, Volume 183, Issue 6, pp 979–985 | Cite as

Fatal Pulmonary and Cerebellar Zygomycosis due to Rhizomucor pusillus in a Ringed Seal (Pusa hispida)

  • Shotaro Nakagun
  • Masako Okazaki
  • Takahito Toyotome
  • Nobuki Sugiyama
  • Kenichi Watanabe
  • Noriyuki Horiuchi
  • Yoshiyasu Kobayashi
Short Communication


A 4-year-old captive ringed seal (Pusa hispida) was treated with subcutaneous antibacterial injections for pus exuding wounds in the skin and associated blubber following a bite attack. Three months after the incident, the animal presented nystagmus and died the following day. At necropsy, there was a 25 × 18 × 25 mm well-delineated, opaque nodular mass in the lung, besides the skin ulcers and localized areas of discoloration in the blubber correlating with the bite wound and injection sites. Histopathology of the pulmonary mass demonstrated severe eosinophilic inflammatory infiltration among numerous intralesional fungal hyphae. The hyphae were irregularly branched, broad and aseptate, consistent of zygomycosis. Magnetic resonance imaging was conducted on the head, which was initially frozen intact, revealing diffuse areas of hyperintensity in the cerebellum. Restricted histopathologic examination of the cerebellum showed severe granulomatous inflammation well spread within the neuroparenchyma, associated with abundant intralesional fungal hyphae similar to those appreciated in the pulmonary mass. Molecular analyses of the fungi in the pulmonary and cerebellar tissue identified the etiologic agent in both sites as Rhizomucor pusillus. The likely route of infection is through inhalation of R. pusillus spores or fragmented hyphae from the environment that developed into an initial pulmonary infection, becoming the source of hematogenous dissemination to the cerebellum. The skin and blubber lesions likely contributed to immunosuppression. Zygomycosis is uncommon in pinnipeds, and the present report emphasizes the importance of considering zygomycete dissemination even when the primary focus is highly confined.


Rhizomucor pusillus Zygomycosis Lung Cerebellum Ringed seal Ceroid 



The authors thank the staff of Okhotsk Tokkari Center for their assistance in necropsy and sample collection.


This study was partially funded by the Sasakawa Scientific Research Grant (Grant Number 28-736) from The Japan Science Society.

Compliance with Ethical Standards

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11046_2018_268_MOESM1_ESM.xlsx (42 kb)
Supplementary material 1 (XLSX 41 kb)


