Avian Flu Diary: Preprint: Rapid mortality in Captive Bush Dogs (Speothos venaticus) Caused by H5N1 At A Wildlife Center In the UK

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#18,016

Just over 13 months ago the UK government announced (see below) the deaths of 10 captive bush dogs (in November of 2022) apparently due to HPAI H5N1. At the time it wasn't clear why there had been a 5-month delay in detecting the virus.

Research and analysis
Confirmed findings of influenza of avian origin in captive mammals

Published 17 March 2023
Applies to England, Scotland and Wales

Details of confirmed findings of influenza of avian origin in captive mammals in Great Britain (England, Scotland and Wales).
South American bush dogs, March 2023

Ten South American bush dogs (Speothos venaticus venaticus) have tested positive for highly pathogenic avian influenza (H5N1) in March 2023.

These animals were part of a captive breeding programme at a zoological premises in England. They were tested as part of a routine investigation into an unusual mammal die-off in November 2022. Ten animals died or were euthanised in a group of 15 bush dogs, over a 9 day period.

The bush dogs had minimal clinical signs before death, and APHA cannot definitively state whether or not H5N1 caused the clinical signs. Influenza of avian origin was not suspected at the time; the virus has since been detected in postmortem samples.

There is no clear evidence suggesting mammal to mammal transmission. It is very likely all animals were exposed to the same source of infected wild birds.

Today we have a preprint from scientists at the UK's APHA and other agencies which presents a somewhat different narrative.

Instead of blaming infection on exposure to `infected wild birds' we now learn these animals were most likely infected from being fed infected meat

Instead of exhibiting `minimal clinical signs before death' as reported above, we now learn that some of these animals exhibited neurological manifestations and histopathic examination revealed `severe acute systemic disease characterised by vasculitis, and widespread necrosis and inflammation in many organs, specifically the liver, brain, lung, and adrenal glands.'

We also learn from this preprint that - despite earlier reports of H5N1/H5N8 spillover into mammals in the UK and elsewhere in Europe (see here, here, and here) - that `Influenza A virus infection was not on the list of differentials for causative agent in this disease event'.

The preprint (excerpts below) is highly detailed, and very much worth reading in its entirety. I'll have a bit more after the break.

Rapid mortality in captive bush dogs (Speothos venaticus) caused by influenza A of avian origin (H5N1) at a wildlife collection in the United Kingdom

Marco Falchieri, Scott Reid, Akbar Dastderji, Jonathan Cracknell, Caroline Janet Warren, Benjamin Mollett, Jacob Peers-Dent, Audra-Lynne Schlachter, Natalie Mcginn, Richard Hepple, Saumya Thomas, Susan Ridout, Jen Quayle, Romain Pizzi, Alejandro Nunez, Alexander M P Byrne, Joe James, Ashley C Banyard

doi: https://doi.org/10.1101/2024.04.18.590032

Abstract

Europe has suffered unprecedented epizootics of high pathogenicity avian influenza (HPAI) clade 2.3.4.4b H5N1 since Autumn 2021. As well as impacting upon commercial and wild avian species, the virus has also infected mammalian species more than ever observed previously.

Mammalian species involved in spill over events have primarily been scavenging terrestrial carnivores and farmed mammalian species although marine mammals have also been affected. Alongside reports of detections in mammalian species found dead through different surveillance schemes, several mass mortality events have been reported in farmed and wild animals.

During November 2022, an unusual mortality event was reported in captive bush dogs (Speothos venaticus) with clade 2.3.4.4b H5N1 HPAIV of avian origin being the causative agent. The event involved an enclosure of fifteen bush dogs, ten of which succumbed during a nine-day period with some dogs exhibiting neurological disease. Ingestion of infected meat is proposed as the most likely infection route.

(SNIP)

Here we report on the infection and severe mortality within a pack of bush dogs (Speothos venaticus) in captivity with avian origin H5N1 clade 2.3.4.4b HPAIV. Bush dogs are a near threatened species of wild canids that are of conservation concern. Wild populations of these dogs range from northern regions of Panama (Central America) to northeastern Argentina and Paraguay; with populations also being present in Colombia, Venezuela, the Guianas, Brazil, and eastern Bolivia and Peru.

This species is characterized by its small size, elongated body, small eyes, short snout, short tail, short legs, and small and rounded ears, in addition to gregarious and diurnal behaviour (35).

In this disease event which occurred in November 2022, two thirds of the pack of bush dogs, held captive in a wildlife collection the UK, became clinically unwell with a disease that had a short duration and led to death and/or the need for euthanasia on welfare grounds with a range of clinical signs including neurological disease.

Avian influenza was not suspected at first and several tests and analysis were performed at private laboratories to ascertain cause of death and to exclude the involvement of more common canine pathogens. Overall inconclusive results led bush dog samples to be submitted retrospectively to the Animal and Plant Health Agency (APHA), Virology Department for shotgun metagenomic assessment, which detected presence of influenza type A virus sequences in internal organs. We describe the disease event, timeline, virological and pathological impact of disease and sequence analysis of the causative agent.

(SNIP)
The exposure route to influenza A virus of avian origin in this case is hard to conclusively define. The bush dogs had been fed a diet that included frozen shot wild birds and game. In the absence of local disease events that may have been transferred to the bush dogs in the enclosure, infection through ingestion of infected meat / offal would appear to be the most likely route of infection.

Another potential infection route is through scavenging of any wild bird carcases/any sick wild birds landing in the un-netted pen. Other routes of infection including indirect contact (e.g., wild bird faeces) are possible but less likely and would not fit with the rapid onset of infection across a number of dogs within a short time frame.

(SNIP)
From the perspective of zoonotic risk, the well-established marker of mammalian adaptation (E627K) was detected in all but one of the bush dog sequences generated. This mutation alone is insufficient to drive an increase in zoonotic risk and so the risk to human populations must be considered very low.

(Continue . . . )

The suspected route of infection - from being fed raw infected birds - is one we've seen repeatedly in Asia with captive big cats, going back to 2004. The neurological manifestations reported in these bush dogs are quite similar to reports in other mammals (both in North America & Europe), including several widely reported prior to the bush dog outbreak:

CDC EID Journal: Encephalitis and Death in Wild Mammals at An Animal Rehab Center From HPAI H5N8 - UK

EID Journal: HPAI A(H5N1) Virus in Wild Red Foxes, the Netherlands, 2021

Netherlands DWHC Reports another Mammal (Polecat) Infected With H5N1

While hindsight is admittedly 20-20, it does seem as if there might have been enough clues here to at least merit testing for influenza A. But apparently, it wasn't on the list . . . .

Just like it wasn't on the list to test cattle, which started falling ill with a `mystery illness' last January in Texas.

While previously experiments (and outbreaks) had shown that cattle could be infected with influenza A (see A Brief History Of Influenza A In Cattle/Ruminants), it took weeks before anyone thought to test for it.