Role of Wild Small Ruminants in the Epidemiology of Peste Des Petits Ruminants

Peste des petits ruminants virus (PPRV) causes one of the most contagious and highly infectious respiratory diseases in sheep and goats known as peste des petits ruminants (PPR). Reports of outbreaks of PPR in captive and wild small ruminants have extended the known spectrum of susceptible species to include antelopes. Phylogenetic analysis of nucleoprotein and fusion genes indicates that all PPRVs isolated from wild ungulate outbreaks belong to lineage IV. While it is clear that a number of wildlife species are susceptible to infection, the role of wildlife in the epidemiology of PPR remains uncertain. The available information about the occurrence of disease in free‐ranging wildlife is mainly derived from surveys based on serological evidence. Data on the genetic nature of circulating PPRV strains are scarce. Given the scope of PPR in wild ungulates that are widespread in many countries, current disease surveillance efforts are inadequate and warrant additional investment. This is crucial because domestic and wild ruminants mingle together at several points, allowing inter‐species transmission of PPRV. There is no reason to believe that PPRV circulates in wild animals and acts as a potential source of virus for domestic species. Irrespective of the possibility of wild small ruminants as the reservoir of PPRV, concerns about the role of susceptible species of antelopes need to be addressed, due to the fact that the disease can pose a serious threat to the survival of endangered species of wild ruminants on the one hand and could act as a constraint to the global eradication of PPR on the other hand. In this review, knowledge gained through research or surveillance on the sustainability of PPRV in wild ruminants is discussed.     

Detection and Phylogenetic Analysis of Peste des Petits Ruminants Virus Isolated from Outbreaks in Punjab,Pakistan

Peste des Petits Ruminants (PPR) is an important viral disease of small ruminants and is endemic in Pakistan. In the following study, samples from two outbreaks of PPR in goats have been subjected to laboratory investigations. The Peste des Petits Ruminants virus (PPRV) genome was detected using both conventional and real‐time PCR. Genetic characterization of the local PPRV field isolates was conducted by sequencing 322 bp of the fusion (F) gene and 255 bp of the nucleoprotein (N) gene. The phylogenetic tree based on the F gene clustered samples from both outbreaks into lineage 4 along with other Asian isolates, specifically into subcluster 1 along with isolates from Middle East. Analysis of N gene revealed a different pattern. In this case, the Pakistani samples clustered with Chinese, Tajikistani and Iranian isolates, which probably represents the true geographical pattern of virus circulation. This is the first report presenting the phylogenetic tree based on N gene as well as performing a parallel comparison of the trees of F and N gene together from Pakistani isolates. The results of this study shed light on the PPRV population in Pakistan and emphasize the importance of using molecular methods to understand the epidemiology. Such understanding is essential in any efforts to control the number and impact of outbreaks that are occurring in endemic countries such as Pakistan, especially in the current scenario where OIE and FAO are eager to control and subsequently eradicate PPR from the globe, as has been achieved for Rinderpest.     

Molecular Characterization of Peste des Petits Ruminants Viruses From Outbreaks Caused by Unrestricted Movements of Small Ruminants in Pakistan

Peste des petits ruminants (PPR) is an endemic disease of small ruminants, and vaccination has been the method of control but outbreaks are continuously occurring in Pakistan. The following study presents a detailed investigation of an outbreak, suspected to be PPR, probably introduced by PPRV‐infected sheep and goats from Sindh Province (north‐west) to Punjab Province (central) of Pakistan during the flood relief campaign in 2011. A total of 70 serum samples from 28 different flocks were tested with competitive ELISA (H antibodies), which detected 24 (34.2%) samples positive for PPRV antibodies. Nasal swabs and faeces were tested with immunocapture ELISA (N antigen), which detected 18 (25.7%) samples positive for PPRV antigen. The RNA detected positive (n = 28, 40%) using real‐time PCR was subjected to conventional PCR for the amplification of the fusion and nucleoprotein genes. Sequencing of both genes and subsequent phylogenetic analysis indicated the grouping of all the sequences to be in lineage IV along with other Asian isolates of PPRV. However, sequences of both genes were divided into two groups within lineage IV. One group of viruses clustered with previously characterized Pakistani isolates, whereas the other group was distinctly clustered with isolates from the Middle East or India. The sequence identity indicated the introduction of at least one population of PPRV from a different source and circulation in the local flocks of small ruminants, which emphasized the need to obtain health clearance certificate before movement of animals. The results of this study provide baseline data for the genetic characterization of different PPRV populations in Pakistan.     

