M Bennett

University of Liverpool, Liverpool, ENG, United Kingdom

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Publications (90)373.79 Total impact

  • Source
    Article: The prevalence of antimicrobial‐resistant Escherichia coli in sympatric wild rodents varies by season and host
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    ABSTRACT: Aims:  To investigate the prevalence and temporal patterns of antimicrobial resistance in wild rodents with no apparent exposure to antimicrobials.Methods and Results:  Two sympatric populations of bank voles and wood mice were trapped and individually monitored over a 2- year period for faecal carriage of antimicrobial-resistant Escherichia coli. High prevalences of ampicillin-, chloramphenicol-, tetracycline- and trimethoprim-resistant E. coli were observed. A markedly higher prevalence of antimicrobial-resistant E. coli was found in wood mice than in bank voles, with the prevalence in both increasing over time. Superimposed on this trend was a seasonal cycle with a peak prevalence of resistant E. coli in mice in early- to mid-summer and in voles in late summer and early autumn.Conclusions:  These sympatric rodent species had no obvious contact with antimicrobials, and the difference in resistance profiles between rodent species and seasons suggests that factors present in their environment are unlikely to be drivers of such resistance.Significance and Impact of the Study:  These findings suggest that rodents may represent a reservoir of antimicrobial-resistant bacteria, transmissible to livestock and man. Furthermore, such findings have implications for human and veterinary medicine regarding antimicrobial usage and subsequent selection of antimicrobial-resistant organisms.
    Journal of Applied Microbiology 02/2011; 110(4):962 - 970. · 2.34 Impact Factor
  • Article: The prevalence of antimicrobial-resistant Escherichia coli in sympatric wild rodents varies by season and host.
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    ABSTRACT: Aims:  To investigate the prevalence and temporal patterns of antimicrobial resistance in wild rodents with no apparent exposure to antimicrobials. Methods and Results:  Two sympatric populations of bank voles and wood mice were trapped and individually monitored over a 2- year period for faecal carriage of antimicrobial-resistant Escherichia coli. High prevalences of ampicillin-, chloramphenicol-, tetracycline- and trimethoprim-resistant E. coli were observed. A markedly higher prevalence of antimicrobial-resistant E. coli was found in wood mice than in bank voles, with the prevalence in both increasing over time. Superimposed on this trend was a seasonal cycle with a peak prevalence of resistant E. coli in mice in early- to mid-summer and in voles in late summer and early autumn. Conclusions:  These sympatric rodent species had no obvious contact with antimicrobials, and the difference in resistance profiles between rodent species and seasons suggests that factors present in their environment are unlikely to be drivers of such resistance. Significance and Impact of the Study:  These findings suggest that rodents may represent a reservoir of antimicrobial-resistant bacteria, transmissible to livestock and man. Furthermore, such findings have implications for human and veterinary medicine regarding antimicrobial usage and subsequent selection of antimicrobial-resistant organisms.
    Journal of Applied Microbiology 01/2011; · 2.34 Impact Factor
  • Article: Isolation of a novel Campylobacter jejuni clone associated with the bank vole, Myodes glareolus.
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    ABSTRACT: Campylobacter jejuni can be isolated from different animal hosts. Various studies have used multilocus sequence typing to look for associations between particular clones of C. jejuni and specific hosts. Here, we describe the isolation of a novel clone (sequence type 3704 [ST-3704]) of C. jejuni associated with the bank vole (Myodes glareolus).
    Applied and environmental microbiology 11/2010; 76(21):7318-21. · 3.69 Impact Factor
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    Article: Multi-locus sequence typing of Salmonella enterica serovar Typhimurium isolates from wild birds in northern England suggests host-adapted strain.
