Epidemiological consequences of immune sensitisation by pre-exposure to vector saliva

PLoS Negl Trop Dis. 2017 Oct 9;11(10):e0005956. doi: 10.1371/journal.pntd.0005956. eCollection 2017 Oct.

Abstract

Blood-feeding arthropods-like mosquitoes, sand flies, and ticks-transmit many diseases that impose serious public health and economic burdens. When a blood-feeding arthropod bites a mammal, it injects saliva containing immunogenic compounds that facilitate feeding. Evidence from Leishmania, Plasmodium and arboviral infections suggests that the immune responses elicited by pre-exposure to arthropod saliva can alter disease progression if the host later becomes infected. Such pre-sensitisation of host immunity has been reported to both exacerbate and limit infection symptoms, depending on the system in question, with potential implications for recovery. To explore if and how immune pre-sensitisation alters the effects of vector control, we develop a general model of vector-borne disease. We show that the abundance of pre-sensitised infected hosts should increase when control efforts moderately increase vector mortality rates. If immune pre-sensitisation leads to more rapid clearance of infection, increasing vector mortality rates may achieve greater than expected disease control. However, when immune pre-sensitisation prolongs the duration of infection, e.g., through mildly symptomatic cases for which treatment is unlikely to be sought, vector control can actually increase the total number of infected hosts. The rising infections may go unnoticed unless active surveillance methods are used to detect such sub-clinical individuals, who could provide long-lasting reservoirs for transmission and suffer long-term health consequences of those sub-clinical infections. Sensitivity analysis suggests that these negative consequences could be mitigated through integrated vector management. While the effect of saliva pre-exposure on acute symptoms is well-studied for leishmaniasis, the immunological and clinical consequences are largely uncharted for other vector-parasite-host combinations. We find a large range of plausible epidemiological outcomes, positive and negative for public health, underscoring the need to quantify how immune pre-sensitisation modulates recovery and transmission rates in vector-borne diseases.

MeSH terms

  • Animals
  • Arthropod Vectors / immunology*
  • Culicidae / immunology
  • Host-Parasite Interactions / immunology
  • Humans
  • Immune Tolerance
  • Insect Bites and Stings / immunology
  • Models, Biological*
  • Psychodidae / immunology
  • Saliva / immunology*
  • Ticks / immunology

Grants and funding

NM and MAG are supported by the Natural Science and Engineering Research Council of Canada (Discovery Grant 436171: nserc-crsng.gc.ca) and the Human Frontier Science Program (RGP0046/2013: hfsp.org). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.