Schinus terebinthifolius (Brazilian Peppertree) extract used as antifungal to control Candida spp. in planktonic cultures and biofilms

Authors

  • Daiane de Jesus Viegas Federal University of Rio de Janeiro (UFRJ). Institute of Biodiversity and Sustainability (NUPEM). Av. São José Barreto, 764 - Macaé, RJ, Brazil. 27965-045. https://orcid.org/0000-0002-4829-6395
  • Isabela Amêndola University of Taubaté (UNITAU). Basic Institute of Biosciences. Av. Tiradentes, 500 - Taubaté, SP, Brazil. 12030-180.
  • Tássia Marchetti Botrel São Paulo State University (UNESP). Institute of Science and Technology. Av. Eng. Francisco José Longo, 777 - São José dos Campos, SP, Brazil. 12245-000. https://orcid.org/0000-0002-3054-301X
  • Felipe Eduardo de Oliveira University Center Brazcubas. Brazcubas Faculty of Dentistry. Av. Francisco Rodrigues Filho, 1233 - Mogi das Cruzes, SP, Brazil. 08773-380.
  • Leandro Wagner Figueira São Paulo State University (UNESP). Institute of Science and Technology. Av. Eng. Francisco José Longo, 777 - São José dos Campos, SP, Brazil. 12245-000. https://orcid.org/0000-0002-8504-2183
  • Fábia Lugli Sper São Paulo State University (UNESP). Institute of Science and Technology. Av. Eng. Francisco José Longo, 777 - São José dos Campos, SP, Brazil. 12245-000. https://orcid.org/0000-0002-9708-046X
  • Jonatas Rafael de Oliveira Anhembi Morumbi University. School of Medicine. Av. Dep. Benedito Matarazzo, 4050, São José dos Campos, SP, Brazil. 12230-002. https://orcid.org/0000-0003-2398-6506
  • Luciane Dias de Oliveira São Paulo State University (UNESP). Institute of Science and Technology. Av. Eng. Francisco José Longo, 777 - São José dos Campos, SP, Brazil. 12245-000. https://orcid.org/0000-0001-9956-7768

DOI:

https://doi.org/10.14295/bds.2020.v23i4.2077

Abstract

Objective: The use of medicinal plants may be an alternative method for the control of Candida spp. responsible for human infections. This study evaluated the antifungal effect of Schinus terebinthifolius extract (Brazilian Peppertree) on C. albicans, C. dubliniensis, C. glabrata, and C. krusei planktonic cultures and biofilms. Material and Methods: Minimum inhibitory concentration (MIC) and minimum fungal concentration (MFC) of the plant extract were determined by the broth microdilution method. Biofilms formed in microplate wells were exposed to the extract for 5 min (50, 100 and 200 mg/mL) or 24 h (25, 50 and 100 mg/mL). After determination of colony-forming units per milliliter (CFU/mL), the data were analyzed by one-way ANOVA and Tukey’s Test (P ? 0.05). Results: Different MIC (mg/mL) were found, such as 0.39 (C. dubliniensis), 1.56 (C. albicans), and 3.13 (C. glabrata and C. krusei). Besides, MFC (mg/mL) of 0.78 (C. dubliniensis) and 3.13 (C. albicans, C. glabrata and C. krusei) were also observed. Regarding the biofilms, significant reductions (log10) were found after 5 min and 24 h exposure to the plant extract, compared to the control group. However, C. dubliniensis was significantly affected only in 24 h treatment. Conclusion: S. terebinthifolius extract presented a significant antifungal effect on C. albicans, C. dubliniensis, C. glabrata, and C. Krusei both in planktonic cultures and biofilms.

References

Pereira EMR, Gomes RT, Freire NR, Aguiar EG, Santos VR. In vitro antimicrobial activity of brazilian medicinal plant extracts against pathogenic microorganisms of interest to dentistry. Planta Med. 2011;77:401–4. doi: 10.1055/s-0030-1250354.

Tsai PW, Chen YT, Hsu PC, Lan CY. Study of Candida albicans and its interactions with the host: A mini review. Biomed. 2013;3:51-64.

Giri S, Kindo AJ. A review of Candida species causing blood stream infection. Ind J of Med Microbiol. 2012;30:270-8. doi: 10.4103/0255-0857.99484.

Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J. Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev. 2012;36:288–305. doi: 10.1111/j.1574-6976.2011.00278.x

Rodrigues CF, Silva S, Henriques M. Candida glabrata: a review of its features and resistance. Eur J Clin Microbiol Infect Dis. 2013;33:673–88. doi: 10.1007/s10096-013-2009-3.

Ferreira GLS, Pérez ALAL, Rocha IM, Pinheiro MA, de Castro RD, Carlo HL, et al. Does scientific evidence for the use of natural products in the treatment of oral candidiasis exist? A systematic review. Evid Based Complement Alternat Med. 2015;2015:147804. doi: 10.1155/2015/147804.

