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Landscape Epidemiology of Vector-Borne Diseases Landscape Epidemiology of Vector-Borne Diseases William K. Reisen Center for Vectorborne Diseases and Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, California 95616; email: [email protected] Annu. Rev. Entomol. 2010. 55:461–83 Key Words First published online as a Review in Advance on vector, host, pathogen, climate, spatial dynamics, nidus, refugia September 8, 2009 The Annual Review of Entomology is online at Abstract ento.annualreviews.org Landscape epidemiology describes how the temporal dynamics of host, This article’s doi: vector, and pathogen populations interact spatially within a permissive 10.1146/annurev-ento-112408-085419 environment to enable transmission. The spatially defined focus, or Copyright c 2010 by Annual Reviews. nidus, of transmission may be characterized by vegetation as well as by Texas A&M University - College Station on 06/09/12. For personal use only. All rights reserved Annu. Rev. Entomol. 2010.55:461-483. Downloaded from www.annualreviews.org by climate, latitude, elevation, and geology. The ecological complexity, 0066-4170/10/0107-0461$20.00 dimensions, and temporal stability of the nidus are determined largely by pathogen natural history and vector bionomics. Host populations, transmission efficiency, and therefore pathogen amplification vary spa- tially, thereby creating a heterogeneous surface that may be defined by remote sensing and statistical tools. The current review describes the evolution of landscape epidemiology as a science and exemplifies se- lected aspects by contrasting the ecology of two different recent disease outbreaks in North America caused by West Nile virus, an explosive, highly virulent mosquito-borne virus producing ephemeral nidi, and Borrelia burgdorferi, a slowly amplifying chronic pathogen producing semipermanent nidi. 461 INTRODUCTION have destabilized climax communities that have been intruded upon by agriculture and human Geographical information systems, remote habitation and must respond to anthropogenic- Vector: competent sensing, and modern computing have provided driven climate and ecosystem change (31). The arthropod that carries new tools to re-examine old, and perhaps syn- resulting heterogeneous matrix (http://www. a pathogen to and thesize contemporary, concepts concerning the infects a vertebrate eoearth.org/article/Anthropogenic biomes) landscape epidemiology of vector-borne dis- host consists of habitat patches that change in di- eases. The current review extends previous WNV: West Nile mension owing to human and other activities summaries focused on methods of study (3, 7, virus and are linked by a series of transitional 52, 56), defines the components of vector-borne Amplification: boundaries (or ecotones) characterized by their disease foci, examines factors driving their dy- increase of a pathogen distinct and diverse vegetative types, enhanced namics in time and space, and describes how ex- and therefore the primary productivity, species diversity, and number of infections panding human populations have altered their complex interactions (also referred to as the within the ecology, thereby enhancing the risk of transmis- edge effect). environment sion. The emergence and ongoing epidemics of Concurrent with the emergence of land- Nidus: place where Lyme borreliosis (Spirochaetales, Spirochaetaceae, scape ecology as a science, Pavloskiy proposed pathogen transmission Borrelia burgdorferi ) and West Nile virus (Fla- occurs (from Latin the concept of nidality (or focality) of dis- viviridae, Flavivirus, WNV) in North America meaning “nest,” ease (86, 87), where pathogens are associated provide excellent comparative examples of how synonym of focus) with specific landscapes. The nidus of infection different vector biology and landscape dynam- Reservoir host: contains three critical elements: (a) competent ics determine foci composition, enable enzootic arthropod or and infectious vectors, (b) competent vertebrate vertebrate host that amplification, and determine human infection reservoirs, and (c) susceptible recipient (tangen- provides a long-term (51, 59, 61, 77). Although most examples in the tial) hosts such as humans or domestic animals. source of infection current review relate to these two pathogens, In his original concept based on tick-borne Anthroponoses: the overarching concepts should be extrapola- pathogens in Russia, humans became infected diseases in which tive to other arthropod-borne pathogens. humans function as the when they traveled into the nidus and contacted Landscape epidemiology is linked closely primary vertebrate the infectious vector or perhaps the reservoir to its ecological parallel, landscape ecology, a host host. The disjunct distribution of infection