Effects of temperature on emergence and seasonality of West Nile virus in California - PubMed (original) (raw)

Comparative Study

Effects of temperature on emergence and seasonality of West Nile virus in California

David M Hartley et al. Am J Trop Med Hyg. 2012 May.

Abstract

Temperature has played a critical role in the spatiotemporal dynamics of West Nile virus transmission throughout California from its introduction in 2003 through establishment by 2009. We compared two novel mechanistic measures of transmission risk, the temperature-dependent ratio of virus extrinsic incubation period to the mosquito gonotrophic period (BT), and the fundamental reproductive ratio (R(0)) based on a mathematical model, to analyze spatiotemporal patterns of receptivity to viral amplification. Maps of BT and R(0) were created at 20-km scale and compared throughout California to seroconversions in sentinel chicken flocks at half-month intervals. Overall, estimates of BT and R(0) agreed with intensity of transmission measured by the frequency of sentinel chicken seroconversions. Mechanistic measures such as these are important for understanding how temperature affects the spatiotemporal dynamics of West Nile virus transmission and for delineating risk estimates useful to inform vector control agency intervention decisions and communicate outbreak potential.

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Figures

Figure 1.

Figure 1.

Schematic of the SEIR model constructed for West Nile virus circulation in California. Birds (B) are categorized as highly competent (1), moderately competent (2), or incompetent (3), and adult mosquitoes (M) may emerge from uninfected (P) or vertically infected (Q) eggs. See the text for a complete explanation.

Figure 2.

Figure 2.

Calculated fundamental reproductive ratio (R0) estimates during the period of WestNile virus (WNV) introduction and spread in California, 2003 (A) and 2004 (B). Green colors indicate R0 estimates below or above the threshold value of 1, with less intense colors indicating values greater than 1 (see scale). For comparison of R0 values with observed transmission patterns, sentinel chicken flocks are indicated by circles, with red or white circles representing flocks with or without serological evidence of WNV transmission during each half-month, respectively.

Figure 2.

Figure 2.

Calculated fundamental reproductive ratio (R0) estimates during the period of WestNile virus (WNV) introduction and spread in California, 2003 (A) and 2004 (B). Green colors indicate R0 estimates below or above the threshold value of 1, with less intense colors indicating values greater than 1 (see scale). For comparison of R0 values with observed transmission patterns, sentinel chicken flocks are indicated by circles, with red or white circles representing flocks with or without serological evidence of WNV transmission during each half-month, respectively.

Figure 3.

Figure 3.

Relationship between seroconversions in sentinel chickens and calculated values for fundamental reproductive ratio (R0) (A) and the temperature-dependent ratio of virus extrinsic incubation period to the mosquito gonotrophic period (BT) (B) during May–October 2003–2009. Graph shows means (height of gray bars) and 90th percentiles (total height of gray plus blue bars; if the blue bar is not visible, mean was > 90th percentile) for the percentage of chickens that seroconverted to West Nile virus in each agency over the range of R0 values calculated in this study.

Figure 4.

Figure 4.

R0 as a function of time (plotted in red) for representative mosquito control districts along the cool northern coast of California (Marin-Sonoma; bottom panel), in the warm Central Valley (Sacramento-Yolo; middle panel), and in the hot southeastern deserts (Coachella Valley; top panel). BT, the ratio of extrinsic incubation period to the gonotrophic period as a function of time, is plotted in black. Values of BT are shown only for periods when West Nile virus (WNV) amplification is theoretically possible (i.e., when temperatures were above the WNV replication threshold of 14.3°C). For comparison, sentinel chicken flocks are indicated along the x-axis by circles, with black and gray circles representing flocks with or without serologic evidence of WNV transmission, respectively. R0 = fundamental reproductive ratio.

Figure 5.

Figure 5.

A, Red = extrinsic incubation period (EIP); black = gonotrophic period (GP). B, Ratio of EIP to GP (ratio of extrinsic incubation period to the gonotrophic period as a function of time). In both panels, the red vertical line denotes 14.3°C, the replication threshold of West Nile virus.

Figure 6.

Figure 6.

BT, the ratio of extrinsic incubation period to gonotrophic period for West Nile virus (WNV) based on estimated mean mosquito exposure temperatures during 2004 as WNV spread northward across California. Hatched areas are below the estimated threshold for WNV replication in mosquitoes. Serologic evidence of WNV transmission to sentinel chickens is shown for comparison of extrinsic incubation periods with observed transmission patterns, with closed and open circles representing flocks with or without serologic evidence of WNV transmission during the half-month, respectively. N/A = not applicable.

Figure 7.

Figure 7.

Proportion of mosquitoes surviving the minimum number of gonotrophic cycles required for West Nile virus transmission (temperature-dependent ratio of virus extrinsic incubation period to the mosquito gonotrophic period [BT]) after infection for the estimated mosquito exposure temperatures in this study. Because survival decreases with increasing temperature (daily survival = 0.943 − 0.0092 × temperature), for each value of BT, the greatest proportionate survival occurs at the lower end of the temperature range.

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