Avian Bornavirus: A Common and Emerging Pathogen in North American Waterfowl

Avian Bornavirus Order Mononegavirales; Family Bornaviridae Order Mononegavirales; Family Bornaviridae Enveloped Enveloped Non-segmented, negative strand RNA genome; encodes 6 proteins Non-segmented, negative strand RNA genome; encodes 6 proteins Neurotropic Neurotropic Replication is nuclear, non-cytopathic, highly cell-associated Replication is nuclear, non-cytopathic, highly cell-associated ABV-CG infected DEF showing intense nuclear staining (anti-N) and diffuse cytoplasmic staining

N G M P L X Enveloped Helical nucleocapsid Single glycoprotein Anatomy of a bornavirus

Genome Arrangement S1S3 S2 T1T3T2T4 5’ 3’ S1-3 transcript Start sites T1-4 transcript Termination sites At least 8 transcripts generated by use of alternative transcript start and stop sites and splicing

BORNA Type Species: Borna disease virus (BDV) Until 2008 the only bornavirus Highly neurotropic Highly neurotropic

The highest mortality is in horses and sheep The highest mortality is in horses and sheep BDV infects other mammals, including cats (staggering disease) and humans (psychiatric disease?) BDV infects other mammals, including cats (staggering disease) and humans (psychiatric disease?) Natural transmission of BDV via small mammalian vectors (and birds?) Natural transmission of BDV via small mammalian vectors (and birds?) Borna Disease Bank vole Bi-colored white toothed shrew

Neurologic and Digestive tract components Major killer of parrots in aviculture since the 1970s Avian bornavirus identified at the etiologic agent in 2008 ‘Avian Bornavirus Syndrome’ Ataxia Blindness Abnormal head movements Seizures Neuronal Signs Gastrointestinal Signs Undigested food Diarrhea Weight loss Starvation Enlarged proventriculus ABV Transmission: Fecal Oral Airborne spread Vertical transmission

ABV4 and ABV2 are by far the most common in the captive parrot population

Proventricular Impaction Associated with Nonsuppurative Encephalomyelitis and Ganglioneuritis in 2 Canada Geese. Journal of Wildlife Diseases : When and how did avian bornavirus enter the captive parrot population?

Detection of ABV in Cloacal Swabs 4% 2.7% 6.4% Samples were collected by USDA-Fish and Wildlife services, for H5N1 AIV detection Used RT-PCR to test > 600 samples

Incidence of ABV RNA in Brain Samples No. individuals 44% 9% 14.5% 19% 10% 24% 33% 6.5% 22% 8.3% 15.3% Culled for airplane avoidance

Avian Bornavirus in Waterfowl

(0/7) (0/4) (4/36) (0/7) (4/12) (0/1) (0/35) Incidence of ABV in Gulls in NY and NJ

Mute Swan MallardGull Canada Goose

ABV1 ABV2 ABV3 ABV4 ABV5 ABV7 ABV Canada goose ABV Canary BDV ABV EF Units of measure are substitutions per nucleotide of the bornavirus genome Bornavirus phylogeny (2012) 81 – 83% nt identity 70 – 72% nt identity

ABV1 ABV2 ABV3 ABV4 ABV5 ABV7 ABV Canada goose ABV Canary BDV ABV EF Units of measure are substitutions per nucleotide of the bornavirus genome Bornavirus phylogeny (2014) 81 – 83% nt identity 70 – 72% nt identity

Is ABV a major cause of morbidity and mortality in wild birds?

Retrospective Study: Canada Geese and Trumpeter Swans Delnatte, P. Ojkic, D. DeLay, J. Campbell, D., Crawshaw, G & D. Smith Pathology and diagnosis of avian bornavirus infection in wild Canada geese (Branta canadensis), trumpeter swans (Cygnus buccinator) and mute swans (Cygnus olor) in Canada: a retrospective study. Avian Pathology, 42:2, , DOI: / Samples collected between 1992 and samples met the case criteria (non-supportive encephalitis, no diagnosis) 40 (78%) were ABV positive 9 ‘control’ samples 1 (11%) was ABV positive

Lymphocytic infiltrates in brain of a PCR positive gull Gull, New Jersey, US

Mallard 89 (2014) retina, IHC00 ABV antigen in retina of a PCR positive mallard duck

Ongoing study: ABV infection in a Canada goose with ataxia and weight- loss (2014)* Maureen Murray, DVM, DABVP Clinical Assistant Professor Wildlife Clinic Tufts Cummings School of Veterinary Medicine *Submitted to the Wildlife Clinic, Tufts Cummings School of Veterinary Medicine PCR + Virus growth + Lymphocytic infiltrates (H&E) + Immunohistochemistry (ABV N) +

Ongoing study: White-winged dove* Neurologic signs PCR + (ABV2) Lymphocytic infiltrates (H&E) + Immunohistochemistry (ABV N) + *Submitted to Texas A&M College of Veterinary Medicine

ABV1 ABV2 ABV3 ABV4 ABV5 ABV7 ABV Canada goose ABV Canary BDV ABV EF Units of measure are substitutions per nucleotide of the bornavirus genome Bornavirus phylogeny (2014) 81 – 83% nt identity 70 – 72% nt identity

Acknowledgements Texas A&M Jianhua Guo Lina Covaleda Negin Yousefpour Sameer Hamid Jean Leal de Araujo Debra Turner J. Jill Heatley Sharman Hoppes Jeffrey Musser Ian Tizard USDA/APHIS Wildlife Services Seth Swafford John Barock California Animal Health and Food Safety Laboratory H. L. Shivaprasad University of Guelph Dale Smith Pauline Delnatte This work was funded in part by the Richard M Schubot Endowment at Texas A&M University.

January 15, 2009, US Airways Flight 1549 Do ABV-infected geese get out of the way?