BTSF. Better Training for Safer Food. Initiative. PPRV infection and disease in wildlife. Bryony Jones, Royal Veterinary College, University of London

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Better Training for Safer Food PPRV infection and disease in wildlife Initiative Bryony Jones, Royal Veterinary College, University of London SHEEP AND

eu/chafea). The content of this presentation is the sole

1 Better Training for Safer Food PPRV infection and disease in wildlife Initiative Bryony Jones, Royal Veterinary College, University of London SHEEP AND GOAT PLAGUE (PPR) This presentation is delivered under contract with the Consumers, Health, Agriculture and Food Executive Agency ( The content of this presentation is the sole responsibility of Opera S.u.r.l., the Istituto Zooprofilattico Sperimentale Lombardia e Emilia Romagna and the State Food and Veterinary Service of Latvia and it can in no way be taken to reflect the views of the Consumers, Health, Agriculture and Food Executive Agency or any other body of the European Union. The Consumers, Health, Agriculture and Food Executive Agency or any other body of the European Union will not be responsible under any circumstances for the contents of communication items prepared by the contractors. BTSF Sofia, Bulgaria 6 th -8 th June 2018

nayaur) Serological evidence Experimental infections Implications for

2 Outline Role of wild animals in PPR epidemiology Evidence of infection and disease in wild animals Disease outbreaks Bharals (Pseudois nayaur) Serological evidence Experimental infections Implications for PPR surveillance and control 1 African buffalo (Syncerus caffer) photo: B Jones

hartebeest, topi Antelopes gazelle, saiga African buffalo, eland Caprines; ibex, wild

3 Wild goat (Capra aegagrus) PPRV hosts Domestic species Sheep and goat Cattle, buffalo, yak, camel, pig Wild animals Order Artiodactyla Ruminants Deer Impala Wildebeest, hartebeest, topi Antelopes gazelle, saiga African buffalo, eland Caprines; ibex, wild sheep & goats Duiker Oryx Waterbuck, Kob Suids pigs 2 Wildebeest (Connochaetes taurinus) photo: R Kock

4 Which species of wild animals are present in Bulgaria and Greece? Ruminants? Suids? 3

5 Why is wild animal PPRV infection important? Risk to endangered species Possible role in spread of PPRV Possible role in maintenance of PPRV Wild species as sentinels Saiga antelope (Saiga tatarica) 4

6 What is the role of wild animals in PPR epidemiology? Dead end hosts: virus spill-over from small ruminants to wild species followed by burn-out Bridge hosts: virus spill-over from small ruminants to wild species, with subsequent spill-back into domestic animals, connecting otherwise unconnected domestic populations Maintenance hosts: PPR virus transmission is maintained by one or more species, or a community of species, in the absence of domestic animal infection 5

7 Sheep and goats PPR infection Virus transmission Wildlife Dead-end host? - virus spill-over from small ruminants to wild species, followed by burn-out. - If we eliminate PPRV from sheep and goats there will be no source of infection for wildlife. 6

domestic animals. Infection burns out in wildlife without repeated spill-over.

8 Sheep and goats Wildlife Sheep and goats PPR infection Virus transmission Bridge host? virus spill-over from small ruminants to wild species, spill-back into domestic animals. Infection burns out in wildlife without repeated spill-over. Elimination of PPRV from sheep and goats removes source of infection for wildlife. 7

9 Sheep and goats Wildlife Sheep and goats PPR infection Virus transmission Maintenance host? PPRV transmission is maintained by one or more wildlife species, or community of species, in the absence of domestic animal infection. If PPRV is eliminated from small ruminants, there is risk of re-infection from wildlife. 8

10 What evidence is there of infection and disease in wild animals? Clinical outbreaks in wild populations Clinical outbreaks in captive/managed animals Natural infection sero-positive animals Experimental infection 9