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    ABSTRACT: Recent studies have suggested that Salmonella Typhimurium strains associated with mortality in UK garden birds are significantly different from strains that cause disease in humans and livestock and that wild bird strains may be host adapted. However, without further genomic characterization of these strains, it is not possible to determine whether they are host adapted. The aim of this study was to characterize a representative sample of Salm. Typhimurium strains detected in wild garden birds using multi-locus sequence typing (MLST)to investigate evolutionary relationships between them. Multi-locus sequence typing was performed on nine Salm. Typhimurium strains isolated from wild garden birds. Two sequence types were identified, the most common of which was ST568. Examination of the public Salmonella enterica MLST database revealed that only three other ST568 isolates had been cultured from a human in Scotland. Two further isolates of Salm. Typhimurium were determined to be ST19. Results of MLST analysis suggest that there is a predominant strain of Salm. Typhimurium circulating among garden bird populations in the United Kingdom, which is rarely detected in other species, supporting the hypothesis that this strain is host adapted. Host-pathogen evolution is often assumed to lead to pathogens becoming less virulent to avoid the death of their host; however, infection with ST568 led to high mortality rates among the wild birds examined, which were all found dead at wild bird-feeding stations. We hypothesize that by attracting unnaturally high densities of birds, wild bird-feeding stations may facilitate the transmission of ST568 between wild birds, therefore reducing the evolutionary cost of this pathogen killing its host, resulting in a host-adapted strain with increased virulence.
    Letters in Applied Microbiology 10/2010; 51(4):477-9. · 1.62 Impact Factor
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    Article: Risk factors for the occurrence of Escherichia coli virulence genes eae, stx1 and stx2 in wild bird populations.
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    ABSTRACT: Shiga toxin-producing Escherichia coli (STEC) can cause serious disease in human beings. Ruminants are considered to be the main reservoir of human STEC infections. However, STEC have also been isolated from other domestic animals, wild mammals and birds. We describe a cross-sectional study of wild birds in northern England to determine the prevalence of E. coli-containing genes that encode Shiga toxins (stx1 and stx2) and intimin (eae), important virulence determinants of STEC associated with human disease. Multivariable logistic regression analysis identified unique risk factors for the occurrence of each virulence gene in wild bird populations. The results of our study indicate that while wild birds are unlikely to be direct sources of STEC infections, they do represent a potential reservoir of virulence genes. This, coupled with their ability to act as long-distance vectors of STEC, means that wild birds have the potential to influence the spread and evolution of STEC.
    Epidemiology and Infection 04/2009; 137(11):1574-82. · 2.84 Impact Factor
  • Article: Host condition and individual risk of cowpox virus infection in natural animal populations: cause or effect?
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    ABSTRACT: Recent studies have provided evidence that endemic pathogens may affect dynamics in animals. However, such studies have not typically considered that infected individuals might have a preceding underlying poor condition. We examined whether individuals in poor condition are more likely to become infected by an endemic pathogen, using as a system the dynamics of cowpox virus in field voles. With data from monthly sampled vole populations, a nested case-control study evaluated whether susceptible individuals with poorer condition had higher probabilities of contracting cowpox. The influence of condition was found to be considerable, especially for males. At times when a susceptible male with good body condition had a relatively low probability of becoming infected, a susceptible male with poor body condition was twice as likely to contract cowpox; if this male was also anaemic, the chances were almost quadrupled. We discuss the care needed when interpreting the findings of wildlife disease studies.
    Epidemiology and Infection 02/2009; 137(9):1295-301. · 2.84 Impact Factor
  • Article: Parasite interactions in natural populations: insights from longitudinal data.
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    ABSTRACT: The physiological and immunological state of an animal can be influenced by current infections and infection history. Consequently, both ongoing and previous infections can affect host susceptibility to another parasite, the biology of the subsequent infection (e.g. infection length) and the impact of infection on host morbidity (pathology). In natural populations, most animals will be infected by a succession of different parasites throughout the course of their lives, with probably frequent concomitant infections. The relative timing of different infections experienced by a host (i.e. the sequence of infection events), and the effects on factors such as host susceptibility and host survival, can only be derived from longitudinal data on individual hosts. Here we review some of the evidence for the impact of co-infection on host susceptibility, infection biology and pathology focusing on insights obtained from both longitudinal studies in humans and experiments that explicitly consider the sequence of infection. We then consider the challenges posed by longitudinal infection data collected from natural populations of animals. We illustrate their usefulness using our data of microparasite infections associated with field vole (Microtus agrestis) populations to examine impacts on susceptibility and infection length. Our primary aim is to describe an analytical approach that can be used on such data to identify interactions among the parasites. The preliminary analyses presented here indicate both synergistic and antagonistic interactions between microparasites within this community and emphasise that such interactions could have significant impacts on host-parasite fitness and dynamics.
