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SHEEP AND GOAT PLAGUE (PPR) BTSFThis presentation is delivered under contract with theConsumers, Health, Agriculture and Food Executive Agency(http://ec.europa.eu/chafea). The content of this presentation isthe sole responsibility of Opera S.u.r.l., the IstitutoZooprofilattico Sperimentale Lombardia e Emilia Romagna andthe State Food and Veterinary Service of Latvia and it can in noway be taken to reflect the views of the Consumers, Health,Agriculture and Food Executive Agency or any other body of theEuropean Union. The Consumers, Health, Agriculture and FoodExecutive Agency or any other body of the European Union willnot be responsible under any circumstances for the contents ofcommunication items prepared by the contractors.

PPRV infection and disease in wildlife

Bryony Jones, Royal Veterinary College, University of London

Food safety

Outline

1

▪ Role of wild animals in PPR

epidemiology

▪ Evidence of infection and disease in

wild animals

▪ Disease outbreaks

▪ Serological evidence

▪ Experimental infections

▪ Implications for PPR surveillance

and control

African buffalo (Syncerus caffer) photo: B Jones

Bharals (Pseudois nayaur)

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PPRV hosts

2

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

Wildebeest (Connochaetes taurinus) photo: R Kock

Wild goat (Capra aegagrus)

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3

Which species of wild animals are present in Bulgaria and Greece?

Ruminants?

Suids?

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Why is wild animal PPRV infection important?

4

▪ Risk to endangered species

▪ Possible role in spread of PPRV

▪ Possible role in maintenance of

PPRV

▪ Wild species as sentinels

Saiga antelope (Saiga tatarica)

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5

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

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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

Sheep and goats Wildlife

PPR infection

Virus transmission

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7

Sheep and goats Wildlife

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.

Sheep and

goats

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8

Sheep and goats Wildlife

PPR infection

Virus transmission

Sheep and

goats

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.

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9

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

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10

PPR outbreaks in wild animal populations

Outbreak in wild population

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Bharals (Himalayan blue sheep) in Tibet, China (Bao et al, 2011)

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▪ 2007-08 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

▪ 1.2 million bharals in Tibet, also in

Himalayas of Nepal, India, Pakistan, Bhutan

Bharals (Himalayan blue sheep)

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Sindh ibex in Pakistan (Abubakar et al, 2011)

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▪ 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

▪ Approx. 15,000 ibex in the park, also deer

and markhor goats

Fig. 1 Female ibex showing clinical signs: oculonasal discharges and emaciation

Fig. 2 Caseous material on gums and mouth lesions

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Wild goat (bezoar ibex) in Kurdistan, Iraq (Hoffman et al., 2012)

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▪ 2010-2011 high mortality in wild goats

(Capra aegagrus), >2,700 deaths

▪ Confirmed PPR antigen, sequencing

showed similar to a Turkish strain

▪ 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

(a) Mucopurulent nasal discharge

(b) Ulcerative keratitis and conjunctivitis

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Siberian ibex in Xinjiang, China (Zhu et al., 2016, Xia et al., 2016, Li et al, 2017)

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▪ Deaths of ibex (Capra ibex sibirica); PPR-

like signs (fever, ocular & nasal discharge,

mouth lesions, pneumonia, diarrhoea),

2014-2015

▪ 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: https://commons.wikimedia.org/wiki/File:Siberian_ibex_(Capra_sibirica)_04.jpg

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Wild goats and wild sheep, Iran (Marashi et al 2017)

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▪ PPRV confirmed in wild goats (Capra

aegagrus) and wild sheep (Ovis orientalis)

▪ PPR-like signs, high mortality

▪ six national parks affected, 2014-2015

▪ PPR disease confirmed in sheep and goats

around one of the parks prior to wild

animal deaths.Wild goats (Capra aegagrus)Source: http://awwp.alwabra.com/?page_id=1362

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Saiga antelope, Mongolia (Kock and Bolortuya,

2017)

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▪ 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, MongoliaSource: Richard Kock

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17

PPR outbreaks in wild animal populations

Outbreak in wild population

Outbreak in captive/managed animals

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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

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Outbreak in wild population

Outbreak in captive/managed animals

Antigen in healthy animals

Positive serology

PPR outbreaks, antigen detection, serology in wild animal populations

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PPR serology in Turkey

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▪ 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

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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)

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• PPR serology in East and Central Africa

• 1990-early 2000s

▪ 1994-2003 rinderpest (RP) surveillance in East Africa (Kock et al 2006)

▪ 10/675 seropositive (1.5%) – buffalo, eland, topi and warthog from

southwest Ethiopia

▪ 1996-2004 RP surveillance, East and Central Africa (Kock 2008) - 998 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

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• PPR serology in East and Central Africa - recent▪ Uganda - PPR reported in sheep and goats 2003, official report to OIE 2007

▪ 15/51 buffalo (29%) sero-positive - 2005 (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 2006-2008

▪ 15/115 (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 2010-2012 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

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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

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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

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Discussion

26

▪ 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

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ReferencesAbubakar, 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, 745-747. doi: 10.1007/s11250-010-9776-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, 68-71. doi: 10.1111/j.1439-0450.2004.00731.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, 238-240. doi: 10.1016/j.rvsc.2010.05.031.

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), 10885-6.

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, 869-877.

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, 443-447.

Gur, S. and Albayrak, H. (2010). Seroprevalance of peste des petits ruminants (PPR) in goitered gazelle (Gazellasubgutturosa subgutturosa) in Turkey. J Wildl Dis, 46, 673-677.

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, 516-522.

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, 173-176. doi: 10.1111/j.1865-1682.2011.01270.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, 1211-1214. doi: 10.1017/S0950268809991592.

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ReferencesKock, 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, 63-80. doi: DOI 10.1016/j.prevetmed.2006.01.016.

Kock, R. A. (2008). The Role of Wildlife in the Epidemiology of Rinderpest in East and Central Africa 1994-2004: A Study Based on Serological Surveillance and Disease Investigation. In Faculty of Clinical Veterinary Medicine pp. 264. 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, 2037-2040.

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, 2013-2016', TransboundEmerg 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, 2014-2016', Emerg Infect Dis, 23(4), 704-706.

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, 59-61.

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, 489-494.

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 pestedes 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. 2016 Genetic Characterization of a Novel Mutant of Peste Des PetitsRuminants Virus Isolated from Capra ibex in China during 2015. Biomed Res Int. 2016;2016:7632769. doi: 10.1155/2016/7632769.

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This presentation is delivered under contract with the Consumers, Health, Agriculture and Food Executive Agency (http://ec.europa.eu/chafea). Thecontent of this presentation is the sole responsibility of Opera S.u.r.l., the Istituto Zooprofilattico Sperimentale Lombardia e Emilia Romagna and theState Food and Veterinary Service of Latvia and it can in no way be taken to reflect the views of the Consumers, Health, Agriculture and FoodExecutive Agency or any other body of the European Union. The Consumers, Health, Agriculture and Food Executive Agency or any other body of theEuropean Union will not be responsible under any circumstances for the contents of communication items prepared by the contractors.

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