Molecular epidemiology of peste des petits ruminants in Niger: An update

Like many West African countries, outbreaks of peste des petits ruminants (PPR), an economically important disease of goats and sheep, are regularly reported in Niger. The causative virus, peste des petits ruminants virus (PPRV), can be differentiated into four genetically distinct lineages. A publication in 2018 identified three PPRV lineages circulating in the country in 2001 (lineages I and II) and 2013 (lineage IV), respectively. In this present study, more recent samples were collected from goats and sheep in locations throughout Niger between 2011 and 2017. Twelve PPRV‐positive samples were characterized by sequencing of a segment of the nucleocapsid protein (N) gene. Phylogenetic analysis of the sequences identified viruses from lineages II and IV only. The analysis also indicated a shared origin of the viruses from Niger with PPRVs from neighbouring countries suggesting transboundary movement.     

Molecular characterization of Peste des petits ruminants viruses in the Marmara Region of Turkey

Recent outbreaks of Peste des petits ruminants (PPR) in the Marmara region of Turkey including the European part of Thrace is important due to its proximity to Europe (Greece and Bulgaria) and the potential threat of spread of PPR into mainland Europe. In order to investigate the circulation of PPRV in the region suspect clinical and necropsy samples were collected from domestic sheep (n = 211) in the Marmara region of Turkey between 2011 and 2012. PPR virus (PPRV) genome was detected in 10.4% (22 out of 211) of sheep samples by real‐time RT‐PCR, and PPR virus was isolated from lungs of two sheep that died from infection. Of the 22 positive samples nine were used for partial N‐gene amplification and sequencing. The phylogenetic analyses indicated that the virus belongs to lineage IV, the same lineage that is circulating in eastern and central part of Turkey since its first official report in 1999. In addition, samples from 100 cattle were collected to investigate potential subclinical circulation of PPRV. However all were found to be negative by real‐time RT‐PCR, and also in serological tests indicating the large ruminants were likely not exposed or infected with the virus. The impact of these findings on the potential threat of spread of PPR to Europe including the first PPR outbreak in Europe in Bulgaria on 23rd June 2018 is discussed.     

Co‐circulation of Peste‐des‐Petits‐Ruminants Virus Asian lineage IV with Lineage II in Nigeria

Peste‐des‐petits‐ruminants (PPR), a major small ruminant transboundary animal disease, is endemic in Nigeria. Strains of the causal agent, peste‐des‐petits‐ruminants virus (PPRV), have been differentiated into four genetically distinct lineages based on the partial sequence of the virus nucleoprotein (N) or fusion (F) genes. Peste‐des‐petits‐ruminants virus strains that were identified initially in Africa were grouped into lineages I, II and III and viruses from Asia were classified as lineage IV and referred to as the Asian lineage. Many recent reports indicate that the Asian lineage is now also present in Africa. With this in mind, this study was conducted to reassess the epidemiology of PPRV in Nigeria. A total of 140 clinical samples from 16 sheep and 63 goats with symptoms suggestive of PPR were collected from different states of Nigeria during a four‐year period (2010–2013). They were analysed by the amplification of fragments of the N gene. Results for 33 (42%) animals were positive. The phylogenetic analysis of the N gene sequences with those available in GenBank showed that viruses that were detected belong to both lineage II and IV. Based on an analysis of the N gene sequences, the lineage IV isolates grouped into two clades, one being predominant in the north‐eastern part of the country and the other found primarily in the southern regions of the country. This study reports the presence of PPRV Asian lineage IV in Nigeria for the first time.     

