Abstract
Peste des petits ruminants (PPR) is a contagious viral disease of domestic small ruminants. It also affects wild ungulates but there are comparatively few studies of the incidence of natural infection, clinical signs and pathology, and confirmation of the virus, and in these species. In this article, we list the wild ungulates in which PPRV infection has been confirmed and summarize available information about the presentation of the disease, its identification, and impact of virus on wildlife populations. Considering recent reports of outbreaks by the World Organization for Animal Health (OIE), it is important to understand the transmission of this disease within wildlife populations in PPR endemic regions.
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Introduction
Peste des petits ruminants virus (PPRV) is the cause of peste des petits ruminants (PPR), a contagious, transboundary disease of small domestic ruminants and some wild ungulates (Kinne et al. 2010; Munir et al. 2012). Because of its impact on small ruminants, and its similarity to the recently eradicated rinderpest virus, the World Organization for Animal Health (OIE) and the Food and Agricultural Organization (FAO) launched a joint program to eradicate PPRV by 2030 (FAO 2015). PPR is also a threat to wildlife and therefore to the conservation of endangered species (Munir 2014).
It was first assumed that PPRV only affected sheep and goats (Lefevre and Diallo 1990), but it has since been observed clinically and pathologically in a wider range of species and confirmed diagnostically either directly through detection of virus, viral antigens, or specific viral RNA or indirectly through detection of antibodies in wild ruminants (Kinne et al. 2010), cattle and domestic buffaloes (Balamurugan et al. 2012a), yaks (Abubakar et al. 2015), camels (Kwiatek et al. 2011), Asiatic lion (Balamurugan et al. 2012b), and dogs (Ratta et al. 2016). Some wild ruminant species are at high risk from PPRV (Rossiter 2008) and domestic small ruminants most likely play a role in the spread of the virus to them. However, disease may also be disseminated from infected wildlife to other susceptible wildlife. Most of the available data on the disease and on PPRV are from domestic small ruminants, and data from wildlife is more limited. Host and virus-related factors in the spread of PPRV infection need better understanding if PPR is to be eradicated locally and globally. This brief report lists the known wild ungulates in which PPRV infection has been confirmed and highlights some key emerging issues regarding this infection in these species. The term “wild” covers free-ranging, semi-captive, and captive animals. In the text, species are referred to by their English or colloquial names, with their Latin binomials being given in Table 1.
Virus transmission in wild small ruminants
In many areas where PPR is endemic, domestic animals intermingle with wildlife, allowing interspecies transmission of PPRV during grazing and at water sources (Banyard and Parida 2015). Abubakar et al. (2011) speculated that an outbreak of PPR in Sindh ibex was due to spillover of virus from a recent outbreak of PPR in nearby domestic small ruminants. Similar spillovers to wild hosts are believed to have occurred in Tibet (Bao et al. 2011) and in the Ngorongoro Conservation Area in northern Tanzania (Mahapatra et al. 2015).
From an epidemiological point of view, there is potential for interspecies transmission between wild species and from wild species back to domestic ruminants, but the dynamics of such transmission mechanisms are uncertain. The transfer of wildlife to zoological collections and seasonal migration of animals are two possibilities for disease spread over significant distances and across country borders (Mallon and Kingswood 2001).
Clinical and pathological presentation
The clinical presentation of PPRV in wild ungulates is essentially the same as in domestic small ruminants. Initial involvement of the respiratory system causes lacrimation and nasal and ocular discharges (Bao et al. 2011; Abubakar et al. 2011; Hoffmann et al. 2012) which may lead to crusts forming over the nostrils and lip commissure (reported in antelopes; Kinne et al. 2010). Subsequent involvement of the alimentary tract epithelia causes cheesy necrotic material on the gums (reported in ibex; Abubakar et al. 2011) and erosions of the oral cavity membranes (reported in gazelle; Sharawi et al. 2010). Unilateral corneal opacity has also been observed in gazelle (Abu-Elzein et al. 2004). Death from respiratory arrest has been reported in gazelle, ibex, gemsbok, and Laristan sheep (Furley et al. 1987; Abu-Elzein et al. 2004).
The severity of PPR infection (Bao et al. 2011) is seen from pathological changes in different visceral organs, including syncytia and multifocal hepatocellular coagulation via necrosis (Kinne et al. 2010), and postmortem histopathology was used to confirm PPRV infection in dorcas and Thomson’s gazelles (Furley et al. 1987). Similar features are found in infected small domestic ruminants (Brown et al. 1991).
Impact of PPR on genetic depletion
According to the International Union for Conservation of Nature and Natural Resources (IUCN), rare species are at risk of genetic depletion when outbreaks of serious disease, such as PPR, lead to high mortality (Osofsky 2005). The global attention and response to the recent high mortalities of free-ranging saiga antelope, including one outbreak confirmed to be caused by PPRV in Mongolia where at least 10% of the population was depleted (FAO 2017), is a clear example of the potential impact of PPRV on rare species. Rare wildlife kept and raised under captive or semi-captive conditions for conservation purposes is also at risk, as seen in the 70% mortality reported for Nubian ibex in an Israeli zoo (OIE 2017a). Implementation of quarantine measures and transfer of only seronegative animals should reduce the incidence of such events (Rossiter 2008) but global eradication offers a longer lasting solution.
Concluding remarks
In this article, we have briefly summarized the current knowledge on PPRV occurrence in wild ungulates and listed (Table 1) those wild species of in which disease has been recorded and confirmed, some of which are endangered and at elevated risk of genetic losses if infected by PPRV. The list can be expected to change: growing as more species are found to be susceptible to PPRV, altering as the classification of closely related host species and sub-species is refined, and as new and more accurate information about PPRV infection in these species becomes available.
To date, there is no evidence that wild species play a different epidemiological role in PPR to that played in the past by wild species infected by rinderpest virus. Wildlife proved incapable of permanently maintaining rinderpest virus but was valuable clinical and serological sentinels for virus in nearby cattle, and more study is required to establish the contribution wild species can play as sentinels during the eradication of PPRV (Couacy-Hymann et al. 2005). Additional study is also needed on the impact of PPRV on the genetic diversification capacity of wild host species, and on the transmission pathways for PPRV into and within wild populations. The existing evidence of the severity of PPRV infection in endangered wildlife that associate with infected small ruminants is compelling support for global eradication of the virus and for better control strategies targeted at these wildlife-livestock interfaces.
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Acknowledgements
All authors are highly indebted to Dr. Muhammad Munir (The Pirbright Institute, UK) for his sincere guidance and Dr. Mohammed Afzal for his permission to include the data on blackbuck.
Funding
JJW is supported by the Swedish Research Council for PPR research (Grant Nos. SRC 348-2013-6402 and SRC 348-2014-4293).
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AR, JJW, and MA initiated the idea and drafted the skeleton of the manuscript. MZS, JJW, and AR gave technical guidance and support. JJW, MZS, and PBR provided input, guidance, support, and editing of the manuscript. All authors approved the final manuscript.
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This article belongs to the Topical Collection: The Gordon Scott Collection - articles on PPR and other infectious diseases of tropical livestock
Guest Editor: Paul Rossiter
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Aziz-ul-Rahman, Wensman, J.J., Abubakar, M. et al. Peste des petits ruminants in wild ungulates. Trop Anim Health Prod 50, 1815–1819 (2018). https://doi.org/10.1007/s11250-018-1623-6
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DOI: https://doi.org/10.1007/s11250-018-1623-6