One Health

People, Animals, and the Environment

Ronald M. Atlas, Stanley Maloy, Ronald M. Atlas, Stanley Maloy

• Publisher: ASM Press
• Year: 2014
• ISBN:
  9781683673460
• Edition: 1
• Topic: Medicine
• Subtopic: Infectious Diseases

Emerging infectious diseases are often due to environmental disruption, which exposes microbes to a different niche that selects for new virulence traits and facilitates transmission between animals and humans. Thus, health of humans also depends upon health of animals and the environment – a concept called One Health. This book presents core concepts, compelling evidence, successful applications, and remaining challenges of One Health approaches to thwarting the threat of emerging infectious disease.

Written by scientists working in the field, this book will provide a series of "stories" about how disruption of the environment and transmission from animal hosts is responsible for emerging human and animal diseases.

• Explains the concept of One Health and the history of the One Health paradigm shift.
• Traces the emergence of devastating new diseases in both animals and humans.
• Presents case histories of notable, new zoonoses, including West Nile virus, hantavirus, Lyme disease, SARS, and salmonella.
• Links several epidemic zoonoses with the environmental factors that promote them.
• Offers insight into the mechanisms of microbial evolution toward pathogenicity.
• Discusses the many causes behind the emergence of antibiotic resistance.
• Presents new technologies and approaches for public health disease surveillance.
• Offers political and bureaucratic strategies for promoting the global acceptance of One Health.

Zoonotic and Environmental Drivers of
Emerging Infectious Diseases

Chapter 6

RNA Viruses: A Case Study of the Biology of Emerging Infectious Diseases

Mark E. J. Woolhouse,1 Kyle Adair,1 and Liam Brierley1

1Centre for Immunity, Infection & Evolution, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom.

INTRODUCTION

Viruses account for only a small fraction of the 1400 or more different species of pathogen that plague humans—the great majority are bacteria, fungi, or helminths (1). However, as both the continuing toll of childhood infections such as measles and recent experience of AIDS and influenza pandemics illustrate, viruses are rightly high on the list of global public health concerns (2). Moreover, the great majority of newly recognized human pathogens over the past few decades have been viruses (3) and a large fraction of emerging infectious disease “events” have involved viruses (4).

There are two kinds of viruses: RNA viruses and DNA viruses. The latter largely consist, with the exception of a handful of pox- and herpesviruses, of viruses that have probably been present in and coevolved with humans for long periods of time. RNA viruses are very different. The majority of RNA viruses that infect humans are zoonotic, meaning that they can infect vertebrate hosts other than humans. Many of those that are not regarded as zoonotic are believed to have had recent (in evolutionary terms) zoonotic origins. So it is the RNA viruses that are of greatest interest in the context of One Health.

In this chapter, we review current knowledge of how RNA viruses in humans and other vertebrates are related, in terms of both of their evolution and their ecology, with the intention of trying to understand where human RNA viruses came from in the past and where new ones might emerge in the future. Until recently, research on these topics was essentially a series of case studies. Extraordinary work has been done detailing events such as the historical emergence of HIV-1 in Central Africa (5) and the more recent emergence of Nipah virus in Southeast Asia (6). But while every emergence event is a fascinating story in its own right, our aim here is to look beyond the specifics and to try to identify any underlying generalities that tell us something useful about the emergence of RNA viruses as a biological process.

We begin by comparing the RNA viruses reported to infect humans with RNA virus diversity as a whole and exploring the overlap between viruses in humans and viruses in other kinds of hosts. Next, we refine the analysis by distinguishing among viruses according to their ability not just to infect humans but also to transmit from one human to another, which is a prerequisite for a virus being able to cause major epidemics and/or become an established, endemic human pathogen. We then consider in more detail the subset of human RNA viruses that can persist in human populations without the need for a nonhuman reservoir. Next, we attempt to identify characteristics of RNA viruses that allow them to cross the species barrier and those that predispose them to cause severe disease, as such viruses are of particular public health concern. We go on to discuss how new human RNA viruses arise (sometimes to subsequently disappear again). From the information assembled we construct a conceptual model of the relationship between RNA viruses in humans and other hosts. We consider how this model might be of practical value, concentrating on risk assessments for newly discovered viruses and also the much discussed topic of the design of surveillance programs for emerging infectious diseases.

