Vet Med - Czech, 2015, 60(5):235-247 | DOI: 10.17221/8175-VETMED
Use of natural substances for boar semen decontaminationOriginal Paper
- 1 Faculty of Chemical-Technology, University of Pardubice, Czech Republic
- 2 Institute of Animal Science, Prague-Uhrineves, Workplace Kostelec nad Orlici, Czech Republic
- 3 Faculty of Military Health Sciences, University of Defence, Hradec Kralove
- 4 Faculty of Pharmacy, Hradec Kralove, Charles University, Prague, Czech Republic
The aim of this study was to investigate the antibacterial activity and toxicity for sperm cells of the natural substances gallic acid, methyl gallate, ethyl gallate, propyl gallate, octyl gallate, thymol, carvacrol and eugenol. The antibacterial activity of these natural substances and selected combinations of them against bacterial strains isolated from boar ejaculates was determined using the microdilution and macrodilution method in Mueller-Hinton broth. The most effective natural substances against Gram-negative and Gram-positive bacteria included in our study were thymol and carvacrol with minimum inhibitory concentration (MIC) values in the range of 300-600 µg/ml. Gallic acid exhibited the best antibacterial activity against Pseudomonas aeruginosa strains (MIC values of 300-2400 µg/ml), whereas the ranges of MIC values against Escherichia coli, Enterococcus faecalis and Staphylococcus sp. strains were higher. Octyl gallate exhibited stronger antibacterial activity against staphylococci and enterococci (MIC values of 18.8-75 µg/ml) than against Escherichia coli and Pseudomonas aeruginosa strains with MIC values in the ranges of 300-600 µg/mland 1200-2400 µg/ml, respectively. Thymol combined with carvacrol was the most effective combination against enterococci (MIC values of 75-300 : 150 thymol : carvacrol) and Pseudomonas aeruginosa (MIC values of 75-300 : 300 thymol : carvacrol), bacteria which are known to be frequently resistant to antimicrobials. Similar results were determined for the combination of carvacrol and eugenol against staphylococci and enterococci. The results of the combinations revealed more of an additive rather than a synergistic effect. Thymol and carvacrol were the most effective natural substances against the bacteria included in this study, with a low toxicity for sperm cells compared to other substances, suggesting their possible use for boar semen decontamination.
Keywords: thymol; carvacrol; eugenol; gallic acid; gallates; antibacterial activity; bacteria; spermiotoxicity
Published: May 31, 2015 Show citation
References
- Alma MH, Mavi A, Yildirim A, Digrak M, Hirata T (2003): Screening chemical composition and in vitro antioxidant and antimicrobial activities of the essential oils from Origanum syriacum L. growing in Turkey. Biological and Pharmaceutical Bulletin 26, 1725-1729.
Go to original source...
Go to PubMed...
- Al-Zahrani SHM (2012): Antibacterial activities of gallic acid and gallic acid methyl ester on methicillin-resistant Staphylococcus aureus. Journal of American Science 8, 7-12.
- Archana PR, Rao BN, Rao BSS (2011): Modulation of gamma ray-induced genotoxic effect by thymol, a monoterpene phenol derivative of cymene. Integrative Cancer Therapies 10, 374-383.
Go to original source...
Go to PubMed...
- Bassole IHN, Juliani HR (2012): Essential oils in combinations and their antimicrobial properties. Molecules 17, 3989-4006.
Go to original source...
Go to PubMed...
- Bassole IHN, Lamien-Meda A, Bayala B, Tirogo S, Franz C, Novak J, Nebie RC, Dicrko MH (2010): Composition and antimicrobial activities of Lippia multiflora Moldenke, Mentha × piperita L. and Ocimum basilicum L. essential oils and their major monoterpene alcohols alone and in combination. Molecules 15, 7825-7839.
Go to original source...
Go to PubMed...
- Bendahoua M, Muselli A, Grignon-Dubois M, Benyoucef M, Desjobert JM, Bernardini AF, Costa J (2008): Antimicrobial activity and chemical composition of Origanum glandulosum Desf. essential oil and extract obtained by microwave extraction: Comparison with hydrodistillation. Food Chemistry 106, 132-139.
Go to original source...
- Binutu OA, Cordell GA (2000): Gallic acid derivatives from Mezoneuron benthamianum leaves. Pharmaceutical Biology 38, 284-286.
Go to original source...
Go to PubMed...
- Brewer MS (2011): Natural antioxidants: sources, compounds, mechanisms of action, and potential applications. Comprehensive Reviews in Food Science and Food Safety 10, 221-247.
