Viral Gastroenteritis. Molecular Epidemiology and Pathogenesis

563 Pages·2016·30.298 MB·English

by  Lennart Svensson, Ulrich Desselberger, Mary K Estes, Harry B Greenberg

Viral Gastroenteritis
Molecular Epidemiology and Pathogenesis
Edited by
Lennart Svensson
Division of Molecular Virology
Departments of Clinical and Experimental Medicine
Medical Faculty, Linköping University
Linköping, Sweden
Ulrich Desselberger
Department of Medicine, University of Cambridge
Addenbrooke’s Hospital, Cambridge, United Kingdom
Harry B. Greenberg
Departments of Microbiology and Immunology
Department of Medicine Stanford University, Stanford;
VA Palo Alto Health Care System
Palo Alto, CA, United States
Mary K. Estes
Departments of Molecular Virology and Microbiology
Baylor College of Medicine
Houston, TX, United States
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Contributors
N.J. Ajami, The Alkek Center for Metagenomics and Microbiome Research, Baylor
College of Medicine; Department of Molecular Virology and Microbiology, Baylor
College of Medicine, Houston, TX, United States
J. Angel, Instituto de Genética Humana, Facultad de Medicina, Pontificia Universidad
Javeriana, Bogotá, Colombia
M. Angel, Laboratory of Infectious Diseases, National Institute of Allergy and Infectious
Diseases, National Institutes of Health, Bethesda, MD, United States
C.F. Arias, Departamento de Genética del Desarrollo y Fisiología Molecular,
Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca,
Morelos, México
R.L. Atmar, Departments of Molecular Virology and Microbiology, and Medicine,
Baylor College of Medicine, Houston, TX, United States
K. Bányai, Institute for Veterinary Medical Research, Centre for Agricultural Research,
Hungarian Academy of Sciences, Budapest, Hungary
P. Brandtzaeg, Laboratory for Immunohistochemistry and Immunopathology (LIIPAT),
Centre for Immune Regulation (CIR), University of Oslo and Department of Pathology,
Oslo University Hospital Rikshospitalet, Oslo, Norway
W. Cheung, Department of Medicine, University of Cambridge, Addenbrooke’s
Hospital, Cambridge, United Kingdom
J.-M. Choi, Verna and Marrs McLean Department of Biochemistry and Molecular
Biology, Baylor College of Medicine, Houston, TX, United States
S.E. Crawford, Department of Molecular Virology and Microbiology, Baylor College
of Medicine, Houston, TX, United States
J.B. Cunha, Department of Microbiology and Immunology, University of Michigan
Medical School, Ann Arbor, MI, United States
U. Desselberger, Department of Medicine, University of Cambridge, Addenbrooke’s
Hospital, Cambridge, United Kingdom
M.A. Díaz-Salinas, Departamento de Génetica del Desarrollo y Fisiología Molecular,
Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca,
Morelos, México
P.R. Dormitzer, Novartis Influenza Vaccines, Cambridge, MA, United States
xv
xvi Contributors
M.D. Elftman, Department of Biomedical and Diagnostic Sciences, University of
Detroit Mercy, School of Dentistry, Detroit, MI, United States
M.K. Estes, Departments of Molecular Virology and Microbiology, and Medicine,
Baylor College of Medicine, Houston, TX, United States
M.A. Franco, Instituto de Genética Humana, Facultad de Medicina, Pontificia
Universidad Javeriana, Bogotá, Colombia
R.R. Garg, College of Medicine, Department of Molecular Genetics and
Microbiology, Emerging Pathogens Institute, University of Florida, Gainesville, FL,
United States
E. Gaunt, Department of Medicine, University of Cambridge, Addenbrooke’s Hospital,
Cambridge, United Kingdom
I. Goodfellow, Division of Virology, Department of Pathology, University of Cambridge,
Addenbrooke’s Hospital, Cambridge, United Kingdom
K.Y. Green, Caliciviruses Section, Laboratory of Infectious Diseases, National Institute
of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD,
United States
H.B. Greenberg, Departments of Microbiology and Immunology, Department of
Medicine, Stanford University, School of Medicine, Stanford; VA Palo Alto Health Care
System, Palo Alto, CA, United States
M. Hagbom, Division of Molecular Virology, Department of Clinical and Experimental
Medicine, Medical Faculty, Linköping University, Linköping, Sweden
L. Hammarström, Division of Clinical Immunology and Transfusion Medicine,
Department of Laboratory Medicine, Karolinska Institutet at Karolinska University
