The activity of propolis against pathogenic fungi isolated from human infections

Wolska, Katarzyna; Antosik, Katarzyna

doi:10.1590/s2175-97902023e19978

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Brazilian Journal of Pharmaceutical Sciences

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Article • Braz. J. Pharm. Sci. 59 • 2023 • https://doi.org/10.1590/s2175-97902023e19978 copy

The activity of propolis against pathogenic fungi isolated from human infections

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Propolis is a resinous hive product collected by bees from the buds or other parts of plants. It is known for having various biological properties, including antifungal activity. Among the substances present in propolis, flavonoids and phenolic acids and their esters are responsible for its antifungal properties. This means that propolis is ideal for use as an antifungal agent in alternative medicine to treat a number of both topical and systemic infections caused by Candida species and other yeast-like fungi, dermatophyte and nondermatophyte moulds, without the serious side effects typical of synthetic treatment. It is also active against strains of fungi that are resistant to polyenes and azoles, the classes of drugs most commonly used to treat fungal infections. In this article, we review current knowledge about the activity of propolis from different parts of the world and its components in vitro and in vivo against pathogenic fungi isolated from human infections. The article also indicates the possible mechanism of antifungal activity of propolis and its components.

Keywords:
Propolis; Antifungal activity; Human infections

Propolis type	Geographic origin	Plant source	Main bioactive compounds
Poplar propolis	Europe, non-tropic regions of Asia	Populus spp., most often P. nigra L.	Phenolic acids (cinnamic, p-coumaric (4-hydroxycinnamic acid), ferulic, caffeic acid (caffeic acid phenethyl ester-CAPE); flavonoids (chrysin, tectochrysin, apigenin, pinocembrin, pinobanksin, pinobanksin O-acetate, galangin, kaempferol, kaempferide, quercetin)
Green Popolis	Brazil	Baccharis spp., predominatly B. dracunculifolia DC.	Phenolic acids (dihydrocinnamic acid, p-coumaric acid, 3,5-diprenyl-4-hydroxycinnamic acid (artepillin C), 3-prenyl-4-(dihydrocinnamoyloxy)-cinnamic acid (baccharin), 3-prenyl-4-hydroxycinnamic acid (drupanin); flavonoids (kaempferol, kaempferide, sakuranetin, quercetin, chrysin, galangin, pinobanksin O-acetate)

