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Transmission cycles, host range, evolution and emergence of arboviral disease

Nature Reviews Microbiology volume 2, pages 789–801 (2004)Cite this article

Key Points

  • Many recent viral pandemics have been attributed to the ability of some RNA viruses, for example HIV, dengue virus and possibly the severe acute respiratory syndrome (SARS) coronavirus, to change their host range to include humans. The authors discuss the mechanisms of host-range alteration used by a selection of viruses, including Venezuelan equine and Japanese encephalitis viruses (VEEV and JEV, respectively), dengue virus and West Nile virus (WNV).

  • Venezuelan equine encephalitis (VEE) was first recognized as a disease of horses, donkeys and mules in northern South America during the mid 1930s, but there has been renewed interest in this virus because of its potential as a biological weapon. Molecular analysis of epidemic strains — which exploit horses for amplification — and comparison with strains that do not cause epidemic disease, have shown that a few amino-acid mutations can affect host-range alteration. Changes on the surface of the VEE virion seem to be important for these host range changes.

  • JEV causes epidemics of encephalitis in India, Korea, China, South-East Asia and Indonesia. The disease affects children, and is associated with a mortality rate of greater than 20%. However, unlike VEEV, there is no evidence that JEV undergoes mutation and selection to replicate in different hosts. Pigs amplify transmission in peridomestic settings, and migratory birds have a role in dispersion of JEV. Although different genotypes have been isolated, their relevance to pathology and host range is unclear.

  • WNV is now endemic in the United States after first emerging in New York in 1999. WNV has a very broad host range. Forty-nine species of mosquitoes and ticks, and 225 species of birds are susceptible to infection. Other hosts include horses, cattle, llamas, alligators, cats, dogs, wolves and sheep. Transmission of WNV among these species has not been reported. Although humans are probably dead-end hosts, infection with WNV can cause severe disease.

  • Dengue viruses are very important human arboviral pathogens and use humans as reservoir hosts. Aedes aegypti and Aedes albopictus mosquitoes are the most common vectors in urban settings. It is thought that the human epidemic form of dengue virus evolved in the last 2000 years, and genetic analysis indicates that mutations have resulted in adaptation to the urban mosquito host. However, links between mutations and human pathogenicity have not been established.

  • Finally, the authors discuss how host-range changes can be studied experimentally. Cell-culture model systems can be used to find mutations that correlate with virus fitness and adaptation in different host strains. Viruses that replicate in useful laboratory animal models can also be studied in whole animal hosts.

Abstract

Many pandemics have been attributed to the ability of some RNA viruses to change their host range to include humans. Here, we review the mechanisms of disease emergence that are related to the host-range specificity of selected mosquito-borne alphaviruses and flaviviruses. We discuss viruses of medical importance, including Venezuelan equine and Japanese encephalitis viruses, dengue viruses and West Nile viruses.

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Figure 1: Locations of Venezuelan equine encephalitis virus outbreaks in the Americas.
Figure 2: Venezuelan equine encephalitis emergence — a phylogenetic tree.
Figure 3: Phylogenetic trees of Japanese encephalitis virus.
Figure 4: Evolutionary history of dengue virus emergence.

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Acknowledgements

S.C.W. is suppported by the National Institutes of Health. A.D.T.B. is supported by the State of Texas Higher Education Coordinating Board and the Centers for Diseases Control.

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Authors and Affiliations

  1. Department of Pathology, Microbiology and Immunology, Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, 77555-0609, Texas, USA

    Scott C. Weaver

  2. Department of Pathology, Microbiology and Immunology, Center for Tropical Diseases, University of Texas Medical Branch, Galveston, 77555-0609, Texas, USA

    Alan D. T. Barrett

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DATABASES

Entrez

DENV

JEV

VEEV

WNV

Infectious Disease Database

arboviral infections

dengue haemorrhagic fever

Japanese encephalitis

WNV infection

FURTHER INFORMATION

Disease watch Focus: Dengue

Glossary

EPIZOOTIC

Higher than average amplification, or occurrence, of a disease or pathogen in non-human animals.

STRAINS

Individual isolates or variants of a virus.

VIRAEMIA

Presence of virus in the bloodstream — usually essential for transmission of arboviruses by arthropod vectors.

SYLVATIC

Occurring in forest habitats.

ENZOOTIC

A disease or maintenance transmission cycle occurring continuously among non-human animals in a particular region or locality.

SUBTYPE

A distinct virus variant that can be antigenically distinguished from other closely related variants.

SYMPATRIC

Having overlapping geographical distributions.

ZOONOTIC

Pathogens or diseases that normally circulate among non-human animals but that can be transmitted to humans.

OLD WORLD

Those parts of the world known to Europeans before the voyages of Christopher Columbus — Europe, Asia and Africa. The New World refers to the American continents.

PERIDOMESTIC

In, and around, human habitations.

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Weaver, S., Barrett, A. Transmission cycles, host range, evolution and emergence of arboviral disease. Nat Rev Microbiol 2, 789–801 (2004). https://doi.org/10.1038/nrmicro1006

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