دورية أكاديمية
أعرض في EDS

CHARACTERIZATION OF THE FUNGAL MICROBIOTA IN THE NOSTRILS AND RECTUM OF AMAZONIAN MANATEES ( TRICHECHUS INUNGUIS ) FROM A REHABILITATION PROGRAM IN BRAZIL.

التفاصيل البيبلوغرافية
العنوان: CHARACTERIZATION OF THE FUNGAL MICROBIOTA IN THE NOSTRILS AND RECTUM OF AMAZONIAN MANATEES ( TRICHECHUS INUNGUIS ) FROM A REHABILITATION PROGRAM IN BRAZIL.
المؤلفون: Colombo SA; Department of Preventive Veterinary Medicine, School of Veterinary Medicine, Federal University of Minas Gerais, Belo Horizonte, MG 31270-901, Brazil., de Mello DMD; Laboratory of Aquatic Mammals, National Institute of Amazonian Research-INPA, Manaus, AM 69060-001, Brazil., Morais BRM; Department of Preventive Veterinary Medicine, School of Veterinary Medicine, Federal University of Minas Gerais, Belo Horizonte, MG 31270-901, Brazil., Salvato LA; Department of Preventive Veterinary Medicine, School of Veterinary Medicine, Federal University of Minas Gerais, Belo Horizonte, MG 31270-901, Brazil., Dorella FA; Department of Preventive Veterinary Medicine, School of Veterinary Medicine, Federal University of Minas Gerais, Belo Horizonte, MG 31270-901, Brazil., Tavares GC; Department of Preventive Veterinary Medicine, School of Veterinary Medicine, Federal University of Minas Gerais, Belo Horizonte, MG 31270-901, Brazil., da Silva VMF; Laboratory of Aquatic Mammals, National Institute of Amazonian Research-INPA, Manaus, AM 69060-001, Brazil., de Azevedo MI; Department of Preventive Veterinary Medicine, School of Veterinary Medicine, Federal University of Minas Gerais, Belo Horizonte, MG 31270-901, Brazil, beelazevedo@gmail.com.
المصدر: Journal of zoo and wildlife medicine : official publication of the American Association of Zoo Veterinarians [J Zoo Wildl Med] 2024 Mar; Vol. 55 (1), pp. 125-135.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: American Association Of Zoo Veterinarians Country of Publication: United States NLM ID: 8915208 Publication Model: Print Cited Medium: Internet ISSN: 1042-7260 (Print) Linking ISSN: 10427260 NLM ISO Abbreviation: J Zoo Wildl Med Subsets: MEDLINE
أسماء مطبوعة: Publication: Lawrence Ks : American Association Of Zoo Veterinarians
Original Publication: Lawrence, Kan. : The Association, [1989-
مواضيع طبية MeSH: Trichechus inunguis* , Mycobiome*, Animals ; Cattle ; Antifungal Agents/pharmacology ; Brazil/epidemiology ; Rectum ; Nasal Cavity ; Saccharomyces cerevisiae ; Trichechus ; Fungi
مستخلص: The present study characterized the filamentous and yeast-like fungal microbiota of the nasal cavity and rectum of Amazonian manatees ( Trichechus inunguis ) undergoing rehabilitation at the Laboratory of Aquatic Mammals, National Institute of Amazonian Research, Manaus, Amazonas, and determined the antifungal susceptibility of these organisms. Nasal and rectal swabs were collected from 22 calves and three juveniles. The samples were seeded in Sabouraud agar supplemented with chloramphenicol 10%, incubated at 26°C, and observed daily for up to 7 d. The growth of different filamentous and yeast-like fungi was observed among the two anatomical sites. Filamentous fungi were categorized by macro- and microscopic characteristics of the colonies. Representatives of each group were selected for molecular identification based on the internal transcribed spacer region. Yeast identification was performed using MALDI-TOF MS and molecular analyses. Thirteen genera of filamentous fungi and six genera of yeasts were isolated and identified. The dominant filamentous species were Fusarium spp., Aspergillus spp., and Cochliobolus lunatus in the nostril samples and Aspergillus melleus in the rectal samples. Candida was the dominant genus among the identified yeasts at both anatomical sites. In the antifungal susceptibility test, 28 isolates showed resistance to fluconazole (78%), itraconazole (39%), and nystatin (42%). The knowledge of fungal microbiota composition of Amazonian manatees provides information that assists in monitoring the health status of individuals maintained in captivity, as these organisms can behave either as opportunists or as primary pathogens. Moreover, the composition and resistance of these organisms may vary among different rehabilitation institutions or different time frames of search, reinforcing the importance of constant in loco surveillance of these microorganisms. This study provides new perspectives on the fungal diversity in the microbiota of manatees and supports future studies concerning the clinical and epidemiological aspects and the impacts of these agents on the health of Amazonian manatees undergoing rehabilitation.
