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Fragile Transmission Cycles of Tick-Borne Encephalitis Virus May Be Disrupted by Predicted Climate Change

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Fragile Transmission Cycles of Tick-Borne Encephalitis Virus May Be Disrupted by Predicted Climate Change doi 10.1098/rspb.2000.1204 Fragiletransmissionc yclesof tick-borne encephalitisvirusmaybedisruptedbypredicted climatechange Sarah E.Randolph * and David J.Rogers Department of Zoology,University of Oxford, SouthP arks Road, Oxford OX13PS, U K Repeatedpredictions that vector-bornedisease prevalencewill increase withglobal warming are usually basedon univariatemodels. T oaccommodatethe fullrange of constraints, the present-daydistribution of tick-borneencephalitis virus (TBEv) was matched statistically tocurrent climatic variables,to provide a multivariatedescription of present-day areas of disease risk.This was then appliedto outputs ofageneral circulationmodel that predicts howclimatic variablesmay change in the future, andfuture distributions ofTBEv were predicted forthem. Theexpected summer rise intemperature anddecrease inmoisture appearsto drive the distributionof TBEv into higher-latitude and higher-altitude regions progressively throughthe 2020s,2050s and 208 0s.The ¢ naltoe-hold in the 2080smay be con¢ ned to a small partof Scandinavia,including new foci in southern Finland. The reason for this apparentcontraction of the rangeof TBEv is that its transmission cycles dependon a particularpattern oftick seasonal dynamics, whichmay be disrupted byclimate change.The observed marked increase inincidence of tick-borne encephalitisin most parts ofEuropesince 1993may be dueto non-biological causes, such aspoliticaland sociologicalchanges. Keywords: ticks; tick-borneencephalitis; global warming ;climate matching;risk maps the winter withminimum temperatures below 712 8C. 1.INTRODUCTION Further south,in areas with medium tohigh tick densi- Tick-borneencephalitis (TBE) ,causedby two subtypes of ties, further increases intick abundance were related to a £avivirus(TBEv) transmitted bythe ticks Ixodes ricinus combinationof milder winters (fewer dayswith minimum and I.persulcatus ,is the most signi¢cant vector-borne temperatures below 7 7 8C)and extended spring and disease inEurope and Eurasia. Central nervous system autumnseasons (more dayswith minimum temperatures pathologycauses acase morbidityrate of1 0^30%and a of 5^8 8C).Usingthe excellentnational registration of case mortalityrate oftypically1^2% but as highas 24% TBEcases inSweden since the 1950s,Lindgren ( 1998 b) inthe FarEast (ImmunoAg 1997).Priorto 1 992,infec- related the increase inTBE incidence from 1 960to1995 tionincidence was typically 2^40% in endemic areasbut inStockholm County ,ahigh-endemicregion, to higher since 1993TBE cases haveincreased two -to1 7-foldin winter temperatures permitting aprolongedseason of tick manyparts ofEurope (Immuno Ag1 997;Su « ss & Kahl activityand hence pathogen transmission. Here the major 1997;S.Dittman andW .Jilg,unpublished data) and new increase occurredfrom 1984 onwards: 1 960^1983,mean focihave been identi¢ ed. TBE is atypicalzoonosis, with annualcases 18.6(range 6^36); 1 984^1995,mean annual enzooticcycles maintainedin natural rodent ^tick cycles cases 45.1(range33^74) . (Labuda& Randolph1 999);humans may be infected if Events atthe extreme limit ofan organism’ sdistribu- accidentallybitten byan infected tickor by drinking tion,however ,maynot re£ ect future events atthe coreof untreated milkfrom infected sheep orgoats (which the range.In Europe, TBEv is highlyfocal in its distribu- cannotthemselves pass the virusto ticks) (Labuda et al. tion,limited toa well-de¢ned region in central Europe, 1997).Increased risk tohumans may therefore arise in wherethe distributionis verypatchy ,anda quasi- three ways:(i) improvedconditions for natural trans- separateregion covering the Balticstates andthe south- mission cycles resulting inhigher densities ofinfected eastern rim ofScandinavia, where the distributionis ticks; (ii) changedhuman behaviour resulting ingreater more continuous(¢ gure 1 ).Thispattern hasbeen exposureto ticks; and(iii) changedagricultural practices predicted with85% accuracy from satellite-derived data resulting ina higherconsumption of rawmilk. As bothof onenvironmental conditions (Randolph 20 00)and its the ¢rst twofactors are climate dependent,TBEv is biologicalbasis is nowclearly understood. The reason includedin the list ofvector-borne pathogens anticipated TBEvoccurs inonly a narrowsubset ofsuitabletick habi- tobecome more ofa threat tohumans in a predicted tats is becauseits cycles aremaintained by transmission warmerworld (Lindgren 1998 a;Martens 1999). ofnon-systemic infectionsbetween infected nymphsand Onlyin Sweden has this predictionbeen explicitly uninfectedlarval ticks co-feedingon small rodenthosts, tested forTBEv .Lindgren et al.