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Antifungal Resistance and Virulence Among Candida spp. from Captive Amazonian manatees and West Indian Manatees: Potential Impacts on Animal and Environmental Health

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Abstract

This work aimed at evaluating the antifungal susceptibility and production of virulence factors by Candida spp. isolated from sirenians in Brazil. The isolates (n = 105) were recovered from the natural cavities of Amazonian and West Indian manatees and were tested for the susceptibility to amphotericin B, itraconazole, and fluconazole and for the production of phospholipases, proteases, and biofilm. The minimum inhibitory concentrations (MICs) for amphotericin B ranged from 0.03 to 1 µg/mL, and no resistant isolates were detected. Itraconazole and fluconazole MICs ranged from 0.03 to 16 µg/mL and from 0.125 to 64 µg/mL, respectively, and 35.2% (37/105) of the isolates were resistant to at least one of these azole drugs. Concerning the production of virulence factors, phospholipase activity was observed in 67.6% (71/105) of the isolates, while protease activity and biofilm production were detected in 50.5% (53/105) and 32.4% (34/105) of the isolates, respectively. Since the natural cavities of manatees are colonized by resistant and virulent strains of Candida spp., these animals can act as sources of resistance and virulence genes for the environment, conspecifics and other animal species, demonstrating the potential environmental impacts associated with their release back into their natural habitat.

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References

  • Arendrup MC (2013) Update on antifungal resistance in Aspergillus and Candida. Clinical Microbiology and Infection 20:42–48. DOI: 10.1111/1469-0691.12513

    Article  Google Scholar 

  • Arkush KD (2001) Water quality. In: Handbook of marine mammal medicine, Dierauf LA, Gulland FMD (editors), Boca Raton, FL: CRC Press, pp 779-790.

    Chapter  Google Scholar 

  • Attademo FLN (2014) Detecção da infecção de rotavírus, coronavírus, enterobactérias, Leptospira spp., Brucella abortus e Toxoplasma gondii em peixe-boi marinho (Trichechus manatus) em cativeiro no Brasil. PhD Thesis, Federal Rural University of Pernambuco, Recife, Brazil.

  • Ben-Ami R, Olshtain-Pops K, Krieger M, Oren I, Bishara J, Dan M et al. (2012) Antibiotic exposure as a risk factor for fluconazole-resistant Candida bloodstream infection. Antimicrobial Agents and Chemotherapy 56:2518–2523 DOI: 10.1128/AAC.05947-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berardi T, Shapiro K, Byrne BA, Miller W (2014) Prevalence and characterization of Salmonella shed by captive and free-range California sea lions (Zalophus californianus) from a rehabilitation center and three state reserves along the California coast. Journal of Zoo and Wildlife Medicine 45: 527-533; DOI: 10.1638/2013-0197R1.1

    Article  PubMed  Google Scholar 

  • Bonde RK, Aguirre AA, Powell J (2004) Manatees as Sentinels of Marine Ecosystem Health: Are They the 2000-pound Canaries? Ecohealth 1: 255-262; DOI: 10.1007/s10393-004-0095-5

    Article  Google Scholar 

  • Bonde RK, Garrett A, Belanger M, Askin N, Tan L, Wittnich C (2012). Biomedical health assessments of the Florida manatee in Crystal River-providing opportunities for training during the capture, handling, and processing of this endangered aquatic mammal. Journal of Marine Animal Ecology 5:17-28.

    Google Scholar 

  • Bossart GD (2001) Manatees. In: Handbook of marine mammal medicine, Dierauf LA, Gulland FMD (editors), Boca Raton, FL: CRC Press, pp 939−958.

    Chapter  Google Scholar 

  • Bossart GD (2010) Marine Mammals as Sentinel Species for Oceans and Human Health. Veterinary Pathology 48:676-690 DOI: 110.1177/0300985810388525

    Article  PubMed  Google Scholar 

  • Brownstein D, Miller MA, Oates SC, Byrne BA, Jang S, Murray MJ, Gill VA, Jessup DA (2011). Antimicrobial susceptibility of bacterial isolates from sea otters (Enhydra lutris). Journal of Wildlife Disease 47: 278-292.

