Temperatures Without Fevers?

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Science  08 Sep 2000:
Vol. 289, Issue 5485, pp. 1697-1698
DOI: 10.1126/science.289.5485.1697

…And the houses shall be full of swarms of insects, and also the ground on which they stand…” [HN1] (1). Or maybe not, after all. In the face of repeated prophecies that insect vectors and pathogens causing diseases [HN2] such as malaria [HN3], Dengue, and yellow fever [HN4] will spread as the world warms up (26), Rogers and Randolph [HN5] (7) offer a more benign outlook on the future (see page 1763 in this issue). Taking a multidimensional view that combines several climatic variables, they predict that the distribution of the parasite that causes the most severe form of malaria (Plasmodium falciparum) [HN6] is unlikely to change much if the world gets hotter. We may still become victims of crop failures, freshwater shortages, forest diebacks, a rise in sea-level, and all the rest [HN7], but if the findings of this latest work are correct, we should at least be spared an increased burden of malaria.

Biologists grappling with the complexity of vector-borne diseases are wary of existing predictions that forecast how disease distribution will change in the future, especially when such predictions are based on an alteration of just one variable—temperature. “Global warming” is about the world's atmosphere getting hotter, but only to a first approximation. More precisely, it is about temperature, rainfall, and humidity covarying spatially and temporally, and how these variables impact the numerous components of the vector and pathogen life cycle. For malaria, these components are not just limited to the temperature-sensitive incubation period of parasites in mosquitoes, but include the abundance, longevity, choice of host, and blood-feeding frequency of the vector, its susceptibility to the parasite, and a plethora of other factors that affect the host-parasite-vector interaction.

Stepping into this multifactorial world, Rogers and Randolph have incorporated five critical measures of temperature, rainfall, and saturation vapor pressure into a multivariate model [HN8]. They use this model to draw a map of present-day malaria distribution that is 78% correct with respect to the current reported presence or absence of malaria cases—substantially better than any previous fit. They then use the predicted values of these variables to redraw the map as it might appear in 2050. The anticipated distribution of P. falciparum in 2050 is strikingly similar to its current distribution. The model predicts an overall change of less than 1% in the number of people suffering from malaria in 2050 compared to today.

One reason that malaria may not claim much new territory is that climatic factors affect mosquito, human host, and parasite populations interactively, rather than independently [HN9]. Some of these interactions are obvious. A rise in temperature speeds the development of the plasmodia parasites in mosquitoes. But if there is insufficient water for the mosquitoes to breed in, and limited contact with humans, higher temperatures won't matter. The south of England may be getting warmer, but the malaria that was prevalent in the 17th century in the “Dengie marshes” of Essex and other areas [HN10] has been absent for nearly a century—mosquito habitat has largely been eliminated, and the living conditions of the human population are greatly changed (8). Other interactions are more subtle. High temperatures in the West African country of Mali [HN11] mean that a 3 month rainy season is enough to sustain transmission of P. falciparum by mosquitoes; in contrast, cooler parts of southern and eastern Africa need 5 consecutive months of rain to enable mosquitoes to achieve the abundance and longevity necessary to sustain transmission of malaria (9).

An in-depth look at malaria.

Distribution of INDEPTH field sites (purple) in Africa. Field sites collect data on health and demographics in selected populations that can be used to predict the course of vector-borne diseases such as malaria. [Adapted from (13)]

Multiple regression [HN12] with a series of climatic variables may provide a perfect explanation, statistically speaking, for the current distribution of malaria. But it does not follow that the range of the disease is solely determined by climate. P. falciparum was endemic in southern Europe (10) and the United States (11) until the middle of the 20th century. Given the right combination of social, environmental, and climatic changes, these regions could again become vulnerable. Similarly, although the disease has recently become more prevalent in many highland areas of Africa [HN13], it has yet to return to the maximum altitudes reported before large-scale control measures were implemented in the 1960s (12). Nevertheless, Rogers and Randolph have opened up a new clearing in the methodological jungle of statistical forecasting. Further work emulating their approach need not be restricted to vector-borne diseases; their methods are applicable to any phenomenon that has the potential to be influenced by climate change. Indeed, their results lead us to question whether other climate-related health warnings—for asthma, cholera epidemics, or heat-induced deaths, for example—would stand up to a more sophisticated multivariate analysis.