References: Abramson D, Mills JT, Marquardt RR, Frohlich AA. Mycotoxins in fungal contaminated samples of animal feed from western Canada, 1982–1994. Can J Vet Res. 1997;61(1):49–52.
Adeyeye AOS. Aflatoxigenic fungi and mycotoxins in food: a review. Crit Rev Food Sci Nutr. 2020;60(5): 709–721.
Adimey N, Mignucci-Giannoni AA, Auil-Gomez NE, da Silva VMF, de Carvalho Alvite CM, Morales-Vela B, de Lima RP, Rosas FCW. Manatee rescue, rehabilitation, and release efforts as a tool for species conservation. Sirenian conservation. In: Hines EM, Reynolds JE, Aragones L V, Mignucci-Giannoni AA, Marmontel M (eds.). Sirenian conservation: issues and strategies in developing countries. Gainesville (FL): Univ. Press of Florida; 2012. p. 204–218.
Alvarez-Perez S, Mateos A, Dominguez L, Martinez-Nevado E, Blanco JL, Garcia ME. Isolation of Rhodotorula mucilaginosa from skin lesions in a Southern sea lion ( Otaria fl avescens ): a case report. Vet Med (Praha). 2010;55(6): 297–301.
Amaral RS, da Silva VMF, Iazzarini SM, JA DAffonsêca Neto, Ribeiro D, Rosas FCW. Assessment of sexual maturity in captive Amazonian manatees ( Trichechus inunguis ). Mar Mamm Sci. 2018;34(1): 190–199.
Antwis RE, Edwards KL, Unwin B, Walker SL, Shultz S. Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino. Microbiome. 2019;7(1):1–12.
Aruo SK. Necrotizing cutaneous rhodotorulosis in chickens in Uganda. Avian Dis. 1980;24(4):1038–1043.
Attademo FLN, Oliveira REM de, De Sousa GP, Luna FO. Infectious and non-infectious diseases in manatees in Brazil. Acta Sci Vet. 2020;48:1–12.
Bahrndorff S, Alemu T, Alemneh T, Lund Nielsen J. The microbiome of animals: implications for conservation biology. Int J Genomics. 2016;5304028. doi:10.1155/2016/5304028.
Balashov SV., Gardiner R, Park S, Perlin DS. Rapid, high-throughput, multiplex, real-time PCR for identification of mutations in the cyp51a gene of Aspergillus fumigatus that confer resistance to itraconazole. J Clin Microbiol. 2005;43(1):214–222.
Ball RL, Malmi M, Zgibor J. Trends of the Florida manatee ( Trichechus manatus latirostris ) rehabilitation admissions 1991–2017. PLoS One. 2020;15(7): 1–11.
Barkai-Golan R. Species of Penicillium causing decay of stored fruits and vegetables in Israel. Mycopathol Mycol Appl. 1974;54(1):141–145.
Berkow EL, Lockhart SR, Ostrosky-Zeichner L. Antifungal susceptibility testing: current approaches. Clin Microbiol Rev. 2020;33(3). doi:10.1128/CMR.00069-19.
Brum S, Rosas-Ribeiro P, Amaral R de S, de Souza DA, Castello L, da Silva VMF. Conservation of Amazonian aquatic mammals. Aquat Conserv. 2021; 31(5):1068–1086.
