Origin, Evolution, and Virulence of Porcine Deltacoronaviruses in the United States

ABSTRACT A novel porcine deltacoronavirus (PdCV) was first discovered in Ohio and Indiana in February 2014, rapidly spread to other states in the United States and Canada, and caused significant economic loss in the swine industry. The origin and virulence of this novel porcine coronavirus are not k...

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Main Authors: Yuanmei Ma, Yu Zhang, Xueya Liang, Fangfei Lou, Michael Oglesbee, Steven Krakowka, Jianrong Li
Format: Article
Language:English
Published: American Society for Microbiology 2015-05-01
Series:mBio
Online Access:https://journals.asm.org/doi/10.1128/mBio.00064-15
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author Yuanmei Ma
Yu Zhang
Xueya Liang
Fangfei Lou
Michael Oglesbee
Steven Krakowka
Jianrong Li
author_facet Yuanmei Ma
Yu Zhang
Xueya Liang
Fangfei Lou
Michael Oglesbee
Steven Krakowka
Jianrong Li
author_sort Yuanmei Ma
collection DOAJ
description ABSTRACT A novel porcine deltacoronavirus (PdCV) was first discovered in Ohio and Indiana in February 2014, rapidly spread to other states in the United States and Canada, and caused significant economic loss in the swine industry. The origin and virulence of this novel porcine coronavirus are not known. Here, we characterized U.S. PdCV isolates and determined their virulence in gnotobiotic and conventional piglets. Genome analyses revealed that U.S. PdCV isolates possess unique genetic characteristics and share a close relationship with Hong Kong and South Korean PdCV strains and coronaviruses (CoVs) of Asian leopard cats and Chinese ferret-badgers. The PdCV-positive intestinal content (Ohio CVM1) and the cell culture-adapted PdCV Michigan (MI) strain were orally inoculated into gnotobiotic and/or conventional piglets. Within 1 to 3 days postinfection, profuse watery diarrhea, vomiting, and dehydration were observed. Clinical signs were associated with epithelial necrosis in the gastric pits and small intestine, the latter resulting in severe villous atrophy. Mild interstitial pneumonia was identified in the lungs of PdCV-infected piglets. High levels of viral RNA (8 to 11 log RNA copies/g) were detected in intestinal tissues/luminal contents and feces of infected piglets, whereas moderate RNA levels (2 to 5 log RNA copies/g) were detected in blood, lung, liver, and kidney, indicating multisystemic dissemination of the virus. Polyclonal immune serum against PdCV but not immune serum against porcine epidemic diarrhea virus (PEDV) reacted with PdCV-infected small-intestinal epithelial cells, indicating that PdCV is antigenically distinct from PEDV. Collectively, we demonstrate for the first time that PdCV caused severe gastrointestinal diseases in swine. IMPORTANCE Porcine coronaviruses (CoVs) are major viral infectious diseases of swine. Examples of porcine CoVs include porcine transmissible gastroenteritis coronavirus (TGEV), porcine epidemic diarrhea virus (PEDV), and porcine respiratory coronavirus (PRCV). In February 2014, another porcine CoV, porcine deltacoronavirus (PdCV), emerged in Ohio and Indiana and subsequently spread rapidly across the United States and Canada, causing significant economic losses. Here, we report the detailed genetic characterization, phylogeny, and virulence of emergent PdCV strains in the United States. We found that PdCV caused severe diarrhea, vomiting, and dehydration in gnotobiotic and conventional piglets, signs that were clinically indistinguishable from those caused by PEDV and TGEV. In addition to extensive intestinal lesions, PdCV caused significant lesions in the stomach and mild pulmonary lesions that have not been reported for TGEV and PEDV. The finding that PdCV is a significant enteric disease of swine highlights the need to develop effective measures to control this disease.
