Ascorbic Acid may Exacerbate Aspirin-Induced Increase in Intestinal Permeability

Basic and Clinical Pharmacology and Toxicology

Volumn 117, Issue 3, 2015, Pages 195-203

  Sequeira, Ivana R ^a   Kruger, Marlena C ^a   Hurst, Roger D ^b   Lentle, Roger G ^a  

^a MASSEY UNIVERSITY   (New Zealand)

^b THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; ASCORBIC ACID; LACTULOSE; MANNITOL; PLACEBO; NONSTEROID ANTIINFLAMMATORY AGENT;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DISEASE EXACERBATION; DRUG INDUCED DISEASE; FEMALE; GASTROINTESTINAL DISEASE; HUMAN; INTESTINE MUCOSA PERMEABILITY; PRIORITY JOURNAL; SINGLE DRUG DOSE; URINARY EXCRETION; DOUBLE BLIND PROCEDURE; DRUG EFFECTS; DRUG POTENTIATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INTESTINE MUCOSA; PERMEABILITY; RANDOMIZED CONTROLLED TRIAL; SMALL INTESTINE; TIGHT JUNCTION; URINE; YOUNG ADULT;

ADULT; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ASCORBIC ACID; ASPIRIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; DRUG SYNERGISM; FEMALE; HUMANS; INTESTINAL MUCOSA; INTESTINE, SMALL; LACTULOSE; MANNITOL; PERMEABILITY; TIGHT JUNCTIONS; YOUNG ADULT;

EID: 84938556601     PISSN: 17427835     EISSN: 17427843     Source Type: Journal    
DOI: 10.1111/bcpt.12388     Document Type: Article

References (58)