    Article  Google Scholar 

  • Brilhante RS, Paiva MAN, Sampaio CMS, Teixeira CEC, Castelo-Branco DSCM, Leite JJG et al. (2011) Yeasts from Macrobrachium amazonicum: a focus on antifungal susceptibility and virulence factors of Candida spp. FEMS Microbiology Ecology 76: 268-277; DOI: 10.1111/j.1574-6941.2011.01050.x

    Article  CAS  PubMed  Google Scholar 

  • Brilhante RSN, Castelo-Branco, DSCM, Duarte GPS, Paiva MAN, Teixeira CEC, Zeferino JPO et al. (2012) Yeast microbiota of raptors: a possible tool for environmental monitoring. Environmental Microbiology Reports 1: 189-193; DOI: 10.1111/j.1758-2229.2011.00319.x

    Article  Google Scholar 

  • Brilhante RSN, Alencar LP, Cordeiro RA, Castelo Branco DSCM, Teixeira CEC, Macedo RB et al. (2013) Detection of Candida species resistant to azoles in the microbiota of rheas (Rhea americana): possible implications for human and animal health. Journal of Medical Microbiology 62:889–895; DOI: 10.1099/jmm.0.055566-0

    Article  CAS  PubMed  Google Scholar 

  • Brito EH, Fontenelle RO, Brilhante RS, Cordeiro RA, Monteiro AJ, Sidrim JJ, Rocha MF (2009) The anatomical distribution and antimicrobial susceptibility of yeast species isolated from healthy dogs. The Veterinary Journal 182: 320-326; DOI: 10.1016/j.tvjl.2008.07.001

    Article  CAS  PubMed  Google Scholar 

  • Carroll D, Wang J, Fanning S, McMahon BJ (2015) Antimicrobial resistance in wildlife: implications for public health. Zoonoses and Public Health 1–9 DOI: 10.1111/zph.12182

  • Castelo-Branco DSCM, Brilhante RSN, Paiva MAN, Teixeira CEC, Caetano EP, Ribeiro JF et al. (2013) Azole-resistant Candida albicans from a wild Brazilian porcupine (Coendou prehensilis): a sign of an environmental imbalance? Medical Mycology 51:555-560; DOI: 10.3109/13693786.2012.752878

    Article  CAS  PubMed  Google Scholar 

  • Cordeiro RA, Oliveira JS, Castelo Branco DSCM, Teixeira CEC, Marques FJF, Bittencourt PV et al. (2015) Candida tropicalis isolates obtained from veterinary sources show resistance to azoles and produce virulence factors. Medical Mycology 53: 145-152; DOI: 10.1093/mmy/myu081.

    Article  Google Scholar 

  • Clinical and Laboratory Standards Institute (2012) Reference method for broth dilution antifungal susceptibility testing of yeasts; 4th informational supplement. CLSI document M27-S4. Wayne, PA: Clinical and Laboratory Standards Institute.

  • D’Affonseca Neto JA, Vergara-Parente JE (2007) Sirenia (Peixe-boi Marinho e Amazônico). In: Tratado de Animais Selvagens, Cubas ZA, Silva JCR, Catão-Dias JL (editors). São Paulo, Brazil: Roca.

    Google Scholar 

  • Hower S, Phillips MC, Brodsky M, Dameron A, Tamargo MA, Salazar NC et al. (2013) Clonally related methicillin-resistant Staphylococcus aureus isolated from short-finned pilot whales (Globicephala macrorhynchus), human volunteers, and a bayfront cetacean rehabilitation facility. Microbial Ecology 65: 1024-1038; DOI: 10.1007/s00248-013-0178-3

    Article  CAS  PubMed  Google Scholar 

  • Hughes SN, Greig DJ, Miller WA, Byrne BA, Gulland FM, Harvey JT (2013) Dynamics of Vibrio with virulence genes detected in Pacific harbor seals (Phoca vitulina richardii) off California: implications for marine mammal health. Microbial Ecology 65: 982-994; DOI: 10.1007/s00248-013-0188-1.