Go to original source...
- Burt SA, Vlielander R, Haagsman HP, Veldhuizen EJA (2005): Increase in activity of essential oil components carvacrol and thymol against Escherichia coli O157:H7 by addition of food stabilizers. Journal of Food Protection 68, 919-926.
Go to original source...
Go to PubMed...
- Choi JG, Kang OH, Lee YS, Oh YC, Chae HS, Jang HJ, Shin DW, Kwon DY (2009): Antibacterial activity of methyl gallate isolated from galla rhois or carvacrol combined with nalidixic acid against nalidixic acid resistant bacteria. Molecules 14, 1773-1780.
Go to original source...
Go to PubMed...
- Choi JG, Kang OH, Lee YS, Oh YC, Chae HS, Jang HJ, Kim JH, Sohn DH, Shin DW, Park H, Kwon DY (2008): In vitro activity of methyl gallate isolated from galla rhois alone and in combination with ciprofloxacin against clinical isolates of salmonella. Journal of Microbiology and Biotechnology 18, 1848-1852.
Go to original source...
Go to PubMed...
- Chusri S, Voravuthikunchai SP (2011): Damage of staphylococcal cytoplasmic membrane by Quercus infectoria G. Olivier and its components. Letters in Applied Microbiology 52, 565-572.
Go to original source...
Go to PubMed...
- Cosentino S, Tuberoso CIG, Pisano B, Satta M, Mascia V, Arzedi E, Palmas F (1999): In-vitro antimicrobial activity and chemical composition of Sardinian Thymus essential oils. Letters in Applied Microbiology 29, 130-135.
Go to original source...
Go to PubMed...
- Cristani M, D'Arrigo M, Mandalari G, Castelli F, Sarpietro MG, Micieli D, Venuti V, Bisignano G, Saija A, Trombetta D (2007): Interaction of four monoterpenes contained in essential oils with model membranes: Implications for their antibacterial activity. Journal of Agricultural and Food Chemistry 55, 6300-6308.
Go to original source...
Go to PubMed...
- Daneshfar A, Ghaziaskar HS, Homayoun N (2008): Solubility of gallic acid in methanol, ethanol, water and ethyl acetate. Journal of Chemical and Engineering Data 53, 776-778.
Go to original source...
- Darvishi M, Omidi M, Bushehri AK, Golshani A, Smith ML (2013): Thymol antifungal mode of action involves telomerase inhibition. Medical Mycology 51, 826-834.
Go to original source...
Go to PubMed...
- Demirci B, Kosar M, Demirci F, Dinc M, Baser KHC (2007) Antimicrobial and antioxidant activities of the essential oil of Chaerophyllum libanoticum Boiss. et Kotschy. Food Chemistry 105, 1512-1517.
Go to original source...
- Devi KP, Nisha SA, Sakthivel R, Pandian SK (2010): Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. Journal of Ethnopharmacology 130, 107-115.
Go to original source...
Go to PubMed...
- Didry N, Dubreuil L, Pinkas M (1993): Antibacterial activity of thymol, karvakrol and cinnamaldehyde alone or in combination. Die Pharmazie 48, 301-304.
Go to PubMed...
- Dorman HJD, Deans SG (2000): Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology 88, 308-316.
Go to original source...
Go to PubMed...
- Elissondo MC, Albani CM, Gende L, Equaras M, Denegri G (2008): Efficacy of thymol against Echinococcus granulosus protoscoleces. Parasitology International 57, 185-190.
Go to original source...
Go to PubMed...
- Farag RS, Daw ZY, Abo-Raya SH (1989): Influence of some spice essential oils on Aspergillus parasiticus growth and production of aflatoxins in a synthetic medium. Journal of Food Science 54, 74-76.
Go to original source...
- Garcia-Garcia R, Lopez-Malo A, Palou E (2011): Bactericidal action of binary and ternary mixtures of carvacrol, thymol, and eugenol against Listeria innocua. Journal of Food Science 76, 95-100.
Go to original source...
Go to PubMed...
- Giweli A, Dzamic AM, Sokovic M, Ristic MS, Marin PD (2012): Antimicrobial and antioxidant activities of essential oils of Satureja thymbra growing wild in Libya. Molecules 17, 4836-4850.
Go to original source...
Go to PubMed...
- Goren AC, Topcu G, Bilsel G, Bilsel M, Wilkinson JM, Cavanagh HMA (2004): Analysis of essential oil of Satureja thymbra by hydrodistillation, thermal desorber, and headspace GC/MS techniques and its antimicrobial activity. Natural Product Research 18, 189-195.
