1887

Abstract

There is growing interest in breeding rheas () in Brazil. However, there are no data on the yeast microbiota of the gastrointestinal tract of this avian species, and the phenotypic characteristics of these yeasts are not known. Therefore, the aim of this work was to isolate species from the digestive tract of rheas and to evaluate the antifungal susceptibility and secretion of phospholipases of the recovered isolates. For this purpose, 58 rheas from breeding operations in the cities of Fortaleza and Mossoró, north-eastern Brazil, were used. Samples were gathered from the oropharynx and cloaca of the animals using sterile swabs. Stool samples were collected from their pens by scraping with a scalpel blade. For the primary isolation, the material was seeded onto 2 % Sabouraud dextrose agar supplemented with chloramphenicol (0.5 g l). The isolates were identified based on morphological and biochemical features. After identification, all the strains were submitted to antifungal susceptibility testing for amphotericin B, itraconazole and fluconazole. The phospholipase activity of the species isolates was also tested by culturing on egg yolk agar. species were isolated from at least one anatomical site in 36/58 birds (14/17 juveniles and 22/41 adults) and in 6/10 faecal samples. Mostly, only a single species was isolated from each collection site (36/56 positive sites), with up to three species being observed only in four cases (4/56). A total of 77 isolates were obtained, belonging to the species (19), (18), (13), (12), (10) and (5). was more prevalent in the oropharynx of the juvenile rheas when compared with adult ones (<0.001). All tested isolates were susceptible to amphotericin B, but 16 isolates were simultaneously resistant to the two azole derivatives (11/18 , 1/10 , 2/19 and 2/13 ). presented a particularly high resistance rate to fluconazole (15/18) and itraconazole (13/18). Finally, 23/77 strains secreted phospholipases. In summary, healthy rheas carry potentially pathogenic species in their gastrointestinal tract, including azole-resistant strains that secrete phospholipases, and are prone to disseminating them in the environment. Thus, breeding and handling these animals may have some implications for human and animal health.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.055566-0
2013-06-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/jmm/62/6/889.html?itemId=/content/journal/jmm/10.1099/jmm.0.055566-0&mimeType=html&fmt=ahah

References

  1. Azevedo C. S. , Ferraz J. B. , Tinoco H. P. , Young R. J. , Rodrigues M. . ( 2010; ). Time-activity budget of greater rheas (Rhea americana, Aves) on a human-disturbed area: the role of habitat, time of the day, season and group size. . Acta Ethol 13:, 109–117. [CrossRef]
    [Google Scholar]
  2. Brilhante R. S. N. , Castelo-Branco D. S. , Soares G. D. P. , Astete-Medrano D. J. , Monteiro A. J. , Cordeiro R. A. , Sidrim J. J. C. , Rocha M. F. G. . ( 2010; ). Characterization of the gastrointestinal yeast microbiota of cockatiels (Nymphicus hollandicus): a potential hazard to human health. . J Med Microbiol 59:, 718–723. [CrossRef] [PubMed]
    [Google Scholar]
  3. Brilhante R. S. N. , Paiva M. A. N. , Sampaio C. M. S. , Teixeira C. E. C. , Castelo-Branco D. S. C. M. , Leite J. J. G. , Moreira C. A. , Silva L. P. , Cordeiro R. A. . & other authors ( 2011; ). Yeasts from Macrobrachium amazonicum: a focus on antifungal susceptibility and virulence factors of Candida spp. . FEMS Microbiol Ecol 76:, 268–277. [CrossRef] [PubMed]