    Parasitology 07/2008; 135(7):767-81. · 2.96 Impact Factor
  • Article: The laboratory diagnosis of Orthopoxvirus infection in the domestic cat
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    ABSTRACT: Twenty-eight cases of naturally occurring feline Orthopoxvirus infection were diagnosed by combinations of virus isolation, electron microscopy, agar gel precipitation, histopathology and serology. Twenty-five of 28 cases were positive by virus isolation on the chorioallantoic membrane of hens' eggs and in tissue culture, 22 of 28 by electron microscopy, three of five by histopathology, none by agar gel precipitation, and 17 of 17 by serology.The techniques used are described, and the results compared and discussed.
    Journal of Small Animal Practice 04/2008; 26(11):653 - 661. · 1.00 Impact Factor
  • Article: Tuberculosis (Mycobacterium microti) in wild field vole populations.
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    ABSTRACT: Vole tuberculosis (TB; Mycobacterium microti) is an understudied endemic infection. Despite progressing slowly, it causes severe clinical pathology and overt symptoms in its rodent host. TB was monitored for 2 years in wild field voles in Kielder Forest, UK. The prevalence of characteristic cutaneous TB lesions was monitored longitudinally at 4 sites, with individuals live-trapped and repeatedly monitored. A prevalence of 5.2% of individuals with lesions was recorded (n=2791). In a cross-sectional study, 27 sites were monitored bi-annually, with TB assessed by post-mortem examination for macroscopic lesions, and by culture and histopathology. Seventy-nine voles (10.78%; n=733) were positive for mycobacteria, with the highest prevalence in spring (13.15%; n=327). TB prevalence varied, with between 0% and 50% of voles infected per site. Prevalence increased with age (mass), and apparent seasonality was due to a higher proportion of older animals in spring. Survival analysis supported this result, with cutaneous lesions only manifesting in the advanced stages of infection, and therefore only being found on older voles. The body condition of individuals with lesions declined at the time when the lesion was first recorded, when compared to individuals without lesions, suggesting there may be an acute phase of infection during its advanced stage. Although predicted survival following the appearance of a cutaneous lesion was lower than for uninfected individuals, this was not significant.
    Parasitology 04/2008; 135(3):309-17. · 2.96 Impact Factor
  • Article: Plague metapopulation dynamics in a natural reservoir: the burrow system as the unit of study.
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    ABSTRACT: The ecology of plague (Yersinia pestis infection) in its ancient foci in Central Asia remains poorly understood. We present field data from two sites in Kazakhstan where the great gerbil (Rhombomys opimus) is the major natural host. Family groups inhabit and defend burrow systems spaced throughout the landscape, such that the host population may be considered a metapopulation, with each occupied burrow system a subpopulation. We examine plague transmission within and between family groups and its effect on survival. Transmission of plague occurred disproportionately within family groups although not all gerbils became infected once plague entered a burrow system. There were no spatial patterns to suggest that family groups in close proximity to infected burrow systems were more at risk of infection than those far away. At one site, infection increased the chances of burrow-system extinction. Overall, it is useful to consider the burrow system as the unit of study within a much larger metapopulation.
    Epidemiology and Infection 08/2007; 135(5):740-8. · 2.84 Impact Factor
  • Article: Haemoparasites of common shrews (Sorex araneus) in Northwest England.
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    ABSTRACT: The presence of haemoparasites belonging to the taxa Anaplasma, Bartonella and Trypanosoma was determined among 76 common shrews (Sorex araneus) from Northwest England. Anaplasma phagocytophilum DNA was recovered from the blood of 1 shrew (1.3%), with the amplified 16S rRNA sequence identical to one previously reported from a bank vole (Clethrionomys glareolus). Trypanosoma spp. DNA was detected in 9 shrews (11.8%), the amplified 18S rDNA fragments being indistinguishable from one another, and distinct from previously published data. This represents the first report of trypanosome infection in S. araneus and suggests they are susceptible to an uncharacterized Trypanosoma species. Blood from 11 shrews (14.5%) yielded Bartonella spp., with characterization of isolates using comparative sequence analysis of partial gltA and 16S-23S rRNA intergenic spacer regions revealing 2 different genotypes. Phylogenetic inference from alignment of partial gltA sequences found that both UK S. araneus types formed a well-supported cluster with Bartonella sp. isolated from S. araneus in Sweden. No significant effect of host age, sex, or year of collection was found on prevalence of Bartonella or trypanosome infections. The results of this survey demonstrate that common shrews in the UK are susceptible to haemoparasitic infections, at prevalences similar to those reported from sympatric rodents.