Go to original source...
Go to PubMed...
- Guarda A, Rubilar JV, Miltz J, Galotto MJ (2011): The antimicrobial activity of microencapsulated thymol and carvacrol. International Journal of Food Microbiology 146, 144-150.
Go to original source...
Go to PubMed...
- Ha TJ, Nihei KI, Kubo I (2004): Lipoxygenase inhibitory activity of octyl gallate. Journal of Agricultural and Food Chemistry 52, 3177-3187.
Go to original source...
Go to PubMed...
- Hammer KA, Heel KA (2012): Use of multiparameter flow cytometry to determine the effects of monoterpenoids and phenylpropanoids on membrane polarity and permeability in staphylococci and enterococci. International Journal of Antimicrobial Agents 40, 239-245.
Go to original source...
Go to PubMed...
- Hanbali FEL, Akssira M, Ezoubeiri A, Gadhi CEA, Melloukia F, Benherraf A, Blazquez AM, Boira H (2005): Chemical composition and antibacterial activity of essential oil of Pulicaria odora L. Journal of Ethnopharmacology 99, 399-401.
Go to original source...
Go to PubMed...
- Helander IM, Alakomi HL, Latva-Kala K, Mattila-Sandholm T, Pol I, Smid EJ, Gorris LGM, von Wright A (1998): Characterization of the action of selected essential oil components on Gram-negative bacteria. Journal of Agricultural and Food Chemistry 46, 3590-3595.
Go to original source...
- Hsu FL, Chang HT, Chang ST (2007): Evaluation of antifungal properties of octyl gallate and its synergy with cinnamaldehyde. Bioresource Technology 98, 734-738.
Go to original source...
Go to PubMed...
- Hyldgaard M, Mygind T, Meyer RL (2012): Essential oils in food preservation: Mode of action, synergies, and interactions with food matrix components. Frontiers in Microbiology 3, 1-24.
Go to original source...
Go to PubMed...
- Ivanova A, Delcheva I, Tsvetkova I, Kujumgiev A, Kostova I (2002): GC-MS analysis and anti-microbial activity of acidic fractions obtained from Paeonia peregrina and Paeonia tenuifolia Roots. Zeitschrift fur Naturforschung 57c, 624-628.
Go to original source...
Go to PubMed...
- Jacobsen C, Hartvigsen K, Lund P, Meyer AS, Adler-Nissen J, Holmer JHG (1999): Oxidation in fish-oil-enriched mayonnaise 1. Assessment of propyl gallate as an antioxidant by discriminant partial least squares regression analysis. European Food Research and Technology 210, 13-30.
Go to original source...
- Janseen AM, Chin NLJ, Scheffer JJC, Svendsen AB (1986): Screening for antimicrobial activity of some essential oils by the agar overlay technique. Pharmaceutisch Weekblad 8, 289-292.
Go to original source...
Go to PubMed...
- Johnstone DB, Little JE (1953): Bacteriostatic, bactericidal, and drug resistance studies of ethyl gallate on Mycobacterium tuberculosis. Journal of Bacteriology 66, 320-323.
Go to original source...
Go to PubMed...
- Joshi RK (2013): Chemical composition, in vitro antimicrobial and antioxidant activities of the essential oils of Ocimum gratissimum, O. sanctum and their major constituents. Indian Journal of Pharmaceutical Sciences 75, 457-462.
Go to original source...
Go to PubMed...
- Kalemba D, Kunicka A (2003): Antibacterial and antifungal properties of essential oils. Current Medicinal Chemistry 10, 813-829.
Go to original source...
Go to PubMed...
- Kane CJ, Menna JH, Sung CC, Yeh, YC (1988): Methyl gallate, methyl-3,4,5-trihydoxybenzoate, is a potent and highly specific inhibitor of herpes simplex virus in vitro. II. Antiviral activity of methyl gallate and its derivatives. Bioscience Reports 8, 95-102.
Go to original source...
Go to PubMed...
- Kang MS, OH JS, Kang ICH, Hong SJ, Choi CHH (2008): Inhibitory effect of methyl gallate and gallic acid on oral bacteria. Journal of Microbiology 46, 744-750.
Go to original source...
Go to PubMed...
- Kim TJ, Silva JL, Jung YS (2011): Enhanced functional properties of tannic acid after thermal hydrolysis. Food Chemistry 126, 116-120.
Go to original source...
- Kubo I, Fujita KI, Nihei KI (2002): Anti-salmonella activity of alkyl gallates. Journal of Agricultural and Food Chemistry 50, 6692-6696.
