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Volume 29, Number 12—December 2023
Research Letter

Mass Mortality of Sea Lions Caused by Highly Pathogenic Avian Influenza A(H5N1) Virus

Author affiliations: Grupo de Investigaciones en Biología de la Conservación, Laboratorio Ecotono, INIBIOMA, Universidad Nacional del Comahue—CONICET, Bariloche, Argentina (V. Gamarra-Toledo, P.I. Plaza, S.A. Lambertucci); Museo de Historia Natural, Universidad Nacional de San Agustín de Arequipa, Arequipa, Peru (V. Gamarra-Toledo, R. Gutiérrez); Servicio Nacional de Áreas Naturales Protegidas por el Estado, Lima, Peru (R. Gutiérrez, G. Inga-Diaz, P. Saravia-Guevara, O. Pereyra-Meza, E. Coronado-Flores, A. Calderón-Cerrón, G. Quiroz-Jiménez, P. Martinez, D. Huamán-Mendoza, J.C. Nieto-Navarrete, S. Ventura); Asociación Convive Perú, Madre de Dios, Perú (G. Inga-Diaz)

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Abstract

We report a massive mortality of 5,224 sea lions (Otaria flavescens) in Peru that seemed to be associated with highly pathogenic avian influenza A(H5N1) virus infection. The transmission pathway may have been through the close contact of sea lions with infected wild birds. We recommend evaluating potential virus transmission among sea lions.

The panzootic (2020–2023) caused by the highly pathogenic avian influenza (HPAI) A(H5N1) caused numerous global outbreaks in 2022 (1). At the end of the year, the H5N1 virus reached South America, causing alarming bird mortalities in Peru (2). Comprehensive surveys suggest the virus killed >100,000 wild birds by the end of March 2023 only in protected areas (and >200,000 birds including other areas); particularly affected were Peruvian boobies (Sula variegata), guanay cormorants (Leucocarbo bougainvilliorum), and Peruvian pelicans (Pelecanus thagus) (3). The large biomass of infected wild birds may have led to a spillover event affecting marine mammals cohabiting with them, as reported in other parts of the world (4). Here, we report the death of several thousand sea lions (Otaria flavescens) on the coast of Peru within a few months; the sea lions manifested neurologic and respiratory signs. Clinical signs we observed suggest they were affected by HPAI H5N1, which was later confirmed by government and scientific reports (5,6).

Figure

Sea lion deaths and investigation associated with outbreak of highly pathogenic avian influenza A(H5N1) in Paracas National Reserve, Peru, on the coastline, February 2023. A) Sea lion carcasses on the beach. B) Dying sea lion with ataxia. C) Dead sea lion with avian influenza clinical signs (whitish secretions). D) Sea lion necropsy showing a congestive brain. E) Sea lion trapping and eating a sick guanay cormorant, January 23, 2023. F) Field work sampling on a beach with a large number of bathers in the surroundings of infected carcasses. Red arrow indicates study staff wearing health protection equipment conducting field survey. Photograph credits: A, B, and D, Daniel Ampuero; C and F, Giancarlo Inga; E, Sandra Lizarme.

Figure. Sea lion deaths and investigation associated with outbreak of highly pathogenic avian influenza A(H5N1) in Paracas National Reserve, Peru, on the coastline, February 2023. A) Sea lion carcasses on the...

During January–April 2023, we performed detailed surveillance of dead and agonal sea lions in protected marine areas of Peru (Figure). We found 5,224 animals dead or dying on beaches (Table). The synchronized high mortality rate we observed was concerning; up to 100 dead animals were found floating together in the sea, and 1,112 animals died on 1 island that has one of highest populations of sea lions in Peru (San Gallan, Ica, Reserva Nacional Paracas; Table). Those unprecedented massive mortalities for this region and even the entire world killed ≈5% of Peru’s population of this species in a few months (Figure, panels A, B; Appendix Figure) (7).

Video 1

Individual sea lion (Otaria flavescens) with acute respiratory distress and showing white foam from the mouth and nervous incoordination caused by highly pathogenic avian influenza A(H5N1) virus. The video was recorded on a beach in the city of Lima, Peru.

Video 1. Individual sea lion (Otaria flavescens) with acute respiratory distress and showing white foam from the mouth and nervous incoordination caused by highly pathogenic avian influenza A(H5N1) virus. The...

Video 2

Female sea lion (Otaria flavescens) with acute respiratory distress, aborting and exhibiting nervous incoordination consistent with highly pathogenic avian influenza A(H5N1) virus. The video was recorded on a beach near the city of Paracas, Peru.

Video 2. Female sea lion (Otaria flavescens) with acute respiratory distress, aborting and exhibiting nervous incoordination consistent with highly pathogenic avian influenza A(H5N1) virus. The video was recorded on a...

National health authorities implemented restrictions regarding the manipulation of sick animals; for this reason, we were able to perform 1 necropsy, and the other observations were made by veterinarians at prudent distance. The clinical signs of agonal individuals were mainly neurologic, such as tremors, convulsions, and paralysis (Video 1; Video 2). The animals also showed respiratory signs such as dyspnea, tachypnea, and nasal and buccal secretions (Figure, panel C). The body condition of the necropsied sea lion ranged from good to very good. We observed substantial quantities of whitish secretions filling the upper respiratory tract (trachea and pharynx) (Figure, panel C). Lungs were congestive, with hemorrhagic focus compatible with interstitial pneumonia. Brain was also congestive, with hemorrhagic focus compatible with encephalitis (Figure, panel D).

Given the epidemiologic situation produced by HPAI H5N1 in wild birds that cohabit with the sea lions (2,3), the most plausible diagnosis causing this mass mortality event was acute disease caused by the virus. Clinical signs observed were similar to those reported in marine mammals infected with HPAI H5N1 in the United States (4). Official information from the Peru government and associated scientific research confirmed that not only birds but also sea lions tested positive for H5N1 virus (3,5,6). As of April 2023, sea lion deaths have surpassed 5,000 in Peru; thousands of sea lions with similar clinical signs died in Chile (8). This massive mortality event associated with HPAI H5N1 could be attributed to the large aggregations of sea lions that occur during the December–March breeding season (9).

In conclusion, sea lions in Peru experienced a deadly outbreak of disease that has caused mass deaths in several regions of the coastline (Figure). The sea lion mass mortality we described is compatible with systemic HPAI H5N1 that resulted in acute encephalitis and pneumonia. The source of the H5N1 virus affecting these sea lions was most probably the large number of infected live birds or their carcasses on the Peru coastline (2,3). Sea lions may be infected by close contact with those carcasses and through consuming them (Figure, panel E). The potential for direct transmission among sea lions from their colonial breeding behavior, in which they congregate by hundreds in the same area, should be evaluated, as should the large number of animals affected and the findings that many animals died simultaneously in groups in both Peru and Chile. Recent research described potential mammal-to-mammal infection in minks (Neovison vison) (10). In fact, unique mutations that merit further surveillance were found through viral sequencing of some of the deceased sea lions we surveyed (5).

Further research is required to confirm the HPAI H5N1 virus as the main factor affecting the sea lions and to address the transmission pathway in this social species. We call for more attention to human–infected animal interaction in this geographic region (Figure, panel F) to identify any rise in infections and prevent a new pandemic.

Mr. Gamarra-Toledo is a biologist and research associate at the Museum of Natural History, Universidad Nacional de San Agustín de Arequipa, Peru. His primary research interest is wildlife conservation in coastal ecosystems of Peru. Dr. Plaza is a veterinarian and research associate at the Conservation Biology Research Group of the Laboratorio Ecotono, Instituto de Investigaciones en Biodiversidad y Medioambiente, Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina. His primary research interests are wildlife health and epidemiology, human-wildlife interactions, and animal conservation.

