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  • Review Article
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The arrival, establishment and spread of exotic diseases: patterns and predictions

Nature Reviews Microbiology volume 8, pages 361–371 (2010)Cite this article

Subjects

Key Points

  • Six case studies illustrate how the common emergence of exotic vector-borne zoonotic infections depends on the three sequential steps of arrival, establishment and spread.

  • Within the marginally suitable environmental conditions of northern Europe, the re-establishment of malaria following its common importation in travellers is evidently impeded by non-biological factors. High standards of living allow effective control, and modern farming practices have reduced the rate of human biting by mosquitoes.

  • The widespread dispersal of a new vector, Aedes albopictus, largely through trade in used car tyres and other water-carrying goods, is determined by volume of traffic as well as climatic similarity to its original range. The vectorial capacity of this mosquito species for primate-transmitted dengue virus, however, is evidently limited by its feeding behaviour and ecology, usually resulting in much more modest outbreaks than are supported by Aedes aegypti.

  • A mutation that adapts chikungunya virus to transmission by A. albopictus has evidently occurred on three independent occasions that are associated with epidemics in the Indian Ocean islands (for example, La Réunion) and West Africa, and a short-lived outbreak in Italy. The potent combination of a vector disseminated by trade and a genetically labile virus repeatedly transported by infected travellers poses particular challenges for predictive risk mapping based on present knowledge.

  • Both West Nile and bluetongue viruses have been catapulted by human agency across major geographical barriers into the New World and northern Europe, respectively, where they found latently hospitable abiotic and biotic environments. The particular feeding behaviour of abundant and diverse American mosquitoes, aided by viral genetic change and high virulence in avian transmission hosts, created a different West Nile virus epidemiology to that observed in the Old World.

  • Since 1998 bluetongue virus has spread northwards into southern Europe, making apparently new use of resident Palaearctic midge vectors.

  • The epidemic of Crimean–Congo haemorrhagic fever in Turkey, still growing since 2002, illustrates that a markedly new epidemiological situation can arise in endemic regions. The cause is unknown, but historically such events elsewhere have been associated with disruption of stable environmental and social conditions through military and civil unrest, leading to greater abundance of, and human exposure to, infected ticks.

  • Predictive models can identify remote areas of similar climatic and host conditions to those in countries of origin of vectors and diseases, and thus can contribute to warnings of future potential emergence to allow public health services to develop preventive or rapid response measures. However, the development of new or more efficient vector pathways (for example, for West Nile and bluetongue viruses), subtle evolutionary changes in the pathogens (for example, in chikungunya virus) or changes in the socioeconomic conditions affecting the degree of human exposure to risk (for example, tick-borne encephalitis and possibly Crimean–Congo haemorrhagic fever) will limit the ability of models to predict the future based on past experience.

Abstract

The impact of human activities on the principles and processes governing the arrival, establishment and spread of exotic pathogens is illustrated by vector-borne diseases such as malaria, dengue, chikungunya, West Nile, bluetongue and Crimean–Congo haemorrhagic fevers. Competent vectors, which are commonly already present in the areas, provide opportunities for infection by exotic pathogens that are introduced by travel and trade. At the same time, the correct combination of environmental conditions (both abiotic and biotic) makes many far-flung parts of the world latently and predictably, but differentially, permissive to persistent transmission cycles. Socioeconomic factors and nutritional status determine human exposure to disease and resistance to infection, respectively, so that disease incidence can vary independently of biological cycles.

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Figure 1: Distribution of Aedes albopictus at regional administrative levels in Europe and neighbouring countries up until January 2008.
Figure 2: Comparison of climates in world ports.
Figure 3: West Nile virus incidence.
Figure 4: Annual case numbers of Crimean–Congo haemorrhagic fever.

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Acknowledgements

S.E.R. is grateful to the organizers of the Keystone Symposium in Bangkok in October 2008, where her lecture triggered this invited review. S.E.R. is partially supported by the European Union grant GOCE-2003-010,284 EDEN; this paper is catalogued by the EDEN Steering Committee as EDEN0156 (http://www.eden-fp6project.net). The contents are the sole responsibility of the authors and do not necessarily reflect the views of the European Commission.

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Authors and Affiliations

  1. Oxford Tick Research Group,

    Sarah E. Randolph

  2. Department of Zoology, TALA Research Group, University of Oxford, South Parks Road, OX1 3PS, Oxford, UK

    David J. Rogers

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  1. Sarah E. Randolph
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Correspondence to Sarah E. Randolph.

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The authors declare no competing financial interests.

Supplementary information

Supplementary information S1 | Figure 4

Bluetongue virus distribution in Europe, a) predicted in 2002 according to methods described in text (pale green, zero/low abundance; yellow, intermediate abundance; dark green, high abundance; grey, no predictions), and b) observed. (PDF 1242 kb)

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DATABASES

Entrez Genome

bluetongue virus

chikungunya virus

dengue virus

West Nile virus

Entrez Genome Project

Aedes aegypti

Aedes albopictus

Plasmodium falciparum

Plasmodium vivax

FURTHER INFORMATION

David Rogers' homepage

Sarah E. Randolph's homepage

UPI news article

ProMED mail website

Centre for Disease Control website

Glossary

Zoonosis

An infectious agent that is maintained by transmission among wildlife hosts and that only infects humans by their incidental contact with infected wild hosts or vectors. No human to human transmission is possible unless the pathogen evolves to achieve this.

Anthropophilic

Showing preferences for humans. In this case, anthropophilic refers to a vector's feeding behaviour.

Catholic feeding behaviour

Feeding from a wide range of hosts, typically owing to opportunism rather than specialization.

Sylvatic cycle

Cycle of infectious agent maintained among wild animals, especially those living in forests.

Transovarially

An infectious agent being transmitted vertically from female to the next generation through the eggs.

Enzootic

When a zoonosis is habitually present in a wildlife population, rather than appearing only periodically as an epidemic in human populations.

Ornithophilic

Showing preferences for birds. In this case ornithophilic refers to the vectors' feeding behaviour.

Patent infection

An infection in which the infectious agent is shed from the patient.

Serotypes

A particular strain of a pathogen defined by its stimulation of a specific immune response.

Lagomorph

An animal belonging to an order of mammals that includes rabbits and hares.

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Randolph, S., Rogers, D. The arrival, establishment and spread of exotic diseases: patterns and predictions. Nat Rev Microbiol 8, 361–371 (2010). https://doi.org/10.1038/nrmicro2336

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