DIVERSITY OF HUMAN RNA VIRUSES

The diversity of human RNA viruses was recently surveyed using a formal methodology (3), and we update that information here. All RNA viruses known to infect humans were included, with the exception of those only known to do so as the result of deliberate laboratory exposures.

In this chapter, we use virus species as designated by the Ninth Report of the International Committee for the Taxonomy of Viruses (ICTV) (7) (noting that this differs from earlier ICTV reports used in previous work and that it will doubtless change again in the not-too-distant future). ICTV designations may not always accurately reflect the biological meaning of a “species,” i.e., reproductive isolation. The operational criteria used for RNA viruses may include any or all of (i) phylogenetic relatedness based on sequence data, (ii) serological cross-reactivity, (iii) host range, and (iv) transmission route. It is also important to note that any analysis at the level of a virus species implicitly ignores a great deal of biomedically relevant diversity. This point is best illustrated by the influenza A viruses: the epidemiology and public health importance of seasonal influenza A and the H5N1 or H7N9 “bird flu” variants are very different, but all are included within a single species. Less variable virus species than influenza A may still contain multiple serotypes and other functionally distinct subtypes. Despite these limitations, the species remains the most useful unit for studying virus diversity currently available.

Updating the earlier survey (3) with new taxonomic information (7) reveals 180 recognized species of RNA viruses that have been reported to infect humans. These viruses represent 50 genera and 17 families (with one genus, Deltavirus, currently unassigned to a family). It is not immediately obvious what we should make of this. Is 180 a large number or a small one? Should we be surprised that it is not much higher or that it is not much lower? We consider such questions further below. We can, at least, be sure that 180 is an underestimate. New human RNA virus species are still being discovered or recognized at a rate of approximately 2 per year, although recent work (8) has suggested that the pool of undiscovered species could be much smaller than previously proposed (3). Even if we still have very little idea of the number of species “out there,” it is, as we will consider in detail later on, possible to say something about where “out there” is.

The possibility of large numbers of as yet unrecognized viruses also raises the specter of ascertainment bias. Certain kinds of RNA viruses may be underrepresented, perhaps dramatically so, among those currently recognized. These might be viruses from particular taxonomic groups, those associated with less severe disease or certain kinds of symptoms, or simply those that are rare and/or occur in less studied regions of the world. While this is clearly an issue, it is worth pointing out that both the rates and kinds of RNA viruses being discovered or recognized have been remarkably consistent for the past half century, despite massive changes in the technologies for virus detection and identification and considerable variability in the effort put into virus discovery in different places and at different times (3).

RNA VIRUSES OF HUMANS AND NONHUMANS

One striking observation is that 160 species of human-infective RNA virus species (89% of the total) are regarded as zoonotic; i.e., they can also infect other kinds of vertebrate hosts. (The definition of “zoonotic” ignores arthropod vectors; these are regarded as specialized transmission routes rather than alternative host species.) The nonhuman hosts usually (>90% of all zoonotic RNA virus species) include other mammals and less commonly (<40%) birds. Humans rarely, if ever, share their RNA viruses with anything else. Although the bias toward sharing viruses with other mammals is obvious, it is less clear whether we preferentially share viruses with particular kinds of mammals. Many human viruses (both RNA and DNA) are shared with ungulates, carnivores, rodents, primates, or bats (3), but our knowledge of the host range of most viruses is too incomplete for us to be confident about any underlying patterns. The remaining 20 RNA viruses are not known to naturally infect nonhuman hosts. However, most of these have close relatives that can infect other mammals. The only exceptions are hepatitis C, hepatitis delta, and rubella virus.

The overlap between the ability to infect humans and the ability to infect other mammals can be illustrated in other ways, too. Of the 62 recognized RNA virus genera containing species that can infect at least one kind of mammal, 50 (81%) contain species that can infect humans. And of the 19 recognized RNA virus families that contain species reported to infect mammals, all but 2 include species found in humans. The exceptions are the Nodavi...