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A review of influenza viruses in seals and the implications for public health.

Influenza is a common virus that affects many species to varying degrees of severity. Pinnipeds are particularly interesting animal models because both influenza A and B virus infections have been identified in wild populations. This is significant because, before the year 2000, influenza B virus infection had only been reported in primates. (1) Influenza virus infections in seals have historically caused mass mortality events in affected populations. (2-6) An influenza virus was first isolated from harbor seals (Phoca vitulina (Linnaeus)) in 1980; the virus was identified as belonging to the H7N7 subgroup and the naturally infected cases were described by Geraci et al and Webster et al. (5-7) The first isolation of a seal influenza virus from a human occurred in a researcher studying this first known epizootic, confirming that influenza viruses carried by seals could infect humans. (5)

Pigs are commonly known to be a species in which genetic reassortment of novel influenza viruses can occur because they have receptors that allow attachment to both mammalian and avian influenza virus strains. (8) Receptors that recognize avian sialyloligosaccharide 2,3 Galactose (SA[alpha]2,3Gal), and mammalian sialyloligosaccharide 2,6 Galactose (SAa2,6Gal), influenza viruses have been identified in seal lung tissue. (3,9) The H3N8 strain isolated from dead seals in the 2011 outbreak was found to bind both mammalian and avian influenza receptors. (3) Additionally, experimental infections in primates with a 1980 seal influenza virus resulted in significant systemic disease. (10) These findings demonstrate the potential for seals to harbor viruses to which humans are susceptible and immunologically naive.

Shortridge and Stuart-Harris proposed the idea of an influenza epicenter; a geographical area where birds, humans, and other animals live in intimate contact, providing optimal conditions for viruses to cross species. (11) Traditionally, research has focused on agricultural influenza epicenters, that is, where humans, birds, and pigs live in close contact. Waterfowl are the natural reservoir for all known subtypes of influenza A viruses and share many resources with pinnipeds at sea. (12,13) Additionally, between subsistence hunting, managed animals, and shared shoreline habitat, humans are more likely to interact with pinnipeds than any other marine mammal. This article provides a review of influenza viruses in pinnipeds with the goal of increasing recognition of potential wildlife influenza epicenters, particularly in coastal centers with large pinniped populations.


Search Strategy

The PubMed database was searched in July 2007, February 2010, and again in August 2012. The searches were performed without language restriction and used the key words "seal," "Phoca," "phocid," "pinniped," "otaria," "otariid," "otariidae," "Arctocephalus," Zalophus," "Callorhinus," "fur seal," "sea lion," "marine," or "marine mammal," along with "influenza," "orthomyxovirus," "zoonoses," "zoonosis," "zoonotic," "H1," "H3," "H4," "H5," or "H7" to find reports on cases of influenza in seals or seal strains found in man. Additional articles were located through the reference sections of the selected papers.

Selection of Articles

The title and abstracts of all search results were reviewed for inclusion using the following criteria: the article mentioned at least one case of influenza in pinnipeds, a seal influenza strain found in humans, or discussion of pathology or environmental interaction of influenza strains found in seals.


The PubMed searches yielded 112 different results. Of these, 26 articles, spanning from 1978 to 2012, were selected for review because they met the above inclusion criteria. The remaining 86 studies were not applicable to this review.


