Antifungal activity of essential oils from Cinnamomum cassia, Myristica fragrans and Syzygium aromaticum against Rhodotorula mucilaginosa

Juliana Caroline Butzge; Simone Krause Ferrão; Letícia Mezzomo; Luciane Noal Calil; Adelina Mezzari; Renata Pereira Limberger; Miriam Anders Apel

doi:10.22456/2527-2616.104615

Authors

Juliana Caroline Butzge Programa de Pós‐Graduação em Ciências Farmacêuticas, Faculdade de Farmácia - Universidade Federal do Rio Grande do Sul
Simone Krause Ferrão Programa de Pós‐Graduação em Ciências Farmacêuticas, Faculdade de Farmácia - Universidade Federal do Rio Grande do Sul
Letícia Mezzomo Departamento de Análises Clínicas - Faculdade de Farmácia - Universidade Federal do Rio Grande do Sul
Luciane Noal Calil Departamento de Análises Clínicas - Faculdade de Farmácia - Universidade Federal do Rio Grande do Sul
Adelina Mezzari Departamento de Análises Clínicas - Faculdade de Farmácia - Universidade Federal do Rio Grande do Sul
Renata Pereira Limberger Programa de Pós‐Graduação em Ciências Farmacêuticas, Faculdade de Farmácia, Departamento de Análises Clínicas - Universidade Federal do Rio Grande do Sul
Miriam Anders Apel Programa de Pós‐Graduação em Ciências Farmacêuticas, Faculdade de Farmácia, Departamento de Análises Clínicas - Universidade Federal do Rio Grande do Sul

DOI:

https://doi.org/10.22456/2527-2616.104615

Keywords:

Rhodotorula mucilaginosa, essential oils, antifungal

Abstract

Rhodotorula genus comprises yeasts from Sporidiobolaceae family. Considered as non-pathogenic until the last two decades, different species of Rhodotorula are emerging as pathogens in humans, with R. mucilaginosa being the most commonly involved in infections, ranging from simpler clinical conditions such as skin manifestations to more severe cases such as meningitis and endocarditis. The major facilitating agents for the emergence of these infections are invasive procedures such as catheter implants. The primary drugs of choice used to treat these infections are amphotericin B and fluconazole. However, some strains of this yeast show different degrees of resistance to these substances, thus justifying the search for new therapeutic agents. Considering this, the present study aims the investigation of the antifungal activity of the essential oils of Cinnamomum cassia (cinnamon), Syzygium aromaticum (clove) and Myristica fragrans (nutmeg) against clinical isolates of R. mucilaginosa. The essential oils were obtained by hydrodistillation and characterized by GC-MS. The investigation of the antifungal action activity was performed by the agar disc-diffusion test followed by the Minimum Inhibitory Concentration (MIC) determination. All the essential oils were species present their oil characterized by the presence of phenylpropanoids, with eugenol (77.6 to 94.4%) as the main compound of clove and E-cinnamaldehyde (90.4 to 100%) of cinnamon. Nutmeg oil is characterized by the presence of showed as main compounds the myristicin (1.8 a 12.8%) and elemicin (4.3 a 11.1%) phenylpropanoids, besides sabinene (28.2 to 44.4%) and terpinen-4-ol (16.0 to 19.5%) monoterpenes. In the investigation of antifungal activity, all the oils showed potential action against clinical isolates of R. mucilaginosa, with MICs ranging from 8 to 500 µg/mL. The results demonstrate that these oils are promising candidates in the search for new anti-Rhodotorula agents, enabling the treatment of aforementioned infections.

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References

Wirth F, Goldani LZ. Epidemiology of Rhodotorula: An Emerging Pathogen. Interdiscip Perspect Infect Dis. 2012;1–7.

Alves KP. Realidade e desafios de infecções emergentes por Rhodotorula spp. em pacientes hospitalizados. Universidade Federal de Santa Catarina; 2019.

Louria DB, Greenberg SM, Molander DW. Fungemia caused by certain nonpathogenic strains of the family Cryptococcaceae. N Engl J Med. 1960;263(25):1281– 4.

Tuon FF, Duboc de Almeida GM, Costa SF. Central venous catheter-associated fungemia due to Rhodotorula spp. - A systematic review. Med Mycol. 2007;45(5):441–7.

Franconieri F, Bonhomme J, Doriot A, Bonnamy C, Ficheux M, Lobbedez T, et al. Fungal peritonitis caused by Rhodotorula mucilaginosa in a CAPD patient treated with liposomal amphotericin B: A case report and literature review. Perit Dial Int. 2018;38(1):69–73.