Cassle SE, Landrau-Giovannetti N, Farina LL, Leone A, Wellehan JFX, Stacy NI, Thompson P, Herring H, Mase-Guthrie B, Blas-Machado U, Saliki JT, Walsh MT, Waltzek TB. Coinfection by Cetacean morbillivirus and Aspergillus fumigatus in a juvenile bottlenose dolphin ( Tursiops truncatus ) in the Gulf of Mexico. J Vet Diagn Invest. 2016;28(6):729–734.
Castello L, Macedo MN. Large-scale degradation of Amazonian freshwater ecosystems. Glob Chang Biol. 2016;22(3):990–1007.
Cheng Y, Fox S, Pemberton D, Hogg C, Papenfuss AT, Belov K. The Tasmanian devil microbiome—implications for conservation and management. Microbiome. 2015;3:76. doi:10.1186/s40168-015-0143-0.
Clinical and Laboratory Standards Institute (CLSI). Method for antifungal disk diffusion susceptibility testing of yeasts; approved guideline. CLSI document M44-A2. Wayne (PA): Clinical and Laboratory Standards Institute; 2009.
Cordeiro RA, Oliveira JS, Castelo-Branco DSCM, Teixeira CEC, Marques FJF, Bittencourt PV, Carvalho VL, Bandeira TJPG, Brilhante RSN, Moreira JLB, Pereira-Neto WA, Sidrim JJC, Rocha MFG. Candida tropicalis isolates obtained from veterinary sources show resistance to azoles and produce virulence factors. Med Mycol. 2015;53(2):145–152.
Dargatz DA, Erdman MM, Harris B. A survey of methods used for antimicrobial susceptibility testing in veterinary diagnostic laboratories in the United States. J Vet Diagn Invest. 2017;29(5):669–675.
da Silva VMF, de Souza DA, d'Affonsêca Neto JA, Amaral R de S, Romero R. Mamíferos aquáticos da Amazônia—aquatic mammals of the Amazon. 1st ed. Manaus (Brazil): Editora INPA; 2019.
Delta D, da Silva V, Amaral R, Kikuchi M, JA d'Affonseca Neto, Rosas F. Amazonian manatees in Brazil. In: Soorae PS (ed.). Global reintroduction perspectives: 2018. Case studies from around the globe. IUCN, International Union for Conservation of Nature [Internet]. 2018. p. 187–192. https://portals.iucn.org/library/node/47668.
Diogo HC, Melhem M, Sarpieri A, Pires MC. Avaliação do método de disco-difusão para determinação da eficácia da terbinafina in vitro em agentes de micoses superficiais e subcutâneas [Evaluation of the disk-diffusion method to determine the in vitro efficacy of terbinafine against subcutaneous and superficial mycoses agents]. An Bras Dermatol [Braz An Dermatol]. 2010;85(3):324–330.
Enikova RK, Stoynovska MR, Karcheva MD. Mycotoxins in fruits and vegetables. J IMAB Annu Proc Sci Pap. 2020;26(2):3139–3143.
Feldhaar H. Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol. 2011;36(5):533–543.
Guo W, Mishra S, Wang C, Zhang H, Ning R, Kong F, Zeng B, Zhao J, Li Y. Comparative study of gut microbiota in wild and captive giant pandas ( Ailuropoda melanoleuca ). Genes (Basel). 2019;10(10):827.
Hagiwara D, Watanabe A, Kamei K, Goldman GH. Epidemiological and genomic landscape of azole resistance mechanisms in Aspergillus fungi. Front Microbiol. 2016;7:1382. doi:10.3389/fmicb.2016.01382.
Halvorsen KM, Keith EO. Immunosuppression cascade in the Florida manatee ( Trichechus manatus latirostris ). Aquat Mamm. 2008;34(4):412–419.
Hassan RM, Kadry Ismail D, Samy Elkholy Y. Comparison of E test and disc diffusion methods for susceptibility testing of filamentous fungi; experience of a routine lab. Arch Clin Infect Dis. 2018;13(3): e57889. doi:10.5812/archcid.57889.
Hesse SE, Luethy PM, Beigel JH, Zelazny AM. Penicillium citrinum : opportunistic pathogen or idle bystander? A case analysis with demonstration of galactomannan cross-reactivity. Med Mycol Case Rep. 2017;17:8–10.
