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Surveillance of foot-and-mouth disease (FMD) in susceptiblewildlife and domestic ungulates in Southeast of Bulgariafollowing a FMD case in wild boar

Tsviatko Alexandrov a, Dimitar Stefanov b, Pencho Kamenov a,Alexandra Miteva a, Sergei Khomenko c, Keith Sumption d,Hinrich Meyer-Gerbaulet e, Klaus Depner f,*a Animal Health & Welfare Directorate, Bulgarian Food Safety Agency, 15 A Pencho Slaveikov Blvd, 1606 Sofia, Bulgariab Regional Veterinary Office, 50 Silistra Street, 7600 Tutrakan, Bulgariac Food and Agriculture Organization of the United Nations (FAO), Viale delle Terme di Caracalla, 00153 Rome, Italyd European Commission for the Control of Foot-and-Mouth Disease, Viale delle Terme di Caracalla, 00153 Rome, Italye Federal Ministry of Food, Agriculture and Consumer Protection, Rochusstraße 1, 53123 Bonn, Germanyf Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Sudufer 10, D-17493 Greifswald – Insel Riems, Germany

1. Introduction

The first index case of foot-and-mouth disease (FMD)in wildlife in the European Union (EU) was reported in

south-east Bulgaria beginning of January 2011. It was astrong solitaire four-year old male wild boar (Sus scrofa),shot in Strandzha mountain, 2 km north of the Turkishborder in the municipality of Tsarevo (Region of Burgas).The animal showed about 14 days old FMD lesions on allfeet. Two additional wild boar shot on the same day but inthe neighbouring hunting ground were not affected.During the following four months eleven FMD outbreaksaffecting cattle, buffalos, sheep, goats and pigs were

Veterinary Microbiology 166 (2013) 84–90

A R T I C L E I N F O

Article history:

Received 7 January 2013

Received in revised form 6 May 2013

Accepted 22 May 2013

Keywords:

Foot-and-mouth disease

Surveillance

Wild boar

A B S T R A C T

Following a foot-and-mouth disease (FMD) case of serotype O in wild boar in Southeast of

Bulgaria, notified in January 2011 and eleven FMD outbreaks in livestock, a control and

eradication plan according to the EU legislation was implemented. Based on the

epidemiological considerations a ‘‘Cordon Sanitaire’’ along the border to Turkey, consisting

of a defined infected area (1240 km2) and two areas of risk (2160 km2) was established.

Within these areas a total of 812 wild boar, 68 roe deer, 7 red deer and 2 mouflons, hunted

between February 2011 and January 2012, were tested for the presence of FMD. No FMD

virus could be detected. Seropositive animals were found in wild boar (6.9%) and roe deer

(4.4%), most of them spatially clustered around the FMD outbreaks in livestock, limited

within a radius of 20 km.

The outbreaks in domestic ungulates were controlled in the framework of EU

legislation, including stamping out, standstill and no use of vaccination. All villages within

the Cordon Sanitaire were examined for the presence of FMD according to the control and

eradication plan. Neither clinical signs nor seroconversion was detected and the region

could regain its status of FMD freedom without vaccination.

The relatively low seroprevalence and clustered spatial distribution of seropositive

wild boar and roe deer suggest that the FMD infection in wildlife was mainly a short living

event, which failed to develop into a large scale epidemic.

� 2013 Elsevier B.V. All rights reserved.

* Corresponding author. Tel.: +49 38351 71268.

E-mail addresses: [email protected],

[email protected] (K. Depner).

Contents lists available at SciVerse ScienceDirect

Veterinary Microbiology

jou r nal h o mep ag e: w ww .e ls evier . co m/lo c ate /vetm i c

0378-1135/$ – see front matter � 2013 Elsevier B.V. All rights reserved.

http://dx.doi.org/10.1016/j.vetmic.2013.05.016


notified in several villages nearby (OIE, 2011) (Fig. 1). Adetailed analysis of the full genome sequences of theisolated viruses has been described by Valdazo-Gonzalezet al. (2012).

