Skip to main content

Advertisement

Log in

Evidence of Fluconazole-Resistant Candida Species in Tortoises and Sea Turtles

  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

The aim of this study was to evaluate the antifungal susceptibility of Candida spp. recovered from tortoises (Chelonoidis spp.) and sea turtles (Chelonia mydas, Caretta caretta, Lepidochelys olivacea, Eretmochelys imbricata). For this purpose, material from the oral cavity and cloaca of 77 animals (60 tortoises and 17 sea turtles) was collected. The collected specimens were seeded on 2 % Sabouraud dextrose agar with chloramphenicol, and the identification was carried out by morphological and biochemical methods. Sixty-six isolates were recovered from tortoises, out of which 27 were C. tropicalis, 27 C. famata, 7 C. albicans, 4 C. guilliermondii and 1 C. intermedia, whereas 12 strains were obtained from sea turtles, which were identified as Candida parapsilosis (n = 4), Candida guilliermondii (n = 4), Candida tropicalis (n = 2), Candida albicans (n = 1) and Candida intermedia (n = 1). The minimum inhibitory concentrations for amphotericin B, itraconazole and fluconazole ranged from 0.03125 to 0.5, 0.03125 to >16 and 0.125 to >64, respectively. Overall, 19 azole-resistant strains (14 C. tropicalis and 5 C. albicans) were found. Thus, this study shows that Testudines carry azole-resistant Candida spp.

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.

Similar content being viewed by others

References

  1. Harris JR, Neil KP, Behravesh CB, Sotir MJ, Angulo FJ. Recent multistate outbreaks of human Salmonella infections acquired from turtles: a continuing public health challenge. Clin Infect Dis. 2010;50:554–9.

    Article  PubMed  Google Scholar 

  2. Benites NR, Pessoa C, Bandini L, Saidenberg A, Moreno A, Sakata S, et al. Microbiota bacteriana e fúngica presentes na cloaca de jabutis-piranga (Geochelone carbonaria) criados em domicílio. Vet Zootec. 2013;20:102–10.

    Google Scholar 

  3. Warwick C, Arena PC, Steedman C. Health implications associated with exposure to farmed and wild sea turtles. JRSM Short Rep. 2013;4:8.

    Article  PubMed Central  PubMed  Google Scholar 

  4. Cafarchia C, Romito D, Iatta R, Camarda A, Montagna MT, Otranto D. Role of birds of prey as carriers and spreaders of Cryptococcus neoformans and other zoonotic yeasts. Med Mycol. 2006;44:485–92.

    Article  CAS  PubMed  Google Scholar 

  5. Cafarchia C, Romito D, Coccioli C, Camarda A, Otranto D. Phospholipase activity of yeasts from wild birds and possible implications for human disease. Med Mycol. 2008;46:429–34.

    Article  CAS  PubMed  Google Scholar 

  6. Brito EHS, Fontenelle ROS, Brilhante RSN, Cordeiro RA, Monteiro AJ, Sidrim JJC, et al. The anatomical distribution and antimicrobial susceptibility of yeast species isolated from healthy dogs. Vet J. 2009;182:320–6.

  7. Sidrim JJC, Castelo-Branco DSCM, Brilhante RSN, Soares GDP, Cordeiro RA, Monteiro AJ, et al. Candida species isolated from the gastrointestinal tract of cockatiels (Nymphicus hollandicus): in vitro antifungal susceptibility profile and phospholipase activity. Vet Microbiol. 2010;145:324–8.

  8. Brilhante RSN, de Alencar LP, Cordeiro RS, Castelo-Branco DSCM, Teixeira CEC, Macedo RDB, et al. Detection of Candida species resistant to azoles in the microbiota of rheas (Rhea americana): Possible implications for human and animal health. J Med Microbiol. 2013;62:889–95.

  9. Brilhante RSN, Paiva MAN, Sampaio CMS, Teixeira CEC, Castelo-Branco DSCM, Leite JJG, et al. Yeasts from Macrobrachium amazonicum: a focus on antifungal susceptibility and virulence factors of Candida spp. FEMS Microbiol Ecol. 2011;76:268–77.

  10. Cordeiro RA, Bittencourt PV, Brilhante RSN, Teixeira CEC, Castelo-Branco DSCM, Silva ST, et al. Species of Candida as a component of the nasal microbiota of healthy horses. Med Mycol. 2013;51:731–6.

