There is growing interest in breeding rheas (Rhea americana) 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 Candida species from the digestive tract of rheas and to evaluate the in vitro 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−1). 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 Candida species isolates was also tested by culturing on egg yolk agar. Candida 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 Candida parapsilosis sensu lato (19), Candida albicans (18), Candida tropicalis (13), Candida guilliermondii (12), Candida krusei (10) and Candida famata (5). C. albicans was more prevalent in the oropharynx of the juvenile rheas when compared with adult ones (P<0.001). All tested isolates were susceptible to amphotericin B, but 16 isolates were simultaneously resistant to the two azole derivatives (11/18 C. albicans, 1/10 C. krusei, 2/19 C. parapsilosis sensu lato and 2/13 C. tropicalis). C. albicans 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 Candida 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.
AzevedoC. S.,
FerrazJ. B.,
TinocoH. P.,
YoungR. J.,
RodriguesM.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 [View Article]
BrilhanteR. S. N.,
Castelo-BrancoD. S.,
SoaresG. D. P.,
Astete-MedranoD. J.,
MonteiroA. J.,
CordeiroR. A.,
SidrimJ. J. C.,
RochaM. 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 [View Article][PubMed]
BrilhanteR. S. N.,
PaivaM. A. N.,
SampaioC. M. S.,
TeixeiraC. E. C.,
Castelo-BrancoD. S. C. M.,
LeiteJ. J. G.,
MoreiraC. A.,
SilvaL. P.,
CordeiroR. A.other authors2011; Yeasts from Macrobrachium amazonicum: a focus on antifungal susceptibility and virulence factors of Candida spp. FEMS Microbiol Ecol 76:268–277 [View Article][PubMed]
BrilhanteR. S. N.,
Castelo-BrancoD. S. C. M.,
DuarteG. P. S.,
PaivaM. A. N.,
TeixeiraC. E. C.,
ZeferinoJ. P. O.,
MonteiroA. J.,
CordeiroR. A.,
SidrimJ. J. C.,
RochaM. F. G.2012; Yeast microbiota of raptors: a possible tool for environmental monitoring. Environ Microbiol Rep 4:189–193 [View Article]
BritoE. H. S.,
FontenelleR. O. S.,
BrilhanteR. S. N.,
CordeiroR. A.,
MonteiroA. J.,
SidrimJ. J. C.,
RochaM. F. G.2009; The anatomical distribution and antimicrobial susceptibility of yeast species isolated from healthy dogs. Vet J 182:320–326 [View Article][PubMed]
CafarchiaC.,
RomitoD.,
IattaR.,
CamardaA.,
MontagnaM. T.,
OtrantoD.2006a; Role of birds of prey as carriers and spreaders of Cryptococcus neoformans and other zoonotic yeasts. Med Mycol 44:485–492 [View Article][PubMed]
CafarchiaC.,
RomitoC.,
CoccioliC.,
CamardaA.,
OtrantoD.2008; Phospholipase activity of yeasts from wild birds and possible implications for human diseases. Med Mycol 46:1–6 [View Article][PubMed]
CostaA. K. F.,
SidrimJ. J. C.,
CordeiroR. A.,
BrilhanteR. S. N.,
MonteiroA. J.,
RochaM. 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 [View Article][PubMed]
EdelmannA.,
KrügerM.,
SchmidJ.2005; Genetic relationship between human and animal isolates of Candida albicans
. J Clin Microbiol 43:6164–6166 [View Article][PubMed]
Garcia-EffronG.,
CantonE.,
PemánJ.,
DilgerA.,
RomáE.,
PerlinD. 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 [View Article][PubMed]
GarnerC. D.,
StarrJ. K.,
McDonoughP. L.,
AltierC.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 [View Article][PubMed]
GonçalvesS. S.,
AmorimC. S.,
NucciM.,
PadovanA. C. B.,
BrionesM. R. S.,
MeloA. S. A.,
ColomboA. 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]
LordA. T. K.,
MohandasK.,
SomanathS.,
AmbuS.2010; Multidrug resistant yeasts in synanthropic wild birds. Ann Clin Microbiol Antimicrob 9:11 [View Article][PubMed]
ManciantiF.,
NardoniS.,
CeccherelliR.2002; Occurrence of yeasts in psittacines droppings from captive birds in Italy. Mycopathologia 153:121–124 [View Article][PubMed]
MelvilleP. A.,
CogliatiB.,
MangiaterraM. B. B. C. D.,
PeresM. R.,
MouraS. C. A.,
MatsudaL.,
KimA.,
BenitesN. R.2004; Determinação da microbiota presente na cloaca e orofaringe de avestruzes (Struthio camelus) clinicamente sadios. Ciência Rural 34:1871–1876 [View Article]
MüllerF. M. C.,
StaudigelA.,
SalvenmoserS.,
TredupA.,
MiltenbergerR.,
HerrmannJ. 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 [View Article][PubMed]
NawangeS. R.,
SinghK.,
NaiduJ.,
SinghS. 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 [View Article][PubMed]
OksuzS.,
SahinI.,
YildirimM.,
GulcanA.,
YavuzT.,
KayaD.,
KocA. 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]
OrtegaM.,
MarcoF.,
SorianoA.,
AlmelaM.,
MartínezJ. A.,
LópezJ.,
PitartC.,
MensaJ.2011; Candida species bloodstream infection: epidemiology and outcome in a single institution from 1991 to 2008. J Hosp Infect 77:157–161 [View Article][PubMed]
ParizziR. C.,
MiglinoM. A.,
MaiaM. O.,
SouzaJ. A.,
SantosJ. M.,
OliveiraM. F.,
SantosT. C.2007; Morfologia do ovário da ema (Rhea americana). Pesqui Vet Bras 27:89–94[CrossRef]
PfallerM. A.2012; Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am J Med 125:Suppl.S3–S13 [View Article][PubMed]
PfallerM. A.,
DiekemaD. J.2007; Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133–163 [View Article][PubMed]
ReissigE. C.,
UzalF. A.,
SchettinoA.,
RoblesC. A.2002; Pulmonary aspergillosis in a great rhea (Rhea americana). Avian Dis 46:754–756 [View Article][PubMed]
SidrimJ. J. C.,
MaiaD. C. B. S. C.,
BrilhanteR. S. N.,
SoaresG. D. P.,
CordeiroR. A.,
MonteiroA. J.,
RochaM. 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 [View Article][PubMed]
SoaresH. S.,
AlvesN. D.,
PereiraR. H. M. A.,
MatosS. M.,
PenaH. F. J.,
GennariS. M.,
FeijóF. M. C.,
AmóraS. S. A.,
PeixotoG. 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 [View Article]
TortoranoA. M.,
BiraghiE.,
AstolfiA.,
OssiC.,
TejadaM.,
FarinaC.,
PerinS.,
BonaccorsoC.,
CavannaC.other authors2002; European Confederation of Medical Mycology (ECMM) prospective survey of candidaemia: report from one Italian region. J Hosp Infect 51:297–304 [View Article][PubMed]
VieiraR. G.,
CoutinhoS. D. A.2009; Phenotypical characterization of Candida spp. isolated from crop of parrots (Amazona spp.). Pesqui Vet Bras 29:452–456[CrossRef]