According to Article 85(3) of Council Directive 2003/85/EC, Bulgaria had to prepare and implement a surveillanceand eradication plan for FMD with the aim to prevent thespread of the disease out of the affected area and to limitthe number of outbreaks within the area. However, since itwas the first FMD case in wildlife in the EU, only the controlplans for classical swine fever in wild boar and the generalprovisions in Annex XVIII to Directive 2003/85/EC wereavailable as a blueprint for setting up such a programme.Additionally, insight had to be obtained about theoccurrence and the dynamic of FMD in wildlife and therelative significance of – and the role played by – wild andferal bi-ungulates, notably wild boar and deer species (roedeer Capreolus capreolus, red deer Cervus elaphus) andmouflon (Ovis musimon).

The persistence of FMD in a wildlife population dependson multiple epidemiological and ecological factors, such asspecies composition and density of the animals, theproportion of individuals that recover from the infection,the possible occurrence of carrier animals, the socialstructure, population size, environmental conditions, aswell as human activities as hunting and free rangelivestock breeding (Kramer-Schadt et al., 2007; Ruiz-Fonset al., 2008; EFSA, 2012a,b). With all these uncertaintiesonly a thoroughly designed surveillance scheme can helpto understand the disease situation in wildlife, analyse it,

at least retrospectively, and eventually identify risks ofFMD introduction originating from wildlife reservoir.

In this paper we present and evaluate results of the FMDsurveillance activities in wildlife and domestic ungulatesconducted by the Bulgarian Veterinary Authority during2011/2012 as a part of the effort to control and eradicateFMD in the affected area. The results may also help tounderstand the epidemiological role of wildlife, notablywild boar in the FMD dynamics in general, a problem thathas been long recognized, but rarely addressed throughsystematic surveillance studies (EFSA, 2012a,b).

2. Materials and methods

2.1. Surveillance area

The design of the FMD control and eradication plan hadto take into consideration the estimated wildlife popula-tion as well as the geographical and agricultural particula-rities of that region. Furthermore the close vicinity of theaffected region to Turkish Thrace had to be consideredwhere the FMD situation in wildlife, particularly in wildboar was unknown and potential virus incursion viainfected wild boar could not be excluded at that point oftime. This assumption was based on the genotyping resultsof the Bulgarian FMD virus isolate which showed closerelationship with FMD virus isolates from the Asian part ofTurkey (Valdazo-Gonzalez et al., 2011).

The affected region is a mountainous forest areainhabited by a rich susceptible wild and feral fauna; an

Fig. 1. Locations of the shot FMDV positive wild boar and the 11 outbreaks in domestic livestock within the surveillance area comprising sampling areas A, B

and C and the East-Balkan pig herds.

T. Alexandrov et al. / Veterinary Microbiology 166 (2013) 84–90 85


eco-system allowing outdoor free ranging of cattle, sheep,goats and pigs throughout the year with conditionsfavouring frequent direct and indirect contacts betweenlivestock and wildlife. The holdings are of a family andbackyard type and only few herds have more than 100animals. Livestock density (mainly small ruminants) isvery low and owners are generally not involved inindustrialized animal production and national or interna-tional trade. Most of the animals graze at the communalgrounds around the villages throughout the year and arekept for own consumption or for the local/regional market.

Based on the above mentioned epidemiological con-siderations a defined infected area (area A) and two riskareas (B and C) were established (Fig. 1). Area A is a 20-km-wide region along the Turkish border in southeast Bulgaria,which covers about 1240 km2. Areas B and C are coveringtogether about 2160 km2. It was assumed that in area Avirus might circulate in the wild boar population and/orother susceptible wild species and could escape to theneighbouring areas B and C. All three areas where thoughtto function as a protection area named ‘‘Cordon Sanitaire’’to block further spread of FMD to other parts of Bulgaria.

The estimated number of susceptible wild anddomestic ungulates within the surveillance areas (A, B,C) is shown in Table 1. The wild boar was the mostabundant species with in average 0.9 animals/km2 (vary-ing between 0.43 and 2.14 animals/km2), followed by roedeer with 0.7 animals/km2 (0.57–1.48) and red deer with0.3 animals/km2 (0.24–0.7).

