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Mycopathologia

, Volume 183, Issue 5, pp 793–803 | Cite as

Immunohistochemical Cross-Reactivity Between Paracoccidioides sp. from Dolphins and Histoplasma capsulatum

  • Godai Shumoto
  • Keiichi Ueda
  • Sayaka Yamaguchi
  • Takashi Kaneshima
  • Toshihiro Konno
  • Yoshie Terashima
  • Atsushi Yamamoto
  • Luciene A. Nagashima
  • Eiko N. Itano
  • Ayako SanoEmail author
Original Paper

Abstract

Paracoccidioidomycosis ceti is a cutaneous disease of cetaceans caused by uncultivated Paracoccidioides brasiliensis or Paracoccidioides spp. Serological cross-reactions between paracoccidioidomycosis ceti and paracoccidioidomycosis, paracoccidioidomycosis and histoplasmosis, and paracoccidioidomycosis and coccidioidomycosis have been reported before. The present study aimed to detect immunohistochemical cross-reaction between antibodies to Paracoccidioides sp. and Histoplasma capsulatum, and vice versa. Thirty murine sera, obtained from experimental infections of 6 isolates of H. capsulatum, were reacted with paraffin-embedded yeast-form cells of Paracoccidioides sp. derived from a case of paracoccidioidomycosis ceti in Japan. The murine sera were also reacted with human isolates of H. capsulatum yeast cells, with P. brasiliensis yeast cells, and with fungal cells of Coccidioides posadasii. Three dolphins’ sera from cases of paracoccidioidomycosis ceti, two human sera from patients with paracoccidioidomycosis, and a serum from a healthy person with a history of coccidioidomycosis were used in order to determine that the tested fungal cells reacted properly. Sera derived from mice infected with an isolate of H. capsulatum reacted positively against yeast cells of Paracoccidioides sp., yeast cells of P. brasiliensis, and fungal cells of C. posadasii, while those derived from other strains were negative. The present study recorded for the first time the cross-reaction between the yeast cells of H. capsulatum and antibodies against Paracoccidioides spp., the yeast cells of Paracoccidioides sp. and antibodies against H. capsulatum, the yeast cells of Paracoccidioides sp. and antibodies against Coccidioides sp., and fungal cells of C. posadasii and antibodies against Paracoccidioides spp.

Keywords

Coccidioidomycosis Cross-reaction Histoplasmosis Paracoccidioidomycosis Paracoccidioidomycosis ceti 

Notes

Acknowledgements

We are grateful to Drs. Katsuhiko Kamei and Shahana Sharmin (Medical Mycology Research Center, Chiba University, Chiba, Japan) for allowing the usage of serum samples, and to Drs. Kazuko Nishimura (emeritus professor of Medical Mycology Research Center, Chiba University, Chiba, Japan), to Makoto Miyaji (late emeritus professor of Medical Mycology Research Center, Chiba University, Chiba, Japan), and to Kunie Iabuki Coelho Rabello (emeritus professor of Department of Pathology, Faculty of Medicine, State University of São Paulo, Botucatu, Brazil) for the paraffin-embedded tissue samples. This work was partially supported by JICA Grant No. J17-50165 awarded to Drs. Ayako Sano and Luciene Airy Nagashima. We would like to thank Editage (www.editage.jp) for English language editing.

Compliance with ethical standards

Conflicts of interest

The authors declare no conflicts of interest. The authors alone are responsible for the content and writing of this paper.

Ethical approval

The usage of human sera was permitted by the ethic committee of University of the Ryukyus, No. 383 approved on November 24, 2017. Animal sera were derived from clinical samples, or previously permitted experimental infections, with permission No. 20020018 from Chiba University; therefore, our work did not qualify as an animal experiment according to the animal welfare committee of the University of the Ryukyus.