11 PPR outbreaks in wild animal populations Outbreak in wild population 10

12 Bharals (Himalayan blue sheep) in Tibet, China (Bao et al, 2011) clinical disease - bharals (Pseudois nayaur), Mongolian gazelle (Procarpa gutturosa), Tibetan antelope (Pantholops hodgsoni) Confirmed PPR antigen in bharals sequenced virus closely related to PPRV in sheep and goats in Tibet PPR outbreaks confirmed in sheep and goats in 2007 in same area Bharals (Himalayan blue sheep) 1.2 million bharals in Tibet, also in Himalayas of Nepal, India, Pakistan, Bhutan 11

13 Sindh ibex in Pakistan (Abubakar et al, 2011) 2009 high mortality outbreak in ibex (Capra aegagrus blythi) in a national park, Pakistan history of PPR in sheep and goats in the area - contact with sheep and goats through grazing and watering Fig. 1 Female ibex showing clinical signs: oculonasal discharges and emaciation Approx. 15,000 ibex in the park, also deer and markhor goats 12 Fig. 2 Caseous material on gums and mouth lesions

sequencing showed similar to a Turkish strain (a) Mucopurulent nasal discharge Sheep and goats PCR positive in

14 Wild goat (bezoar ibex) in Kurdistan, Iraq (Hoffman et al., 2012) high mortality in wild goats (Capra aegagrus), >2,700 deaths Confirmed PPR antigen, sequencing showed similar to a Turkish strain (a) Mucopurulent nasal discharge Sheep and goats PCR positive in the area, routine vaccination of small ruminants in region Wild goat rare, ancestor of domestic goats, related to Sindh ibex (b) Ulcerative keratitis and conjunctivitis 13

15 Siberian ibex in Xinjiang, China (Zhu et al., 2016, Xia et al., 2016, Li et al, 2017) Deaths of ibex (Capra ibex sibirica); PPRlike signs (fever, ocular & nasal discharge, mouth lesions, pneumonia, diarrhoea), PCR positives; ibex, argali (Ovis ammon), goitered gazelle (Gazella subgutturosa) PPRV isolated, sequence closely related to 2013 virus from sheep & goats South Xinjiang - large grassland with ibex, argali, wild yak and deer, sharing pasture and water with livestock Siberian ibex Source: (Capra_sibirica)_04.jpg 14

Wild goats and wild sheep, Iran (Marashi et al 2017) PPRV confirmed in wild goats (Capra aegagrus) and wild sheep (Ovis orientalis) PPR-like signs, high mortality six national parks

16 Wild goats and wild sheep, Iran (Marashi et al 2017) PPRV confirmed in wild goats (Capra aegagrus) and wild sheep (Ovis orientalis) PPR-like signs, high mortality six national parks affected, PPR disease confirmed in sheep and goats around one of the parks prior to wild animal deaths. Wild goats (Capra aegagrus) Source: 15

50-60% mortality Confirmed by PCR, sequencing showed closely related to sheep and goat virus

17 Saiga antelope, Mongolia (Kock and Bolortuya, 2017) Outbreak in sheep and goats in confirmed Sept 2016 Dec 2016 Feb 2017 PPR-like signs, 5-6,000 deaths of saiga (Saiga tartaric mongolica), 50-60% mortality Confirmed by PCR, sequencing showed closely related to sheep and goat virus Sibirian ibex, goitered gazelle also infected Sick and dead saiga, Mongolia Source: Richard Kock 16