2.2. Surveillance scheme

The surveillance in wildlife was conducted fromFebruary 2011 to January 2012. Samples were taken eitherfrom hunted or trapped (Alexandrov et al., 2011) animals.The sampling strategy was similar to that proposed formonitoring of classical swine fever (CSF) in wild boarpopulations (EFSA, 2009). Minimum sample sizes for wildboar were set at 59 animals for each of the areas A, B and C.For each of the wild ruminant species (roe deer, red deerand mouflon) sample sizes were set at 35 animals. Thesewould allow for detecting 5% and 10% sero-prevalence ineach of the areas (A, B and C) with 95% confidencerespectively. Blood samples for serological tests and tissuesamples (pharyngeal area and lymph nodes) for virusdetection were collected from both, hunted and trappedanimals.

A total of 812 wild boar, 68 roe deer, 7 red deer and 2mouflons were sampled. Table 2 shows the monthlydistribution of samples in the different species and ageclasses. Most samples were collected from October 2011through January 2012, except for 127 animals hunted ortrapped in spring and summer 2011.

In addition, 4709 carcasses of wild boar shot on thewhole of the territory of Bulgaria during the huntingseason 2011–2012 (Oct–Jan) were investigated by veter-inarians or trained hunters for visible lesions or signs ofcontagious diseases.

Surveillance in domestic livestock was conducted in all106 villages in the surveillance area. All holdings werevisited every 21 days by a team of veterinarians and allsusceptible animals were clinically examined in accor-dance with Annex III to Council Directive 2003/85/EC(European Commission, 2003). Routine blood sampling forserological tests was conducted every third month. Theminimum number of animals to be sampled in anepidemiological unit (village) had to allow the detectionof at least one sero-positive animal based on theassumption that the sero-prevalence is 5% with aconfidence of 95%.

In addition clinical and serological surveillance wascarried out in East-Balkan pig herds outside of the ‘‘CordonSanitaitre.’’ East-Balkan pigs are a national Bulgarian pig

Table 2

Numbers of wild animals tested monthly in the course of surveillance campaign in Bulgaria during the period from February 2011 to January 2012 by

species and age groups.

Species Age group Months, 2011 2011 total 2012 Grand total

2 3 4 5 6 7 8 9 10 11 12 1

Wild boar Adult 5 11 22 7 142 162 160 509 29 538

Juveniles 1 2 30 11 63 93 50 250 7 257

NA 17 17 17

Total 5 12 2 0 52 18 222 255 210 776 36 812

Roe deer Adult 1 5 17 13 4 17 9 66 66

Juveniles 1 1 2 2

Total 1 5 0 17 13 5 18 9 68 68

Red deer Adult 2 3 1 1 7 7

Mouflon Adult 2 2 2

All 4 species Total 6 17 2 0 71 31 3 230 273 220 853 36 889

Table 1

Estimated number of susceptible ungulates within the surveillance areas

(A, B, C).

Susceptible

ungulates

Area A Areas B and C

Animals Villages/

herds

Animals Villages/

herds

Wild boar 1900 2650

Roe and red deer 1900 3600

Cattle 1370 32/491 7303 74/3033

Buffalo 117 59

Sheep 12,975 31,227

Goats 4047 11,549

Pigs 734 2405

T. Alexandrov et al. / Veterinary Microbiology 166 (2013) 84–9086


breed reared outdoor in several herds in particularmountainous regions in the eastern part of the country(Varna, Shumen and Burgas) (Fig. 1) which potentiallyhave regular contacts with wild boar and may act asindicator for epidemics in wildlife.

2.3. Laboratory tests

Since the causative virus isolated from the index caseand RNA detected during the course of the epidemic wasidentified as serotype O of the MIDDLE EAST-SOUTH ASIA(ME-SA) topotype (PanAsia-2 lineage, ANT-10 sub-line-age), serological tests were performed using PriocheckFMD virus type O ELISA for antibody detection. Tissuesamples were tested for the presence of FMD virus genomeby r-RT-PCR according to Callahan et al. (2002). The sampleswere accompanied by information on the geographicallocation where the animal was shot or trapped, the age andsex, and clinical symptoms or pathological findings.

