The ecological dimensions of vector-borne disease research and control Dimensões ecológicas do controle e gerenciamento de doenças transmitidas por vetores

Alarming trends in the resurgence of vector-borne diseases are anticipated to continue unless more effective action is taken to address the variety of underlying causes. Social factors, anthropogenic environmental modifications and/or ecological changes appear to be the primary drivers. The ecological dimension of vector-borne disease research and management is a pervasive element because this issue is essentially an ecological problem with biophysical, social, and economic dimensions. However there is often a lack of clarity about the ecological dimension, the field of ecology (e.g. role, limitations), and related concepts pertinent to ecosystem approaches to health. An ecological perspective can provide foresight into the appropriateness of interventions, provide answers to unexpected vector control responses, and contribute to effective management solutions in an ever-changing environment. The aim of this paper is to explore the ecological dimension of vector-borne diseases and to provide further clarity about the role of “ecological thinking” in the development and implementation of vector control activities (i.e. ecosystem approaches to vector-borne diseases). Dengue; Chagas Disease; Communicable Diseases; Ecological Studies; Ecosystem Introduction Vector-borne diseases pose a significant public health problem today, with a number of “old” diseases resurging in recent decades alongside newly emerging infectious diseases 1. Some of these were effectively controlled just 50 years ago but these previous hard-won gains are now threatened or have already been lost 2,3. Dengue is perhaps the most striking example. From 19501959 less than 1,000 cases were reported worldwide 4. Now an estimated 50-100 million cases occur annually 5. At least 20 other vector-borne diseases have also emerged during this time, having increased in incidence and/or expanding their geographical range 5. Coinciding with this increase in vector-borne diseases have been dramatic ecological changes. Marked increases in the rate and extent of environmental degradation over the last century, largely attributable to human activity, have fueled growing concern and acceptance of the interdependence of man and the environment 6,7. The association of anthropogenic environmental change and infectious diseases in particular has recently begun to attract attention and prominence in relation to policy (e.g. Millenium Ecosystem Assessment, 2005). The growing interest in ecosystem approaches to health is a response to an increasing recognition of “the inextricable links between humans and their biophysical, social, and economic environments, and that ARTIGO ARTICLE Ellis BR, Wilcox BA S156 Cad. Saúde Pública, Rio de Janeiro, 25 Sup 1:S155-S167, 2009 these links are reflected in a population’s state of health” 8 (p. 1). The alarming trends in vector-borne disease emergence are anticipated to continue unless more effective action is taken to address the variety of underlying causes – of which social factors, anthropogenic environmental modifications and/or ecological changes appear to be the primary drivers 9. The systemic nature of these changes and complexity of interactions among factors make simple, targeted or “silver-bullet” solutions ineffective, except for in the short term. As a result, ecosystem-based approaches are now advocated to provide sustainable solutions, as they previously have been the areas of natural resource management and agricultural pest management 10. However, public health research and policy have yet to incorporate the ecological dimension into management and control strategies to any significant degree. This may in large part be due to the complex and abstract nature of the ecosystem concept as well as the lack of an operationally explicit description of what constitutes “the ecosystem approach”. The aim of this paper is to partially address this need by exploring the relevance of ecological science to vectorborne diseases, explaining “ecological thinking” and attempting to describe its role in the development and implementation of vector control activities (i.e. an ecosystem approach to vectorborne diseases). History of ecology in vector-borne disease research and control The importance of the ecological context in the management of vector-borne diseases was likely realized immediately following the discovery of arthropods as vectors of disease in 1877. As early as 1935 Klinger 11 (p. 244) pointed to the “need to have a thorough knowledge of breeding places and habits and to apply the most suitable methods to the situation”. Since about this time a large body of ecologically relevant knowledge has accumulated for these diseases. Basic ecological science has grown in parallel, but neither area has consistently benefited from the knowledge generated by the other 12. Akin to the initial focus of ecological science in the late 19th and early to mid 20th centuries, early vector-borne disease research concentrated on explaining the natural history, taxonomy, biology and distribution of organisms (i.e. vectors and pathogens). This quickly resulted in a great deal of ecological knowledge that was immediately applied to develop vector management strategies. This includes a number of notable early