1. Lichtenberger LM, Zhou Y, Dial EJ, Raphael RM. NSAID injury to the gastrointestinal tract: evidence that NSAIDs interact with phospholipids to weaken the hydrophobic surface barrier and induce the formation of unstable pores in membranes. J Pharm Pharmacol 2006;58:1421-8.
2. Zhou Y, Raphael RM. Effect of salicylate on the elasticity, bending stiffness, and strength of SOPC membranes. Biophys J 2005;89:1789-801.
3. Lichtenberger LM, Zhou Y, Jayaraman V, Doyen JR, O'Neil RG, Dial EJ et al. Insight into NSAID-induced membrane alterations, pathogenesis and therapeutics: characterization of interaction of NSAIDs with phosphatidylcholine. Biochim Biophys Acta 2012;1821:994-1002.
4. Mahmud T, Scott DL, Bjarnason I. A unifying hypothesis for the mechanism of NSAID related gastrointestinal toxicity. Ann Rheum Dis 1996;55:211-3.
5. Kefalakes H, Stylianides T, Amanakis G, Kolios G. Exacerbation of inflammatory bowel diseases associated with the use of nonsteroidal anti-inflammatory drugs: myth or reality? Eur J Clin Pharmacol 2009;65:963-70.
6. Blikslager AT, Roberts MC, Rhoads JM, Argenzio RA. Prostaglandins I2 and E2 have a synergistic role in rescuing epithelial barrier function in porcine ileum. J Clin Invest 1997;100:1928.
7. Oshima T, Miwa H, Joh T. Aspirin induces gastric epithelial barrier dysfunction by activating p38 MAPK via claudin-7. Am J Physiol Cell Physiol 2008;295:C800-6.
8. Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol 2012;5:354-66.
9. Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A. Neutrophil function: from mechanisms to disease. Annu Rev Immunol 2012;30:459-89.
10. Buffinton GD, Doe WF. Altered ascorbic-acid status in the mucosa from inflammatory bowel-disease patients. Free Radical Res 1995;22:131-43.
11. Pohle T, Brzozowski T, Becker J, Van der Voort I, Markmann A, Konturek S et al. Role of reactive oxygen metabolites in aspirin-induced gastric damage in humans: gastroprotection by vitamin C. Aliment Pharmacol Ther 2001;15:677-87.
12. Söderholm JD, Olaison G, Lindberg E, Hannestad U, Vindels A, Tysk C et al. Different intestinal permeability patterns in relatives and spouses of patients with Crohn's disease: an inherited defect in mucosal defence? Gut 1999;44:96-100.
13. Menzies I, Pounder R, Heyer S, Laker M, Bull J, Wheeler P et al. Abnormal intestinal permeability to sugars in villous atrophy. Lancet 1979;314:1107-9.
14. Farhadi A, Keshavarzian A, Kwasny MJ, Shaikh M, Fogg L, Lau C et al. Effects of aspirin on gastroduodenal permeability in alcoholics and controls. Alcohol 2010;44:447-56.
15. Travis S, Menzies I. Intestinal permeability: functional assessment and significance. Clin Sci 1992;82:471-88.
16. Hollander D. Intestinal permeability, leaky gut, and intestinal disorders. Curr Gastroenterol Rep 1999;1:410-6.
17. Bijlsma PB, Peeters RA, Groot JA, Dekker PR, Taminiau J, Vandermeer R. Differential in-vivo and in-vitro intestinal permeability to lactulose and mannitol in animals and humans - a hypothesis. Gastroenterology 1995;108:687-96.
18. Andre C. Food allergy: objective diagnosis and test of therapeutic efficacy by measuring intestinal permeability. Presse Med 1986;15:105-8.
19. Hollander D. The intestinal permeability barrier: a hypothesis as to its regulation and involvement in Crohn's disease. Scand J Gastroenterol 1992;27:721-6.
20. Cooper BT. Small intestinal permeability as an indicator of Jejunal Mucosal recovery in patients with Celiac Sprue on a Gluten-Free diet. J Clin Gastroenterol 1985;7:232-6.
21. Stenhamma L, Fälth-Magnusson K, Jansson G, Magnusson K-E, Sundqvist T. Intestinal permeability to inert sugars and different-sized polyethyleneglycols in children with Celiac disease. J Pediatr Gastroenterol Nutr 1989;9:281-9.
22. Konturek P, Kania J, Hahn E, Konturek J. Ascorbic acid attenuates aspirin-induced gastric damage: role of inducible nitric oxide synthase. J Physiol Pharmacol 2006;57:125.
23. Farhadi A, Banan ALI, Fields J, Keshavarzian ALI. Intestinal barrier: an interface between health and disease. J Gastroenterol Hepatol 2003;18:479-97.
24. Dammann HG, Saleki M, Torz M, Schulz HU, Krupp S, Schurer M et al. Effects of buffered and plain acetylsalicylic acid formulations with and without ascorbic acid on gastric mucosa in healthy subjects. Aliment Pharmacol Ther 2004;19:367-74.
25. McAlindon ME, Muller AF, Filipowicz B, Hawkey CJ. Effect of allopurinol, sulphasalazine, and vitamin C on aspirin induced gastroduodenal injury in human volunteers. Gut 1996;38:518-24.
26. MacDonald L, Thumser AE, Sharp P. Decreased expression of the vitamin C transporter SVCT1 by ascorbic acid in a human intestinal epithelial cell line. Br J Nutr 2002;87:97-100.
27. Mellors AJ, Nahrwold DL, Rose RC. Ascorbic acid flux across mucosal border of guinea pig and human ileum. Am J Physiol 1977;233:E374-9.