Rogers and Randolph's results can also be viewed as an attempt to pinpoint areas at greatest risk for new malaria outbreaks. Climatic variables that predict the presence or absence of malaria are likely to be best suited for forecasting the distribution of this disease at the edges of its range (that is, where its existence or nonexistence is most clearly marked). However, detailed ecological and epidemiological studies [HN14] are still needed to assess the true local risk. Questions to be addressed in such studies should include: How might local species of anopheline mosquitoes extend their breeding ranges in response to altered climate? What is their susceptibility to the malaria parasite? What species interactions—with competitors, predators, and parasites—might influence mosquito abundance? How might changes in abundance affect transmission rates? How do temperature and humidity affect the behavior and longevity of adult mosquitoes? What is the potential for malaria to be imported through human migration?

The resolution and competence of climate models [HN15] is improving rapidly, and this improvement will be of benefit to future analyses that strive for better explanations of the distribution of malaria. It is less certain that such studies will have access to better disease data, because information on insect vectors and malaria incidence is much harder to collect. This is especially true for the regions of Africa that carry most of the world's malaria burden. Much will depend on the success of new systems for data collection, such as INDEPTH [HN16] (13), a network of field sites that produces information on health and demography by continuously monitoring vital events in selected populations. INDEPTH now has 15 sites in Africa (see the figure) and more than 40 worldwide. The present statistical output lists deaths from all causes, but in the future it may provide estimates of deaths attributable to malaria alone.

In some instances, climate variations do produce a detectable signal in malaria incidence, although the dominant fluctuations in caseload are determined by the ups and downs of control programs [HN17] (14). The goal of those involved in malaria control over the next 50 years should be to make certain that climate change is indeed irrelevant to the distribution and prevalence of the disease. Given adequate funding, technology, and, above all, commitment, the campaign to “Roll Back Malaria,” [HN18] spearheaded by the World Health Organization (WHO), will have halved deaths related to P. falciparum by 2010 (15). By 2050, the map of malaria distribution should bear little resemblance to the one drawn by Rogers and Randolph.

HyperNotes Related Resources on the World Wide Web

General Hypernotes

The WWW Virtual Library of Parasitology is maintained by D. Gibson, Department of Zoology, Natural History Museum, London.

A. Adeel's Reference Page on Medical Parasitology offers a section with links to malaria resources.

The World Health Organization (WHO) offers a malaria information page. WHO's Protection of the Human Environment division offers a presentation on climate and health.

The U.S. Centers for Disease Control and Prevention (CDC) provide an information page on malaria with an introduction to the disease and regional malaria information for travelers. Links to relevant articles in Morbidity and Mortality Weekly Report and Emerging Infectious Diseases are also presented.

The Malaria Foundation International provides an overview of malaria and its history, Internet links for malaria, and links to epidemiology and other scientific resources.

Malaria: An On-line Resource is provided by the Division of Laboratory Medicine, Royal Perth Hospital, Australia. A history of malaria is included.

F. Opperdoes, Research Unit for Tropical Diseases, Christian de Duve Institute of Cellular Pathology and Laboratory of Biochemistry, Université Catholique de Louvain, Brussels, Belgium, offers lecture notes for a parasitology course. Lecture notes on malaria are included.

J. Smith, Institute of Parasitology, McGill University, Montreal, provides lecture notes for a course on parasitism and symbiosis. A presentation on malaria is included.

Medical Microbiology, an online textbook edited by S. Baron, Department of Microbiology and Immunology, University of Texas Medical Branch at Galveston, has a chapter on malaria by J. Crutcher and S. Hoffman.

