The Ecology of Infectious Diseases Jane Bradbury
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Feature Beyond the Fire-Hazard Mentality of Medicine: The Ecology of Infectious Diseases Jane Bradbury ifty years ago, many experts able to predict or ameliorate disease and so cholera remains an important believed that the war against outbreaks’. global health problem. Because her infectious diseases had largely studies showed that virtually all the V. F From Ecology to Disease been won. But in the last 30 years of cholerae in water supplies are attached the 20th century, as people entered Prevention: The Cholera Example to 200 µm–long zooplankton, Colwell previously untouched wild areas A good example of how ecological reasoned that it might be possible to or wreaked wide-scale changes on studies can suggest new ways to prevent make water safe to drink simply by established ecosystems, numerous disease outbreaks is provided by the filtering it through layers of cloth. In a viruses (for example, Ebola) have work of Rita Colwell, director of recent trial in rural Bangladesh, cholera jumped from their long-time animal the United States’ National Science rates were halved when villagers filtered hosts to people who, not having the Foundation (Arlington, Virginia, their drinking water through eight appropriate immune layers of sari cloth, a defence, often succumb cheap but effective to virulent ‘emerging’ and socially acceptable diseases. At the same intervention, explains time, old enemies Colwell (Figure 1). such as dengue and Kathryn Cottingham hantavirus pulmonary (Dartmouth College, syndrome have re- Hanover, New emerged to cause Hampshire, United important human States) and her epidemics. All too team are also doing often when faced ecological studies on V. with these emerging cholerae that may help and re-emerging to improve cholera diseases, says hantavirus control in developing researcher Terry Yates countries. ‘We are (University of New recording the temporal Mexico, Albuquerque, dynamics of both free- New Mexico, United living and attached States), ‘society has bacteria in two ponds adopted a fire-hazard in Bangladesh, one that DOI: 10.1371/journal.pbio.0000022.g001 mentality. We have an is largely untouched outbreak and we go Figure 1. Women at a Village Pond in Matlab, Bangladesh, Washing Utensils and by people and one in in and put out the fire Vegetables a village’, she explains. The woman on the right is putting a sari filter onto a water-collecting pot (or without ever asking kalash) to filter water for drinking. (Picture courtesy of Anwar Huq, University ‘By doing this, we hope why there was a fire in of Maryland Biotechnology Institute, Baltimore, Maryland, United States.) to get a better idea of the first place’. Yates which physical and and other experts are now calling for United States). In the 1960s, Colwell chemical changes prompt changes in an integrated approach to disease discovered that pathogenic strains of the V. cholerae population’, information prevention and control, based on a Vibrio cholerae, the cause of cholera, that can be used to build a predictive detailed understanding not only of the could be isolated from Chesapeake model of when and where cholera biology and but also of the ecology of Bay in the United States. Her discovery outbreaks might occur, as can other disease. For animal-borne (zoonotic) created a furore and people were studies that Colwell has underway that and vector-borne diseases, but also for initially reluctant to accept that use satellites to monitor large-scale diseases like cholera, which constantly V. cholerae was a marine organism. environmental changes. re-emerge around the world, ‘it is not However, subsequent studies showed Cottingham’s studies may also lead sufficient to know who the players that V. cholerae is an abundant, naturally are’, says Lyme disease researcher occurring component of aquatic Abbreviations: AHF, Argentine haemorrhagic fever; Rick Ostfeld (Institute of Ecosystem ecosystems worldwide, where it is CDC, United States Centers for Disease Control and Prevention; DHF, dengue haemorrhagic fever Studies, Millbrook, New York, United associated with phytoplankton and States). ‘We also need to know how the zooplankton, in particular copepods. Jane Bradbury is a freelance science news hosts, vectors, and infectious organisms Although boiling removes V. cholerae writer based in Cambridge, United Kingdom. E-mail: [email protected] interact with each other and with their from water, this is often not done environment if we are going to be in villages in the developing world, DOI: 10.1321/journal.pbio.000022 PLoS Biology | http://biology.plosjournals.org Volume 1 | Issue 2 | Page 148 to the development of another low- Carolina, United States) has been tech approach to cholera control. V. trying to discover which, if any, of cholerae do not attach only to copepods, these changes were responsible for she explains. They also attach to the emergence of DHF in Sri Lanka cladocerans, zooplankton that moult in 1989. His recently published regularly throughout their lifetime conclusion, after looking