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S E Randolph

Publications and source records attributed to S E Randolph.

At least 37 records · Page 2Linked to original sources

Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England.

The genetic diversity of Borrelia burgdorferi sensu lato was assessed in a focus of Lyme borreliosis in southern Britain dominated by game birds. Ticks, rodents, and pheasants were analyzed for spirochete infections by PCR-targeting the 23S-5S rRNA genes, followed by genotyping by the reverse line blot method. In questing Ixodes ricinus ticks, three genospecies of B. burgdorferi sensu lato were detected, with the highest prevalences found for Borrelia garinii and Borrelia valaisiana. B. burgdorferi sensu stricto was rare (< 1%) in all tick stages. Borrelia afzelia was not detected in any of the samples. More than 50% of engorged nymphs collected from pheasants were infected with borreliae, mainly B. garinii and/or B. valaisiana. Although 19% of the rodents harbored B. burgdorferi sensu stricto and/or B. garinii in internal organs, only B. burgdorferi sensu stricto was transmitted to xenodiagnostic tick larvae (it was transmitted to 1% of the larvae). The data indicate that different genospecies of B. burgdorferi sensu lato can be maintained in nature by distinct transmission cycles involving the same vector tick species but different vertebrate host species. Wildlife management may have an influence on the relative risk of different clinical forms of Lyme borreliosis.

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Serum complement sensitivity as a key factor in Lyme disease ecology.

The sensitivity of Borrelia burgdorferi sensu lato to animal sera was analyzed. Complement-mediated borreliacidal effects were observed with particular combinations of host serum and Borrelia genospecies. The species-specific pattern of viability and/or lysis is highly consistent with the pattern of reservoir competence of hosts for B. burgdorferi sensu lato, suggesting a key role of complement in the global ecology of Lyme borreliosis.

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A generic population model for the African tick Rhipicephalus appendiculatus.

We present a simulation population model for the African tick Rhipicephalus appendiculatus, based on previous analyses of the mortality factors most closely correlated with observed population changes at 11 sites in equatorial and South Africa. The model incorporates temperature-dependent rates of egg production and development, climate-driven density-independent mortality rates, particularly during the adult-larval stage, and density-dependent regulation of both nymphs and adults. Diapause is also included for tick populations in southern Africa. The model successfully describes both the seasonality and annual range of variation in numbers of each tick stage observed at each of 4 test sites in Uganda, Burundi and South Africa. Sensitivity analysis showed that the final version of the model is robust to 4-fold variation in most parameter values (that were per force based on informed guesses), but is more sensitive to the regression coefficients determining density-dependent interstadial mortality (that were derived from analysis of field data). The model is able to predict the seasonality of ticks from a site in Kenya where a full prior population analysis was not possible because only adults and nymphs had been counted. The model is potentially applicable to other species of ticks, both tropical and temperate, to predict tick abundance and seasonality as risk factors for tick-borne diseases.

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Natural Lyme disease cycles maintained via sheep by co-feeding ticks.

We present observational and experimental evidence that cycles of the Lyme disease spirochaete, Borrelia burgdorferi s.l., can be maintained by sheep in the virtual absence of alternative hosts. A 2-year field study in upland moorland habitats of northwest UK established that sheep feed up to 80% of larval, > 99% of nymphal and all of the adult female tick (Ixodes ricinus) population. Infection prevalence of B. burgdorferi in questing ticks reaches over 20%, but amplification of infection occurs principally as nymphs (20- to 30-fold), rather than larvae (4- to 7-fold), feed on sheep, and transmission from sheep to ticks occurred only during peak tick abundance in May and September. Experimental transmission studies confirmed that sheep, previously exposed to infected ticks on the moorland site, do not support systemic infections of B. burgdorferi, but they can transmit localized infections from infected to uninfected ticks co-feeding at the same site on the sheep's body.

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Abiotic and biotic determinants of the seasonal dynamics of the tick Rhipicephalus appendiculatus in South Africa.

The creation of a generic population model for the tick Rhipicephalus appendiculatus requires a detailed, quantified understanding of the interactions of these ticks with their biotic and abiotic environment in the different parts of their range, from the tropical regions of East Africa to the temperate regions of South Africa. The much greater seasonal variation in climatic conditions, particularly temperature, further from the equator introduces variable development rates and diapause into the life cycle. Estimates of natural temperature-dependent interstadial development periods, derived from a combination of published laboratory and field data, were applied to published data on the seasonal abundance of R.appendiculatus on three farms in the Eastern Cape Province of South Africa. This enabled an assessment of which ticks of one stage give rise to which ticks of the next stage, from which (a) the onset and duration of diapause in unfed adults, and (b) seasonal interstadial mortality indices in the form of k-values, could be estimated. The contribution of biotic (tick density) and abiotic (climatic) factors as predictors of mortality at each life stage was investigated by step-wise multiple regression. Density-independent mortality at the female-to-larval stage is correlated with geographically variable climatic factors, minimum temperature at two farms and minimum relative humidity at the third. The other two stages are governed by density-dependent mortality, which, it is argued, may be caused largely by the hosts' acquired resistance to ticks. As expected on theoretical grounds, this density dependence is weaker nearer to the edge of the tick's range and for the more vulnerable immature stages.

