Download PDF
Planta Med 2024; 90(02): 111-125
DOI: 10.1055/a-2196-2087
Biological and Pharmacological Activity
Original Papers

Synergism Between Essential Oils and Evaluation of Their Activities with a Focus on Malassezia furfur Control

Fábio Cassola 
1   Faculty of Pharmaceutical Science, State University of Campinas, Campinas, Brazil
2   Research Center of Chemical, Biological and Agriculture, Paulínia, Brazil
,
Nedy Ramírez
1   Faculty of Pharmaceutical Science, State University of Campinas, Campinas, Brazil
2   Research Center of Chemical, Biological and Agriculture, Paulínia, Brazil
,
Guilherme Ribeiro
3   Institute of Biology, State University of Campinas, Campinas, Brazil
,
Lucas Henrique Domingos da Silva 
4   Mutagenesis Laboratory, University of Araraquara, Araraquara, Brazil
,
Alessandra Gambero
5   Life Sciences Center, Pontifical Catholic University of Campinas, Campinas, Brazil
,
Adriana da Silva Santos de Oliveira 
2   Research Center of Chemical, Biological and Agriculture, Paulínia, Brazil
,
Pedro Manoel Mendes de Moraes Vieira
3   Institute of Biology, State University of Campinas, Campinas, Brazil
,
Flávia Aparecida Resende Nogueira 
4   Mutagenesis Laboratory, University of Araraquara, Araraquara, Brazil
,
Marta Cristina Teixeira Duarte
2   Research Center of Chemical, Biological and Agriculture, Paulínia, Brazil
› Author AffiliationsThis work was carried out with the support of the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES) – Finance Code 001 (1806495; 88882.435476/2019-01) and the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (2021/10544-4). We are also thankful for the access to equipment and the assistance provided by the Electron Microscopy Laboratory (LME/UNICAMP).
› Further Information
Also available at
    Permissions and Reprints

Abstract

Seborrheic dermatitis is a chronic inflammatory disease caused by Malassezia yeast species that affects the regions of the body where the sebaceous glands are present. The combined use of different essential oils (EOs) can increase their spectrum of action. Thus, the present study aimed to evaluate the action of EOs alone and in combination with each other on M. furfur, in planktonic and biofilm form, and their anti-inflammatory and mutagenic potential, in addition to the effects on the viability of cells lines. Of the 40 evaluated EOs, 22 showed activity against M. furfur at 0.5 – 2.0 mg/mL concentrations. Among the most active species, a blend of essential oils (BEOs) composed of Cymbopogon martini (Roxb.) Will. Watson (MIC = 0.5 mg/mL) and Mentha × piperita L. (MIC = 1.0 mg/mL) was selected, which showed a synergistic effect against yeast when evaluated through the checkerboard assay. The fungicidal activity was maintained by the addition of anti-inflammatory oil from Varronia curassavica Jacq. to BEOs. The BEOs also showed activity in the inhibition of biofilm formation and in the eradication of the biofilm formed by M. furfur, being superior to the action of fluconazole. Furthermore, it did not show mutagenic potential and did not interfere with the cell viability of both evaluated cell lines (HaCaT and BMDMs). TNF-α levels were reduced only by C. martini; however, this property was maintained when evaluating BEOs. BEOs had no effect on IL-8 levels. Thus, the BEOs may be indicated for alternative treatments against seborrheic dermatitis.

Key words

Poaceae - Lamiaceae - Boraginaceae - Cymbopogon martini - Mentha × piperita - Varronia curassavica

Supporting Information

    Tables containing the chemical composition, yield, the major compounds and relative percentage in EOs of some species, the method of EOs dilution, as well the graphs of inhibition and eradication of M. furfur biofilm formation by A. saturejoides, C. articulatus, E. uniflora, and S. aromaticum EOs, are available as Supporting Information.