Influenza viruses belong to the Orthomyxovirus family of enveloped viruses with segmented, single-stranded negative-sense RNA. Influenza viruses are divided into 3 types (A, B, and C) based on the 2 major core proteins, the nucleoprotein and the matrix protein. (14) Of these types, only influenza A and B viruses tend to cause epidemics in humans and are the main focus of this review. Each influenza A virion consists of a host-derived lipid bilayer envelope and an 8-segmented genome, which codes for the 11 virion proteins. These proteins are the 3 transmembrane glycoprotein spikes (hemagglutinin (HA), neuraminidase (NA), and matrix protein 2 (M2)), a nucleocapsid (matrix protein 1 (M1)), a nucleoprotein (NP), 3 polymerase proteins (PA, PB1, and PB2), an apoptosis-inducing protein (PB1-F2), and 2 nonstructural proteins (NS1 and NS2). The segmentation of the genome allows for genetic reassortment within and between viruses, readily creating new phenotypes (antigenic shift). (15) Additionally, mutations may occur, especially in the H region, creating an antigenic drift. (15) M1 and M2 are involved in virion coating and uncoating. (15) Nucleoprotein and polymerases aid in transcription. Hemagglutinin and NA are responsible for viral attachment and release and are also the antigens involved in host immunity. (2) Additionally, HA plays a role in determining host range, since membrane fusion and genome penetration only occur if the proper cellular proteases are present to cleave the HA into the disulfide-linked polypeptides [HA.sub.1] and [HA.sub.2]. (16) Currently, 16 HA and 9 NA serotypes have been recognized for influenza A viruses, all of which have been isolated from birds. (12,13) Each virus has one HA and one NA subtype, which theoretically may occur in any combination. Specific influenza strains are identified by a standard nomenclature specifying virus type, host, geographic origin, sequential number of isolation, and HA and NA serotype, for example: A/Seal/Mass/1/80/(H7N7).

Transmission and Epidemiology

Waterfowl, particularly of the orders Anseriformes and Charadriiformes, are the natural reservoir for all known subtypes of influenza A viruses. (12,13) Avian influenza viruses replicate mainly in the birds' intestinal tract and are spread from bird to bird by a fecal-oral route. (17) Spread of avian influenza viruses to seals may occur through direct contact, such as predation on birds, inhalation of aerosolized virus, or indirect contact with bird feces through contaminated food or water. (17) Avian influenza viruses have been shown to be most stable in fresh to brackish water (0-20,000 ppm) with colder temperatures (4[degrees]C-17[degrees]C), and a slightly basic pH (7.4-8.2). (18) In seals, influenza binds to the same type of sialyloligosaccharide receptors, SA[alpha]2,3Gal, as birds, but the receptors are located in their lungs instead of in their intestinal tract, making inhalation the most likely route of transmission. (9,19)

The first recorded epizootic of influenza in seals occurred from 1979-1980 on the New England coast. An H7N7 influenza virus was repeatedly isolated from the lungs, brain, and hilar lymph nodes of dead seals. (20) Approximately 600 seals died; an estimated mortality of 20%. (5,6) From 1982-1983, an H4N5 influenza virus caused a 2% to 4% mortality of harbor seals on Cape Cod. (2) H4N6 and 3 strains of H3N3 were isolated from harbor seals in another Cape Cod epizootic in 1991 and 1992. (21) In 2011, again on the New England coast, 162 harbor seals died in an outbreak of pneumonia lasting less than 4 months. This was 4 times greater than the expected mortality rate in a healthy, wild seal population. (3) An H3N8 strain was isolated from several of the seals. (3) Antigenic and genetic analyses showed that all genes from each of the epizootic strains were of avian origin. (3-6,9,21,22) Furthermore, a study by Mandler et al demonstrated that the closest-matching avian strains to the 1980 H7N7 virus were from the same geographic region as the seal isolate. (23)

