (2007)
hotel from cases
Contact between passengers Epidemiology and NoV NR, GII.1, Chimonas et al. (2008),
on a ship from cases GII.4, GII.5 Sasaki et al. (2006)
Contact between passengers Epidemiology and NoV NR Holmes and Simmons (2009),
on a flight from cases Kirking et al. (2010)
Contact among evacuees in Epidemiology and NoV NR, GII.17 Nomura et al. (2008), Yee et al. (2007)
a shelter from cases
Contact between infants/ Epidemiology and NoV GI.4, GII.3, Uchino et al. (2006), Tsugawa et al.
children at a nursery from cases GII.6 (2006)
Exposure to vomit Epidemiology and NoV NR, GII.4 Holmes and Simmons (2009), Kuo
from cases et al. (2009b), Schmid et al. (2005b)
Fomites Environmental surfaces in a NoV sequenced from swabs GII.4 Wu et al. (2005)
long-term care facility and cases
 Surfaces in shared NoV detected from swabs NR Jones et al. (2007)
houseboats and cases
Computer surfaces in a NoV sequenced from swabs GII CDC (2008)
school and cases
Juice dispensing taps at a NoV sequenced from cases GII.4 Visser et al. (2010)
hotel with no other contact
Food Rolls prepared by NoV sequenced from GII de Wit et al. (2007)
handlers symptomatic baker worker and cases
Sandwiches and salads NoV sequenced from GI.3 Sala et al. (2005)
prepared by symptomatic worker and cases
handler
Pastry prepared by NoV sequenced from GII.4 Oogane et al. (2008)
symptomatic handler worker and cases
Wedding cakes decorated NoV sequenced from NR Friedman et al. (2005)
by symptomatic handler worker and cases
Salads prepared by NoV sequenced from GII.7 Schmid et al. (2007)
symptomatic handler worker and cases
Burgers assembled by NoV sequenced from GI.3 Zomer et al. (2010)
handler who later became worker and cases
symptomatic
Salads prepared by handler NoV sequenced from GII.6 Vivancos et al. (2009)
who later became worker and cases
symptomatic
Food served at a seminar, NoV sequenced from GI.3 Nordgren et al. (2010)
handler had been recovering worker and
previously symptomatic cases
Sandwiches prepared by NoV amplified from child of GII Kuo et al. (2009a)
asymptomatic handler worker and cases
(continued)
TABLE 1.1 (continued)

Outbreak NoV
type Outbreak source Data available genotype Reference

Sandwiches prepared by NoV detected from worker NR Godoy et al. (2005)

asymptomatic handler and cases
Food Hotel/resort/camp NoV sequenced from water Multiple, GIIb Hewitt et al. (2007), Kim et al. (2005),
and water source and clinical specimens Migliorati et al. (2008),
water ter Waarbeek et al. (2010)
Municipal water supply NoV detected or sequenced NR, multiple, Gallay et al. (2006), Scarcella et al.
in water and clinical GI.5 (2009), Werber et al. (2009)
specimens
Flood water Epidemiology NR Schmid et al. (2005a)
Recreational water NoV detected in water and NR Podewils et al. (2007), Sartorius et al.
clinical specimens (2007)
Shellfish NoV sequenced in food and Multiple David et al. (2007), Gallimore et al.
clinical specimens (2005a), Huppatz et al. (2008),
Iizuka et al. (2010), Le Guyader
et al. (2006b, 2010), Ng et al.
(2005), Sala et al. (2009), Symes
et al. (2007), Webby et al. (2007),
Westrell et al. (2010)
Frozen raspberries Epidemiology, NoV NR, GI.4 Hjertqvist et al. (2006), Korsager
sequenced in food and et al. (2005), Maunula et al. (2009)
clinical specimens
Lettuce Epidemiology, NoV Multiple Ethelberg et al. (2010), Gallimore
sequenced in food and et al. (2005b), Wadl et al. (2010)
clinical specimens
a
NR ¼ not reported.
 Norovirus as a Foodborne Disease Hazard 7