Hurst CJ. Dirt and disease: the ecology of soil fungi and plant fungi that are infectious for vertebrates. In: Hurst CJ. (ed.). Understanding terrestrial microbial communities. Advances in environmental microbiology. Gewerbesraße (Austria): Cham Springer; 2019. p. 289–405. doi:10.1007/978-3-030-10777-2_9.
Ioannou P, Vamvoukaki R, Samonis G. Rhodotorula species infections in humans: a systematic review. Mycoses. 2019;62(0):90–100.
Kang HM, Han JI, Lee SJ, Jang HJ, Na KJ. Isolation of Pichia burtonii from the feces of an enteritis bearded dragon ( Pogona vitticeps ). J. Vet. Clin. 2011; 28(2):254–257.
Luna F de O, Miranda AV de, Sousa GP de, Florez JPT, Fruet PF, Attademo FLN. Protocolo Soltura e monitoramento de peixes-bois [Release and monitoring of manatees]. Brasília (Brazil): ICMBio; 2021. https://www.icmbio.gov.br/cma/images/stories/Publicações/copy_of_Protocolo_Soltura_e_Monitoramento_de_Peixes_boi_ICMBio_CMA_2708.pdf.
Maduro AHP, da Silva VMF, Oliveira RPM, Barbosa PS. Perfil metabólico de filhotes de peixe-boi da Amazônia ( Trichechus inunguis ) em cativeiro, alimentados com diferentes sucedâneos do leite materno [English translation of title]. Arq Bras Med Vet Zootec. 2020;72(5):1830–1838.
Marmontel M, Souza D, Kendall S. Trichechus inunguis , South American manatee. The IUCN Red List of Threatened Species. 2016:e.T22102A43793736. https://www.iucnredlist.org/species/22102/43793736.
McEwen SA, Collignon PJ. Antimicrobial resistance: a One Health perspective. Microbiol Spectr. 2018;6(2). doi:10.1128/microbiolspec.ARBA-0009-2017. PMID: 29600770.
Negri M, Henriques M, Svidzinski TIE, Paula CR, Oliveira R. Correlation between Etest w , disk diffusion, and microdilution methods for antifungal susceptibility testing of Candida species from infection and colonization. J Clin Lab Anal. 2009;23(5):324–330.
Nelson TM, Apprill A, Mann J, Rogers TL, Brown MV. The marine mammal microbiome: current knowledge and future directions. Microbiol Aust. 2015;36(1):8.
Nielsen KA, Owen HC, Mills PC, Flint M, Gibson JS. Bacteria isolated from dugongs ( Dugong dugon ) submitted for postmortem examination in Queensland, Australia, 2000–2011. J Zoo Wildl Med. 2013;44(1):35–41.
Normande IC, Luna FDO, Malhado ACM, Borges JCG, Viana Junior PC, Attademo FLN, Ladle RJ. Eighteen years of Antillean manatee Trichechus manatus manatus releases in Brazil: lessons learnt. Oryx. 2015;49(2):338–344.
Ohno Y, Akune Y, Inoshima Y, Kano R. First isolation of voriconazole-resistant Candida albicans , C. tropicalis , and Aspergillus niger from the blowholes of bottlenose dolphins ( Tursiops truncatus ). J Vet Med Sci. 2019;81(11):1628–1631.
Ozkutuk A, Ergon C, Metin DY, Yucesoy M, Polat SH. Comparison of disk diffusion, E-test and broth microdilution test in determination of susceptibility of Aspergillus species to amphotericin B, itraconazole and voriconazole. J Chemother. 2008;20(1):87–92.
Park S, Kelly R, Kahn JN, Robles J, Hsu M-J, Register E, Li W, Vyas V, Fan H, Abruzzo G, Flattery A, Gill C, Chrebet G, Parent SA, Kurtz M, Teppler H, Douglas CM, Perlin DS. Specific substitutions in the echinocandin target FKS1P account for reduced susceptibility of rare laboratory and clinical Candida sp. isolates. Antimicrob Agents Chemother. 2005;49(8): 3264–3273.
