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The Landscape Epidemiology of Echinococcoses Angela M Cadavid Restrepo et al. Infectious Diseases of Poverty (2016) 5:13 DOI 10.1186/s40249-016-0109-x SCOPINGREVIEW Open Access The landscape epidemiology of echinococcoses Angela M. Cadavid Restrepo1*, Yu Rong Yang2,3, Donald P. McManus3, Darren J. Gray1,3, Patrick Giraudoux4,5, Tamsin S. Barnes6,7, Gail M. Williams8, Ricardo J. Soares Magalhães6,9, Nicholas A. S. Hamm10 and Archie C. A. Clements1 Abstract Echinococcoses are parasitic diseases of major public health importance globally. Human infection results in chronic disease with poor prognosis and serious medical, social and economic consequences for vulnerable populations. According to recent estimates, the geographical distribution of Echinococcus spp. infections is expanding and becoming an emerging and re-emerging problem in several regions of the world. Echinococcosis endemicity is geographically heterogeneous and over time it may be affected by global environmental change. Therefore, landscape epidemiology offers a unique opportunity to quantify and predict the ecological risk of infection at multiple spatial and temporal scales. Here, we review the most relevant environmental sources of spatial variation in human echinococcosis risk, and describe the potential applications of landscape epidemiological studies to characterise the current patterns of parasite transmission across natural and human-altered landscapes. We advocate future work promoting the use of this approach as a support tool for decision-making that facilitates the design, implementation and monitoring of spatially targeted interventions to reduce the burden of human echinococcoses in disease-endemic areas. Keywords: Landscape epidemiology, Helminth infection, Human echinococcosis, Echinococcus spp, Environmental change, Geographic information systems, Remote sensing, Geostatistics Multilingual abstracts physical and/or biological conditions that support a Please see Additional file 1 for translations of the pathogen, its vectors and reservoirs; and third, the con- abstract into the six official working languages of the temporaneous and future risk of a disease can be pre- United Nations. dicted if those conditions are mapped [2]. This conceptual framework has been developed and extended progressively to integrate concepts and approaches from Introduction multidisciplinary studies, including landscape ecology, Landscape epidemiology is the study of the spatial vari- for a better understanding of the complex composition ation in disease risk, in strong connexion with landscape of the landscape and its relationship with the transmis- characteristics and relevant environmental factors that sion processes and geographical distribution of a disease influence the dynamics and distribution of host, vector [3–5]. The current principles of landscape epidemiology and pathogen populations. The fundamental concepts of have been recently summarised in a set of propositions landscape epidemiology were formalised and introduced outlined by Lambin and colleagues (Table 1) [6]. by the Russian parasitologist, Pavlovsky, in 1966 [1]. Ac- Most modern landscape epidemiological studies use cording to Pavlovsky, landscape epidemiology is based Earth observation (EO) to obtain remotely sensed (RS) on three observations: first, diseases tend to be limited and in situ data about the environment [5]. Geographic geographically; second, the spatial variation in the distri- information systems (GIS) are used to capture, store, bution of a disease is determined by variations of analyse and display geo-referenced data that may be * Correspondence: [email protected] exported to various analytical and statistical platforms 1Research School of Population Health, The Australian National University, [5]. The integrated use of these technologies and the ap- Canberra, New South Wales, Australia plication of spatiotemporal statistics allow investigators Full list of author information is available at the end of the article © 2016 Cadavid Restrepo et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Cadavid Restrepo et al. Infectious Diseases of Poverty (2016) 5:13 Page 2 of 13 Table 1 The 10 principles of landscape epidemiology proposed by Lambin and colleagues Principle Description 1 Landscape attributes may influence the level of transmission of an infection 2 Spatial variations in disease risk depend not only on the presence and area of critical habitats but also on their spatial configuration 3 Disease risk depends on the connectivity of habitats for vectors and hosts 4 The landscape is a proxy for specific associations of reservoir hosts and vectors linked with the emergence of multi-host disease 5 To understand ecological factors influencing spatial variations of disease risk, one needs to take into account the pathways of pathogen transmission between vectors, hosts, and the physical environment 6 The emergence and distribution of infection through time and space is controlled by different factors acting at multiple scales 7 Landscape and meteorological factors control not just the emergence but also the spatial concentration and spatial diffusion of infection risk 8 Spatial variation in disease risk depends not only on land cover but also on land use, via the probability of contact between, on one hand, human hosts and, on the other hand, infectious vectors, animal hosts or their infected habitats 9 The relationship between land use and the probability of contact between vectors and animal hosts and human hosts is influenced by land ownership 10 Human behaviour is a crucial controlling factor of vector-human contacts, and of infection. to explore in detail the landscape patterns that influence Both have a wide geographic distribution and cause se- the transmission dynamics of an infectious disease at dif- vere disease in humans that can be fatal if left untreated ferent spatiotemporal scales. EO, GIS and the use of in- [23–25]. The other two less common forms of human novative analytical methods also provide the opportunity infection are polycystic echinococcosis and unicystic to visualise and predict the geographical variations in echinococcosis caused by Echinococcus species restricted disease risk in response to shifting environmental pat- to Central and South America [25]. terns [7, 8]. In this way, landscape epidemiology may There are approximately 200,000 new cases of human offer a feasible and acceptable framework to reduce dis- CE or AE cases diagnosed every year and a total of 2–3 ease burdens by allowing a more precise estimation of million people infected worldwide [26, 27]. According to populations at high risk and the identification of priority the Office International des Epizooties databases and areas where allocation of disease control resources is published case reports, the estimated human burden of most required [9]. CE measured in terms of Disability-Adjusted Life Years To date, landscape epidemiology has been mainly ap- (DALYs) lost is 285,407. When underreporting in plied to examine associations between the environment accounted for, the global burden of this form of infection and the transmission dynamics of mosquito-borne dis- exceeds 1 million DALYS, which results in an annual es- eases such as malaria, dengue, leishmaniasis, filariasis timated cost of $760 million [26]. Global estimates of and trypanosomiasis [10–13]. However, with the advent AE suggest that there are approximately 18,235 people of global environmental change, there has been an in- infected every year and a total of 0.3–0.5 million AE creasing interest in conducting studies centred on the cases diagnosed worldwide. Most of the disease burden understanding of the landscape epidemiological aspects of AE is focused on Western China and results in the of non-mosquito-borne helminth infections, such as loss of 666,434 DALYs per annum [28]. Although these schistosomiasis [14–16]. This approach has been suc- reports may be underestimates due to challenges with cessful in providing valuable information to enhance the the early detection of the diseases and lack of mandatory implementation of strategies for surveillance, control reporting in most countries, it is apparent that the burden and elimination of helminth infections in various set- of echinococcoses has increased in recent years and hu- tings [17–19]. man infection is becoming an emerging or re-emerging Echinococcoses are zoonotic parasitic diseases caused problem in several regions in the world [29–36]. Conse- by larval stages of taeniid cestodes of the genus Echino- quently, landscape epidemiological approaches have been coccus. Currently, there are nine recognised species incorporated progressively into echinococcosis research to within the genus and six of these species cause infection identify the environmental mechanisms underlying the in humans, E. granulosus, E. multilocularis, E. canaden- variation in disease risk and the most plausible drivers of sis, E. ortleppi, E. vogeli and E. oligarthrus [20, 21]. parasite dispersion [37–43]. Among them,
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