3. Results

No dead animals or animals with clinical signssuggesting FMD were found in the surveillance area from4 April 2011 to 4 April 2012.

No FMD virus genome was detected in any of the testedwild animals.

The average seroprevalence in wild boar was 6.9%. Thedetailed results are shown in Table 3. Three out of 68 testedroe deer, of which 66 were adult animals, were seropo-sitive (seroprevalence of 4.4%). All seven red deer and bothmouflons were seronegative.

Most sero-positive animals were clustered in the areaaround the FMD outbreaks in livestock (Table 4 and Fig. 2).The highest seroprevalence in wild boar (13.1%) was foundwithin a radius of 10 km. Further away, at the distance of11–20 km from the outbreaks 5.8% sero-positive wild boarwere diagnosed. No seropositive animals were found at adistance of 21–30 km and only one seropositive male wild

Fig. 2. Serological findings in wild boar around outbreaks in livestock.

Table 3

Results of serological surveillance for FMD in wild boar in Bulgaria by age

groups (February 2011–January 2012).

Age groups Total

sampled (n)

Ab

positive (n)

Prevalence

(%) (95% CI)

Adults 538 51 9.5 (7.1–12.3)

Juveniles 257 4 1.6 (0.4–3.9)

Age unknown 17 1 5.9 (0.1–28.7)

Total 812 56 6.9 (5.2–8.9)

Table 4

Sero-prevalence (with 95% CI) in all age groups of wild boar calculated

according to the direct distance (not accounted for differences in height)

from FMD outbreaks by zones.

Zone

(km)

Negative (n) Positive (n) Total (n) Prevalence (%)

0–10 283 43 326 13.1 (9.7–17.4)

11–20 195 12 208 5.8 (3.0–9.9)

21–30 96 – 96 –

31–50 127 1 128 0.8 (0.01–4.3)

>50 54 – 54 –



boar was tested positive at about 46 km away from theclosest outbreak in livestock, but still within the ‘‘CordonSantaire.’’

Four seropositive wild boar were juvenile animalsand were shot at a distance of 11–20 km from the FMDoutbreaks, 1–10 km north from the Turkish border(Fig. 2). The three seropositive roe deer were adultanimals shot 5–12 km from the FMD outbreaks in June2011 (Fig. 3).

The difference in seroprevalence between adult andyoung wild boar was significant (P < 0.0001) while thedifference between seropositive female and male wild boarwas not significant (P = 0.5702). The difference in ser-oprevalence between wild boar and roe deer was notsignificant (P = 0.6139) and no significant difference(P = 0.2528) was found when prevalence in adult wildboar (n = 538) was compared to that in adult roe deer(n = 66). Differences in sero-prevalence in time (betweenJune, October, November, December 2011 and January

2012) did not prove to be statistically significant (P > 0.6).However, a slight decrease in sero-prevalence could beobserved in wild animals sampled and tested from October2011 onwards (Table 5).

In domestic livestock the surveillance results provedthe absence of FMD virus infection after the last outbreaksin April 2011. All blood samples taken in August 2011(n = 5203) and in November 2011 (n = 5295) from domesticungulates in the ‘‘Cordon Sanitaire’’ were tested negativefor FMD antibodies as well as all samples (n = 5334) takenduring the last round of sampling in February 2012. NoFMD clinical signs have been observed in susceptiblelivestock during the clinical examinations carried out frommid April 2011 to April 2012.

East-Balkan pigs were blood sampled between Febru-ary 2011 and May 2012 in the regions of Burgas (553samples), Shumen (558 samples) and Varna (80 samples).All samples tested negative for antibodies to structuralproteins of the FMD virus.

Table 5

Sero-prevalence in wild boar calculated by months of sampling.