  1. 1.
    Chandler FW, Kaplan W, Ajello L. Zygomycosis. In: Chandler FW, Kaplan W, Ajello L, editors. A colour atlas and textbook of the histopathology of mycotic diseases. Weert/Lochem: Wolfe Medical Publications Ltd; 1980. p. 122–8.Google Scholar
  2. 2.
    Ribes JA, Vanover-Sams CL, Baker DJ. Zygomycetes in human disease. Clin Microbiol Rev. 2000;13:236–301.CrossRefGoogle Scholar
  3. 3.
    Roden MM, Zaoutis TE, Buchanan WL, Knudsen TA, Sarkisova TA, Schaufele RL, Sein M, Sein T, Chiou CC, Chu JH, Kontoyiannis DP, Walsh TJ. Epidemiology and outcome of zygomycosis: review of 929 reported cases. Clin Infect Dis. 2005;41:634–53.CrossRefGoogle Scholar
  4. 4.
    Kaplan W, Goss LJ, Ajello L, Ivens MS. Pulmonary mucormycosis in a harp seal caused by Mucor pusillus. Mycopathol Mycol Appl. 1960;12:101–10.CrossRefGoogle Scholar
  5. 5.
    Reidarson TH, McBain JF, Dalton LM, Rinaldi MG. Mycotic diseases. In: Dierauf LA, Gulland FMD, editors. CRC handbook of marine mammal medicine. 2nd ed. New York: CRC Press; 2001. p. 337–55.CrossRefGoogle Scholar
  6. 6.
    Barnett JEF, Davison NJ, Thornton SM, Riley P, Cooper T, Wessels ME. Systemic mucormycosis in a hooded seal (Cystophora cristata). J Zoo Wildl Med. 2011;42:338–41.CrossRefGoogle Scholar
  7. 7.
    Sosa M, Gamble KC, Delaski K, Righton A. Clinical challenge: systemic Rhizopus microsporus infection with renal cavitation in a grey seal (Halichoerus grypus). J Zoo Wildl Med. 2013;44:1134–8.CrossRefGoogle Scholar
  8. 8.
    Barnett J, Riley P, Cooper T, Linton C, Wessels M. Mycotic encephalitis in a grey seal (Halichoerus grypus) pup associated with Rhizomucor pusillus infection. Vet Rec Case Rep. 2014;2:e000115.CrossRefGoogle Scholar
  9. 9.
    Huckabone SE, Gulland FMD, Johnson SM, Colegrove KM, Dodd EM, Pappagianis D, Dunkin RC, Casper D, Carlson EL, Sykes JE, Meyer W, Miller MA. Coccidiomycosis and other systemic mycoses of marine mammals stranding along the central California, USA coast: 1998–2012. J Wildl Dis. 2015;51:295–308.CrossRefGoogle Scholar
  10. 10.
    White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. San Diego: Academic Press; 1990. p. 315–22.Google Scholar
  11. 11.
    O’Donnell K. Fusarium and its near relatives. In: Reynolds DR, Taylor JW, editors. The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. Wallingford: CAB International; 1993. p. 225–33.Google Scholar
  12. 12.
    Voigt K, Cigelnik E, O’donnell K. Phylogeny and PCR identification of clinically important Zygomycetes based on nuclear ribosomal-DNA sequence data. J Clin Microbiol. 1999;37:3957–64.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Francesconi A, Kasai M, Harrington SM, Beveridge MG, Petraitiene R, Petraitis V, Schaufele RL, Walsh TJ. Automated and manual methods of DNA extraction for Aspergillus fumigatus and Rhizopus oryzae analyzed by quantitative real-time PCR. J Clin Microbiol. 2008;46:1978–84.CrossRefGoogle Scholar
  14. 14.
    Domsch KH, Gams W, Anderson T-H. Rhizomucor pusillus. In: Domsch KH, Gams W, Anderson T-H, editors. Compendium of soil fungi, vol. 1. London: Academic Press Ltd; 1980. p. 700–2.Google Scholar
  15. 15.
    Bonar CJ, Wagner RA. A third report of “golf ball disease” in an Amazonian River dolphin (Inia geoffrensis) associated with Streptococcus iniae. J Zoo Wildl Med. 2003;34:296–301.CrossRefGoogle Scholar
  16. 16.
    Orós J, Monagas P, Calabuig P, Luzardo OP, Camacho M. Pansteatitis associated with high levels of polychlorinated biphenyls in a wild loggerhead sea turtle Caretta caretta. Dis Aquat Org. 2013;102:237–42.CrossRefGoogle Scholar
  17. 17.
    Begg GS, Bruno DW, McVicar H. The histopathology and ultrastructure of steatitis affecting common dab Limanda limanda. Dis Aquat Org. 2000;41:123–33.CrossRefGoogle Scholar
  18. 18.
    Larsen RE, Buergelt C, Cardeilhac PT, Jacobson ER. Steatitis and fat necrosis in captive alligators. J Am Vet Med Assoc. 1983;183:1202–4.PubMedGoogle Scholar
  19. 19.
    Roberts RJ, Agius C. Pan-steatitis in farmed northern bluefin tuna, Thunnus thynnus (L.), in the eastern Adriatic. J Fish Dis. 2008;31:83–8.CrossRefGoogle Scholar
  20. 20.
    Soto S, Fondevila D, Gozález B, Gómez-Campos E, Domingo M. Multifocal granulomatous panniculitis with ceroid pigment in two Mediterranean striped dolphins (Stenella coeruleoalba). J Wildl Dis. 2010;46:320–5.CrossRefGoogle Scholar
  21. 21.
    Feldman MY. Reactions of nucleic acids and nucleoproteins with formaldehyde. Prog Nucleic Acid Res Mol Biol. 1973;13:1–49.CrossRefGoogle Scholar
  22. 22.
    Hagiwara D, Takahashi H, Watanabe A, Takahashi-Nakaguchi A, Kawamoto S, Kamei K, Gonoi T. Whole-genome comparison of Aspergillus fumigatus strains serially isolated from patients with Aspergillosis. J Clin Microbiol. 2014;52:4202–9.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Veterinary PathologyObihiro University of Agriculture and Veterinary MedicineObihiroJapan
  2. 2.Okhotsk Tokkari CenterMombetsuJapan
  3. 3.Diagnostic Center for Animal Health and Food SafetyObihiro University of Agriculture and Veterinary MedicineObihiroJapan
  4. 4.Uminonakamichi Animal HospitalFukuokaJapan

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