Biological and physiological responses of Candida albicans to some natural products and some heavy metals
DOI:
https://doi.org/10.56511/JIPBS.2019.v6.i04.pp42-52Abstract
The factors responsible for Candida albicans pathogenesis are still not fully understood and increasing resistance to commonly used antifungal agents necessitates the search for new formulations. The effect of heavy metals on the growth of Candida albicans (ATCC 10231) was tested, where Se, CO and Zn caused 100%, 72.65 and 17.4% dry weight inhibition, respectively. The inhibitory effect of different natural extracts on Candida albicans such as ethanolic extract of propolis, methanolic extract of Miswak (Salvadora persica), methanolic extract of Black seed (Nigella sativa), Musk oil (Moschus moschiferus), essential oil of clove bud (Syzygium aromaticum and Peppermint oil (Mentha biperatta) on Candida albicans was evaluated. The antifungal agent fluconazole was used as a positive control. Combination between 50ppm of selenium and 50ppm of fluconazole increased the activity of fluconazole against Candida albicans. Moschus moschiferus showed more potent inhibitory effect on the growth of Candida albicans. Addition of 50ppm selenium to Moschus moschiferus, showed highly increase of its antifungal potency against Candida albicans. Total protein and lipid content of Candida albicans decreased greatly in presence Moschus moschiferus, selenium or both together in the growth media, while, carbohydrate content increased slightly in the presence of selenium but sharply decreased in the presence of Moschus moschiferus alone and in the combination between Moschus moschiferus and selenium.100ppm of cobalt prevented formation of germ tube while equivalent 1ml of Moschus moschiferus 100ml media had seemed to destroy the cells of Candida albicans, which can make these formulations an effective and safe alternative source for elimination of Candida albicans.
Keywords:
Candida albicans, Nigella sativa, Syzygium aromaticum, Mentha biperattaDownloads
References
Naglik JR, ChallacombeSJ and Hube B: Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol. Mol. Biol. Rev. 2003; 67: 400-428.
Whiteway Mand Oberholzer U: Candida morphogenesis and host – pathogen interactions. Curr. Opin. Microbiol. 2004; 7: 350 – 357.
Kalemba D and Kunicka A: Antibacterial and antifungal properties of essential oils. Curr. Med. Chem. 2003; 10: 813 – 829.
Jain SK and Agrawal SC:Fungistatic activity of some perfumes against otomycotic pathogens. Mycoses. 2002; 45: 88 – 90.
Moghim H:Antifungal effects of Zatariamultiflora and Nigella sativa extracts against Candida albicans Herb. Med. Pharmacol. 2005; 4(4): 138141.
Rajkowska K, Nowicka-Krawczyk P and Kunicka-Styczy ´nska A: Effect of Clove and Thyme Essential Oils on Candida Biofilm Formation and the Oil Distribution in Yeast Cells. Molecules 2019; 24, 1954.
KimTN, FengQL, KimJO, Wu J, Wang H, Chen GC and CuiFZ: Antimicrobial Effects of Metal Ions (Ag + , Cu 2+ , Zn 2+ ) in Hydroxyapatite. Journal of Materials Science: Materials in Medicine 1998; 9: 29-134.
Deans SG: Evaluation of antimicrobial activity of essential (volatile) oils. In: Linskens HF, Jackson JF, eds. Modern Methods of Plant Analysis. New Series Essential Oils and Waxes. 1998; 12:309 – 18.
Shuford JA, Piper KE, Steckelberg JM, and Patel R: In vitro biofilm characterization and activity of antifungal agents alone and in combination against sessile and planktonic clinical Candida albicans isolates. DiagMicrobiol Infect Dis. 2007; 57:277 – 81.
Sheehan DJ, Hitchcock CA, and Sibley CM: Current and emerging azole antifungal agents. Clin Microbiol Rev . 1999; 12:40 – 79.
Bonjar S.: Evaluation of antibacterial properties of some medicinal plants used in Iran. J Ethnopharmacol. 2004; 94:301 – 5.
Li H, Qing C, Zhang Y, and Zhao Z.: Screening for endophytic fungi with anti-tumour and antifungal activities from Chinese medicinal plants. World J Microbial Biotechnol. 2005; 21:1515 – 21.
Conner DE: Naturally occurring compounds. In: Davidson P, Branen AL, eds. Antimicrobials in Foods. New York: Marcel Dekker 1993; 1993:441 – 68.
Chhabra SC, Shao JF, and Mshiu EN: Antifungal activity among traditionally used herbs in Tanzania. The Dar Med J. 1982; 9: 68-73.
Umbreit WW, Burries RH and Stauffer JF: Manometric techniques. A manual describing methods applicable to the study of tissue metabolism. Burgess Publishing Co., Minneapolis. 1959; 239.
Lowry OH, Rosebrough NJ, Farr AL and Randall RJ: Protein measurement with the Folin Phenol Reagent. J. Biol. Chem. 1951; 193: 265-275.
Barnes H and Blackstock J: Estimation of lipids in marine animals and tissues: detailed investigation of the sulphophosphovanillin method for total lipids. J. Exp. Mar. Biol. Ecol . 1973; 12: 103 – 118.
