In Vitro Antibacterial Activity of Flavonoid Extracts of Two Selected Libyan Algae against Multi-Drug Resistant Bacteria Isolated from Food Products

Download Download as PDF (Size:693KB)  HTML   XML  PP. 26-48  
DOI: 10.4236/jbm.2017.51003    282 Downloads   386 Views  


This study aimed to evaluate the antibacterial activity of flavonoids extracted from two Libyan brown algae namely Cystoseira compressa and Padina pavonica using microwave-assisted extraction method against pathogenic bacteria isolated from meat, meat products, milk and dairy products (Staphylococcus aureus subsp. aureus (5 isolates), Bacillus cereus (3 isolates), Bacillus pumilus (1 isolate), Salmonella enterica subsp. enteric (4 isolates) and Enterohaemor-rhagic Escherichia coli O157 (EHEC O157) (4 isolates)). All of these isolates were muti-drug resistant with high MAR index. The results showed that C. compressa extract exhibited better and stronger antibacterial activities against the seventeen tested isolates with inhibition zones diameter ranged from 14 - 22 mm compared to P. pavonica extract which showed positive effect against 9 isolates with low inhibition zone ranged from 11 - 16.5 mm. Flavonoids extracted from C. compressa also displayed the best spectrum of bactericidal effect with a ratio MBC/MIC ≤ 4 obtained on all susceptible tested bacterial strains. Flavonoids and proanthocyanidins significantly contributed to the antibacterial properties. The mode of action of these active extracts is under investigation.

Cite this paper

Alghazeer, R. , Elmansori, A. , Sidati, M. , Gammoudi, F. , Azwai, S. , Naas, H. , Garbaj, A. and Eldaghayes, I. (2017) In Vitro Antibacterial Activity of Flavonoid Extracts of Two Selected Libyan Algae against Multi-Drug Resistant Bacteria Isolated from Food Products. Journal of Biosciences and Medicines, 5, 26-48. doi: 10.4236/jbm.2017.51003.


[1] Rodrigues, E., Tilvi, S. and Naik, C.G. (2004) Antimicrobial Activity of Marine Organisms Collected off the Coast of East India. Journal of Experimental Marine Biology and Ecology, 309, 121-127.
[2] Cabrita, M., Vale, C. and Rauter, A. (2010) Halogenated Compounds from Marine Algae. Marine Drugs, 8, 2301-2317.
[3] Molinski, T.F., Dalisay, D.S., Lievens, S.L. and Saludes, J.P. (2009) Drug Development from Marine Natural Products. Nature Reviews Drug Discovery, 28, 69-85.
[4] Mayer, A.M.S., Glaser, K.B., Cuevas, C., Jacobs, R.S., Kem, W., Little, R.D., McIntosh, J.M., Newman, D.J., Potts, B.C. and Shuster, D.E. (2010) The Odyssey of Marine Pharmaceuticals: A Current Pipeline Perspective. Trends in Pharmacological Sciences, 31, 255-265.
[5] Colla, L.M., Reinehr, C.O., Reichert, C.J. and Costa, A.V. (2007) Production of Biomass and Nutraceutical Compounds by Spirulina platensis under Different Temperature and Nitrogen Regimes. Bioresource Technology, 98, 1489-1493.
[6] Ross, J. and Kasum, C. (2002) Dietary Flavonoids: Bioavailability, Metabolic Effects and Safety. Annual Review of Nutrition, 22, 19-34.
[7] Williams, R.J., Spencer, J.P. and Rice-Evans, C. (2004) Flavonoids: Antioxidants or Signalling Molecules. Free Radical Biology & Medicine, 36, 838-849.
[8] Cushnie, T.P.T. and Lamb, A.J. (2005) Antimicrobial Activity of Flavonoids. International Journal of Antimicrobial Agents, 26, 343-356.
[9] Markham, K.R. (1988) Distribution of Flavonoids in the Lower Plants and Its Evolutionary Significance. In: Harborne, J.B., Ed., The Flavonoids, Advances in Research Since 1980, Academic Press, New York, 427-468.
