Disease transmission and the ecological context.
PhD thesis, University of Glasgow.
Full text available as:
Epidemiology strongly parallels the study of ecology, primarily being concerned
with the incidence, distribution, reproduction and persistence of species. The
spread of disease, or its transmission, is arguably the most important incident
studied in epidemiology, underpinning a pathogen’s ability to reproduce and
persist within a host population. However, observations of individual
transmission events are often impossible to observe directly, making variation in
this process difficult to study. This has resulted in a great deal of
epidemiological theory being based on homogenous transmission of disease
through host populations. Understanding disease transmission as a
heterogeneous process requires an appreciation of the ecological dynamics
determining a pathogens ability to transmit. In this thesis a cross-disciplinary
approach is taken to examine the ecological dynamics that may affect disease
transmission at different ecological scales.
In Chapter 2 I review empirical evidence in support of density dependent
transmission. Transmission rates of density dependent transmitted diseases are
often assumed to scale linearly with host population density. This assumption is
pertinent to the calculation of the basic reproductive number R0. As R0 is
important in determining optimal vaccination strategies, population thresholds
and epidemic sizes, incorrect assumptions used in its calculation have the
potential to misinform disease control strategies. Alarmingly, there is very little
evidence to suggest that the prior assumption of a linear relationship between
disease transmission rates and host population density exists. Where evidence of
density dependent transmission has been found this has been best explained by
non-linear relationships. Furthermore, density may have much stronger effects
on disease transmission at small, local, scales (for example within one social
grouping of hosts). Disease transmission between groups of hosts, at global
scales, is more likely to follow frequency dependent dynamics. Disease
transmission rates should thus be thought of as variable across populations that
are not homogenously distributed in space, or across social structures.
In Chapter 3 a community of pathogens infecting a population of rural red foxes,
Vulpes vulpes, is described. Foxes cadavers were collected from a private estate
in Canterbury, Kent and a combination of direct and indirect testing for disease
is used to maximise the scope of disease considered as part of this community.
Specifically, I examine if any of the diseases included in this study occur
together, or apart, more frequently than expected by chance alone. Within the
samples collected it is found that the intracellular protozoan Toxoplasma gondii
co-occurs with the virus canine adenovirus type-I (CAV-I) more frequently than
expected by chance. Foxes concomitantly infected with these pathogens have
lower condition scores than foxes who were not positive for both pathogens.
From the data collected it is not clear whether hosts of lower condition are
more susceptible to co-infection or if the co-infection is more harmful to hosts
than being singly infected. T. gondii is not transmitted by foxes, but if infection
with this parasite increases susceptibility to CAV-I then this virus may benefit
from the presence of T. gondii within its host population. If it is the case that
foxes of lower condition are simply more prone to co-infection then it should be
expected that individual differences between hosts would cause heterogeneity
in disease transmission. The need for cross-disciplinary approaches when
studying pathogen communities is well demonstrated by this study, as is the
need for more consideration to be paid to the community ecology of pathogens
in epidemiological studies.
In Chapter 4 a model is formulated to explore the effects of an interaction
between a micro and a macro parasite. This is performed in the context of the
increased prevalence and geographical range of the highly zoonotic small fox
tapeworm Echinococcus multilocularis following successful rabies elimination in
Western Europe. I explore the hypothesis that foxes with extremely high burdens
may be at a higher risk of contracting rabies than foxes with low worm burdens,
and thus rabies may have a regulatory effect on E. multilocularis populations by
preferentially removing “super spreading” hosts. It is demonstrated that rabies
limits E. multilocularis populations by limiting the density of available hosts. An
interaction between rabies transmission rate and worm burden only caused a
weak additional suppression on E. multilocularis populations, regardless of
whether this relationship was linear or exponential. The elimination of rabies
across Western Europe is certainly to be applauded. However, it should be noted
from this work that surveillance of pathogen communities following successful
eradication of one pathogen is of the upmost importance.
Finally, in Chapter 5 I examine how parasites adapt their investment in
transmission in response to environmental changes experienced within a host.
This is done by fitting models to data collected from mice infected with the
malaria parasite Plasmodium chabaudi during the acute stage of inaction.
Parasites are predicted to alter their behaviour in response to host stress,
immunity and the availability of resources. However, theoretical and
experimental studies reach conflicting conclusions regarding the “optimal
response” to degradation of their habitat. Models were fitted to time series data
from infection with one of six distinct genotypes. It is found that proportional
allocation of resources into transmission, rather than replication, is highly
sensitive to red blood cell (RBC) densities, with investment in transmission
increasing as RBC resources become scarce. Investment in transmission also
increases, albeit more weakly, in response to low parasite densities. These
analyses highlight the fact that the complexity of interactions between parasites
and their host hinder the identification of causal relationships, but supports
recent work that questions the role of terminal investment in transmission in
response to changes in the within-host environment.
The broad scope of work presented here investigates a wide range of ecological
factors (including community dynamics, habitat variability and reproductive
success) at different ecological scales, responsible for heterogeneity in disease
transmission. Transmission is a dynamic, and heterogeneous process. To better
understand the ecology of disease it is logical to investigate the mechanisms
behind this variation.
Actions (login required)