Rippon JW. Medical Mycology: The Pathogenic Fungi and the Pathogenic Actinomycetes. Philadelphia: W B Saunders Co; 1992. 707-729 p.

De Hoog GS, Guarro J, Gene J, Figueras MJ. Atlas of clinical fungi. 2nd ed. Amer Society for Microbiology; 2001. 1160 p.

Gomes MC, Firmino AV, de Almeida SSM da S. Eeito inibitório in vitro de extratos de Cinnamomum zeylanicum blume no controle de Cylindrocladium candelabrum. Ciência Florest. 2018;28(4):1559–67.

Ma YN, Chen CJ, Li Q, Wang W, Xu FR, Cheng YX, et al. Fungicidal activity of essential oils from Cinnamomum cassia against the pathogenic fungi of Panax notoginseng diseases. Chem Biodivers. 2019;16(11).

Almeida LFD, Cavalcanti YW, Castro RD, Lima EO. Atividade antifúngica de óleos essenciais frente à Candida albicans isoladas de pacientes HIV positivos. Rev Bras Plantas Med. 2011;(Atcc 76845):649–55.

Chang CT, Chang WL, Hsu JC, Shih Y, Chou ST. Chemical composition and tyrosinase inhibitory activity of Cinnamomum cassia essential oil. Bot Stud. 2013;54(1):2–8.

Chou ST, Chang WL, Chang CT, Hsu SL, Lin YC, Shih Y. Cinnamomum cassia essential oil inhibits αMSH-induced melanin production and oxidative stress in murine B16 melanoma cells. Int J Mol Sci. 2013;14(9):19186–201.

Sun L, Zong SB, Li JC, Lv YZ, Liu LN, Wang ZZ, et al. The essential oil from the twigs of Cinnamomum cassia Presl alleviates pain and inflammation in mice. J Ethnopharmacol [Internet]. 2016;194:904. Available from: http://dx.doi.org/10.1016/j.jep.2016.10.064

Raffaella C, Casettari L, Fagioli L, Cespi M, Bonacucina G, Baffone W. Activity of essential oilbased microemulsions against Staphylococcus aureus biofilms developed on stainless steel surface in different culture media and growth conditions. Int J Food Microbiol [Internet]. 2017;241:132–40. Available from: https://doi.org/10.1016/j.ijfoodmicro.2016.10.021

Veloso DJ, Abrão F, Martins CHG, Bronzato JD, Gomes BPFA, Higino JS, et al. Potential antibacterial and anti-halitosis activity of medicinal plants against oral bacteria. Arch Oral Biol. 2020;110.

Mateen S, Shahzad S, Ahmad S, Naeem SS, Khalid S, Akhtar K, et al. Cinnamaldehyde and eugenol attenuates collagen induced arthritis via reduction of free radicals and pro-inflammatory cytokines. Phytomedicine [Internet]. 2018;53:70–8. Available from: https://doi.org/10.1016/j.phymed.2018.09.004

Sun Q, Li J, Sun Y, Chen Q, Zhang L, Le T. The antifungal effects of cinnamaldehyde against Aspergillus niger and its application in bread preservation. Food Chem [Internet]. 2020;317:1–31. Available from: https://doi.org/10.1016/j.foodchem.2020.126405

Kenawy E, Omer AM, Tamer TM, Elmeligy MA, Eldin MSM. International Journal of Biological Macromolecules Fabrication of biodegradable gelatin / chitosan / cinnamaldehyde crosslinked membranes for antibacterial wound dressing applications. Int J Biol Macromol [Internet]. 2019;139:440–8. Available from: https://doi.org/10.1016/j.ijbiomac.2019.07.191

Ferrao JEM. Especiarias : cultura, tecnologia, comercio. Lisboa: Instituo de Investigacao Cientifica Tropical; 1993.

De Oliveira RA, Reis TV, Do Sacramento CK, Duarte LP, De Oliveira FF. Constituintes químicos voláteis de especiarias ricas em eugenol. Brazilian J Pharmacogn. 2009;19(3):771–5.