[10] Wang, C., Wei, M., Su, J. and Zeng, L. (1998) Research on the Chemical Constituents of Acanthophora spicifera in the South China. Chinese Journal of Magnetic Resonance, 15, 237-242.
[11] Zeng, L.M., Wang, C.-J., et al. (2001) Flavonoids from the Red Alga Acanthophora spicifera. Chinese Journal of Chemistry, 19, 1097-1100.
[12] Sabina, H. and Aliya, R. (2009) Seaweed as a New Source of Flavone, Scutellarein 4’-Methyl ether. Pakistan Journal of Botany, 41, 1927-1930.
[13] Masaru, K., Toyoda, M., Teshima, R., Sasada, J., Hayashi, T., Artsawa, M., Shimizu, M., Morita, N., Inoue, S. and Saito, Y. (1994) In Vitro Antiallergic Activity of Flavonoids in Histamine Release Assay Using Rat Basophilic Leukemia (RBL-2H3) Cells. Journal of the Food Hygienic Society of Japan, 35, 497-503.
[14] Shan, X.U., Li, L., Liqun, Z., Zhuo, L., Lili, Q., Qi, C. and Changfen, X. (2006) Reversale Effect of 4’-Methylether-Scutellarein on Multidrug Resistance of Human Choriocarcinoma JAR/VP 16 Cell Line. Progress in Biochemistry and Biophysics, 33, 1061-1073.
[15] Bicchi, C., Drigo, S. and Rubiolo, P. (2000) Influence of Fiber Coating in Headspace Solid-Phase Microextraction-Gas Chromatographic Analysis of Aromatic and Medicinal Plants. Journal of Chromatography A, 892, 469-485.
[16] Tuney, I., Cadirci, B.H., Unal, D. and Sukatar, A. (2010) Antimicrobial Activities of the Extracts of Marine Algae from the Coast of Urla (Izmir, Turkey). Turkish Journal of Biology, 30, 171-175.
[17] Tiwari, P., Kumar, B., Kaur, M., Kaur, G. and Kaur, H. (2011) Phytochemical Screening and Extraction: A Review. Internationale Pharmaceutica Sciencia, 1, 98- 106.
[18] Kaufmann, B. and Christen, P. (2002) Recent Extraction Techniques for Natural Products: Microwave-Assisted Extraction and Pressurised Solvent Extraction. Phytochemical Analysis, 13, 105-113.
[19] Ioannou, I. and Ghoul, M. (2012) Biological Activities and Effects of Food Processing on Flavonoids as Phenolic Antioxidants. In: Petre, M., Ed., Advances in Applied Biotechnology, Chapter 5, InTech, 101-124.
[20] Palaniappan, K. and Holley, R.A. (2010) Use of Natural Antimicrobials to Increase Antibiotic Susceptibility of Drug Resistant Bacteria. International Journal of Food Microbiology, 140, 164-168.
[21] Bansemir, A., Blume, M., Schroder, S. and Lindequist, U. (2006) Screening of Cultivated Seaweeds for Antibacterial Activity against Fish Pathogenic Bacteria. Aquaculture, 252, 79-84.
[22] Kuda, T., Kunii, T., Goto, H., Suzuki, T. and Yano, T. (2007) Varieties of Antioxidant and Antibacterial Properties of Ecklonia stolonifera and Ecklonia kurome Products Harvested and Processed in the Noto Peninsula, Japan. Food Chemistry, 103, 900-905.
[23] Shanmughapriya, S., Manilal, A., Sujith, S., Selvin, J., Kiran, G. and Seenivasan, K. (2008) Antimicrobial Activity of Seaweeds Extracts against Multi Resistant Pathogens. Annals of Microbiology, 58, 535-541.
[24] Alghazeer, R., Whida, F., Abduelrhman, E., Gammoudi, F. and Azwai, S. (2013) Screening of Antibacterial Activity in Marine Green, Red and Brown Macroalgae from the Western Coast of Libya. Natural Science, 5, 7-14.
[25] Cowan, M.M. (1999) Plant Products as Antimicrobial Agents. Clinical Microbiology Reviews, 12, 564-582.
