Rural-urban gradient in seasonal forcing of measles transmission in Niger

Abstract

Seasonally driven cycles of incidence have been consistently observed for a range of directly transmitted pathogens. Though frequently observed, the mechanism of seasonality for directly transmitted human pathogens is rarely well understood. Despite significant annual variation in magnitude, measles outbreaks in Niger consistently begin in the dry season and decline at the onset of the seasonal rains. We estimate the seasonal fluctuation in measles transmission rates for the 38 districts and urban centres of Niger, from 11 years of weekly incidence reports. We show that transmission rates are consistently in anti-phase to the rainfall patterns across the country. The strength of the seasonal forcing of transmission is not correlated with the latitudinal rainfall gradient, as would be expected if transmission rates were determined purely by environmental conditions. Rather, seasonal forcing is correlated with the population size, with larger seasonal fluctuation in more populous, urban areas. This pattern is consistent with seasonal variation in human density and contact rates due to agricultural cycles. The stronger seasonality in large cities drives deep inter-epidemic troughs and results in frequent local extinction of measles, which contrasts starkly to the conventional observation that large cities, by virtue of their size, act as reservoirs of measles.

Figure 1.

(a) Weekly reported cases for all of Niger from 1995–2005. (b) The mean number of monthly cases in Niger over 1995–2005 (blue) compared with the mean monthly rainfall in Niamey (red). Shaded regions give ±2 s.e. (c) Logarithm of weekly reported measles incidence for all 35 districts and 3 urban centres over the time period 1995–2005. Each row of the matrix indicates one location. Weeks with 0 reported cases are shown in grey. Locations are grouped into the western arrondissements surrounding the city of Niamey, the southern arrondissements surrounding the city of Maradi, and the sparsely populated northern and eastern arrondissements (see map in figure 2).

Figure 2.

(a) Estimated seasonal forcing of measles transmission rate (10× for display) for (a) the 11 districts and the city of Niamey corresponding to the red shaded area in (d), (b) the 18 districts and the cities of Maradi and Zinder shown in the green area in (d) and (c) the six districts shown in blue in (d). (d) Map of the departments and urban centres of Niger with the estimated range of the seasonal forcing (10× for display) shown for each.

Figure 3.

(a) Estimated variance of seasonal forcing for the 38 departments and urban centres as function of mean annual rainfall during the period 2003–2006. Colours indicate the three regions (see map in figure 2). Solid lines are the regression fit for each region. Urban centres are shown as solid points. The department of Magaria, which is a strong outlier and was excluded from the analysis, is indicated. (b) Estimated variance of seasonal forcing for the 38 departments and urban centres as function of district population size (colours and lines are as in a).

Figure 4.

Probability of measles fade-out as a function of population size and the amplitude of seasonal forcing. (a) The percentage of years (out 50) with two consecutive two-week intervals with 0 measles incidence for a model with sinusoidal seasonal forcing. The grey dashed box indicates the approximate parameter range for (b). (b) The same as (a) using estimated seasonal forcing for the 38 districts of Niger. Black dots indicate the population size and amplitude of seasonal forcing for the districts of Niger. (Red, more than 50%; orange, between 10% and 50%; yellow, between 0% and 10%; white, no fade-outs).

Figure 5.

The proportion of years with fade-outs for the 38 districts of Niger (grey dots). The two districts that had fadeouts every year are shown in black. Curves are the best-fit quadratic function with (solid) and without (dashed) Niamey included.