(2000)showed that the principallymurids (Labuda et al.1993).Theforce of northwardexpansion of the geographicalrange of transmission is su¤ciently high only when there isahigh I. ricinus (Talleklint& Jaenson1 998)between the early degreeof coincident feeding of larval and nymphal ticks 1980sand the mid-1990swas related to fewer days during (Randolph et al.1999).Thisdepends on a particular pattern ofseasonal tick-population dynamics determined *Author forcorrespondence (sarah.randolph@zoology .ox.ac.uk) byrather precise climatic conditions,speci¢ cally the Proc. R.Soc.Lond. B (2000) 267, 1741^1744 1741 © 2000The RoyalSociety Received 2 March 2000 Accepted 25 May 2000 1742S. E. Randolphand D .J. Rogers TBE virus transmission disrupted by climate change pointswithin themapped limits of TBEv (Immuno Ag 1 997) and60 0pointsoutside, but within 8 8 oflongitudeor latitude of, thelimits. Data for each point were derived from 30-year (1960^1990)average monthly climate surfaces at 0.5 8 longitude andlatitude resolution (New et al.1999)for the mean ( TM), maximum (TX)andminimum ( TN)temperature,rainfall ( R) andsaturation vapour pressure (SVP) variables. These surfaces werepre-processed by temporal F ourieranalysis (Rogers et al. probability 1996)of themonthly data (essentially smoothing the data) ,from 0.65–1.0 which themean, maximum and minimum of each variable were 0.55–0.649 extractedfor each training-set location. Data were ¢ rstclustered 0.50–0.549 0.45–0.499 using the `k-meanscluster’ option of SPSS (SPSS,Inc., IL, USA) , 0.35–0.449 producingthree clusters each for presence (p) and absence (a) 00–0.349 observed sites.Stepwise discriminant analysis (Rogers et al.1996)of the resultingsix clusters, using the criterion of maximizing the Figure1. The present-daydistribution of tick-borne Mahalanobisdistance between all pairs of dissimilar(i.e. p toa encephalitisvirus in Europe(yellow hatched polygons) and anda top) clusters, chose the minimum TN, minimum TX, distributionpredicted using maximum-like lihoodmethods mean TX, maximum TM andmaximum SVP as the ¢ vemost basedon 1960^1990average monthly climate surfaces (red importantdiscriminating variables for describing the current togreenposterior probability scale in key).Training-set western-typeTBEv situation (¢ gure 1 ).Onlythese, which areall predictions( 4 0.5probability) 86% correct, 12% false consistentwith theresults of the predictive mapping based on positivesand 2% falsenegatives. satellite-deriveddata ( Randolph200 0),wereused to make the predictivemaps of posteriorprobabilities ( Rogers et al. 1996) on seasonalland-surface temperature pro¢le (Randolph ascaleof 0.0(red in ¢gure1 )to1.0 (green) . 2000;Randolph et al.2000).Itmust behotenough in the The resultsof the above exercise were applied to GCM summer toallow rapid tick development, especially of the scenarios( Johns et al.1997)to produce predictions for the eggs,but cooldown rapidly in the autumnto send the future,i.e. the covariance matrices from the present-day emergent larvaeinto behavioural diapause over the climate-matchingexercise were used to identify places where winter.Inthis way,larvaeand nymphs become active in conditionsfor TBEv presence or absence will occurin the synchronyin the springand e¤ cient virustransmission is future.The futureclimate scenarios have been constructed for achieved.At the same time, moisture availabilityto ticks low, medium^low, medium^highand high degrees of change onthe ground,as measured bya remotelysensed vegeta- projectedto the 2020s, 2050s and 2080s, at an original spatial tionindex, must besu¤cient toensure goodtick survival. resolutionof 3.75 8 longitudeand 2.5 8 latitude,but then spatially Likemany vector-borne pathogen cycles that depend interpolatedusing cubic splines to give the same resolution as onthe interactionof so many biotic agents with each thelong-term past climate data sets. GCM predictionsare given other andwith their abioticenvironment, enzootic cycles asthechange from the modelled present to the modelled future ofTBEv have an inherent fragility.Theircontinuing climateand, following standard practice, these values are added survivalor expansion cannot be predicted fromsimple tothe present observed climate averages to predict the future. univariatecorrelations. Ideally ,robust biologicalmodels Forexample, the 2050s `high’ scenario from the HadCM2 areneeded to capture the complexityof such systems. The experiment(http:/ /www.met-o¤ce.gov .uk/sec5/sec5pgl.html)pre- quantitativebiological information needed to give an dictsmean global land surface changes of + 3.45, + 3.63 and accuratedescription of eventhe current situationis notyet + 3.29 8Cin mean,minimum and maximum temperatures, available,however ,sothis approachcannot yet be used to + 1.87hpa for SVP and + 0.127 mm day71 forprecipitation by givereliable predictions about the future. Instead,we here 2050.These ¢ gurestake account of the greater rise in tempera-
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