Ahead of Print -Molecular Evolution of Peste des Petits Ruminants Virus - Volume 20, Number 12—December 2014 - Emerging Infectious Disease journal - CDC

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Ahead of Print -Molecular Evolution of Peste des Petits Ruminants Virus - Volume 20, Number 12—December 2014 - Emerging Infectious Disease journal - CDC

Volume 20, Number 12—December 2014

Research

Molecular Evolution of Peste des Petits Ruminants Virus

On This Page

• Materials and Methods
• Results
• Discussion
• Suggested Citation

Figures

• Figure 1
• Figure 2
• Figure 3
• Figure 4
• Figure 5
• Figure 6

Tables

• Table 1
• Table 2
• Table 3
• Table 4

Murali Muniraju, Muhammad Munir, AravindhBabu R. Parthiban, Ashley C. Banyard, Jingyue Bao, Zhiliang Wang, Chrisostom Ayebazibwe, Gelagay Ayelet, Mehdi El Harrak, Mana Mahapatra, Geneviève Libeau, Carrie Batten, and Satya Parida 

Author affiliations: The Pirbright Institute, Pirbright, UK (M. Muniraju, M. Munir, M. Mahapatra, C. Batten, S. Parida); National Institute for Animal Biotechnology, Hyderabad, India (A.R. Parthiban, S Parida); Animal Health and Veterinary Laboratories Agency, Weybridge, UK (A.C. Banyard); China Animal Health and Epidemiology Centre, Qingdao, China (J. Bao, Z. Wang); National Animal Disease Diagnostics and Epidemiology Centre, Entebbe, Uganda (C. Ayebazibwe); National Veterinary Institute, Debre Zeit, Ethiopia (G. Ayelet); Société de Productions Pharmaceutiques et Vétérinaires, Rabat, Morocco (M. El Harrak); Le Centre de Cooperation Internationale en Recherche Agronomique pour le Développement, Montpellier (G. Libeau)

Suggested citation for this article

Abstract

Despite safe and efficacious vaccines against peste des petits ruminants virus (PPRV), this virus has emerged as the cause of a highly contagious disease with serious economic consequences for small ruminant agriculture across Asia, the Middle East, and Africa. We used complete and partial genome sequences of all 4 lineages of the virus to investigate evolutionary and epidemiologic dynamics of PPRV. A Bayesian phylogenetic analysis of all PPRV lineages mapped the time to most recent common ancestor and initial divergence of PPRV to a lineage III isolate at the beginning of 20th century. A phylogeographic approach estimated the probability for root location of an ancestral PPRV and individual lineages as being Nigeria for PPRV, Senegal for lineage I, Nigeria/Ghana for lineage II, Sudan for lineage III, and India for lineage IV. Substitution rates are critical parameters for understanding virus evolution because restrictions in genetic variation can lead to lower adaptability and pathogenicity.

Peste des petits ruminants is a highly contagious and devastating viral disease of small ruminants that is endemic to much of Africa, the Middle East, and Asia (1,2). The causative agent, PPRV virus (PPRV), belongs to the familyParamyxoviridae, genus Morbillivirus (3) and groups with rinderpest virus (RPV), measles virus (MV), and canine distemper virus. Sheep and goats are the major hosts of PPRV, and infection has also been reported in a few wild small ruminant species (2). Researchers have speculated that RPV eradication has further enabled the spread of PPRV (4,5). Transmission of PPRV from infected goats to cattle has been recently reported (6), and PPRV antigen has been detected in lions (7) and camels (8). These reports suggest that PPRV can switch hosts and spread more readily in the absence of RPV (4,6,8). This host range switch had previously been seen after eradication of smallpox virus, which created a niche for monkeypox and cowpox viruses to cross the species barrier into humans (4).

PPRV has caused numerous serious epidemics in small ruminant populations across sub-Saharan Africa, the Middle East, and major parts of the Indian subcontinent where PPRV is considered endemic (1). In recent years, PPRV has extended its range southward in Africa as far as southern Tanzania (2008) and the Democratic Republic of Congo and Angola (2012). PPR outbreaks have also been reported across North Africa, including within Tunisia (2006), Morocco (2008), and Algeria (2011). In addition, within Europe, Turkey reported ≈20 laboratory-confirmed PPR outbreaks in sheep and goats during 2011–2012. In southwestern Asia, the virus spread to Tibet (2007) and has recently been reported throughout China (2013–2014). It is unclear what factors have favored emergence and spread of the disease, but millions of small ruminants across these regions must now be considered at high risk for infection with PPRV (9). The huge effect on small ruminant production has resulted in PPRV emerging as a global animal health concern.