Elmer WK, Stephen DA and William MJ.: Laboratory approach to the di agnosis of fungal infictions. 14 th ed, J. P. Lipincot t company, Philadelphia. 1992; 387 - 840.
Duncan DB: Multiple range and multiple F test. Biometrics. 1955; 11:1.
Snedecor GW and Cochran WG: Statistical Methods. 6 th ed. Iowa State University. 1967; Press : Ames, IA.
Iwu MW, Duncan AR and Okunji CO: New Antimicrobials of Plant origin. In JanickJ. ed. Perspectives on New Crops and new Uses. Alexandria, VA: ASHS Press. 1999; 457-462.
Prakash S and Jain AK: Antifungal Activity and Preliminary Phytochemical Studies of Leaf extract of Solanumnigrum Linn. International Journal of Pharmacy and Pharmaceutical Sciences. 2011; 3(4):352-355.
Rex JH, Rinaldi MGand Pfaller MA: Resistance of Candida species to fluconazole. Antimicrob Agents Chemother. 1995; 39:1 – 8.
Mukherjee PK, Chandra J, Kuhn DM, and Ghannoum MA: Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect Immun. 2003; 71:4333 – 40.
Santos VR, Pimenta FJ, Aguiar MC, do Carmo MA, Naves MD and Mesquita RA: Oral candidiasis treatment with Brazilian ethanol propolis extract. Phytother. Res. 2005; 19:652-664.
Oliveira AC, Shinobu CS, Longhini R, Franco SL, and Svidzinski TI: Antifungal activity of propolis extract against yeasts isolated from onychomycosis lesions. Mem. Inst. Oswaldo Cruz. 2006; 101:493-7.
Ghasem YB, Ownagh A and Hasanloei M: Antibacterial and antifungal activity of Iranianpropolis against Staphylococcus aureus and Candida albicans. Pak. J. Biol. Sci. 2007; 10:1343-5.
Quintero-Mora ML, Londoño-Orozco A, Hernández-Hernández F, Manzano-Gayosso P, López-Martínez R, Soto-Zárate CI, Carrillo-Miranda L, Penieres-Carrillo G, García-Tovar CG and Cruz-Sánchez TA: Effect of Mexican propolis extracts from Apismellifera on Candida albicans in vitro growth. Rev. Iberoam. Micol. 2008; 25:22-6.
D'Auria FD, Tecca M, Scazzocchio F, Renzini V and Strippoli V: Effect of propolis on virulence factors of Candida albicans. J Chemother. 2003; 15(5):454-60.
Marcucci MC: Propolis: chemical composition, biological properties and therapeutic activity. Apidologie. 1995; 26, 83-99.
Herrera C L, Alvear M, Barrientos L, Montenegro G, and Salazar LA: The antifungal effect of six commercial extracts of Chilean propolis on Candida spp. Cien. Inv. Agr. 2010; 37(1):75-84.
Davidson PM: Chemical preservatives and naturally antimicrobialcompounds. In Food Microbiology. Fundamentals and Frontiers, 2nd Ed. (M.P. Beuchat and L.R. Montville, eds.) pp. 2001; 593 – 628, ASM Press, Washington, DC.
Prindle RF and Wright ES: Phenolic compounds. In Disinfection, Sterilization and Preservation (S.S. Block, ed.) pp. 1977; 115 – 118, Lea & Febiger, Philadelphia, PA.
Fung Dyc, Taylor S and Kahan J: Effects of butylated hydroxyanisole (BHA) and butylated hydroxytoluene (BHT) on growth and aflatoxin production of Aspergillusflavus. J. Food Safety. 1977; 1: 39 – 51.
Lis-Balchin M and Deans SG: Bioactivity of selected plant essential oils against Listeria monocytogenes. J. Appl. Microbiol. 1997; 82:759 – 762.
Conner DE and Beuchat LR : Effects of essential oils from plants on growth of food spoilage yeasts. J. Food Sci. 1984; 49, 429 – 434.
Nzeako BC and Bushra Al Lawati: Comparative studies of antimycotic potential of thyme and clove oil extracts with antifungal antibiotics on Candida albicans. African Journal of Biotechnology 2008; 7 (11):16121619.
He M, Du M, Fan M and Bian Z.: In vitro activity of eugenol against Candida albicans biofilms. Mycopathologia. 2007; 163(3):137-143.
Latifah-Munirah B, Himratul-Aznita WH and Mohd Zain N: Eugenol, an essential oil of clove, causes disruption to the cell wall of Candida albicans (ATCC 14053), Frontiers in Life Science 2015; 8(3):231-240.
Ayoola1 GA, Lawore1 FM, Adelowotan, T, Aibinu IE, Adenipekun E, Coker HAB and Odugbemi TO: Chemical analysis and antimicrobial activity of the essential oil of Syzigiumaromaticum (clove). African Journal of Microbiology Research. 2008; (2):162-166.
Hosseinzadeh H and Parvardeh S : Anticonvulsant effects of thymoquinone, the major constituent of Nigella sativa seeds, in mic e. Phytomedicine. 2004; 11(1): 56 - 64.
