Cyclic Avian Mass Mortality in the Northeastern United States Is Associated with a Novel Orthomyxovirus

Abstract

Since 1998, cyclic mortality events in common eiders (Somateria mollissima), numbering in the hundreds to thousands of dead birds, have been documented along the coast of Cape Cod, MA, USA. Although longitudinal disease investigations have uncovered potential contributing factors responsible for these outbreaks, detecting a primary etiological agent has proven enigmatic. Here, we identify a novel orthomyxovirus, tentatively named Wellfleet Bay virus (WFBV), as a potential causative agent of these outbreaks. Genomic analysis of WFBV revealed that it is most closely related to members of the Quaranjavirus genus within the family Orthomyxoviridae. Similar to other members of the genus, WFBV contains an alphabaculovirus gp64-like glycoprotein that was demonstrated to have fusion activity; this also tentatively suggests that ticks (and/or insects) may vector the virus in nature. However, in addition to the six RNA segments encoding the prototypical structural proteins identified in other quaranjaviruses, a previously unknown RNA segment (segment 7) encoding a novel protein designated VP7 was discovered in WFBV. Although WFBV shows low to moderate levels of sequence similarity to Quaranfil virus and Johnston Atoll virus, the original members of the Quaranjavirus genus, additional antigenic and genetic analyses demonstrated that it is closely related to the recently identified Cygnet River virus (CyRV) from South Australia, suggesting that WFBV and CyRV may be geographic variants of the same virus. Although the identification of WFBV in part may resolve the enigma of these mass mortality events, the details of the ecology and epidemiology of the virus remain to be determined. IMPORTANCEThe emergence or reemergence of viral pathogens resulting in large-scale outbreaks of disease in humans and/or animals is one of the most important challenges facing biomedicine. For example, understanding how orthomyxoviruses such as novel influenza A virus reassortants and/or mutants emerge to cause epidemic or pandemic disease is at the forefront of current global health concerns. Here, we describe the emergence of a novel orthomyxovirus, Wellfleet Bay virus (WFBV), which has been associated with cyclic large-scale bird die-offs in the northeastern United States. This initial characterization study provides a foundation for further research into the evolution, epidemiology, and ecology of newly emerging orthomyxoviruses, such as WFBV, and their potential impacts on animal and/or human health.

Sinu virus, a novel and divergent orthomyxovirus related to members of the genus Thogotovirus isolated from mosquitoes in Colombia

“…Although the current International Committee on Taxonomy of Viruses (2015) (ICTV) (www.ictvonline.org/virustaxonomy.asp) only lists two species within the genus Thogotovirus , there are now actually eight viruses within the genus: Thogoto (THOV), Dhori (DHOV), Batken (BKNV), Upolu (UPOV), Aransas Bay (ABV), Jos (JOSV), Bourbon (BRBV) and Dielmo orthomyxovirus (DOV) (Allison et al, 2015, Bussetti et al, 2014, Lvov et al, 2015, Briese et al, 2014, Lambert et al, 2015, Temmam et al, 2016). The addition of SINUV to the genus will bring the total number of thogotoviruses to nine.…”

Fidelity and Persistence of Ring-Billed (Larus delawarensis) and Herring (Larus argentatus) Gulls to Wintering Sites

“…Wellfleet Bay virus (WFBV) is a recently described orthomyxovirus isolated from the tissues of Common Eiders (Somateria mollissima) collected on Cape Cod, Massachusetts, US (41854 0 15 00 N, À7082 0 33 00 W) during recurrent mortality events (Allison et al 2015). These mortality events occur regularly in the autumn with less-frequent spring events.…”

Experimental Infection of Common Eider Ducklings with Wellfleet Bay Virus, a Newly Characterized Orthomyxovirus

“…Genetic and antigenic comparisons between WFBV and CyRV indicate that they might be genetic variants of the same virus ( 6 ). It has not yet been determined what, if any, role CyRV played in the Muscovy duck deaths, given that salmonellosis alone is capable of causing a mortality event in waterfowl ( 11 ); however, we suggest that the high death rate observed in ducks with salmonellosis (97%) indicates that co-infection with CyRV might have contributed to the severity of this mortality event.…”

“…We collected tissue samples (lungs, trachea, heart, brain, liver, kidneys, spleen, crop, proventriculus, gizzard, small and large intestine, pancreas, thymus, bursa of Fabricius, adrenal glands, and gonads) from each bird, fixed the samples in neutral-buffered 10% formalin solution, and processed them by standard methods for histopathologic examination. We examined slides by light microscopy and stained for WFBV any slides showing lesions by using immunohistochemistry as previously described (i.e., anti-WFBV polyclonal antibody mouse hyperimmune ascites fluid) ( 6 ). …”

“…Acute hepatic necrosis and variable pancreatic, splenic, and intestinal necrosis were diagnosed in all 4 of the submitted eiders, and a novel enveloped RNA virus, since named Wellfleet Bay virus (WFBV), was isolated from the liver of 2 of the 4 birds. Genetic analysis of WFBV demonstrated that it is most closely related to members of the Quaranjavirus genus within the family Orthomyxoviridae ( 6 ). Since 2006, the NWHC has diagnosed hepatic necrosis and variable splenic, intestinal, and pancreatic necrosis in common eiders from which WFBV was isolated during 4 separate mass mortality events occurring at Wellfleet Bay during September 2007–October 2011.…”