Beltrán-Villalobos KL, Déciga-Campos M, AguilarMariscal H, González-Trujano ME, Martínez-Salazar MF, Ramírez-Cisneros M de los Á, et al. Synergistic antinociceptive interaction of Syzygium aromaticum or Rosmarinus officinalis coadministered with ketorolac in rats. Biomed Pharmacother [Internet]. 2017;94:858–64. Available from: http://dx.doi.org/10.1016/j.biopha.2017.07.166

Ma YN, Xu FR, Chen CJ, Li QQ, Wang MZ, Cheng YX, et al. The beneficial use of essential oils from buds and fruit of Syzygium aromaticum to combat pathogenic fungi of Panax notoginseng. Ind Crops Prod [Internet]. 2019;133(November 2018):185–92. Available from: https://doi.org/10.1016/j.indcrop.2019.03.029

Radünz M, da Trindade MLM, Camargo TM, Radünz AL, Borges CD, Gandra EA, et al. Antimicrobial and antioxidant activity of unencapsulated and encapsulated clove (Syzygium aromaticum, L.) essential oil. Food Chem [Internet]. 2019;276:180–6. Available from: https://doi.org/10.1016/j.foodchem.2018.09.173

Guimarães AC, Meireles LM, Lemos MF, Guimarães MCC, Endringer DC, Fronza M, et al. Antibacterial activity of terpenes and terpenoids present in essential oils. Molecules. 2019;24:1–12.

Ju J, Xie Y, Yu H, Guo Y, Cheng Y, Zhang R. Synergistic inhibition effect of citral and eugenol against Aspergillus niger and their application in bread preservation. Food Chem [Internet]. 2020;310:1–7. Available from: https://doi.org/10.1016/j.foodchem.2019.125974

Qian W, Sun Z, Wang T, Yang M, Liu M, Zhang J, et al. Antimicrobial activity of eugenol against carbapenem-resistant Klebsiella pneumoniae and its effect on biofilms. Microb Pathog. 2020;139:1–9.

Cho JY, Choi GJ, Son SW, Jang KS, Lim HK, Lee SO, et al. Isolation and antifungal activity of lignans from Myristica fragrans against various plant pathogenic fungi. Pest Manag Sci. 2007;63:935–940.

Rodianawati I, Hastuti P, Cahyanto MN. Nutmeg’s (Myristica Fragrans Houtt) oleoresin: Effect of heating to chemical compositions and antifungal properties. Procedia Food Sci [Internet]. 2015;3:244– 54. Available from: http://dx.doi.org/10.1016/j.profoo.2015.01.027

Muchtaridi, Subarnas A, Apriyantono A, Mustarichie R. Identification of compounds in the essential oil of nutmeg seeds (Myristica fragrans Houtt.) that inhibit locomotor activity in mice. Int J Mol Sci. 2010;11(11):4771–81.

Baser KHC, Buchbauer G. Handbook of Essential Oils: Science, Technology, and Applications. CRC Press; 2009. 991 p.

Pillai S, Mahmud R, Lee WC, Perumal S. Antiparasitic activity of Myristica fragrans Houtt. essential oil against Toxoplasma gondii parasite. APCBEE Procedia [Internet]. 2012;2:92–6. Available from: http://dx.doi.org/10.1016/j.apcbee.2012.06.017

Das S, Kumar Singh V, Kumar Dwivedy A, Kumar Chaudhari A, Upadhyay N, Singh A, et al. Assessment of chemically characterised Myristica fragrans essential oil against fungi contaminating stored scented rice and its mode of action as novel aflatoxin inhibitor. Nat Prod Res [Internet]. 2018;1– 5. Available from: https://doi.org/10.1080/14786419.2018.1519826

Adams RP. Identification of Essential Oils by Ion Trap Mass Spectroscopy. New York: Academic Press; 1989.

Carović-Stanko K, Orlić S, Politeo O, Strikić F, Kolak I, Milos M, et al. Composition and antibacterial activities of essential oils of seven Ocimum taxa. Food Chem. 2010;119(1):196–201.

CLSI. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. 2007.

Magiatis P, Melliou E, Skaltsounis AL, Chinou IB, Mitaku S. Chemical composition and antimicrobial activity of the essential oils of Pistacia lentiscus var. chia. Planta Med. 1999;65(8):749–52.

CLSI. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard — third edition. M27-A3. Wayne. PA, USA; 2008.

Oliveira LBS, Batista AHM, Fernandes FC, Sales GWP, Nogueira NAP. Atividade antifúngica e possível mecanismo de ação do óleo essencial de folhas de Ocimum gratissimum (linn.) sobre espécies de Candida. Rev Bras Plantas Med. 2016;18(2):511– 23.

Kapadiya S, Desai MA. Isolation of Essential Oil From Buds of Syzygium aromaticum Using Hydrodistillation: Multi-Response Optimization and Predictive Modelling. Int J Adv Res Sci Eng. 2017;11:405–18.

