Climate Cycles and Forecasts of Cutaneous Leishmaniasis, a Nonstationary Vector-Borne Disease

Abstract

Background

Cutaneous leishmaniasis (CL) is one of the main emergent diseases in the Americas. As in other vector-transmitted diseases, its transmission is sensitive to the physical environment, but no study has addressed the nonstationary nature of such relationships or the interannual patterns of cycling of the disease.

Methods and Findings

We studied monthly data, spanning from 1991 to 2001, of CL incidence in Costa Rica using several approaches for nonstationary time series analysis in order to ensure robustness in the description of CL's cycles. Interannual cycles of the disease and the association of these cycles to climate variables were described using frequency and time-frequency techniques for time series analysis. We fitted linear models to the data using climatic predictors, and tested forecasting accuracy for several intervals of time. Forecasts were evaluated using “out of fit” data (i.e., data not used to fit the models). We showed that CL has cycles of approximately 3 y that are coherent with those of temperature and El Niño Southern Oscillation indices (Sea Surface Temperature 4 and Multivariate ENSO Index).

Conclusions

Linear models using temperature and MEI can predict satisfactorily CL incidence dynamics up to 12 mo ahead, with an accuracy that varies from 72% to 77% depending on prediction time. They clearly outperform simpler models with no climate predictors, a finding that further supports a dynamical link between the disease and climate.

Abstract

Using mathematical models, the authors show that cutaneous leishmaniasis has cycles of approximately three years that are related to temperature cycles and indices of the El Niño Southern Oscillation.

Editors' Summary

Background.

Every year, 2 million people become infected with a pathogenic species of Leishmania, a parasite that is transmitted to humans through the bites of infected sand flies. These flies—the insect vectors for disease transmission—pick up parasites by biting infected animals—the reservoirs for the parasite. Once in a person, some species of Leishmania can cause cutaneous leishmaniasis, a condition characterized by numerous skin lesions. These usually heal spontaneously but can leave ugly, sometimes disabling scars. Leishmaniasis is endemic and constantly present in many tropical and temperate countries, but as with other diseases that are transmitted by insect vectors (for example, malaria), the occurrence of cases has a strong seasonal pattern and also varies from year to year (interannual variability). These fluctuations suggest that leishmaniasis transmission is sensitive to seasonal changes in the climate and to climatic events like the El Niño Southern Oscillation (ENSO), a major cause of interannual weather and climate variation around the world that repeats every 3–4 years. This sensitivity arises because the climate directly affects the abundance of sand flies and how quickly the parasites replicate.

Why Was This Study Done?

It would be very useful to have early warning systems for leishmaniasis and other vector-transmitted diseases so that public health officials could prepare for epidemics—or spikes in the number of cases—of these diseases. Monitoring of climatic changes could form the basis of such systems. But although it is clear that the transmission of cutaneous leishmaniasis is affected by fluctuations in the climate, there have been no detailed studies into the dynamics of its seasonal or yearly variation. In this study, the researchers used climatic data and information about cutaneous leishmaniasis in Costa Rica to build statistical models that investigate how climate affects leishmaniasis transmission.

What Did the Researchers Do and Find?

The researchers obtained the monthly records for cutaneous leishmaniasis in Costa Rica for 1991 to 2001. They then used several advanced statistical models to investigate how these data relate to climatic variables such as the sea surface temperature (a measure of El Niño, a large-scale warming of the sea), average temperature in Costa Rica, and the MEI (the Multivariate ENSO Index, a collection of temperature and air pressure measurements that predicts when the ENSO is going to occur). Their analyses show that cutaneous leishmaniasis cases usually peak in May and that the incidence of the disease (number of cases occurring in the population over a set time period) rises and falls in three-year cycles. These cycles, they report, match up with similar-length cycles in the climatic variables that they investigated. Furthermore, when the researchers tested the models they had constructed with data that had not been used to construct the models (“out of fit” data), the models predicted variations in the incidence of cutaneous leishmaniasis for up 12 months with an accuracy of about 75% (that is, the predictions were correct three times out of four).

What Do These Findings Mean?

The finding that interannual cycles of climate variables and cutaneous leishmaniasis coincide provides strong evidence that climate does indeed affect the transmission of this disease. This link is strengthened by the ability of the statistical models described by the researchers to predict outbreaks with high accuracy. The researchers' new insights into how climate affects the transmission of cutaneous leishmaniasis are important because they open the door to the possibility of setting up an early warning system for this increasingly common disease. The same statistical approach could be used to improve understanding of how climate affects the dynamics of other vector-transmitted diseases and to design early warning systems for them as well—the World Health Organization has identified 18 diseases for which climate-based early warning systems might be useful but no such systems are currently being used to plan disease control strategies. Finally, the improved understanding of the relationship between climate and disease transmission that the researchers have gained through their study is an important step towards being able to predict how the incidence and distribution of leishmaniasis and other vector-transmitted diseases will be affected by global warming.

Additional Information.

Please access these Web sites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.0030295.

• United States Centers for Disease Control and Prevention fact sheet on leishmaniasis

• MedlinePlus encyclopedia entry on leishmaniasis

• World Health Organization information on leishmaniasis and on climate change and health

• Wikipedia pages on leishmaniasis and on the El Niño Southern Oscillation (note that Wikipedia is a free online encyclopedia that anyone can edit)