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EC Wildlife Conference 5th May 2015

WHEN Foot-and-Mouth Disease GOES WILD

It forces a rethink - and demands new approaches

Keith Sumption (EuFMD) Sergei Khomenko, Sinan Aktas, Daniel Beltran (FAO), Tsviatko Alexandrov (BFSA), Naci Bulut (SAP, Ankara) Foot-and-Mouth Disease (FMD) and wildlife

 FMDV extremely infectious – and rightly feared

 EU is recognised as free - also the European part of (Thrace)

 Even a single small outbreak in Europe is extremely damaging (100 m €+, to countries if involved in extensive trade).

Foot-and-Mouth Disease (FMD) and wildlife

 Short lived period of infectivity (hit and run agent) : (NB carcasses may aid persistence))  Domestic and wild easily infected by oral route and shed very large quantities of virus  WIDE Range of wildlife can be infected ( mainly by aerosols)  European wildlife species susceptible: , all species, , , ibex,…(hedgehogs)  Natural reservoir in (long term carriers), probably original host before adaptation in evolution to /other species  Wildlife might acquire from domestic /carcasses of dead wildlife (gazelle-wild boar cycle ) Experimental • incubation period 4 days; • most severe and evident lesions infection of wild – 7th Day PI; • Viraemia: 1 DPI through at least boar 9 DPI; • NSP antibodies detected 7-8 DPI; • Virus RNA in saliva normally found up to 14 DPI and up to DPI 24 DPI (intermittently). • Later and less severe signs than domesticated pigs

CREDITS: A. Breithaupt, K. Depner, B. Haas, M. Beer (FLI – Federal Research Institute for Health Institute of Diagnostic Virology) 1*1 km + = resolution density data product

If wild boar important as natural long term reservoir might expect intra- and inter-regional spread of FMDV strains through wildlife - No evidence

Khomenko, Robinson, Gilbert (in prep.) Historical range of Sus scrofa FMD in wild boar:

1. Caucasus 1902 1908 1911 2 1917 5 1919 1925

2. Kazakh- 1927 1 stan 1931 1941 3 2011 ? 4 3. Kyrgyz- 1953 stan

4. Israel 1987- 1999 2007 2011 ?

5. Europe 1920s? 2011 Marek & Hutÿra, 1931; Sludskiy, 1956; Danilkin, 2002 Foot-and-Mouth Disease and European wildlife

Until 2011  No evidence of wildlife involvement in the recent major epidemics in Europe 1920s-2007  It was assumed wildlife will have limited role in domestic FMD outbreaks (spillovers of limited consequence)

SHOCK !!!! FMD in Bulgaria- 2011  Detected first in hunted wild boar  lab staff familiar with FMD  Lesions along coronary band  FMDV detected and reported bovines 194 South East Bulgaria 2011 117 149 Kosti – the village of the bones. pigs 72 Index Case

30th Dec 2010: wild boar shot nr Kosti - with lesions 9h January – 7th April: 11 outbreaks in domestic animals Two main foci separated in time and space FAO-EU FMD /EC/OIE Tripartitt Group Meeting,Plovdiv, Bulgaria, 25 March,2011 ------

FAO-EU FMD /EC/OIE Tripartite Group Meeting, Plovdiv, Bulgaria, 25 March,2011 Bulgarian FMD epidemic: many missing links between the waves of domestic animal cases

Secon Phase/wave March -April

Goliamo Black Sea Bukovo

Fakia Granichar Kirovo

Kosti

Wild boar First phase/wave January/February Rezovo

Turkey FMD virus genome sequencing: evidence for undetected transmissions – did these occur in wild life? Credit: Begoña Valdazo-Gonzalez, Nick J. Knowles, Donald P. King

30/12/2010 BUL/1/2010 Wild boar 02/2011 8 nt changes 12LPN1 Kosti 02/2011 4 nt changes 14 nt changes 12LPN3