    Parasitology 07/2007; 134(Pt 6):819-26. · 2.96 Impact Factor
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    Article: Serological survey of virus infection among wild house mice (Mus domesticus) in the UK.
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    ABSTRACT: The serological prevalence of 13 murine viruses was surveyed among 103 wild-caught and 51 captive-bred house mice (Mus domesticus), originating from several trapping locations in northwest England, using blood samples obtained during routine health screening of an established wild mouse colony. A high proportion of recently caught wild mice were seropositive for mouse hepatitis virus (86%), mouse cytomegalovirus (79%), mouse thymic virus (78%), mouse adenovirus (68%), mouse parvovirus (59%) and minute virus of mice (41%). Seroprevalences of lymphocytic choriomeningitis virus (LCMV), orthopoxvirus, reovirus-3 and murid herpesvirus 4 (MuHV-4, also called murine gamma-herpesvirus [MHV-68]) were low (3-13%), and no animals were seropositive to Sendai virus, pneumonia virus or polyomavirus. Seroprevalence in wild-caught animals that had been in captivity for over six months was generally consistent with the range found in recently caught wild animals, while seroprevalence was generally much lower in captive-bred mice despite no attempt to prevent viral spread. A notable exception to this was LCMV, which appeared to have spread efficiently through the captive population (both captive-bred and wild-caught animals). Given the known viral life cycles in laboratory mice, it appears that viral persistence in the host was an important contributing factor in the spread of infection in captivity.
    Laboratory Animals 05/2007; 41(2):229-38. · 1.21 Impact Factor
  • Article: Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics.
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    ABSTRACT: Many zoonotic disease agents are transmitted between hosts by arthropod vectors, including fleas, but few empirical studies of host-vector-microparasite dynamics have investigated the relative importance of hosts and vectors. This study investigates the dynamics of 4 closely related Bartonella species and their flea vectors in cyclic populations of field voles (Microtus agrestis) over 3 years. The probability of flea infestation was positively related to field vole density 12 months previously in autumn, but negatively related to more recent host densities, suggesting a dilution effect. The 4 Bartonella species exhibited contrasting dynamics. Only B. grahamii, showed a distinct seasonal pattern. Infection probability increased with field vole density for B. doshiae, B. taylorii and BGA (a previously unidentified species) and with density of coexisting wood mice for B. doshiae and B. grahamii. However, only the infection probability of BGA in spring was related to flea prevalence. B. doshiae and BGA were most common in older animals, but the other 2 were most common in non-reproductive hosts. Generally, host density rather than vector abundance appears most important for the dynamics of flea-transmitted Bartonella spp., possibly reflecting the importance of flea exchange between hosts. However, even closely related species showed quite different dynamics, emphasising that other factors such as population age structure can impact on zoonotic risk.
    Parasitology 04/2007; 134(Pt 3):413-25. · 2.96 Impact Factor
  • Article: A role for vector-independent transmission in rodent trypanosome infection?
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    ABSTRACT: Within host-pathogen systems where vector-borne transmission is the primary route of infection, little or no attention has been paid to the relative importance of secondary or alternative routes of transmission. Here, by contrast, we report the results from a controlled longitudinal field-scale experiment in which the prevalence of fleas (Siphonaptera) was manipulated and the occurrence and distribution of a flea-borne protozoan (Trypanosoma (Herpetosoma) microti) in a natural field vole (Microtus agrestis) population was monitored over a 2-year period. A non-systemic insecticide was applied to individual voles within two treatment grids and the prevalences of fleas and of T. microti were monitored on these and on two control grids. Blood samples were taken from all voles and PCR-based methods used to determine infection status. Insecticidal treatment was highly effective at reducing overall flea prevalence and recaptured animals (treated ca. 4 weeks previously) were very rarely infested (ca. 3%, compared with 50-70+% normally). On the other hand, the probability of trypanosome infection was reduced in treated animals on experimental grids to only around one-third of that normally observed. This suggests that direct, as opposed to flea-borne, transmission may not only occur, it may also be of epidemiological importance. The possibility that the importance of such transmission routes may have been underestimated in 'vector-borne' infections more generally is discussed.