Peste des Petits Ruminants (PPR) virus serological surveillance in goats in Lao PDR: Issues for disease eradication in a low‐resource disease‐free setting

Peste des Petits ruminants (PPR) is an economically important transboundary viral disease of goats. This study aimed to determine a baseline of serological evidence for Peste des petits ruminants virus (PPRV) in Lao goats. A total of 1,072 serum samples were collected by convenience sampling across five provinces in Laos and tested for antibody response to PPRV using a commercially available competitive ELISA. Positive antibody responses were found in 2.2% (95% CI 1.4, 3.2) of the samples. True prevalence calculations indicated a total overall sample prevalence of 1.7% (95% CI 0.9, 2.8). The highest provincial seroprevalences were Xiangkhouang (3.5%, 95% CI 1.6, 6.9) and Xayaboury (2.9% (95% CI 1.3, 5.7). There was no association between antibody response and each of the following factors: location, breed, gender or age. Considering the apparent absence of disease manifestation of PPR in Laos, likely explanations for the antibody positivity could include cross reaction to other Morbilliviruses such as Measles or Canine Distemper, importation of pre‐vaccinated goats, need for test cut‐off re‐evaluation to be region specific, or a subclinical and a less virulent circulating virus. This study highlights that the sampled Lao goat population is highly likely to be naïve to PPRV and therefore at risk of an outbreak, possibly by transboundary incursion of livestock from PPR endemic China. Further work is required in the testing of small ruminants in Laos that may eventually provide evidence for a status of freedom from disease, particularly in support of programs aimed at global PPR eradication.     

First genetic characterization of Peste des Petits Ruminants from Niger: On the advancing front of the Asian virus lineage

Peste des Petits Ruminants (PPR ) is a serious transboundary infectious disease of small ruminants. The causal agent, PPR virus (PPRV ), can be separated into four genetically distinct lineages using phylogenetic analysis. In recent decades, lineage IV of PPRV has dramatically extended its geographic distribution from Asia to the Middle East and to Africa, where it has progressively replaced other PPRV lineages. Lineages I and II are historically distributed in West Africa. Currently, lineage II appears to dominate the region, whereas the last recorded occurrence of lineage I dates back to 1994. Recent studies reported the presence of lineage IV in Nigeria, suggesting that this lineage is expanding in West Africa. In Niger, a close neighbour of Nigeria, PPRV has never been genetically characterized, despite reports of PPR incidence. In this study, pathological samples collected from sick goats were collected in 2013 during a suspected PPR outbreak in southern Niger close to the Nigerian border were compared to samples collected in a previous investigation in October 2001 in south‐western Niger. These strains were characterized by sequencing and phylogenetic analysis to identify their genetic lineage. Our results show that in 2001, lineages I and II were cocirculating in south‐western Niger, whereas the strain that caused the outbreak in 2013 belonged to lineage IV and is closely related to strains identified in Nigeria. These results confirm the progression of lineage IV in West Africa. The process of PPRV lineage replacement and its implications for the epidemiology and the control of the disease in this region are unclear and should be the subject of further studies in the field.     

Peste Des Petits Ruminants in Benin: Persistence of a Single Virus Genotype in the Country for Over 42 Years

Peste des petits ruminants (PPR) is a contagious and often fatal disease affecting sheep and goats. Currently, it is endemic in Africa, the Middle and Near East, the Indian subcontinent and China. Understanding the molecular epidemiology and evolution of PPR virus (PPRV) can assist in the control of the transboundary spread of this economically important disease. We isolated PPRV from pathological and swab samples collected 42 years apart (1969 and 2011) in Benin, West Africa, and sequenced the full genome of two isolates (Benin/B1/1969 and Benin/10/2011). Phylogenetic analysis showed that all of the characterized isolates clustered within viral lineage II and that the 2011 isolates fell into two distinct subgroups. Comparison of the full genome sequences revealed a 95.3% identity at the nucleotide level, while at the protein level, the matrix protein was the most conserved between the two viruses with an identity of 99.7% and only one amino acid substitution over the 42‐year sampling period. An analysis of specific amino acid residues of known or putative function did not identify any significant changes between the two viruses. A molecular clock analysis of complete PPRV genomes revealed that the lineage II viruses sampled here arose in the early 1960s and that these viruses have likely persisted in Benin since this time.     

