Pomegranate seed oil reduces intestinal damage in a rat model of necrotizing enterocolitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 303, Issue 6, 2012, Pages

  Coursodon Boyiddle, Christine F ^a   Snarrenberg, Chelsea L ^a   Adkins Rieck, Camille K ^a   Bassaganya Riera, Josep ^b   Hontecillas, Raquel ^b   Lawrence, Peter ^c   Thomas Brenna, J ^c   Jouni, Zeina E ^d   Dvorak, Bohuslav ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d Mead Johnson Nutritionals   (United States)

Author keywords

Cytokines; Enteral nutrition; Intestinal injury; Mucosal inflammation

Indexed keywords

CYTOKINE; INTERLEUKIN 12; INTERLEUKIN 23; INTERLEUKIN 6; INTERLEUKIN 8; INTESTINAL TREFOIL FACTOR; LINOLENIC ACID; MUCIN; POMEGRANATE SEED OIL; PUNICIC ACID; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VEGETABLE OIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASPHYXIA; CELL PROLIFERATION; COLD STRESS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIGESTIVE SYSTEM INJURY; DISEASE SEVERITY; DRUG EFFECT; EPITHELIUM CELL; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE INJURY; LIPID COMPOSITION; NECROTIZING ENTEROCOLITIS; NEWBORN; NONHUMAN; POMEGRANATE; PRIORITY JOURNAL; RAT; TREATMENT RESPONSE;

ANIMALS; ANIMALS, NEWBORN; DIET; ENTEROCOLITIS, NECROTIZING; FEMALE; GENE EXPRESSION REGULATION; ILEUM; LIPIDS; MUCIN-2; NEUROPEPTIDES; PLANT OILS; PREGNANCY; PUNICACEAE; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RNA; SEEDS;

EID: 84866396389     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00248.2012     Document Type: Article

References (56)

