ENSO-driven climate variability promotes periodic major outbreaks of dengue in Venezuela.

Dengue is a mosquito-borne viral disease of global impact. In Venezuela, dengue has emerged as one of the most important public health problems of urban areas with frequent epidemics since 2001. The long-term pattern of this disease has involved not only a general upward trend in cases but also a dramatic increase in the size and frequency of epidemic outbreaks. By assuming that climate variability has a relevant influence on these changes in time, we quantified the periodicity of dengue incidence in time-series of data from two northern regions of Venezuela. Disease cycles of 1 and 3-4 years (p < 0.05) were detected. We determined that dengue cycles corresponded with local climate and the El Niño Southern Oscillation (ENSO) variation at both seasonal and inter-annual scales (every 2-3 years). Dengue incidence peaks were more prevalent during the warmer and dryer years of El Niño confirming that ENSO is a regional climatic driver of such long-term periodicity through local changes in temperature and rainfall. Our findings support the evidence of the effect of climate on dengue dynamics and advocate the incorporation of climate information in the surveillance and prediction of this arboviral disease in Venezuela.

Diurnal biting periodicity of parous Simulium (Diptera: Simuliidae) vectors in the onchocerciasis Amazonian focus.

We describe the hourly patterns of parous biting activity of the three main simuliid vectors of human onchocerciasis in the Amazonian focus straddling between Venezuela and Brazil, namely, Simulium guianense s.l. Wise; S. incrustatum Lutz, and S. oyapockense s.l. Floch and Abonnenc. Time series of the hourly numbers of host-seeking parous flies caught in five Yanomami villages during dry, rainy, and their transition periods from 1995 to 2001 were investigated using harmonic analysis (assuming an underlying circadian rhythm) and periodic correlation (based on Spearman's r). Parous S guianense s.l. showed a bimodal activity pattern, with a minor peak in mid-morning and a major peak at 16:00 h. S. incrustatum exhibited mainly unimodal activity during either early morning or midday according to locality. S. oyapockense s.l. bit humans throughout the day mainly between 10:00 and 16:00 h but also showed bimodal periodicity in some localities. Superimposed on the endogenous, species-specific daily cycles, parous activity showed variation according to locality, season, air temperature and relative humidity, with biting being promoted by warmer and drier hours during wet seasons/periods and reduced during hotter times in dry seasons or transitions. The results are discussed in terms of their implications for blackfly biology and ecology as well as onchocerciasis epidemiology and control.

Human onchocerciasis in the Amazonian area of southern Venezuela: spatial and temporal variations in biting and parity rates of black fly (Diptera: Simuliidae) vectors.

We investigated some entomological factors underlying altitudinal prevalence variation in the Venezuelan Amazonia human onchocerciasis focus. Spatial and temporal variation in relative abundance, daily biting rate, proportion of parous flies, and monthly parous biting rate were studied for the three main simuliid vectors (based on their vectorial competence: Simulium oyapockense s.l. Floch & Abonnenc approximately = S. incrustatum Lutz << S. guianense s.l. Wise). Yanomami villages were selected among sentinel communities of the ivermectin control program, representing hypo- to hyperendemicity conditions of infection. Spatial variation was explored via increasing village altitude on two river systems (A: Ocamo-Putaco and B: Orinoco-Orinoquito). Temporal variation was studied between 1995 and 1999 by sampling the biting population during dry and rainy mouths. Environmental variables included monthly rainfall and maximum river height. Simuliid species composition itself varied along the altitudinal and prevalence gradient. S. oyapockense s.l. prevailed below 150 m. Above this altitude and up to 240 m, S. incrustatum and S. guianense s.l. became more frequently and evenly collected along A but not along B, where S. incrustatum remained absent. The daily biting rate of S. oyapockense s.l. was higher during the dry season along A, whereas the converse took place along B. Daily biting rate of S. incrustatum was lowest during early rains. By contrast, the daily biting rate of S. guianense s.l. was highest during this period. There was a significant negative cross-correlation between proportion of parous of S. oyapockense s.l. and river height (2 and 3 mo lagged), whereas this variable (1 and 2 mo lagged) was positively correlated with the proportion of parous flies for S. incrustatum. Monthly parous biting rate values suggest that the months contributing most to onchocerciasis transmission in the area are likely to be the dry season and the transition periods between seasons.