References

  1. 1.
    Vilela R, Bossart GD, St. Leger JA, Dalton LM, Reif JS, Schaefer AM, McCarthy PJ, Fair PA, Mendoza L. Cutaneous granulomas in dolphins caused by novel uncultivated Paracoccidioides brasiliensis. Emerg Infect Dis. 2016;22:2063–9.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Minakawa T, Ueda K, Tanaka M, Tanaka N, Kuwamura M, Izawa T, Konno T, Yamate J, Itano EN, Sano A, Wada S. Detection of multiple budding yeast cells and a partial sequence of 43-kDa glycoprotein coding gene of Paracoccidioides brasiliensis from a case of lacaziosis in a female Pacific white-sided dolphin (Lagenorhynchus obliquidens). Mycopathologia. 2016;181:523–9.CrossRefPubMedGoogle Scholar
  3. 3.
    Sacristán C, Esperón F, Ewbank AC, Kolesnikovas CKM, Catão-Dias JL. Paracoccidioidomycosis ceti in an Atlantic bottlenose dolphin (Tursiops truncatus), Brazil. Transbound Emerg Dis. 2018;65:585–7.CrossRefPubMedGoogle Scholar
  4. 4.
    Esperón F, García-Párraga D, Bellière EN, Sánchez-Vizcaíno JM. Molecular diagnosis of lobomycosis-like disease in a bottlenose dolphin in captivity. Med Mycol. 2012;50:106–9.CrossRefPubMedGoogle Scholar
  5. 5.
    Ueda K, Sano A, Yamate J, Itano EN, Kuwamura M, Izawa T, Tanaka M, Hasegawa Y, Chibana H, Izumisawa Y, Miyahara H, Uchida S. Two cases of lacaziosis in bottlenose dolphins (Tursiops truncatus) in Japan. Case Rep Vet Med. 2013.  https://doi.org/10.1155/2013/318548.CrossRefGoogle Scholar
  6. 6.
    Ueda K, Nakamura I, Itano EN, Takemura K, Nakazato Y, Sano A. Trichosporon asteroides isolated from cutaneous lesions of a suspected case of “ paracoccidioidomycosis ceti “ in a bottlenose dolphin (Tursiops truncatus). Mycopathologia. 2017;182:937–46.CrossRefPubMedGoogle Scholar
  7. 7.
    Ramos EA, Castelblanco-Martínez DN, Garcia J, Rojas Arias J, Foley JR, Audley K, Van Waerebeek K, Van Bressem MF. Lobomycosis-like disease in common bottlenose dolphins Tursiops truncatus from Belize and Mexico:bridging the gap between the Americas. Dis Aquat Organ. 2018;128:1–12.CrossRefPubMedGoogle Scholar
  8. 8.
    Van Bressem MF, Simões-Lopes PC, Félix F, Kiszka JJ, Daura-Jorge FG, Avila IC, Secchi ER, Flach L, Fruet PF, du Toit K, Ott PH, Elwen S, Di Giacomo AB, Wagner J, Banks A, Van Waerebeek K. Epidemiology of lobomycosis-like disease in bottlenose dolphins Tursiops spp. from South America and southern Africa. Dis Aquat Organ. 2015;117:59–75.CrossRefPubMedGoogle Scholar
  9. 9.
    Rotstein DS, Burdett LG, McLellan W, Schwacke L, Rowles T, Terio KA, Schultz S, Pabst A. Lobomycosis in offshore bottlenose dolphins (Tursiops truncatus), North Carolina. Emerg Infect Dis. 2009;15:588–90.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Ramos-E-Silva M, Aguiar-Santos-Virela F, Cardoso-de-Brito A, Coelho-Carneiro S. Lobomycosis: literature review and future perspectives. Actas Dermosifiliogr. 2009;100:92–100.CrossRefPubMedGoogle Scholar
  11. 11.
    Talhari S, Talhari C. Lobomycosis. Clin Dermatol. 2012;30:420–4.CrossRefPubMedGoogle Scholar
  12. 12.
    Reif JS, Schaefer AM, Bossart GD. Risk of zoonotic transmission from dolphins to humans. Vector Borne Zoonotic Dis. 2013;13:689–93.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Paniz-Mondolfi A, Talhari C, Sander Hoffmann L, Connor DL, Talhari S, Bermudez-Villapol L, Hernandez-Perez M, Van Bressem MF. Lobomycosis: an emerging disease in humans and delphinidae. Mycoses. 2012;55:298–309.CrossRefPubMedGoogle Scholar
