Pandemic H1N1 Influenza Isolated from Free-Ranging Northern Elephant Seals in 2010 off the Central California Coast
Tracey Goldstein equal contributor,
Ignacio Mena equal contributor,
Simon J. Anthony,
Rafael Medina,
Patrick W. Robinson,
Denise J. Greig,
Daniel P. Costa,
W. Ian Lipkin,
Adolfo Garcia-Sastre,
Walter M. Boyce
Abstract
Interspecies transmission of influenza A is an important factor in the evolution and ecology of influenza viruses. Marine mammals are in contact with a number of influenza reservoirs, including aquatic birds and humans, and this may facilitate transmission among avian and mammalian hosts. Virus isolation, whole genome sequencing, and hemagluttination inhibition assay confirmed that exposure to pandemic H1N1 influenza virus occurred among free-ranging Northern Elephant Seals (Mirounga angustirostris) in 2010. Nasal swabs were collected from 42 adult female seals in April 2010, just after the animals had returned to the central California coast from their short post-breeding migration in the northeast Pacific. Swabs from two seals tested positive by RT-PCR for the matrix gene, and virus was isolated from each by inoculation into embryonic chicken eggs. Whole genome sequencing revealed greater than 99% homology with A/California/04/2009 (H1N1) that emerged in humans from swine in 2009. Analysis of more than 300 serum samples showed that samples collected early in 2010 (n = 100) were negative and by April animals began to test positive for antibodies against the pH1N1 virus (HI titer of ≥1:40), supporting the molecular findings. In vitro characterizations studies revealed that viral replication was indistinguishable from that of reference strains of pH1N1 in canine kidney cells, but replication was inefficient in human epithelial respiratory cells, indicating these isolates may be elephant seal adapted viruses. Thus findings confirmed that exposure to pandemic H1N1 that was circulating in people in 2009 occurred among free-ranging Northern Elephant Seals in 2010 off the central California coast. This is the first report of pH1N1 (A/Elephant seal/California/1/2010) in any marine mammal and provides evidence for cross species transmission of influenza viruses in free-ranging wildlife and movement of influenza viruses between humans and wildlife.
Citation: Goldstein T, Mena I, Anthony SJ, Medina R, Robinson PW, et al. (2013) Pandemic H1N1 Influenza Isolated from Free-Ranging Northern Elephant Seals in 2010 off the Central California Coast. PLoS ONE 8(5): e62259. doi:10.1371/journal.pone.0062259
Editor: Ian C. Davis, The Ohio State University, United States of America
Received: January 8, 2013; Accepted: March 19, 2013; Published: May 15, 2013
Copyright: ? 2013 Goldstein et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Funding for this research was provided by CRIP (Center for Research on Influenza Pathogenesis), under the Centers of Excellence for Influenza Research and Surveillance (CEIRS) program supported by the National Institute of Allergy and Infectious Diseases (contract HHSN266200700009C), the Tagging of Pacific Pelagics program with grants from the National Ocean Partnership Program (N00014-02-1-1012), the Office of Naval Research (N00014-00-1-0880, N00014-03-1-0651 and N00014-08-1-1195), International Association of Oil and Gas Producers contract JIP2207-23, the Moore, Packard, and Sloan Foundations, and benefited from intellectual developments from the PREDICT project of the United States Agency for International Development (USAID) Emerging Pandemic Threats Program, CONICYT Insertion of Human Capital to the Academy grant (79100014) and by the Program Iniciativa Cient?fica Milenio from the Chilean Ministry of Economy, Development and Tourism. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