1. Akisu M, Baka M, Coker I, Kultursay N, Huseyinov A. Effect of dietary n-3 fatty acids on hypoxia-induced necrotizing enterocolitis in young mice. N-3 fatty acids alter platelet-activating factor and leukotriene B4 production in the intestine. Biol Neonate 74: 31-38, 1998.
2. Bassaganya-Riera J, Diguardo M, Climent M, Vives C, Carbo A, Jouni ZE, Einerhand AW, O'Shea M, Hontecillas R. Activation of PPARgamma and delta by dietary punicic acid ameliorates intestinal inflammation in mice. Br J Nutr: 1-9, 2011.
3. Bassaganya-Riera J, Hontecillas R. CLA and n-3 PUFA differentially modulate clinical activity and colonic PPAR-responsive gene expression in a pig model of experimental IBD. Clin Nutr 25: 454-465, 2006.
4. Bassaganya-Riera J, Hontecillas R, Horne WT, Sandridge M, Herfarth HH, Bloomfeld R, Isaacs KL. Conjugated linoleic acid modulates immune responses in patients with mild to moderately active Crohn's disease. Clin Nutr. 2012 Apr 19. [Epub ahead of print]. doi:10.1016/ j.clnu.2012.03.002.
5. Bassaganya-Riera J, Reynolds K, Martino-Catt S, Cui Y, Hennighausen L, Gonzalez F, Rohrer J, Benninghoff AU, Hontecillas R. Activation of PPAR gamma and delta by conjugated linoleic acid mediates protection from experimental inflammatory bowel disease. Gastroenterology 127: 777-791, 2004.
6. Bhattacharya A, Banu J, Rahman M, Causey J, Fernandes G. Biological effects of conjugated linoleic acids in health and disease. J Nutr Biochem 17: 789-810, 2006.
7. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917, 1959.
8. Boussetta T, Raad H, Letteron P, Gougerot-Pocidalo MA, Marie JC, Driss F, El-Benna J. Punicic acid a conjugated linolenic acid inhibits TNFalpha-induced neutrophil hyperactivation and protects from experimental colon inflammation in rats. PLoS One 4: e6458, 2009.
9. Buck C, Bundschu J, Gallati H, Bartmann P, Pohlandt F. Interleukin-6: a sensitive parameter for the early diagnosis of neonatal bacterial infection. Pediatrics 93: 54-58, 1994.
10. Cao Y, Chen J, Yang L, Chen ZY. Differential incorporation of dietary conjugated linolenic and linoleic acids into milk lipids and liver phospholipids in lactating and suckling rats. J Nutr Biochem 20: 685-693, 2009.
11. Caplan MS, Jilling T. The role of polyunsaturated fatty acid supplementation in intestinal inflammation and neonatal necrotizing enterocolitis. Lipids 36: 1053-1057, 2001.
12. Caplan MS, Russell T, Xiao Y, Amer M, Kaup S, Jilling T. Effect of polyunsaturated fatty acid (PUFA) supplementation on intestinal inflammation and necrotizing enterocolitis (NEC) in a neonatal rat model. Pediatr Res 49: 647-652, 2001.
13. Carlisle EM, Poroyko V, Caplan MS, Alverdy JA, Liu D. Gram negative bacteria are associated with the early stages of necrotizing enterocolitis. PLoS One 6: e18084, 2011.
14. Carlson SE, Montalto MB, Ponder DL, Werkman SH, Korones SB. Lower incidence of necrotizing enterocolitis in infants fed a preterm formula with egg phospholipids. Pediatr Res 44: 491-498, 1998.
15. Clark JA, Doelle SM, Halpern MD, Saunders TA, Holubec H, Dvorak K, Boitano SA, Dvorak B. Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment. Am J Physiol Gastrointest Liver Physiol 291: G938-G949, 2006.
16. Clark JA, Lane RH, Maclennan NK, Holubec H, Dvorakova K, Halpern MD, Williams CS, Payne CM, Dvorak B. Epidermal growth factor reduces intestinal apoptosis in an experimental model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 288: G755-G762, 2005.
17. Dvorak B, Halpern MD, Holubec H, Dvorakova K, Dominguez JA, Williams CS, Meza YG, Kozakova H, McCuskey RS. Maternal milk reduces severity of necrotizing enterocolitis and increases intestinal IL-10 in a neonatal rat model. Pediatr Res 53: 426-433, 2003.
