Menno J. Bouma

El Niño and health

El Niño Southern Oscillation (ENSO) is a climate event that originates in the Pacific Ocean but has wide-ranging consequences for weather around the world, and is especially associated with droughts and floods. The irregular occurrence of El Niño and La Niña events has implications for public health. On a global scale, the human effect of natural disasters increases during El Niño. The effect of ENSO on cholera risk in Bangladesh, and malaria epidemics in parts of South Asia and South America has been well established. The strongest evidence for an association between ENSO and disease is provided by time-series analysis with data series that include more than one event. Evidence for ENSOs effect on other mosquito-borne and rodent-borne diseases is weaker than that for malaria and cholera. Health planners are used to dealing with spatial risk concepts but have little experience with temporal risk management. ENSO and seasonal climate forecasts might offer the opportunity to target scarce resources for epidemic control and disaster preparedness.

Inapparent infections and cholera dynamics.

In many infectious diseases, an unknown fraction of infections produce symptoms mild enough to go unrecorded, a fact that can seriously compromise the interpretation of epidemiological records. This is true for cholera, a pandemic bacterial disease, where estimates of the ratio of asymptomatic to symptomatic infections have ranged from 3 to 100 (refs 1–5). In the absence of direct evidence, understanding of fundamental aspects of cholera transmission, immunology and control has been based on assumptions about this ratio and about the immunological consequences of inapparent infections. Here we show that a model incorporating high asymptomatic ratio and rapidly waning immunity, with infection both from human and environmental sources, explains 50 yr of mortality data from 26 districts of Bengal, the pathogen’s endemic home. We find that the asymptomatic ratio in cholera is far higher than had been previously supposed and that the immunity derived from mild infections wanes much more rapidly than earlier analyses have indicated. We find, too, that the environmental reservoir (free-living pathogen) is directly responsible for relatively few infections but that it may be critical to the disease’s endemicity. Our results demonstrate that inapparent infections can hold the key to interpreting the patterns of disease outbreaks. New statistical methods, which allow rigorous maximum likelihood inference based on dynamical models incorporating multiple sources and outcomes of infection, seasonality, process noise, hidden variables and measurement error, make it possible to test more precise hypotheses and obtain unexpected results. Our experience suggests that the confrontation of time-series data with mechanistic models is likely to revise our understanding of the ecology of many infectious diseases.

Cholera and climate: revisiting the quantitative evidence

Cholera dynamics in endemic regions display regular seasonal cycles and pronounced interannual variability. We review here the current quantitative evidence for the influence of climate on cholera dynamics with reference to the early literature on the subject. We also briefly review the incipient status of mathematical models for cholera and argue that these models are important for understanding climatic influences in the context of the population dynamics of the disease. A better understanding of disease risk related to the environment should further underscore the need for changing the socioeconomic conditions conducive to cholera.

The El-Nino Southern Oscillation and the historic malaria epidemics on the Indian subcontinent and Sri Lanka: an early warning system for future epidemics?

The recurrent great malaria epidemics which occurred in the Punjab province of former British India and Ceylon before the introduction of residual insecticides have been related to excessive and failing monsoon rains respectively. In the arid Punjab, rainfall facilitated breeding and increased the lifespan of the mosquito vector and, in the wet part of Ceylon, failing monsoon rains caused rivers to pool, creating more favourable breeding conditions. The periodic fluctuations in monsoon rainfall and epidemic malaria are here explained in relation to the El Niño Southern Oscillation. In the Punjab, epidemic malaria between 1868 and 1943 correlates significantly (r=0.34, P<0.005) with the sea surface temperature anomalies in the Eastern Equatorial Pacific, a parameter of the oscillation, and epidemics were significantly more prevalent in a year with a wet monsoon following a dry El Niño year than in other years. In Ceylon, epidemics were significantly more prevalent during El Niño years, when the same south‐west monsoon tends to fail. With the reduced reliance on residual insecticides and the recurrence of epidemic malaria on the Indian subcontinent, advances made in predicting El Niño events may be used to forecast high and low risk years for future malaria epidemics.

Altitudinal Changes in Malaria Incidence in Highlands of Ethiopia and Colombia

Altitude Sickness Whether the incidence of malaria will be (or has been) affected by the warming climate is poorly resolved. Global-scale analyses are fraught with technical difficulties, including problems with separating out changes resulting from destruction of mosquito habitat, insecticide use, and antimalarial drug use from multidecadal trends in climate change. Siraj et al. (p. 1154) performed parallel analyses of highland malaria in Ethiopia and Colombia to ask whether interannual changes in temperature could explain variation in malaria incidence with altitude. Modeling the data confirmed that malaria moves up in elevation in warmer years and allowed estimates of how many more millions of cases could be expected in tropical highland areas if the mean temperature increased by 1° to 3°C. Warmer years promote malaria cases at higher altitudes. The impact of global warming on insect-borne diseases and on highland malaria in particular remains controversial. Temperature is known to influence transmission intensity through its effects on the population growth of the mosquito vector and on pathogen development within the vector. Spatiotemporal data at a regional scale in highlands of Colombia and Ethiopia supplied an opportunity to examine how the spatial distribution of the disease changes with the interannual variability of temperature. We provide evidence for an increase in the altitude of malaria distribution in warmer years, which implies that climate change will, without mitigation, result in an increase of the malaria burden in the densely populated highlands of Africa and South America.

