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Seroprevalence of Antibodies Against Paracoccidioides Spp. in Captive Dolphins from Three Aquaria in Japan

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Abstract

The skin disease paracoccidioidomycosis ceti occurs in several dolphin species globally. Infection by the unculturable fungi Paracoccidioides brasilensis or other Paracoccidioides spp. results in chronic cutaneous and granulomatous lesions. In this study we used immunohistochemistry to investigate the seroprevalence of antibodies to Paracoccidioides spp. in captive dolphins from three aquaria in Japan. We had previously reported that there were serological cross-reactions for Paracoccidioides spp. with related species in the order Onygenales. We hypothesized that the degree of serological cross-reactions for Paracoccidioides spp. might be lower in areas, such as Japan, where the fungal diseases coccidiodomycosis and paracoccidiodomycosis are not endemic. Sera from 41 apparently healthy dolphins, including 20 Atlantic bottlenose dolphins (BD: Tursiops truncatus), 6 Indo-Pacific bottlenose dolphins (IPBD: Tursiops aduncus), 2 F1 generation of a cross between BD and IPBD (F1), 3 Pacific white-sided dolphins (PWD: Lagenorhynchus obliquidens), 2 pantropical spotted dolphins (PSD: Stenella attenuata), 6 false killer whales (FKW: Pseudorca crassidens), and 2 rough-toothed dolphins (RTD: Steno bredanensis) were investigated. Sera from three dolphins with paracoccidioidomycosis ceti were used as a positive control. The yeast-form cells of Paracoccidioides spp. in the cutaneous tissue sample derived from the first Japanese paracoccidioidomycosis ceti case were used as the antigen for the immunohistochemistry. Of the 41 dolphins tested, 61.0% had antibodies against Paracoccidioides spp. This indicates that dolphins of several species in Japanese aquaria have likely been exposed to the pathogen Paracoccidioides spp.

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Acknowledgements

The present research was performed under an agreement between the Okinawa Churashima Foundation and the University of the Ryukyus. This research was supported by the University of the Ryukyus Research Project Grant Program for women researchers from the University of the Ryukyus, Nishihara, Okinawa, Japan (No. 7, Project 18SP05107), to Dr. Ayako Sano. We would like to thank Editage (www.editage.jp) for English language editing.

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Author notes

  1. Tomoko Minakawa and Godai Shumoto have contributed equally.

Authors and Affiliations

  1. Okinawa Churashima Foundation, Kunigami-Gun, Aza Ishikawa 888, Motobu-Cho, Okinawa, 905-0206, Japan

    Tomoko Minakawa & Keiichi Ueda

  2. Ryukyu Animal Medical Center, Yone 5-24, Tomigusuku, Okinawa, 901-0224, Japan

    Godai Shumoto & Ayako Sano

  3. The United Graduate School of Agricultural Sciences, Kagoshima University, 1-21-24 Korimoto, Kagoshima, 890-0065, Japan

    Godai Shumoto, Toshihiro Konno & Ayako Sano

  4. Suma Aqualife Park, Wakamiya-Cho 1-3-5, Suma-Ku, Kobe, Hyogo, 654-0049, Japan

    Chiho Kezuka & Naoki Kamezaki

  5. Laboratory of Veterinary Pathology, Division of Veterinary Sciences, Rinku-Campus, Osaka Prefecture University, Rinku-OraiKita 1-58, Izumisano, Osaka, 598-8531, Japan

    Takeshi Izawa & Jyoji Yamate

  6. Chiran Meat Inspection Center, Kagoshima Prefecture, 22216-1 Minamibeppu Chiran-Cho Minamikyushu-Shi, Kagoshima, 891-0912, Japan

    Kyoko Sasaki

  7. Department of Dermatology, Faculty of Medicine, University of the Ryukyus, Uehara, Nakagusuku-Gun, Nishihara, Okinawa, 903-0215, Japan

    Sayaka Yamaguchi

  8. Tropical Bioresources Research Center, University of the Ryukyus, Sembaru 1, Nakagusuku-Gun, Nishihara-Cho, Okinawa, 903-0213, Japan

    Toshihiro Konno & Ayako Sano

  9. Faculty of Agriculture, University of the Ryukyus, Sembaru 1, Nakagusuku-Gun, Nishihara-Cho, Okinawa, 903-0213, Japan

    Toshihiro Konno & Ayako Sano

  10. Department of Pathological Science, CCB, State University of Londrina, P.O. Box 6001, Londrina, PR, 86051-970, Brazil

    Eiko Nakagawa Itano

  11. Laboratory of Aquatic Medicine, School of Veterinary Medicine, Nippon Veterinary and Life Science University, Kyonan-Cho 1-7-1, Musashino, Tokyo, 180-8602, Japan

    Shinpei Wada

  12. College of International Studies, Meio University, 1220-1 Biimata, Nago, Okinawa, 905-8585, Japan

    Chris Willson

Authors
  1. Tomoko Minakawa
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  2. Godai Shumoto
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  4. Takeshi Izawa
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  5. Kyoko Sasaki
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  6. Sayaka Yamaguchi
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  7. Naoki Kamezaki
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  8. Jyoji Yamate
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  9. Toshihiro Konno
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  10. Ayako Sano
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  11. Eiko Nakagawa Itano
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  12. Shinpei Wada
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  13. Chris Willson
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  14. Keiichi Ueda
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Contributions

TM helped in judgment for the immune staining, manuscript writing on the dolphin materials, and statistical analysis, GS contributed to judgment for the immune staining and whole manuscript writing, CK judged the health conditions of the dolphins, TI helped in stabilization for the immune staining, KS helped in judgment for the health conditions of the dolphins, SY contributed to stabilization for the immune staining and judgment, NK judged the health conditions of the dolphins, JY helped in stabilization for the immune staining, TK contributed to stabilization for the immune staining, AS designed experimentally and revised the manuscript, ENI helped in experimental design and concept, SW statistically analyzed and adviced for TM, CW biologically discussed and revised the manuscript, and KU corresponding for whole manuscript.

Corresponding author

Correspondence to Keiichi Ueda.

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Conflicts of interest

The authors declare that they have no conflict of interest. A part of the present study was used in the thesis for the doctoral degree of Dr. Tomoko Minakawa.

Human and Animal Rights

The usage of cetacean sera was permitted by the Animal Welfare Committee of the University of the Ryukyus (No. 2018079). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

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Minakawa, T., Shumoto, G., Kezuka, C. et al. Seroprevalence of Antibodies Against Paracoccidioides Spp. in Captive Dolphins from Three Aquaria in Japan. Mycopathologia 185, 1013–1020 (2020). https://doi.org/10.1007/s11046-020-00501-5

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  • DOI: https://doi.org/10.1007/s11046-020-00501-5

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