    Article  PubMed  Google Scholar 

  • ICMBio (2011). Plano de ação nacional para a conservação dos sirênios: peixe-boi-da- Amazônia: Trichechus inunguis e peixe-boi-marinho: Trichechus manatus. Brasília, Brazil: Instituto Chico Mendes de Conservação da Biodiversidade.

    Google Scholar 

  • IUCN (2013). IUCN Red List of Threatened Species. Version 2013.2. www.iucnredlist.org. Accessed Apr 22, 2015

  • Junqueira JC, Vilela SF, Rossoni RD, Barbosa JO, Costa ACB, Rasteiro V et al. (2012). Oral colonization by yeasts in HIV-positive patients in Brazil. Revista do Instituto de Medicina Tropical de São Paulo 54: 17-24; DOI: 10.1590/S0036-46652012000100004

    Article  PubMed  Google Scholar 

  • Mariano V, McCrindle CM, Cenci-Goga B, Picard JA (2009) Case-control study to determine whether river water can spread tetracycline resistance to unexposed impala (Aepyceros melampus) in Kruger National Park (South Africa). Applied Environmental Microbiology 75: 113-118; DOI: 10.1128/AEM.01808-08

    Article  CAS  PubMed  Google Scholar 

  • Marsh H, O’Shea T, Reynolds JE (2011) Ecology and Conservation of the Sirenia: Dugongs and Manatees, 1st edn. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Müller FMC, Staudigel A, Salvenmoser S, Tredup A, Miltenberger R, Herrmann JV (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. Antimicrobial Agents and Chemotherapy 51: 3014-3016; DOI: 10.1128/AAC.00459-07

    Article  PubMed  PubMed Central  Google Scholar 

  • Peeters E, Nelis H J, Coenye T (2008) Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. Journal of Microbiological Methods 72: 157-165; DOI: 10.1016/j.mimet.2007.11.010

    Article  CAS  PubMed  Google Scholar 

  • Potter SL (2013) Antimicrobial Resistance in Orcinus orca Scat: Using Marine Sentinels as Indicators of Pharmaceutical Pollution in the Salish Sea. Masters Dissertation, The Evergreen State College, Olympia, United States.

  • Radhouani H, Silva N, Poeta P, Torres C, Correia S, Igrejas G (2014). Potential impact of antimicrobial resistance in wildlife, environment and human health. Frontiers in Microbiology 5; DOI: 10.3389/fmicb.2014.00023

    Article  Google Scholar 

  • Rajendran R, Sherry L, Nile CJ, Sherriff A, Johnson E, Hanson M, Williams C, Munro C, Jones B, Ramage G (2015) Biofilm formation is a risk factor for mortality in patients with Candida albicans bloodstream infection—Scotland, 2012–2013. Clinical Microbiology and Infection (DOI: 10.1016/j.cmi.2015.09.018)

  • Ramos LS, Barbedo LS, Braga-Silva LA, Santos ALS, Pinto MRP, Sgarb DBG. (2015) Protease and phospholipase activities of Candida spp. isolated from cutaneous candidiasis. Revista Iberoamericana de Micologia 32: 122-125; DOI: 10.1016/j.riam.2014.01.003

    Article  Google Scholar 

  • Ravi S, Pierce C, Witt C, Wormley Jr FL (2009) Biofilm formation by Cryptococcus neoformans under distinct environmental conditions. Mycopathologia 167: 307-314; DOI: 10.1007/s11046-008-9180-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Rose JM, Gast RJ, Bogomolni A, Ellis JC, Lentell BJ, Touhey K, Moore M (2009) Occurrence and patterns of antibiotic resistance in vertebrates off the Northeastern United States coast. FEMS Microbiology Ecology 67:421-431; DOI: 10.1111/j.1574-6941.2009.00648.x

