Is the incidence of malaria now increasing due to recent climate changes?
Expert response by Professor Paul Reiter
Paul Reiter is a professor of medical entomology at the Pasteur Institute in Paris, France. He is a member of the World Health Organization Expert Advisory Committee on Vector Biology and Control. He was a staff member of the Center for Disease Control (Dengue Branch) for 22 years. He is a Fellow of the Royal Entomological Society. He is a specialist in mosquito-borne diseases such as malaria and dengue fever. (Professor Reiter wishes to make it clear that his response below relates only to causes of malaria, not to whether or not there is man-made global warming).
Malaria is not related to climate change
Speculations on the potential impact of climate change on human health frequently focus on malaria. Predictions are common that in the coming decades, tens – even hundreds – of millions more cases will occur in regions where the disease is already present, and that transmission will extend to higher latitudes and altitudes. Such predictions, sometimes supported by simple models, are persuasive because they are intuitive, but they sidestep factors that are key to the transmission and epidemiology of the disease: the ecology and behaviour of both humans and vectors, and the immunity of the human population.
Numerous review publications and substantial media attention have had a major impact on public perceptions of the issue. In most cases, these publications make brief mention of where malaria occurs and how it is transmitted, followed by a succession of statements on the action of temperature, rainfall and other climate variables on specific components of the transmission cycle. These statements – often valid in themselves – are used to justify disquieting predictions that are persuasive because they are intuitive. Some are based on mathematical models that select a climate variable (usually temperature), propose a direct interaction with a transmission parameter (e.g. multiplication of the parasite, survival of the vector), and inevitably arrive at the same conclusions. Many focus on the vulnerability of people in poorer countries and place the blame squarely on the activities of the industrial nations. A deplorable trend in the scientific press is the inclusion of a political message, much as in the popular media.
The great majority of these publications sidestep four factors that are key to the transmission and epidemiology of the disease: the ecology and behaviour of humans, and the ecology and behaviour of the vectors. There is rarely any mention of a fifth, the immunity of the host and of the host population. These factors interact with each other, and are themselves made up of an intricate network of highly variable parameters. The true dynamics of transmission can only be assessed by taking this daunting complexity into account. Moreover, the key climate variables – temperature, rainfall and humidity – cannot be viewed independently; the effects of temperature are modified by humidity, the daily range of each may be more significant than the daily mean, brief periods of atypical heat or cold can be more significant than long-term averages, heavy storms can have a different impact than light prolonged rainfall, one year’s events may have a significant impact on subsequent years, and so on.
In summary, a holistic view of the complex natural history of malaria in the precise setting where it is transmitted is mandatory for any speculation on the role of climate variables; the significance of these variables, and their putative role in future climates, can only be assessed in the perspective of this complexity.
There is a widespread misconception that mosquito-borne diseases require tropical temperatures, or at least the temperatures of the warmer temperate regions. A glance at a map of global isotherms reveals that summer temperatures in many temperate regions are at least as high as in the warmest seasons of many regions in the tropics. The crucial difference is that the tropics do not have cold winters. Moreover, if tropical mosquito-borne pathogens are introduced to temperate regions in the right season, they can be transmitted, if suitable vectors are present.
There is also a misconception that mosquitoes die in winter, and that more die in colder winters, but it is obvious that mosquitoes – and indeed all life-forms that are native to temperate regions – have evolved strategies to survive low temperatures. In the tropics, comparable adaptations are necessary for survival during unfavourable dry periods that may last for several years. In both cases, such adaptations merely impose seasonality on transmission.
The physical environment is an important modifier of local climate. Anopheles arabiensis, an important vector of malaria in Africa, can survive in the Sudan when outdoor temperatures are above 55°C by hiding in the thatch of buildings in the daytime, feeding after mid-night, and ovipositing at dawn or dusk. In Lapland, in the past, anopheline species survived the winter in houses and stables, feeding occasionally, and transmitting malaria when outdoor temperatures were below -40°C.
These examples underline the limited value of meteorological variables as a guide to the behaviour and geographic range of vector species, and of the pathogens they transmit.
Malaria in temperate regions
Few people are aware that it is less than forty years since the final eradication of malaria in Europe and the United States. Indeed, the disease was common in the period from the 16th to 18th centuries that climatologists term the Little Ice Age, and data from burial records around the Thames estuary reveal that mortality in “marsh parishes” of England was comparable to that in areas of transmission in sub-Saharan Africa today [40,41].
Until the mid-19th century, the northern limit of transmission was roughly defined by the present 15°C July isotherm. Denmark and parts of Sweden suffered devastating epidemics until the 1860s. Incidence diminished thereafter and the disease had essentially disappeared around the turn of the 20th Century. The same was true in Finland, except for a brief recrudescence in 1941, during the Russo-Finnish war. In England, there was a gradual decrease in transmission until the 1880s, after which it dropped precipitously and became relatively rare, except in a short period following World War I. In Germany, transmission also diminished rapidly. After World War I it was mainly confined to a few marshy localities.
Reasons for decline
This regional decline is attributed to a combination of factors:
Ecological change: Improved drainage, reclamation of swampy land for cultivation and the adoption of new farming methods all served to eliminate mosquito habitat (there is an old Italian saying: “malaria flees before the plough”).