Siebenga et al., 2007b; Zheng et al., 2010). In each year, a novel strain was seen
to circulate, the number of NoV outbreaks increased to atypical levels in
many countries simultaneously ( Johansen et al., 2008; Lopman et al., 2004;
Siebenga et al., 2010). The testing of archived patient sera supports a hypoth-
esis where herd immunity is acquired at the community level to an existing
GII.4 strain, reducing the number and size of outbreaks in years without
novel variants (Cannon et al., 2009). The detection of a new variant strain in
the summer has been proposed as a predictor for winter epidemic seasons of
NoV infection (Verhoef et al., 2008).
GII.4 NoVs are the most common genotype in outbreak statistics. How-
ever, most data is obtained from institutions, and it is primarily in closed or
semiclosed settings that GII.4 NoVs have the largest impact (Blanton et al.,
2006; Bruggink et al., 2010; Kittigul et al., 2010; Lopman et al., 2003; Pang
et al., 2010). Studies that examine NoV genetic diversity in sewage and in
environmental samples typically identify a much larger proportion of GI
and other GII viruses. For example, 11 different NoV types were detected in
only 49 Dutch sewage samples (van den Berg et al., 2005). Testing in France
and Italy also determined that sewage samples contained a mixture of GI
and GII viruses in raw and treated sewage (da Silva et al., 2007; La Rosa
et al., 2010). Environmental water samples have also been shown to contain
both GI and GII NoVs (Kamel et al., 2010; La Rosa et al., 2007).
When outbreak surveillance focuses on food and waterborne trans-
mission routes, the GII.4 NoV no longer predominate as a source of illness
(Bon et al., 2005; Koek et al., 2006; Lysen et al., 2009; Pang et al., 2010). GI
NoVs are the most common strains identified in cases of waterborne
transmission (Lysen et al., 2009), while a mixture of GI and GII genotypes
has been associated with shellfish-related outbreaks (Bon et al., 2005;
Kageyama et al., 2004). This distinction has been presented as a mecha-
nism to predict the origin of an outbreak based on the genetic typing of
the infecting NoV strain, with a non-GII.4 etiology indicative of potential
food or waterborne transmission (Verhoef et al., 2009; Verhoef et al., 2010).
The GII.4 NoVs circulate widely in the community and exhibit very little
sequence variation within an epidemic season (Dingle, 2004), making it
difficult to establish an unambiguous epidemiological link between a
positive food product and the patient. Food testing could therefore be
focused on non-GII.4 outbreaks where the link between clinical and
environmental samples is more likely to be clearly established.

III. NOROVIRUS OUTBREAKS SPREAD PERSON TO PERSON

NoV can spread directly from person to person due to their low infectious
dose. Human volunteer studies have estimated that a single infectious NoV
particle could cause illness in a susceptible individual (Teunis et al., 2008).
8 Kirsten Mattison

There is a wide range of reported NoV attack rates during outbreaks (Harris
et al., 2010), but this is probably complicated by differing genetic suscept-
ibilities among those exposed. Different blood groups or Lewis antigen
profiles may confer susceptibility to different NoV genetic types
(Cheetham et al., 2007; Hutson et al., 2005; Lindesmith et al., 2003). Although
most studies agree that secretor positive individuals (with a functional
FUT2 allele) are susceptible to NoV infection, there are reports of NoV
illness in secretor negative persons (Carlsson et al., 2009; Marionneau
et al., 2005).
Many large surveillance studies have shown that the majority of NoV
outbreaks are caused by GII.4 NoV spread directly from person to person
in hospitals and long-term care facilities (Doyle et al., 2009; Godoy et al.,
2009; Kelly et al., 2008). It has been suggested that the predominance of
GII.4 infections can be explained by higher attack rates and more symp-
tomatic disease during GII.4 outbreaks than during infections with other
genetic types (Friesema et al., 2009b).
There is a large reservoir of NoV in the community, as evidenced by
surveys of community acquired and sporadic cases of gastroenteritis
(Buesa et al., 2002; Haustein et al., 2009; Karsten et al., 2009; Lindell et al.,
2005). Syndromic surveillance of vomiting reports also indicates that the
presence of NoV infections is constantly fluctuating in different areas
(Cooper et al., 2008). This widespread reservoir means that NoVs are
continually introduced into hospital settings where they can spread rap-
idly despite efforts to interrupt transmission (Cunliffe et al., 2010;
Koopmans, 2009; Sommer et al., 2009). Preventing the introduction of
this widespread pathogen is nearly impossible (Koopmans, 2009;
Yee et al., 2007).
NoV outbreaks that are spread directly from person to person do not
usually implicate a single-point source introduction, and the course of the
outbreak can be complicated (Grmek Kosnik et al., 2007). Multiple links
between outbreaks in different sectors or in different institutions may be
suggested, but only some of these will be supported by epidemiological
evidence (Calderon-Margalit et al., 2005; Lopman, 2006; Schmid et al.,
2005b). Multiple strains circulating in a single outbreak and the transfer
of infected persons between facilities can complicate epidemiology and
prolong the outbreak (Uchino et al., 2006; Yamagami and Hara, 2007).
There is the additional complication that hospital patients and long-term
care facility residents have other, pre-existing health concerns that can
contribute to an increased severity or prolonged course of NoV
disease (Siebenga et al., 2008; Simon et al., 2006; Tsang et al., 2008;
Westhoff et al., 2009).
Other closed or semiclosed settings where large person-to-person NoV
outbreaks have been documented are associated with travel, on cruise
ships and on airplanes. Cruise ships represent an interesting situation
 Norovirus as a Foodborne Disease Hazard 9