Months, 2011 2011 total 2012 Grand total

2 3 4 5 6 7 8 9 10 11 12 1

Total, n 5 12 2 – 52 – 18 – 222 255 210 776 36 812

Positive, n – – – – 2 – – – 19 20 14 55 1 56

Prevalence, % – – – – 3.8 – – – 8.5 7.8 6.7 7.1 2.8 6.9

Fig. 3. Serological findings in roe deer around outbreaks in livestock.



4. Discussion

The relatively low and clustered spatial distribution ofseropositive wild boar (6.9%) indicates that no widespreadFMD epidemic occurred in that area, but a rather localizedspread around 15 km from the outbreaks in livestock. Thefact that the seropositive adult animals, which were shotlate in 2011 at a distance of more than 10 km from theoutbreaks in livestock, were only males, which aregenerally more mobile, suggests that virus circulationdid not take place outside the infected zone (<10 km fromoutbreaks). It can be assumed that the seropositive animalsshot outside the infected zone were individuals that movedfrom the infected zone in search of their own socio-graphical territory (Danilkin, 2002).

The significant difference in sero-prevalence betweenadult and juvenile wild boar suggests that the FMD viruscirculation occurred before February–March 2011, whichare the main farrowing months in wild boar in that area. Alarge emigration of seropositive juveniles outside theinfected area as a result of local movements or dispersioncan be excluded since no seropositive wild boar weredetected more than 20 km away from the outbreaklocations (one exception, the one male animal testedpositive for antibody 47 km away from the outbreaks).

The absence of significant differences in the seropre-valence between males and females, irrespective of theirage, suggests that the sex of the animals was no risk factor.

Only four juvenile wild boar were found to beseropositive. Based on the estimated date of birth of theseanimals and on the assumption that maternal antibodiesdisappear within the first three months of life, it might bethat these piglets had contact with the virus andseroconverted.

From the serological data obtained in roe deer (4.4%seropositive), red deer and mouflons (both species sero-negative) it seems unlikely that the wild ruminants haveplayed a significant epidemiological role. The absence ofsignificant differences in sero-prevalence between wildboar and roe deer supports the speculation that bothspecies had a similar probability of becoming infected.However, since roe deer switch in summer to verydispersed social organization (Danilkin, 1999) it seemsunlikely that juvenile roe deer could have played moreimportant epidemiological role as compared to wild boar.

The relatively low sero-prevalence in wild boar anddeer and the clustered spatial distribution of sero-positiveanimals suggest that the FMD event in wildlife failed todevelop into a large scale epidemic wave. Significantdifference in sero-prevalence found between adult andjuvenile wild boar also suggests that for the surveyedpopulation the main period of exposure to the virus lastedmost likely from December 2010 to February 2011, wellbefore March to April 2011, when the second wave ofoutbreaks occurred. This also indirectly implies thatoccasional introductions from wildlife to livestock mighthave had taken place, particularly during the winter 2010/2011. Proven absence of the disease in domestic livestockfor a period of more than one year also suggests that thesylvatic FMD epidemic in the South-East Bulgaria was ashort living disease event, which ended shortly after the

last outbreaks in livestock in April 2011. This conclusion isin line with earlier historical observations of FMD infectionin wild boar (Sludskiy, 1956; Goreglyad, 1972; Danilkin,2002), and wildlife in general (Thomson et al., 2003).

So far only few serological surveys for FMD antibodiesin wild boar have been conducted. In Israel in 1997–199914.6% of animals were found sero-positive (ProMED-mail,2007). However, in the absence of information on sex andage, of precise locations and timing, of spatial and temporalcorrelation with outbreaks in livestock and of laboratorymethods used, the findings are difficult to be comparedwith the results of the present study.

Follow up to the FMD case in wild boar in Bulgariaserological and virological surveillance was carried out inwild boar in Turkish Thrace between February 2011 andJanuary 2012. No virus was detected. However 11.5% of thewild boar were found to be seropositive for antibody tonon-structural proteins of the FMD virus. Most of thepositive cases were clustered in the area bordering toBulgaria across the FMD outbreaks in livestock althoughsome were found further from the border in Turkish Thrace(EFSA, 2012a,b).

