BACKGROUND: Powassan virus, a North American tick-borne flavivirus, can cause severe neuroinvasive disease in humans. While Ixodes scapularis are the primary vectors of Powassan virus lineage II (POWV II), also known as deer tick virus, recent laboratory vector competence studies showed that other genera of ticks can horizontally and vertically transmit POWV II. One such tick is the Haemaphysalis longicornis, an invasive species from East Asia that recently established populations in the eastern USA and already shares overlapping geographic range with native vector species such as I. scapularis. Reports of invasive H. longicornis feeding concurrently with native I. scapularis on multiple sampled hosts highlight the potential for interspecies co-feeding transmission of POWV II. Given the absence of a clearly defined vertebrate reservoir host for POWV II, it is possible that this virus is sustained in transmission foci via nonviremic transmission between ticks co-feeding on the same vertebrate host. The objective of this study was to evaluate whether uninfected H. longicornis co-feeding in close proximity to POWV II-infected I. scapularis can acquire POWV independent of host viremia.
METHODS: Using an in vivo tick transmission model, I. scapularis females infected with POWV II (\"donors\") were co-fed on mice with uninfected H. longicornis larvae and nymphs (\"recipients\"). The donor and recipient ticks were infested on mice in various sequences, and mouse infection status was monitored by temporal screening of blood for POWV II RNA via quantitative reverse transcription polymerase chain reaction (q-RT-PCR).
RESULTS: The prevalence of POWV II RNA was highest in recipient H. longicornis that fed on viremic mice. However, nonviremic mice were also able to support co-feeding transmission of POWV, as demonstrated by the detection of viral RNA in multiple H. longicornis dispersed across different mice. Detection of viral RNA at the skin site of tick feeding but not at distal skin sites indicates that a localized skin infection facilitates transmission of POWV between donor and recipient ticks co-feeding in close proximity.
CONCLUSIONS: This is the first report examining transmission of POWV between co-feeding ticks. Against the backdrop of multiple unknowns related to POWV ecology, findings from this study provide insight on possible mechanisms by which POWV could be maintained in nature.

Co-feeding is a mode of pathogen transmission for a wide range of tick-borne diseases where susceptible ticks can acquire infection from co-feeding with infected ticks on the same hosts. The significance of this transmission pathway is determined by the co-occurrence of ticks at different stages in the same season. Taking this into account, we formulate a system of differential equations with tick population dynamics and pathogen transmission dynamics highly regulated by the seasonal temperature variations. We examine the global dynamics of the model systems, and show that the two important ecological and epidemiological basic reproduction numbers can be used to fully characterize the long-term dynamics, and we link these two important threshold values to efficacy of co-feeding transmission.

By extending a mechanistic model for the tick-borne pathogen systemic transmission with the consideration of seasonal climate impacts, host movement as well as the co-feeding transmission route, this paper proposes a novel modeling framework for describing the spatial dynamics of tick-borne diseases. The net reproduction number for tick growth and basic reproduction number for disease transmission are derived, which predict the global dynamics of tick population growth and disease transmission. Numerical simulations not only verify the analytical results, but also characterize the contribution of co-feeding transmission route on disease prevalence in a habitat and the effect of host movement on the spatial spreading of the pathogen.

Trypanosoma rangeli (T. rangeli), a parasite, is not pathogenic to human but pathogenic to some vector species to induce the behavior changes of infected vectors and subsequently impact the transmission dynamics of other diseases such as Chagas disease which shares the same vector species. Here we develop a mathematical model and conduct qualitative analysis for the transmission dynamics of T. rangeli. We incorporate both systemic and co-feeding transmission routes, and account for the pathogenic effect using infection-induced fecundity and fertility change of the triatomine bugs. We derive two thresholds Rv (the triatomine bug basic reproduction number) and R0 (the T. rangeli basic reproduction number) to delineate the dynamical behaviors of the ecological and epidemiological systems. We show that when Rv>1 and R0>1, a unique parasite positive equilibrium E* appears. We find that E* can be unstable and periodic oscillations can be observed where the pathogenic effect plays a significant role. Implications of the qualitative analysis and numerical simulations suggest the need of an integrative vector-borne disease prevention and control strategy when multiple vector-borne diseases are transmitted by the same set of vector species.