The molecular epidemiology of PPRV, which is based on sequence comparison of a small region of the fusion (F) gene (322 nt) or the nucleoprotein (N) gene (255 nt), has identified 4 distinct lineages (I–IV) of PPRV (2). However, this analysis has not generated much information on the evolution and dispersal of PPRV lineages. Lineage I PPRV had gone undetected for 19 years being detected in Senegal in 1994. Lineage IV PPRV, which was believed initially to be confined to India and the Middle East, now has a wider geographic presence and appears to be evolving rapidly. Many aspects of PPRV evolution, such as ancestral virus location, divergence and time of origin, and historical and geographic patterns of spread, are poorly understood (10). A better understanding of the evolution of PPRV would enable prediction of how these viruses will lead to further outbreaks and epidemics and provide data for control strategies.

Advanced sequencing technologies have enabled molecular epidemiologic studies of viruses in which whole gene and complete genome data are used to enhance and clarify the evolutionary dynamics of viral infectious disease (11). We analyzed genome data for all 4 lineages of PPRV. This analysis will enable a more precise evolutionary and phylogenetic assessment of the relationships between lineages by reducing the associated estimation errors and increased higher confidence in estimates.

Mr Muniraju is a final year doctoral student at The Pirbright Institute, Pirbright, UK. His primary research interests are epidemiologic studies of PPRV and developing marker vaccines for peste des petits ruminants by using reverse genetics techniques.

Acknowledgments

We thank Vincent Michaud for his critical reading of and comments on the manuscript.

This study was supported by grants EU-BBSRC Anihwa BB/L013657/1, BBSRC-DFID CIDLID BB/H009485/1, and DBT-BBSRC FADH BB/L004801/1.

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Figures

• Figure 1. Mean ratios of nonsynonymous (dN) to synonymous (dS) substitutions per site of concatenated coding regions of peste des petits ruminants virus genome. Proportion of dS substitutions per potential dS...
• Figure 2. Time-scaled Bayesian maximum clade credibility phylogeny tree based on peste des petits ruminants virus complete genome sequences. The tree was constructed by using the uncorrelated exponential distribution model and...
• Figure 3. Time-scaled Bayesian MCC phylogeny tree based on peste des petits ruminants virus (PPRV), rinderpest virus (RPV), and measles virus (MV) complete genome sequences. The tree was constructed by using...
• Figure 4. Bayesian skyline plot showing demographic history of global peste des petits ruminants viruses sampled during 1968–2012. Genetic diversity was estimated by using a partial nucleoprotein gene dataset (n =...
• Figure 5. Maximum clade credibility tree constructed for the geospatial analysis of peste des petits ruminants viruses by using complete genome data. Nodes are colored according to the most probable location...
• Figure 6. Probability of root locations of the most recent common ancestral peste des petits ruminants (PPRV). MCC trees were obtained by using the continuous time Markov chain and Bayesian stochastic...

Tables

• Table 1. Peste des petits ruminants virus isolates used for complete genome analysis
• Table 2. Nucleotide and amino acid sequence differences in complete genomes of peste des petits ruminants virus lineages
• Table 3. Nucleotide substitution rates at codon positions of peste des petits ruminants virus genes by BEAST analysis and dN/dS by SLAC
• Table 4. Bayesian Markov chain Monte Carlo analysis for genomes of peste des petits ruminants virus

Suggested citation for this article: Muniraju M, Munir M, Parthiban AR, Banyard AC, Bao J, Wang Z, et al. Molecular evolution of peste des petits ruminants virus. Emerg Infect Dis [Internet]. 2014 Dec [date cited]. http://dx.doi.org/10.3201/eid2012.140684

DOI: 10.3201/eid2012.140684

1Preliminary results were presented at the 15th International Negative Strand Virus Meeting; Granada, Spain, June 16–21, 2013 (http://www.nsvmeeting2013.com/sites/default/files/nsvmeeting2013_program.pdf).