Go to original source...
Go to PubMed...
- Kubo I, Fujita KI, Nihei KI, Nihei T (2004): Antibacterial activity of alkyl gallates against Bacillus subtilis. Journal of Agricultural and Food Chemistry 52, 1072-1076.
Go to original source...
Go to PubMed...
- Kubo I, Masuoka N, Ha TJ, Shimizu K, Nihei KI (2010): Multifunctional antioxidant activities of alkyl gallates. Open Bioactive Compounds Journal 3, 1-11.
Go to original source...
- Kubo I, Xiao P, Fujita K (2001): Antifungal activity of octyl gallate: Structural criteria and mode of action. Bioorganic and Medicinal Chemistry Letters 11, 347-350.
Go to original source...
Go to PubMed...
- Lambert RJW, Skandamis PN, Coote PJ, Nychas GJE (2001): A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. Journal of Applied Microbiology 92, 453-462.
Go to original source...
Go to PubMed...
- Lee SP, Buber MT, Yang Q, Cerne R, Cortes RY, Sprous DG, Bryant RW (2008): Thymol and related alkyl phenols activate the hTRPA1 channel. British Journal of Pharmacology, 153, 1739-1749.
Go to original source...
Go to PubMed...
- Lu LL, Lu XY (2007): Solubilities of gallic acid and its esters in water. Journal of Chemical and Engineering Data 52, 37-39.
Go to original source...
- Medina E, Brenes M, Garcia A, Romero C, De Castro A. (2009): Bactericidal activity of glutaraldehyde-like compounds from olive products. Journal of Food Protection, 72, 2611-2614.
Go to original source...
Go to PubMed...
- Miller D, Hawthorne SB (2000): Solubility of liquid organic flavor and fragrance compounds in subcritical (hot/liquid) water from 298 K to 473 K. Journal of Chemical and Engineering Data 45, 315-318.
Go to original source...
- Nohynek LJ, Alakomi HL, Kahkonen MP, Heinonen M, Helander IM, Oksman-Caldentey KM, Puupponen-Pimia RH (2006): Berry phenolics: Antimicrobial properties and mechanisms of action against severe human pathogens. Nutrition and Cancer 54, 18-32.
Go to original source...
Go to PubMed...
- Ow YY, Stupans I (2003): Gallic acid and gallic acid derivatives: Effects on drug metabolizing enzymes. Current Drug Metabolism 4, 241-248.
Go to original source...
Go to PubMed...
- Oyedemi SO, Okoh AI, Mabinya LV, Pirochenva G, Afolayan AJ (2009): The proposed mechanism of bactericidal action of eugenol, α-terpineol and γ-terpinene against Listeria monocytogenes, Streptococcus pyogenes, Proteus vulgaris and Escherichia coli. African Journal of Biotechnology 8, 1280-1286.
- Ozcelik B, Kartal M, Orhan I (2011): Cytotoxicity, antiviral and antimicrobial activities of alkaloids, flavonoids, and phenolic acids. Pharmaceutical Biology 49, 396-602.
Go to original source...
Go to PubMed...
- Palaniappan K, Holley RA (2010): Use of natural antimicrobials to increase antibiotic susceptibility of drug resistant bacteria. International Journal of Food Microbiology 140, 164-168.
Go to original source...
Go to PubMed...
- Perrin C, Meyer L (2002): Quantification of synthetic phenolic antioxidants in dry foods by reversed-phase HPLC with photodiode array detection. Food Chemistry 77, 93-100.
Go to original source...
- Rangel LP, Fritzen M, Yunes RA, Leal PC, Creczynski-Pasa TB, Ferreira-Pereira A (2010): Inhibitory effects of gallic acid ester derivatives on Saccharomyces cerevisiae multidrug resistance protein Pdr5p. FEMS Yeast Research 10, 244-251.
Go to original source...
Go to PubMed...
- Rua J, Fernandez-Alvarez L, de Castro C, Del Valle P, de Arriaga D, Garcia-Armesto MR (2011): Antibacterial activity against foodborne Staphylococcus aureus and antioxidant capacity of various pure phenolic compounds. Foodborne Pathogens and Disease 8, 149-157.
Go to original source...
Go to PubMed...
- Sharma OP, Bhat TK (2009): DPPH antioxidant assay revisited. Food Chemistry 113, 1202-1205.
Go to original source...
- Shibata H, Kondo K, Katsuyama R, Kawazoe K, Sato Y, Murakami K, Takaishi Y, Arakaki N, Higuti T (2005): Alkyl gallates, intensifiers of β-lactam susceptibility in methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 49, 549-555.