Pereira GMP, Bahniuk G, Batista KZS, Corsini LM, Müller M. Micotoxinas e micotoxicoses em cães [Mycotoxins and mycotoxicosis in dogs]. Rev Ed Cont Med Vet Zootec CRMV-SP [J Cont Ed Vet Med Zootec CRMV-SP]. 2021;19(1):e38135. doi:10.36440/recmvz.v19i1.38135.
Reidarson TH, García-Párraga D, Wiederhold, Nathan P. Marine mammal mycoses. In: Gulland FMD, Dierauf LA, Whitman KL (eds.). CRC handbook of marine mammal medicine. 3rd ed. Boca Raton (FL): CRC Press; 2018. p. 410–424.
Reisfeld L, Ikuta CY, Ippolito L, Silvatti B, Neto JSF, Catão-Dias JL, Rosas FCW, Neto JADA, da Silva VMF. Cutaneous mycobacteriosis in a captive Amazonian manatee Trichechus inunguis . Dis Aquat Organ. 2018;127(3):231–236.
Ren J, Jin X, Zhang Q, Zheng Y, Lin D, Yu Y. Fungicides induced triazole-resistance in Aspergillus fumigatus associated with mutations of TR46/Y121F/T289A and its appearance in agricultural fields. J Hazard Mater. 2017;326:54–60.
Revie NM, Iyer KR, Robbins N, Cowen LE. Antifungal drug resistance: evolution, mechanisms and impact. Curr Opin Microbiol. 2018;45:70–76.
Rico A, de Oliveira R, Silva de Souza Nunes G, Rizzi C, Villa S, de Caroli Vizioli B, Montagner CC, Waichman AV. Ecological risk assessment of pesticides in urban streams of the Brazilian Amazon. Chemo-sphere. 2022;291(1):132821. doi:10.1016/j.chemosphere.2021.132821.
Ridley EV, Wong ACN, Westmiller S, Douglas AE. Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster . PLoS One. 2012;7(5):e 36765.
Saika H, Murayama N, Kano R. Molecular typing and antifungal drug susceptivity profile of Rhodotorula mucilaginosa from canine skin and ear canal. J Vet Med Sci. 2021;83(10):1545–1548.
Sato S. Mycobacteriosis in two captive Florida manatees ( Trichechus manatus latirostris ). J Zoo Wildl Med. 2003;34(2):184–188.
Schiesari L, Waichman A, Brock T, Adams C, Grillitsch B. Pesticide use and biodiversity conservation in the Amazonian agricultural frontier. Philos Trans R Soc B Biol Sci. 2013;368:20120378. doi:10.1098/rstb.2012.0378.
Shotts EB, Albert TF, Wooley RE, Brown1 J. Microflora associated with the skin of the bowhead whale ( Balaena mysticetus ). J Wildl Dis. 1990;26(3):351–359.
Sidrim JJC, Carvalho VL, Castelo-Branco DSCM, Brilhante RSN, Bandeira TJPG, Cordeiro RA, Guedes GMM, Barbosa GR, Lazzarini SM, Oliveira DCR, de Meirelles ACO, Attademo FLN, Freire ACB, Moreira JLB, Monteiro AJ, Rocha MFG. Yeast microbiota of natural cavities of manatees ( Trichechus inunguis and Trichechus manatus ) in Brazil and its relevance for animal health and management in captivity. Can J Microbiol. 2015; 61(10):763–769.
Sidrim JJC, Carvalho VL, de Souza Collares Maia Castelo-Branco D, Brilhante RSN, de Melo Guedes GM, Barbosa GR, Lazzarini SM, Oliveira DCR, de Meirelles ACO, Attademo FLN, da Bôaviagem Freire AC, de Aquino Pereira-Neto W, de Aguiar Cordeiro R, Moreira JLB, Rocha MFG. Antifungal resistance and virulence among candida spp. from captive Amazonian manatees and west Indian manatees: potential impacts on animal and environmental health. Ecohealth. 2016;13(2):328–338.