    [Google Scholar]
  4. Brilhante R. S. N. , Castelo-Branco D. S. C. M. , Duarte G. P. S. , Paiva M. A. N. , Teixeira C. E. C. , Zeferino J. P. O. , Monteiro A. J. , Cordeiro R. A. , Sidrim J. J. C. , Rocha M. F. G. . ( 2012; ). Yeast microbiota of raptors: a possible tool for environmental monitoring. . Environ Microbiol Rep 4:, 189–193. [CrossRef]
    [Google Scholar]
  5. Brito E. H. S. , Fontenelle R. O. S. , Brilhante R. S. N. , Cordeiro R. A. , Monteiro A. J. , Sidrim J. J. C. , Rocha M. F. G. . ( 2009; ). The anatomical distribution and antimicrobial susceptibility of yeast species isolated from healthy dogs. . Vet J 182:, 320–326. [CrossRef] [PubMed]
    [Google Scholar]
  6. Cafarchia C. , Romito D. , Iatta R. , Camarda A. , Montagna M. T. , Otranto D. . ( 2006a; ). Role of birds of prey as carriers and spreaders of Cryptococcus neoformans and other zoonotic yeasts. . Med Mycol 44:, 485–492. [CrossRef] [PubMed]
    [Google Scholar]
  7. Cafarchia C. , Camarda A. , Romito D. , Campolo M. , Quaglia N. C. , Tullio D. , Otranto D. . ( 2006b; ). Occurrence of yeasts in cloacae of migratory birds. . Mycopathologia 161:, 229–234. [CrossRef] [PubMed]
    [Google Scholar]
  8. Cafarchia C. , Romito C. , Coccioli C. , Camarda A. , Otranto D. . ( 2008; ). Phospholipase activity of yeasts from wild birds and possible implications for human diseases. . Med Mycol 46:, 1–6. [CrossRef] [PubMed]
    [Google Scholar]
  9. CLSI ( 2008; ). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard M27-A3, 3rd edn.. , Wayne, PA:: Clinical and Laboratory Standards Institute;.
  10. Copetti M. V. , Segabinazi S. D. , Flores M. L. , Alves S. H. , Santurio J. M. . ( 2004; ). Pulmonary aspergillosis outbreak in Rhea americana in southern Brazil. . Mycopathologia 157:, 269–271. [CrossRef] [PubMed]
    [Google Scholar]
  11. Costa A. K. F. , Sidrim J. J. C. , Cordeiro R. A. , Brilhante R. S. N. , Monteiro A. J. , Rocha M. F. G. . ( 2010; ). Urban pigeons (Columba livia) as a potential source of pathogenic yeasts: a focus on antifungal susceptibility of Cryptococcus strains in Northeast Brazil. . Mycopathologia 169:, 207–213. [CrossRef] [PubMed]
    [Google Scholar]
  12. De Hoog G. S. , Guarro J. , Gené J. , Figueiras M. J. . ( 2000; ). Atlas of Clinical Fungi. Utrecht:: Centraalbureau voor Schimmslcultures;.
    [Google Scholar]
  13. Deem S. L. . ( 2003; ). Fungal diseases of birds of prey. . Vet Clin North Am Exot Anim Pract 6:, 363–376. [CrossRef] [PubMed]
    [Google Scholar]
  14. Desnos-Ollivier M. , Ragon M. , Robert V. , Raoux D. , Gantier J. C. , Dromer F. . ( 2008; ). Debaryomyces hansenii (Candida famata), a rare human fungal pathogen often misidentified as Pichia guilliermondii (Candida guilliermondii). . J Clin Microbiol 46:, 3237–3242. [CrossRef] [PubMed]
    [Google Scholar]
  15. Edelmann A. , Krüger M. , Schmid J. . ( 2005; ). Genetic relationship between human and animal isolates of Candida albicans . . J Clin Microbiol 43:, 6164–6166. [CrossRef] [PubMed]
    [Google Scholar]
  16. Garcia-Effron G. , Canton E. , Pemán J. , Dilger A. , Romá E. , Perlin D. S. . ( 2012; ). Epidemiology and echinocandin susceptibility of Candida parapsilosis sensu lato species isolated from bloodstream infections at a Spanish university hospital. . J Antimicrob Chemother 67:, 2739–2748. [CrossRef] [PubMed]
