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Food safety
Better Training for Safer FoodInitiative
Sofia, Bulgaria 6th -8th June 2018
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
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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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Which species of wild animals are present in Bulgaria and Greece?
Ruminants?
Suids?
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Why is wild animal PPRV infection important?
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▪ 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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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.
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Sheep and goats Wildlife
PPR infection
Virus transmission
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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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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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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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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
Food safety
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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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
Food safety
Discussion
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▪ 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
Food safety
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.
Food safety
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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