    Article  CAS  PubMed  Google Scholar 

  • Sarkar S, Uppuluri P, Pierce CG, Lopez-Ribot JL (2014). In vitro study of sequential fluconazole and caspofungin treatment against Candida albicans biofilms. Antimicrobial Agents and Chemotherapy 58:1183–1186; DOI: 10.1128/AAC.01745-13

    Article  PubMed  PubMed Central  Google Scholar 

  • Sidrim JJC, Castelo-Branco DCSM, Brilhante RSN, Soares GDP, Cordeiro RA, Monteiro AJ, Rocha MFG (2010) Candida species isolated from the gastrointestinal tract of cockatiels (Nymphicus hollandicus): In vitro antifungal susceptibility profile and phospholipase activity. Veterinary Microbiology 145: 324-328; DOI: 10.1016/j.vetmic.2010.04.006

    Article  CAS  PubMed  Google Scholar 

  • Schaefer AM, Goldstein JD, Reif JS, Fair PA, Bossart GD (2009) Antibiotic-resistant organisms cultured from Atlantic bottlenose dolphins (Tursiops truncatus) inhabiting estuarine waters of Charleston, SC and Indian River Lagoon, FL. Ecohealth 6: 33-41; DOI: 10.1007/s10393-009-0221-5

    Article  PubMed  Google Scholar 

  • Sidrim JJC, Carvalho VL, Castelo-Branco DSCM, Brilhante RSN, Bandeira TJPG, Cordeiro RA, Guedes GMM, Barbosa GR, Lazzarini SM, Oliveira DC, Meirelles AC, Attademo FL, Freire AC, Moreira JLB, Monteiro AJ, Rocha MFG (2015) Yeast microbiota of natural cavities of manatees (Trichechus inunguis and Trichechus manatus) in Brazil and its relevance for animal health and management in captivity. Canadian Journal of Microbiology 61: 763-769; DOI: 10.1139/cjm-2015-0341

    Article  CAS  PubMed  Google Scholar 

  • Skurnik D, Ruimy R, Andremont A, Amorin C, Rouquet P, Picard B et al. (2006) Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. Journal of Antimicrobial Chemotherapy 57: 1215–1219; DOI: 10.1093/jac/dkl122

    Article  CAS  PubMed  Google Scholar 

  • Skurnik D, Bonnet D, Bernede-Bauduin C, Michel R, Guette C, Becker JM et al. (2008) Characteristics of human intestinal Escherichia coli with changing environments. Environmental Microbiology 10: 2132–2137; DOI:10.1111/j.1462-2920.2008.01636.x [Online May, 4, 2008]

    Article  PubMed  Google Scholar 

  • Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M (2000) A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods 40: 175–179. doi:10.1016/S0167-7012(00)00122-6

    Article  PubMed  Google Scholar 

  • Takahashi H, Ueda K, Itano EN, Yanagisawa M, Murata Y, Murata M et al. (2010). Candida albicans and C. tropicalis isolates from the expired breathes of captive dolphins and their environments in an aquarium. Veterinary Medicine International 2010: 1-12; DOI: 10.4061/2010/349364

    Article  Google Scholar 

  • Tenaillon O, Skurnik D, Picard B, Denamur E (2010) The population genetics of commensal Escherichia coli. Nature Reviews Microbiology 8: 207–217; DOI: 10.1038/nrmicro2298

    Article  CAS  PubMed  Google Scholar 

  • Vergara-Parente JE, Sidrim JJC, Pessoa APBGP, Parente CL, Marcondes MCC, Teixeira MFS, Rocha MFG (2003) Bacterial flora of upper respiratory tract of captive Antillean manatees. Aquatic Mammals 29: 124–130

    Article  Google Scholar 

  • Vidotto V, Pontón J, Aoki S, Quindós G, Mantoan B, Pugliese, A et al. (2004) Differences in extracellular enzymatic activity between Candida dubliniensis and Candida albicans isolates. Revista Iberoamericana de Micología 21: 70-74.