  14. 14.
    Lane EP, de Wet M, Thompson P, Siebert U, Wohlsein P, Plön S. A systematic health assessment of Indian ocean bottlenose (Tursiops aduncus) and Indo-Pacific humpback (Sousa plumbea) dolphins incidentally caught in shark nets off the KwaZulu-Natal Coast, South Africa. PLoS ONE. 2014;9:e107038.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Palmer C, Peterson A. First report of a lacaziosis-like disease (LLD) observed in the Australian snubfin dolphin (‘Orcaella heinsohni’) in Darwin Harbour, Northern Territory, Australia. North Territ Nat. 2014;25:3–6.Google Scholar
  16. 16.
    Van Bressem MF, Minton G, Sutaria D, Kelkar N, Peter C, Zulkarnaen M, Mansur RM, Porter L, Vargas LH, Rajamani L. Cutaneous nodules in Irrawaddy dolphins: an emerging disease in vulnerable populations. Dis Aquat Organ. 2014;107:181–9.CrossRefPubMedGoogle Scholar
  17. 17.
    Sacristán C, Réssio RA, Castilho P, Fernandes N, Costa-Silva S, Esperón F, Daura-Jorge FG, Groch KR, Kolesnikovas CK, Marigo J, Ott PH, Oliveira LR, Sánchez-Sarmiento AM, Simões-Lopes PC, Catão-Dias JL. Lacaziosis-like disease in Tursiops truncatus from Brazil: a histopathological and immunohistochemical approach. Dis Aquat Organ. 2016;117:229–35.CrossRefPubMedGoogle Scholar
  18. 18.
    Camargo ZP, Baruzzi RG, Maeda SM, Floriano MC. Antigenic relationship between Loboa loboi and Paracoccidioides brasiliensis as shown by serological method. Med Mycol. 1998;36:413–7.CrossRefPubMedGoogle Scholar
  19. 19.
    Yang MC, Magee DM, Kaufman L, Zhu Y, Cox RA. Recombinant Coccidioides immitis complement-fixing antigen: detection of an epitope shared by C. immitis, Histoplasma capsulatum, and Blastomyces dermatitidis. Clin Diagn Lab Immunol. 1997;4:19–22.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Wheat J, Wheat H, Connolly P, Kleiman M, Supparatpinyo K, Nelson K, Bradsher R, Restrepo A. Cross-reactivity in Histoplasma capsulatum variety capsulatum antigen assays of urine samples from patients with endemic mycoses. Clin Infect Dis. 1997;24:1169–71.CrossRefPubMedGoogle Scholar
  21. 21.
    Ferreira JB, Navarro IT, Freire RL, Oliveira GG, Omori AM, Belitardo DR, Itano EN, Camargo ZP, Ono MA. Evaluation of Paracoccidioides brasiliensis Infection in dairy goats. Mycopathologia. 2013;176:95–9.CrossRefPubMedGoogle Scholar
  22. 22.
    Reidarson TH, McBain JF, Dalton LM, Rinaldi MG. Chapter 17: Mycotic Diseases. In: Dierauf LA, Gulland FMD, editors. CRC handbook of marine mammal medicine. 2nd ed. Washington, DC: CRC; 2001. p. 337–55.CrossRefGoogle Scholar
  23. 23.
    Cates MB, Kaufman L, Grabau JH, Pletcher JM, Schroeder JP. Blastomycosis in an Atlantic bottlenose dolphin. J Am Vet Med Assoc. 1986;189:1148–50.PubMedGoogle Scholar
  24. 24.
    Reidarson TH, Griner LA, Pappagianis D, McBain J. Coccidioidomycosis in a bottlenose dolphin. J Wildlife Dis. 1998;34:629–31.CrossRefGoogle Scholar
  25. 25.
    Jensen ED, Lipscomb T, Van Bonn B, Miller G, Fradkin JM, Ridgway SH. Disseminated histoplasmosis in an Atlantic bottlenose dolphin (Tursiops truncatus). J Zoo Wildlife Med. 1998;29:456–60.Google Scholar
  26. 26.
    Kamei K, Sano A, Kikuchi K, Makimura K, Niimi M, Suzuki K, Uehara Y, Okabe N, Nishimura K, Miyaji M. The trend of imported mycoses in Japan. J Infect Chemother. 2003;9:16–20.CrossRefPubMedGoogle Scholar
  27. 27.