Tao D, Li Y, Lu D, Luo Y, Yu S, Ye S. The essential oil components of Cinnamomum cassia: an analysis under different thinning models of plantation Pinus massoniana. J For Res. 2015;

Matulyte I, Jekabsone A, Jankauskaite L, Zavistanaviciute P, Sakiene V, Bartkiene E, et al. The essential oil and hydrolats from Myristica fragrans seeds with magnesium aluminometasilicate as excipient: Antioxidant, antibacterial, and antiinflammatory Activity. Foods. 2020;37(9).

Souza AA, Dias NAA, Piccoli RH, Bertolucci SKV. Composição química e concentração mínima bactericida de dezesseis óleos essenciais sobre Escherichia coli enterotoxigênica. Rev Bras Plantas Med. 2016;18(1):105–12.

Zhao X, Wu H, Wei J, Yang M. Quantification and characterization of volatile constituents in Myristica fragrans Houtt . by gas chromatography-mass spectrometry and gas chromatography quadrupoletime-of- fl ight mass spectrometry. Ind Crop Prod [Internet]. 2019;130(151):137–45. Available from: https://doi.org/10.1016/j.indcrop.2018.12.064

Schlemmer KB, Jesus FPK, Tondolo JSM, Weiblen C, Azevedo MI, Machado VS, et al. In vitro activity of carvacrol, cinnamaldehyde and thymol combined with antifungals against Malassezia pachydermatis. J Mycol Med [Internet]. 2019;29(4):375–7. Available from: https://doi.org/10.1016/j.mycmed.2019.08.003

Shreaz S, Bhatia R, Khan N, Muralidhar S, Basir SF, Manzoor N, et al. Spice oil cinnamaldehyde exhibits potent anticandidal activity against fluconazole resistant clinical isolates. Fitoterapia [Internet]. 2011;82(7):1012–20. Available from: http://dx.doi.org/10.1016/j.fitote.2011.06.004

Ranasinghe L, Jayawardena B, Abeywickrama K. Fungicidal activity of essential oils of Cinnamomum zeylanicum (L.) and Syzygium aromaticum (L.) Merr et L.M.Perry against crown rot and anthracnose pathogens isolated from banana. Lett Appl Microbiol. 2002;35(3):208–11.

Park M, Gwak K, Yang I, Choi W, Jo H, Chang J, et al. Antifungal activities of the essential oils in Syzygium aromaticum (L.) Merr. Et Perry and Leptospermum petersonii Bailey and their constituents against various dermatophytes. J Microbiol. 2007;45(5):460–5.

Pinto E, Vale-Silva L, Cavaleiro C, Salgueiro L. Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species. J Med Microbiol. 2009;58(11):1454–62.

Nardoni S, Najar B, Fronte B, Pistelli L, Mancianti F. In vitro activity of essential oils against Saprolegnia parasitica. Molecules. 2019;24(7):6–13.

Rajkowska K, Nowicka-Krawczyk P, KunickaStyczynska A. Effect of clove and thyme essential oils on Candida biofilm formation and the oil distribution in yeast cells. Molecules. 2019;24(10):1– 12.

Khan SN, Khan S, Misba L, Sharief M, Hashmi A, Khan AU. Synergistic fungicidal activity with low doses of eugenol and amphotericin B against Candida albicans. Biochem Biophys Res Commun [Internet]. 2019;518(3):459–64. Available from: https://doi.org/10.1016/j.bbrc.2019.08.053

Iyer M, Gujjari AK, Gowda V, Angadi S. Antifungal response of oral‑associated candidal reference strains (American Type Culture Collection) by supercritical fluid extract of nutmeg seeds for geriatric denture wearers: An in vitro screening study Meenakshi. J Indian Prosthodont Soc. 2019;17(3):267–72.

Holley RA, Patel D. Improvement in shelf-life and safety of perishable foods by plant essential oils and smoke antimicrobials. Food Microbiol. 2005;22(4):273–92.

Tepe B, Daferera D, Sokmen A, Sokmen M, Polissiou M. Antimicrobial and antioxidant activities of the essential oil and various extracts of Salvia tomentosa Miller (Lamiaceae). Food Chem. 2005;90:333–40.

Miguel MG. Antioxidant and Anti-Inflammatory activities of essential oils: A short review. Molecules. 2010;15:9252–87.

Cai R, Hu M, Zhang Y, Niu C, Yue T, Yuan Y. Antifungal activity and mechanism of citral , limonene and eugenol against Zygosaccharomyces rouxii. LWT - Food Sci Technol [Internet]. 2019;106(January):50–6. Available from: https://doi.org/10.1016/j.lwt.2019.02.059

Sukcharoen O, Sirirote P, Thanaboripat D. Management of aflatoxigenic strains via vapor and contact treatment with essential oil obtained from Myristica Fragrans. Biotropia (Bogor). 2019;26(1):16–22.