    PubMed  Google Scholar 

  • Wallace CC, Yund PO, Ford TE, Matassa KA, Bass AL (2013). Increase in antimicrobial resistance in bacteria isolated from stranded marine mammals of the Northwest Atlantic. EcoHealth 10:201–210 DOI: 10.1007/s10393-013-0842-6

    Article  PubMed  Google Scholar 

  • Wrobel L, Whittington JK, Pujol C, Oh SH, Ruiz MO, Pfaller MA, Diekema DJ, Soll DR, Hoyer LL (2008) Molecular phylogenetic analysis of a geographically and temporally matched set of Candida albicans isolates from humans and nonmigratory wildlife in central Illinois. Eukaryotic Cell 7: 1475-1486; DOI: 10.1128/EC.00162-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgement

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; 474563/2013-8; 307606/2013-9; 443167/2014-1) and by the Cordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). The rehabilitation of Antillean manatees at AQUASIS is performed by Projeto Manati, sponsored by Petrobras.

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Authors and Affiliations

  1. Centro Especializado em Micologia Médica (CEMM), Universidade Federal do Ceará (UFC), Rua Coronel Nunes de Melo, 1315, Rodolfo Teófilo, Fortaleza, Ceará, 60430-27, Brazil

    José Júlio Costa Sidrim, Vitor Luz Carvalho, Débora de Souza Collares Maia Castelo-Branco, Raimunda Sâmia Nogueira Brilhante, Gláucia Morgana de Melo Guedes, Giovanna Riello Barbosa, Rossana de Aguiar Cordeiro, José Luciano Bezerra Moreira & Marcos Fábio Gadelha Rocha

  2. Associação de Pesquisa e Preservação de Ecossistemas Aquáticos (AQUASIS), Caucaia, Ceará, Brazil

    Vitor Luz Carvalho & Ana Carolina Oliveira de Meirelles

  3. Centro de Preservação e Pesquisa de Mamíferos Aquáticos (CPPMA) da Eletrobras Amazonas Energia, Distrito de Balbina, Presidente Figueiredo, Amazonas, Brazil

    Stella Maris Lazzarini & Daniella Carvalho Ribeiro Oliveira

  4. Centro Nacional de Manejo, Conservação e Pesquisa de Mamíferos Aquáticos (CMA/ICMBio), Ilha de Itamaracá, Pernambuco, Brazil

    Fernanda Löffler Niemeyer Attademo & Augusto Carlos da Bôaviagem Freire

  5. Departamento de Engenharia de Transportes, Universidade Federal do Ceará (UFC), Fortaleza, Ceará, Brazil

    Waldemiro de Aquino Pereira-Neto

  6. Programa de Pós-Graduação em Ciências Veterinárias (PPGCV), Faculdade de Veterinária, Universidade Estadual do Ceará (UECE), Fortaleza, Ceará, Brazil

    Marcos Fábio Gadelha Rocha

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  1. José Júlio Costa Sidrim
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  2. Vitor Luz Carvalho
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  3. Débora de Souza Collares Maia Castelo-Branco
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Correspondence to Raimunda Sâmia Nogueira Brilhante.

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Sidrim, J.J.C., Carvalho, V.L., de Souza Collares Maia Castelo-Branco, D. et al. Antifungal Resistance and Virulence Among Candida spp. from Captive Amazonian manatees and West Indian Manatees: Potential Impacts on Animal and Environmental Health. EcoHealth 13, 328–338 (2016). https://doi.org/10.1007/s10393-015-1090-8

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