Antibacterial activities of almond skins on cagA-positive and-negative clinical isolates of Helicobacter pylori

BMC Microbiology

Giuseppina Mandalari²  Maria Teresa Fera¹  Sebastiana Zummo¹  Erminia La Camera³  Angela Filocamo³  Carlo Bisignano³ 

[1] Dipartimento di Scienze Pediatriche, Ginecologiche, Microbiologiche e Biomediche, University of Messina, Policlinico Universitario, Viale Gazzi, Messina, 98125, Italy;The Model Gut, Institute of Food Research, Norwich Research Park, Colney Lane, Norwich, NR4 7UA, UK;Dipartimento di Scienze del Farmaco e Prodotti per la Salute, University of Messina, Viale Annunziata, Messina, 98100, Italy

关键词: Protocatechuic acid;    Epicathechin, Naringerin;    Almond skins;    Flavonoids;    Helicobacter pylori;   

Others  :  1143724
DOI  :  10.1186/1471-2180-13-103

 received in 2013-01-20, accepted in 2013-04-26,  发布年份 2013

【 摘 要 】

Background

Helicobacter pylori is known to be a gastric pathogen of humans. Eradication regimens for H. pylori infection have some side effects, compliance problems, relapses, and antibiotic resistance. Therefore, the need for alternative therapies for H. pylori infections is of special interest. We have previously shown that polyphenols from almond skins are active against a range of food-borne pathogens. The aim of this study was to evaluate the antibacterial effects of natural almond skins before and after simulated human digestion and the pure flavonoid compounds epicatechin, naringenin and protocatechuic acid against H. pylori.

Results

H. pylori strains were isolated from gastric biopsy samples following standard microbiology procedures. Also, cagA and vacA genes were identified using PCR. Susceptibility studies on 34 strains of H. pylori, including two reference strains (ATCC 43504, ATCC 49503), were performed by the standard agar dilution method.

Natural almond skin was the most effective compound against H. pylori (MIC range, 64 to 128 μg/ml), followed by natural skin post gastric digestion (MIC range, 128 to 512 μg/ml), and natural almond skin post gastric plus duodenal digestion (MIC range, 256 to 512 μg/ml). Amongst the pure flavonoid compounds, protocatechuic acid showed the greatest activity (MIC range, 128 to 512 μg/ml) against H. pylori strains.

Conclusions

Polyphenols from almond skins were effective in vitro against H. pylori, irrespective of genotype status and could therefore be used in combination with antibiotics as a novel strategy for antibiotic resistance.