Nocchi SR, de Moura-Costa GF, Novello CR, Rodrigues J, Longhini R, de Mello JC, et al. In vitro cytotoxicity and anti-Herpes simplex virus type 1 activity of hydroethanolic extract, fractions, and isolated compounds from stem bark of Schinus terebinthifolius Raddi. Pharmacogn Mag. 2016;12:160-4. doi: 10.4103/0973-1296.177903.

Barbieri DV, Tonial F, Lopez PVA, Sales Maia BH. Antiadherent activity of Schinus terebinthifolius and Croton urucurana extracts on in vitro biofilm formation of Candida albicans and Streptococcus mutans. Arch Oral Biol. 2014;59:887-76. doi: 10.1016/j.archoralbio.2014.05.006.

CLSI. Reference method for broth dilution in tests for determining the sensitivity to antifungal therapy of yeast. Approved standard, CLSI document M27-A2. 2002. 2nd ed. USA.

CLSI. Reference method for broth dilution antifungal susceptibility testing of yeasts. Fourth Informational Supplement M27-S4. 2012. USA.

Alves LA, Freires Ide A, Pereira TM, de Souza A, Lima Ede O, de Castro RD. Effect of Schinus terebinthifolius on Candida albicans growth kinetics, cell wall formation and micromorphology. Acta Odontol Scand. 2013;71:965-71. doi: 10.3109/00016357.2012.741694.

Moura-Costa GF, Nocchi SR, Ceole LF, de Mello JC, Nakamura CV, Dias Filho BP, et al. Antimicrobial activity of plants used as medicinals on an indigenous reserve in Rio das Cobras, Paraná, Brazil. J Ethnopharmacol. 2012;143:631-8. doi: 10.1016/j.jep.2012.07.016.

Alves LA, Freires Ide A, de Souza TM, de Castro RD. In vitro activity of Schinus terebinthifolius (Brazilian pepper tree) on Candida tropicalis growth and cell wall formation. Acta Odontol Latinoam. 2012;25:287-92.

Martínez MJ, Alonso GN, Badell JB. Actividad antimicrobiana del Schinus terebinthifolius Raddi (Copal). Rev Cuba Plantas Med. 1996;1:37–9.

Gomes FS, Procópio TF, Napoleão TH, Coelho LC, Paiva PM. Antimicrobial lectin from Schinus terebinthifolius leaf. J Appl Microbiol. 2013;114:672-9. doi: 10.1111/jam.12086.

Johann S, Pizzolatti MG, Donnici CL, Resende MA. Antifungal properties of plants used in Brazilian traditional medicine against clinically relevant fungal pathogens. Braz J Microbiol. 2007;38:632-7.

Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O'Toole GA. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature. 2003;426:306-10.

Das PP, Saikia L, Nath R, Phukan SK. Species distribution & antifungal susceptibility pattern of oropharyngeal Candida isolates from human immunodeficiency virus infected individuals. Indian J Med Res. 2016;143:495-501. doi: 10.4103/0971-5916.184288.

Gong X, Luan T, Wu X, Li G, Qiu H, Kang Y, et al. Invasive candidiasis in intensive care units in China: Risk factors and prognoses of Candida albicans and non-albicans Candida infections. Am J Infect Control. 2016;44:e59-63. doi: 10.1016/j.ajic.2015.11.028.

Mukasa KJ, Herbert I, Daniel A, Sserunkuma KL, Joel B, Frederick B. Antifungal susceptibility patterns of vulvovaginal Candida species among women attending antenatal clinic at mbarara regional referral hospital, South Western Uganda. Br Microbiol Res J. 2015;5:322-31.

Sullivan DJ, Westerneng TJ, Haynes KA, Bennett DE, Coleman DC. Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals. Microbiology. 1995;141:1507–21.

Jackson AP, Gamble JA, Yeomans T, Moran GP, Saunders D, Harris D, et al. Comparative genomics of the fungal pathogens Candida dubliniensis and Candida albicans. Genome Res. 2009;19:2231–44. doi: 10.1101/gr.097501.109.

McManus BA, Coleman DC. 2014. Molecular epidemiology, phylogeny and evolution of Candida albicans. Infect Genet Evol. 21:166–78. doi: 10.1016/j.meegid.2013.11.008.

Samaranayake LP, Samaranayake YH. Candida krusei: biology, epidemiology, pathogenicity and clinical manifestations of an emerging pathogen. J Med Microbiol. 1994;41:295-310.

Santos JD, Piva E, Vilela SF, Jorge AO, Junqueira JC. Mixed biofilms formed by C. albicans and non-albicans species: a study of microbial interactions. Braz Oral Res. 2016;30.pii:S1806-83242016000100232. doi: 10.1590/1807-3107BOR-2016.vol30.0023.

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Published

2020-09-30

Issue

Vol. 23 No. 4 (2020): Oct - Dec / 2020 - published Sep 2020

Section

Clinical or Laboratorial Research

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