    International Journal for Parasitology 12/2006; 36(13):1359-66. · 3.39 Impact Factor
  • Article: Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom?
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    ABSTRACT: The importance of wild rodents as reservoirs of zoonotic tick-borne pathogens is considered low in the United Kingdom because, in studies to date, those parasitized by exophilic Ixodes ricinus ticks carry almost exclusively larvae and thus have a minor role in transmission cycles. In a cross-sectional study, 11 (6.7%) of 163 field voles (Microtus agrestis) captured at field sites in Northern England were PCR-positive for Anaplasma phagocytophilum. The voles were found to act as hosts for both larval and nymphal I. ricinus and all stages of the nidicolous tick I. trianguliceps, and eight individuals were infested with ticks of both species at the same time. Two of 158 larval and one of 13 nymphal I. ricinus, as well as one of 14 larval and one of 15 nymphal I. trianguliceps collected from the rodents were PCR-positive. These findings suggest that habitats where field voles are abundant in the United Kingdom may pose a risk of A. phagocytophilum infection because (i) field voles, the most abundant terrestrial mammal in the United Kingdom, may be a competent reservoir; (ii) the field voles are hosts for both nymphal and larval ixodid ticks so they could support endemic cycles of A. phagocytophilum; and (iii) they are hosts for nidicolous I. trianguliceps, which may alone maintain endemic cycles, and exophilic I. ricinus ticks, which could act as a bridge vector and transmit infections to humans and domesticated animals.
    Vector Borne and Zoonotic Diseases 02/2006; 6(4):404-10. · 2.44 Impact Factor
  • Article: Trypanosomes, fleas and field voles: ecological dynamics of a host-vector--parasite interaction.
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    ABSTRACT: To investigate the prevalence of a flea-borne protozoan (Trypanosoma (Herpetosoma) microti) in its field vole (Microtus agrestis) host, we monitored over a 2-year period a range of intrinsic and extrinsic parameters pertaining to host demographics, infection status and vector (flea) prevalence. Generalized Linear Mixed Modelling was used to analyse patterns of both flea and trypanosome occurrence. Overall, males of all sizes and ages were more likely to be infested with fleas than their female counterparts. Flea prevalence also showed direct density dependence during the winter, but patterns of density dependence varied amongst body mass (age) classes during the summer. Trypanosome prevalence did not vary between the sexes but was positively related to past flea prevalence with a lag of 3 months, with the highest levels occurring during the autumn season. A convex age-prevalence distribution was observed, suggesting that individuals develop a degree of immunity to trypanosome infection with age and exposure. An interaction between age and whether the individual was new or recaptured suggested that infected animals are less likely to become territory holders than their uninfected counterparts.
    Parasitology 10/2005; 131(Pt 3):355-65. · 2.96 Impact Factor
  • Article: Trypanosomes, fleas and field voles: ecological dynamics of a host-vector–parasite interaction
    S.  BURTHE , M.  BENNETT , M.  BEGON 
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    ABSTRACT: To investigate the prevalence of a flea-borne protozoan (Trypanosoma (Herpetosoma) microti) in its field vole (Microtus agrestis) host, we monitored over a 2-year period a range of intrinsic and extrinsic parameters pertaining to host demographics, infection status and vector (flea) prevalence. Generalized Linear Mixed Modelling was used to analyse patterns of both flea and trypanosome occurrence. Overall, males of all sizes and ages were more likely to be infested with fleas than their female counterparts. Flea prevalence also showed direct density dependence during the winter, but patterns of density dependence varied amongst body mass (age) classes during the summer. Trypanosome prevalence did not vary between the sexes but was positively related to past flea prevalence with a lag of 3 months, with the highest levels occurring during the autumn season. A convex age-prevalence distribution was observed, suggesting that individuals develop a degree of immunity to trypanosome infection with age and exposure. An interaction between age and whether the individual was new or recaptured suggested that infected animals are less likely to become territory holders than their uninfected counterparts.
    Parasitology 08/2005; 131(03):355 - 365. · 2.96 Impact Factor
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    Article: New world origins for haemoparasites infecting United Kingdom grey squirrels (Sciurus carolinensis), as revealed by phylogenetic analysis of bartonella infecting squirrel populations in England and the United States.