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spelling doaj.art-d67087ae96fd4b51a174095006fce6f22022-12-21T20:37:06ZengAmerican Society for MicrobiologymBio2150-75112015-05-016210.1128/mBio.00064-15Origin, Evolution, and Virulence of Porcine Deltacoronaviruses in the United StatesYuanmei Ma0Yu Zhang1Xueya Liang2Fangfei Lou3Michael Oglesbee4Steven Krakowka5Jianrong Li6Department of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio, USADepartment of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio, USADepartment of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio, USADepartment of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio, USADepartment of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio, USADepartment of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio, USADepartment of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio, USAABSTRACT A novel porcine deltacoronavirus (PdCV) was first discovered in Ohio and Indiana in February 2014, rapidly spread to other states in the United States and Canada, and caused significant economic loss in the swine industry. The origin and virulence of this novel porcine coronavirus are not known. Here, we characterized U.S. PdCV isolates and determined their virulence in gnotobiotic and conventional piglets. Genome analyses revealed that U.S. PdCV isolates possess unique genetic characteristics and share a close relationship with Hong Kong and South Korean PdCV strains and coronaviruses (CoVs) of Asian leopard cats and Chinese ferret-badgers. The PdCV-positive intestinal content (Ohio CVM1) and the cell culture-adapted PdCV Michigan (MI) strain were orally inoculated into gnotobiotic and/or conventional piglets. Within 1 to 3 days postinfection, profuse watery diarrhea, vomiting, and dehydration were observed. Clinical signs were associated with epithelial necrosis in the gastric pits and small intestine, the latter resulting in severe villous atrophy. Mild interstitial pneumonia was identified in the lungs of PdCV-infected piglets. High levels of viral RNA (8 to 11 log RNA copies/g) were detected in intestinal tissues/luminal contents and feces of infected piglets, whereas moderate RNA levels (2 to 5 log RNA copies/g) were detected in blood, lung, liver, and kidney, indicating multisystemic dissemination of the virus. Polyclonal immune serum against PdCV but not immune serum against porcine epidemic diarrhea virus (PEDV) reacted with PdCV-infected small-intestinal epithelial cells, indicating that PdCV is antigenically distinct from PEDV. Collectively, we demonstrate for the first time that PdCV caused severe gastrointestinal diseases in swine. IMPORTANCE Porcine coronaviruses (CoVs) are major viral infectious diseases of swine. Examples of porcine CoVs include porcine transmissible gastroenteritis coronavirus (TGEV), porcine epidemic diarrhea virus (PEDV), and porcine respiratory coronavirus (PRCV). In February 2014, another porcine CoV, porcine deltacoronavirus (PdCV), emerged in Ohio and Indiana and subsequently spread rapidly across the United States and Canada, causing significant economic losses. Here, we report the detailed genetic characterization, phylogeny, and virulence of emergent PdCV strains in the United States. We found that PdCV caused severe diarrhea, vomiting, and dehydration in gnotobiotic and conventional piglets, signs that were clinically indistinguishable from those caused by PEDV and TGEV. In addition to extensive intestinal lesions, PdCV caused significant lesions in the stomach and mild pulmonary lesions that have not been reported for TGEV and PEDV. The finding that PdCV is a significant enteric disease of swine highlights the need to develop effective measures to control this disease.https://journals.asm.org/doi/10.1128/mBio.00064-15
spellingShingle Yuanmei Ma
Yu Zhang
Xueya Liang
Fangfei Lou
Michael Oglesbee
Steven Krakowka
Jianrong Li
Origin, Evolution, and Virulence of Porcine Deltacoronaviruses in the United States
mBio
title Origin, Evolution, and Virulence of Porcine Deltacoronaviruses in the United States
title_full Origin, Evolution, and Virulence of Porcine Deltacoronaviruses in the United States
title_fullStr Origin, Evolution, and Virulence of Porcine Deltacoronaviruses in the United States
title_full_unstemmed Origin, Evolution, and Virulence of Porcine Deltacoronaviruses in the United States
title_short Origin, Evolution, and Virulence of Porcine Deltacoronaviruses in the United States
title_sort origin evolution and virulence of porcine deltacoronaviruses in the united states
url https://journals.asm.org/doi/10.1128/mBio.00064-15
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