New farm crops: New root crops such as turnips and mangel-wurzels were adopted as winter fodder. These enabled farmers to maintain larger numbers of animals, particularly cattle, throughout the year. European vectors of malaria readily bite cattle, so the increasing size of herds diverted mosquitoes from feeding on humans. Human malaria parasites cannot infect cattle, so this diversion reduced the number of infected mosquitoes and infective bites.
New rearing practices: Selective breeding of cattle, and new introductions (e.g. the Chinese domestic pig), in combination with the new fodder crops, enabled farmers to keep large populations of stock in farm buildings rather than in open fields and woodland. These buildings provided attractive sites for adult mosquitoes to rest and feed, diverting them from human habitation.
Urbanization and mechanization: Rural populations declined as industrialization drew people to urban areas. The increased ratio of cattle to people further reduced the attack rates of mosquitoes on humans.
Human living conditions: New building materials and improvements in construction methods made houses more mosquito-proof, especially in winter, another factor that reduced contact with the vector.
Medical care: Greater access to medical care, and wider use of quinine (in part due to a major reduction in price) reduced the survival rate of the malaria parasite in its human host, thus limiting the infection rate of mosquitoes.
Decline not due to climate change
These factors are a classic illustration of the role of ecology and behaviour in the prevalence and incidence of a mosquito-borne disease. Moreover, the decline cannot be attributed to climate change, for it occurred at the start of the current warming phase. Nor can it be attributed, as is often stated, to deliberate mosquito control, for it came before recognition of the role of the vector.
In contrast, in countries that lagged in these changes, malaria did not decline “spontaneously”. In the Soviet-block countries, for example, from Poland to eastern Siberia, major epidemics occurred throughout the 19th century and the disease remained one of the principal public health problems for the entire first half of the 20th century.
The advent of DDT revolutionized malaria control. Cheap, safe, effective applications of the chemical could be targeted at the site where most infections occur – in the home. Initial efforts in Italy, Cyprus and Greece were so successful that a decision was made to eradicate the disease from all of Europe. The entire continent was finally declared free of endemic malaria in 1975. One of the last countries affected was Holland.
Ninety percent of the estimated 300–500 million cases of malaria worldwide occur each year in sub-Saharan Africa. Statements on climate change and human health often focus on this region, with predictions that, by the mid-21st century, tens of millions more cases will occur there as a direct result of increasing temperatures.
The world’s population has grown from 2.5 billion in 1950 to over 6.7 billion. In sub-Saharan Africa, there are now nearly five times as many people (ca. 750 million) as there were in 1955. In some countries, more than half the population is under 15 years of age. High birth rates often give rise to larger communities with higher densities of people, which can lead to a higher attack rate; clinical studies in some parts of Africa quote 998 infections per 1,000 infants.
Forest clearance; Many malaria vectors breed in open, sunlit pools. Forest clearance provides abundant new habitat for these species, a classic cause of the emergence of malaria problems.
Agriculture: Irrigation creates an ideal habitat for mass-production of mosquitoes, as can construction of dams for hydroelectric power. Rice cultivation provides an environment for many of the most efficient malaria vectors. Conversely, the cultivation of ground depressions can suppress such vectors and thereby reduce transmission.
Movement of people: Infected people in pursuit of work can introduce malaria to areas where it is rare. Non-immune people are at high risk if they move to areas of transmission. Extensive road building and modern transportation have greatly exacerbated this factor.
Urbanization: Water storage and inadequate water disposal can provide habitat for mosquitoes, particularly in rapidly expanding urban areas. The absence of cattle can promote stable transmission by forcing zoophilic species to feed on people. Moreover, many tropical cities are surrounded by densely-populated, satellite settlements that are essentially rural in nature.
Insecticide resistance: Physiological resistance to insecticides is common in many regions. Behavioural resistance can also be a major problem: species that prefer to feed and rest indoors (endophilic) can switch to outdoor (exophilic) activity in response to treatment of indoor surfaces with insecticides.
Drug resistance: In many parts of the world, the malaria parasite has evolved resistance to commonly used anti-malarial drugs. Substitutes are available, but are much more expensive.
Degradation of the health infrastructure: Lack of funding, institutional difficulties, rapid urbanization and other problems associated with rapid development have eroded the public health sector of many countries. In addition, the AIDS pandemic has overwhelmed the ability of authorities to deal with other diseases.
Simplistic reasoning on the future prevalence of malaria is ill-founded; malaria is not limited by climate in most temperate regions, nor in the tropics, and in nearly all cases, “new” malaria at high altitudes is well below the maximum altitudinal limits for transmission. Future changes in climate may alter the prevalence and incidence of the disease, but obsessive emphasis on “global warming” as a dominant parameter is indefensible; the principal determinants are linked to ecological and societal change, politics and economics. There is a critical need for cheap, effective control campaigns, as were implemented during the DDT era. A creative and organized search for new strategies, perhaps based on new technologies, is urgently required, irrespective of future climate change.
The foregoing is a condensation of an article by Dr Reiter in the Malaria Journal: