A Cryptococcus gattii Outbreak in Porpoises and Dolphins from the Salish Sea: 1997–2016
IAAAM 2021
Sarah J. Teman1*; Joseph K. Gaydos1; Stephanie A. Norman2; Jessica L. Huggins3; Dyanna M. Lambourn4; John Calambokidis3; John Ford5; M. Bradley Hanson6; Martin Haulena7; Erin Zabek8; Paul Cottrell9; Linda Hoang10; Michael M. Garner11; Stephen Raverty8
1The SeaDoc Society, Karen C. Drayer Wildlife Health Center, UC Davis School of Veterinary Medicine, Eastsound, WA, USA; 2Marine-Med: Marine Research, Epidemiology, and Veterinary Medicine, Bothell, WA, USA; 3Cascadia Research, Olympia, WA, USA; 4Marine Mammal Investigations, Washington Department of Fish and Wildlife, Lakewood, WA, USA; 5Fisheries and Oceans Canada, Nanaimo, BC, Canada; 6Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, WA, USA; 7Vancouver Aquarium, Vancouver, BC, Canada; 8Animal Health Centre, British Columbia Ministry of Agriculture, Abbotsford, BC, Canada; 9Fisheries and Oceans Canada, Vancouver, BC, Canada; 10BC Centre for Disease Control, Vancouver, BC, Canada; 11Northwest ZooPath, Monroe, WA, USA

Abstract

Cryptococcus gattii is a fungal pathogen that primarily affects the respiratory and nervous systems of humans and animals.1,2 Previously thought to only occur in tropical and subtropical areas, C. gattii emerged in temperate North America in 1999 when it caused a multispecies outbreak in British Columbia (Canada), Washington State (USA), and Oregon (USA).3 The epizootic affected humans, domestic animals (e.g., dogs, cats, ferrets, llamas), and wildlife, including Eastern gray squirrels (Sciurus carolinensis) and cetaceans.4,5 While case reports of C. gattii in cetaceans have been documented in endemic areas, to the best of our knowledge, an epizootic in cetaceans has not been previously described. Using the case definition of a stranded odontocete in which C. gattii was cultured or amplified by PCR from case material or yeast consistent with C. gattii were identified microscopically, we found the index case of C. gattii in a Dall’s porpoise in 1997. This was two years prior to the terrestrial outbreak initially recognized in 1999.3 We identified 44 cases from 1997 to 2016, including 29 harbor porpoises (Phocoena phocoena), 13 Dall’s porpoises (Phocoenoides dalli), and 2 Pacific white-sided dolphins (Lagenorhynchus/Sagmatias obliquidens). There have also been 2 cases in harbor seals (Phoca vitulina) which may have been exposed in the marine environment or on land.6 The majority of cases in small odontocetes (n=31) were clustered between 2003 and 2010. We defined the spatiotemporal extent of the outbreak, identified the risk factors for disease, and documented cases of maternal/fetal transmission.

Other fungal diseases reported in odontocetes include blastomycosis, lacaziosis, and mucormycosis. Previously, mycoses were rarely associated with epidemics in marine mammals due to their environmental source of exposure and generally poor transmissibility.7 This epizootic and other data, however, suggest that fungal pathogens are an emerging source of mortality for odontocetes, particularly in environments associated with human disturbance such as agriculture, construction, and forestry.8 Large-scale mycotic outbreaks have been associated with dust storms, volcanic eruptions, and other events, and in temperate areas disease could increase with climate change and increased environmental disturbance.9

There was no apparent reason for the relatively sudden decline in cases of C. gattii in small odontocetes in 2016, however, another novel fungal disease, mucormycosis, emerged in the Salish Sea in 2012. To date, harbor seals (Phoca vitulina), harbor porpoises, and an endangered southern resident killer whale (Orcinus orca) have succumbed to mucormycosis.10

Retrospectively, it appears that porpoises were a sentinel species for the emergence of C. gattii in North America. Despite surveillance, cases of C. gattii have not been detected in this region in four years.

Acknowledgements

We thank the West Coast Marine Mammal Stranding Network partners who helped with carcass recovery and sample collection; particularly Anna Hall, Kristin Wilkinson (NOAA Fisheries), Jennifer Olson and Alyssa Scott (San Juan County Marine Mammal Stranding Network), and the staff and volunteers of Cascadia Research Collective, Central Puget Sound Marine Mammal Stranding Network, Whatcom Marine Mammal Stranding Network, and the Washington Department of Fish and Wildlife Marine Mammal Investigations. The authors also thank Dr. Abby Stanger for early help compiling these data and the staff of Animal Health Centre in British Columbia for fungal culturing and molecular typing. All stranding response activities were conducted under permit from NOAA Fisheries and Canada’s Department of Fisheries and Oceans. Funding was provided through multiple grants to stranding networks through the John H. Prescott Marine Mammal Rescue and Assistance Grant Program.

*Presenting author

Literature Cited

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6.  Rosenberg JF, Haulena M, Hoang LMN, Morshed M, Zabek E, Raverty SA. 2016. Cyrptococcus gattii type VGIIa infection in harbor seals (Phoca vitulina) in British Columbia, Canada. J Wildl Dis 52:1–5.

7.  Reidarson TH, Garcia-Parraga D, Wiederhold NP. 2018. Marine mammal mycoses. In: CRC Handbook of Marine Mammal Medicine, Third edition. Gulland FMD, Dierauf LA, Whitman KL. Boca Raton (FL): CRC Press. p 389–423.

8.  Miller RM, Lodge DJ. 2007. Fungal responses to disturbance: agriculture and forestry. In: Environmental and Microbial Relationships, The Mycota, Volume 4. Kubicek C and Druzhinina I. Berlin (Gemany): Springer Nature. p 47–68.

9.  Benedict K, Park BJ. 2014. Invasive fungal infections after natural disasters. Emerg Infect Dis 20:349–355.

10.  Huggins JL, Garner MM, Raverty SA, Lambourn DM, Norman SA, Rhodes LD, Gaydos JK, Olson JK, Haulena M, Hanson MB. 2020. The emergence of mucormycosis in free-ranging marine mammals of the Pacific Northwest. Front Mar Sci 7:1–9.

 

Speaker Information
(click the speaker's name to view other papers and abstracts submitted by this speaker)

Sarah Teman
The SeaDoc Society
Karen C. Drayer Wildlife Health Center
UC Davis School of Veterinary Medicine
Eastsound, WA, USA


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