Rezovo 6 nt changes BUL/11/11 26/07/2010 changes

Kirovo nt

(Bursa) 19/03/2011

31 4 nt changes

TUR/926/2010 28/03/2011 BUL/26/11 13 nt changes 28/03/2011 Granichar BUL/20/11 11 nt changes BUL/30/11 Golyamo Fakia Bukovo 01/04/2011 Putative common ancestor of Bulgarian wild board and first phase of the outbreaks Putative common ancestor of the second phase of the Bulgarian outbreaks FMD antibody +ve Wild Boar in Thrace Problems – the FMD epidemic in Thrace • Entry of infection to free region - unable to prove if started in wild animals or domestic • Duration of epidemic in domestic stock: 4 months • Total period to regain freedom : 17 months (UK 2001, 11 months) • Extremely difficult to prove freedom when wildlife have been shown to be involved • Issues between neighbouring countries re: wildlife – fear of being infection being driven across borders

EFSA, 2012; Alexandrov et al (in prep.), Dhollander et al (in prep.) Modelling of the Thrace epidemic (EFSA Opinion 2012, Lange 2012) : suggested wildlife alone in this area will not maintain infection but timescales are NOT comforting (duration ~1-4 years, 80 km radius). Note: WB density 2.2/km Every day lost to FMD costs €€€ in lost trade.

Duration: B – Boar, D- deer. B+D = Distance of spread from origin mixed species model Conclusions – the FMD epidemic in Thrace

Very well analysed and reported in the EFSA Opinion (10) 4, : 2635, 2012 Epidemiologically: – Fade –out in wildlife within months – between livestock and wildlife was both ways (facilitated by humans?); – Disease event in wildlife developed in winter and died away end of spring – NOT highest density wildlife and domestic interactions in Europe – longer persistence elsewhere??? On surveillance – Hunting or trapping wild boar – problematic, severe limitations – Antibodies in wildlife do not indicate WHEN infection occurred – Far more intensive sampling of wildlife (for active infection) needed than possible – Early detection (~1 month after introduction) needs 59 shot per week throughout year)* – Tragetted, risk based surveillace needed- but how?

Research supported by DG-SANTE through EuFMD, 2011-15

1. How frequent are FMD spill-overs to wild boar? Studies in Turkey (Anatolia, 2011-12) 2. Tracking wild boar movements – tools for potential in epidemic situations 3. Development of non-invasive approaches to survey wildlife without capture/killing (2012-15)

Surveillance in wild boar for FMD 2011- 2012 ANATOLIA (TR) Dec 2011 – Feb 2012 N=252

THRACE (BG+TR) Jan 2011 – Jan 2012 N=1004 Sero-positivity to FMDV

Thrace (epidemic O) versus Anatolia (endemic O, A, Asia)

AGE THRACE ANATOLIA GROUP n NSP+ (95 % CI), % n NSP+ (95 % CI), % P

ADULT 628 9.1 (6.9 – 11.6) 185 24.9 (18.3 - 32.4) <0.05

JUVENILE 358 5.6 (3.4 – 8.5) 67 7.5 (2.5 - 16.6) ns

ALL 1004 7.8 (6.2-9.6) 252 20.2 (15.5 - 25.7) <0.05

NO DIFFERENCE BETWEEN SEXES FOUND, ONLY BETWEEN AGES Implications for disease surveillance and control

1. FMD spillover to wild boar is a frequent event 2. Infection in WB correlates with disease occurrence in livestock, particularly in SR. 3. Spillovers may develop into localised epidemics (3-6 months) affecting up to 20 % of the population and virus spread for to 15-20 km 4. Winter is most risky period for horizontal transmission of FMD in wild boar population; 5. Different serotypes may perform differently in wild boar. Telemetry project

Strandzha – 4 (2) Tutrakan – 15 (7) • 20 GPS/GSM Tellus collars (1 year – 24 fixes a day); • 19 animals collared, 16 collars used (6 reused), 4 were BULGARIA destroyed / failed, 1 lost; • Sex, age, and seasonal variation in home ranges; • Individual movements and group interactions in a small population (70 animals) to simulate disease spread.

