- About this Journal
- Abstracting and Indexing
- Aims and Scope
- Annual Issues
- Article Processing Charges
- Articles in Press
- Author Guidelines
- Bibliographic Information
- Citations to this Journal
- Contact Information
- Editorial Board
- Editorial Workflow
- Free eTOC Alerts
- Publication Ethics
- Reviewers Acknowledgment
- Submit a Manuscript
- Subscription Information
- Table of Contents
Evidence-Based Complementary and Alternative Medicine
Volume 2013 (2013), Article ID 247145, 11 pages
A Review on the Anti-Inflammatory Activity of Pomegranate in the Gastrointestinal Tract
1Department of Pharmacological and Biomolecular Sciences, Università degli Studi di Milano, Via Balzaretti 9, Milano, Italy
2Research Centre for Characterization and Safe Use of Natural Compounds-G. Galli, Università degli Studi di Milano, Via Balzaretti 9, 20133 Milano, Italy
Received 28 December 2012; Accepted 20 February 2013
Academic Editor: David Heber
Copyright © 2013 Elisa Colombo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- J. Jurenka, “Therapeutic applications of pomegranate (Punica granatum L.): a review,” Alternative Medicine Review, vol. 13, no. 2, pp. 128–144, 2008.
- M. Dell'Agli, G. V. Galli, Y. Corbett et al., “Antiplasmodial activity of Punica granatum L. fruit rind,” Journal of Ethnopharmacology, vol. 125, no. 2, pp. 279–285, 2009.
- M. Dell'Agli, G. V. Galli, M. Bulgari et al., “Ellagitannins of the fruit rind of pomegranate (Punica granatum) antagonize in vitro the host inflammatory response mechanisms involved in the onset of malaria,” Malaria Journal, vol. 9, no. 1, article 208, 2010.
- S. D. Johanningsmeier and G. K. Harris, “Pomegranate as a functional food and nutraceutical source,” Annual Review of Food Science Technology, vol. 2, pp. 181–201, 2011.
- A. Faria and C. Conceição, “The bioactivity of pomegranate: impact on health and disease,” Critical Reviews in Food Science and Nutrition, vol. 51, no. 7, pp. 626–634, 2011.
- J. E. Crabtree, P. Peichl, J. I. Wyatt, U. Stachl, and I. J. D. Lindley, “Gastric interleukin-8 and IgA IL-8 autoantibodies in Helicobacter pylori infection,” Scandinavian Journal of Immunology, vol. 37, no. 1, pp. 65–70, 1993.
- J. E. Crabtree, Z. Xiang, I. J. D. Lindley, D. S. Tompkins, R. Rappuoli, and A. Covacci, “Induction of interleukin-8 secretion from gastric epithelial cells by a cagA negative isogenic mutant of Helicobacter pylori,” Journal of Clinical Pathology, vol. 48, no. 10, pp. 967–969, 1995.
- K. Yasumoto, S. I. Okamoto, N. Mukaida, S. Murakami, M. Mai, and K. Matsushima, “Tumor necrosis factor α and interferon γ synergistically induce interleukin 8 production in a human gastric cancer cell line through acting concurrently on AP-1 and NF-kB-like binding sites of the interleukin 8 gene,” Journal of Biological Chemistry, vol. 267, no. 31, pp. 22506–22511, 1992.
- R. Caruso, D. Fina, I. Peluso et al., “IL-21 is highly produced in Helicobacter pylori-infected gastric mucosa and promotes gelatinases synthesis,” Journal of Immunology, vol. 178, no. 9, pp. 5957–5965, 2007.
- B. Romier, Y. J. Schneider, Y. Larondelle, and A. During, “Dietary polyphenols can modulate the intestinal inflammatory response,” Nutrition Reviews, vol. 67, no. 7, pp. 363–378, 2009.
- R. Al-Ashy, I. Chakroun, M. E. El-Sabban, and F. R. Homaidan, “The role of NF-κB in mediating the anti-inflammatory effects of IL-10 in intestinal epithelial cells,” Cytokine, vol. 36, no. 1-2, pp. 1–8, 2006.
- E. P. Lansky and R. A. Newman, “Punica granatum (pomegranate) and its potential for prevention and treatment of inflammation and cancer,” Journal of Ethnopharmacology, vol. 109, no. 2, pp. 177–206, 2007.