successes, such as the first systematic effort to control mosquito vectors in 1901 by William Gorgas, the eradication of a number of important diseases in the United States from 1910-1948 (e.g. yellow fever, dengue and malaria), and the successful eradication of the dengue vector Aedes aegypti and, as a result, dengue throughout much of the Americas from 1950-1970 13,14. Ecology-based vector control methods received a boost beginning in the 1960s when the use of persistent chemical pesticides like DDT came into question due to their potentially negative environmental health and ecological impacts. The importance of using biological and ecological approaches, including undertaking ecosystem studies, thus began to be advocated 15. In fact, the ecological impacts of DDT and other chemicals became the environmental cause célèbre of this period and arguably helped usher in the modern “environmental awakening” 16. To this day, ecology is often equated solely with research and policy that deals with the natural environment and its protection. That is, with humans as being outside of nature and external stressors. This is contrary to the perspective, discussed further below, that humans and nature are intertwined and interdependent. Nonetheless, these concerns and the extensive environmental protection legislation that emerged led vector ecology research and policy toward more environmentally sound methodologies. These methods went beyond chemical control to include environmental management and biological and social control methods. Subsequently, another set of environmental challenges to vector control has emerged stemming from the profound ecological changes, particularly (but not limited to) the tropics where most vector-borne diseases originate and by far the largest number of people suffer or are at risk. A phase shift has taken place during the past few decades in which most regional ecosystems in the world have transformed from what largely was natural landscape and non-intensively cultivated cropland to primarily human dominated landscape 17. Rapid and widespread urbanization, agricultural intensification and exploitation of natural resources now make it difficult to draw boundaries between urban and rural as well as rural and natural landscape – thus between what is human and what is nature. Exceptions include the boundaries of national parks or other protected areas, assuming they are aggressively and effectively enforced. Nonetheless, people often flock in great numbers to many of these areas or aggregate outside the boundaries, so that the effects of dramatically increased human densities are not necessarily limited to urban areas. As a THE ECOLOGICAL DIMENSIONS OF VECTOR-BORNE DISEASE S157 Cad. Saúde Pública, Rio de Janeiro, 25 Sup 1:S155-S167, 2009 result of this shift, marked by the recent discovery that humans now or will soon be responsible for essentially “consuming” over 50% of the earth’s net ecological productivity 18, science is increasingly emphasizing an integrated, human-nature model for understanding ecosystems and their dynamics (e.g., Michener et al. 19). This has resulted in a growing shift in ecological research towards concern with not only the degradation of the natural environment but an acceptance and recognition by a growing number of ecological scientists and researchers who focus on the “human-built” environment of our inseparable role as part of all ecosystems 20. This is evidenced by the new journal Urban Ecosystems (Springer) for example. None of this should be taken to suggest that (predominantly) natural ecosystems, landscapes and natural populations do not remain a significant aspect of ecology research or vector-borne diseases. However, vector ecology and control now face a dramatically different set of challenges as the disease transmission arena today is fundamentally different from what it was just a few decades ago. As is the case for all “complex adaptive systems”, ecosystems are continuously evolving as non-equilibrium systems within the environment – in which host-vector-pathogen complexes are inextricably embedded 21,22. In sum, despite some set-backs, such as the over-reliance on chemical pesticide solutions that is characteristic of the post-WWII era of technological “quick fixes”, vector borne disease management has been evolving towards a more integrated, holistic, ecology-based science. This is reflected in the emergence of “integrated control” in the 1960s, followed by “integrated pest management” in the 1970s and “integrated vector control” and “community-based participatory” approaches emerging in the 1980s 12,23. What is by far the most holistic and disciplinarily inclusive approach yet, “the ecosystem approach” began in the 1990s 8. It is noteworthy that in all of these approaches the idea and policy impetus behind them generally has been out in front of the science (the conventional hypothesis-driven experimental evidence) and the capacity of academic and public health institutions to readily grasp and implement them. The ecology of dengue and Chagas disease Vector-borne disease transmission cycles typically involve a set of important pathogen(s), arthropod vector(s), vertebrate host(s), and occur within a variety of particular environments (Figure 1). Dengue and Chagas are examples discussed here and occupy different ends of a wide spectrum of vector borne disease ecologies.