Evidence of influenza virus infection by many different influenza serotypes has been found through antibody and virus isolation from seals around the world. Sero types H7N7, H4N5, H4N6, H3N8, and H3N3 have been found in harbor seals (Phoca vitulina) on the New England coast of the United States. (3-7,21,22) De Boer et al found antibodies to H1, H3, H4, H7, and H12 in sera from seals from the Bering Sea. (24) Interestingly, all NP-ELISA positive sea lions were negative in Hemagglutinin inhibition tests, suggesting the sea lions carried antibodies to a then unknown hemagglutanin serotype. (24) Danner and McGregor found H3 and H7 antibodies in a ringed seal (Phoca hispida) in Alaska. (25) In contrast, Calle et al did not find antibodies to influenza A in sera from the 6 bearded seals (Erignathus barbatus) sampled near St. Lawrence Island, Alaska. (26) Austin and Webster did not find antibodies to influenza A or B virus in sera from the 237 Weddell seals (Leptonychotes weddelli) sampled near Cape Armitage, Antarctica. (27) In Arctic Canada, 2.5% of the ringed seals that were tested by Nielsen et al were seropositive for influenza A, but were not tested for serotype. (28) Antibodies from H3 and H6 were found in sera from Kuril harbor seals (Phoca vitulina stejnegeri) in Hokkaido, Japan. (29) Ohishi et al reported evidence of H3N2 in Baikal (Pusa sibirica) and ringed seals from Lake Baikal and the Kara Sea in Russia. (22) Researchers believe seals caught this serotype from humans. (1,13,22) Additionally, in 2002, Ohishi et al found antibodies to H3N2, H2N2, H3N8, and influenza B in Caspian seals (Pusa caspica) from the Caspian Sea. (30) Until Osterhaus et al identified antibodies to an influenza B virus in 2000 from a harbor seal in Pieterburen, Netherlands, influenza B was thought to be a strictly human virus. (1) More recently, antibodies to influenza B virus and to H1N1 have been isolated in fur seals (Arctocephalus australis) from Lobos Island, Uruguay. (31) It appears that severe influenza virus infection is sporadic in seals and, fortunately, does not usually lead to a mass die-off. More research is needed to explore the cause, likely multifactorial, for such epizootics and the role of evolving influenza viruses and influenza-associated mortality events in pinnipeds.

Clinical Signs and Pathology

Clinically affected seals appear weak and may exhibit respiratory distress and ataxia. Additional clinical signs include a frothy white or blood-tinged nasal discharge, mild cough, pneumonia, conjunctivitis, and swollen, emphysematous necks. (3,5-7) Affected seals are often in good body condition due to the rapid course of disease. Experimental infection of harbor seals induced clinical signs in as little as 24 hours and naturally infected seals were observed to have died just hours after feeding normally. (5-7) Cause of death is acute hemorrhagic pneumonia. Postmortem lesions include necrotizing bronchitis and bronchiolitis and hemorrhagic alveolitis. (5-7)


Virus isolation from culture of nasal or pharyngeal swabs or enzyme-linked immunosorbent assay (ELISA) can be used to test for influenza antibodies in serum. (5-7,21,22,24,28-32,33) Hemagglutinin inhibition and Neuraminidase inhibition tests are necessary for subtyping isolates. (24) Differential diagnoses include phocine and canine distemper viruses, phocine herpesvirus-1, and Mycoplasma. (7)

Treatment and Control

Due to the viral etiology, there is no specific treatment for influenza virus infection in seals. Supportive care may be helpful in rehabilitation, though may not be feasible in the case of an epizootic event. The development of antibodies in naturally and experimentally infected seals suggest that immunity through vaccination is possible, but this would be impractical and cost prohibitive in wild pinniped populations. (4) Measures to prevent influenza transmission to captive pinnipeds include covering pens to minimize exposure to bird feces and designing enclosures to prevent direct contact with feral pinnipeds. Additionally, in zoo settings, vaccination of birds in conjunction with strict biosecurity measures and viral monitoring can reduce the amount of influenza virus present in the environment, decreasing the likelihood of viral transfer to other species in the collection. (34)

Human Cases

The first recorded cases of influenza transfer from seals to humans were during the study of the 1979-1980 epizootic on Cape Cod. Within 2 days of known contamination of the eyes during seal necropsies, 4 people developed purulent conjunctivitis with intense periorbital swelling and pain. Recovery was uneventful and complete in 4 to 5 days. (6) Another case occurred during a study of experimental infection of harbor seals with A/Seal/Mass/1/80 (H7N7) when an infected seal sneezed into the face and right eye of an investigator. A severe conjunctivitis developed in the person's right eye within 40 hours and the periauricular lymph nodes were enlarged by 96 hours postexposure. High levels of the virus, confirmed as A/ Seal/Mass/1/80 (H7N7), were recovered in conjunctival swabs from the infected eye. The conjunctivitis resolved by the fourth day. (6) Antibodies to the seal virus were not detected in sera from any of the human cases, but this is not unusual since a blood-ocular barrier exists, preventing induction of a systemic immune response when only the eye has been exposed. (6)


The subject of influenza in seals raises many questions. There appears to be several ways in which seal-human interactions, both direct and indirect, could contribute to the development, spread, or exacerbation of influenza outbreaks.

