How does tick ecology determine risk?

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How does tick ecology determine risk? Sarah Randolph Department of Zoology, University of Oxford, UK LDA, Leicester, July.00 Tick species found in the UK Small rodents Water voles Birds (hole nesting) Birds (cliffs & buildings) Foxes, badgers (in lairs) Birds (small passerines) Hedgehogs (in nests) Birds (sand martins) All vertebrates in reach Birds (marine, coastal) Birds (marine, coastal) Rabbits Bats Sea birds Small rodents (in burrows) Livestock Tortoises Birds (small migrants) Sheep, cattle, birds Dogs (kennels & houses) Pigeons Bats Sea birds Ixodes acuminatus Ixodes apronophorus Ixodes arboricola Ixodes caledonicus Ixodes canisuga Ixodes frontalis Ixodes hexagonus Ixodes lividus Ixodes ricinus Ixodes rothschildi Ixodes unicavatus Ixodes ventalloi Ixodes vespertilionis Ixodes uriae Ixodes trianguliceps Dermacentor reticulatus Hyalomma aegyptium Hyalomma m. marginatum Haemaphysalis punctata Rhipicephalus sanguineus Argas reflexus Argas vespertilionis Ornithodoros maritimus Adult Ixodes ricinus

Examples of tick-borne parasites from UK and Europe DISEASE - medical/veterinary n VIRUSES n BACTERIA Tick-borne Encephalitis Louping ill Borrelia burgdorferi s.l. (Lyme borreliosis) Francisella tularensis (Tularemia) Europe UK N hemisphere N hemisphere n RICKETTSIA Anaplasma phagocytophilum UK, Europe (Tick-borne fever) (Human Ehrlichiosis) Rickettsia conori S Europe (Med spotted fever) Coxiella bourneti (Q fever) Europe n PIROPLASMS Babesia divergens (redwater) Babesia microti UK, Europe UK, Europe Adult Ixodes ricinus Ticks as blood feeders Tick mouthparts (chelicerae and hypostome), ventral view

Tick mouthparts, front dorsal view Chelicera for cutting thro skin Hypostome for sucking up blood Backwardly pointing teeth for gripping Ticks as vectors No wings n Very immobile n Only feed once per life stage - larva, nymph, adult

Ixodid ticks - triphasic life cycle Oviposition on ground Transovarial transmission c.% larvae infected female 000 eggs Vertebrate host mm 0 nymphs 00 larvae Temperature-dependent delay in transmission Transstadial maintenance High tick mortality Development on ground Seasonal activity of Ixodes ricinus in Dorset, UK Larvae 0oC oc 00 000 Ticks counted per 00 m 00 0 00 0 0 0 0 0 0 Nymphs 00 00 Adults 0 0 0 0

Ixodes ricinus life cycle with typical reproductive rates, mortality rates and host relationships Competent to transmit Borrelia Reproduction c. 0% survival female + male 0 nymphs deer sheep hares pheasants squirrels blackbirds rodents,000 eggs 00 larvae c. % survival c. 0% survival Biotic variability in Lyme disease systems q Genetic diversity of the Borrelia burgdorferi complex ÿ B. burgdorferi s.s. - arthritis ÿ B. afzelii ÿ B. garinii ÿ B. valaisiana ÿ B. lusitaniae q Host diversity - cutaneous disorders - neurological symptoms ÿ Feed different fractions of tick populations ÿ Differential transmission competence for each Borrelia genospecies - mammals - mammals - birds - birds - lizards? Deer feed adult ticks, but cannot transmit Borrelia

Epidemiology What determines variation in risk in space and time? Increasing laboratory-confirmed cases of Lyme disease in England and Wales Estimated,000-,000 additional cases diagnosed on clinical symptoms without lab-confirmation Annual case numbers?? Acquired in UK Acquired abroad % Passive surveillance: voluntary reporting of lab-confirmed cases Enhanced Improved reporting: surveillance: specialised LD tests questionnaires offered only by the sent to Lyme Diagnostic Unit, clinicians Southampton reporting labconfirmed cases

What sort of change in which conditions? Differential increase in national mean TBE incidence from Slovenia TBE incidence per 00,000 population Czech Republic Estonia Latvia Lithuania Network of independent but synergistic biological and non-biological factors Examples of data from Estonia, Latvia, Lithuania, Slovenia and Czech Republic. Socio-economic transition employees LT output Reduced industrial pollution Environmental awareness? Global brightening?? Decline of agriculture Higher unemployment SI Sudden increase in Spring temperature SI wooded field crops More wealth &leisure Greater human exposure to ticks in forests TBE cases/00,000 population SI More infected ticks.mar-0.apr Increased co-feeding transmission of TBEV More hosts for adult ticks ES -0.Apr Regeneration of shrubs Increase in rodent populations (transmission hosts) More ticks updated from PLoS ONE 00 e00

Correlations between socio-economic factors and increases in TBE incidence across CEE countries R = 0. LT R = 0. LT Relative increase in mean TBE incidence from -0 to - PL PL SI SK HU EE SI HU SK EE Perceived poverty 00* % of total expenditure spent on food, * n Shift from correlations in time to correlations in space - substantiates causality Šumiloetal(00) Revs Med Virol,,- *Data from Heyns 00, Ann Rev Sociol, - What are risk factors and who is at greatest risk? q Survey data from Latvia, 00: n Unemployment and low income - significant factors pre-disposing people to m visit forests frequently m nottobeprotectedbytbevaccinationto by n Increased risk of infection with TBE virus Šumilo,Detal(00)Vaccine,0- Data source: SKDS population survey, 00

Human-tick contact rates influenced by human behaviour and weather q Mushroom or berry collecting is most common purpose of frequent forest visits n Principal reason for women, older, less educated, unemployed, pensioners, low earners n Risk of tick bite highest for mushroom collectors (x.)andforestworkers(x) Ticks per km: Nymphs Adults Latvia: tick monitoring site, Tireli,, Riga county 00 00 No. tick bites reported to Public Health Agency, Riga 00 n Mushrooms grow best when it rains n Dry weekends following week with heavy rainfall (l):( tick bites more common when weather favours mushroom harvest, independent of tick abundance 00 Šumilo, D et al(00) Vaccine, 0- Data source: Public Health Agency of Latvia Other tick-borne infections of humans in UK transmitted by I. ricinus q Louping ill ÿ caused by virus of tick-borne encephalitis group ÿ common infection of sheep and grouse ÿ human cases recorded between and q Human Granulocytic Ehrlichiosis ÿ caused by rickettsia Anaplasma phagocytophylum ÿ same microbe that causes sheep-borne fever ÿ -% I. ricinus ticks infected; >0% roe deer sero-+ve q Babesiosis ÿ Babesia divergens causes red-water in cattle ÿ Babesia microti circulates amongst rodents ÿ sporadic human cases recorded - splenectomy is risk factor ÿ increasing incidence in USA