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J Virol. 2016 Dec 16;91(1). pii: e01711-16. doi: 10.1128/JVI.01711-16. Print 2017 Jan 1.

Differential Infection Patterns and Recent Evolutionary Origins of Equine Hepaciviruses in Donkeys.

Author information

1
Institute of Experimental Virology, TWINCORE, Center for Experimental and Clinical Infection Research Hannover, Hannover, Germany.
2
Institute of Virology, University of Bonn Medical Centre, Bonn, Germany.
3
German Centre for Infection Research (DZIF), Bonn-Cologne, Germany.
4
Department of Microbiology and Immunology, Rega Institute, KU Leuven-University of Leuven, Leuven, Belgium.
5
Medical Immunology Research Unit, National Medical Center Siglo XXL, Mexican Social Security Institute (IMSS), Mexico City, Mexico.
6
Equine Medicine and Surgery Department FMVZ-UNAM, Mexico City, Mexico.
7
ANSES, Laboratory for Equine Diseases, Goustranville, France.
8
Clinic for Obstetrics, Gynecology and Andrology of Large and Small Animals, Justus-Liebig-Universität Giessen, Giessen, Germany.
9
Koret School of Veterinary Medicine, Rehovot, Israel.
10
Istituto Zooprofilattico Sperimentale Lazio e Toscana, Rome, Italy.
11
Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy.
12
Trakia University, Faculty of Veterinary Medicine, Department of Veterinary Microbiology, Infectious and Parasitic Diseases, Stara Zagora, Bulgaria.
13
Trakia University, Faculty of Veterinary Medicine, Department of Internal Diseases, Stara Zagora, Bulgaria.
14
Trakia University, Faculty of Veterinary Medicine, Department of Pharmacology, Veterinary Physiology, and Physiological Chemistry, Stara Zagora, Bulgaria.
15
Department of Animal Health, University of Córdoba, Córdoba, Spain.
16
International Livestock Research Institute, Nairobi, Kenya.
17
Institute of Veterinary Bacteriology, University of Bern, Bern, Switzerland.
18
Faculty of Veterinary Medicine, Università degli Studi di Teramo, Teramo, Italy.
19
Department of Veterinary Medicine, Università degli Studi di Milano, Milan, Italy.
20
Clinic for Horses, University of Veterinary Medicine Hannover, Foundation, Hannover, Germany.
21
Institute of Experimental Virology, TWINCORE, Center for Experimental and Clinical Infection Research Hannover, Hannover, Germany Eike.Steinmann@twincore.de drexler@virology-bonn.de.
22
Institute of Virology, University of Bonn Medical Centre, Bonn, Germany Eike.Steinmann@twincore.de drexler@virology-bonn.de.

Abstract

The hepatitis C virus (HCV) is a major human pathogen. Genetically related viruses in animals suggest a zoonotic origin of HCV. The closest relative of HCV is found in horses (termed equine hepacivirus [EqHV]). However, low EqHV genetic diversity implies relatively recent acquisition of EqHV by horses, making a derivation of HCV from EqHV unlikely. To unravel the EqHV evolutionary history within equid sister species, we analyzed 829 donkeys and 53 mules sampled in nine European, Asian, African, and American countries by molecular and serologic tools for EqHV infection. Antibodies were found in 278 animals (31.5%), and viral RNA was found in 3 animals (0.3%), all of which were simultaneously seropositive. A low RNA prevalence in spite of high seroprevalence suggests a predominance of acute infection, a possible difference from the mostly chronic hepacivirus infection pattern seen in horses and humans. Limitation of transmission due to short courses of infection may explain the existence of entirely seronegative groups of animals. Donkey and horse EqHV strains were paraphyletic and 97.5 to 98.2% identical in their translated polyprotein sequences, making virus/host cospeciation unlikely. Evolutionary reconstructions supported host switches of EqHV between horses and donkeys without the involvement of adaptive evolution. Global admixture of donkey and horse hepaciviruses was compatible with anthropogenic alterations of EqHV ecology. In summary, our findings do not support EqHV as the origin of the significantly more diversified HCV. Identification of a host system with predominantly acute hepacivirus infection may enable new insights into the chronic infection pattern associated with HCV.

IMPORTANCE:

The evolutionary origins of the human hepatitis C virus (HCV) are unclear. The closest animal-associated relative of HCV occurs in horses (equine hepacivirus [EqHV]). The low EqHV genetic diversity implies a relatively recent acquisition of EqHV by horses, limiting the time span for potential horse-to-human infections in the past. Horses are genetically related to donkeys, and EqHV may have cospeciated with these host species. Here, we investigated a large panel of donkeys from various countries using serologic and molecular tools. We found EqHV to be globally widespread in donkeys and identify potential differences in EqHV infection patterns, with donkeys potentially showing enhanced EqHV clearance compared to horses. We provide strong evidence against EqHV cospeciation and for its capability to switch hosts among equines. Differential hepacivirus infection patterns in horses and donkeys may enable new insights into the chronic infection pattern associated with HCV.

KEYWORDS:

donkey; equine hepacivirus; evolution; hepatitis C virus; pathogenesis

PMID:
27795428
PMCID:
PMC5165184
DOI:
10.1128/JVI.01711-16
[Indexed for MEDLINE]
Free PMC Article

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