18. Dvorak B, Halpern MD, Holubec H, Williams CS, McWilliam DL, Dominguez JA, Stepankova R, Payne CM, McCuskey RS. Epidermal growth factor reduces the development of necrotizing enterocolitis in a neonatal rat model. Am J Physiol Gastrointest Liver Physiol 282: G156-G164, 2002.
19. Dvorak B, McWilliam DL, Williams CS, Dominguez JA, Machen NW, McCuskey RS, Philipps AF. Artificial formula induces precocious maturation of the small intestine of artificially reared suckling rats. J Pediatr Gastroenterol Nutr 31: 162-169, 2000.
20. Edelson MB, Bagwell CE, Rozycki HJ. Circulating pro-and counterinflammatory cytokine levels and severity in necrotizing enterocolitis. Pediatrics 103: 766-771, 1999.
21. Elfalleh W, Ying M, Nasri N, Sheng-Hua H, Guasmi F, Ferchichi A. Fatty acids from Tunisian and Chinese pomegranate (Punica granatum L.) seeds. Int J Food Sci Nutr 62: 200-206, 2011.
22. Grave GD, Nelson SA, Walker WA, Moss RL, Dvorak B, Hamilton FA, Higgins R, Raju TN. New therapies and preventive approaches for necrotizing enterocolitis: report of a research planning workshop. Pediatr Res 62: 510-514, 2007.
23. Guesnet P, Alessandri JM. Docosahexaenoic acid (DHA) and the developing central nervous system (CNS)-Implications for dietary recommendations. Biochimie 93: 7-12, 2011.
24. Guthrie SO, Gordon PV, Thomas V, Thorp JA, Peabody J, Clark RH. Necrotizing enterocolitis among neonates in the United States. J Perinatol 23: 278-285, 2003.
25. Halpern MD, Clark JA, Saunders TA, Doelle SM, Hosseini DM, Stagner AM, Dvorak B. Reduction of experimental necrotizing enterocolitis with anti-TNF-α. Am J Physiol Gastrointest Liver Physiol 290: G757-G764, 2006.
26. Halpern MD, Holubec H, Dominguez JA, Williams CS, Meza YG, McWilliam DL, Payne CM, McCuskey RS, Besselsen DG, Dvorak B. Up-regulation of IL-18 and IL-12 in the ileum of neonatal rats with necrotizing enterocolitis. Pediatr Res 51: 733-739, 2002.
27. Halpern MD, Khailova L, Molla-Hosseini D, Arganbright K, Reynolds C, Yajima M, Hoshiba J, Dvorak B. Decreased development of necrotizing enterocolitis in IL-18-deficient mice. Am J Physiol Gastrointest Liver Physiol 294: G20-G26, 2008.
28. Hennessy AA, Ross RP, Devery R, Stanton C. The health promoting properties of the conjugated isomers of alpha-linolenic acid. Lipids 46: 105-119, 2011.
29. Hora JJ, Maydew ER, Lansky EP, Dwivedi C. Chemopreventive effects of pomegranate seed oil on skin tumor development in CD1 mice. J Med Food 6: 157-161, 2003.
30. Hue S, Ahern P, Buonocore S, Kullberg MC, Cua DJ, McKenzie BS, Powrie F, Maloy KJ. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J Exp Med 203: 2473-2483, 2006.
31. Innis SM. Human milk: maternal dietary lipids and infant development. Proc Nutr Soc 66: 397-404, 2007.
32. Jung HC, Eckmann L, Yang SK, Panja A, Fierer J, Morzycka-Wroblewska E, Kagnoff MF. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 95: 55-65, 1995.
33. Khailova L, Dvorak K, Arganbright KM, Halpern MD, Kinouchi T, Yajima M, Dvorak B. Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 297: G940-G949, 2009.
34. Khailova L, Mount Patrick SK, Arganbright KM, Halpern MD, Kinouchi T, Dvorak B. Bifidobacterium bifidum reduces apoptosis in the intestinal epithelium in necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 299: G1118-G1127, 2010.
35. Kohno H, Suzuki R, Yasui Y, Hosokawa M, Miyashita K, Tanaka T. Pomegranate seed oil rich in conjugated linolenic acid suppresses chemically induced colon carcinogenesis in rats. Cancer Sci 95: 481-486, 2004.
36. Lansky EP, Newman RA. Punica granatum (pomegranate) and its potential for prevention and treatment of inflammation and cancer. J Ethnopharmacol 109: 177-206, 2007.
37. Lawrence P, Brenna JT. Acetonitrile covalent adduct chemical ionization mass spectrometry for double bond localization in non-methyleneinterrupted polyene fatty acid methyl esters. Anal Chem 78: 1312-1317, 2006.