    [Google Scholar]
  17. Garner C. D. , Starr J. K. , McDonough P. L. , Altier C. . ( 2010; ). Molecular identification of veterinary yeast isolates by use of sequence-based analysis of the D1/D2 region of the large ribosomal subunit. . J Clin Microbiol 48:, 2140–2146. [CrossRef] [PubMed]
    [Google Scholar]
  18. Gonçalves S. S. , Amorim C. S. , Nucci M. , Padovan A. C. B. , Briones M. R. S. , Melo A. S. A. , Colombo A. L. . ( 2010; ). Prevalence rates and antifungal susceptibility profiles of the Candida parapsilosis species complex: results from a nationwide surveillance of candidaemia in Brazil. . Clin Microbiol Infect 16:, 885–887.[PubMed] [CrossRef]
    [Google Scholar]
  19. IUCN (2012). Bird Life international 2012. Rhea americana. IUCN Red List of Threatened Species, version 2012.2. http://www.iucnredlist.org
  20. Kanafani Z. A. , Perfect J. R. . ( 2008; ). Antimicrobial resistance: resistance to antifungal agents: mechanisms and clinical impact. . Clin Infect Dis 46:, 120–128. [CrossRef] [PubMed]
    [Google Scholar]
  21. Lass-Flörl C. . ( 2009; ). The changing face of epidemiology of invasive fungal disease in Europe. . Mycoses 52:, 197–205. [CrossRef] [PubMed]
    [Google Scholar]
  22. Lord A. T. K. , Mohandas K. , Somanath S. , Ambu S. . ( 2010; ). Multidrug resistant yeasts in synanthropic wild birds. . Ann Clin Microbiol Antimicrob 9:, 11. [CrossRef] [PubMed]
    [Google Scholar]
  23. Mancianti F. , Nardoni S. , Ceccherelli R. . ( 2002; ). Occurrence of yeasts in psittacines droppings from captive birds in Italy. . Mycopathologia 153:, 121–124. [CrossRef] [PubMed]
    [Google Scholar]
  24. Melville P. A. , Cogliati B. , Mangiaterra M. B. B. C. D. , Peres M. R. , Moura S. C. A. , Matsuda L. , Kim A. , Benites N. R. . ( 2004; ). Determinação da microbiota presente na cloaca e orofaringe de avestruzes (Struthio camelus) clinicamente sadios. . Ciência Rural 34:, 1871–1876. [CrossRef]
    [Google Scholar]
  25. Müller F. M. C. , Staudigel A. , Salvenmoser S. , Tredup A. , Miltenberger R. , Herrmann J. V. . ( 2007; ). Cross-resistance to medical and agricultural azole drugs in yeasts from the oropharynx of human immunodeficiency virus patients and from environmental Bavarian vine grapes. . Antimicrob Agents Chemother 51:, 3014–3016. [CrossRef] [PubMed]
    [Google Scholar]
  26. Nawange S. R. , Singh K. , Naidu J. , Singh S. M. . ( 2010; ). Naturally acquired systemic dual infection caused by Candida famata (Debaryomyces hansenii) and Candida catenulata in albino rats bred for sale in the market at Jabalpur (Madhya Pradesh), India. . Mycoses 53:, 173–175. [CrossRef] [PubMed]
    [Google Scholar]
  27. Oksuz S. , Sahin I. , Yildirim M. , Gulcan A. , Yavuz T. , Kaya D. , Koc A. N. . ( 2007; ). Phospholipase and proteinase activities in different Candida species isolated from anatomically distinct sites of healthy adults. . Jpn J Infect Dis 60:, 280–283.[PubMed]
    [Google Scholar]
  28. Ortega M. , Marco F. , Soriano A. , Almela M. , Martínez J. A. , López J. , Pitart C. , Mensa J. . ( 2011; ). Candida species bloodstream infection: epidemiology and outcome in a single institution from 1991 to 2008. . J Hosp Infect 77:, 157–161. [CrossRef] [PubMed]
    [Google Scholar]