Sidrim JJC, Carvalho VL, de Souza Collares Maia DCB, Brilhante RSN, de Meirelles ACO, Silva CPN, de Aguiar Cordeiro R, Moreira JLB, de Bandeira TJPG, Rocha MFG. Bipolaris hawaiiensis as an emerging cause of cutaneous phaeohyphomycosis in an Antillean manatee Trichechus manatus manatus . Dis Aquat Organ. 2015;113(1):69–73.
Simpson VR, Borman AM, Fox RI, Mathews F. Cutaneous mycosis in a Barbastelle bat ( Barbastella barbastellus ) caused by Hyphopichia burtonii . J Vet Diagn Invest. 2013;25(4):551–554.
Snelders E, Camps SMT, Karawajczyk A, Schaftenaar G, Kema GHJ, van der Lee HA, Klaassen CH, Melchers WJG, Verweij PE. Triazole fungicides can induce cross-resistance to medical triazoles in Aspergillus fumigatus . PLoS One. 2012;7(3):e31801.
Staden R. The Staden sequence analysis package. Appl Biochem Biotechnol B Mol Biotechnol. 1996;5(3): 233–241.
Staggs L, St. Leger J, Bossart G, Townsend FI, Hicks C, Rinaldi M. A novel case of Fusarium oxysporum infection in an Atlantic bottlenose dolphin ( Tursiops truncatus ). J Zoo Wildl Med. 2010;41(2):287–290.
Stephens N, Duignan PJ, Wang J, Bingham J, Finn H, Bejder L, Patterson AP, Holyoake C. Cetacean morbillivirus in coastal Indo-Pacific bottlenose dolphins, Western Australia. Emerg Infect Dis. 2014;20(4): 672–676.
Suzuki A, Ueda K, Segawa T, Suzuki M. Fecal microbiota of captive Antillean manatee Trichechus manatus manatus . FEMS Microbiol Lett. 2019;366(11):1–5.
Takahashi H, Ueda K, Itano EN, Yanagisawa M, Murata Y, Murata M, Yaguchi T, Murakami M, Kamei K, Inomata T, Miyahara H, Sano A, Uchida S. Candida albicans and C. tropicalis isolates from the expired breathes of captive dolphins and their environments in an aquarium. Vet Med Int. 2010;349364. doi: 10.4061/2012/349364.
Tomé LMR, Badotti F, Assis GBN, Fonseca PLC, da Silva GA, da Silveira RMB, Costa-Rezende DH, dos Santos ERD, de Carvalho Azevedo VA, Figueiredo HCP, Góes-Neto A. Proteomic fingerprinting for the fast and accurate identification of species in the Polyporoid and Hymenochaetoid fungi clades. J Proteomics. 2019;203:103390. doi:10.1016/j.jprot.2019.103390.
West AG, Waite DW, Deines P, Bourne DG, Digby A, McKenzie VJ, Taylor MW. The microbiome in threatened species conservation. Biol Conserv. 2019;229:85–98.
White TJ, Bruns T, Lee SJWT, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds.). PCR protocols: a guide to methods and applications. San Diego (CA): Academic Press; 1990. p. 315–322.
Wirth F, Goldani LZ. Epidemiology of Rhodotorula : an emerging pathogen. Interdiscip Perspect Infect Dis. 2012:465717. doi:10.1155/2012/465717.
Zhou D, Wang R, Li X, Peng B, Yang G, Zhang K-Q, Zhang Y, Xu J. Genetic diversity and azole resistance among natural Aspergillus fumigatus populations in Yunnan, China. Microb Ecol. 2022;83:869–885. doi: 10.1007/s00248-021-01804-w.
Zhu L, Wang J, Bahrndorff S. The wildlife gut microbiome and its implication for conservation biology. Front Microbiol. 2021;(12):697499. doi:10.3389/fmicb.2021.697499.
المشرفين على المادة: 0 (Antifungal Agents)
تواريخ الأحداث: Date Created: 20240307 Date Completed: 20240311 Latest Revision: 20240311
رمز التحديث: 20240311
DOI: 10.1638/2022-0069
PMID: 38453495
قاعدة البيانات: MEDLINE
الوصف
تدمد:1042-7260
DOI:10.1638/2022-0069