Go to original source...
Go to PubMed...
- Silva NCC, Fernandes JA (2010): Biological properties of medicinal plants: a review of their antimicrobial activity. Journal of Venomous Animals and Toxins including Tropical Diseases 16, 402-413.
Go to original source...
- Sisak F, Havlickova H, Hradecka H, Rychlik I, Kolackova I, Karpiskova R (2006): Antibiotic resistance of Salmonella spp. isolates from pigs in the Czech Republic. Veterinarni Medicina 51, 303-310.
Go to original source...
- Solorzano-Santos F, Miranda-Novales, MG (2012): Essential oils from aromatic herbs as antimicrobial agents. Current Opinion in Biotechnology 23, 136-141.
Go to original source...
Go to PubMed...
- Strlic M, Radovic T, Kolar J, Pihlar B (2002). Anti- and prooxidative properties of gallic acid in fenton-type systems. Journal of Agricultural and Food Chemistry 50, 6313-6317.
Go to original source...
Go to PubMed...
- Takai E, Hirano A, Shiraki K (2011): Effects of alkyl chain length on self-association and membrane binding. Journal of Biochemistry 150, 165-171.
Go to original source...
Go to PubMed...
- Tippayatum P, Chonhenchob V (2007): Antibacterial activities of thymol, eugenol, and nisin against some food spoilage bacteria. Kasetsart Journal, Natural Science 41, 319-323.
- Trombetta D, Castelli F, Sarpietro MG, Venuti V, Cristani M, Daniele C, Saija A, Mazzanti G, Bisignano G (2005): Mechanism of antibacterial action of three monoterpenes. Antimicrobial Agents and Chemotherapy 49, 2474-2478.
Go to original source...
Go to PubMed...
- Ultee A, Slump RA, Steging G, Smid EJ (2000): Antimicrobial activity of carvacrol towards Bacillus cereus on rice. Journal of Food Protection 63, 620-624.
Go to original source...
Go to PubMed...
- Uozaki M, Yamasaki H, Katsuyama Y, Higuchi M, Higuti T, Koyama AH (2007): Antiviral effect of octyl gallate against DNA and RNA viruses. Antiviral Research 73, 85-91.
Go to original source...
Go to PubMed...
- Vardar-Unlu G, Candan F, Sokmen A, Daferera D, Polissiou M, Sokmen M, Donmez E, Tepe B (2003): Antimicrobial and antioxidant activity of the essential oil and methanol extracts of Thymus pectinatus Fisch. et Mey. var. pectinatus (Lamiaceae). Journal of Agricultural and Food Chemistry 51, 63-67.
Go to original source...
Go to PubMed...
- Veldhuizen EJA, Tjeerdsma-Van Bokhoven JM, Zweijtzer C, Burt SA, Haagsman HP (2006): Structural Requirements for the Antimicrobial Activity of Carvacrol. Journal of Agricultural and Food Chemistry 54, 1874-1879.
Go to original source...
Go to PubMed...
- Vondruskova H, Slamova R, Trckova M, Zraly Z, Pavlik I (2010): Alternatives to antibiotic growth promoters in prevention of diarrhoea in weaned piglets: a review. Veterinarni Medicina 55, 199-224.
Go to original source...
- Walsh SE, Maillard JY, Russell AD, Catrenich CE, Charbonneau DL, Bartolo RG (2003): Activity and mechanisms of action of selected biocidal agents on Gram-positive and -negative bacteria. Journal of Applied Microbiology 94, 240-247.
Go to original source...
Go to PubMed...
- Wattanasatcha A, Rengpipat S, Wanichwecharungruang S (2012): Thymol nanospheres as an effective anti-bacterial agent. International Journal of Pharmaceutics 434, 360-365.
Go to original source...
Go to PubMed...
- Xu J, Zhou F, Ji BP, Pei RS, Xu N (2008): The antibacterial mechanism of carvacrol and thymol against Escherichia coli. Letters in Applied Microbiology 47, 174-179.
Go to original source...
Go to PubMed...
- Zarrini G, Delgosha ZB, Moghaddam MK, Shahverdi AR (2010): Post-antibacterial effect of thymol. Pharmaceutical Biology 48, 633-636.
Go to original source...
Go to PubMed...
- Zhou L, Wang LD, Liu Y, Wu J (2007): Antibacterial phenolic compounds from the spines of Gleditsia sinensis Lam. Natural Product Research 21, 283-291.
Go to original source...
Go to PubMed...
This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.