Hospital Huddinge, Stockholm, Sweden
S.C. Harrison, Laboratory of Molecular Medicine, Boston Children’s Hospital,
Harvard Medical School, and Howard Hughes Medical Institute, Boston, MA,
United States
D. Herrera, Instituto de Genética Humana, Facultad de Medicina, Pontificia Universidad
Javeriana, Bogotá, Colombia
P. Isa, Departamento de Génetica del Desarrollo y Fisiología Molecular, Instituto de
Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos,
Mexico
S. Kandasamy, Food Animal Health Research Program, The Ohio Agricultural
Research and Development Center, Department of Veterinary Preventive Medicine, The
Ohio State University, Wooster, OH, United States
G. Kang, The Wellcome Trust Research Laboratory, Division of Gastrointestinal
Sciences, Christian Medical College, Vellore, Tamil Nadu, India
S.M. Karst, College of Medicine, Department of Molecular Genetics and Microbiology,
Emerging Pathogens Institute, University of Florida, Gainesville, FL, United States
Contributors xvii
P. Khamrin, Department of Microbiology, Faculty of Medicine, Chiang Mai University,
Chiang Mai, Thailand
A.O. Kolawole, Department of Microbiology and Immunology, University of Michigan
Medical School, Ann Arbor, MI, United States
G. Larson, Department of Clinical Chemistry and Transfusion Medicine, Sahlgrenska
Academy, University of Gothenburg, Gothenburg, Sweden
J. Le Pendu, Inserm, CNRS, Nantes University, IRS UN, Nantes, France
A. Lever, Department of Medicine, University of Cambridge, Addenbrooke’s Hospital,
Cambridge, United Kingdom
S. López, Departamento de Génetica del Desarrollo y Fisiología Molecular, Instituto
de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos,
México
T. López, Departamento de Génetica del Desarrollo y Fisiología Molecular, Instituto
de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos,
México
N. Maneekarn, Department of Microbiology, Faculty of Medicine, Chiang Mai
University, Chiang Mai, Thailand
H. Marcotte, Division of Clinical Immunology and Transfusion Medicine, Department
of Laboratory Medicine, Karolinska Institutet at Karolinska University Hospital
Huddinge, Stockholm, Sweden
S. Marvin, Department of Infectious Diseases, St. Jude Children’s Research Hospital,
Memphis, TN, United States
V.A. Meliopoulos, Department of Infectious Diseases, St. Jude Children’s Research
Hospital, Memphis, TN, United States
Z. Muhaxhiri, Verna and Marrs McLean Department of Biochemistry and Molecular
Biology, Baylor College of Medicine, Houston, TX, United States
A. Murillo, Departamento de Genética del Desarrollo y Fisiología Molecular, Instituto
de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos,
México
W. Nasir, Department of Clinical Chemistry and Transfusion Medicine, Sahlgrenska
Academy, University of Gothenburg, Gothenburg, Sweden
A. Navarro, Laboratory of Infectious Diseases, National Institute of Allergy and
Infectious Diseases, National Institutes of Health, Bethesda, MD, United States
M. Parra, Instituto de Genética Humana, Facultad de Medicina, Pontificia Universidad
Javeriana, Bogotá, Colombia
J.T. Patton, Laboratory of Infectious Diseases, National Institute of Allergy and
Infectious Diseases, National Institutes of Health, Bethesda, MD, United States; Virginia-
Maryland College of Veterinary Medicine, University of Maryland, MD, United States
xviii Contributors
J.F. Petrosino, The Alkek Center for Metagenomics and Microbiome Research, Baylor
College of Medicine, Department of Molecular Virology and Microbiology, Baylor
College of Medicine, Houston, TX, United States
V.E. Pitzer, Department of Epidemiology of Microbial Diseases, Yale School of Public
Health, New Haven, CT, United States
B.V. Venkataram Prasad, Verna and Marrs McLean Department of Biochemistry
and Molecular Biology; Departments of Molecular Virology and Microbiology, and
Medicine, Baylor College of Medicine, Houston, TX, United States
S. Ramani, Department of Molecular Virology and Microbiology, Baylor College of
Medicine, Houston, TX, United States
G.E. Rydell, Department of Infectious Diseases, Sahlgrenska Academy, University of
Gothenburg, Gothenburg, Sweden
L.J. Saif, Food Animal Health Research Program, The Ohio Agricultural Research and
Development Center, Department of Veterinary Preventive Medicine, The Ohio State
University, Wooster, OH, United States