    Bahr NC, Antinori S, Wheat LJ, Sarosi GA. Histoplasmosis infections worldwide: thinking outside of the Ohio River valley. Curr Trop Med Rep. 2015;2:70–80.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Sano A, Takahashi H, Murata Y, Toujimbara K. Histoplasmosis and pseudofarcy in Japan. Jpn J Vet Hist. 2011;48:1–21.Google Scholar
  29. 29.
    Sharmin S, Ohori A, Sano A, Kamei K, Yamaguchi M, Takeo K, Uno J, Nishimura K, Miyaji M. Histoplasma capsulatum variety duboisii isolated in Japan from an HIV-infected Ugandan patient. Nihon Ishinkin Gakkai Zasshi. 2003;44:299–306.CrossRefPubMedGoogle Scholar
  30. 30.
    Kwon-Chung KJ, Bennett JE. 18. Histoplasmosis. In: Kwon-Chung KJ, Bennett JE, editors. Medical mycology. Malven: Lea & Febiger; 1992. p. 464–513.Google Scholar
  31. 31.
    de Teixeira M, Patané JS, Taylor ML, Gómez BL, Theodoro RC, de Hoog S, Engelthaler DM, Zancopé-Oliveira RM, Felipe MS, Barker BM. Worldwide phylogenetic distributions and population dynamics of the genus Histoplasma. PLoS Negl Trop Dis. 2016;10:e0004732.  https://doi.org/10.1371/journal.CrossRefPubMedCentralGoogle Scholar
  32. 32.
    Tristão FS, Leonello PC, Nagashima LA, Sano A, Ono MA, Itano EM. Carbohydrate-rich high-molecular-mass antigens are strongly recognized during experimental Histoplasma capsulatum infection. Rev Soc Bras Med Trop. 2012;45:232–7.CrossRefPubMedGoogle Scholar
  33. 33.
    Turissini DA, Gomez OM, Teixeira MM, McEwen JG, Matute DR. Species boundaries in the human pathogen Paracoccidioides. Fungal Genet Biol. 2017;106:9–25.CrossRefPubMedGoogle Scholar
  34. 34.
    Amper NA, Einstein HE, Galgiani JN, Pappagianis D, Wieden M. Coccidioidomycosis. In: Mandell GL, editor. Atlas of infectious diseases. Philadelphia: Current Medicine, Inc.; 2000. p. 24–41.Google Scholar
  35. 35.
    Sano A, Miyaji M, Kamei K, Mikami Y, Nishimura K. Reexamination of Coccidioides spp. reserved in the Research Center for Pathogenic Fungi and Microbial Toxicoses, Chiba University, based on a multiple gene analysis. Med Mycol J. 2006;47:113–7.CrossRefGoogle Scholar
  36. 36.
    Garrison R. Studies of Respiratory activity of Histoplasma capsulatum. 1. Aspects of the aerobic metabolism of the yeast phase. J Infect Dis. 1961;108:120–4.CrossRefPubMedGoogle Scholar
  37. 37.
    Yamato H, Hitomi H, Maekawa S, Mimura K. A case of histoplasmosis. Acta Med Okayama. 1957;11:347–64.Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Godai Shumoto
    • 1
    • 2
    • 5
  • Keiichi Ueda
    • 3
  • Sayaka Yamaguchi
    • 4
  • Takashi Kaneshima
    • 1
  • Toshihiro Konno
    • 2
    • 5
    • 6
  • Yoshie Terashima
    • 2
    • 6
  • Atsushi Yamamoto
    • 2
    • 7
  • Luciene A. Nagashima
    • 8
  • Eiko N. Itano
    • 9
  • Ayako Sano
    • 1
    • 2
    • 5
    • 6
    Email author
  1. 1.Ryukyu Animal Medical CenterTomigusukuJapan
  2. 2.The United Graduate School of Agriculture SciencesKagoshima UniversityKagoshimaJapan
  3. 3.Okinawa Churashima FoundationKunigami-GunJapan
  4. 4.Department of Dermatology, Faculty of MedicineUniversity of the RyukyusNakagusuku-GunJapan
  5. 5.Department of Animal Sciences, Faculty of AgricultureUniversity of the RyukyusNakagusuku-GunJapan
  6. 6.Tropical Bioresources Research CenterUniversity of the RyukyusNakagusuku-GunJapan
  7. 7.Faculty of FisheriesKagoshima UniversityKagoshimaJapan
  8. 8.Institute of Technology of ParanaCuritibaBrazil
  9. 9.Department of Pathological Science, CCBState University of LondrinaLondrinaBrazil

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