where a few infected passengers embarking can spread a low level of

infection among staffs and passengers with whom they have direct con-
tact (Cramer et al., 2006; Koopmans et al., 2006; Neri et al., 2008). The
presence of infection control measures does not seem to prevent NoV
transmission in this setting (Takkinen, 2006), and risk is more significantly
associated with case behavior than with environmental health measures
(Chimonas et al., 2008; Isakbaeva et al., 2005). Multiple viruses or strains
can cocirculate in these conditions and complicate efforts to trace the
source of infection (Sasaki et al., 2006). Transmission on airplanes is
more easily traced to an index event of vomiting or diarrhea within the
confined space of the aircraft (Holmes and Simmons, 2009; Kirking et al.,
2010). Attack rates of 5% or less among airplane passengers are not likely
to be linked to the flight and would probably be considered to be sporadic
cases in the absence of a dramatic reason for linking the cases
(Kornylo et al., 2009).
NoV outbreaks in hotels or schools have also been initiated by virus
spread directly from person to person. The cause can be a significant
vomiting event to which a large group is simultaneously exposed (Kuo
et al., 2009b; Michel et al., 2007), or it can be unknown but clearly diffuse in
origin (Honish et al., 2008). Outbreaks with no clear beginning or end and
no association with food or water are frequently identified as transmitted
from person to person, although fomite contamination is also often
suspected as a possible contributor to the spread of infection (Honish
et al., 2008).
NoV outbreaks in hospital settings can be expensive, with one case
report identifying costs totaling over $650,000 for a single outbreak
( Johnston et al., 2007). A 2007 review found that NoV outbreaks in
hospitals had a 44% rate of requiring unit closures, much higher than
the rates for other nosocomial pathogens (Hansen et al., 2007).
Recommendations for preventing and limiting the spread of person-
to-person outbreaks of NoV generally follow commonsense guidelines for
limiting the transmission of other infectious diseases (Friesema et al.,
2009a; Greig and Lee, 2009; Harris et al., 2010). However, NoV has a
very low infectious dose (Teunis et al., 2008) and resists environmental
disinfection (Girard et al., 2010; Terpstra et al., 2007), so the efficacy of any
individual control measure can be less than for bacterial or enveloped
viral targets. In fact, systematic literature reviews have failed to find a
statistical difference in the duration of NoV outbreaks whether pathogen-
specific control measures were or were not followed (Friesema et al.,
2009a; Greig and Lee, 2009; Harris et al., 2010). These reviews are all
complicated by the fact that they cannot account for the impact of basic
infection control measures already present before an outbreak (Harris
et al., 2010). Mathematical modeling indicates that one important param-
eter for stopping NoV outbreaks in semiclosed settings is the short-term
10 Kirsten Mattison

immunity acquired by the exposed population during the course of the

outbreak (Vanderpas et al., 2009).
Nonetheless, infection control measures are universally recommended
to limit the person-to-person spread of NoV (Harris et al., 2010). One
study identified reduced illness among staff members as a result of
infection control (Vivancos et al., 2010b), and a review has identified
that some measures can reduce the number of illnesses, if not the duration
of the outbreak (Friesema et al., 2009a). It is important to note that as a
direct result of the person-to-person transmission route, the enhanced
disinfection of surfaces is not sufficient to control these outbreaks (CDC,
2009a,b; Vivancos et al., 2010a). This distinguishes them from outbreaks
transmitted via point source fomite contamination, which are discussed
in Section IV. For outbreaks spread directly between individuals, limiting
interaction between infected and uninfected persons is critical. Cohorting
of patients within medical facilities, exclusion of staff for up to 72 h
following an attack of gastroenteritis, and cancellation of social events
have all been recommended (CDC, 2009a; Rao et al., 2009; Vivancos et al.,
2010b). The use of personal protective equipment when working with
patients or patient samples has been identified as a factor affecting out-
break spread (CDC, 2009b; Ebihara et al., 2008). In addition, hand hygiene
has been particularly well studied as a method of interrupting transmis-
sion of NoV during outbreaks (Gilbride et al., 2009; Heijne et al., 2009; Moe
et al., 2001; Surgeoner et al., 2009), although the efficacy of alcohol-based
hand rubs against NoV is controversial (Bloomfield et al., 2007; Cheng
et al., 2009; Liu et al., 2010; Macinga et al., 2008; Steinmann et al., 2010).
Some studies indicate that washing with soap and water is required to
eliminate NoV transmission (Bidawid et al., 2004; Lages et al., 2008; Liu
et al., 2010; Martin et al., 2008), while others suggest that ethanol-based
rubs are sufficient as an infection control tool (Cheng et al., 2009). All
authors agree that the use of hand rubs is indicated where soap and water
are not available (CDC, 2009a; Steinmann et al., 2010).