N.P. Sastri, Department of Molecular Virology and Microbiology, Baylor College of
Medicine, Houston, TX, United States
S. Schultz-Cherry, Department of Infectious Diseases, St. Jude Children’s Research
Hospital, Memphis, TN, United States
A. Sen, Departments of Microbiology and Immunology, Department of Medicine,
Stanford University, School of Medicine, Stanford; VA Palo Alto Health Care System,
Palo Alto, CA, United States
S. Shanker, Verna and Marrs McLean Department of Biochemistry and Molecular
Biology, Baylor College of Medicine, Houston, TX, United States
D. Silva-Ayala, Departamento de Genética del Desarrollo y Fisiología Molecular,
Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca,
Morelos, México
L. Svensson, Division of Molecular Virology, Department of Clinical and Experimental
Medicine, Medical Faculty, Linköping University, Linköping, Sweden
S. Taube, Institute of Virology and Cell Biology, University of Lübeck, Lübeck,
Germany
H. Ushijima, Division of Microbiology, Department of Pathology and Microbiology,
Nihon University School of Medicine, Tokyo, Japan
T. Vesikari, Vaccine Research Center, University of Tampere Medical School, Tampere,
Finland
A.N. Vlasova, Food Animal Health Research Program, The Ohio Agricultural Research
and Development Center, Department of Veterinary Preventive Medicine, The Ohio
State University, Wooster, OH, United States
Contributors xix
L. Williamson, Laboratory of Infectious Diseases, National Institute of Allergy and
Infectious Diseases, National Institutes of Health, Bethesda, MD, United States
C.E. Wobus, Department of Microbiology and Immunology, University of Michigan
Medical School, Ann Arbor, MI, United States
N.C. Zachos, Hopkins Conte Digestive Disease Basic and Translational Research Core
Center, Department of Medicine, Division of Gastroenterology and Hepatology, Johns
Hopkins University School of Medicine, Baltimore, MD, United States
Introduction
Acute gastroenteritis (AGE) in infants and young children (of <5 years of age)
is a very frequent disease worldwide. A decade ago, 1.4 billion cases of AGE
were recorded in this age group annually, of which 475 million occurred in
children of <1 years of age and 945 million in those of 1–4 years of age (Para-
shar et al., 2003). For 2010, worldwide 1.7 billion cases of AGE were estimated
to have occurred in children of <5 years of age (Fischer Walker et al., 2013).
In 2003, most episodes of acute diarrhea (1.3 billion) were cared for at home,
124 million required a visit to a general practitioner, pediatrician or primary
care center, and for 9 million children hospitalization was necessary. On aver-
age association with rotavirus infection was 1.8% for children in home care
and 19–21% for children requiring medical advice and intervention (Parashar
et al., 2003). In terms of mortality, in 2008 AGE in children ranged in third
place as a cause after neonatal disease and pneumonia worldwide (Table 1; Liu
et al., 2012). In absolute numbers, 11.7 million children/annum died from all
causes, of those 1.3 million from diarrhea and dehydration, with rotavirus (RV)
disease as leading cause of death in 453,000 children (34.8%; Table 2; Tate
et al., 2012). Childhood mortality from RV disease was highest in India, Nige-
ria, Pakistan, DR of Congo, Ethiopia, and Afghanistan, where almost two thirds
of all cases occurred (Table 2, Tate et al., 2012). However, for 2011 the num-
ber of death from RV-associated diarrhea worldwide was estimated to be lower
at about 193,000 (95% CI 133,000–284,000) (Fischer Walker et al., 2013).
Since 2006 two live attenuated RV vaccines have been licensed and become
part of universal childhood vaccination schedules in over 80 countries. RV vac-
cination has reduced hospitalization and clinical visits for RV disease signifi-
cantly in countries of temperate climate (eg, Payne et al., 2013a; Gastañaduy
et al., 2013a; Akikusa et al., 2013), less so in countries of the developing world
(sub-Saharan Africa, SE Asia) where RV vaccination is needed most (Armah
et al., 2010; Madhi et al., 2010; Zaman et al., 2010). In several countries, a very
substantial reduction of RV-associated disease and mortality has been recorded
(Gastañaduy et al., 2013b; Zhang et al., 2015), contributing to the overall de-
crease of death from RV-associated AGE (Fischer Walker et al., 2013).
