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Sea Otters Can Get the Flu, Too - Human H1N1 Pandemic Virus Infected Washington State Sea Otters (USGS/CDC, April 8 2014)

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  • Sea Otters Can Get the Flu, Too - Human H1N1 Pandemic Virus Infected Washington State Sea Otters (USGS/CDC, April 8 2014)

    [Source: USGS, full page: (LINK).]

    Sea Otters Can Get the Flu, Too - Human H1N1 Pandemic Virus Infected Washington State Sea Otters

    Released: 4/8/2014 12:45:13 PM / Contact Information: U.S. Department of the Interior, U.S. Geological Survey, Office of Communications and Publishing, 12201 Sunrise Valley Dr, MS 119, Reston, VA 20192, Gail Moede Rogall, USGS, Phone: 608-270-2438, Marisa Lubeck, USGS, Phone: 303-526-6694 / CDC Media Relations, Phone: 404-639-3286

    In partnership with: Centers for Disease Control and Prevention

    Northern sea otters living off the coast of Washington state were infected with the same H1N1 flu virus that caused the world-wide pandemic in 2009, according to a new U.S. Geological Survey and Centers for Disease Control and Prevention study.

    During an August 2011 health monitoring project, USGS and CDC scientists found evidence that the Washington sea otters were infected with the pandemic 2009 H1N1 virus, although the exact date and source of exposure could not be determined. The findings suggest that human flu can infect sea otters.

    ?Our study shows that sea otters may be a newly identified animal host of influenza viruses,? said Hon Ip, a USGS scientist and co-author of the study.

    The researchers discovered antibodies for the 2009 H1N1 flu virus in blood samples from 70 percent of the sea otters studied. None of the otters were visibly sick, but the presence of antibodies means that the otters were previously exposed to influenza. Further tests concluded that the antibodies were specific to the pandemic 2009 H1N1 flu virus, and not from exposure to other human or avian H1N1 viruses.

    ?We are unsure how these animals became infected,? said Zhunan Li, CDC scientist and lead author on the paper. ?This population of sea otters lives in a relatively remote environment and rarely comes into contact with humans.?

    An unrelated 2010 study showed that northern elephant seals sampled off the central California coast had also been infected with the 2009 pandemic H1N1 virus. This elephant seal exposure is the only other known pandemic H1N1 influenza infection in marine mammals, and similar to sea otters, it is unclear how the seals were exposed.

    ?Our new study identifies sea otters as another marine mammal species that is susceptible to influenza viruses and highlights the complex interspecies transmission of flu viruses in the marine environment,? said USGS scientist LeAnn White.

    The 2009 H1N1 virus has spread globally among people since 2009 and was the predominant flu virus in circulation during the 2013-2014 flu season. This study is the first time that evidence of influenza infection has been detected in sea otters, although these viruses have previously been found in many different animals, including ducks, chickens, pigs, whales, horses and the elephant seals.

    The study is published in the journal Emerging Infectious Diseases and is available online.

    Sea otter sampling was performed by a collaboration of the USGS National Wildlife Health Center, USGS Alaska Science Center, USGS Western Ecological Research Center, Monterey Bay Aquarium and Seattle Aquarium.

    The USGS and the Interior Department work with CDC and other state and federal partners on research related to zoonotic diseases ? diseases that can be passed between animals and humans ? to help provide an early warning to the agriculture, public health and wildlife communities, as well as to the public. For more information, please visit the USGS National Wildlife Health Center or CDC websites.


  • #2
    Re: Sea Otters Can Get the Flu, Too - Human H1N1 Pandemic Virus Infected Washington State Sea Otters (USGS/CDC, April 8 2014)

    [Source: US Centers for Disease Control and Prevention (CDC), Emerging Infectious Diseases Journal, full page: (LINK). Edited.]

    Volume 20, Number 5?May 2014 / Letter

    Serologic Evidence of Influenza A(H1N1)pdm09 Virus in Northern Sea Otters

    To the Editor:

    Sporadic epizootics of pneumonia among marine mammals have been associated with multiple animal-origin influenza A virus subtypes (1?6); seals are the only known nonhuman host for influenza B viruses (7).

    Recently, we reported serologic evidence of influenza A virus infection in free-ranging northern sea otters (Enhydra lutris kenyoni) captured off the coast of Washington, USA, in August 2011 (8). To investigate further which influenza A virus subtype infected these otters, we tested serum samples from these otters by ELISA for antibody-binding activity against 12 recombinant hemagglutinins (rHAs) from 7 influenza A hemagglutinin (HA) subtypes and 2 lineages of influenza B virus (Technical Appendix [PDF - 52 KB - 2 pages] Table 1). Estimated ages for the otters were 2?19 years (Technical Appendix [PDF - 52 KB - 2 pages] Table 2); we also tested archived serum samples from sea otters of similar ages collected from a study conducted during 2001?2002 along the Washington coast (9).