  11. Brilhante RSN, Castelo-Branco DSCM, Soares GDP, Astete-Medrano DJ, Monteiro AJ, Cordeiro RA, et al. Characterization of the gastrointestinal yeast microbiota of cockatiels (Nymphicus hollandicus): a potential hazard to human health. J Med Microbiol. 2010;59:718–23.

  12. De Hoog G, Guarro J, Gené J, Figueras M. Atlas of clinical fungi. 2nd ed. Utrecht: Centraalbureau voor Schimmelcultures (CBS); 2000.

    Google Scholar 

  13. CLSI. Reference method for broth dilution antifungal susceptibility testing of yeasts: approved standard. CLSI Document M27-A3. Wayne: Clinical and Laboratory Standards Institute; 2008.

  14. CLSI. Reference method for broth dilution antifungal susceptibility testing of yeasts—fourth informational supplement. CLSI Document M27-S4. Wayne: Clinical and Laboratory Standards Institute; 2012.

  15. Juniantito V, Izawa T, Kuwamura M, Yonezawa M, Ito S, Yamate J. Gastrointestinal candidiasis in an Aldabra giant tortoise (Geochelone gigantea). J Vet Med Sci. 2009;71:1269–72.

    Article  PubMed  Google Scholar 

  16. Hernandez-Divers SJ. Pulmonary candidiasis caused by Candida albicans in a Greek tortoise (Testudo graeca) and treatment with intrapulmonary amphotericin B. J Zoo Wildl Med. 2001;32:352–9.

    Article  CAS  PubMed  Google Scholar 

  17. Vieira RG, Coutinho SDA. Phenotypical characterization of Candida spp. isolated from crop of parrots (Amazona spp.). Pesqui Vet Bras. 2009;29:452–6.

    Article  Google Scholar 

  18. Rodríguez-Galán MC, Sotomayor CE, Cano R, Porporatto C, Renna MS, Paraje MG, et al. Immune neuroendocrine interactions during a fungal infection in immunocompetent or immunosuppressed hosts. Neuroimmunomodulation. 2010;17:188–91.

    Article  PubMed  Google Scholar 

  19. Hernández E, Rodriguez JL, Herrera-León S, García I, de Castro V, Muniozguren N. Salmonella Paratyphi B var Java infections associated with exposure to turtles in Bizkaia, Spain, September 2010 to October 2011. Eurosurveillance. 2012;17:47–51.

    Google Scholar 

  20. Vogel C, Rogerson A, Schatz S, Laubach H, Tallman A, Fell J. Prevalence of yeasts in beach sand at three bathing beaches in South Florida. Water Res. 2007;41:1915–20.

    Article  CAS  PubMed  Google Scholar 

  21. Lord ATK, Mohandas K, Somanath S, Ambu S. Multidrug resistant yeasts in synanthropic wild birds. Ann Clin Microbiol Antimicrob. 2010;9:11.

    Article  PubMed Central  PubMed  Google Scholar 

  22. Yang Y-L, Lin C-C, Chang T-P, Lauderdale T-L, Chen H-T, Lee C-F, et al. Comparison of human and soil Candida tropicalis isolates with reduced susceptibility to fluconazole. PLoS One. 2012;7:e34609.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Ortega M, Marco F, Soriano A, Almela M, Martínez JA, López J, et al. Candida species bloodstream infection: Epidemiology and outcome in a single institution from 1991 to 2008. J Hosp Infect. 2011;77:157–61.

    Article  CAS  PubMed  Google Scholar 

  24. Bogusławska-Was E, Dabrowski W. The seasonal variability of yeasts and yeast-like organisms in water and bottom sediment of the Szczecin Lagoon. Int J Hyg Environ Health. 2001;203:451–8.

    Article  PubMed  Google Scholar 

  25. Brilhante RSN, Castelo Branco DSCM, Duarte GPS, Paiva MAN, Teixeira CEC, Zeferino JPO, et al. Yeast microbiota of raptors: a possible tool for environmental monitoring. Environ Microbiol Rep. 2012;4:189–93.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Grants from the National Council for Scientific and Technological Development (CNPq; Brazil; Processes 504189/2012-3; 307606/2013-9; 445670/2014-2).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raimunda Sâmia Nogueira Brilhante.

Ethics declarations

Conflict of interest

None to declare.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brilhante, R.S.N., de Aragão Rodrigues, P.H., de Alencar, L.P. et al. Evidence of Fluconazole-Resistant Candida Species in Tortoises and Sea Turtles. Mycopathologia 180, 421–426 (2015). https://doi.org/10.1007/s11046-015-9923-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-015-9923-0

Keywords

Navigation