Dynamic behavior of sylvatic yellow fever in Brazil (1954-2008).

INTRODUCTION
Sylvatic yellow fever (SYF) is enzootic in Brazil, causing periodic outbreaks in humans living near forest borders or in rural areas. In this study, the cycling patterns of this arbovirosis were analyzed.


METHODS
Spectral Fourier analysis was used to capture the periodicity patterns of SYF in time series.


RESULTS
SYF outbreaks have not increased in frequency, only in the number of cases. There are two dominant cycles in SYF outbreaks, a seven year cycle for the central-western region and a 14 year cycle for the northern region. Most of the variance was concentrated in the central-western region and dominated the entire endemic region.


CONCLUSIONS
The seven year cycle is predominant in the endemic region of the disease due the greater contribution of variance in the central-western region; however, it was possible identify a 14 cycle that governs SYF outbreaks in the northern region. No periodicities were identified for the remaining geographical regions.

Palavras-chaves: Febre amarela silvestre.Periodicidade.Análise espectral.Epidemiologia.VV Urban yellow fever has been eradicated in Brazil since 1942 1 ; however, the zoonotic form of this arbovirosis, sylvatic yellow fever (SYF), remains active in the forest regions and their borders, causing sporadic human cases and small outbreaks.The resurgence of the mosquito Aedes aegypti (Ae.aegypti) in Brazilian urban areas about 40 years ago 2 brought back dengue fever virus to Brazil 3 and has been an important matter of concern regarding the possibility of the re-urbanization of yellow fever in the country 1,4 .Historically, this mosquito has been the urban vector of YF virus in Brazil.
In the Brazilian rain forest, the yellow fever virus is maintained by the sylvatic mosquito vectors Haemagogus sp. and Sabethes sp., in a enzootic cycle involving primates 1 .Sporadic human cases of SYF have been reported since 1954, with a total of 964 cases between 1954 and 2008 5,6 and a mortality rate around 50%.The endemic region for SYF is composed by the northern and central-western regions and the State of Maranhão, in the northeastern region 7 , which forms about 68% of the Brazilian territory.Some states from the southeastern, northeastern (State of Bahia) and southern regions have reported sporadic cases imported from the endemic region.
In this paper, the periodic behavior of SYF in Brazil from 1954 to 2008 was analyzed.

Areas studied
Brazil is divided in 5 geographical regions: south, southeast, central-west, north and northeast.The southeastern region is the most populated (demographic density about 78 inhabitants/km 2 ) and the northern region is the least populated (about 3 inhabitants/km 2 ).The endemic area for SYF in Brazil comprises the northern and centralwestern regions and part of the State of Maranhão (northeastern region), corresponding to about 68% of Brazilian territory.A part of the State of Maranhão has ecological landscapes similar to the northern region.

Data
Sylvatic yellow fever annual case data was obtained from the National Health Foundation (Fundação Nacional de Saúde) 5 and the Secretariat of Health Surveillance of the Brazilian Ministry of Health (Secretaria de Vigilância em Saúde, Ministério da Saúde do Brasil) 6 .
Spectral Fourier analysis Normal data series and log transformed data series were analyzed using the Statistica 7.0 software package.Spectral analysis was performed after data was subtracted from the mean and detrended before analysis.Spectral analysis was performed by smoothing the series using the Hamming method (a weighted moving averages technique) to obtain the frequencies that significantly contribute to the cyclical behavior of the series.In order to improve the precision of analysis, window width was adjusted to sets of three data.for each geographical region of the country; the region was not represented because cases were rare and sporadic during this period.Analysis of Figure 1A confirmed that the number of SYF cases increased significantly after 1980 in the southeastern region (State of Minas Gerais) and northeastern region (States of Maranhão and Bahia); however, the difference between number of outbreaks before and after 1980 for these regions was not statistically significant.Analysis of Figure 1B revealed that the central-western and northern regions concentrated significantly more outbreaks than the southeastern and northeastern regions (Chi square, p= 0.015).Analysis of Figure 1C presents comparisons between SYF cases in the endemic region and in the entire country.Analysis confirmed that outbreaks in both areas are connected; however, an outbreak occurred in the southeastern region in 2003 that was apparently not connected to endemic cases.
Figure 2, on the left, shows the spectral densities for the central-western and northern regions.In Figure 2, on the right, the central-western region showed a dominant cycle of approximately 7 years, while the northern region displayed a dominant cycle of approximately 14 years, followed by a minor cycle of 3 years.The southwest and northeast showed no cyclic behavior, because outbreaks in these areas are sporadically and probably imported from the endemic region.

FIGURE 1 -
FIGURE 1 -(A) and (B) show the number of SYF cases in the southeastern/ northeastern regions and in the central-western/northern regions, respectively.(C) Number of SYF cases in the endemic region and in Brazil as a whole (all registered cases).Legends are shown in the figures.SYF: sylvatic yellow fever, SE: south eastern, NE: north eastern, MN: midwest region, NO: northern.

Figure 1
Figure1shows the time series for SYF cases from 1954 to 2008 for each geographical region of the country; the region was not represented because cases were rare and sporadic during