Transmission from the vertebrate host to the arthropod vector is a critical step in the life-cycle of any vector-borne pathogen. How the probability of host-to-vector transmission changes over the duration of the infection is an important predictor of pathogen fitness. The Lyme disease pathogen Borrelia afzelii is transmitted by Ixodes ricinus ticks and establishes a chronic infection inside rodent reservoir hosts. The present study compares the temporal pattern of host-to-tick transmission between two strains of B. afzelii.
Laboratory mice were experimentally infected via tick bite with one of two strains of B. afzelii: A3 and A10. Mice were repeatedly infested with pathogen-free larval Ixodes ricinus ticks over a period of 4 months. Engorged larval ticks moulted into nymphal ticks that were tested for infection with B. afzelii using qPCR. The proportion of infected nymphs was used to characterize the pattern of host-to-tick transmission over time.
Both strains of B. afzelii followed a similar pattern of host-to-tick transmission. Transmission decreased from the acute to the chronic phase of the infection by 16.1 and 29.3% for strains A3 and A10, respectively. Comparison between strains found no evidence of a trade-off in transmission between the acute and chronic phase of infection. Strain A10 had higher lifetime fitness and established a consistently higher spirochete load in nymphal ticks than strain A3.
Quantifying the relationship between host-to-vector transmission and the age of infection in the host is critical for estimating the lifetime fitness of vector-borne pathogens.

Rickettsiae are obligately intracellular bacteria that are transmitted to vertebrates by a variety of arthropod vectors, primarily by fleas and ticks. Once transmitted or experimentally inoculated into susceptible mammals, some rickettsiae may cause febrile illness of different morbidity and mortality, and which can manifest with different types of exhanthems in humans. However, most rickettsiae circulate in diverse sylvatic or peridomestic reservoirs without having obvious impacts on their vertebrate hosts or affecting humans. We have analyzed the key features of tick-borne maintenance of rickettsiae, which may provide a deeper basis for understanding those complex invertebrate interactions and strategies that have permitted survival and circulation of divergent rickettsiae in nature. Rickettsiae are found in association with a wide range of hard and soft ticks, which feed on very different species of large and small animals. Maintenance of rickettsiae in these vector systems is driven by both vertical and horizontal transmission strategies, but some species of Rickettsia are also known to cause detrimental effects on their arthropod vectors. Contrary to common belief, the role of vertebrate animal hosts in maintenance of rickettsiae is very incompletely understood. Some clearly play only the essential role of providing a blood meal to the tick while other hosts may supply crucial supplemental functions for effective agent transmission by the vectors. This review summarizes the importance of some recent findings with known and new vectors that afford an improved understanding of the eco-epidemiology of rickettsiae; the public health implications of that information for rickettsial diseases are also described. Special attention is paid to the co-circulation of different species and genotypes of rickettsiae within the same endemic areas and how these observations may influence, correctly or incorrectly, trends, and conclusions drawn from the surveillance of rickettsial diseases in humans.

The vector-to-host and host-to-vector transmission steps are the two critical events that define the life cycle of any vector-borne pathogen. We expect negative genetic correlations between these two transmission phenotypes, if parasite genotypes specialized at invading the vector are less effective at infecting the vertebrate host and vice versa. We used the tick-borne bacterium Borrelia afzelii, a causative agent of Lyme borreliosis in Europe, to test whether genetic trade-offs exist between tick-to-host, systemic (host-to-tick), and a third mode of co-feeding (tick-to-tick) transmission. We worked with six strains of B. afzelii that were differentiated according to their ospC gene. We compared the three components of transmission among the B. afzelii strains using laboratory rodents as the vertebrate host and a laboratory colony of Ixodes ricinus as the tick vector. We used next generation matrix models to combine these transmission components into a single estimate of the reproductive number (R0) for each B. afzelii strain. We also tested whether these strain-specific estimates of R0 were correlated with the strain-specific frequencies in the field. We found significant genetic variation in the three transmission components among the B. afzelii strains. This is the first study to document genetic variation in co-feeding transmission for any tick-borne pathogen. We found no evidence of trade-offs as the three pairwise correlations of the transmission rates were all positive. The R0 values from our laboratory study explained 45% of the variation in the frequencies of the B. afzelii ospC strains in the field. Our study suggests that laboratory estimates of pathogen fitness can predict the distribution of pathogen strains in nature.

Biotic factors contributing to the survival of tick-borne viruses in nature are poorly understood. Using tick-borne encephalitis virus (TBEV) and its principal European vector, Ixodes ricinus, we examined the relative roles of salivary gland infection, co-feeding transmission, and moulting in virus survival. Virus titres in the salivary glands increased after blood-feeding in a time- and dose-dependent manner. This was observed in ticks infected by inoculation but not in ticks infected by the natural route of co-feeding. Amplification of infection prevalence occurred via co-feeding. However, when larvae or nymphs subsequently moulted, the infection prevalence dramatically declined although this was not observed when ticks were infected by inoculation. Trans-stadial survival is a hitherto overlooked parameter that may contribute to the low incidence of TBEV infection in field-collected I. ricinus ticks.