Are influenza outbreaks in seals more prevalent than realized?

Harkonen et al investigated a 2007 epizootic of harbor seals from the Danish island of Anholt and along the Swedish coast. (35) Thousands of seals were reported to have perished in the outbreak. Observation and necropsy of affected seals revealed weakness, swollen, emphysematous necks, dyspnea, hemoptysis, interstitial pneumonia, and necrotizing tracheitis and bronchitis. (35) Additionally, an increase in stranded harbor porpoise (Phocoena phocoena) carcasses, also exhibiting emphysema, was found in the same area. (35) Bacteriology and PCR for phocine distemper virus performed on seal and porpoise samples yielded no answers as to the cause of the mass mortality. (35) Agreeably, due to the lack of recovery of pathogenic bacteria in combination with the histpathological findings, Harkonen et al suggested the etiology was viral. (35) It is possible this was an influenza mortality event. Influenza infection causes similar symptoms and pathology as those described by Harkonen et al, and has also been reported in cetaceans, who also have SA[alpha]2,3Gal influenza receptors in their lungs. (5-7,9,17,19,28,35-37) This, however, would be the first recorded influenza epizootic affecting both pinnipeds and cetaceans and could indicate either an independent, yet simultaneous, introduction of novel influenza virus into both species or an important cross-species transmission. ELISA for influenza virus could be performed on remaining samples to rule this out as a cause.

Can marine mammals act as an intermediary species in the spread of avian influenza from birds to humans?

Antigenic and genetic analyses of epizootic strains from seals revealed that all genes from each of the epizootic strains were of avian origin. (3-7,9,22) Additionally, researchers believe that seals acquired, and may be reservoirs for, human H3N2 and influenza B viruses. (1,13,22,30) A study by Scheiblauer et al demonstrated that a variant of A/Seal/ Massachusetts/1/80 adapted to cause severe systemic disease in mice, ferrets, and rats, all commonly used animal models for human influenza studies. (38) It has already been shown that influenza virus from seals can replicate in human tissue and that seal influenza viruses can be systemically virulent in primates. (5,10) Perhaps most concerning is the fact that the H3N8 virus isolated from carcasses in the 2011 seal outbreak has the ability to transmit between seals, which may become infected with multiple influenza virus subtypes. (3) It is probable that seals could act as a "mixing vessel" for creating pandemic strains by mixing genes from avian and mammalian viruses. (3,30)

Can marine mammals spread avian influenza viruses through their migrations?

Little is known about the role of migratory patterns of and interactions between the various species of pinnipeds in the spread of disease. Harris et al used an individual-based model of seal movement to evaluate the influence of epidemiological parameters and host ecology on the spread of phocine distemper virus through populations of harbor seals. (39) It was determined that short foraging trips with short haulout durations or long infectious periods allowed for more traveling by the seals and increased the likelihood that disease would spread between haulouts. (39) Since phocine distemper virus, a morbillivirus, has a similar mode of transmission and pathology as influenza virus in seals, this model might be useful in predicting the spread of influenza infections in seals as well. (7) More research is needed to better understand the behavior of seals and its effect on epidemiology.

Do fish and sediment harbor influenza?

