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    Inefficient co-feeding transmission of Borrelia afzelii in two common European songbirds
    (2017)
    Heylen, D.
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    Sprong, H.
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    Krawczyk, A.
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    Van Houtte, N.
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    Genne, D.
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    Gomez-Chamorro, A.
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    van Oers, K.
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  • Publication
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    Strain-specific antibodies reduce co-feeding transmission of the Lyme disease pathogen, Borrelia afzelii
    Vector-borne pathogens use a diversity of strategies to evade the vertebrate immune system. Co-feeding transmission is a potential immune evasion strategy because the vector-borne pathogen minimizes the time spent in the vertebrate host. We tested whether the Lyme disease pathogen, Borrelia afzelii, can use co-feeding transmission to escape the acquired immune response in the vertebrate host. We induced a strain-specific, protective antibody response by immunizing mice with one of two variants of OspC (A3 and A10), the highly variable outer surface protein C of Borrelia pathogens. Immunized mice were challenged via tick bite with B.afzelii strains A3 or A10 and infested with larval ticks at days 2 and 34 post-infection to measure co-feeding and systemic transmission respectively. Antibodies against a particular OspC variant significantly reduced co-feeding transmission of the targeted (homologous) strain but not the non-targeted (heterologous) strain. Cross-immunity between OspC antigens had no effect in co-feeding ticks but reduced the spirochaete load twofold in ticks infected via systemic transmission. In summary, OspC-specific antibodies reduced co-feeding transmission of a homologous but not a heterologous strain of B.afzelii. Co-feeding transmission allowed B.afzelii to evade the negative consequences of cross-immunity on the tick spirochaete load.
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    Cross-reactive acquired immunity influences transmission success of the Lyme disease pathogen, Borrelia afzelii
    Cross-reactive acquired immunity in the vertebrate host induces indirect competition between strains of a given pathogen species and is critical for understanding the ecology of mixed infections. In vector-borne diseases, cross-reactive antibodies can reduce pathogen transmission at the vector-to-host and the host-to-vector lifecycle transition. The highly polymorphic, immunodominant, outer surface protein C (OspC) of the tick-borne spirochete bacterium Borrelia afzelii induces a strong antibody response in the vertebrate host. To test how cross-immunity in the vertebrate host influences tick-to-host and host-to-tick transmission, mice were immunized with one of two strain-specific recombinant OspC proteins (A3, A10), challenged via tick bite with one of the two B. afzelii ospC strains (A3, A10), and infested with xenodiagnostic ticks. Immunization with a given rOspC antigen protected mice against homologous strains carrying the same major ospC group allele but provided little or no cross-protection against heterologous strains carrying a different major ospC group allele. There were cross-immunity effects on the tick spirochete load but not on the probability of host-to-tick transmission. The spirochete load in ticks that had fed on mice with cross-immune experience was reduced by a factor of two compared to ticks that had fed on naive control mice. In addition, strain-specific differences in mouse spirochete load, host-to-tick transmission, tick spirochete load, and the OspC-specific IgG response revealed the mechanisms that determine variation in transmission success between strains of B. afzelii. This study shows that cross-immunity in infected vertebrate hosts can reduce pathogen load in the arthropod vector with potential consequences for vector-to-host pathogen transmission. (C) 2015 Elsevier B.V. All rights reserved.
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    Infection dynamics in frog populations with different histories of decline caused by a deadly disease
    (2015-12)
    Sapsford, Sarah J.
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    Alford, Ross A.
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    Schwarzkopf, Lin
    Pathogens can drive host population dynamics. Chytridiomycosis is a fungal disease of amphibians that is caused by the fungus Batrachochytrium dendrobatidis (Bd). This pathogen has caused declines and extinctions in some host species whereas other host species coexist with Bd without suffering declines. In the early 1990s, Bd extirpated populations of the endangered common mistfrog, Litoria rheocola, at high-elevation sites, while populations of the species persisted at low-elevation sites. Today, populations have reappeared at many high-elevation sites where they presently co-exist with the fungus. We conducted a capture-mark-recapture (CMR) study of six populations of L. rheocola over 1 year, at high and low elevations. We used multistate CMR models to determine which factors (Bd infection status, site type, and season) influenced rates of frog survival, recapture, infection, and recovery from infection. We observed Bd-induced mortality of individual frogs, but did not find any significant effect of Bd infection on the survival rate of L. rheocola at the population level. Survival and recapture rates depended on site type and season. Infection rate was highest in winter when temperatures were favourable for pathogen growth, and differed among site types. The recovery rate was high (75.7-85.8 %) across seasons, and did not differ among site types. The coexistence of L. rheocola with Bd suggests that (1) frog populations are becoming resistant to the fungus, (2) Bd may have evolved lower virulence, or (3) current environmental conditions may be inhibiting outbreaks of the fatal disease.