Shifting patterns: malaria dynamics and rainfall variability in an African highland

The long-term patterns of malaria in the East African highlands typically involve not only a general upward trend in cases but also a dramatic increase in the size of epidemic outbreaks. The role of climate variability in driving epidemic cycles at interannual time scales remains controversial, in part because it has been seen as conflicting with the alternative explanation of purely endogenous cycles exclusively generated by the nonlinear dynamics of the disease. We analyse a long temporal record of monthly cases from 1970 to 2003 in a highland of western Kenya with both a time-series epidemiological model (time-series susceptible–infected–recovered) and a statistical approach specifically developed for non-stationary patterns. Results show that multiyear cycles of malaria outbreaks appear in the 1980s, concomitant with the timing of a regime shift in the dynamics of cases; the cycles become more pronounced in the 1990s, when the coupling between disease and rainfall is also stronger as the variance of rainfall increased at the frequencies of coupling. Disease dynamics and climate forcing play complementary and interacting roles at different temporal scales. Thus, these mechanisms should not be viewed as alternative and their interaction needs to be integrated in the development of future predictive models.

Predicting high-risk years for malaria in Colombia using parameters of El Niño Southern Oscillation.

The interannual variation in malaria cases in Colombia between 1960 and 1992 shows a close association with a periodic climatic phenomenon known as El Niño Southern Oscillation (ENSO). Compared with other years, malaria cases increased by 17.3% during a Niño year and by 35.1% in the post‐Niño year. The annual total number of malaria cases is also strongly correlated (r= 0.62, P < 0.001) with sea surface temperature (SST) anomalies in the eastern equatorial Pacific, a principal parameter of ENSO. The strong relation between malaria and ENSO in Colombia can be used to predict high and low‐risk years for malaria with sufficient time to mobilize resources to reduce the impact of epidemics. In view of the current El Niño conditions, we anticipate an increase in malaria cases in Colombia in 1998. Further studies to elucidate the mechanisms which underlie the association are required. As Colombia has a wide range of climatic conditions, regional studies relating climate and vector ecology to malaria incidence may further improve an ENSO‐based early warning system. Predicting malaria risk associated with ENSO and related climate variables may also serve as a short‐term analogue for predicting longer‐term effects posed by global climate change.

Epidemic malaria and warmer temperatures in recent decades in an East African highland

Climate change impacts on malaria are typically assessed with scenarios for the long-term future. Here we focus instead on the recent past (1970–2003) to address whether warmer temperatures have already increased the incidence of malaria in a highland region of East Africa. Our analyses rely on a new coupled mosquito–human model of malaria, which we use to compare projected disease levels with and without the observed temperature trend. Predicted malaria cases exhibit a highly nonlinear response to warming, with a significant increase from the 1970s to the 1990s, although typical epidemic sizes are below those observed. These findings suggest that climate change has already played an important role in the exacerbation of malaria in this region. As the observed changes in malaria are even larger than those predicted by our model, other factors previously suggested to explain all of the increase in malaria may be enhancing the impact of climate change.

Permethrin-treated chaddars and top-sheets: appropriate technology for protection against malaria in Afghanistan and other complex emergencies.

Insecticide-treated mosquito nets (ITN) provide excellent protection against malaria; however, they have a number of shortcomings that are particularly evident in politically unstable countries or countries at war: not everyone at risk can necessarily afford a net, nets may be difficult to obtain or import, nets may not be suitable for migrants or refugees sleeping under tents or plastic shelter. There is a need to develop cheaper, locally appropriate alternatives for the most impoverished and for victims of complex emergencies. Afghan women, in common with many Muslim peoples of Asia, wear a veil or wrap known as a chaddar to cover the head and upper body. This cloth doubles as a sheet at night, when they are used by both sexes. A randomized controlled trial was undertaken in which 10% of the families of an Afghan refugee camp (population 3950) in north-western Pakistan had their chaddars and top-sheets treated with permethrin insecticide at a dosage of 1 g/m2 while a further 10% had their chaddars treated with placebo formulation. Malaria episodes were recorded by passive case detection at the camps health centre. From August to November the odds of having a falciparum or vivax malaria episode were reduced by 64% in children aged 0-10 years and by 38% in refugees aged < 20 years in the group using permethrin-treated chaddars and top-sheets. Incidence in refugees over 20 years of age was not significantly reduced. The cost of the permethrin treatment per person protected (US

Forcing Versus Feedback: Epidemic Malaria and Monsoon Rains in Northwest India

0.17) was similar to that for treating bednets (and cost only 10-20% of the price of a new bednet). An entomological study simulating real-life conditions indicated that host-seeking mosquitoes were up to 70% less successful at feeding on men sleeping under treated chaddars and some were killed by the insecticide. Permethrin-treated top-sheets and blankets should provide appropriate and effective protection from malaria in complex emergencies. In Islamic and non-Islamic countries in Asia, treated chaddars and top-sheets should offer a satisfactory solution for the most vulnerable who cannot afford treated nets.