Skip to main content
Log in

Histopathology, Molecular Identification and Antifungal Susceptibility Testing of Nannizziopsis arthrosporioides from a Captive Cuban Rock Iguana (Cyclura nubila)

  • Original Article
  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Chrysosporium-related fungi, the cause of superficial and deep mycoses, are an emerging infectious disease affecting not only reptiles but also immunocompromized humans. However, the information on Nannizziopsis arthrosporioides is extremely scarce. We herein characterized N. arthrosporioides isolated from a Cuban rock iguana (Cyclura nubila). Three skin ulcers were found in a Cuban rock iguana after captivity for 8 years. Microscopic examination revealed hyperplastic, hyperkeratotic, and ulcerative dermatitis coupled with numerous branched, septate fungal hyphae. The fungal culture yielded growth of zonate, felted cottony-powdery colonies with lobate margins on medium. Maximum-likelihood phylogeny tree based on the combined partial actin and partial β-tubulin genes demonstrated that current isolates were mostly close to N. arthrosporioides. Furthermore, antifungal susceptibility test demonstrated that N. arthrosporioides had lowest minimal inhibitory concentration (MIC) values to isavuconazole, efinaconazole, and luliconazole, which may be the potential treatment of choice for N. arthrosporioides infection. The current study describes the first confirmed case of dermatomycosis caused by N. arthrosporioides of a captive reptile in Asia with detailed descriptions of the clinical, histopathological, and mycological features. The current findings provide new information on global distribution and host range of N. arthrosporioides and can raise the concern on the transboundary or emerging disease of N. arthrosporioides in Asian region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Cabanes FJ, Sutton DA, Guarro J. Chrysosporium-related fungi and reptiles: a fatal attraction. PLoS Pathog. 2014;10(10):e1004367.

    Article  Google Scholar 

  2. Nourrisson C, Vidal-Roux M, Cayot S, Jacomet C, Bothorel C, Ledoux-Pilon A, et al. Invasive infections caused by Nannizziopsis spp. molds in immunocompromised patients. Emerg Infect Dis. 2018;24(3):549–52.

    Article  Google Scholar 

  3. Pare JA, Sigler L, Hunter DB, Summerbell RC, Smith DA, Machin KL. Cutaneous mycoses in chameleons caused by the Chrysosporium anamorph of Nannizziopsis vriesii (Apinis) Currah. J Zoo Wildl Med. 1997;28(4):443–53.

    CAS  PubMed  Google Scholar 

  4. Sigler L, Hambleton S, Pare JA. Molecular characterization of reptile pathogens currently known as members of the Chrysosporium anamorph of Nannizziopsis vriesii complex and relationship with some human-associated isolates. J Clin Microbiol. 2013;51:3338–57.

    Article  CAS  Google Scholar 

  5. Wellehan JFX, Divers SJ. Mycology. In: Divers SJ, Stahl SJ, editors. Mader’s reptile and amphibian medicine and surgery. St. Louis: W.B. Saunders; 2019. p. 270–80.

    Chapter  Google Scholar 

  6. Stchigel AM, Sutton DA, Cano-Lira JF, Cabanes FJ, Abarca L, Tintelnot K, et al. Phylogeny of chrysosporia infecting reptiles: proposal of the new family Nannizziopsiaceae and five new species. Persoonia. 2013;31:86–100.

    Article  CAS  Google Scholar 

  7. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evolut. 2016;33:1870–4.

    Article  CAS  Google Scholar 

  8. Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi. 3ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2017.

  9. Toplon DE, Terrell SP, Sigler L, Jacobson ER. Dermatitis and cellulitis in leopard geckos (Eublepharis macularius) caused by the Chrysosporium anamorph of Nannizziopsis vriesii. Vet Pathol. 2013;50:585–9.

    Article  CAS  Google Scholar 

  10. Han J-I, Lee S-J, Na K-J. Necrotizing Dermatomycosis caused by Chrysosporium spp. in three captive green iguanas (Iguana iguana) in South Korea. J Exot Pet Med. 2010;19:240–4.

    Article  Google Scholar 

  11. Rhim H, Han J-I. Nannizziopsis chlamydospora associated necrotizing dermatomycosis in a bearded dragon (Pogona vitticeps). J Exot Pet Med. 2019;31:1–2.

    Article  Google Scholar 

  12. Schmidt-Ukaj S, Loncaric I, Spergser J, Richter B, Hochleithner M. Dermatomycosis in three central bearded dragons (Pogona vitticeps) associated with Nannizziopsis chlamydospora. J Vet Diagn Invest. 2016;28:319–22.

    Article  CAS  Google Scholar 

  13. Paré JA, Jacobson ER. Mycotic diseases of reptiles. In: Jacobson ER, editor. Infectious diseases and pathology of reptiles: a color atlas and text. Boca Raton: CRC Press; 2007. p. 527–70.

    Chapter  Google Scholar 

  14. Hill AG, Sandy JR, Begg A. Mycotic dermatitis in juvenile freshwater crocodiles (Crocodylus Johnstoni) caused by Nannizziopsis crocodili. J Zoo Wildl Med. 2019;50:225–30.

    Article  Google Scholar 

  15. Rachowicz LJ, Hero J-M, Alford RA, Taylor JW, Morgan JAT, Vredenburg VT, et al. The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conserv Biol. 2005;19:1441–8.

    Article  Google Scholar 

  16. Warwick C. The morality of the reptile “pet” trade. J Anim Ethics. 2014;4:74–94.

    Article  Google Scholar 

  17. Moutou F, Pastoret PP. Invasive reptiles and amphibians. Rev Sci Technol. 2010;29:235–40.

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank all the staff at the Institute of Wildlife Conservation and the Pingtung Rescue Center for Endangered Wild Animals, National Pingtung University of Science and Technology, for excellent animal care and sample collection. We also thank Phoebe Chi-Fei Kao, Yu-Han Hsieh, Cheng-Hsin Shih, and Ting-Wei Lee at the Graduate Institute of Molecular and Comparative Pathobiology, National Taiwan University, for discussions.

Funding

This study has been funded and supported by the Ministry of Science & Technology, Taiwan under Grant MOST108-2314-B-182 -047 to Pei-Lun Sun and MOST109-2313-B-002 -018 -MY3 to Pin-Huan Yu.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wen-Ta Li.

Ethics declarations

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical approval

The patient was treated using the highest standards of care at the veterinary teaching hospital in all steps of diagnosis and treatment.

Informed Consent

We obtained consent from the Institute of Wildlife Conservation, National Pingtung University of Science and Technology.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Mario Augusto Ono.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, YH., Chi, MJ., Sun, PL. et al. Histopathology, Molecular Identification and Antifungal Susceptibility Testing of Nannizziopsis arthrosporioides from a Captive Cuban Rock Iguana (Cyclura nubila). Mycopathologia 185, 1005–1012 (2020). https://doi.org/10.1007/s11046-020-00481-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-020-00481-6

Keywords

Navigation