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Role of grey squirrels and pheasants in the transmission of Borrelia burgdorferi sensu lato, the Lyme disease spirochaete, in the U.K.

In Britain, grey squirrels (Sciurus carolinensis Gmelin) and pheasants (Phasianus colchicus Linnaeus) are important hosts of larvae and nymphs of Ixodes ricinus L., the principal European vector of the Lyme disease spirochaete, Borrelia burgdorferi sensu lato. To test whether squirrels are competent hosts of B. burgdorferi s.l., three females were trapped in the wild and then held in captivity. Following treatment, each animal was exposed to uninfected xenodiagnostic I. ricinus ticks. Squirrel A (an adult) which was inoculated experimentally with B. burgdorferi s.l., transmitted the infection to xenodiagnostic ticks. In contrast, squirrel B (a juvenile that was not inoculated)-showed no evidence of infection. Xenodiagnostic ticks that fed on control squirrel C (an adult) became infected and subsequently transmitted the infection experimentally to an uninfected hamster. The results indicated that squirrel C had a disseminated infection acquired in the wild and which persisted for at least 11 weeks. These data clearly demonstrate that grey squirrels are amplifying and reservoir hosts of B. burgdorferi s.l. The strain associated with squirrels was related to the B. afzelii genotype. Two observations implicated pheasants in a similar role: (i) a high prevalence of infection in engorged larvae collected from trapped pheasants, and (ii) the detection of B. burgdorferi s.l. (B. garinii genotype) in the wattle of 1/10 pheasants using PCR. Xenodiagnostic experiments similar to those undertaken with the squirrels are needed to confirm the role of pheasants in the transmission cycle of Lyme disease spirochaetes.

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Co-feeding ticks: Epidemiological significance for tick-borne pathogen transmission.

Until recently, the transmission of tick-borne pathogens via vertebrates was thought to depend on the development of a systemic infection in the vertebrate hosts. Pathogen transmission has now been shown to occur between infected and uninfected ticks co-feeding in time or space in the absence of a systemic infection, originally for viruses, but now also for bacteria. The epidemiological consequences of this new non-systemic transmission pathway necessitate a major reassessment of the components and dynamics of tick-borne pathogen enzootic cycles. Here Sarah Randolph, Lise Gern and Pat Nuttall show that a much wider range of natural hosts than was previously recognized may contribute significantly to the transmission of tick-borne diseases, and compare quantitatively the relative contributions made by the systemic and non-systemic transmission pathways.

Journal Article↗

Quantifying parameters in the transmission of Babesia microti by the tick Ixodes trianguliceps amongst voles (Clethrionomys glareolus).

The estimation of two parameters in the transmission of Babesia microti by the tick Ixodes trianguliceps amongst small mammals, (1) the duration of infectivity in natural hosts and (2) the probability of transmission from an infected to a susceptible vole, is described. When B. microti was maintained by direct tick transmission, the probability of a complete cycle of transmission via the larval-nymphal and nymphal-adult transstadial routes was 1.0 and 0.71 respectively, but only if the larvae or nymphs had engorged, as distinct from feeding slowly, while the source parasitaemia exceeded 2 or 0.2% respectively, but had not yet passed the peak level. The duration of this condition for infectivity in voles infected by nymphal bites was only 1-4 days, whilst infections delivered by adult ticks barely reached the threshold level necessary for successful transmission. When syringe passage was introduced into the parasite maintenance schedule (a) the probability of transmission declined markedly and (b) the time-course of the parasitaemia was altered. If these parameter values are put into a simple model, together with field data on tick and host survival rates, it becomes apparent that additional factors, such as the highly aggregated distribution of ticks on their hosts, must account for the maintenance of B. microti at the levels seen in wild small mammal populations.

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General framework for comparative quantitative studies on transmission of tick-borne diseases using Lyme borreliosis in Europe as an example.