Salman MJ, Khan RA, and Shukla I: Antimicrobial activity of N. sativa oil against Staphylococcu s aureus obtained from clinical specimens. The 38th Annual Conference of Indian Pharmacological Society 2005; 28-30 th ; Chennai India.
Islam SKN, and Ahsan M.: Antifungal activities of the oils of Nigella sativa seeds. Pak J Pharm Sci. 1989; 2: 25-8.
Topozada HH, Mazolum HA, and El-Dakhakhny M.: The antibacterial properties of Nigella sativa seeds. Active principle with some clinical applications. J Egypt Med Assoc. 1965; 48:187 – 202.
Hanafy MS, and Hatem ME.: Studies on the antimicrobial activity of Nigella sativa seed (black cumin). J Ethnopharmacol. 1991; 34:275 – 8.
Mishra RP.: Effect of Metal Ions and Drugs on Antibacterial Activities of Nigella Sati va (L.) Seeds. Webmed Central Ayurvedic Medicine 2011; 2(8):WMC002074.
Shokri H, Davati A, Khazaei A and Akbari A.: In vitro antifungal effect of herbal mixture (Nigella sativa, Foeniculumvulgare and Camellia sinensis) against Candida species isolated from denture wearers. J Herbmed Pharmacol. 2017; 6(2):74-79.
Al-Lafi T, Ababneh H.: The effect of the extract of miswak (chewing sticks) used in Jordan and the Middle East on oral bacteria. Int Dent J. 1995; 45: 218-22.
Al-Bagieh NH, Idowu A, and Salako NO.: Effect of aqueous extract of miswak on the in vitro growth of Candida albicans. Microbios Lett. 1994; 80: 107-113.
Darout I, Christy A, Skaug N.: Identification and Quantification of Some Potentially Antimicrobial Anionic Components in Miswak Extract. Indian J Pharmacol. 2000; 32: 11-14.
Kamel MS, Ohtani K, Assaf MH.: Lignan glycosides from stems of Salvadora persica. Phytochem. 1992; 31: 2469-2471.
Abd EL Rahman HF, Skaug N, Whyatt A.: Volatile compounds in crude Salvadora persica extracts. Pharmaceut Biol. 2003; 41: 399-404.
El-Desoukey RMA: Comparative Microbiological Study between the Miswak (Salvadora persica) and the Toothpaste International Journal of Microbiological Research 2015; 6 (1): 47-53.
Deidda D, Lampis G, Maullu G, Pompei R, Isaia F, Lippolis V and Verani G.: Antifungal, antibacterial, antiviral and cytotoxic activity of novel thioand seleno-azoles. Pharmacological Research 1997; 36 (3): 19397.
Holmes AR, Cannon RD and Shepherd MG.: Effect of calcium ion uptake on Candida albicansmorphology. FEMS Microbiol Lett. 1991; 61 (2-3): 187-193.
Falih AM.: Comparative toxicity of heavy metals to some yeasts isolated from Saudi Arabian soil. Bioresource Technology. 1998; 64: 193-98.
Ryder NS, Wagner S and LeitherI: In vitro activities of Terbinafine against Cutaneous Isolates of C. albicans and other Pathogenic Yeasts. Antimicrob. Agents Chemother. 1998; 42: 1037-1061.
Fries N.: Effects of volatile organic compounds on the growth and development of fungi. Trans. Br. Mycol. Soc.1973; 60: 1.
Jain SK and Agrawal SC.:Fungistatic activity of some perfumes against otomycotic pathogens. Mycoses. 2003; 45(3-4): 88 – 90.
Meruzzella JC, Scrandis DA, Scrandis JB and Grabon G.: Article Title. Plant Dis. Reporter.1960; 44: 789.
Auger P, Cohn P, Joly J, Poirier Sand Cohn D.: Treat ment of cutaneous candidosis in guinea pigs: effect of zinc oxide on the antifungal efficacy of nystatin. Mycoses. 1989; 32 (9): 455 - 60.
Gomberg MA and Mashkilleison AL.: The use of Ecalin for the treatment of candidiomycosis. Bulletin of Dermatology and V enerology. 1997; 97 (4): 1 - 6.
Siau H and Kerridge D.: The effect of antifungal drugs in combination on the growth of Candida glabrata in solid and liquid media, Journal of Antimicrobial Chemotherapy. 1998; 41: 357-366.
Shepherd MG.: Morphogenesis in Candidaalbicans. In Candida albicans: Cellular and Molecular Biology, Edited by R. Prasad. Heideberg : Springer – Verlag. 1991; 5-19.
Borgers M, Bossche HVD, Brabander MD and Van Cutsem J.: Promotion of pseudomycelium formation of Candida albicans in cultur e: a morphologic study of the e ffects of miconazole and ketoconazole. Postgrad. Med. Postgrad. Med. J. 1979; 55: 687 - 691.
Nychas GJE.: Natural antimicrobials from plants. In New Methods of Food Preservation (G.W. Gould, ed.) pp. 1995; 58 – 69, Blackie Academic and Professional, New York, NY.
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