Emergence and prevalence of human vector-borne diseases in sink vector populations

Abstract

Vector-borne diseases represent a major public health concern in most tropical and subtropical areas, and an emerging threat for more developed countries. Our understanding of the ecology, evolution and control of these diseases relies predominantly on theory and data on pathogen transmission in large self-sustaining 'source' populations of vectors representative of highly endemic areas. However, there are numerous places where environmental conditions are less favourable to vector populations, but where immigration allows them to persist. We built an epidemiological model to investigate the dynamics of six major human vector borne-diseases in such non self-sustaining 'sink' vector populations. The model was parameterized through a review of the literature, and we performed extensive sensitivity analysis to look at the emergence and prevalence of the pathogen that could be encountered in these populations. Despite the low vector abundance in typical sink populations, all six human diseases were able to spread in 15-55% of cases after accidental introduction. The rate of spread was much more strongly influenced by vector longevity, immigration and feeding rates, than by transmission and virulence of the pathogen. Prevalence in humans remained lower than 5% for dengue, leishmaniasis and Japanese encephalitis, but substantially higher for diseases with longer duration of infection; malaria and the American and African trypanosomiasis. Vector-related parameters were again the key factors, although their influence was lower than on pathogen emergence. Our results emphasize the need for ecology and evolution to be thought in the context of metapopulations made of a mosaic of sink and source habitats, and to design vector control program not only targeting areas of high vector density, but working at a larger spatial scale.

Figure 1. Distribution of the pathogen’s basic reproduction number (R₀) for each of the six vector-borne diseases considered.

(A) Diseases with only human hosts: human African trypanosomiasis (HAT), dengue (DEN) and malaria (MAL). (B) Diseases with non-human hosts: Chagas disease (CD), Japanese encephalitis (JE), and visceral leishmaniasis (VL). Distributions were obtained from 10,000 simulations for each disease.

Figure 2. Sensitivity of the basic reproduction number (R₀) to vector’s demography and feeding rates, and to pathogen’s transmissibility and virulence.

All six vector-borne diseases appear on the same graph. Squares correspond to diseases with only human hosts: human African trypanosomiasis (HAT), dengue (DEN) and malaria (MAL). Circles correspond to diseases with non-human hosts: Chagas disease (CD), Japanese encephalitis (JE), and visceral leishmaniasis (VL). Larger symbols correspond to the key determinants of the variations of R₀ (see main text for comments). Sensitivities were calculated from 10,000 simulations for each disease.

Figure 3. Distribution of the prevalence of infectious and recovered humans when no immigrant vector is infectious ().

Black and grey bars give the prevalence of infectious () and recovered () humans, respectively. Numbers above bars give (if any) the percentage of simulations leading to prevalence larger than 5%. Distributions were obtained from 10,000 simulations for each disease.

Figure 4. Distribution of the prevalence of infected and recovered humans when some immigrant vectors are infectious ().

Black and grey bars give the prevalence of infectious () and recovered () humans, respectively. Numbers above bars give (if any) the percentage of simulations leading to prevalence larger than 5%. Distributions were obtained from 10,000 simulations for each disease.

Figure 5. Sensitivity of the prevalence of infectious () and ‘recovered’ () humans to vector’s demography and feeding rates, and to the pathogen’s transmission and within-host dynamics.

(A) No immigrant vector is infectious (). (B) Some immigrant vectors are infectious (). All six vector-borne diseases appear on each of the two graphs. Squares and diamonds correspond to the prevalence of infectious and recovered humans, respectively, for diseases with only human hosts: human African trypanosomiasis (HAT), dengue (DEN) and malaria (MAL). Circles and triangles correspond to the prevalence of infectious and recovered humans, respectively, for diseases with non-human hosts: Chagas disease (CD), Japanese encephalitis (JE), and visceral leishmaniasis (VL). Larger symbols correspond to the key determinants of the variations of prevalence in humans (see main text for comments). Sensitivities were calculated from 10,000 simulations for each disease.