Models of tick-borne diseases must take account of the particular biological features of ticks that contrast with those of insect vectors. A general framework is proposed that identifies the parameters of the transmission dynamics of tick-borne diseases to allow a quantitative assessment of the relative contributions of different host species and alternative transmission routes to the basic reproductive number, Ro, of such diseases. Taking the particular case of the transmission of the Lyme borreliosis spirochaete, Borrelia burgdorferi, by Ixodes ticks in Europe, and using the best, albeit still inadequate, estimates of the parameter values and a set of empirical data from Thetford Forest, England, we show that squirrels and the transovarial transmission route make quantitatively very significant contributions to Ro. This approach highlights the urgent need for more robust estimates of certain crucial parameter values, particularly the coefficients of transmission between ticks and vertebrates, before we can progress to full models that incorporate seasonality and heterogeneity among host populations for the natural dynamics of transmission of borreliosis and other tick-borne diseases.

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Seasonal variation in the role of grey squirrels as hosts of Ixodes ricinus, the tick vector of the Lyme disease spirochaete, in a British woodland.

Data are presented on the variable patterns of the seasonal dynamics of Ixodes ricinus L. ticks seen questing on the vegetation and feeding on small rodents (mice and voles) and squirrels within a British woodland focus of Lyme borreliosis. Information on tick infestation levels on pheasants is also presented. The results show a prolonged, unimodal pattern of tick activity, with ticks feeding throughout the year in this sheltered habitat. If host density is taken into account, squirrels are quantitatively more important than small mammals as hosts for larval ticks from April until July, and overwhelmingly so for nymphal ticks throughout the year. The observed inter- and intraspecific differences in tick infestation levels are related to the behaviour of both hosts and ticks. Squirrels, as competent hosts for Borrelia burgdorferi and frequent occupants of habitats closely associated with man, will contribute significantly to the risk of Lyme disease.

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Nearly right or precisely wrong? Natural versus laboratory studies of vector-borne diseases.

Recent studies that compare experimental vector-borne disease systems incorporating elements of natural pathogen-vector-host interactions with model systems using unnatural associations have highlighted quantitative, and even qualitative, differences in the results. Here, Sarah Randolph and Pat Nuttall argue that the use of mathematical models to explore epidemiological processes and patterns depends on accurate parameter values obtained from natural systems.

Journal Article↗

Density-dependent acquired resistance to ticks in natural hosts, independent of concurrent infection with Babesia microti.

The question of whether the known immunosuppressive effects of Babesia microti may disrupt the development of acquired resistance to its tick vector, Ixodes trianguliceps, in natural rodent hosts (Clethrionomys glareolus), and thus enhance the disease transmission potential, is addressed experimentally. The results show for the first time that natural hosts can acquire resistance to ticks; that this acquired resistance is manifested chiefly by a strongly density-dependent reduction in the percentage of attached larvae that engorge; that the density dependence is quantitatively similar whether the host receives occasional large tick challenges or frequent low infestations; but that infection with B. microti does not disrupt this pattern of acquired resistance. Of two important natural host species, Apodemus sylvaticus can support repeated infestations of I. trianguliceps, but is a poor host to B. microti, while C. glareolus develops acquired resistance to the tick vector, but supports much higher-level, longer-lasting B. microti infections.

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Population dynamics and density-dependent seasonal mortality indices of the tick Rhipicephalus appendiculatus in eastern and southern Africa.

Eight sets of previously published data on the seasonal abundance of the tick Rhipicephalus appendiculatus in Burundi, Uganda, Tanzania and Zimbabwe are analysed to yield seasonal mortality indices. Correlations between these indices and abiotic (climatic) and biotic (tick density) variables suggest that it is the stage from females to larvae that is most sensitive to adverse abiotic conditions, specifically low moisture availability. Mortality at the other stages of the tick's life cycle is strongly density-dependent. The precise nature of this density-dependence suggests that it may be caused by acquired resistance to ticks by cattle. Robust correlations between satellite-derived vegetation indices, climatic factors and mortality indices suggest that detailed climatic data, often unavailable, may be replaced by satellite data, now widely available, for use in modelling tick populations.

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Distribution of tsetse and ticks in Africa: past, present and future.

The current concern over the effects of global warming has rekindled interest in the neglected topic of vector distribution. In order to predict the future, however, we must first comprehend the past and present. In this review, David Rogers and Sarah Randolph discuss the alternative biological and statistical approaches to understanding the present-day distributions of vectors, and make predictions about how these might change with global warming.

Journal Article↗

Climate, satellite imagery and the seasonal abundance of the tick Rhipicephalus appendiculatus in southern Africa: a new perspective.