38. Lu J, Jilling T, Li D, Caplan MS. Polyunsaturated fatty acid supplementation alters proinflammatory gene expression and reduces the incidence of necrotizing enterocolitis in a neonatal rat model. Pediatr Res 61: 427-432, 2007.
39. Lucas A, Cole TJ. Breast milk and neonatal necrotising enterocolitis. Lancet 336: 1519-1523, 1990.
40. Mahdihassan S. Outline of the beginnings of alchemy and its antecedents. Am J Chin Med 12: 32-42, 1984.
41. McElroy SJ, Weitkamp JH. Innate immunity in the small intestine of the preterm infant. Neoreviews 12: e517-e526, 2011.
42. Meerts IA, Verspeek-Rip CM, Buskens CA, Keizer HG, Bassaganya-Riera J, Jouni ZE, van Huygevoort AH, van Otterdijk FM, van de Waart EJ. Toxicological evaluation of pomegranate seed oil. Food Chem Toxicol 47: 1085-1092, 2009.
43. Mehta R, Lansky EP. Breast cancer chemopreventive properties of pomegranate (Punica granatum) fruit extracts in a mouse mammary organ culture. Eur J Cancer Prev 13: 345-348, 2004.
44. Molto-Puigmarti C, Castellote AI, Lopez-Sabater MC. Conjugated linoleic acid determination in human milk by fast-gas chromatography. Anal Chim Acta 602: 122-130, 2007.
45. Morecroft JA, Spitz L, Hamilton PA, Holmes SJ. Plasma cytokine levels in necrotizing enterocolitis. Acta Paediatr Suppl 396: 18-20, 1994.
46. Morrison PJ, Ballantyne SJ, Kullberg MC. Interleukin-23 and T helper 17-type responses in intestinal inflammation: from cytokines to T-cell plasticity. Immunology 133: 397-408, 2011.
47. Nanthakumar N, Meng D, Goldstein AM, Zhu W, Lu L, Uauy R, Llanos A, Claud EC, Walker WA. The mechanism of excessive intestinal inflammation in necrotizing enterocolitis: an immature innate immune response. PLoS One 6: e17776, 2011.
48. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med 364: 255-264, 2011.
49. Oppmann B, Lesley R, Blom B, Timans JC, Xu Y, Hunte B, Vega F, Yu N, Wang J, Singh K, Zonin F, Vaisberg E, Churakova T, Liu M, Gorman D, Wagner J, Zurawski S, Liu Y, Abrams JS, Moore KW, Rennick D, de Waal-Malefyt R, Hannum C, Bazan JF, Kastelein RA. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715-725, 2000.
50. Ran-Ressler RR, Khailova L, Arganbright KM, Adkins-Rieck CK, Jouni ZE, Koren O, Ley RE, Brenna JT, Dvorak B. Branched chain fatty acids reduce the incidence of necrotizing enterocolitis and alter gastrointestinal microbial ecology in a neonatal rat model. PLoS One 6: e29032, 2011.
51. Sarra M, Pallone F, Macdonald TT, Monteleone G. IL-23/IL-17 axis in IBD. Inflamm Bowel Dis 16: 1808-1813, 2010.
52. Sassano G, Sanderson P, Franx J, Groot P, van Straalen J, Bassaganya-Riera J. Analysis of pomegranate seed oil for the presence of jacaric acid. J Sci Food Agric 89: 1046-1052, 2009.
53. Sharma R, Tepas JJ 3rd, Hudak ML, Mollitt DL, Wludyka PS, Teng RJ, Premachandra BR. Neonatal gut barrier and multiple organ failure: role of endotoxin and proinflammatory cytokines in sepsis and necrotizing enterocolitis. J Pediatr Surg 42: 454-461, 2007.
54. Suemori S, Lynch-Devaney K, Podolsky DK. Identification and characterization of rat intestinal trefoil factor: tissue-and cell-specific member of the trefoil protein family. Proc Natl Acad Sci USA 88: 11017-11021, 1991.
55. Vroegrijk IO, van Diepen JA, van den Berg S, Westbroek I, Keizer H, Gambelli L, Hontecillas R, Bassaganya-Riera J, Zondag GC, Romijn JA, Havekes LM, Voshol PJ. Pomegranate seed oil, a rich source of punicic acid, prevents diet-induced obesity and insulin resistance in mice. Food Chem Toxicol 49: 1426-1430, 2011.
56. Weitkamp JH, Koyama T, Rock MT, Correa H, Goettel JA, Matta P, Oswald-Richter K, Rosen MJ, Engelhardt BG, Moore DJ, Polk DB. Necrotising enterocolitis is characterised by disrupted immune regulation and diminished mucosal regulatory (FOXP3)/effector (CD4, CD8) T cell ratios. Gut. 2012 Jan 20. [Epub ahead of print]. doi:10.1136/gutjnl-2011-301551.