- F. Afaq, V. M. Adhami, and H. Mukhtar, “Photochemoprevention of ultraviolet B signaling and photocarcinogenesis,” Mutation Research, vol. 571, no. 1-2, pp. 153–173, 2005.
- D. Heber, “Pomegranate ellagitannins,” in Herbal Medicine: Biomolecular and Clinical Aspects, I. F. F. Benzie and S. Wachtel-Galor, Eds., CRC Press, Boca Raton, Fla, USA, 2nd edition, 2011.
- M. I. Gil, F. A. Tomas-Barberan, B. Hess-Pierce, D. M. Holcroft, and A. A. Kader, “Antioxidant activity of pomegranate juice and its relationship with phenolic composition and processing,” Journal of Agricultural and Food Chemistry, vol. 48, no. 10, pp. 4581–4589, 2000.
- S. Quideau, Chemistry and Biology of Ellagitannins, World Scientific, Singapore, 2009.
- N. P. Seeram, R. Lee, and D. Heber, “Bioavailability of ellagic acid in human plasma after consumption of ellagitannins from pomegranate (Punica granatum L.) juice,” Clinica Chimica Acta, vol. 348, no. 1-2, pp. 63–68, 2004.
- N. P. Seeram, Y. Zhang, R. McKeever et al., “Pomegranate juice and extracts provide similar levels of plasma and urinary ellagitannin metabolites in human subjects,” Journal of Medicinal Food, vol. 11, no. 2, pp. 390–394, 2008.
- B. Cerdá, J. C. Espín, S. Parra, P. Martínez, and F. A. Tomás-Barberán, “The potent in vitro antioxidant ellagitannins from pomegranate juice are metabolised into bioavailable but poor antioxidant hydroxy-6H-dibenzopyran-6-one derivatives by the colonic microflora of healthy humans,” European Journal of Nutrition, vol. 43, no. 4, pp. 205–220, 2004.
- A. Pérez-Vicente, A. Gil-Izquierdo, and C. García-Viguera, “In vitro gastrointestinal digestion study of pomegranate juice phenolic compounds, anthocyanins, and vitamin C,” Journal of Agricultural and Food Chemistry, vol. 50, no. 8, pp. 2308–2312, 2002.
- G. J. McDougall, S. Fyffe, P. Dobson, and D. Stewart, “Anthocyanins from red wine—their stability under simulated gastrointestinal digestion,” Phytochemistry, vol. 66, no. 21, pp. 2540–2548, 2005.
- T. K. McGhie and M. C. Walton, “The bioavailability and absorption of anthocyanins: towards a better understanding,” Molecular Nutrition and Food Research, vol. 51, no. 6, pp. 702–713, 2007.
- A. M. Aura, P. Martin-Lopez, K. A. O'Leary et al., “In vitro metabolism of anthocyanins by human gut microflora,” European Journal of Nutrition, vol. 44, no. 3, pp. 133–142, 2005.
- J. Fleschhut, F. Kratzer, G. Rechkemmer, and S. E. Kulling, “Stability and biotransformation of various dietary anthocyanins in vitro,” European Journal of Nutrition, vol. 45, no. 1, pp. 7–18, 2006.
- P. Saniee, M. Hajimahmoodi, P. Foroumadi, et al., “Antibacterial activity of plant extracts against H. pylori,” Helicobacter, vol. 14, pp. 393–394, 2009.
- M. Hajimahmoodi, M. Shams-Ardakani, P. Saniee et al., “In vitro antibacterial activity of some Iranian medicinal plant extracts against Helicobacter pylori,” Natural Product Research, vol. 25, no. 11, pp. 1059–1066, 2011.
- S. P. Voravuthikunchai and H. Mitchell, “Inhibitory and killing activities of medicinal plants against multiple antibiotic-resistant Helicobacter pylori,” Journal of Health Science, vol. 54, no. 1, pp. 81–88, 2008.
- P. J. Oates and J. P. Hakkinen, “Studies on the mechanism of ethanol-induced gastric damage in rats,” Gastroenterology, vol. 94, no. 1, pp. 10–21, 1988.
- K. B. Ajaikumar, M. Asheef, B. H. Babu, and J. Padikkala, “The inhibition of gastric mucosal injury by Punica granatum L. (pomegranate) methanolic extract,” Journal of Ethnopharmacology, vol. 96, no. 1-2, pp. 171–176, 2005.