Other viral causes of AGE in childhood are infections with human cali-
civiruses (noroviruses, sapoviruses), astroviruses, and more rarely, enteric
adenoviruses, enteroviruses and picobirnaviruses (Gray and Desselberger, 2009;
Estes and Greenberg, 2013). Human noroviruses (NoVs) have become the most
frequent viral enteric pathogen in childhood several years after introduction of
xxi
xxii Introduction
TABLE 1 Causes of Childhood Mortality Worldwide in 2010
Childhood mortality 2010
Global causes %
Neonatal causes 40
Pneumonia 18
Diarrhea 11
Malaria 7
AIDS 2
Meningitis 2
Measles 1
Other 19
From Liu et al., 2012. Lancet 379, 2151–2161.
TABLE 2 Mortality in Children <5 Years of Age From Diarrhea Worldwide
No./annum
All causes 11,700,000
Diarrhea (11% of all) 1,300,000
Rotavirus-associated diarrhea 453,000 38.4%a
(95% CI 423,000–494,000)
Countries with greatest
mortality No. of deaths % of all
India 98,600 22
Nigeria 41,100 9
Pakistan 39,100 9
DR of Congo 32,600 7
Ethiopia 28,200 6
Afghanistan 25,400 6 59%
aPercentage of all deaths from severe diarrhea.
From Tate et al., 2012. Lancet Infect. Dis. 12, 136–141.
universal RV vaccination (Payne et al., 2013b; Koo et al., 2013). Work on de-
veloping a vaccine against NoV disease is ongoing (Atmar and Estes, 2012;
Richardson et al., 2013).
The facts outlined above emphasize the enormous significance of viruses as
cause of diarrheal disease in humans, particularly young children, worldwide.
During the last decade substantial progress has been made in characterizing the
molecular biology (structure–function relationships, replication), pathogenesis
Introduction xxiii
of and immune responses to the viruses causing AGE. In the course of this, a lot
has been learned about various functions of gastrointestinal cells and the gastro-
intestinal immune system, and the opportunities for further discoveries in these
research areas are immense. There is a huge potential for applying the knowl-
edge obtained from basic and translational studies of the enteric viral pathogens
to counteract the impact of these viruses on acute illness and public health.
The book has been subdivided into five sections. The first (overview) sec-
tion presents recent advances in gastrointestinal physiology and pathophysiol-
ogy (Chapter 1.1), mechanisms and functions of gut immunity (Chapter 1.2),
primary immunodeficiencies and their significance for gastrointestinal disease
(Chapter 1.3), and outlines of present day therapy of AGE in children (Chapter1.4).
The second section is devoted to rotaviruses (RVs). Based on exact knowl-
edge of the RV particle structure at the atomic level and assigned functions
(Chapter 2.1), several chapters are committed to viral replication issues: cellular
receptors and coreceptors involved in RV entry (Chapter 2.2), structure-function
studies of the RV enterotoxin NSP4 (Chapter 2.4), the structural and functional
interaction of cellular lipid droplets with RV viroplasms (Chapter 2.5), and an
overview of the RV replication mechanisms and of attempts to create a tracta-
ble, nucleic acid only-based reverse genetics (RG) system (Chapter 2.3). Newer
data on RV pathophysiology (Chapter 2.6), on innate immune responses to RV
infection (Chapter 2.8) and on acquired immunity to RV disease including a dis-
cussion on correlates of protection (Chapter 2.9) are substantially based on the
availability of animal models of RV infection and disease (Chapter 2.7). The ad-
vent of whole genome sequencing combined with bio-informatics has advanced
RV classification and has revitalized studies of the molecular epidemiology and
evolution of human and animal RV strains (Chapter 2.10). Rotavirus vaccine
development is lively: in addition to the two licensed RV vaccines mentioned
above, new RV vaccines are under investigation or have recently been licensed
in various parts of the world (Chapter 2.11).
The successes of RV vaccination programs have directed increasing attention
to human caliciviruses and, more specifically, the human NoVs that are major
causes of children’s AGE besides being the lead agents of food-borne, nonbac-
terial AGE outbreaks in population groups of all ages worldwide. Norovirus
particle structures have been studied in great detail (Chapter 3.1). In contrast to
RVs, for certain NoVs fully tractable RG systems have been successfully estab-
lished (Chapter 3.2), permitting rational genotype–phenotype correlation stud-
ies. However, the continued failure to identify a tractable cell culture replication
system or animal model system for human NoVs has limited the extent to which
the NoV RG system can be optimally used. Human histo-blood group antigens
were recognized as cellular receptors for NoVs (Chapter 3.3) and recently also
for RVs (Chapter 2.2) (Hu et al., 2012; Tan and Jiang, 2014). Mouse NoVs
grow in murine macrophage cultures, have an established RG system, and can
be tested in various animal models (Chapter 3.4). The increasing significance of
human NoVs has been analysed in numerous molecular epidemiological studies