【 授权许可】

   
2013 Bisignano et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Ferreira AC, Isomoto H, Moriyama M, Fujioka T, Machado JC, Yamaoka Y: Helicobacter and gastric malignancies. Helicobacter 2008, 13:28-34.
• [2]Kandulski A, Selgrad M, Malfertheiner P: Helicobacter pylori infection: a clinical overview. Dig Liver Dis 2008, 40:619-626.
• [3]Minami M, Ando T, Hashikawa SN, Torii K, Hasegawa T, Israel DA, Ina K, Kusugami K, Goto H, Ohta M: Effect of glycine on Helicobacter pylori in vitro. Antimicrob Agents Chemother 2004, 48:3782-3788.
• [4]Covacci A, Telford JL, Del Giudice G, Parsonnet J, Rappuoli R: Helicobacter pylori virulence and genetic geography. Science 1999, 284:1328-1333.
• [5]Atherton JC, Cao P, Peek RM Jr, Tummuru MK, Blaser MJ, Cover TL: Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration. J Biol Chem 1995, 270:17771-17777.
• [6]van Doorn LJ, Figueiredo C, Sanna R, Plaisier A, Schneeberger P, de Boer W, Quint W: Clinical relevance of the cagA, vacA, and iceA status of Helicobacter pylori. Gastroenterology 1998, 115:58-66.
• [7]Covacci A, Censini S, Bugnoli M, Petracca R, Burroni D, Macchia G, Massone A, Papini E, Xiang Z, Figura N, Rappuoli R: Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc Natl Acad Sci USA 1993, 90:5791-5795.
• [8]Akopyants NS, Clifton SW, Kersulyte D, Crabtree JE, Youree BE, Reece CA, Bukanov NO, Drazek ES, Roe BA, Berg DE: Analyses of the cag pathogenicity island of Helicobacter pylori. Mol Microbiol 1998, 28:37-53.
• [9]Peek RM Jr, Blaser MJ, Mays DJ, Forsyth MH, Cover TL, Song SY, Krishna U, Pietenpol JA: Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res 1999, 59:6124-6131.
• [10]Bagnoli F, Buti L, Tompkins L, Covacci A, Amieva MR: Helicobacter pylori CagA induces a transition from polarized top invasive phenotypes in MDCK cells. Proc Natl Acad Sci USA 2005, 102:16339-16344.
• [11]Kusters JG, van Vliet AH, Kuipers EJ: Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 2006, 19:449-490.
• [12]Graham DY: Therapy of Helicobacter pylori: current status and issues. Gastroenterology 2000, 118(Suppl 1):S2-S8.
• [13]Gerrits MM, van Vliet AH, Kuipers EJ, Kusters JG: Helicobacter pylori and antimicrobial resistance: molecular mechanisms and clinical implications. Lancet Infect Dis 2006, 6:699-709.
• [14]Bae EA, Han MJ, Kim DH: In vitro anti-Helicobacter pylori activity of some flavonoids and their metabolites. Planta Med 1999, 65:442-443.
• [15]Fukai T, Marumo A, Kaitou K, Kanda T, Tereda S, Nomura T: Anti-Helicobacter pylori flavonoids from licorice extract. Life Sci 2002, 71:1449-1463.
• [16]Nostro A, Cellini L, Di Bartolomeo S, Di Campli E, Grande R, Cannatelli MA, Marzio L, Alonzo V: Antibacterial effect of plants extracts against Helicobacter pylori. Phytother Res 2005, 19:198-202.
• [17]Shin JE, Kim JM, Bae EA, Hyun YJ, Kim DH: In vitro inhibitory effect of flavonoids on growth, infection and vacuolation of Helicobacter pylori. Planta Med 2005, 71:197-201.
• [18]Martini S, D’Addario C, Colacevich A, Focardi S, Borghini F, Santucci A, Figura N, Rossi C: Antimicrobial activity against Helicobacter pylori strains and antioxidant properties of blackberry leaves (Rubus ulmifolius) and isolated compounds. Int J Antimicrob Agents 2009, 34:50-59.
• [19]Mandalari G, Faulks RM, Rich GT, Lo Turco V, Picout DR, Lo Curto RB, Bisignano G, Dugo P, Dugo G, Waldron KW, Ellis PR, Wickham MS: Release of protein, lipid, and vitamin E from almond seeds during digestion. J Agric Food Chem 2008, 56:3409-3416.
• [20]Mandalari G, Tomaino A, Arcoraci T, Martorana M, Lo Turco V, Cacciola F, Rich GT, Bisignano C, Saija A, Dugo P, Cross KL, Parker ML, Waldron KW, Wickham MS J: Characterization of polyphenols, lipids and dietary fibre from almond skins (Amygdalus communis L.). J Food Comp Anal 2010, 23:166-174.
• [21]Mandalari G, Tomaino A, Rich GT, Lo Curto R, Arcoraci T, Martorana M, Bisignano C, Saija A, Parker ML, Waldron KW, Wickham MSJ: Polyphenol and nutrient release from skin of almonds during simulated human digestion. Food Chem 2010, 122:1083-1088.
