Human population movement can impede the elimination of soil-transmitted helminth transmission in regions with heterogeneity in mass drug administration coverage and transmission potential between villages: a metapopulation analysis

Abstract

Background: Soil-transmitted helminth (STH) infections affect predominantly socio-economically disadvantaged populations in sub-Saharan Africa, East Asia and the Americas. Previous mathematical modelling studies have evaluated optimal intervention strategies to break STH transmission in clusters of villages. These studies assumed that villages are closed independent units with no movement of people in or out of communities. Here we examine how human population movement, for example, of seasonal migrant labourers, affect the outcome of mass drug administration (MDA) programmes.

Results: We used a stochastic individual-based metapopulation model to analyse the impact of human population movement at varying rates on STH elimination efforts. Specifically, we looked at seasonal clumped movement events of infected individuals into a village. We showed that even if on average 75% of the entire resident population within a village are treated, an annual rate of 2-3% of the population arriving from an untreated source village can reduce the probability of STH elimination to less than 50% in high-prevalence settings. If a village is infection-free, an annual movement rate of 2-3% from an infected source village imposes a risk of re-introduction of STH of 75% or higher, unless the prevalence in the source village is less than 20%. Even a single arrival of 2-3% of the population can impose a risk of re-introducing STH of 50% or greater depending on the prevalence in the source village. The risk of re-introduction also depends on both the age group of moving individuals and STH species, since the pattern of cross-sectional age-prevalence and age-intensity profiles of infection in the human host are species-specific.

Conclusions: Planning for STH elimination programmes should account for human mobility patterns in defined regions. We recommend that individuals arriving from areas with ongoing STH transmission should receive preventive chemotherapy for STHs. This can most easily be implemented if migration is seasonal and overlaps with treatment rounds, e.g. seasonal migrant labour. Moreover, transmission hotspots in or near treatment clusters should be eliminated, for example, by implementing appropriate water, sanitation and hygiene (WASH) measures and targeting treatment to individuals living in hotspots.

Keywords: Elimination of transmission; Human population movement; Soil-transmitted helminths.

Fig. 1

Probability of transmission resuming after an isolated movement event depending on the percentage of the population moving from a source village to an infection-free village and the STH prevalence in the source village. The probability estimate is based on the percentage of simulations out of 300 iterations in which the STH prevalence in the previously infection-free village reaches at least half of the equilibrium prevalence, given the transmission intensity and parasite aggregation in the source village. The solid line is the mean of ten sets of 300 iterative simulation runs. The shaded area is one standard deviation above and below the mean value. a, b Individuals moving from the source village are young adults (15–35 years). c, d Individuals moving from the source village are children (< 15 years-old). a, c Results for A. lumbricoides. b, d Results for hookworm. Population size per village n = 500. Prevalence levels: low: < 20%; medium: 25–30%; high 60–70%

Fig. 2

Probability of transmission resuming during twenty years of regular, seasonal movement. The probability of transmission resuming depends on the percentage of the population moving between villages and the STH prevalence in the source village. The probability estimate is based on the percentage of simulations out of 300 iterations in which the STH prevalence in the previously infection-free village reaches at least half of the equilibrium prevalence during the twenty-year observational period, given the transmission intensity and parasite aggregation in the source village. The solid line is the mean of ten sets of 300 iterative simulation runs. The shaded area is one standard deviation above and below the mean value. a, b Individuals moving between villages are young adults (15–35 years-old). c, d Individuals moving between villages are children (< 15 years-old). a, c Results for A. lumbricoides. b, d Results for hookworm. Population size per village n = 500. Prevalence levels: low: < 20%; medium: 25–30%; high 60–70%

Fig. 3

Probability of elimination determined two years after cessation of a five-year MDA programme dependent on annual movement rate during and after MDA. The probability of elimination depends on the percentage of the population moving between villages and the STH prevalence in the source village. The probability estimate is based on the percentage of simulations out of 300 iterations in which the STH prevalence in the treated village is beneath a previously determined threshold value that predicts with 95% probability whether the transmission breakpoint has been reached or not (20% for A. lumbricoides, 9% for hookworm). The solid line is the mean of ten sets of 300 iterative simulation runs. The shaded area is one standard deviation above and below the mean value. a, b The whole community receives MDA once a year with 75% coverage across all age groups. c, d The whole community receives MDA twice a year with 75% coverage across all age groups. a, c Results for A. lumbricoides. b, d Results for hookworm. Population size per village n = 500. Prevalence levels: low: < 20%; medium: 25–30%; high 60–70%

Fig. 4

Probability of elimination determined fifteen years after cessation of a five-year MDA programme dependent on annual movement rate during and after MDA. The probability of elimination depends on the percentage of the population moving between villages and the STH prevalence in the source village. The probability estimate is based on the percentage of simulations out of 300 iterations in which STH infections have gone extinct in the treated village. The solid line is the mean of ten sets of 300 iterative simulation runs. The shaded area is one standard deviation above and below the mean value. a, b The whole community receives MDA once a year with 75% coverage across all age groups. c, d The whole community receives MDA twice a year with 75% coverage across all age groups. a, c Results for A. lumbricoides. b, d Results for hookworm. Population size per village n = 500. Prevalence levels: low: < 20%; medium: 25–30%; high 60–70%