Cutaneous Leishmaniasis and Sand Fly Fluctuations Are Associated with El Nino in Panama

BackgroundCutaneous Leishmaniasis (CL) is a neglected tropical vector-borne disease. Sand fly vectors (SF) and Leishmania spp parasites are sensitive to changes in weather conditions, rendering disease transmission susceptible to changes in local and global scale climatic patterns. Nevertheless, it is unclear how SF abundance is impacted by El Nino Southern Oscillation (ENSO) and how these changes might relate to changes in CL transmission.Methodology and FindingsWe studied association patterns between monthly time series, from January 2000 to December 2010, of: CL cases, rainfall and temperature from Panama, and an ENSO index. We employed autoregressive models and cross wavelet coherence, to quantify the seasonal and interannual impact of local climate and ENSO on CL dynamics. We employed Poisson Rate Generalized Linear Mixed Models to study SF abundance patterns across ENSO phases, seasons and eco-epidemiological settings, employing records from 640 night-trap sampling collections spanning 2000?2011. We found that ENSO, rainfall and temperature were associated with CL cycles at interannual scales, while seasonal patterns were mainly associated with rainfall and temperature. Sand fly (SF) vector abundance, on average, decreased during the hot and cold ENSO phases, when compared with the normal ENSO phase, yet variability in vector abundance was largest during the cold ENSO phase. Our results showed a three month lagged association between SF vector abundance and CL cases.ConclusionAssociation patterns of CL with ENSO and local climatic factors in Panama indicate that interannual CL cycles might be driven by ENSO, while the CL seasonality was mainly associated with temperature and rainfall variability. CL cases and SF abundance were associated in a fashion suggesting that sudden extraordinary changes in vector abundance might increase the potential for CL epidemic outbreaks, given that CL epidemics occur during the cold ENSO phase, a time when SF abundance shows its highest fluctuations

Generalized linear mixed Poisson rate model parameter estimates.

<p>PAC =  proportional abundance change, Est =  Estimate, Var =  Variance. Model assumptions were met, thus ensuring a sound inference.</p><p>*Statistically significant (P<0.05);</p>¶<p>Estimated Abundance/trap-night/month for domiciliary samples, collected in January during the normal phase of ENSO.</p><p>Generalized linear mixed Poisson rate model parameter estimates.</p

Correlation between selected lags of the Cutaneous Leishmaniasis cases from Republic of Panamá time series, and climatic covariates.

<p>Time lags are indicated inside parenthesis “()” and SST4, Temp and Rain are, respectively, abbreviations for Sea Surface Temperature 4 (El Niño 4 Index), Temperature and Rainfall. Circle size indicates the magnitude of the association, while color indicates the sign of the correlation, a scale is presented in the right margin of the figure.</p

Cutaneous Leishmaniasis cases (CL) seasonality.

<p>(A) Boxplots of monthly incidence. Boxes contain data within the 25^th to 75^th quantiles. Lines inside the boxes show the median of the distribution for each month. (B) Seasonal (year-long) time series. Colors indicate the ENSO phase, see inset legend for details.</p

Sand Fly vector species abundance during the different ENSO phases and by eco-epidemiological environment.

<p>Abundance by ENSO phase: (A) <i>Lutzomyia gomezi</i> (B) <i>Lu trapidoi</i> (C) <i>Lu panamensis</i>. Abundance by eco-epidemiological environment: (D) <i>Lu gomezi</i> (E) <i>Lu trapidoi</i> (F) <i>Lu panamensis</i>. Panels A, B and C show data only for April, October and November where the number of trap-nights was above 30. In all panels the y-axis is in a logarithmic scale.</p

Parameter estimates for the best model.

<p>AR, SST4 and T stand, respectively, for Autoregressive, Sea Surface Temperature 4 (El Niño 4 Index) and Temperature.</p><p>Parameter estimates for the best model.</p

Monthly time series data (2000–2010).

<p>(A) Cutaneous Leishmaniasis cases in the Republic of Panamá (B) Rainfall (C) Temperature. The solid line indicates the averages and dashed lines the extremes. (D) Sea Surface Temperature 4 (El Niño 4 Index). All time series start in January 2000 and end in December 2010. In the plots colors indicate the ENSO phase, for details refer to the inset legend in panel A.</p

Cross-wavelet coherence analysis.

<p>Coherence between (A) Cutaneous Leishmaniasis cases in the Republic of Panamá, Leish, and Sea Surface Temperature 4, a.k.a., El Niño 4 index, SST4 (B) Leish and Rainfall, Rain (C) Leish and Average Temperature, Temp (D) Rain and SST4 (E) Temp and SST4. A cross wavelet coherence scale is presented at the bottom of the figure, which goes from zero (blue) to one (red). Red regions in the plots indicate frequencies and times for which the two series share power (i.e., variability). The cone of influence (within which results are not influenced by the edges of the data) and the significant coherent time-frequency regions (p<0.05) are indicated by solid lines.</p