    Figure. Results of ELISA and hemagglutinin inhibition (HI) testing for influenza viruses in serum samples from northern sea otters captured off the coast of Washington, USA, during studies conducted in August 2011...

    Of the 30 sea otter serum samples collected during 2011, a total of 21 (70%) had detectable IgG (>200) for rHA of influenza A(H1N1)pdm09 virus (pH1N1) strain A/Texas/05/2009. Four of 7 serum samples that showed IgG ≥6,400 against pH1N1 rHA also showed low cross-reactivity (IgG 200) against rHA of A/Brisbane/59/2007, a previous seasonal influenza A(H1N1) virus (Figure, panel A; Technical Appendix [PDF - 52 KB - 2 pages] Table 1). No IgG was detected in any samples for any of the other 11 rHAs tested (IgG ≤100), and the sea otter serum samples collected during 2001?2002 did not react with any of the rHAs tested, including pH1N1 (IgG ≤100; Figure, panel A).

    Next, we tested serum samples by using a hemagglutination inhibition (HI) assay with whole influenza virus to detect strain-specific antibodies that inhibit receptor binding. Of the 30 samples collected during 2011, a total of 22 (73%) showed HI antibody titers of ≥40 against pH1N1 virus. Titers against all other human and avian viruses tested were ≤10 for all samples by HI assay using turkey red blood cells (RBCs) (Figure, panel B; Technical Appendix [PDF - 52 KB - 2 pages] Table 3). No influenza A or B virus?specific HI antibodies were detected in the samples collected during 2001?2002 (data not shown). Although nasal swab specimens were collected from sea otters in the 2011 study, all specimens were negative for influenza virus by testing in embryonated eggs and by real-time PCR for detection of influenza A viral RNA (data not shown). These results suggest that sea otters were infected with influenza A virus sometime before the August 2011 sample collection date.

    Although none of the 2011 samples showed HI titers to influenza A/duck/New York/96 (H1N1) virus (dk/NY/96) by testing using turkey RBCs (Technical Appendix [PDF - 52 KB - 2 pages] Table 2), titers against this strain were detected when using horse RBCs, which is a more sensitive means for the detection of mammalian antibodies against some avian influenza subtypes (10). Of the 22 samples that had HI titers >40 to pH1N1 virus, 16 also had HI titers >40 against dk/NY/96 by horse RBC HI assay (Technical Appendix [PDF - 52 KB - 2 pages] Table 2). However, titers against this strain were on average ≈4?8-fold lower than those for the pH1N1 virus strain, which suggests that that the titers against dk/NY/96 were the result of serologic cross-reactivity with avian- and swine-origin pH1N1 viruses.

    To further test for cross-reactivity, 4 sea otter serum samples were adsorbed with purified pH1N1 and dk/NY/96 virions. Adsorption with pH1N1, but not dk/NY/96, removed HI antibodies to pH1N1, whereas adsorption with either virus removed HI antibodies against dk/NY/96 (Technical Appendix [PDF - 52 KB - 2 pages] Table 4). A comparison of amino acid sequences comprising the known HA antigenic sites on the pH1N1 structure confirmed high sequence identity and structural similarity with dk/NY/96 HA in Sa (12/13 aa residues) and Sb (8/12 aa residues) antigenic sites (data not shown). These results indicate that HI antibodies detected in sea otters are the result of pH1N1 virus infection but cross-react with the avian influenza A(H1N1) virus.

    Although we cannot exclude the possibility that sea otters were infected with classical swine influenza A(H1N1) virus, which shares high HA genetic and antigenic similarity with pH1N1 virus, our serologic evidence is consistent with isolation of pH1N1 virus from northern elephant seals (1). Therefore, we conclude that these sea otters were infected with pH1N1 virus. The origin and transmission route of pH1N1 virus infection in sea otters remain unknown. Potential contact between northern elephant seals and sea otters is one possibility; elephant seals? summer feeding ranges and breeding areas along the Northeast Pacific coast overlap with areas where the Washington sea otter population is distributed (1).

    In conclusion, our results show that sea otters are susceptible to infection with influenza A virus and highlight the complex nature of interspecies transmission of influenza viruses in the marine environment. Further surveillance, especially in other sea otter populations, is required to determine virus origin, potential pathogenesis, and consequences for the marine ecosystem.