M. Wiser, Department of Tropical Medicine and Parasitology, Tulane University School of Public Health and Tropical Medicine, provides lecture notes on malaria. Included are presentations on the biochemistry and cellular and molecular biology of Plasmodium. is a gateway to global change data and information on the Internet. The U.S. Global Change Research Program Web site provides summary information from the 1996 WHO reportClimate Change and Human Health, as well as Internet links.

The Climate Diagnostics Center of the National Oceanic and Atmospheric Administration (NOAA) provides links to climate resources on the Web. The NOAA Office of Global Programs Library offers a collection of links to Internet climate resources. NOAA's National Climatic Data Center provides information about climate research and applications and other climate resources including a FAQ about global warming.

The United Nations Framework Convention on Climate Change Web site provides a Climate Change Information Kit, which includes a fact sheet on the consequences of climate change to human health.

The Hadley Centre for Climate Prediction and Research of the UK Meteorology Office provides information resources on climate and climate change. A 1999 report includes a section on the impacts of climate change on human health.

K. Carslow, School of the Environment, University of Leeds, UK, presents lecture notes for a course on the scientific issues of climate change.

E. Takle, Department of Geological and Atmospheric Sciences, Iowa State University, offers lecture notes and other resources for an Internet course on global change.

R. Myneni, Department of Geography, Boston University, offers lecture notes and links to Web resources for a course on global climate change and environmental impacts.

“Malaria, climate, and poverty” is a July 1999 discussion paper by J. Gallup and J. Sachs, made available by the Harvard Center for International Development.

The American Council on Science and Health makes available a 1997 position paper (in Adobe Acrobat format) by S. Shindell and J. Raso titled “Global climate change and human health.”

The 16 July 1999 issue of Science had an Enhanced Perspective by P. Epstein titled “Climate and health.”

The August 2000 issue of Scientific American had an article by P. Epstein titled “Is global warming harmful to health?”

The August 1997 issue of the Atlantic Monthly had an article about malaria by E. Shell titled “The resurgence of a deadly disease.”

Numbered Hypernotes

1. Links to different versions of the translated text of Exodus 8 are made available by the Christian Classics Ethereal Library Web site provided by Calvin College, Grand Rapids, MI. The New English Translation Web page provides notes on the translation of Exodus 8:21.

2. L. Higley, Department of Entomology, University of Nebraska, provides lecture notes on insect-borne diseases, malaria, and mosquitoes for an entomology course on insects, science, and society. Insects, Disease, and History, a Web site provided by G. Miller and R. Peterson, focuses on the influence of insect-borne disease on history. The Military Pest Management Handbook, made available on the Web by the U. S. Armed Forces Pest Management Board, has a chapter on medically important arthropods, which includes a section on mosquitoes. A student review article by G. Walker titled “Anopheles gambiae, the vector of malaria” was prepared for a course on insect behavior taught by L. Bjostad, Department of Entomology, Colorado State University. The July-September 1998 issue of Emerging Infectious Diseases had an article by D. Gubler titled “Resurgent vector-borne diseases as a global health problem.” The 1 August 2000 issue of the Proceedings of the National Academy of Sciences had an article by S. Hay et al. titled “Etiology of interepidemic periods of mosquito-borne disease.” The Center for International Earth Science Information Network at Columbia University provides a thematic guide to human health and global environmental change that has a section on changes in the incidence of vector-borne diseases attributable to climate change.

3. PDPx (Identification and Diagnosis of Parasites of Public Health Concern), a reference resource provided by the CDC's Division of Parasitic Diseases, offers a introduction to malaria. The National Institute of Allergy and Infectious Diseases makes available a brochure on malaria and other malaria information resources. provides Encyclopædia Britannica articles on malaria, Plasmodium, and mosquitoes. Malaria Website is a student project for a course on vaccine development at Brown University; a presentation on the epidemiology of malaria is included. The history of malaria is discussed in a presentation by T. Bradley on malaria and drug resistance for a microbiology course offered by the Department of Microbiology and Immunology, University of Leicester, UK; an introduction to malaria is also available.The Proceedings of the Royal College of Physicians of Edinburgh (vol. 28, no. 3, 1998) had an article by M. Jones titled “Modern malaria.” The 1902 Nobel Prize in Physiology or Medicine was awarded to Ronald Ross “for his work on malaria, by which he has shown how it enters the organism and thereby has laid the foundation for successful research on this disease and methods of combating it.”