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Acknowledgment

We thank the Unidad Operativa Funcional Monitoreo, Vigilancia y Control (Dirección de Gestión de Áreas Naturales Protegidas) of the Servicio Nacional de Áreas Naturales Protegidas por el Estado of the Peruvian Ministry of Environment, for permission to access and use the information provided (Expediente Tupa no. 0108-2023; CARTA no. 053 - 2023-SERNANP-AIP). We especially thank SERNANP park rangers for their help in the field survey and their involvement in the conservation and monitoring of wildlife in response to this health emergency. We thank the staff of the Wildlife Conservation Society, especially Paulo Colchao, Jorge Martinez, and Mariana Montoya, for their institutional and logistical support during field sample collection. Finally, we thank all public institutions that contribute to the monitoring of this epizootic and epidemiological surveillance in Peru.

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References

  1. Wille  M, Barr  IG. Resurgence of avian influenza virus. Science. 2022;376:45960. DOIPubMedGoogle Scholar
  2. Gamarra-Toledo  V, Plaza  PI, Gutiérrez  R, Luyo  P, Hernani  L, Angulo  F, et al. Avian flu threatens Neotropical birds. Science. 2023;379:246246. DOIPubMedGoogle Scholar
  3. Gamarra-Toledo  V, Plaza  PI, Angulo  F, Gutiérrez  R, García-Tello  O, Saravia-Guevara  P, et al. Highly pathogenic avian influenza (HPAI) strongly impacts wild birds in Peru. Biol Conserv. 2023;286:110272. DOIGoogle Scholar
  4. Puryear  W, Sawatzki  K, Hill  N, Foss  A, Stone  JJ, Doughty  L, et al. Highly pathogenic avian influenza A(H5N1) virus outbreak in New England seals, United States. Emerg Infect Dis. 2023;29:78691. DOIPubMedGoogle Scholar
  5. Leguia  M, Garcia-Glaessner  A, Muñoz-Saavedra  B, Juarez  D, Barrera  P, Calvo-Mac  C, et al. Highly pathogenic avian influenza A (H5N1) in marine mammals and seabirds in Peru. Nat Commun. 2023;14:5489. DOIPubMedGoogle Scholar
  6. Peru Ministry of Health. Avian influenza room [in Spanish]. 2023 [cited 2023 Sep 29]. https://www.dge.gob.pe/influenza-aviar-ah5
  7. International Union for Conservation of Nature and Natural Resources. IUCN red list of threatened species. 2017 [cited 2023 Sep 29]. https://www.iucnredlist.org
  8. National Fisheries and Aquaculture Service. Sernapesca reports that more than 11 thousand marine animals have been affected by avian influenza [in Spanish]. 2023. [cited 2023 Sep 29]. http://www.sernapesca.cl/noticias/sernapesca-informa-que-mas-de-11-mil-animales-marinos-han-sido-afectados-por-la-influenza
  9. Soto  KH, Trites  AW. South American sea lions in Peru have a lek-like mating system. Mar Mamm Sci. 2011;27:30633. DOIGoogle Scholar
  10. Agüero  M, Monne  I, Sánchez  A, Zecchin  B, Fusaro  A, Ruano  MJ, et al. Highly pathogenic avian influenza A(H5N1) virus infection in farmed minks, Spain, October 2022. Euro Surveill. 2023;28:2300001. DOIPubMedGoogle Scholar

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Figures
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Cite This Article

DOI: 10.3201/eid2912.230192

Original Publication Date: October 30, 2023

1These two authors contributed equally to the study.

Table of Contents – Volume 29, Number 12—December 2023

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Víctor Gamarra-Toledo, Museo de Historia Natural de la Universidad Nacional de San Agustín de Arequipa—Area de Ornitología, Arequipa, Arequipa 04000, Peru

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Page created: October 30, 2023
Page updated: November 18, 2023
Page reviewed: November 18, 2023
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
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