• [22]Vuorela S, Kreander K, Karonen M, Nieminen R, Hämäläinen M, Galkin A, Laitinen L, Salminen JP, Moilanen E, Pihlaja K, Vuorela H, Vuorela P, Heinonen M: Preclinical evaluation of rapeseed, raspberry, and pine bark phenolics for health related effects. J Agric Food Chem 2005, 53:5922-5931.
• [23]Marino A, Bellinghieri V, Nostro A, Miceli N, Taviano MF, Guvenc A, Bisignano G: In vitro effect of branch extracts of Juniperus species from Turkey on Staphylococcus aureus biofilm. FEMS Immunol Med Microbiol 2010, 59:470-476.
• [24]Miceli N, Trovato A, Marino A, Bellinghieri V, Melchini A, Dugo P, Cacciola F, Donato P, Mondello L, Guvenc A, De Pasquale R, Taviano MF: Phenolic composition and biological activities of Juniperus drupacea Labill. Berries from Turkey. Food Chem Toxicol 2011, 49:2600-2608.
• [25]Mandalari G, Bisignano C, D’Arrigo M, Ginestra G, Arena A, Tomaino A, Wickham MS: Antimicrobial potential of polyphenols extracted from almond skins. Lett Appl Microbiol 2010, 51:83-89.
• [26]Arena A, Bisignano C, Stassi G, Mandalari G, Wickham MSJ, Bisignano G: Immunomodulatory and antiviral activity of almond skins. Immunol Lett 2010, 132:18-23.
• [27]Mandalari G, Bisignano C, Genovese T, Mazzon E, Wickham MS, Paterniti I, Cuzzocrea S: Natural almond skin reduced oxidative stress and inflammation in an experimental model of inflammatory bowel disease. Int Immunopharmacol 2011, 11:915-924.
• [28]Faundez G, Troncoso M, Figueroa G: cagA and vacA in strains of Helicobacter pylori from ulcer and non-ulcerative dyspepsia patients. BMC Gastroenterol 2002, 2:20. BioMed Central Full Text
• [29]Clinical and Laboratory Standards Institute: Performance standards for antimicrobial susceptibility testing; twentieth informational supplement. M100-S22. Wayne: PA: CLSI; 2012.
• [30]Martini S, Bonechi C, Rossi C, Figura N: Increased susceptibility to resveratrol of Helicobacter pylori strains isolated from patients with gastric carcinoma. J Nat Prod 2011, 74:2257-2260.
• [31]Liu W, Hsu C, Yin M: In vitro anti-Helicobacter pylori activity of diallyl sulphides and protocathecuic acid. Phytother Res 2008, 22:53-57.
• [32]Funatogawa K, Hayashi S, Shimomura H, Yoshida T, Hatano T, Ito H, Hirai Y: Antibacterial activity of hydrolysable tannins derived from medicinal plants against Helicobacter pylori. Microbiol Immunol 2004, 48:251-261.
• [33]Toyoda T, Tsukamoto T, Mizoshita T, Nishibe S, Deyama T, Takenata Y, Hirano N, Tanaka H, Takasu S, Ban H, Kumagai T, Inada K, Utsunomiya H, Tatematsu M: Inhibitory effect of nordihydroguaiaretic acid, a plant lignan, on Helicobacter pylori-associated gastric carcinogenesis in Mongolian gerbils. CancSci 2007, 98:1689-1695.
• [34]Xiao Z-P, Shi D-H, Li H-Q, Zhang L-N, Xu C, Zhu H-L: Polyphenols based on isoflavones as inhibitors of Helicobacter pylori urease. Bioorg Med Chem 2007, 15:3703-3710.
• [35]Ansari FL, Umbreen S, Hussain L, Makhmoor T, Nawaz SA, Lodhi MA, Khan SN, Shaheen F, Choudhary MI, Atta-ur-Rahman: Syntheses and biological activities of chalcones and 1,5-benzothiazepine derivatives: promising new free-radical scavengers, and esterases, ureases and α-glucosidase inhibitors. Chem Biodivers 2005, 2:487-496.
• [36]Tombola F, Campello S, De Luca L, Ruggiero P, Del Giudice G, Papini E, Zoratti M: Plant polyphenols inhibit VacA, a toxin secreted by the gastric pathogen Helicobacter pylori. FEBS Lett 2003, 543:184-189.
• [37]Lee KM, Yeo M, Choue JS, Jin JH, Park SJ, Cheong JY, Lee KJ, Kim JH, Hahm KB: Protective mechanism of epigallocatechin-3-gallate against Helicobacter pylori-induced gastric epithelial cytotoxicity via the blockage of TLR-4 signalling. Helicobacter 2004, 9:632-642.
• [38]Makobongo MO, Gancz H, Carpenter BM, McDaniel DP, Merrel DS: The oligo-acyl lysyl antimicrobial peptide C12K-2 exhibits a dual mechanism of action and demonstrated strong in vivo efficacy against Helicobacter pylori. Antimicrob Ag Chemother 2012, 56:378-390.