Little is known about the influence of abiotic or biotic environmental factors on the persistence and spread of influenza virus. Brown et al reported that water is intimately connected with the transmission of avian influenza viruses and that these viruses can remain infective in this medium for months under natural conditions. (18) Influenza virus can also be preserved in environmental ice or concentrated in filter-feeding invertebrates. (40,41) Fish feed on many things, including sediment, bird feces, and detritus, which could potentially contain large quantities of influenza virus. (11) Piscivorous birds, such as those in the order Charadriiformes, who ate these virus-laden fish would have the virus in their gastrointestinal tract, where influenza virus receptors are concentrated. (17) In addition to sharing shoreline habitats, seals and seabirds may also feed on the same fish species. (17) Thanawongnuwech et al proposed an oral route of transmission for avian influenza virus infection for tigers feeding on H5N1 infected bird carcasses. (42) The virus may enter the gastrointestinal tract of carnivorous mammals and infect the liver through the portal system. (17,42) The demonstration of avian influenza virus receptors (SA[alpha]2,3Gal) in the liver, kidney, spleen, brain, intestine, and endothelium of humans supports this theory, but it has not been investigated in pinnipeds. (43)

Can marine mammals be sentinels for the presence of highly pathogenic avian influenza (HPAI)?

Because of seals' increased risk of acquiring avian influenzas due to their intimate association with seabirds, and their possible role as "mixing vessels" for pandemic strains, they could be used as sentinels for HPAI. Wildlife rehabilitation centers could opportunistically monitor seal populations through their stranded patients' serology. In addition to HPAI surveillance, this data could also be used in marine mammal conservation efforts. Admittedly, since the prevalence of influenza in seals is suspected to be low, waterfowl would be more sensitive sentinels. (28)

Can indigenous peoples involved in the hunting or consumption of marine mammals be at greater risk for transfer of avian influenza?

This has been suggested by multiple researchers. (22,28) Seals are still commonly hunted in the Arctic Ocean for food and fur. (22,28) Since human endothelial cells have avian influenza virus receptors (SA[alpha]2,3Gal), knife injuries during processing of seal carcasses could potentially cause vasculitis or systemic infection. (43) These carcasses undergo no official inspection and are sometimes consumed raw, presenting the opportunity for oral virus transmission as well. (28,42) To date, no such infections have been reported. This may be due to a lack of recognition, reporting, or incidence. A study by Siembieda et al reported that waterfowl hunters were 8 times more likely to be exposed to avian influenza-infected wildlife than were biologists, veterinarians, and the general public. (44) It would be reasonable to extrapolate these findings for seal subsistence hunters, though their risk may be smaller due to the low prevalence of viral infection in seals. (28)

Can active metabolites of antivirals, such as oseltamivir (Tamiflu[R]), in wastewater lead to antiviral resistance in marine mammals and birds, creating a cycle that breeds increasingly virulent strains?

Research has shown that the antiviral Tamiflu is largely excreted from the human body in its active form and that current methods of wastewater treatment do not remove many types of antiviral drugs from effluent. (45,46) A study by Ellis reported low risk exposure levels of oseltamivir in wastewater and underscored that little is known about long term chronic exposure to low-level water and sediment concentrations of antiviral drugs. (45) It stands to reason that waterfowl, such as ducks, sifting through antiviral-contaminated sediment would provide a good breeding ground for resistant strains of influenza. This would increase the risk of both seals, who share haul out sites with and predate on waterfowl, and subsistence hunters of acquiring antiviral-resistant influenza infections. (17,28,47) More research is needed on long term effects on wildlife and humans and on the effective removal of antiviral drugs and their metabolites from wastewater.

Further research is needed in these areas, including whether each potential threat could act in tandem with another to produce a greater negative effect than each alone. Such research would also be instrumental in allowing public health professionals to form plans of action and intercession in the event of an influenza outbreak.


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CPT Virginia C. White, VC, USA

CPT White is Chief, Leavenworth Branch Veterinary Services, Fort Leavenworth, Kansas.
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Author:White, Virginia C.
Publication:U.S. Army Medical Department Journal
Article Type:Report
Geographic Code:1USA
Date:Jan 1, 2013
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