    Zhu-Nan Li, Hon S. Ip, Jessica F. Trost, C. LeAnn White, Michael J. Murray, Paul J. Carney, Xiang-Jie Sun, James Stevens, Min Z. Levine, and Jacqueline M. Katz

    Author affiliations: Centers for Disease Control and Prevention, Atlanta, Georgia, USA (Z.-N. Li, J.F. Trost, P.J. Carney, X.-J. Sun, J. Stevens, M.Z. Levine, J.M. Katz); United States Geological Survey National Wildlife Health Center, Madison, Wisconsin, USA (H.S. Ip, C.L. White); Monterey Bay Aquarium, Monterey, California, USA (M.J. Murray).


    We thank Heather Tatum, Leilani Thomas, and Peter Browning for specimen management and Tina Egstad, Katy Griffin, Renee Long, and Zac Najacht for technical assistance.

    Sample collection was done in collaboration with United States Geological Survey?Alaska Science Center, Monterey Bay Aquarium, and Seattle Aquarium. Recombinant HAs with Histidine Tag from A/Japan/305/57 (H2N2), FR-700; A/Netherlands/219/2003 (H7N7), FR-71; A/Hong Kong/1073/99 (H9N2), FR-88; A/shorebird/DE/68/2004 (H13N9), FR-73; globular head domain HA1 rHAs of B/Brisbane/60/2008, FR-836; and B/Wisconsin/1/2010 FR-843, were obtained through the Influenza Reagent Resource, Influenza Division, World Health Organization Collaborating Center for Surveillance, Epidemiology and Control of Influenza, Centers for Disease Control and Prevention.

    1. Goldstein T, Mena I, Anthony SJ, Medina R, Robinson PW, Greig DJ, Pandemic H1N1 influenza isolated from free-ranging Northern Elephant Seals in 2010 off the central California coast. PLoS ONE. 2013;8:e62259 . DOI ? PubMed
    2. Hinshaw VS, Bean WJ, Geraci J, Fiorelli P, Early G, Webster RG. Characterization of two influenza A viruses from a pilot whale. J Virol. 1986;58:655?6 .PubMed
    3. Hinshaw VS, Bean WJ, Webster RG, Rehg JE, Fiorelli P, Early G, Are seals frequently infected with avian influenza viruses? J Virol. 1984;51:863?5 .PubMed
    4. Geraci JR, St Aubin DJ, Barker IK, Webster RG, Hinshaw VS, Bean WJ, Mass mortality of harbor seals: pneumonia associated with influenza A virus. Science. 1982;215:1129?31 . DOI ? PubMed
    5. Anthony SJ, St Leger JA, Pugliares K, Ip HS, Chan JM, Carpenter ZW, Emergence of fatal avian influenza in New England harbor seals. MBio. 2012;3:e00166?12 . DOI ? PubMed
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    8. White CL, Schuler KL, Thomas NJ, Webb JL, Saliki JT, Ip HS, Pathogen exposure and blood chemistry in the Washington, USA population of northern sea otters (Enhydra lutris kenyoni). J Wildl Dis. 2013;49:887?99 . DOI ? PubMed
    9. Brancato MS, Milonas L, Bowlby CE, Jameson R, Davis JW. Chemical contaminants, pathogen exposure and general health status of live and beach-cast Washington sea otters (Enhydra lutris kenyoni). Marine Sanctuaries Conservation Series ONMS-09?01. Silver Spring (MD): US Department of Commerce, National Oceanic and Atmospheric Administration, Office of National Marine Sanctuaries; 2009. p. 181.
    10. Stephenson I, Wood JM, Nicholson KG, Zambon MC. Sialic acid receptor specificity on erythrocytes affects detection of antibody to avian influenza haemagglutinin. J Med Virol. 2003;70:391?8. DOI ? PubMed


    Figure. Results of ELISA and hemagglutinin inhibition (HI) testing for influenza viruses in serum samples from northern sea otters captured off the coast of Washington, USA, during studies conducted in August...

    Technical Appendix

    Technical Appendix. Titers for influenza A and B viruses detected in serum samples from northern sea otters captured off the coast of Washington, USA, during studies conducted in August 2011. 52 KB

    Suggested citation for this article: Li Z-N, Ip HS, Trost JF, White CL, Murray MJ, Carney PJ, et al. Serologic evidence of influenza A(H1N1)pdm09 virus in northern sea otters [letter]. Emerg Infect Dis [Internet]. 2014 May [date cited].

    DOI: 10.3201/eid2005.131890