IV. NOROVIRUS OUTBREAKS SPREAD BY FOMITE

CONTAMINATION

NoV are readily transferred from hands to fomites and vice versa
(Bidawid et al., 2004; D’Souza et al., 2006). The pronounced environmental
stability of NoV particles also contributes to the spread of outbreaks from
point sources of surface contamination. All stability studies have made
use of surrogate organisms to model NoV response to conditions, since
the human virus is not easily grown in cell culture (Duizer et al., 2004b;
Straub et al., 2007). The murine norovirus (MNV) and the feline calicivirus
(FCV) have both been used, with the mouse virus providing more
 Norovirus as a Foodborne Disease Hazard 11

relevant data under conditions of low pH (Cannon et al., 2006). Efforts

have been made to develop methods to quantify human NoV persistence
and disinfection by detection of genetic material (Lamhoujeb et al., 2008;
Mormann et al., 2010; Ngazoa et al., 2008; Nuanualsuwan and Cliver, 2002;
Topping et al., 2009), but the correlation of genetic material to infectious
titer remains controversial (Baert et al., 2008c; Hewitt et al., 2009;
Rodriguez et al., 2009). Persistence of infectious FCV has been demon-
strated for up to 7 days dried on stainless steel, formica, or ceramic
surfaces (D’Souza et al., 2006; Mattison et al., 2007). Other more complex
inanimate surfaces, such as telephone buttons and computer keyboards,
support the survival of infectious FCV for 0.5–3 days (Clay et al., 2006).
The particular resistance of NoV to disinfection is an additional factor
in the spread of NoV infections from contaminated fomites. Table 1.2
presents a summary of studies on disinfection of the FCV and MNV
surrogates. Data from disinfection studies must be interpreted with
care, as many demonstrate efficacy in suspension tests (Beekes et al.,
2010; Belliot et al., 2008; Duizer et al., 2004a; Poschetto et al., 2007), but
the carrier test using surface-dried virus is more appropriate for surface
cleaners (Terpstra et al., 2007). Contact time also plays an important role,
with some disinfectants exhibiting efficacy after 10 min that cannot be
demonstrated after 1 min ( Jimenez and Chiang, 2006; Whitehead and
McCue, 2010). In general, 1000 ppm of available chlorine effectively
inactivates the FCV and MNV surrogates (D’Souza et al., 2009; Girard
et al., 2010; Whitehead and McCue, 2010). Hypochlorous acid, trisodium
phosphate, sodium bicarbonate, and glutaraldehyde are also effective on
surfaces, at sufficient concentrations and contact times (D’Souza et al.,
2009; Magulski et al., 2009; Malik and Goyal, 2006; Malik et al., 2006a; Park
et al., 2007). Alcohols and quaternary ammonium compounds are less
effective against the Caliciviruses (D’Souza et al., 2009; Gulati et al., 2001;
Magulski et al., 2009; Malik et al., 2006b; Solomon et al., 2009; Whitehead
and McCue, 2010), although combinatorial formulations can be effective
(Malik et al., 2006a; Whitehead and McCue, 2010). These should be eval-
uated on a case-by-case basis, using a protocol based on their proposed
use (i.e., surface carrier test for surface disinfectants, fingerpad test for
hand rubs) (Macinga et al., 2008; Whitehead and McCue, 2010). More
complex surfaces, such as woven fabrics, carpets, or porous materials,
can be more difficult to disinfect (Malik et al., 2006a). UV disinfection
overcomes some of the issues with soft fabrics, but the light must reach
all crevices to be effective (Lee et al., 2008). The use of gas disinfection in
sealed rooms is an interesting alternative to reach all areas, but
this requires long incubation times and the ability to seal an area
(Hudson et al., 2007).
There is not always a clear distinction between outbreaks transmitted
via inanimate surfaces as compared to those that are linked to direct
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