- M. S. Alam, M. A. Alam, S. Ahmad, A. K. Najmi, M. Asif, and T. Jahangir, “Protective effects of Punica granatum in experimentally-induced gastric ulcers,” Toxicology Mechanisms and Methods, vol. 20, no. 9, pp. 572–578, 2010.
- S. Lai, Q. Zhou, Y. Zhang, J. Shang, and T. Yu, “Effects of Pomegranate tannins on experimental gastric damages,” Zhongguo Zhongyao Zazhi, vol. 34, no. 10, pp. 1290–1294, 2009.
- K. Gharzouli, S. Khennouf, S. Amira, and A. Gharzouli, “Effects of aqueous extracts from Quercus ilex L. root bark, Punica granatum L. fruit peel and Artemisia herba-alba Asso leaves on ethanol-induced gastric damage in rats,” Phytotherapy Research, vol. 13, no. 1, pp. 42–45, 1999.
- A. M. S. E. S. Beserra, P. I. Calegari, M. D. C. Souza et al., “Gastroprotective and ulcer-healing mechanisms of ellagic acid in experimental rats,” Journal of Agricultural and Food Chemistry, vol. 59, no. 13, pp. 6957–6965, 2011.
- S. Fiorucci, E. Antonelli, and A. Morelli, “Mechanism of non-steroidal anti-inflammatory drug-gastropathy,” Digestive and Liver Disease, vol. 33, supplement 2, pp. S35–S43, 2001.
- C. J. Hawkey, “Prostaglandins: mucosal protection and peptic ulceration,” Methods and Findings in Experimental and Clinical Pharmacology, vol. 11, no. 1, pp. 45–51, 1989.
- A. Chatterjee, S. Chatterjee, and S. Das, “Ellagic acid facilitates indomethacin-induced gastric ulcer healing via COX-2 up-regulation,” Acta Biochimica et Biophysica Sinica, vol. 44, no. 7, pp. 565–576, 2012.
- R. Gautam and S. C. Sharma, “Anti-ulcer activity of Punica granatum L. in diabetic rats,” International Journal of Pharmacy and Pharmaceutical Sciences, vol. 4, no. 3, pp. 451–461, 2012.
- S. Murakami, Y. Isobe, H. Kijima, H. Nagai, M. Muramatu, and S. Otomo, “Inhibition of gastric H+,K+-ATPase and acid secretion by ellagic acid,” Planta Medica, vol. 57, no. 4, pp. 305–308, 1991.
- T. Iino, K. Tashima, M. Umeda et al., “Effect of ellagic acid on gastric damage induced in ischemic rat stomachs following ammonia or reperfusion,” Life Sciences, vol. 70, no. 10, pp. 1139–1150, 2002.
- L. S. Adams, N. P. Seeram, B. B. Aggarwal, Y. Takada, D. Sand, and D. Heber, “Pomegranate juice, total pomegranate ellagitannins, and punicalagin suppress inflammatory cell signaling in colon cancer cells,” Journal of Agricultural and Food Chemistry, vol. 54, no. 3, pp. 980–985, 2006.
- B. Romier-Crouzet, J. van de Walle, A. During et al., “Inhibition of inflammatory mediators by polyphenolic plant extracts in human intestinal Caco-2 cells,” Food and Chemical Toxicology, vol. 47, no. 6, pp. 1221–1230, 2009.
- S. Hollebeeck, J. Winand, M. F. Herent, et al., “Anti-inflammatory effects of pomegranate (Punica granatum L.) husk ellagitannins in Caco-2 cells, an in vitro model of human intestine,” Food & Function, vol. 3, no. 8, pp. 875–885, 2012.
- R. A. Rastall, G. R. Gibson, H. S. Gill et al., “Modulation of the microbial ecology of the human colon by probiotics, prebiotics and synbiotics to enhance human health: an overview of enabling science and potential applications,” FEMS Microbiology Ecology, vol. 52, no. 2, pp. 145–152, 2005.
- D. Bialonska, S. G. Kasimsetty, K. K. Schrader, and D. Ferreira, “The effect of pomegranate (Punica granatum l.) byproducts and ellagitannins on the growth of human gut bacteria,” Journal of Agricultural and Food Chemistry, vol. 57, no. 18, pp. 8344–8349, 2009.