[26] Yee, Y.K. and Koo, M.W.L. (2000) Anti-Helicobacter Pylori Activity of Chinese Tea: In Vitro Study. Alimentary Pharmacology and Therapeutics, 14, 635-638.
[27] Odebiyi, A. and Sofowora, A.E. (1990) Phytochemical Screening of Nigerian Medicinal Plants. Part III. Lloydia, 41, 234-246.
[28] Quan, P.T., Hang, T.V., Ha, N.H., De, N.X. and Tuyen, T.N. (2006) Microwave- Assisted Extraction of Polyphenols from Fresh Tea Shoot. Science and Technology Development, 9, 69-75.
[29] Naas, T., Oxacelay, C. and Nordmann, P. (2007) Identification of CTX-M-Type Extended-Spectrum-Beta-Lactamase Genes Using Real-Time PCR and Pyrosequencing. Antimicrobial Agents and Chemotherapy, 51, 223-230.
[30] Garabaj, A.M., Naas, H.T., Azwai, S.M. and Gammoudi, F.T. (2007) Incidence of Staphylococci with Special Reference to Staphylococcus aureus in Two Types of Locally Processed Soft Cheese in Tripoli, Libya. Benha Veterinary Medical Journal, 18, 139-147.
[31] Azwai, S., Alfallani, E., Abdulaziz, A., Abolghait, S., Garbaj, A., Naas, H., Moawad, A., Gammoudi, F., Rayes, H., Barbieri, I. and Eldaghayes, I. (2016) Isolation and Molecular Identification of Vibrio spp. by Sequencing of 16S rDNA from Seafood, Meat and Meat Products in Libya. Open Veterinary Journal, 6, 36-42.
[32] CLSI (2012) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grows Aerobically. Approved Standard, 9th Edition, CLSI Document MO7- A9, Clinical and Laboratory Standards Institute, Wayne.
[33] NCCLS (National Committee for Clinical Laboratory Standard) (2003) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. Approved Standard, NCCLS DocumentM7-A6, Wayne.
[34] Hinton, M. and Linton, A. (1983) Antibacterial Drug Resistance among Escherichia coli Isolated from Calves Fed Milk Substitute. Veterinary Record, 112, 567-568.
[35] Saravanakumar, A., Amutha, P., Gandhimathi, R. and Dhanapal, R. (2009) Study on Phytochemical Profile and Antiepileptic Activity of Inner Bark of Guettarda speciosa (L.). Iranian Journal of Pharmacology &Therapeutics, 8, 73-76.
[36] Pundir, R.K. and Bishnoi, S. (2011) Antimicrobial Activity of Mitragyna parvifolia Barks and Butea monosperma Leaves Extracts against Human Pathogenic Microbial Strains. International Journal of Drug Development & Research, 3, 141-147.
[37] Zhishen, J., Mengcheng, T. and Jianming, W. (1999) The Determination of Flavonoid Contents in Mulberry and Their Scavenging Effects on Superoxide Radicals. Food Chemistry, 64, 555-559.
[38] Li, Y., Guo, C., Yang, J., Wei, J., Xu, J. and Cheng, S. (2006) Evaluation of Antioxidant Properties of Pomegranate peel Extract in Comparison with Pomegranate pulp Extract. Food Chemistry, 96, 254-260.
[39] Krumperman, P.H. (1985) Multiple Antibiotic Indexing of E. coli to Identify High Risk Sources of Fecal Contamination of Foods. Applied and Environmental Microbiology, 46, 165-170.
[40] Lushniak, B.D. (2014) Antibiotic Resistance: A Public Health Crisis. Public Health Report, 129, 314-316.
[41] Cox, S., Abu-Ghannam, N. and Gupta, S. (2010) An Assessment of the Antioxidant and Antimicrobial Activity of Six Species of Edible Irish Seaweeds. International Food Research Journal, 17, 205-220.
[42] Seenivasan, R., Indu, H., Archana, G. and Geetha, S. (2010) The Antibacterial Activity of Some Marine Algae from South East Coast of India. Journal of Pharmacy Research, 3, 1907-1912.