4. The CDC provides information on dengue fever and yellow fever; the April-June 1995 issue of the CDC's Emerging Infectious Diseases had an article titled “Dengue/dengue hemorrhagic fever: The emergence of a global health problem.” WHO provides information on dengue and yellow fever; information about yellow fever is also available on WHO's Diseases and Vaccines Web site.

5. D. Rogers is in the Trypansomiasis and Land Use in Africa Research Group, Department of Zoology, University of Oxford. S. Randolph is at the Oxford Tick Research Group, Department of Zoology, University of Oxford.

6. The Atlas of Medical Parasitology, made available by the Carlo Denegri Foundation, Torino, Italy, includes an illustrated introduction to Plasmodium falciparum. A student-prepared tutorial and case study of Plasmodium falciparum is offered for a course on protistology taught by J. Berger, Department of Zoology, University of British Columbia. L. Simpson, Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, provides lecture notes on Plasmodium for a course on molecular parasitology; an introduction to protozoa and parasites with information on the history of parasitology is also provided. Parasites and Parasitological Resources includes an illustrated introduction to Plasmodium and its life cycle. The Malaria Database offers a presentation on Plasmodium parasites and malaria. The 20 June 2000 issue of the Proceedings of the National Academy of Sciences had an article by S. Rich and F. Ayala titled “Population structure and recent evolution of Plasmodium falciparum.”

7. The Global Warming Web site of he U.S. Environmental Protection Agency provides information about the impacts of global warming. The Climate Change Web site from Environment Canada offers a feature titled “The science of climate change.” The Education Center Web site of the Atmospheric Radiation Measurement Program provides background papers on global warming and its possible effects. The Natural Resources Defense Council provides a presentation on global warming. The Union of Concerned Scientists offer a presentation on global warming including a fact sheet on the science of global warming.

8. The Department of Statistics, Pennsylvania State University, provides a description of multivariate analysis. A. Fielding, Department of Biological Sciences, Manchester Metropolitan University, UK, provides an introduction to multivariate techniques. M. Walker, Department of Environmental, Population, and Organismic Biology, University of Colorado, provides lecture notes for a course on multivariate analysis for ecologists. D. Cook, Department of Statistics, Iowa State University, provides lecture notes for a course on multivariate statistical methods. M. Wulder, Pacific Forestry Centre, Natural Resources Canada, Victoria, offers a practical guide to the use of multivariate statistics.

9. Background information on climate and malaria and climate change and malaria is provided by C. Reid in a student thesis titled “Implications of climate change on malaria in Karnataka, India,” which is made available on the Web by the Center for Environmental Studies, Brown University.

10. The January-February 2000 issue of Emerging Infectious Diseases had an article by P. Reiter titled “From Shakespeare to Defoe: Malaria in England in the Little Ice Age.”

11. The National Geographic Society provides a map of Africa. Information about Mali is provided in the CIA's World Factbook. A guide to Mali is provided by the Lonely Planet Web site.

12. J. Hinde, School of Mathematical Sciences, University of Exeter, UK, provides an introduction to multiple regression for a course on multivariate analysis.

13. The National Institute of Allergy and Infectious Diseases makes available the final report of the 1997 International Conference on Malaria in Africa. The July-September 1998 issue of Emerging Infectious Diseases had an article by T. Nchinda titled “Malaria: A reemerging disease in Africa.” “Towards an atlas of malaria risk in Africa” is a 1998 technical report of the MARA/ARMA (Mapping Malaria Risk in Africa / Atlas du Risque de la Malaria en Afrique) collaboration; chapters on data collection, modeling, and highlands malaria are included. The Multilateral Initiative on Malaria is a collaborative alliance to maximize the impact of scientific research against malaria in Africa; links to other anti-malaria programs and summaries of news about malaria are provided. Malaria and Infectious Diseases in Africa, sponsored by SmithKline Beecham International, is an online French/English bilingual journal; a list of malaria-related conferences is maintained.

