How does tick ecology determine risk?
Sarah Randolph
Department of Zoology, University of Oxford, UK
LDA, Leicester, July.2008
Tick species found in the UK
Small rodents Ixodes acuminatus Water voles Ixodes apronophorus Birds (hole nesting) Ixodes arboricola Birds (cliffs & buildings) Ixodes caledonicus Foxes, badgers (in lairs) Ixodes canisuga Birds (small passerines) Ixodes frontalis Hedgehogs (in nests) Ixodes hexagonus Birds (sand martins) Ixodes lividus All vertebrates in reach Ixodes ricinus Birds (marine, coastal) Ixodes rothschildi Birds (marine, coastal) Ixodes unicavatus Rabbits Ixodes ventalloi Bats Ixodes vespertilionis Sea birds Ixodes uriae Small rodents (in burrows) Ixodes trianguliceps Livestock Dermacentor reticulatus Tortoises Hyalomma aegyptium Birds (small migrants) Hyalomma m. marginatum Sheep, cattle, birds Haemaphysalis punctata Dogs (kennels & houses) Rhipicephalus sanguineus Pigeons Argas reflexus Bats Argas vespertilionis Sea birds Ornithodoros maritimus Adult Ixodes ricinus
1 Examples of tick-borne parasites from UK and Europe
DISEASE - medical/veterinary n VIRUSES Tick-borne Encephalitis Europe Louping ill UK n BACTERIA Borrelia burgdorferi s.l. N hemisphere (Lyme borreliosis) Francisella tularensis N hemisphere (Tularemia) 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 UK, Europe (redwater) Babesia microti UK, Europe
Adult Ixodes ricinus
Ticks as blood feeders Tick mouthparts (chelicerae and hypostome), ventral view
2 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
3 Ixodid ticks - triphasic life cycle Oviposition on ground Transovarial transmission • c.1% larvae infected 1 female 2000 eggs Vertebrate host 1 mm
10 nymphs 100 larvae • Temperature-dependent delay in transmission • Transstadial maintenance • High tick mortality Development on ground
Seasonal activity of Ixodes ricinus in Dorset, UK Larvae 7oC 10oC 1500
1000
500
0 2 1 2 3 4 5 6 7 8 9101112 1 2 3 4 5 6 7 8 9101112
500 Nymphs
300
100
1 2 3 4 5 6 7 8 9101112 1 2 3 4 5 6 7 8 9101112 Ticks counted per 100 m Ticks counted per 100 m Adults 60
40
20
0 1 2 3 4 5 6 7 8 9101112 1 2 3 4 5 6 7 8 9101112 1998 1999
4 Ixodes ricinus life cycle with typical reproductive rates, mortality rates and host relationships Competent to transmit Borrelia Reproduction
1 female + 1 male deer sheep 2,000 eggs hares c. 20% survival pheasants c. 5% survival squirrels blackbirds 10 nymphs 100 larvae rodents
c. 10% survival
Biotic variability in Lyme disease systems
q Genetic diversity of the Borrelia burgdorferi complex ÿ B. burgdorferi s.s. - arthritis - mammals ÿ B. afzelii - cutaneous disorders - mammals ÿ B. garinii - neurological symptoms - birds ÿ B. valaisiana - birds ÿ B. lusitaniae - lizards?
q Host diversity ÿ Feed different fractions of tick populations ÿ Differential transmission competence for each Borrelia genospecies
Deer feed adult ticks, but cannot transmit Borrelia
5 Epidemiology What determines variation in risk in space and time?
Increasing laboratory-confirmed cases of Lyme disease in England and Wales Estimated 1,000-2,000 additional cases diagnosed on clinical symptoms without lab-confirmation
Annual case ?? numbers Acquired in UK
Acquired abroad 18%
Passive Enhanced Improved reporting: surveillance: surveillance: specialised LD tests voluntary questionnaires offered only by the reporting sent to Lyme Diagnostic Unit, of lab-confirmed clinicians Southampton cases reporting lab- confirmed cases
6 What sort of change in which conditions? Differential increase in national mean TBE incidence from 1993
Slovenia
TBE incidence per 100,000 Czech Republic population
Estonia
Latvia
Lithuania
Network of independent but synergistic biological and non-biological factors Examples of data from Estonia, Latvia, Lithuania, Slovenia and Czech Republic.
employees LT Reduced Environmental Socio-economic industrial awareness? transition pollution output LV Global brightening ?? Decline of agriculture Higher Sudden increase unemployment in Spring temperature SI LV
1.Mar-20.Apr ES 21-30.Apr SI CZ
CZ LV CZ
More wealth & leisure SI
LV TBE cases/100,000 population wooded Increased co-feeding transmission of TBEV More hosts field crops LV Greater human for adult ticks exposure to ticks More infected ticks in forests LV CZ
LV Regeneration of Increase in rodent shrubs populations (transmission hosts)
More ticks
updated from PLoS ONE 2007 e500
7 Correlations between socio-economic factors and increases in TBE incidence across CEE countries
LT LT R2 = 0.533 R2 = 0.716
Relative increase in mean TBE incidence PL PL from 1985-90 to 1993-98
LV LV EE EE SK SI CZ SI SK CZ HU HU
Perceived poverty 2002* % of total expenditure spent on food, 1999*
n Shift from correlations in time to correlations in space - substantiates causality
Šumilo et al (2008) Revs Med Virol 18, 81-95 *Data from Heyns 2005, Ann Rev Sociol 31, 163-97
What are risk factors and who is at greatest risk?
q Survey data from Latvia, 2001:
n Unemployment and low income - significant factors pre-disposing people to m visit forests frequently m not to be protected by TBE vaccination
n Increased risk of infection with TBE virus
Šumilo, D et al (2008) Vaccine 26, 2580-8 Data source: SKDS population survey, 2001
8 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 2.8) and forest workers (x 4)
Latvia:Latvia tick monitoring site, Tireli, Riga county Ticks per km: Nymphs Adults
2002 2003
No. tick bites reported to Public Health Agency, Riga
2002 2003 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
Šumilo, D et al (2008) Vaccine 26, 2580-8 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 34 human cases recorded between 1934 and 1991
q Human Granulocytic Ehrlichiosis ÿ caused by rickettsia Anaplasma phagocytophylum ÿ same microbe that causes sheep-borne fever ÿ 2-7% I. ricinus ticks infected; >50% 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
9