18 PPR outbreaks in wild animal populations Outbreak in wild population Outbreak in captive/managed animals 17

19 Clinical PPR outbreaks in captive/managed animals Dorcas gazelle, Laristan sheep, Nubian ibex, gemsbok United Arab Emirates (Furley 1987) Likely source was nearby flock of goats with recent high mortality Unaffected Arabian oryx, scimitar-horned oryx, red deer, defassa waterbuck, nilgai, dama gazelle, bontebok, blackbuck. Dorcas gazelle, Thomson s gazelle - Saudi Arabia (Abu Elzein et al 2004) PPR in Saudi Arabia since 1990, PPR-like disease seen in sheep and goats in the area Unaffected blesbok, gemsbok, fallow deer, zebra Impala, springbok, Arabian mountain gazelle, Rheem gazelle, bushbuck, Nubian ibex, Markhor goat, Barbary sheep 2 outbreaks in UAE (Kinne 2010) Source unknown Arabian mountain gazelle Saudi Arabia (Sharawi 2010) One flock affected, neighbouring sheep and goats flocks with PPR-like disease Chowsingha India (Jaisree et al., 2017) Chowsingha antelope (Tetracerus quadricornis) in a zoological park, 20/25 animals died with acute respiratory signs no direct contact with domestic animals Chinese water deer China (Zhou et al., 2017) Chinese water deer (Hydropotes inermis) on farm in Anhui Province, east China Sequence showed close relationship to sheep and goat virus 18

20 PPR outbreaks, antigen detection, serology in wild animal populations Outbreak in wild population Outbreak in captive/managed animals Antigen in healthy animals 19 Positive serology

21 PPR serology in Turkey 10/82 sera (12%) sero-positive from goitered gazelle (Gur and Albayrak, 2010) No clinical disease Endangered native species, approx. 850 animals kept on a state farm, south-east Anatolia PPR previously confirmed in sheep and goats in this region 20

22 PPR serology in West and Central Africa 2/247 (0.8%) seropositive from parks in Cote d Ivoire (Couacy-Hymann et al., 2005) Positives - buffalo, waterbuck Negatives - kob, hartebeest, roan antelope, bushbuck, red-flanked duikers, blue duikers, warthogs Sero-positives in Burkina Faso, Chad and CAR - hartebeest, kob and buffalo (PACE Veterinary Wildlife Project, Chardonnet and Kock 2001) Benin 3/16 (19%) buffaloes seropositive (PACE project, 2003) African grey duiker 4/38 (10.5%) sero-positive, Nigeria (Ogunsanmi et al 2003) 21

23 PPR serology in East and Central Africa 1990-early 2000s rinderpest (RP) surveillance in East Africa (Kock et al 2006) 10/675 seropositive (1.5%) buffalo, eland, topi and warthog from southwest Ethiopia RP surveillance, East and Central Africa (Kock 2008) sera collected 30/576 (5%) buffalo and 1/33 eland (3%) seropositive in Kenya, Ethiopia-Sudan, DRC-Chad-CAR All other species sampled were negative: Grant s gazelle, giraffe, hartebeest, impala, kob, kudu, nyala, oryx, roan antelope, topi, warthog, waterbuck, wildebeest, bushbuck, gerenuk, sable antelope Uganda and Tanzania all negative 22

24 PPR serology in East and Central Africa - recent Uganda - PPR reported in sheep and goats 2003, official report to OIE /51 buffalo (29%) sero-positive (Kock 2008) 12/67 buffalo (17.9%), 5/39 kob (12.8%) sero-positive 2015* 5/30 buffalo (16.7%) sero-positive 2017* Kenya - Major outbreak in sheep and goats /115 (13.0%) sero-positive; buffalo, impala, Thomson s gazelle, Grant s gazelle, wildebeest, gerenuk, warthog, 2016* Tanzania 2008 outbreak in sheep and goats in north, spread to south by 2010 Buffalo, Thomson s gazelle, Grant s gazelle samples collected in northern protected areas, all negative (Lembo et al. 2013) 29/46 (63%) sero-positive 2014; buffalo, Grant s gazelle, wildebeest, impala* 11/18 (61%) sero-positive 2015; buffalo, Grant s gazelle, topi, hartebeest* *unpublished data from EU ANIHWA ERANET Improved Understanding of PPR (IUEPPR) Project 23

25 Experimental infection American white-tailed deer; developed clinical disease, transmitted to other deer (Hamdy and Dardiri, 1976) Wild boar; developed mild-moderate clinical signs (fever, diarrhoea, nasal discharge, conjunctivitis, leucopenia) and infected in-contact goats* *unpublished data from EU ANIHWA ERANET Improved Understanding of PPR (IUEPPR) Project 24