and science with beginnings in the early 1930s to residence complicated the initial understanding study interactions between the environment of the epidemiology of transmission, especially and vegetation (122). Geomorphology and for highly clustered tick-borne pathogens such climate combine to delineate plant communi- as tick-borne encephalitis virus (83). This nidal- ties and therefore ecosystem structure. These ity concept blended with landscape ecology has biomes were first classified at a global scale in led to the emergence of the contemporary sci- the early 1900s by Koppen,¨ who proposed that ence of landscape epidemiology (37), in which by Texas A&M University - College Station on 06/09/12. For personal use only. climatic zones could be effectively defined by Annu. Rev. Entomol. 2010.55:461-483. Downloaded from www.annualreviews.org diseases may be associated with distinct land- their resulting plant communities. This clas- scape features or ecological settings where vec- sification system was updated recently for the tor, host, and pathogen intersect within a per- 1951–2000 period (88) and broadly delineates missive climate (Figure 1). When placed into ecosystems with varying capacity to support the recent context of anthropogenically altered different vectors, hosts, and pathogens. Some biomes or anthromes (31), the nidus now ranges pathogens such as WNV have invaded almost from remote, sparsely inhabited landscapes to all but the most extreme climates, whereas residential settings and may be delineated by others, such as Barmah Forest virus, seem various mapping and statistical tools (56). For more restrictive in their distribution. How- many vector-borne anthroponoses, the nidus ever, landscapes are spatially and temporally may be the human residence where commensal dynamic. The increasing size and expanding vectors reside and blood feed. distribution of the global human population 462 Reisen COMPONENTS OF THE NIDUS Environment Climate Although delineated spatially by landscape features, disease foci invariably arise within Host Vector a permissive climate where competent host and vector populations intersect (Figure 1). Within these environments, moisture governs Pathogen Nidus of vegetative structure and the extent of suitable pathogen habitat, whereas temperature governs the rates transmission at which processes occur. Climate varies spa- tially and temporally at different scales, which Figure 1 may be divided into seasonal (intraannual), Conceptual nidus showing how vector, host, and pathogen populations annual (interannual), and long-term (decadal intersect within a permissive environment to enable pathogen transmission. or longer) change. For transmission to occur, climate must attain seasonal ranges within entering hibernation, or migrating, whereas the tolerances of host and vector species and vector populations may remain active at be suitable for pathogen replication within permissive refugia, enter aestivation (summer), the poikilothermic arthropod vector. Most quiescence or diapause (winter), or become pathogens have a minimal thermal develop- regionally extinct and require annual reintro- mental threshold below which replication, duction. Despite the negative effect of elevated and therefore transmission, will not occur. temperatures on vector survival (94, 96), most This is especially pertinent for arboviruses amplification transmission occurs during the within diapausing insects, where termination, warmest periods of the year, because the rate temperature increases, and even reproductive of pathogen replication in the vector typically activity may be necessary for pathogen repli- increases and therefore the duration of extrinsic cation and detection (5). Seasonal changes incubation decreases as a curvilinear function in day length, temperature, and precipitation of ambient temperature (104). also delineate ecosystem primary productivity, The duration and intensity of favor- food availability, and therefore host and vector able periods often fluctuate due to climate reproductive periods. During unfavorable cycles or show long-term patterns related weather periods, nidus dimensions often con- to change. Intermediate duration changes tract to spatially delimited refugia that enable in ocean temperatures create interannual host and/or vector and pathogen persistence. variation in climate over broad areas often Under permissive temperatures, moisture- affecting pathogen dynamics. The El Nino˜ by Texas A&M University - College Station on 06/09/12. For personal use only. Annu. Rev. Entomol. 2010.55:461-483. Downloaded from www.annualreviews.org related focus contraction actually may enhance phase of the El Nino–Southern˜ Oscillation host-vector contact and therefore transmission. (ENSO)
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