Serological Detection of Antibodies to Peste des Petits Ruminants Virus in Large Ruminants

Peste des petits ruminants (PPR) is an economically important disease of small ruminants with a rapidly expanding geographical distribution. Peste des petits ruminants virus may manifest in a variety of ways with disease ranging from acute to subclinical. We investigated the exposure of large ruminants to PPRV in areas where the virus is endemic in the small ruminant population by assessing the serological status of groups of animals. This study focused on the Punjab province of Pakistan as an area where the virus is endemic and where mixed farming practices occur enabling close interactions between small and large ruminant populations. An overall PPR seropositivity was detected in 10.0% of cattle and 14.16% of buffaloes. Following an assessment of serological profiles in large ruminants within different age groups, a maximum seroprevalence was observed in cattle (17.5%) and buffaloes (22.5%) over 2 years of age indicating the potential utility of sampling large ruminant populations for PPR serosurveillance. The large ruminants sampled between one and two years of age had similar levels of seropositivity within populations with 11.2% and 16.2% of animals being seropositive, respectively. Current PPR vaccination strategies do not enable the differentiation between infected and vaccinated small ruminants, and as such, the serological surveillance of sheep and goats is of little value. When considering eradication programmes for PPRV, this factor is of great significance. However, where large and small ruminants are farmed together, serological surveillance of large ruminants may provide a snapshot of virus infection within populations where mild disease is present or where small ruminants are regularly vaccinated.     

Detection and molecular characterization of Peste des Petits Ruminants virus from outbreaks in Burundi,December 2017–January 2018

In December 2017, Peste des Petits Ruminants (PPR) emerged in Burundi (East Africa) and rapidly spread to five provinces (Gitega, Kirundo, Mwaro, Muramvya and Karuzi) in the country, causing severe disease and killing more than 4,000 goats in the province of Gitega alone. An initial outbreak investigation was conducted in December 2017 by the Burundi Government Veterinary Services and samples were collected for laboratory confirmation. A competitive Enzyme Linked Immuno‐Sorbent Assay (cELISA: Chinese Patent No. ZL201210278970.9) supplied by the Lanzhou Veterinary Research Institute was used to test 112 sera and results showed around 37.5% positive samples. This high level of PPR positive sera in an animal population where PPR infection and vaccination had not been previously reported indicated the exposure of the animals to PPRV. Subsequently in January 2018, the laboratory tests conducted at the African Union‐Pan African Veterinary Vaccine Centre (AU‐PANVAC) laboratories following a joint investigative mission by the African Union‐Interafrican Bureau for Animal Resources (AU‐IBAR), AU‐PANVAC and the East African Community (EAC) confirmed the presence of PPR in Burundi. Samples tested by conventional RT‐PCR indicated the presence of the PPR virus (PPRV). Confirmatory isolation of the virus was also performed. Phylogenetic analysis revealed that the virus belongs to lineage III and shows a close relationship with PPRV isolates from Kenya in 2011 and Uganda in 2012. A possible explanation for the outbreaks of PPR in Burundi between December 2017 and February 2018 is presented.     

Sequence and Phylogenetic Analyses of the Structural Genes of Virulent Isolates and Vaccine Strains of Peste Des Petits Ruminants Virus from India

Peste des petits ruminants (PPR) is an acute, highly contagious, notifiable and economically important transboundary viral disease of sheep and goats. In this study, sequence and phylogenetic analyses of structural protein genes, namely the nucleocapsid (N), the matrix (M), the fusion (F) and the haemagglutinin (H) coding sequences of virulent and vaccine strains of PPR virus (PPRV), were undertaken to determine the genetic variations between field isolates and vaccine strains. The open reading frame (ORF) of these genes of the isolates/strains was amplified by RT‐PCR, cloned and sequenced. The ORF of N, M, F and H genes was 1578, 1008, 1641 and 1830 nucleotides (nt) in length and encodes polypeptides of 525, 335, 546 and 609 amino acids (aa), respectively, as reported earlier. Comparative sequence analyses of these four genes of isolates/strains were carried out with published sequences. It revealed an identity of 97.7–100% and 97.7–99.8% among the Asian lineage IV and 89.6–98.7% and 89.8–98.9% with other lineages of PPRV at nt and aa levels, respectively. The phylogenetic analyses of these isolates based on the aa sequences showed that all the viruses belonged to lineage IV along with other Asian isolates. This is in agreement with earlier observations that only PPRV lineage IV is in circulation in India since the disease was first reported. Further, sequence analysis of the thermostable/thermo‐adapted vaccine strains showed no significant changes in the functional or structural surface protein–coding gene sequences. It is important to monitor the circulation of the PPRV in susceptible animals by H gene‐based sequence comparisons in addition to the F gene‐ and N gene‐based approaches to identify the distribution and spread of virus in the regular outbreaks that occur in endemic countries like India.     