  29. Parizzi R. C. , Miglino M. A. , Maia M. O. , Souza J. A. , Santos J. M. , Oliveira M. F. , Santos T. C. . ( 2007; ). Morfologia do ovário da ema (Rhea americana). . Pesqui Vet Bras 27:, 89–94.[CrossRef]
    [Google Scholar]
  30. Pfaller M. A. . ( 2012; ). Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. . Am J Med 125: (Suppl.), S3–S13. [CrossRef] [PubMed]
    [Google Scholar]
  31. Pfaller M. A. , Diekema D. J. . ( 2007; ). Epidemiology of invasive candidiasis: a persistent public health problem. . Clin Microbiol Rev 20:, 133–163. [CrossRef] [PubMed]
    [Google Scholar]
  32. Pfaller M. A. , Diekema D. J. , Mendez M. , Kibbler C. , Erzsebet P. , Chang S.-C. , Gibbs D. L. , Newell V. A. . Global Antifungal Surveillance Group ( 2006; ). Candida guilliermondii, an opportunistic fungal pathogen with decreased susceptibility to fluconazole: geographic and temporal trends from the ARTEMIS DISK antifungal surveillance program. . J Clin Microbiol 44:, 3551–3556. [CrossRef] [PubMed]
    [Google Scholar]
  33. Reissig E. C. , Uzal F. A. , Schettino A. , Robles C. A. . ( 2002; ). Pulmonary aspergillosis in a great rhea (Rhea americana). . Avian Dis 46:, 754–756. [CrossRef] [PubMed]
    [Google Scholar]
  34. Rodríguez-Galán M. C. , Sotomayor C. E. , Cano R. , Porporatto C. , Renna M. S. , Paraje M. G. , Cejas H. , Correa S. G. . ( 2010; ). Immune neuroendocrine interactions during a fungal infection in immunocompetent or immunosuppressed hosts. . Neuroimmunomodulation 17:, 188–191. [CrossRef] [PubMed]
    [Google Scholar]
  35. Sidrim J. J. C. , Maia D. C. B. S. C. , Brilhante R. S. N. , Soares G. D. P. , Cordeiro R. A. , Monteiro A. J. , Rocha M. F. G. . ( 2010; ). Candida species isolated from the gastrointestinal tract of cockatiels (Nymphicus hollandicus): in vitro antifungal susceptibility profile and phospholipase activity. . Vet Microbiol 145:, 324–328. [CrossRef] [PubMed]
    [Google Scholar]
  36. Soares H. S. , Alves N. D. , Pereira R. H. M. A. , Matos S. M. , Pena H. F. J. , Gennari S. M. , Feijó F. M. C. , Amóra S. S. A. , Peixoto G. C. X. . ( 2010; ). Ocorrência de anticorpos anti-Toxoplasma gondii em emas (Rhea americana) do Centro de Multiplicação de Animais Silvestres de Mossoró, Rio Grande do Norte. . Arq Bras Med Vet Zootec 62:, 489–491. [CrossRef]
    [Google Scholar]
  37. Tortorano A. M. , Biraghi E. , Astolfi A. , Ossi C. , Tejada M. , Farina C. , Perin S. , Bonaccorso C. , Cavanna C. . & other authors ( 2002; ). European Confederation of Medical Mycology (ECMM) prospective survey of candidaemia: report from one Italian region. . J Hosp Infect 51:, 297–304. [CrossRef] [PubMed]
    [Google Scholar]
  38. Trofa D. , Gácser A. , Nosanchuk J. D. . ( 2008; ). Candida parapsilosis, an emerging fungal pathogen. . Clin Microbiol Rev 21:, 606–625. [CrossRef] [PubMed]
    [Google Scholar]
  39. Vieira R. G. , Coutinho S. D. A. . ( 2009; ). Phenotypical characterization of Candida spp. isolated from crop of parrots (Amazona spp.). . Pesqui Vet Bras 29:, 452–456.[CrossRef]
    [Google Scholar]
  40. Ying S. , Chunyang L. . ( 2012; ). Correlation between phospholipase of Candida albicans and resistance to fluconazole. . Mycoses 55:, 50–55. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.055566-0
Loading
/content/journal/jmm/10.1099/jmm.0.055566-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error