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    ABSTRACT: Phylogenetic analyses of bartonella have suggested divergence between bartonellae that infect mammals native to the Old and New Worlds. We characterized bartonella isolated from Eastern grey squirrels (Sciurius carolinensis) in the United States and from grey and red squirrels (Sciurus vulgaris) in the United Kingdom by nucleotide sequence comparison (gltA and groEL). Isolates from grey squirrels in the United States and the United Kingdom were identical, and most similar to Bartonella vinsonii, a species associated with New World rodents. A single and novel bartonella genotype was obtained from all 12 red squirrel isolates. Although grey squirrels were first introduced into the United Kingdom over 125 years ago, they continue to be infected solely by the bartonella associated with grey squirrels native to the United States. These results illustrate that exotic species may be accompanied by the introduction and maintenance, over many generations, of their microparasites.
    Epidemiology and Infection 01/2003; 129(3):647-53. · 2.84 Impact Factor
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    Article: A clarification of transmission terms in host-microparasite models: numbers, densities and areas.
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    ABSTRACT: Transmission is the driving force in the dynamics of any infectious disease. A crucial element in understanding disease dynamics, therefore, is the 'transmission term' describing the rate at which susceptible hosts are 'converted' into infected hosts by their contact with infectious material. Recently, the conventional form of this term has been increasingly questioned, and new terminologies and conventions have been proposed. Here, therefore, we review the derivation of transmission terms, explain the basis of confusion, and provide clarification. The root of the problem has been a failure to include explicit consideration of the area occupied by a host population, alongside both the number of infectious hosts and their density within the population. We argue that the terms 'density-dependent transmission' and 'frequency-dependent transmission' remain valid and useful (though a 'fuller' transmission term for the former is identified), but that the terms 'mass action', 'true mass action' and 'pseudo mass action' are all unhelpful and should be dropped. Also, contrary to what has often been assumed, the distinction between homogeneous and heterogeneous mixing in a host population is orthogonal to the distinction between density- and frequency-dependent transmission modes.
    Epidemiology and Infection 09/2002; 129(1):147-53. · 2.84 Impact Factor
  • Article: GranulocyticEhrlichiainfection in Ixodid ticks and mammals in woodlands and uplands of the U.K.
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    ABSTRACT: The prevalence of infection with Ehrlichiae of the Ehrlichia phagocytophila genogroup (the granulocytic Ehrlichiae), in questing Ixodes ricinus ticks of U.K. upland and woodland habitats, was investigated by PCR. The prevalence of infection in the three feeding stages of I. ricinus indicated that granulocytic Ehrlichiae are transmitted transstadially with no, or inefficient, transovarial transmission. The presence of infected ticks in both habitats indicates that endemic cycles of granulocytic Ehrlichia (GE) infection are maintained by both domesticated sheep and by wild reservoirs, and coexist with endemic cycles of Borrelia burgdorferi infection. Moreover, demonstration, for the first time, of GE infection in engorged Ixodes trianguliceps ticks and blood collected from wild rodents, suggests that European wild rodents are competent reservoirs. GE infection prevalence in nymphal and adult I. ricinus was significantly greater in uplands than woodlands, which is consistent with ticks of all three feeding stages feeding on reservoir-competent sheep in uplands. In one woodland studied, pheasants are important hosts for nymphal I. ricinus but are incompetent or inefficient reservoirs, so reducing GE infection prevalence in I. ricinus ticks in this habitat. 16S rRNA sequences of GE from ticks of these U.K. habitats, showed a high degree of homology with those of granulocytic Ehrlichiae isolated from humans, but also showed some evidence of genetic diversity of granulocytic ehrlichiae in the U.K. The implications of these findings, for the taxonomy of granulocytic ehrlichiae and the potential for human infections to occur in the U.K., is discussed.
    Medical and Veterinary Entomology 06/2002; 12(4):423 - 429. · 1.91 Impact Factor

Institutions

  • 1989–2011
    • University of Liverpool
      • • Institute of Infection & Global Health
      • • School of Biological Sciences
      • • School of Veterinary Science
      Liverpool, ENG, United Kingdom
  • 2007
    • Universiteit Utrecht
      • Department of Biology
      Utrecht, Provincie Utrecht, Netherlands
  • 2000–2001
    • University of Bristol
      Bristol, ENG, United Kingdom
  • 1995–1996
    • University of Liège
      • Faculté de Médecine Vétérinaire
      Liège, WAL, Belgium