- N. P. Seeram, S. M. Henning, Y. Zhang, M. Suchard, Z. Li, and D. Heber, “Pomegranate juice ellagitannin metabolites are present in human plasma and some persist in urine for up to 48 hours,” Journal of Nutrition, vol. 136, no. 10, pp. 2481–2485, 2006.
- D. Bialonska, P. Ramnani, S. G. Kasimsetty, K. R. Muntha, G. R. Gibson, and D. Ferreira, “The influence of pomegranate by-product and punicalagins on selected groups of human intestinal microbiota,” International Journal of Food Microbiology, vol. 140, no. 2-3, pp. 175–182, 2010.
- B. Dobroslawa, S. G. Kasimsetty, S. I. Khan, and F. Daneel, “Urolithins, intestinal microbial metabolites of pomegranate ~ellagitannins, exhibit potent antioxidant activity in a cell-based assay,” Journal of Agricultural and Food Chemistry, vol. 57, no. 21, pp. 10181–10186, 2009.
- T. Sergent, N. Piront, J. Meurice, O. Toussaint, and Y. J. Schneider, “Anti-inflammatory effects of dietary phenolic compounds in an in vitro model of inflamed human intestinal epithelium,” Chemico-Biological Interactions, vol. 188, no. 3, pp. 659–667, 2010.
- A. González-Sarrías, J. C. Espín, F. A. Tomás-Barberán, and M. T. García-Conesa, “Gene expression, cell cycle arrest and MAPK signalling regulation in Caco-2 cells exposed to ellagic acid and its metabolites, urolithins,” Molecular Nutrition and Food Research, vol. 53, no. 6, pp. 686–698, 2009.
- A. González-Sarrías, M. Larrosa, F. A. Toms-Barberán, P. Dolara, and J. C. Espín, “NF-κB-dependent anti-inflammatory activity of urolithins, gut microbiota ellagic acid-derived metabolites, in human colonic fibroblasts,” British Journal of Nutrition, vol. 104, no. 4, pp. 503–512, 2010.
- J. A. Gimenez-Bastida, M. Larrosa, A. Gonzalez-Sarrias, et al., “Intestinal ellagitannin metabolites ameliorate cytokine-induced inflammation and associated molecular markers in human colon fibroblasts,” Journal of Agricultural and Food Chemistry, vol. 60, no. 36, pp. 8866–8876, 2012.
- Y. Ogawa, K. Kanatsu, T. Iino et al., “Protection against dextran sulfate sodium-induced colitis by microspheres of ellagic acid in rats,” Life Sciences, vol. 71, no. 7, pp. 827–839, 2002.
- K. Singh, A. S. Jaggi, and N. Singh, “Exploring the ameliorative potential of Punica granatum in dextran sulfate sodium induced ulcerative colitis in mice,” Phytotherapy Research, vol. 23, no. 11, pp. 1565–1574, 2009.
- S. Umesalma and G. Sudhandiran, “Differential inhibitory effects of the polyphenol ellagic acid on inflammatory mediators NF-κB, iNOS, COX-2, TNF-α, and IL-6 in 1,2-dimethylhydrazine-induced rat colon carcinogenesis,” Basic and Clinical Pharmacology and Toxicology, vol. 107, no. 2, pp. 650–655, 2010.
- M. A. Rosillo, M. Sanchez-Hidalgo, A. Cárdeno, and C. A. de la Lastra, “Protective effect of ellagic acid, a natural polyphenolic compound, in a murine model of Crohn's disease,” Biochemical Pharmacology, vol. 82, no. 7, pp. 737–745, 2011.
- M. A. Rosillo, M. Sanchez-Hidalgo, A. Cardeno, et al., “Dietary supplementation of an ellagic acid-enriched pomegranate extract attenuates chronic colonic inflammation in rats,” Pharmacological Research, vol. 66, no. 3, pp. 235–242, 2012.
- J. Lian, W. Ding, J. X. Sun, and X. M. Lü, “Experimental study of aqueous extract of Pericarpium granati for treating ulcerative colitis of rats,” Pharmaceutical Care and Research, vol. 9, no. 2, pp. 107–110, 2009.
- A. M. Neyrinck, V. F. van Hee, L. B. Bindels, et al., “Polyphenol-rich extract of pomegranate peel alleviates tissue inflammation and hypercholesterolaemia in high-fat diet-induced obese mice: potential implication of the gut microbiota,” British Journal of Nutrition, vol. 7, pp. 1–8, 2012.
