The antimicrobial effect of a novel flavonoid (7- O-butylnaringenin) on Helicobacter pylori 26695, 51, and SS1 strains and its inhibitory effect on the urease activity of the strains were evaluated and compared with those of several natural flavonoids. First, various flavonoids were screened for antimicrobial activities using the paper disc diffusion method. Hesperetin and naringenin showed the strongest antimicrobial effects among the natural flavonoids tested, and thus hesperetin and naringenin were selected for comparison with 7- O-butylnaringenin. The antimicrobial effect of 7- O-butylnaringenin was greater than that of the hesperetin and naringenin. H. pylori 51 was more sensitive to 7- O-butylnaringenin (2 log reduction of colony forming units, p < 0.05) than the other two strains at 200 μM. 7- O-Butylnaringenin also showed the highest inhibitory effect against urease activity of H. pylori. Morphological changes of H. pylori 26695 treated with these flavonoids indicated that both hesperetin and 7- O-butylnaringenin at 200 μM damaged the cell membranes.
References
[1]
Marshall, B.J. Campylobacter pyloridis and gastritis. J. Infect. Dis. 1986, 153, 650–657, doi:10.1093/infdis/153.4.650.
[2]
Fukai, T.; Marumo, A.; Kaitou, K.; Kanda, T.; Terada, S.; Nomura, T. Anti-Helicobacter pylori flavonoids from licorice extract. Life Sci. 2002, 71, 1449–1463.
[3]
Jiang, X.; Doyle, M.P. Optimizing enrichment culture conditions for detecting Helicobacter pylori in foods. J. Food Prot. 2002, 65, 1949–1954.
[4]
Smith, J.L. The role of gastric acid in preventing foodborne disease and how bacteria overcome acid conditions. J. Food Prot. 2003, 66, 1292–1303.
[5]
Stamatis, G.; Kyriazopoulos, P.; Golegou, S.; Basayiannis, A.; Skaltsas, S.; Skaltsa, H. In vitro anti-Helicobacter pylori activity of Greek herbal medicines. J. Ethnopharmacol. 2003, 88, 175–179.
[6]
Shin, J.E.; Kim, J.M.; Bae, E.A.; Hyun, Y.J.; Kim, D.H. In vitro inhibitory effects of flavonoids on growth, infection and vacuolation of Helicobacter pylori. Planta Med. 2005, 71, 197–201.
[7]
Stingel, K.; Reuse, H.D. Staying alive overdose: How does Helicobacter pylori control urease activity? Int. J. Med. Microbiol. 2005, 295, 307–315.
[8]
Hazell, S.L.; Lee, A. Campylobacter pyloridis, urease, hydrogen ion back diffusion and gastric ulcers. Lancet 1986, 5, 15–17, doi:10.1016/S0140-6736(86)92561-4.
[9]
Hazell, S.L.; Borody, T.J.; Lee, A. Campylobacter pyloridis gastritis. I: Detection of urease as a marker of bacterial colonization and gastritis. Am. J. Gastroenterol. 1987, 82, 292–296.
[10]
Muhammad, A.; Farooq, A.; Muhammad, R.J.; Muhammad, A.I.; Umer, R. Green synthesis of silver nanoparticles through reduction with Solanum xanthocarpum L. Berry extract: Characterization, antimicrobial and urease inhibitory activities against Helicobacter pylori. Int. J. Mol. Sci. 2012, 13, 9923–9941.
[11]
Jiang, X.; Doyle, M.P. Effect of environmental and substrate factors on survival and growth of Helicobacter pylori. J. Food Prot. 1998, 61, 929–933.
[12]
Nicoline, F.T.; Lucy, M.N.; Roland, N.N. DNA sequence analysis of South African Helicobacter pylori vacuolating cytotoxin gene (vacA). Int. J. Mol. Sci. 2011, 12, 7459–7468.
[13]
Masuda, H.; Naohide, K.; Woo, G.J.; Shin, I.S. Inhibitory effects of gochoonangi (Wasabia japonica) against Helicobacter pylori and its urease activity. Food Sci. Biotechnol. 2004, 13, 191–196.
[14]
Silvia, M.; Claudia, D.A.; Andrea, C.; Silvia, F.; Francesca, B.; Annalisa, S.; Natale, F.; Claudio, R. Antimicrobial activity against Helicobacter pylori strains and antioxidant properties of blackberry leaves (Rubus ulmifolius) and isolated compounds. Int. J. Antimicrob. Agric. 2009, 34, 50–59.