at all the and graze on unattached V. cholerae. available data on changes in the Cottingham’s hope is that by changing human population, exposure to the fishing practices in rural ponds, fish Aedes aegypti vector, the environment, communities can be established that and the virus itself, is that ‘very little prey on copepods in preference to happened in Sri Lanka apart from a cladocerans, thus reducing bacterial change in the virus that could explain loads in drinking water. the emergence and persistence of DHF’. That change—the arrival of Bring in the Vectors a dengue serotype 3, subtype III Zooplankton in a sense are V. virus that originated in the Indian cholerae vectors, but the term ‘disease subcontinent—was most likely caused vectors’ is more usually applied to by people bringing this virulent virus mosquitoes and other biting insects. serotype into Sri Lanka. However, the The recognition that malarial control, question remains as to what selective for example, requires an understanding pressures drove the original viral of mosquito populations goes back at change and what prevented the virulent least a century. Worryingly, however, serotype arriving in Sri Lanka earlier. DOI: 10.1371/journal.pbio.0000022.g003 numerous arboviral diseases—diseases transmitted by blood-feeding One Host or More? Figure 3. Acorns at the Base of a Red Oak (Quercus rubra) during a Heavy Year of Mast arthropods—have recently emerged Dengue is unique among arboviruses Production or become established in new in that it is fully adapted to using Many species of wildlife, including white- geographical regions. For example, human beings as its vertebrate host. footed mice (P. leucopus), an important some dengue viruses, which are also Most arboviruses have co-evolved with disease reservoir for Lyme disease, transmitted by mosquitoes, have their animal or bird hosts, which are feast on acorns during years of high availability. (Picture courtesy of Rick recently extended their range. Before required for their lifecycle, and people Ostfeld; photograph by Molly Ahearn.) 1970, the most severe form of dengue are only incidental hosts. Factoring infection—dengue haemorrhagic fever in additional hosts greatly increases (DHF)—had caused epidemics in only system complexity. Take West Nile belonging to about 10 genera. ‘Twenty- nine countries. By 1995 that figure had virus, for example, a mosquito-borne nine or so of these mosquito species more than quadrupled. disease agent that requires birds for are mammal feeders or opportunistic Greater urbanisation, human its maintenance. Until recently, the feeders, and although we have isolated population growth, increased human geographical range of West Nile virus the virus from about 25 species of travel, and a global reduction of disease extended from Africa through mammals, we simply do not know what effective mosquito control programmes the Middle East to southern and part these species play in the lifecycle have all been implicated in the eastern Europe and western Asia. Then, of West Nile’, says Gubler. Really observed changes in dengue dynamics. in 1999, the first 62 cases were reported effective control, he stresses, will rely Ecologist William Messer (University in the United States. Last year, there on knowing which vectors and hosts are of North Carolina, Chapel Hill, North were 4,156 human cases in the United critical for virus maintenance and for States and West Nile virus was found in bringing the virus into the areas around all but six states. human habitation where people Duane Gubler, director of the become infected. Division of Vector-Borne Diseases at This research will involve many the United States’ Centers for Disease different specialists, including mosquito Control and Prevention (CDC; Fort experts like Colin Malcolm (Queen Collins, Colorado, United States), is Mary, University of London, United under no illusion that preventing West Kingdom). Malcolm is trying to predict Nile virus disease outbreaks will be easy. whether West Nile virus disease could ‘We really don’t know enough about establish itself in the United Kingdom. the ecology of this disease to target our ‘There must be a big difference control efforts appropriately’, he says. between the ecology and biology of the ‘We know that the mosquito–bird–viral different physiological forms of Culex DOI: 10.1371/journal.pbio.0000022.g002 maintenance cycle requires certain pipiens in Europe, where it only causes Figure 2. The Emergence of AHF species of birds, but we don’t know all sporadic West Nile outbreaks, and the The emergence of AHF coincided the bird hosts’. Similarly, Culex pipiens United States where it has spread like with wide-scale changes in agricultural practices on the pampas of Argentina. mosquitoes are clearly important in wildfire’, says Malcolm. ‘We need to (Picture courtesy of Delia Enria, Instituto the West Nile virus lifecycle, but the understand that difference and to know Nacional de Enfermedades Virales virus has been isolated from 37 species exactly which Culex pipiens we have Humanas, Pergamino, Argentina.) of mosquito in the United States, in the UK’.