Density-dependent processes in the transmission of human onchocerciasis: relationship between microfilarial intake and mortality of the simuliid vector

Abstract

In order to construct an analytical model of onchocerciasis transmission, it is necessary to elucidate the functional relationships of the various population rate processes taking place within the human and vector hosts. Two previous papers have explored the evidence for density-dependent regulation in relation to microfilarial intake by, and larval development within, the Simulium host. This paper investigates the survivorship of wild-caught blackfly samples fed on subjects with different intensities of Onchocerca volvulus microfilarial infection. Analyses were based on data for Guatemalan S. ochraceum s.l. (possessing a well-developed cibarial armature), West African S. damnosum s.l. (forest species), and South Venezuelan S. guianense (the latter two lacking a toothed cibarium). The mean survival times of samples of the 3 species, kept under laboratory conditions, decreased as parasite intake increased, the rate of mortality being dependent on the fly's age (measured as time post-feeding) and on the worm load acquired. An empirical, time-dependent hazard function was fitted to observed death rates/fly/day which rose very shortly after engorgement, declined subsequently, and rose again throughout the extrinsic incubation period of the parasite. The parameters of this hazard model were all positively correlated with the density of microfilariae in the bloodmeal. Expressions of survivorship and life-expectancy as explicit functions of time post-feeding and mean parasite intake were derived. The average expectation of life at engorgement for uninfected flies in the laboratory was estimated to be around 1 week for both, armed and unarmed blackflies. Residual life-expectancy decreased with time post-feeding and microfilarial load in both categories of vectors. This decline (resulting from age- and parasite-dependent mortality rates) was much more pronounced in those species lacking a toothed fore-gut. Whilst a fraction of heavily infected S. ochraceum was able to survive the latent period of the parasite, being therefore potentially capable of transmitting the infection, equivalent worm loads in S. guianense resulted in a drastic reduction of the expectation of infective life. These results provide additional evidence to support the hypothesis that, in the case of intrinsically susceptible vectors, unarmed simuliids are more efficient at low microfilarial loads, when the transmission rate from human to vector host is higher, and parasite-induced fly mortality is negligible. The opposite takes place in armed flies, which perform poorly at low parasite burdens and better at heavier loads, with little parasite-induced vector death.

The Population Biology and Transmission Dynamics of Loa loa

“…Fitting a piecewise exponential hazard function to the data highlights that much of the excess mortality arises from the ingestion of high numbers of microfilariae, occurring within the first 2-3 days following a bloodmeal ( Figure 3C). This is similar to observations on excess mortality in blackflies ingesting O. volvulus microfilariae [54]. This conclusion is further supported by less formal evidence from other studies suggesting that infection with the parasite, and the intensity of the infection, both influence vector mortality [41,55].…”

“…The main differentiating feature between the two curves occurs in the first 2 days, where flies feeding on humans with a high microfilarial concentration had greater mortality than flies feeding on humans with low concentrations. This is in keeping with observations on Simulium species of blackfly vectors of Onchocerca volvulus, in which ingestion of high microfilarial loads by the fly is associated with substantial excess mortality [54]. Motivated by this, a piecewise exponential model was fitted to the data (panel B), with different (constant) hazards over the initial 3 days but the same thereafter.…”

“…The emergence of larvae from the head causes great irritation to the fly, eliciting proboscis 'milking' actions associated with stress, and damage to the labio[ 2 9 6 _ T D $ D I F F ] -hypopharyngeal membrane and musculature [54]. Indeed, whilst it has been shown experimentally that flies can remain infective for up to 5 days following the first L3 larval emergence, with infective larvae emerging each time a bloodmeal is taken over that period, the vast majority of flies die within 24 h of taking a bloodmeal in which L3 larvae emerge [16].…”

Transmission intensity and the patterns of Onchocerca volvulus infection in human communities.

“…A species with a well-developed armature (which seems to have evolved for reasons other than selection pressures imposed by filarial parasites), 72 damages an important proportion of ingested mf. Such a species is, therefore, less likely to be affected by parasite-induced mortality 4 or decreased fecundity, 73 two components of lifetime fitness. Consequently, this species may have been subjected to lesser evolutionary pressures to evolve effective immune or apoptotic mechanisms against filarial larvae of the kind described for S. damnosum 74 (an 'unarmed' simuliid).…”

“…In an attempt to further understanding of such processes, a number of researchers have explored the properties of simple and complex mathematical models of the transmission dynamics of human onchocerciasis. 1 Considerable progress has been made concerning the regulatory constraints operating within the vector, [2][3][4][5][6] with some progress being recently made in investigating those acting within the human host. 7,8 A previous mathematical model 9 used an empirical relationship between the observed mean microfilarial (mf) load per milligram of skin per person in the community and the intensity of transmission in such a community, measured by the annual transmission potential (ATP).…”