- E. V. Khokhlova, V. V. Smeianov, B. A. Efimov, et al., “Anti-inflammatory properties of intestinal Bifidobacterium strains isolated from healthy infants,” Microbiology and Immunology, vol. 56, no. 1, pp. 27–39, 2012.
- M. Larrosa, A. González-Sarrías, M. J. Yáñez-Gascón et al., “Anti-inflammatory properties of a pomegranate extract and its metabolite urolithin-A in a colitis rat model and the effect of colon inflammation on phenolic metabolism,” Journal of Nutritional Biochemistry, vol. 21, no. 8, pp. 717–725, 2010.
- K. Nagao and T. Yanagita, “Conjugated fatty acids in food and their health benefits,” Journal of Bioscience and Bioengineering, vol. 100, no. 2, pp. 152–157, 2005.
- D. M. Hwang, J. K. Kundu, J. W. Shin, J. C. Lee, H. J. Lee, and Y. J. Surh, “cis-9,trans-11-Conjugated linoleic acid down-regulates phorbol ester-induced NF-κB activation and subsequent COX-2 expression in hairless mouse skin by targeting IκB kinase and PI3K-Akt,” Carcinogenesis, vol. 28, no. 2, pp. 363–371, 2007.
- T. Boussetta, H. Raad, P. Lettéron et al., “Punicic acid a conjugated linolenic acid inhibits TNFα-induced neutrophil hyperactivation and protects from experimental colon inflammation in rats,” PLoS ONE, vol. 4, no. 7, Article ID e6458, 2009.
- J. Bassaganya-Riera, M. DiGuardo, M. Climent et al., “Activation of PPARγ and δ by dietary punicic acid ameliorates intestinal inflammation in mice,” British Journal of Nutrition, vol. 106, no. 6, pp. 878–886, 2011.
- K. Katayama, K. Wada, A. Nakajima et al., “A novel PPARγ gene therapy to control inflammation associated with inflammatory bowel disease in a murine model,” Gastroenterology, vol. 124, no. 5, pp. 1315–1324, 2003.
- C. F. Coursodon-Boyiddle, C. L. Snarrenberg, C. K. Adkins-Rieck, et al., “Pomegranate seed oil reduces intestinal damage in a rat model of necrotizing enterocolitis,” American Journal of Physiology, vol. 303, no. 6, pp. G744–G751, 2012.
- R. Hasan, M. Hossain, R. Akter et al., “Antioxidant, antidiarrhoeal and cytotoxic properties of Punica granatum Linn.,” Latin American Journal of Pharmacy, vol. 28, no. 5, pp. 783–788, 2009.
- E. Y. Qnais, A. S. Elokda, Y. Y. A. Ghalyun, and F. A. Abdulla, “Antidiarrheal activity of the aqueous extract of Punica granatum (pomegranate) peels,” Pharmaceutical Biology, vol. 45, no. 9, pp. 715–720, 2007.
- C. V. Rao, A. R. Verma, M. Vijayakumar, and S. Rastogi, “Gastroprotective effect of standardized extract of Ficus glomerata fruit on experimental gastric ulcers in rats,” Journal of Ethnopharmacology, vol. 115, no. 2, pp. 323–326, 2008.
- R. Govindarajan, M. Vijayakumar, M. Singh et al., “Antiulcer and antimicrobial activity of Anogeissus latifolia,” Journal of Ethnopharmacology, vol. 106, no. 1, pp. 57–61, 2006.
- P. Tamashiro-Filho, B. Sikiru Olaitan, D. A. Tavares de Almeida, et al., “Evaluation of antiulcer activity and mechanism of action of methanol stem bark extract of Lafoensia pacari A. St.-Hil. (Lytraceae) in experimental animals,” Journal of Ethnopharmacology, vol. 144, no. 3, pp. 497–505, 2012.
- V. Da Mota Menezes, Á. N. Atallah, A. J. Lapa, and W. R. Catapani, “Assessing the therapeutic use of Lafoensia pacari St. Hil. extract (Mangava-Brava) in the eradication of Helicobacter pylori: double-blind randomized clinical trial,” Helicobacter, vol. 11, no. 3, pp. 188–195, 2006.