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    Cross-immunity and community structure of a multiple-strain pathogen in the tick vector
    Many vector-borne pathogens consist of multiple strains that circulate in both the vertebrate host and the arthropod vector. Characterization of the community of pathogen strains in the arthropod vector is therefore important for understanding the epidemiology of mixed vector-borne infections. Borrelia afzelii and B. garinii are two species of tick-borne bacteria that cause Lyme disease in humans. These two sympatric pathogens use the same tick, Ixodes ricinus, but are adapted to different classes of vertebrate hosts. Both Borrelia species consist of multiple strains that are classified using the highly polymorphic ospC gene. Vertebrate cross-immunity against the OspC antigen is predicted to structure the community of multiple-strain Borrelia pathogens. Borrelia isolates were cultured from field-collected I. ricinus ticks over a period spanning 11 years. The Borrelia species of each isolate was identified using a reverse line blot (RLB) assay. Deep sequencing was used to characterize the ospC communities of 190 B. afzelii isolates and 193 B. garinii isolates. Infections with multiple ospC strains were common in ticks, but vertebrate cross-immunity did not influence the strain structure in the tick vector. The pattern of genetic variation at the ospC locus suggested that vertebrate cross-immunity exerts strong selection against intermediately divergent ospC alleles. Deep sequencing found that more than 50% of our isolates contained exotic ospC alleles derived from other Borrelia species. Two alternative explanations for these exotic ospC alleles are cryptic coinfections that were not detected by the RLB assay or horizontal transfer of the ospC gene between Borrelia species.
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    Serological signature of tick-borne pathogens in Scandinavian brown bears over two decades
    (2015-7-28) ;
    Jones, Krista L.
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    Evans, Alina L.
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    Lienhard, Reto
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    Arnemo, Jon M.
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    Swenson, Jon E.
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    Background: Anthropogenic disturbances are changing the geographic distribution of ticks and tick-borne diseases. Over the last few decades, the tick Ixodes ricinus has expanded its range and abundance considerably in northern Europe. Concurrently, the incidence of tick-borne diseases, such as Lyme borreliosis and tick-borne encephalitis, has increased in the human populations of the Scandinavian countries. Methods: Wildlife populations can serve as sentinels for changes in the distribution of tick-borne diseases. We used serum samples from a long-term study on the Scandinavian brown bear, Ursus arctos, and standard immunological methods to test whether exposure to Borrelia burgdorferi sensu lato, the causative agent of Lyme borreliosis, and tick-borne encephalitis virus (TBEV) had increased over time. Bears had been sampled over a period of 18 years (1995-2012) from a southern area, where Ixodes ricinus ticks are present, and a northern area where ticks are uncommon or absent. Results: Bears had high levels of IgG antibodies against B. burgdorferi sensu lato but not TBEV. Bears at the southern area had higher values of anti-Borrelia IgG antibodies than bears at the northern area. Over the duration of the study, the value of anti-Borrelia IgG antibodies increased in the southern area but not the northern area. Anti-Borrelia IgG antibodies increased with the age of the bear but declined in the oldest age classes. Conclusions: Our study is consistent with the view that ticks and tick-borne pathogens are expanding their abundance and prevalence in Scandinavia. Long-term serological monitoring of large mammals can provide insight into how anthropogenic disturbances are changing the distribution of ticks and tick-borne diseases.
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    The Lyme Disease Pathogen Has No Effect on the Survival of Its Rodent Reservoir Host
    (2015-2-17) ;
    Lachish, Shelly
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    Dolan, Marc C.
    Zoonotic pathogens that cause devastating morbidity and mortality in humans may be relatively harmless in their natural reservoir hosts. The tick-borne bacterium Borrelia burgdorferi causes Lyme disease in humans but few studies have investigated whether this pathogen reduces the fitness of its reservoir hosts under natural conditions. We analyzed four years of capture-mark-recapture (CMR) data on a population of white-footed mice, Peromyscus leucopus, to test whether B. burgdorferi and its tick vector affect the survival of this important reservoir host. We used a multi-state CMR approach to model mouse survival and mouse infection rates as a function of a variety of ecologically relevant explanatory factors. We found no effect of B. burgdorferi infection or tick burden on the survival of P. leucopus. Our estimates of the probability of infection varied by an order of magnitude (0.051 to 0.535) and were consistent with our understanding of Lyme disease in the Northeastern United States. B. burgdorferi establishes a chronic avirulent infection in their rodent reservoir hosts because this pathogen depends on rodent mobility to achieve transmission to its sedentary tick vector. The estimates of B. burgdorferi infection risk will facilitate future theoretical studies on the epidemiology of Lyme disease.