[15]
Muhammad, A.; Farooq, A.; Fauqia, N.; Tahir, M.; Nazamid, S. Anti-Helicobacter pylori and urease inhibition activities of some traditional medicinal plants. Molecules 2013, 18, 2135–2149.
[16]
Stojanovic, G.; Radulovic, N.; Hashimoto, T.; Palic, R. In vitro antimicrobial activity of extracts of four Achillea species: The composition of Achillea clavennae L. (Asteraceae) extract. J. Ethnopharmacol. 2005, 101, 185–190.
[17]
Maria, H.; Concepción, S.-M.; Sonia, P.T. Flavonoid-flavonoid interaction and its effect on their antioxidant activity. Food Chem. 2010, 121, 691–696.
[18]
Bang, M.H.; Jung, Y.J.; Kim, W.K. Effect of several flavonoids on cancer cell motility in human fibrosarcoma HT 1080 cells. Food Sci. Biotechnol. 2004, 13, 739–743.
[19]
Kim, K.T.; Moon, S.H.; Yeo, E.J.; Han, Y.S.; Nah, S.Y.; Paik, H.-D. Inhibitory effect of 7-O-butyl naringenin on growth of Helicobacter pylori ATCC 26695. Food Sci. Biotechnol. 2006, 15, 466–468.
[20]
Ghaleb, A.; Bassam, A.-S.; Kamel, A. Antibacterial activities of some plant extracts alone and in combination with different antimicrobials against multidrug-resistant Pseudomonas aeruginosa strains. Asian Pac. J. Trop. Med. 2010, 3, 266–269.
[21]
Son, D.J.; Lee, S.E.; Park, B.S. Inhibitory effects of naturally occurring flavonoids on a human intestinal bacterium, Clostridium perfringens. Food Sci. Biotechnol. 2003, 12, 180–182.
[22]
Tim, C.T.P.; Lamb, A.J. Antimicrobial activity of flavonoids. Int. J. Antimicrob. Agric. 2005, 26, 343–356.
[23]
Tim, C.T.P.; Hamilton, V.E.S.; Lamb, A.J. Assessment of the antibacterial activity of selected flavonoids and consideration of discrepancies between previous reports. Microbial. Res. 2003, 158, 281–289.
[24]
Christy, E.M.L.; Clarke, A.M.; Munzhelele, T.; Ezekiel, G.; Noxolo, F.M.; Roland, N.N. Selected South African honeys and their extracts possess in vitro anti-Helicobacter pylori activity. Arch. Med. Res. 2010, 41, 324–331.
[25]
Yerra, K.R.; Lien, H.-M.; Lin, Y.H.; Hsu, Y.-M.; Yeh, C.-T.; Chen, C.C.; Lai, C.H.; Tzeng, Y.M. Antibacterial activities of Anisomeles indica constituents and their inhibition effect on Helicobacter pylori-induced inflammation in human gastric epithelial cells. Food Chem. 2012, 132, 780–787.
[26]
Kim, K.T.; Paik, H.-D. Propolis as a Multi-Functional Natural Material for Health. In Natural Products as Future Medicinal Agents; Hawthorne, S., Ed.; Transworld Research Network: Kerala, India, 2008; pp. 33–48.
[27]
Malekzadeh, F.; Ehsanifar, H.; Shahamat, M.; Levin, M.; Colwell, R.R. Antibacterial activity of black myrobalan (Terminalia chebulaetz) against Helicobacter pylori. Int. J. Antimicrob. Agric. 2001, 18, 85–88.
[28]
Mobley, H.L.T.; Cortesia, M.J.; Roseuthal, L.E.; Jones, B.D. Characterization of urease from Campylobacter pylori. J. Clin. Microbiol. 1988, 26, 831–836.
[29]
Tsugawa, H.; Suzuki, H.; Nakagawa, I.; Nishizawa, T.; Saito, Y.; Suematsu, M.; Hibi, T. Alpha-ketoglutarate oxidoreductase, an essential salvage enzyme of energy metabolism, in coccoid form of Helicobacter pylori. Biochem. Biophys. Res. Commun. 2008, 376, 46–51.
[30]
Paulo, L.; Oleastro, M.; Gallardo, E.; Queiroz, J.A.; Domi, F. Anti-Helicobacter pylori and urease inhibitory activities of resveratrol and red wine. Food Res. Int. 2011, 44, 964–969.