  • Supporting Information


Publication History

Received: 07 May 2023

Accepted after revision: 16 October 2023

Article published online:
07 November 2023

© 2023. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Hau CS, Tada Y, Kanda N, Watanabe S. Immunoresponses in dermatomycoses. J Dermatol 2015; 42: 236-244
    CrossrefPubMedSearch in Google Scholar
  • 2 Monir RL, Schoch JJ. Clinical relevance of the microbiome in pediatric skin disease: A review. Dermatol Clin 2022; 40: 117-126
    CrossrefPubMedSearch in Google Scholar
  • 3 Galvis-Marín JC, Rodríguez-Bocanegra MX, Pulido-Villamarín AP, Castañeda-Salazar R, Celis-Ramírez AM, Linares-Linares MY. Actividad antifúngica in vitro de azoles y anfotericina B frente a Malassezia furfur por el método de microdilución M27-A3 del CLSI y Etest® . Rev Iberoam Micol 2017; 34: 89-93
    CrossrefPubMedSearch in Google Scholar
  • 4 Peyrí J, Lleonart M. Clinical and therapeutic profile and quality of life of patients with seborrheic dermatitis. Actas Dermosifiliogr 2007; 98: 476-482
    PubMedSearch in Google Scholar
  • 5 Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: A global multifaceted phenomenon. Pathog Glob Health 2015; 109: 309-318
    CrossrefPubMedSearch in Google Scholar
  • 6 Blankenship JR, Mitchell AP. How to build a biofilm: A fungal perspective. Curr Opin Microbiol 2006; 9: 588-594
    CrossrefPubMedSearch in Google Scholar
  • 7 Cui X, Wang L, Lü Y, Yue C. Development and research progress of anti-drug resistant fungal drugs. J Infect Public Health 2022; 15: 986-1000
    CrossrefPubMedSearch in Google Scholar
  • 8 Yap PSX, Yiap BC, Ping HC, Lim SHE. Essential oils, a new horizon in combating bacterial antibiotic resistance. Open Microbiol J 2014; 8: 6-14
    CrossrefPubMedSearch in Google Scholar
  • 9 Santana AS, Baldin ELL, Santos TLB, Baptista YA, Santos MC, Lima APS, Tanajura LS, Vieira TM, Crotti AEM. Synergism between essential oils: A promising alternative to control Sitophilus zeamais (Coleoptera: Curculionidae). Crop Prot 2022; 153: 105882
    CrossrefPubMedSearch in Google Scholar
  • 10 El Atki Y, Aouam I, El Kamari F, Taroq KN, Mohammed T, Badiaa L, Abdelfattah A. Antibacterial activity of cinnamon essential oils and their synergistic potential with antibiotics. J Adv Pharm Technol Res 2019; 10: 63
    CrossrefPubMedSearch in Google Scholar
  • 11 Siva Sai C, Mathur N. Inhibitory potential of essential oils on Malassezia strains by various plants. Biol Life Sci Forum 2021; 4: 1-6
    CrossrefPubMedSearch in Google Scholar
  • 12 Lee JH, Lee JS. Chemical composition and antifungal activity of plant essential oils against Malassezia furfur . Korean J Microbiol Biotechnol 2010; 38: 315-321
    PubMedSearch in Google Scholar
  • 13 Paulino BN, Silva GNS, Araújo FF, Néri-Numa IA, Pastore GM, Bicas JL, Molina G. Beyond natural aromas: The bioactive and technological potential of monoterpenes. Trends Food Sci Technol 2022; 128: 188-201
    CrossrefPubMedSearch in Google Scholar
  • 14 Salakhutdinov NF, Volcho KP, Yarovaya OI. Monoterpenes as a renewable source of biologically active compounds. Pure Appl Chem 2017; 89: 1105-1117
    CrossrefPubMedSearch in Google Scholar
  • 15 Prashar A, Locke IC, Evans CS. Cytotoxicity of clove (Syzygium aromaticum) oil and its major components to human skin cells. Cell Prolif 2006; 39: 241-248
    CrossrefPubMedSearch in Google Scholar
  • 16 Bickers D, Calow P, Greim H, Hanifin JM, Rogers AE, Saurat JH, Sipes IG, Smith RL, Tagami H. A toxicologic and dermatologic assessment of cinnamyl alcohol, cinnamaldehyde and cinnamic acid when used as fragrance ingredients. Food Chem Toxicol 2005; 43: 799-836
    CrossrefPubMedSearch in Google Scholar