[43] Yumiko, Y.S., Yaa-Pei, H. and Takeshi, S. (2003) Distribution of Flavonoids and Related Compounds from Seaweeds in Japan. Journal of Tokyo University of Fisheries, 89, 1-6.
[44] Alghazeer, R., Ibrahim, A., Abdulaziz, A. and Abouamer, K. (2016) In-Vitro Antioxidant Activity of Five Selected Species of Libyan Algae. International Journal of Medicine and Pharmaceutical Research, 4, 1-9.
[45] Tatke, P. and Jaiswal, Y. (2011) An Overview of Microwave Assisted Extraction and Its Applications in Herbal Drug Research. Research Journal of Medicinal Plant, 5, 21-31.
[46] Alghazeer, R., Whida, F., Al-Najjar, A., Majdoob, H. and Al-Mazoghi, E. (2008) Assessment of Antioxidant Activity and Phenolic Content of Some Marine Algae from the Libyan Coast. Ain Shams Science Bulletin, 46, 67-78.
[47] Bachi, B.B. (2002) Resistance Mechanisms of Gram Positive Bacteria. International Journal of Medical Microbiology, 292, 27-35.
[48] Nagi, A.A.H., Mashan, N.I., Shamsudin, M.N., Mohamad, H. and Vairappan, C.S. (2010) Antibacterial Activity of Marine Source Extracts against Multidrug Resistance Organisms. American Journal of Pharmacology and Toxicology, 5, 95-102.
[49] Didic, S., Suskovic, J. and Kos, B. (2008) Antibiotic Resistance Mechanisms in Bacteria: Biochemical and Genetic Aspects. Food Technology and Biotechnology, 46, 11-21.
[50] Hellio, C., De La Broise, D., Dufosse, L., Le Gal, Y. and Bourgougnon, N. (2001) Inhibition of Marine Bacteria by Extracts of Macroalgae: Potential Use for Environmentally Friendly Antifouling Paints. Marine Environmental Research, 52, 231-247.
[51] Dubber, D. and Harder, T. (2008) Extracts of Ceramium rubrum, Mastocarpus stellatus and Laminaria digitata Inhibit Growth of Marine and Fish Pathogenic Bacteria at Ecologically Realistic Concentrations. Aquaculture, 274, 196-200.
[52] Nakamura, C.V., Ueda-Nakamura, T., Bando, E., Melo, A.F., Cortez, D.A. and Dias Filho, B.P. (1999) Antibacterial Activity of Ocimum gratissimum L. Essential Oil. Memórias do Instituto Oswaldo Cruz, 94, 675-678.
[53] Noumedem, J., Mihasan, M., Lacmata, S., Stefan, M., Kuiate, J. and Kuete, V. (2013) Antibacterial Activities of the Methanol Extracts of Ten Cameroonian Vegetables against Gram-Negative Multidrug-Resistant Bacteria. BMC Complementary and Alternative Medicine, 17, 13-26.
[54] Cushnie, T.P.T. and Lamb, A.J. (2005) Detection of Galangin-Induced Cytoplasmic Membrane Damage in Staphylococcus aureus by Measuring Potassium Loss. Journal of Ethnopharmacology, 101, 243-248.
[55] Marijana, K., Branislav, R. and Tatjana, S. (2015) Biological Potential of Marine Macroalgae of the Genus Cystoseira. Acta Biologica Hungarica, 66, 374-384.
[56] Mandalari, G., Bennett, R.N., Bisignano, G., Trombetta, D., Saija, A., Faulds, C.B., Gasson, M.J. and Narbad, A. (2007) Antimicrobial Activity of Flavonoids Extracted from Bergamot (Citrus bergamia Risso) Peel. A Byproduct of the Essential Oil Industry. Journal of Applied Microbiology, 103, 2056-2064.
[57] Heijenoort, J. (2001) Formation of the Glycan Chains in the Synthesis of Bacterial Peptidoglycan. Glycobiology, 11, 25-36.
[58] Kosanic, M., Rankovic, B. and Stanojkovic, T. (2012) Antioxidant, Antimicrobial and Anticancer Activity of 3 Umbilicaria Species. Journal of Food Science, 77, 20- 25.