26 In summary wild outbreaks only in Asia (so far), mainly in wild caprines no clinical PPR disease seen in Africa (so far) African species are susceptible to disease in captivity or managed conditions in Middle East All outbreaks were per-acute or acute, typical PPR clinical signs, high mortality but has milder disease gone unnoticed? All outbreaks were associated with confirmed or suspected disease in domestic sheep and goats 25

27 Discussion What are the implications of these findings for PPR surveillance and control in Europe? Possible susceptible wild species? Role of wild animals: sentinel of domestic animal infection bridge host? maintenance host? Beisa oryx in Ethiopia photo: B Jones 26

28 References Abubakar, M., Rajput, Z. I., Arshed, M. J., Sarwar, G. and Ali, Q. (2011). Evidence of peste des petits ruminants virus (PPRV) infection in Sindh Ibex (Capra aegagrus blythi) in Pakistan as confirmed by detection of antigen and antibody. Trop Anim Health Prod, 43, doi: /s y. Abu Elzein, E. M., Housawi, F. M., Bashareek, Y., Gameel, A. A., Al-Afaleq, A. I. and Anderson, E. (2004). Severe PPR infection in gazelles kept under semi-free range conditions. J Vet Med B Infect Dis Vet Public Health, 51, doi: /j x. Bao, J., Wang, Z., Li, L., Wu, X., Sang, P., Wu, G., Ding, G., Suo, L., Liu, C., Wang, J., Zhao, W., Li, J. and Qi, L. (2011). Detection and genetic characterization of peste des petits ruminants virus in free-living bharals (Pseudois nayaur) in Tibet, China. Res Vet Sci, 90, doi: /j.rvsc Bao, J., Wang, Q., Parida, S., Liu, C., Zhang, L., Zhao, W. and Wang, Z. (2012) 'Complete genome sequence of a Peste des petits ruminants virus recovered from wild bharal in Tibet, China', J Virol, 86(19), Couacy-Hymann, E., Bodjo, C., Danho, T., Libeau, G. and Diallo, A. (2005). Surveillance of wildlife as a tool for monitoring rinderpest and peste des petits ruminants in West Africa. Revue Scientifique et Technique - Office International des Épizooties, 24, Furley, C. W., Taylor, W. P. and Obi, T. U. (1987). An outbreak of peste des petits ruminants in a zoological collection. Vet Rec, 121, Gur, S. and Albayrak, H. (2010). Seroprevalance of peste des petits ruminants (PPR) in goitered gazelle (Gazella subgutturosa subgutturosa) in Turkey. J Wildl Dis, 46, Hamdy, F. M. and Dardiri, A. H. (1976). Response of white-tailed deer to infection with peste des petits ruminants virus. J Wildl Dis, 12, Hoffmann, B., Wiesner, H., Maltzan, J., Mustefa, R., Eschbaumer, M., Arif, F. A. and Beer, M. (2012). Fatalities in wild goats in Kurdistan associated with Peste des Petits Ruminants virus. Transbound Emerg Dis, 59, doi: /j x. Jaisree, S., Aravindhbabu, R. P., Roy, P. and Jayathangaraj, M. G. (2017) 'Fatal peste des petits ruminants disease in Chowsingha', Transbound Emerg Dis. Kinne, J., Kreutzer, R., Kreutzer, M., Wernery, U. and Wohlsein, P. (2010). Peste des petits ruminants in Arabian wildlife. Epidemiol Infect, 138, doi: /S