Peste des petits ruminants in China since its first outbreak in 2007: A 10‐year review

Peste des petits ruminants (PPR ) is a highly infectious disease of small ruminants and caused by small ruminant morbillivirus (SRMV ), formerly called peste‐des‐petits‐ruminants virus (PPRV ). This disease is circulating in Africa (except most countries in southern Africa), the Arabian Peninsula, the Middle East, and Central, East and South‐East Asia. Peste des petits ruminants is still regarded as an exotic disease in China, where its first outbreak was reported in the Ngari region of Tibet in 2007, but effectively controlled by slaughter, vaccination and animal movement restriction in PPR ‐infected areas. However, PPR re‐emerged in Xinjiang of China in December 2013, rapidly spread into much of China in the first half of 2014, but since then was substantially inhibited countrywide. Phylogenetic analysis shows that SRMV s from China share the highest homology with others from its neighbouring countries, possibly indicating the transboundary transmission of SRMV s. In 2015, a national eradication program for PPR was issued and has been being implemented in China, expecting to achieve a PPR‐eradicating aim countrywide by 2020. Here, we reviewed a 10‐year history (2007–2017) of PPR in China, including two major outbreaks, its infection in wild species, development of diagnostics and vaccines, and implementation of the national eradication program.     

First Evidence of Peste des Petits Ruminants (PPR) Virus Circulation in Algeria (Sahrawi Territories): Outbreak Investigation and Virus Lineage Identification

Following reports of increased mortality in the small ruminant population of the Sahrawi territories, western Algeria, between January and May 2010, local veterinary authorities suspected an outbreak of peste des petits ruminants (PPR). An investigation was implemented in May 2010 and followed up in October 2010 in the Sahrawi refugee camps, Tindouf province, with the objective of confirming the circulation of the peste des petits ruminants virus (PPRV). Laboratory results confirmed the presence of PPRV in 33.3% of the samples. Sequence analysis revealed that the virus belonged to Lineage IV and phylogenetic analysis indicated a close relationship (99.3%) with the PPRV isolated during the Moroccan outbreak in 2008.     

Concurrent infection of Bluetongue and Peste‐des‐petits‐ruminants virus in small ruminants in Haryana State of India

Bluetongue (BT ) and peste‐des‐petits‐ruminants (PPR ) are major transboundary diseases of small ruminant, which are endemic in India. Testing of bluetongue virus (BTV ) and peste‐des‐petits‐ruminants virus (PPRV ) from recent outbreaks (2015–2016) in different regions of Haryana State of India revealed that 27.5% of the samples showed the presence of dual infection of BTV and PPRV . Analysis of Seg‐2 of BTV (the serotype‐determining protein) showed the presence of BTV ‐12w in several isolates. However, analysis of N gene fragment amplicons showed that viruses belong to lineage IV were most closely related to a pathogenic strain of PPRV from Delhi. This is the first report of co‐circulation of PPRV lineage IV and bluetongue virus serotype 12 in the state.     

Detection and Genetic Characterization of Lineage IV Peste Des Petits Ruminant Virus in Kazakhstan

Peste des petits ruminant (PPR) is endemic in many Asian countries with expansion of the range in recent years including across China during 2013–2014 (OIE, 2014). Till the end of 2014, no cases of PPR virus (PPRV) were officially reported to the Office Internationale des Epizooties (OIE) from Kazakhstan. This study describes for the first time clinicopathological, epidemiological and genetic characterization of PPRV in 3 farm level outbreaks reported for the first time in Zhambyl region (oblast), southern Kazakhstan. Phylogenetic analysis based on partial N gene sequence data confirms the lineage IV PPRV circulation, similar to the virus that recently circulated in China. The isolated viruses are 99.5–99.7% identical to the PPRV isolated in 2014 from Heilongjiang Province in China and therefore providing evidence of transboundary spread of PPRV. There is a risk of further maintenance of virus in young stock despite vaccination of adult sheep and goats, along livestock trade and pastoral routes, threatening both small livestock and endangered susceptible wildlife populations throughout Kazakhstan.