http://www.followit.se/wildliferesearch.html

Tracking: year round study. Animals send multiple SMS per day on their locations Valuable insights on potential spillovers – but very hard to use in a crisis 4-year male, 1 Jan - 22 March – 894 positions –a total of 338 km

Crossed Danube into Romania one occasion Development of natural sampling methods Chichikin et (“non-invasive”) al, 2012 • Saliva contains pathogens of interest • Uses baits attractive to animals to chew/suck • Aims at early detection of pathogen, but might work for antibody • No killing of animals involved (repeated sampling, cost effectiveness, logistical simplicity) • Proof of concept studies - 2012

EXPERIMENT WITH A TAME WILD BOAR EASY TO INCORPORATE ANY SWABS INTO

6 1

7 2

8 3

SUITED FOR COMMERCIAL FEEDERS 9 4

10 5 Non-invasive sampling for FMD – method optimisation  Optimised tests or virus (PCR)  Comparison of bait (pSWAB) and Q-Tips in maize cobs  Comparable sensitivities  Detection of FMDV days 1 to 9 (experimental infection pigs)  Promising stability (for field use) Studies commissioned by EuFMD at FLI, Insel Riems, 2014: Putting it together : promising options for surveillance and control of FMD epidemics in wildlife

1. Use risk based, non- invasive methods for DETECTING spread into wildlife

Risk based, where spill over or incursion expected

May require feeding wild boar – prelude to NI sampling in risk locations 2. Manage: natural territoriality and anticipated local movements. Avoid dispersion peace time or crisis.

From Telemetry studies Escaping in BG: hunting • WB normally small home ranges 5-30 km2 Daytime (more during hunting) • Very boring schedules 

Nighttime • Disrupted by only food availability or disturbance Future farrowing • Individuals may switch area home ranges repeatedly 1 hour resolution movements of a tracked wild boar sow in Bulgaria Use local expertise on expected local movements

Young male Movements January dispersal of males and rut

Farrowing

Pre- hunting stock

Re- unification Movements of female to crops & groups food-rich June areas 3. Put this into Contingency Plans - use of feeding sites and non-invasive measures if infection detected

Consider:  Integrated approach  Use of feeding programmes to encourage bait use and avoid dispersion  Use of feeding sites to accelerate natural process of infection and recovery (natural immunity, shorter duration epidemic)  Risks  Advantages- active use of options for non- invasive surveillance to monitor impact of controls ANIMO Active, Non-Invasive Management of Outbreaks Suite of approaches including NI sampling and Accelerated Natural Immunity (ANI)

Detect

Manage

Prove free Infection in one hunting area but Natural spread? not another: example of natural Antibody positive “local burn out””controlling animals in more than spread? one area… 1. Low density feeding is used throughout the risk period; 2. FMDV detected through NI surveillance; ANIMO - 3. Hunting suspended & over feeding applied; 4. Increase transmission rate and fragment population; FUTURE FMD 5. Disease fades out and natural herd immunity will prevent further local spread( +useful immunity vs re- management introduction from domestic cycle); 6. Use NI sampling for evidence for local virus extinction scenario 7. Repeat cycle as needed

State border Feeding stations:

a)Early NI detection b)Population High risk of FMD introduction (e.g. Thrace, Caucasus) management The way ahead: an integrated approach?

Contingency planning to protect wildlife populations and minimise impact if overspill occurs Operationalise plans to 1. Prevent - reduce spillovers from domestic animal infections  Risks practises identified, targetted measures/communication 2. Manage epidemics in wildlife more actively :  Part of FMD contingency planning (not only domestic!)  ANIMO approach – including NI sampling of wildlife and ANI (accelerated natural immunity) 3. Recover : Use NI (non-invasive) sampling to prove freedom

ANIMO approaches need optimisation and testing in the field – options in Turkey , Caucasus and parts of mid-east for FMD Thank you

Acknowledgement: the support that was provided rapidly from DG-SANTE through the EuFMD Research Fund to enable these studies. The Government of Turkey for positive, continuous support to field work.

Don’t Forget!

In Europe:

20 – 22 million FMD susceptible ungulates after reproduction