14. The WWW Virtual Library of Epidemiology is maintained by the Department of Epidemiology and Biostatistics at the University of California, San Francisco. The library of the Karolinska Institutet, Stockholm, provides links to Internet resources for epidemiology and biostatistics. The Web Supercourse on epidemiology, the Internet, and global health offers lecture notes by H. Guerra on malaria. T. Terry, Department of Molecular and Cell Biology, University of Connecticut, provides lecture notes on epidemiology for a microbiology course. S. Baron's Medical Microbiology includes a chapter by P. Brachman on epidemiology. The British Medical Journal (BMJ) makes available Epidemiology for the Uninitiated by D. Coggon, G. Rose, and D. Barker.

15. The NASA Goddard Institute for Space Studies offers a presentation on global climate modeling.The Hadley Centre for Climate Prediction and Research includes a section on modeling climate change in a report titled “Climate change and its impacts - A global perspective.” The Climatic Research Unit of the University of East Anglia, Norwich, UK, provides an information sheet on modeling climate change and general circulation models. R. Myneni offers lecture notes titled “Climate models: Projections of future climate change” and lecture notes titled “Global climate models and their evaluation” for a course on global climate change. K. Carslow presents lecture notes on climate models for a course on the scientific issues of climate change. E. Takle provides lecture notes on climate models with links to Web resources for a course on global change. R. Gallop, School of Environmental Sciences and Land Management, University College Worcester, UK, provides lecture notes and Web links for a course on modeling Earth's climate.

16. INDEPTH (International Network of field sites with continuous Demographic Evaluation of Populations and Their Health in developing countries) provides links to network sites and other related Internet resources.

17. Radcliffe's IPM World Textbook, from the University of Minnesota, includes a chapter by C. Curtis on the control of malaria vectors in Africa and Asia. The science education page of the Department of Bacteriology, University of Wisconsin, makes available an article titled “The worldwide malaria eradication effort of 1957-1974.” The WHO World Health Report 1999 includes a chapter (in Adobe Acrobat format) titled “Rolling back malaria” that has a section on the past, present, and future of malaria control. R. C. Sponsler's Web site, a resource for malaria information, includes a presentation on malaria control. The 23 January 1998 issue of Science had an article by B. Mons, E. Klasen, R. van Kessel, and T. Nchinda titled “Partnership between South and North crystallizes around malaria.” The August-September 1997 issue of Technology Review had an article by D. Wirth and J. Cattani titled “Winning the war against malaria.” The 1 July 2000 issue of Science News had an article by J. Raloff titled “The case for DDT: What do you do when a dreaded environmental pollutant saves lives?” A report by R. Tren titled “The economic costs of malaria in South Africa: Malaria control and the DDT issue” is made available by the Institute for Economic Affairs, London. The MEASURE Evaluation Web site makes available in Adobe Acrobat format a working paper by T. Eisele et al. titled “Evaluating malaria interventions in Africa: A review and assessment of recent research.”

18. Roll Back Malaria, a global partnership of the World Bank, the World Health Organization, the United Nations Children's Fund, and the United Nations Development Programme, makes available the Twentieth Report of the WHO Expert Committee on Malaria, which reviews the progress made since 1992 in the implementation of the Global Malaria Control Strategy and analyzes the effect of health sector reforms on malaria control programs. The 28 June 1998 issue of Science had an article by D. Nabarro and E. Tayler titled “The ‘Roll Back Malaria' campaign.”

19. C. Dye is the Department of Communicable Diseases Control, Prevention and Eradication, World Health Organization, Geneva. P. Reiter is the Dengue Branch, Division of Vector-Borne Infectious Diseases, National Center for Infectious Diseases, CDC.

References and Notes

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