Fungi	EEP dose	Type of propolis	in vitro/in vivo	Place of isolation of fungi	Reference
C. albicans	1-12 mg/ml	Brazilian green	In vitro	Saliva of patients with dentures	*Ota et al., 2001*Ota C, Unterkircher C, Fantinato V, Shimizu MT. Antifungal activity of propolis on different species of Candida. Mycoses. 2001;44(9-10):375-378.
C. tropicalis	1-12 mg/ml
C. glabrata	1-12 mg/ml
C. crusei	1-12 mg/ml
C. quilliermondii	1-12 mg/ml
Candida spp.	20%	Brazilian green	In vivo	Isolates from patients with denture stomatitis	*Santos et al., 2005*Santos VR, Pimenta FJGS, Aguiar MCF, Do Carmo MAV, Naves MD, Mesquita RA. Oral candidiasis treatment with Brazilian ethanol propolis extract. Phytother Res. 2005;19(7):652-654.
C. albicans	EEP with a total phenol content of 550.30 μg/ml	Brazilian green	In vitro	Isolates from patients with vulvovaginal candidiosis	*Dalben-Dota et al., 2011*Dalben-Dota KF, Consolaro MEL, Svidzinski TIE, Bruschi ML. Antifungal Activity of Brazilian propolis microparticles against yeasts isolated from vulvovaginal candidiasis. Evid Based Complement Alternat Med Volume 2011, Article ID 201953, 8 pages.
C. glabrata	EEP with a total phenol content of 550.30 μg/ml
C. parapsilosis	EEP with a total phenol content of 550.30 μg/ml
C. quilliermondii	1.56 mg/ml
C. albicans	32-64 µg/ml	Brazilian red	In vitro	Isolates from patients with chronic periodontitis	*Siqueira et al., 2015*Siqueira ABS, de Araújo Rodriquez LRN, Santos RKB, Marinho RRB, Sheila Abreu S, Peixoto RF, et al. Antifungal activity of propolis against Candida species isolated from cases of chronic periodontitis. Braz Oral Res . 2015;29(1):1-6.
C. tropicalis	32-64 µg/ml
C. glabrata	64 µg/ml
C. albicans	0.23-15 mg/ml	Romanian	In vitro	Tracheal secretions of patients with respiratory tract infection	*Stan et al., 2017*Stan T, Teodor ED, Gatea F, Chifiriuc MC, Lazar V. Antioxidant and antifungal activity of Romanian propolis. Roman Biotechnol Lett. 2017;22(6):13116-13124.
C. albicans	0.006-0.5 µg/ml	Turkish	In vitro	blood isolates	*Sariguzel et al., 2016*Sariguzel FM, Berk E, Koc AN, Sav H, Demir G. Antifungal activity of propolis against yeasts isolated from blood culture: in vitro evaluation. J Clin Lab Anal. 2016;30(5):513-516
C. albicans	200 mg/ml	Yemen	In vitro	Throat swabs of patients with upper respiratory infections	*El-Shouny et al., 2012*El-Shouny W, Muagam F, Sadik Z, Hamza W. Antimicrobial activity of propolis extract on URT infections in pediatric patients admitted to Al-Thowrah Hospital, Hodeidah City, Yemen. World J Med Sci. 2012;7(3):172-177.
C. albicans	1.56 mg/ml	Malaysian	In vitro	Isolates from patients with respiratory infections	*Shehu et al., 2006*Shehu A, Ismail S, Rohin MAK, Harun A, Aziz AA, Haque M. Antifungal properties of Malaysian Tualang honey and stingless bee propolis against Candida albicans and Cryptococcus neoformans. J Appl Pharm Sci. 2006;6(02):044-050.
C. neoformans	1.56 mg/ml
C. albicans	1.56 mg/ml	Korean	In vitro	Clinical isolates	Chee, 2002Chee HY. In vitro evaluation of the antifungal activity of propolis extract on Cryptococcus neoformans and Candida albicans. Mycobiology. 2002;30(2):93-95.
C. neoformans	2 mg/ml
C. albicans	EEP with 500 µg flavonoids	Brazilian green	In vitro	Isolates from patients with onycomycosis	*Oliveira et al., 2006*Oliveira AC, Shinobu CS, Longhini R, Franco SL, Svidzinski TI. Antifungal activity of propolis extract against yeasts isolated from onychomycosis lesions. Mem Inst Oswaldo Cruz. 2006;101(5):493-497.
C. non-albicans	EEP with 500 µg flavonoids
Trichosporon spp.	EEP with 125 µg flavonoids
Triphophyton spp.	30%	Brazilian green	In vivo	Isolates from patients with onycomycosis	*Veiga et al., 2018*Veiga FF, Gadelha MC, da Silva MRT, Costa MI, Kischkel B, de Castro-Hoshino LV, et al. Propolis extract for onychomycosis topical treatment: from bench to clinic. Front Microbiol. 9:779.doi:10.3389/fmicb. 2018.00779. eCollection. 2018. https://doi.org/10.3389/fmicb. 2018.0077...
T. rubrum	64-512 µg/ml	Brazilian green	In vitro	Clinical isolates	*Siqueira et al., 2009*Siqueira AB, Gomes BS, Cambuim I, Maia R, Abreu S, Souza-Motta CM, et al. Trichophyton species susceptibility to green and red propolis from Brazil. Lett Appl Microbiol . 2009;48(1):90-96.
T. rubrum	64-512 µg/ml	Brazilian green	In vivo	Clinical isolates
T. tonsurans	128-1024 µg/ml
T. mentagrophytes	128-1024 µg/ml
T. rubrum	8-128 µg/ml	Brazilian red	In vitro	Clinical isolates	*Siqueira et al., 2009*Siqueira AB, Gomes BS, Cambuim I, Maia R, Abreu S, Souza-Motta CM, et al. Trichophyton species susceptibility to green and red propolis from Brazil. Lett Appl Microbiol . 2009;48(1):90-96.
T. rubrum	8-128 µg/ml	Brazilian red	In vivo	Clinical isolates
T. tonsurans	32-128 µg/ml
T. mentagrophytes	16-128 µg/ml
T. mentagrophytes	125 µg/ml	Brazilian green	In vitro	Isolates from patients with tinea pedis	Soares and Cury, 2001Soares MMSR, Cury AE. In vitro activity of antifungal and antiseptic agents against dermatophyte isolates from patients with tinea pedis. Braz J Microbiol.2001;32:130-134.
T. rubrum	250 µg/ml
Epidermophyton floccosum	125-250 µg/ml
T. mentagrophytes	≤64 µg/ml	Slovak, Czech	In vitro	Clinical isolates	Buchta, Černý, Opletalová, 2011Buchta V, Černý J, Opletalová V. In vitro antifungal activity of propolis samples of Czech and Slovak origin. Cent Eur J Biol. 2011;6(2):160-166.
C. albicans	≤64 µg/ml	Slovak, Czech	In vitro	Clinical isolates
A spergillus spp.	250 µg/ml	Iranian	In vitro	Clinical isolates	Diba, Mahmoudi, Hashemi, 2018Diba K, Mahmoudi M, Hashemi J. In vitro activity of propolis alcoholic extract on opportunistic pathogenic fungi. Int J Res Appl Basic Med Sci. 2018;4(2):68-73.
Candida spp.	250 μg/ml

Universidade de São Paulo, Faculdade de Ciências Farmacêuticas Av. Prof. Lineu Prestes, n. 580, 05508-000 S. Paulo/SP Brasil, Tel.: (55 11) 3091-3824 - São Paulo - SP - Brazil
E-mail: bjps@usp.br

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[1] *Correspondence: K. Wolska. Institute of Health Sciences. University of Natural Sciences and Humanities. Ul. Prusa 14, 08-110 Siedlce, Poland. E-mail: kwolska@uph.edu.pl.