Recent predictive models for the distribution of the African tick Rhipicephalus appendiculatus Neumann, based on the computer packages CLIMEX and BIOCLIM and data derived from meteorological satellites, and for the seasonal dynamics of the same tick using the computer simulation models ECFXPERT and T3HOST, all have their limitations. Statistical analysis of the relationships between the seasonal abundance of all three life stages of this tick and climatic and satellite-derived data from five sites in southern Africa, taken from the literature, supports a new perspective that it is the timing of the questing activity of the desiccation-vulnerable larvae that determines the pattern of the tick's seasonal dynamics. The timing of the activity of nymphs and adults is determined by temperature-dependent development rates plus the delaying phenomenon of photoperiod-sensitive diapause, the timing and duration of which have evolved to achieve maximum generation survival by ensuring the occurrence of eggs and larvae during periods of optimal climatic conditions. The most important environmental factor appears to be night-time minimum temperature, determining condensation and saturation deficit and thus the tick's ability to replenish moisture lost during the daytime and so to survive while questing for hosts. It is the larvae whose numbers are correlated most closely with these factors, consistent with earlier experimental results showing larvae to be most susceptible to desiccating conditions. There is a statistical linkage between larval tick numbers and satellite imagery, arising from the correlation between larval numbers and minimum temperature and saturation deficit conditions, and in turn the relationship between these climatic conditions and the subsequent vegetational changes monitored by the satellites. Moisture availability to larvae is likely to be the critical factor throughout the geographical range of R. appendiculatus, but the precise combination of climatic conditions that optimize moisture availability and questing tick survival can be expected to vary geographically. The relationships between ticks, temperatures and satellite data in parts of equatorial Africa have yet to be established. These correlative patterns highlight both the critical life stage and environmental factors when trying to understand temporal, and ultimately spatial, variations in tick abundance.

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Modelling the effect of feeding-related mortality on the feeding strategy of tsetse (Diptera: Glossinidae).

Free-living haematophagous insects risk death through host grooming responses or through increased susceptibility to predation whenever they take a bloodmeal. In this paper we investigate the effects of these risks on the feeding strategy of tsetse. A model is presented that allows for death of tsetse by starvation if they do not succeed in feeding within a fixed time (set at 6 days in the first instance) and for mortality specifically associated with feeding. In addition there is background mortality that applies to all flies at all times. The model is used to compute the individual life-time fertility (number of female puparia per female) as a function of the probability of obtaining a meal (indicated by field data to be very high, usually > 0.85 per day) and the day on which flies start to search for a meal. We suggest that the feeding strategy that would be selected for is that which allows the maximum reproductive output. The model shows that this strategy involves making no attempts to feed for 3-4 days after the previous meal and then attempting to feed with the greatest possible probability until a meal is obtained. The predicted feeding interval, obtained independently of any trapping data, agrees closely with all previous estimates from field studies using a variety of methods. Preliminary results from a laboratory experiment reveal an increased risk of predation of recently fed as compared with hungry tsetse. The lower the actual feeding mortality the more frequently will flies be able to feed should conditions so demand. It is adaptive, however, for tsetse to delay attempting to feed for as long as they can, which is made possible by the near certainty of locating and feeding on a host within 1 day, using their sophisticated sensory systems.

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Mortality rates and population density of tsetse flies correlated with satellite imagery.

Tsetse flies are a major constraint on animal production in about 10 million km2 of Africa through their transmission of animal trypanosomiasis. Up to 25 million people are at risk from human trypanosomiasis, or sleeping sickness. Tsetse research has been concentrated on the factors that control the distribution and abundance of these vectors and the means by which their numbers can be reduced. Eradication successes in some countries are insignificant compared with the continental scale of the problem and the long-term reduction in the area infested by tsetse has been negligible. We report here that the mortality rates of tsetse from sites in both West and East Africa, the size of male and female tsetse (related to the mortality rate of the parental female population) along a north-south transect in West Africa, and the abundance of two species of tsetse over the northern half of Côte d'Ivoire, are significantly correlated with data from meterological satellites. This information could be used to predict both the mortality rate and the abundance (key determinants of disease transmission potential) of tsetse over very large areas of the continent and to produce maps of high risk areas of disease transmission for the African trypanosomiases and, by implication, for many other vector-borne diseases.

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The effect of Babesia microti on feeding and survival in its tick vector, Ixodes trianguliceps.

Evidence is presented that Babesia microti may promote its transmission amongst rodents by enhancing the feeding success and survival of its tick vector, Ixodes trianguliceps. Both the mean engorged weight of larval ticks and the percentage moult of larvae to nymphs increased as larvae fed on naive hosts later in the parasitaemic cycle up to a point a few days beyond the loss of a patent infection. This increased feeding success and survival was not dependent on the level of infection by B. microti. Two possible, host-mediated mechanisms for the observed parasite-vector interactions are suggested, the antihaemostatic effects induced by babesiosis and the interaction of the immunosuppressive effects of Babesia and the development of immunity to ixodid ticks by their vertebrate hosts.

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