29 References Kock, R. A., Wamwayi, H. M., Rossiter, P. B., Libeau, G., Wambwa, E., Okori, J., Shiferaw, F. S. and Mlengeya, T. D. (2006). Re-infection of wildlife populations with rinderpest virus on the periphery of the Somali ecosystem in East Africa. Preventive Veterinary Medicine, 75, doi: DOI /j.prevetmed Kock, R. A. (2008). The Role of Wildlife in the Epidemiology of Rinderpest in East and Central Africa : A Study Based on Serological Surveillance and Disease Investigation. In Faculty of Clinical Veterinary Medicine pp University of Cambridge. Kock, R. A. and Bolortuya, P. (2017) Mongolia Investigation of Peste des Petits Ruminants (PPR) among wild animals and its potential impact on the current PPR situation in livestock Mission report 20 January - 1 February 2017Crisis Management Centre - Animal Health, FAO and OIE. Lembo, T., Oura, C., Parida, S., Hoare, R., Frost, L., Fyumagwa, R., Kivaria, F., Chubwa, C., Kock, R., Cleaveland, S. and Carrie Batten, C. (2013). Peste des petits ruminants infection among cattle and wildlife in northern Tanzania. Emerg Infect Dis, 19, Li, J., Li, L., Wu, X., Liu, F., Zou, Y., Wang, Q., Liu, C., Bao, J., Wang, W., Ma, W., Lin, H., Huang, J., Zheng, X. and Wang, Z. (2017) 'Diagnosis of Peste des Petits Ruminants in Wild and Domestic Animals in Xinjiang, China, ', Transbound Emerg Dis. Marashi, M., Masoudi, S., Moghadam, M. K., Modirrousta, H., Marashi, M., Parvizifar, M., Dargi, M., Saljooghian, M., Homan, F., Hoffmann, B., Schulz, C., Starick, E., Beer, M. and Fereidouni, S. (2017) 'Peste des Petits Ruminants Virus in Vulnerable Wild Small Ruminants, Iran, ', Emerg Infect Dis, 23(4), Ogunsanmi, A. O., Awe, E. O., Obi, T. U. and Taiwo, V. O. (2003). Peste des petits ruminants (PPR) virus antibodies in African grey duiker (Sylvicapra grimmia). African Journal of Biomedical Research, 6, Sharawi, S. S., Yousef, M. R., Al-Hofufy, A. N. and Al-Blowi, M. H. (2010). Isolation, serological and Real Time PCR diagnosis of peste des petites ruminants virus in naturally exposed Arabian gazelle in Saudi Arabia. Veterinary World, 3, Xia, J., Zheng, X. G., Adili, G. Z., Wei, Y. R., Ma, W. G., Xue, X. M., Mi, X. Y., Yi, Z., Chen, S. J., Du, W., Muhan, M., Duhaxi, C., Han, T., Gudai, B. and Huang, J. (2016) 'Sequence analysis of peste des petits ruminants virus from ibexes in Xinjiang, China', Genet Mol Res, 15(2). Zhou, X. Y., Wang, Y., Zhu, J., Miao, Q. H., Zhu, L. Q., Zhan, S. H., Wang, G. J. and Liu, G. Q. (2017) 'First report of peste des petits ruminants virus lineage II in Hydropotes inermis, China', Transbound Emerg Dis. Zhu Z, Zhang X, Adili G, Huang J, Du X, Zhang X, et al Genetic Characterization of a Novel Mutant of Peste Des Petits Ruminants Virus Isolated from Capra ibex in China during Biomed Res Int. 2016;2016: doi: /2016/

30 This presentation is delivered under contract with the Consumers, Health, Agriculture and Food Executive Agency ( The content of this presentation is the sole responsibility of Opera S.u.r.l., the Istituto Zooprofilattico Sperimentale Lombardia e Emilia Romagna and the State Food and Veterinary Service of Latvia and it can in no way be taken to reflect the views of the Consumers, Health, Agriculture and Food Executive Agency or any other body of the European Union. The Consumers, Health, Agriculture and Food Executive Agency or any other body of the European Union will not be responsible under any circumstances for the contents of communication items prepared by the contractors. OPERA Viale Parioli 96, Roma - Italy Tel / Fax info@opera-italy.it; Better Training for Safer Food BTSF European Commission Consumers, Health and Food Executive Agency DRB A3/042 L-2920 Luxembourg

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