Novel Avian Coronavirus and Fulminating Disease in Guinea Fowl, France

Etienne Liais1, Guillaume Croville1, Jérôme Mariette, Maxence Delverdier, Marie-Noëlle Lucas, Christophe Klopp, Jérôme Lluch, Cécile Donnadieu, James S. Guy, Léni Corrand, Mariette F. Ducatez, and Jean-Luc Guérin

Author affiliations: French National Institute for Agricultural Research (INRA), Toulouse, France (E. Liais, G. Croville, M. Delverdier, M.-N. Lucas, L. Corrand, M.F. Ducatez, J.-L. Guérin);Ecole Nationale Vétérinaire, Toulouse (E. Liais, G. Croville, M. Delverdier, M.-N. Lucas, L. Corrand, M.F. Ducatez, J.-L. Guérin);INRA 31326, Castanet-Tolosan, France (J. Mariette, C. Klopp; J. Lluch, C. Donnadieu); North Carolina State University, Raleigh, North Carolina, USA (J. Guy)

Abstract

For decades, French guinea fowl have been affected by fulminating enteritis of unclear origin. By using metagenomics, we identified a novel avian gammacoronavirus associated with this disease that is distantly related to turkey coronaviruses. Fatal respiratory diseases in humans have recently been caused by coronaviruses of animal origin.

Fulminating disease (also referred to as X disease) of guinea fowl (Numida meleagris) is an acute enteritis characterized by intense prostration and a very high death rate, leading to the almost complete destruction of affected flocks. Lesions are generally limited to severe enteritis and, in some birds, pancreatic degeneration. This disease is uncommon, but its fulminating evolution raises concerns of differential diagnoses with highly pathogenic avian influenza.

Fulminating disease has been reported for decades in the French guinea fowl industry, and although its viral origin was previously suspected, the virus remained unknown. During the 1980s, French groups investigated the etiology of the disease. Because propagation on cells or embryos remained unsuccessful and molecular tools were unavailable, etiologic hypotheses were based mostly on electron microscopy findings. The groups reached different conclusions, proposing candidates such as toga-like virus (1), reovirus, or herpesvirus (2). More recently, astroviruses have been associated with catarrhal enteritis in guinea poults (i.e., young guinea fowl) (3), but these viruses were not detected in birds affected by fulminating disease (data not shown).

We investigated field cases and performed an experimental reproduction of fulminating disease and identified its agent by using unbiased high-throughput sequencing. We propose a gammacoronavirus of a novel genotype as the most likely causal agent of fulminating disease. Coronaviruses (CoVs) are zoonotic. The novel human Middle East respiratory syndrome CoV, a betacoronavirus that was first isolated in 2012 in Saudi Arabia, is most closely related toTylonycteris bat CoV HKU4 and Pipistrellus bat CoV HKU5 (4); severe acute respiratory syndrome–CoV originated from a betacoronavirus that spread from bats to civets and humans (5).