[59] Rahman, M. and Moon, S. (2007) Antimicrobial Phenolic Derivatives from Dendranthema zawadskii var. latilobum kitamura (Asteraceae). Archives of Pharmacal Research, 30, 1374-1379.
[60] Ayaz, F., HayIrlIoglu-Ayaz, S., Alpay-Karaoglu, S., Gruz, J., Valentová, K., Ulrichová, J. and Strnad, M. (2008) Phenolic Acid Contents of Kale (Brassica oleraceae L. var. acephala DC.) Extracts and Their Antioxidant and Antibacterial Activities. Food Chemistry, 107, 19-25.
[61] Rudi, H., Syahida, A., Aspollah, S.M., Yunus, S. and Ehsan, O. (2011) Flavonoid Analyses and Antimicrobial Activity of Various Parts of Phaleria macrocarpa (Scheff.) Boerl Fruit. International Journal of Molecular Sciences, 12, 3422-3431.
[62] Lou, Z., Wang, H., Zhu, S., Ma, C. and Wang, Z. (2011) Antibacterial Activity and Mechanism of Action of Chlorogenic Acid. Journal of Food Science, 76, 398-403.
[63] Farzaneh, V. and Carvalho, I.S. (2015) A Review of the Health Benefit Potentials of Herbal Plant Infusions and Their Mechanisms of Actions. Industrial Crops and Products, 65, 247-258.
[64] Xie, Y., Yang, W., Tang, F., Chen, X. and Ren, L. (2015) Antibacterial Activities of Flavonoids: Structure-Activity Relationship and Mechanism. Current Medicinal Chemistry, 22, 132-149.
[65] Prawat, U., Chairerk, O., Phupornprasert, U., Salae, A.W. and Tuntiwachwuttikul, P. (2013) Two New C-Benzylated Dihydrochalcone Derivatives from the Leaves of Melodorum siamensis. Planta Medica, 79, 83-86.
[66] Rashid, F., Mahmood, A., Ifzal, R. and Malik, A. (2013) Flavonoids of Prunus armeniaca and Their Antibacterial Studies. Journal of the Chemical Society of Pakistan, 35, 905-910.
[67] Sohn, H.Y., Son, K.H., Kwon, C.S., Kwon, G.S. and Kang, S.S. (2004) Antimicrobial and Cytotoxic Activity of 18 Prenylated Flavonoids Isolated from Medicinal Plants: Morus alba L., Morus mongolica Schneider, Broussnetia papyrifera (L.) Vent, Sophora flavescens Ait and Echinosophora koreensis Nakai. Phytomedicine, 11, 666- 672.
[68] Al-Habib, A., Al-Saleh, E., Safer, A.M. and Afzal, M. (2010) Bactericidal Effect of Grape Seed Extract on Methicillin-Resistant Staphylococcus aureus (MRSA). Journal of Toxicological Sciences, 35, 364-375.
[69] Gupta, A., Dwivedi, M., Mahdi, A., Nagana Gowda, G.A., Khetrapal, C. and Bhandari, M. (2012) Inhibition of Adherence of Multi-Drug Resistant E. coli by Proa Nthocyanidin. Urological Research, 40, 143-150.
[70] Ulanowska, K., Tkaczyk, A., Konopa, G. and Wegrzyn, G. (2006) Differential Antibacterial Activity of Genistein Arising from Global Inhibition of DNA, RNA and Protein Synthesis in some Bacterial Strains. Archives of Microbiology, 184, 271-278.
[71] Eumkeb, G. and Chukrathok, S. (2013) Synergistic Activity and Mechanism of Action of Ceftazidime and Apigenin Combination against Ceftazidime-Resistant Enterobacter cloacae. Phytomedicine, 20, 262-269.
[72] Cushnie, T.P.T. and Lamb, A.J. (2011) Recent Advances in Understanding the Antibacterial Properties of Flavonoids. International Journal of Antimicrobial Agents, 38, 99-107.

comments powered by Disqus

Copyright © 2017 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.