Factors associated with distribution of Anopheles aquasalis and Anopheles oswaldoi (Diptera: Culicidae) in a malarious area, northeastern Venezuela.

Spatial and temporal abundance patterns of anopheline larvae and their relationships with wetland conditions were studied in an endemic malaria area in northeastern Venezuela, where Anopheles aquasalis Curry is the main vector. Larvae were sampled over a 2-yr period in 7 wetland types (brackish and freshwater herbaceous swamps, mangrove swamps, freshwater ponds, clear-cut marsh forests, small irrigation canals, and swamp forests), covering 3 environmental gradients (salinity, aquatic vegetation, and habitat permanence). Twelve variable were quantified to describe each habitat. Two species of anophelines were collected. An. aquasalis was the species with the widest distribution, and its highest abundance was in the seasonal brackish mangrove habitat during the rainy season. An. oswaldoi Peryassu was rarely encountered, but was mainly associated with the dry season and with the permanent fresh water wetlands (such as ponds). Principal components and correlation analyses revealed that the physicochemical (salinity, dissolved oxygen) variables of the wetland were associated most strongly with the spatial distribution of both species. Variations in salinity were strongly associated with the abundance of An. aquasalis. Both the occurrence and abundance of An. oswaldoi were most closely correlated with dissolved oxygen. Changes in seasonal abundance of both species were associated with rainfall. The relevance of these results to vector control in northern Venezuela is discussed.

Temporal and spatial patterns of malaria reinfection in northeastern Venezuela.

We stratified the risk of malaria transmission (Plasmodium vivax) in 35 villages along a coastal range in northeastern Venezuela (51 km2) where the main vector is the mosquito Anopheles aquasalis. After 20 years without local malaria transmission, reinfection of the entire area occurred from May to December 1985 by local (continuous) and jump (discontinuous) dispersal. Epidemiologic, environmental, and vector variables were investigated with the aid of a Geographic Information System. Risk factors for malaria transmission were human population density, proximity to pre-adult mosquito habitats (< 500 m), and the number of pre-adult habitats nearby. Most inhabitants, immature mosquito habitats, and malaria cases were located at low elevations and on gentle slopes. High prevalence of malaria during the dry seasons was associated with the presence of permanent bodies of water containing An. aquasalis. Occurrence of a La Niña event in 1988 (wet and cool phase of the El Niño Southern Oscillation) triggered malaria transmission to unusually high levels, consolidating infection in the area, and rendering traditional control efforts useless. We recommend tracking malaria persistence per village and associated risk factors as methods to reduce the cost of malaria control programs.

Onchocerciasis in the Amazonian focus of southern Venezuela: altitude and blackfly species composition as predictors of endemicity to select communities for ivermectin control programmes.

