Possible Role of Songbirds and Parakeets in Transmission of Influenza A(H7N9) Virus to Humans

Jeremy C. Jones; Stephanie Sonnberg; Zeynep A. Koçer; Karthik Shanmuganatham; Patrick Seiler; Yuelong Shu; Huachen Zhu; Yi Guan; Malik Peiris; Richard J. Webby; Robert G. Webster

Disclosures

Emerging Infectious Diseases. 2014;20(3) 

In This Article

Abstract and Introduction

Abstract

Avian-origin influenza A(H7N9) recently emerged in China, causing severe human disease. Several subtype H7N9 isolates contain influenza genes previously identified in viruses from finch-like birds. Because wild and domestic songbirds interact with humans and poultry, we investigated the susceptibility and transmissibility of subtype H7N9 in these species. Finches, sparrows, and parakeets supported replication of a human subtype H7N9 isolate, shed high titers through the oropharyngeal route, and showed few disease signs. Virus was shed into water troughs, and several contact animals seroconverted, although they shed little virus. Our study demonstrates that a human isolate can replicate in and be shed by such songbirds and parakeets into their environment. This finding has implications for these birds' potential as intermediate hosts with the ability to facilitate transmission and dissemination of A(H7N9) virus.

Introduction

The emergence of novel influenza strains from the avian reservoir remains a constant threat to human and animal health, as was recently illustrated by human infections with novel and wholly avian influenza A(H7N9) viruses in China. These viruses show little virulence in birds but can cause severe illness in humans.[1,2] Of the 134 confirmed human cases reported as of August 2013, >30% have been fatal,[3,4] In the 3 index case-patients, the illness progressed to acute respiratory distress syndrome and death,[1] and most persons with confirmed infections required hospital care.[2,5] Retrospective epidemiologic analyses showed >75% of affected patients had had contact with domestic poultry,[6,7] a common source of zoonotic transmission of influenza.[8] Several of the A(H7N9) virus internal genes (polymerase basic protein [PB] 1, matrix, nonstructural protein, and nucleoprotein) originated from the H9N2 subtype commonly found in chickens. When chickens and quail were inoculated with A(H7N9) isolated from humans, they shed the viruses to high titers but had little or no clinical disease.[9,10] Thus, poultry appears to be a reservoir for A(H7N9) viruses and a source of human infections. Yet, multiple lines of evidence suggest avian species other than the usual suspects (waterfowl and poultry) contributed to the emergence of these novel H7N9 viruses: first, H7N9 has been isolated from nonpoultry birds (pigeons) in Chinese live-bird markets;[11] second, 2 genes (PA, PB2) in an initially characterized human isolate (A/Anhui/1/2013) were most closely related to viruses isolated from bramblings (finch-like birds of the large order Passeriformes);[12] and third, the matrix, polymerase acidic protein [PA], PB1 and PB2 gene segments from additional human isolates appear to have been donated by A/brambling/Beijing/16/2012 (H9N2)-like virus(es).[13] Therefore, songbirds and other small, terrestrial birds could have been directly involved in the genesis of novel A(H7N9) viruses and subsequent infection in humans.

Songbirds are common household pets and are in close contact with humans and domesticated animals. Their wild counterparts also are likely to interact with poultry in backyard farms and in many farming sectors.[14,15] Consequently, we examined the replication and transmission of the human isolate A/Anhui/1/2013 (H7N9) in wild and domesticated small birds. A/Anhui/1/2013 was isolated from one of the initially reported human case-patients[1] and is closely related to many of the avian isolates that have been recovered.[12] For this study, we chose 3 species of Passeriformes (zebra finches, society finches, and sparrows), which are related to the bramblings described previously. We also studied the parakeet (budgerigar; order Psittaciformes), a bird found in the wild and in households as a pet, that is known to support the replication of other subtypes of influenza.[16–18] The study was conducted during June and July 2013 at St. Jude Children's Research Hospital (Memphis, TN, USA).

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