  • 17 Martim JKP, Maranho LT, Costa-Casagrande TA. Review: Role of the chemical compounds present in the essential oil and in the extract of Cordia verbenacea DC as an anti-inflammatory, antimicrobial and healing product. J Ethnopharmacol 2021; 265: 113300
    CrossrefPubMedSearch in Google Scholar
  • 18 Parrino B, Schillaci D, Carnevale I, Giovannetti E, Diana P, Cirrincione G, Cascioferro S. Synthetic small molecules as anti-biofilm agents in the struggle against antibiotic resistance. Eur J Med Chem 2019; 161: 154-178
    CrossrefPubMedSearch in Google Scholar
  • 19 Sienkiewicz M, Łysakowska M, Kowalczyk E, Szymanska G, Kochan E, Krukowska J, Olszewski J, Zielinska-Blizniewska H. The ability of selected plant essential oils to enhance the action of recommended antibiotics against pathogenic wound bacteria. Burns 2017; 43: 310-317
    CrossrefPubMedSearch in Google Scholar
  • 20 Teixeira RF, Balbinot Filho CA, Borges CD. Essential oils as natural antimicrobials for application in edible coatings for minimally processed apple and melon: A review on antimicrobial activity and characteristics of food models. Food Packag Shelf Life 2022; 31: 100781
    CrossrefPubMedSearch in Google Scholar
  • 21 Drago L, De Vecchi E, Nicola L, Gismondo MR. In vitro evaluation of antibioticsʼ combinations for empirical therapy of suspected methicillin resistant Staphylococcus aureus severe respiratory infections. BMC Infect Dis 2007; 7: 111
    CrossrefPubMedSearch in Google Scholar
  • 22 Venturoso LR, Bacchi LMA, Gavassoni WL, Conus LA, Pontim BCA, Bergamin AC. Atividade antifúngica de extratos vegetais sobre o desenvolvimento de fitopatógenos. Summa Phytopathol 2011; 37: 18-23
    CrossrefPubMedSearch in Google Scholar
  • 23 Vitale RF, Ribeiro FAQ. The role of Tumor Necrosis Factor-Alpha (TNF-α) in bone resorption present in middle ear cholesteatoma. Braz J Otorhinolaryngol 2007; 73: 117-121
    CrossrefPubMedSearch in Google Scholar
  • 24 Ben Salah I, Makni F, Cheikhrouhou F, Sellami H, Ayadi A. Les levures du genre Malassezia: Pathologie, milieux dʼisolement et dʼidentification. J Mycol Med 2010; 20: 53-60
    CrossrefPubMedSearch in Google Scholar
  • 25 Pintas SK, Quave CL. A review of botanicals exhibiting antifungal activity against Malassezia spp. implicated in common skin conditions. Curr Dermatol Rep 2019; 8: 279-296
    CrossrefPubMedSearch in Google Scholar
  • 26 Zhang YJ, Han Y, Sun YZ, Jiang HH, Liu M, Qi RQ, Gao XH. Extracellular vesicles derived from Malassezia furfur stimulate IL-6 production in keratinocytes as demonstrated in in vitro and in vivo models. J Dermatol Sci 2019; 93: 168-175
    CrossrefPubMedSearch in Google Scholar
  • 27 Suzuki T, Tsuzuki A, Ohno N, Ohshima Y, Yadomae T. Enhancement of IL-8 production from human monocytic and granulocytic cell lines, THP-1 and HL-60, stimulated with Malassezia furfur . FEMS Immunol Med Microbiol 2000; 28: 157-162
    CrossrefPubMedSearch in Google Scholar
  • 28 Chen W, Viljoen AM. Geraniol – A review update. South African J Bot 2022; 150: 1205-1219
    CrossrefPubMedSearch in Google Scholar
  • 29 Andrade BFMT, Conti BJ, Santiago KB, Fernandes Júnior A, Sforcin JM. Cymbopogon martinii essential oil and geraniol at noncytotoxic concentrations exerted immunomodulatory/anti-inflammatory effects in human monocytes. J Pharm Pharmacol 2014; 66: 1491-1496
    CrossrefPubMedSearch in Google Scholar
  • 30 Li Y, Liu Y, Ma A, Bao Y, Wang M, Sun Z. In vitro antiviral, anti-inflammatory, and antioxidant activities of the ethanol extract of Mentha piperita L. Food Sci Biotechnol 2017; 26: 1675-1683
    CrossrefPubMedSearch in Google Scholar
  • 31 Modarresi M, Farahpour MR, Baradaran B. Topical application of Mentha piperita essential oil accelerates wound healing in infected mice model. Inflammopharmacology 2019; 27: 531-537
    CrossrefPubMedSearch in Google Scholar