Results of modelling studies on feral pigs in Australiasuggest that FMD can potentially persist in a populationwith a density exceeding two individuals per km2 (Pechand Hone, 1988). This estimated density is twice as high asthe average spring density of wild boar in the munici-palities in the study area (0.9 heads/km2). Only in themunicipality of Malko Tarnovo (located in between thetwo clusters of outbreaks in livestock, Fig. 1) the springdensity of wild boar did reach the threshold estimated tomaintain virus transmission. Therefore, even when assum-ing that in summer the population doubles, a densitythreshold will hardly be achieved to sustain the infectionin the South-East Bulgaria on the long run (>1 year).

A more recent modelling study, which attempted tomimic main ecological and epidemiological conditions ofthis particular area, also concluded that long-termpersistence of FMDV in the multispecies ungulate com-munities in Thrace region is rather unlikely or evenimpossible (Lange, 2012). However, detection of as manyas 56 sero-positive wild boar clearly shows that horizontaltransmission of FMD did take place. From experimentalstudies conducted with wild boar and the FMD virusisolated in Bulgaria it is known that infected wild boar canshed and transmit horizontally the virus (Breithaupt et al.,2012). The experimentally infected animals started to shedvirus already during the incubation period 1 day afterinfection. The virus excretion via nasal discharged andsaliva lasted up to 9 days and the physical condition of theanimals did not seem to be much compromised.

FMD surveillance in wildlife which is mostly linked tohunting and trapping is a rather time consuming,logistically challenging and hardly efficient exercise.Furthermore, hunting is limited to few months of the yearin particular areas and requires significant human andfinancial resources. Therefore, collecting a statisticallysignificant number of samples for the early detection FMDin wildlife is rather a difficult approach. Our serologicalsurvey proved to be very useful in terms of retrospectiveanalysis of the disease situation in wildlife, but it can



hardly serve as an early warning system for FMD invasionsinto wildlife. According to a study conducted by EFSA(2012a,b) 13–39 weeks would be needed to detect the firstsero-positive wild boar when sampling is linked only to theusual hunting activities.

Therefore, the surveillance system based on huntingwith low numbers of trapped animals can prove freedomfrom FMD in wildlife only if more than one year has passed.It is obvious that the early detection of a new FMDVincursion would require much more frequent, regular andextensive sampling effort. Development of alternativenon-invasive sampling methods could help to meet therequired sample sizes and increase sampling frequency,along with the additional advantages, such as thepossibility to collect data on a year round basis and inthe places where hunting is not applicable (e.g. sub-urbanparks, protected areas etc.).

Our study shows that wildlife species, particularly wildboar, under the conditions of Strandzha Mountains inBulgaria did play a temporarily and spatially limited role inFMD transmission cycle. The modelling and experimentalstudies suggest that the epidemiological role of wild boarwould most strongly depend on the population density/size, and the environmental conditions (season) at the timeof virus introduction (EFSA, 2012a,b). Linking our findingswith historical observational studies in Europe (Marek andHutyra, 1931, cit. from Sludskiy, 1956) and results ofepidemiological modelling it can be concluded that asylvatic FMD epidemic involving wild boar and otherabundant ungulates (such as roe deer) is theoreticallypossible in some European countries, particularly thosewith large, dense and continuously distributed popula-tions of FMD susceptible wildlife (e.g. Germany, France,Italy, etc.). For this reason standardized protocols andguiding documents on how to deal with potential FMDepidemics in wildlife should be developed. A non-invasivesampling technique that would allow early detection ofviruses (e.g. in the saliva) needs to be developed andapplied in due time.

Conflict of interest statement

The authors affirm that no financial or personalrelationship existed that could have inappropriatelyinfluenced the content of this manuscript or the opinionsexpressed.

Acknowledgements

The authors would like to thank Dr. AlfEckbert Fusselfor all technical support and critical readings, the EuropeanCommission for having financed a large part of this study,the whole team from the Bulgarian National ReferenceLaboratory for FMD for their excellent work in carrying out

the diagnostic tests in the framework of the FMDsurveillance as well as all hunters and veterinarians whocollected the samples from susceptible wildlife andlivestock.

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