In preparation for an ivermectin distribution programme, the prevalence and intensity of infection due to Onchocerca volvulus as well as the species composition and abundance of Simulium vectors were investigated in 22 Yanomami communities situated along 2 altitudinal transects in the southern Venezuelan onchocerciasis focus. These transects corresponded to the Ocamo-Putaco and Orinoco-Orinoquito river systems, covering a range of elevation between 50 m and 740 m above sea level (asl). A total of 831 people underwent parasitological examination in this survey and an additional 196 patients from a previous study, at an altitude of 950 m, were included in the analysis. A total of 92,659 man-biting blackflies were collected and identified to morphospecies. S. oyapockense s.l. was the predominant simuliid up to 150 m asl, whereas S. guianense s.l. and S. incrustatum s.l. prevailed above 150 m. Communities located below 150 m were found to range from hypo- to mesoendemic; all villages above 150 m proved to be hyperendemic (> 60% microfilarial prevalence) and mass ivermectin treatment should be implemented. Age above 10-14 years, altitude of the village and biting rate of S. guianense s.l. up to 200 m asl were found to be statistically significant independent predictors of infection by multivariate logistic regression using a spline model. There were no differences in infection status according to sex. Above 200 m, microfilarial rate and density remained approximately constant, prevalence averaging 79% regardless of blackfly abundance. For the implementation of ivermectin-based onchocerciasis control programmes in the Amazonian focus, altitude and species composition of the blackfly population might be adopted as useful indicators aiding selection of the most affected communities. However, below 200 m additional parasitological indicators may also be necessary. As a direct result of this study, regular mass-ivermectin delivery to meso- and hyperendemic communities is now in progress.

Onchocerciasis hyperendemic in the Unturán mountains: an extension of the endemic region in southern Venezuela.

A new region with human onchocerciasis is reported in the Unturán mountains, South Venezuela, affecting Yanomamö populations not surveyed in previous studies conducted in the Venezuelan-Brazilian border area. Its distribution probably extends towards the Upper Toototobi endemic area in Brazil. The age-standardized prevalence of Onchocerca volvulus microfilariae (mf) (67%), the prevalence of infection in those aged > or = 20 years (86%), and the community microfilarial load (CMFL) (24 mf/mg), are consistent with hyperendemic transmission. Both prevalence and mean intensity increased monotonically with age without reaching a plateau, the highest values being recorded in the > or = 45 years age class (respectively, 95% and 42 [geometric mean of Williams] or 172 [arithmetic mean] mf/mg). The degree of parasite overdispersion (measured by the variance/mean ratio) also increased with host age. The CMFL value, the presence of sclerosing keratitis, hanging groin, and severe skin lesions, indicated that the infection poses an important public health problem in the region.

Simulium metallicum cytospecies E larval habitat characterization in the Altamira focus of onchocerciasis, northern Venezuela.

Simulium metallicum sibling species E was identified cytotaxonomically from an onchocerciasis focus at Altamira in northern Venezuela. S. metallicum E larvae were sampled monthly from two small mountain streams over a 15-month period (July 1990 to September 1991) and eleven habitat variables were measured at two altitudes. One stream consistently harboured much higher densities of S. metallicum E larvae than the other, with three annual peaks of abundance: during the dry season and at the beginning and end of the rainy season. These peak densities were correlated with high rainfall 4 months previously. Larvae were most abundant on submerged rocks and fallen leaves, in small shallow areas characterized by slow water current, high conductivity and sparse terrestrial vegetation cover. Stream variables which best explained the temporal changes in abundance were water discharge and conductivity. The population dynamics of S. metallicum E appeared to be influenced primarily by interactions between stream discharge and substrate stability. Relevance of these results to vector control with larvicides is discussed.

Vector competence of Simulium metallicum s.l. (Diptera: Simuliidae) in two endemic areas of human onchocerciasis in northern Venezuela.

Experimental infections of Simulium metallicum s.l. with Onchocerca volvulus were carried out in two onchocerciasis foci, Altamira and Trincheras, in northern Venezuela, to determine vector competence. Wild-caught flies, fed on infected volunteers, were maintained in the laboratory for 13-15 days at 27 degrees C. Parasite development was complete but asynchronous and retarded. No differences in the vector competence of the two populations of S. metallicum s.l. were found. However, a less efficient development of the parasite occurred during the dry season at both localities. The distribution of the parasite within the vector was aggregated and also displayed seasonal variation. The seasonal susceptibility may be a consequence of a density-dependence regulation mechanism of the parasite within the vector. These results indicate a relatively low vector competence for S. metallicum s.l. in northern Venezuela.