  • 32 Rozza AL, Beserra FP, Vieira AJ, Souza EO, Hussni CA, Martinez ERM, Nóbrega RH, Pellizzon CH. The use of menthol in skin wound healing–Anti-inflammatory potential, antioxidant defense system stimulation and increased epithelialization. Pharmaceutics 2021; 13: 1902
    CrossrefPubMedSearch in Google Scholar
  • 33 Su YH, Lin JY. Menthone supplementation ameliorates systemic allergic inflammation in asthmatic mice via regulating Th2-skewed immune balance. Phytomedicine Plus 2022; 2: 100322
    CrossrefPubMedSearch in Google Scholar
  • 34 Basting RT, Spindola HM, Sousa IMO, Queiroz NCA, Trigo JR, de Carvalho JE, Foglio MA. Pterodon pubescens and Cordia verbenacea association promotes a synergistic response in antinociceptive model and improves the anti-inflammatory results in animal models. Biomed Pharmacother 2019; 112: 108693
    CrossrefPubMedSearch in Google Scholar
  • 35 Viveiros MMH, Silva MG, da Costa JGM, Oliveira AG, Rubio C, Padovani CR, Rainho CA, Schellini SA. Anti-inflammatory effects of α-humulene and β-caryophyllene on pterygium fibroblasts. Int J Ophthalmol 2022; 15: 1903-1907
    CrossrefPubMedSearch in Google Scholar
  • 36 El Azab EF, Saleh AM, Yousif SO, Mazhari BBZ, Alrub HA, Elfaki EM, Hamza A, Abdulmalek S. New insights into geraniolʼs antihemolytic, anti-inflammatory, antioxidant, and anticoagulant potentials using a combined biological and in silico screening strategy. Inflammopharmacology 2022; 30: 1811-1833
    CrossrefPubMedSearch in Google Scholar
  • 37 Magouz FI, Mahmoud SA, El-Morsy RAA, Paray BA, Soliman AA, Zaineldin AI, Dawood MAO. Dietary menthol essential oil enhanced the growth performance, digestive enzyme activity, immune-related genes, and resistance against acute ammonia exposure in Nile tilapia (Oreochromis niloticus). Aquaculture 2021; 530: 735944
    CrossrefPubMedSearch in Google Scholar
  • 38 Oliveira CR, Bella LM, Duarte MC, Vieira RP. Brazilian essential oil of Cymbopogon martini (Poaceae): Positive effects on inflammation-induced human fibroblasts and skin aging. Rev Fitos 2021; 15: 444-455
    CrossrefPubMedSearch in Google Scholar
  • 39 Tafrihi M, Imran M, Tufail T, Gondal TA, Caruso G, Sharma S, Sharma R, Atanassova M, Atanassov L, Fokou PVT, Pezzani R. The wonderful activities of the genus Mentha: Not only antioxidant properties. Molecules 2021; 26: 1118
    CrossrefPubMedSearch in Google Scholar
  • 40 Adams RP. Identification of essential oils components by gas chromatography/mass spectroscopy. 4. Ed.. Carol Stream: Allured Pub Corp; 2007
    Search in Google Scholar
  • 41 Cesa S, Sisto F, Zengin G, Scaccabarozzi D, Kokolakis AK, Scaltrito MM, Grande R, Locatelli M, Cacciagrano F, Angiolella L, Campestre C, Granese A, Chimenti P, Basilico N. Phytochemical analyses and pharmacological screening of Neem oil. South African J Bot 2019; 120: 331-337
    CrossrefPubMedSearch in Google Scholar
  • 42 Fratini F, Mancini S, Turchi B, Friscia E, Pistelli L, Giusti G, Cerri D. A novel interpretation of the Fractional Inhibitory Concentration Index: The case Origanum vulgare L. and Leptospermum scoparium J. R. et G. Forst essential oils against Staphylococcus aureus strains. Microbiol Res 2017; 195: 11-17
    CrossrefPubMedSearch in Google Scholar
  • 43 Thangaraju P, Varthya SB. ISO 10993: Biological Evaluation of Medical Devices. In: Shanmugam PST, Palani N, Thangaraju P, Sampath T. eds. Medical Device Guidelines and Regulations Handbook. Cham: Springer International; 2022: 163-187
    Search in Google Scholar
  • 44 Maron DM, Ames BN. Revised methods for the Salmonella mutagenicity test. Mutat Res Mutagen Relat Subj 1983; 113: 173-215
    CrossrefPubMedSearch in Google Scholar
  • 45 Mortelmans K, Zeiger E. The Ames Salmonella/microsome mutagenicity assay. Mutat Res Mol Mech Mutagen 2000; 455: 29-60
    CrossrefPubMedSearch in Google Scholar