The index case was a 5 year old Miniature Schnauzer with 5 days of nasal discharge and sneezing. The dog recovered but the next case, a 3 year old Cocker Spaniel wasn’t so lucky, nor were the 2 Korean hunting dogs (Jindos) or a 3 year old Yorkshire terrier. Then 13 dogs in a shelter started to show signs of nasal discharge, cough and high fever. Antibody studies showed that they had all been suffering from influenza infection, subtype H3N2. These cases happened in the spring and summer of 2007 (NB: this is not flu season). H3N2 is the most common subtype involved in human seasonal influenza. Is that where the virus came from? A team of Korean researchers got specimens from the schnauzer, the cocker spaniel and the Yorkshire terrier and have just reported their findings in the CDC journal, Emerging Infectious Diseases (Song et al., Transmission of Avian Influenza Virus (H3N2) to Dogs).
The specimens were used to inoculate eggs and replicated influenza virus was isolated and subjected to genetic analysis and used to experimentally infect 9 beagle pups intranasally. The researchers were looking for signs of infection, including severe illness, development of antibodies (“seroconversion”) and viral shedding. They got all three. The pathologic findings were confined to the respiratory tract but they were relatively severe. The virus was shed in nasal discharge but not feces. And all inoculated dogs seroconverted.
This virus efficiently infected the dogs, as might be expected from the size of the kennel outbreak. The sequence analysis suggested the virus was of bird origin, not human origin. Certainly this is not the first time a bird flu virus has jumped from birds to mammals and become transmissible there. The 1918 Spanish flu is suspected to be of that kind and an H7N7 bird virus caused a fairly large outbreak of conjunctivitis (and one death) in The Netherlands in 2003. Cats, ferrets and marine mammals have also been infected with avian viruses. The current “bird flu” (H5N1) is also an avian virus. H3N8 has caused outbreaks of influenza in dogs, but this outbreak is H3N2, so it is different. The H3N2 designate only two of the proteins comprising the influenza A proteome and two viruses with serotype H3N2 can have very different “internal” genes. These genes in the Korean isolates bear similarities to internal genes of ducks in Hong Kong, Japan and southeast China.
So why did the dogs get infected with bird H3N2 viruses and not the ubiquitous H3N2 from humans? The authors suggest it is because the dog respiratory tract is mainly equipped with avian type receptors (alphas (2, 3) rather than alpha (2, 6); see our posts here on this topic). This is a reasonable explanation but more work needs to be done.
So how did the dogs get infected? It is common practice to feed them scraps from birds, including untreated duck and chicken muscle, internal organs, and heads. Dogs are not only pets but livestock in Korea, eaten as a delicacy. Fattening them up and selling and keeping them in live animal markets is a common practice:
Live-bird markets are thought to constitute “a missing link in the epidemiology of avian influenza viruses” because they bring together numerous hosts, such as chickens, ducks, turkeys, geese, and doves, in a high-density setting, which represents an ideal environment for virus interspecies transmission. (Song et al. Emerging Infectious Diseases)
So what is the lesson here? One is the usual humbling one: there is still a lot to learn about the influenza virus. Another is that there are a lot of potentially susceptible species that we have not looked for or at in a systematic fashion. In much of southeast asia and asia birds are ubiquitous companions of humans. They live together and sometimes sleep together. In the industrialized west dogs are common companion animals that live in close proximity to humans. If it turns out that they are a common reservoir for bird viruses, then much more of the world’s population could be liable to a virulent influenza virus that got into dogs just as H5N1 got into poultry. The H3N2 case is probably not a likely pandemic source (despite what the Korean scientists say in their Discussion) because there is widespread immunity to H3N2 in the global population, even though changes in the strain mean the protection varies as the virus mutates. On the other hand, H3N2 keeps infecting humans because it changes enough from year to year to make that immunity less effective and H3N2 is sufficiently virulent on its own that it and H1N1 kill an estimated 30,000 to 40,000 Americans yearly. If a variant that was much more virulent came around it could get nasty.
And there are other bird viruses that might also get into dogs or other companion animals. It’s about time a serious, systematic investigation and any indicated surveillance of many more animal species got underway.