28. Wilson JX. Regulation of vitamin C transport. Annu Rev Nutr 2005;25:105-25.
29. Boyer JC, Campbell CE, Sigurdson WJ, Kuo S-M. Polarized localization of vitamin C transporters, SVCT1 and SVCT2, in epithelial cells. Biochem Biophys Res Commun 2005;334:150-6.
30. Sequeira IR, Lentle RG, Kruger MC, Hurst RD. The effect of aspirin and smoking on urinary excretion profiles of lactulose and mannitol in young women: toward a dynamic, aspirin augmented, test of gut mucosal permeability. Neurogastroenterol Motil 2012;24:e401-11.
31. Johnston CS. Biomarkers for establishing a tolerable upper intake level for vitamin C. Nutr Rev 1999;57:71-7.
32. Seleem HS, Ghobashy HA, Zolfakar AS. Effect of aspirin versus aspirin and vitamin C on gastric mucosa (Fundus) of adult male albino rats. Histological and Morphometric Study. Egypt J Histol 2010;33:313-26.
33. Sequeira IR, Lentle RG, Kruger MC, Hurst RD. Standardising the Lactulose Mannitol test of gut permeability to minimise error and promote comparability. PLoS One 2014;9:e99256.
34. Sequeira IR, Lentle RG, Kruger MC, Hurst RD. Differential trafficking of saccharidic probes following aspirin in clinical tests of intestinal permeability in young healthy female subjects. Clin Exp Pharmacol Physiol 2013;41:107-17.
35. Wilkinson L. SYSTAT. Wiley Interdiscip Rev Comput Stat 2010;2:256-7.
36. Ryan BF, Joiner BL, Cryer JD. MINITAB Handbook: Update for Release 16. California, US, Brooks/Cole Publishing Co., 2012.
37. Goddard P, Hills B, Lichtenberger L. Does aspirin damage canine gastric mucosa by reducing its surface hydrophobicity? Am J Physiol 1987;252:G421-30.
38. Lundbæk JA, Koeppe RE, Andersen OS. Amphiphile regulation of ion channel function by changes in the bilayer spring constant. Proc Natl Acad Sci 2010;107:15427-30.
39. Lichtenberger LM. Where is the evidence that cyclooxygenase inhibition is the primary cause of nonsteroidal anti-inflammatory drug (NSAID)-induced gastrointestinal injury?: Topical injury revisited. Biochem Pharmacol 2001;61:631-7.
40. Baskin WN, Ivey KJ, Krause WJ, Jeffrey GE, Gemmell RT. Aspirin-induced ultrastructural changes in human gastric-mucosa-correlation with potential difference. Ann Intern Med 1976;85:299-303.
41. May JM, Qu Z-C. Nitric oxide mediates tightening of the endothelial barrier by ascorbic acid. Biochem Biophys Res Commun 2011;404:701-5.
42. May JM, Qu Z-C, Qiao H. Transfer of ascorbic acid across the vascular endothelium: mechanism and self-regulation. Am J Physiol Cell Physiol 2009;297:C169-78.
43. Drozdowski LA, Thomson ABR. Intestinal sugar transport. World J Gastroenterol 2006;12:1657-70.
44. Taylor C, Colgan S. Hypoxia and gastrointestinal disease. J Mol Med 2007;85:1295-300.
45. Malo C, Wilson J. Glucose modulates vitamin C transport in adult human small intestinal brush border membrane vesicles. J Nutr 2000;130:63-9.
46. Corti A, Casini AF, Pompella A. Cellular pathways for transport and efflux of ascorbate and dehydroascorbate. Arch Biochem Biophys 2010;500:107-15.
47. Savini I, Rossi A, Pierro C, Avigliano L, Catani M. SVCT1 and SVCT2: key proteins for vitamin C uptake. Amino Acids 2008;34:347-55.
48. Rajasekaran SA, Beyenbach KW, Rajasekaran AK. Interactions of tight junctions with membrane channels and transporters. Biochim Biophys Acta 2008;1778:757-69.
49. Turner JR. Show me the pathway!: Regulation of paracellular permeability by Na+-glucose cotransport. Adv Drug Deliv Rev 2000;41:265-81.
50. Berglund JJ, Riegler M, Zolotarevsky Y, Wenzl E, Turner JR. Regulation of human jejunal transmucosal resistance and MLC phosphorylation by Na+-glucose cotransport. Am J Physiol Gastrointest Liver Physiol 2001;281:G1487-93.
51. Lindblad M, Tveden-Nyborg P, Lykkesfeldt J. Regulation of vitamin C homeostasis during deficiency. Nutrients 2013;5:2860-79.
52. Goldenberg H, Schweinzer E. Transport of vitamin C in animal and human cells. J Bioenerg Biomembr 1994;26:359-67.
53. Wang Y, Mackenzie B, Tsukaguchi H, Weremowicz S, Morton CC, Hediger MA. Human vitamin C (l-ascorbic acid) transporter SVCT1. Biochem Biophys Res Commun 2000;267:488-94.
54. Wright EM. Glucose transport families SLC5 and SLC50. Mol Aspects Med 2013;34:183-96.
55. Asard H, May J, Smirnoff N. Vitamin C: Its Functions and Biochemistry in Animals and Plants. London, England, Taylor & Francis, 2003.
56. Mardones L, Ormazabal V, Romo X, Jaña C, Binder P, Peña E et al. The glucose transporter-2 (GLUT2) is a low affinity dehydroascorbic acid transporter. Biochem Biophys Res Commun 2011;410:7-12.
57. Ioannides C, Stone AN, Breacker PJ, Basu TK. Impairment of absorption of ascorbic acid following ingestion of aspirin in guinea pigs. Biochem Pharmacol 1982;31:4035-8.
58. Dixon SJ, Kulaga A, Jaworski EM, Wilson JX. Ascorbate uptake by ROS 17/2.8 osteoblast-like cells: substrate specificity and sensitivity to transport inhibitors. J Bone Miner Res 1991;6:623-9.