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Ahead of Print -Distinct Characteristics and Complex Evolution of PEDV Strains, North America, May 2013–February 2014 - Volume 20, Number 10—October 2014 - Emerging Infectious Disease journal - CDC

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Ahead of Print -Distinct Characteristics and Complex Evolution of PEDV Strains, North America, May 2013–February 2014 - Volume 20, Number 10—October 2014 - Emerging Infectious Disease journal - CDC



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Volume 20, Number 10—October 2014

Research

Distinct Characteristics and Complex Evolution of PEDV Strains, North America, May 2013–February 2014

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Tables

Technical Appendicies

Anastasia N. Vlasova1, Douglas Marthaler1Comments to Author , Qiuhong Wang, Marie R. Culhane, Kurt D. Rossow, Albert Rovira, James Collins, and Linda J. Saif
Author affiliations: The Ohio State University, Wooster, Ohio, USA (A.N. Vlasova, Q. Wang, L.J. Saif); University of Minnesota Veterinary Diagnostic Laboratory, St. Paul, Minnesota, USA (D. Marthaler, M.R. Culhane, K.D. Rossow, A. Rovira, J. Collins)

Abstract

Porcine epidemic diarrhea virus (PEDV), which emerged in the United States in 2013, has spread throughout North America. Limited availability of PEDV complete genomes worldwide has impeded our understanding of PEDV introduction into the United States. To determine the relationship between the North American strains and global emerging and historic PEDV strains, we sequenced and analyzed complete genomes of 74 strains from North America; the strains clustered into 2 distinct clades. Compared with the initially reported virulent US PEDV strains, 7 (9.7%) strains from 4 states contained insertions and deletions in the spike gene (S INDELs). These S INDEL strains share 99.8%–100% nt identity with each other and 96.2%–96.7% nt identity with the initial US strains. Furthermore, the S INDEL strains form a distinct cluster within North American clade II, sharing 98.6%–100% nt identity overall. In the United States, the S INDEL and original PEDV strains are co-circulating and could have been introduced simultaneously.
Porcine epidemic diarrhea virus (PEDV) (family Coronaviridae family, genus alphacoronavirus) has an enveloped, single-stranded, positive-sense RNA genome of ≈28 kb (1). The 5′ two thirds of the genome contains 2 large open reading frames (ORFs), 1a and 1b, that encode 2 nonstructural polyproteins, pp1a and pp1b, that direct genome replication and transcription. The remaining PEDV genome contains ORFs specifying structural and nonstructural proteins in the following order: spike (S), ORF 3, envelope (E), membrane (M) and nucleoprotein (N) (2,3).
Porcine epidemic diarrhea (PED) was first documented in the United Kingdom in 1971 as a swine disease resembling transmissible gastroenteritis (4). In 1978, the etiologic agent of PED was identified in Belgium as a new coronavirus and was designated as PEDV, prototype strain CV777 (1). Within 2 decades, PEDV was reported in several other European countries; Hungary, Italy, Germany, France, Switzerland, and the Czech Republic (5). Currently, the virus causes only isolated outbreaks in Europe. In Asia, PEDV was first identified in 1982 and is now considered endemic, causing substantial economic losses to pork producers in China, South Korea, Thailand, and Vietnam (5). However, it was not until 2010 that massive PED outbreaks were reported in China; the outbreaks have been characterized by 80%–100% illness among infected swine herds and a 50%–90% mortality rate among infected suckling piglets (6–8).
North America was free of PEDV until its sudden and intense emergence in the United States in April 2013 (9). Since then, PEDV has spread rapidly across the United States, causing high rates of death among piglets and substantial economic losses (10–12). As of July 24, 2014, PEDV had been reported in 31 US states (13). In Canada, PEDV was first detected in January 2014 on a pig farm in Ontario Province; since then, the virus has been reported on farms in Manitoba, Prince Edward Island, and Quebec Provinces (14), continuing its spread throughout North America. There are no official reports of PEDV in Mexico; however, in 2013, the University of Minnesota (UM) Veterinary Diagnostic Laboratory (St. Paul, MN, USA) tested swine samples from Mexico and found them positive for PEDV.
The complete genomic sequence of the PEDV prototype strain, CV777, was determined in 2001 (15). A decade later, complete genomes were sequenced for several PEDV strains from China and South Korea (6,8,15–22). Comparisons of full-length genomes showed that different PEDV strains are more closely related to bat alphacoronaviruses than to other known alphacoronaviruses (23), suggesting that interspecies transmission of coronavirus may have occurred decades ago between bats and pigs or through an intermediate host.
Phylogenetic analysis has shown that some PEDV strains that have reported decreased virulence in the field contain distinct insertions and deletions in the S gene (S INDELS). Soon after the emergence of PEDV in the United States, the complete genomes were determined for several strains from Colorado, Minnesota, and Iowa, USA (10,24,25); these PEDV strains shared ≥99.5% nt identity with strain AH2012 from China, suggesting a common ancestor for that strain and US strains (25,26). An additional 43 complete-genome PEDV sequences are now available: 16 from the United States, including a recent PEDV variant from Ohio (OH851) that contains specific S INDELs and was reported with reduced disease severity (27); 23 from China; and 4 from South Korea. In addition, new, complete-genome PEDV sequences are being generated and released almost monthly.
A major impediment to understanding the origin, evolution, and diversity of PEDV in the United States is the lack of complete-genome PEDV sequences worldwide. To determine the phylogenetic relationship between the new US strains and the globally emerging and historic PEDV strains, we sequenced and analyzed the complete genomes of 74 strains from North America.

Dr Vlasova is a research scientist at The Ohio State University. Her primary research interest is the use of a gnotobiotic pig model to focus on viral epidemiology, vaccine development, gut microbiome and probiotic effects on immunity, and innate immune responses to enteric viral infections; and Dr Marthaler is a scientist at the University of Minnesota. His primary research interests are the epidemiology and phylogenetic analysis of porcine enteric viruses.

Acknowledgments

We thank the staff of the UM Veterinary Diagnostic Laboratory for technical assistance.
Funding was provided by the Rapid Agricultural Response Fund, established by the Minnesota legislature and administered by the UM Agricultural Experiment Station; the UM Veterinary Diagnostic Laboratory; and the National Pork Board (grant no. 13-238).

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Technical Appendix

Suggested citation for this article: Vlasova AN, Marthaler D, Wang Q, Culhane MR, Rossow KD, Rovira A, et al. Distinct characteristics and complex evolution of PEDV strains, North America, May 2013–February 2014. Emerg Infect Dis. 2014 Oct [date cited].http://dx.doi.org/10.3201/eid2010.140491
DOI: 10.3201/eid2010.140491
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