NSAID gastropathy and enteropathy: Distinct pathogenesis likely necessitates distinct prevention strategies

British Journal of Pharmacology

Volumn 165, Issue 1, 2012, Pages 67-74

  Wallace, John L ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

analgesic drugs; anti inflammatory drugs; eicosanoids; gastrointestinal pharmacology; inflammation; nitric oxide; peptic ulceration

Indexed keywords

ACETYLSALICYLIC ACID; ANTIBIOTIC AGENT; CELECOXIB; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; HISTAMINE H2 RECEPTOR ANTAGONIST; IBUPROFEN; LANSOPRAZOLE; MISOPROSTOL; NAPROXEN; NONSTEROID ANTIINFLAMMATORY AGENT; OMEPRAZOLE; PHOSPHATIDYLCHOLINE; PROBIOTIC AGENT; PRODRUG; PROSTACYCLIN; PROTON PUMP INHIBITOR;

ANTIINFLAMMATORY ACTIVITY; DISEASE ACTIVITY; DISEASE COURSE; DISEASE SEVERITY; DRUG BLOOD LEVEL; DRUG DOSAGE FORM COMPARISON; DRUG POTENTIATION; DRUG SAFETY; DUODENAL ULCER BLEEDING; DUODENUM INJURY; DUODENUM ULCER; ENTEROPATHY; ENZYME INHIBITION; GASTRIC ULCER BLEEDING; HUMAN; INTESTINE FLORA; INTESTINE INJURY; LOW DRUG DOSE; MUCUS SECRETION; NONHUMAN; OSTEOARTHRITIS; PATHOGENESIS; PRESCRIPTION; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; REVIEW; STOMACH ACID SECRETION; STOMACH INJURY; STOMACH PROTECTION; STOMACH ULCER;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; HUMANS; INTESTINAL DISEASES; STOMACH DISEASES;

EID: 82955184551     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01509.x     Document Type: Review

References (86)

1. Andrews FJ, Malcontenti-Wilson C, O'Brien PE, (1994). Effect of nonsteroidal anti-inflammatory drugs on LFA-1 and ICAM-1 expression in gastric mucosa. Am J Physiol Gastrointest Liver Physiol 266: G657-G664. (Pubitemid 24150922)
2. Antoon JS, Perry MA, (1997). Role of neutrophils and mast cells in acute indomethacin-induced small bowel injury in the rat. J Gastroenterol 32: 747-757. (Pubitemid 27524980)
3. Appleyard CB, McCafferty DM, Tigley AW, Swain MG, Wallace JL, (1996). Tumor necrosis factor mediation of NSAID-induced gastric damage: role of leukocyte adherence. Am J Physiol 270: G42-G48.
4. Asako H, Kubes P, Wallace J, Gaginella T, Wolf RE, Granger DN, (1992a). Indomethacin-induced leukocyte adhesion in mesenteric venules: role of lipoxygenase products. Am J Physiol Gastrointest Liver Physiol 262: G903-G908.
5. Asako H, Kubes P, Wallace J, Wolf RE, Granger DN, (1992b). Modulation of leukocyte adhesion in rat mesenteric venules by aspirin and salicylate. Gastroenterology 103: 146-152.
6. Bjarnason I, Smethurst P, Fenn GC, Lee CE, Menzies IS, Levi AJ, (1989). Misoprostol reduces indomethacin induced changes in human small intestinal permeability. Dig Dis Sci 34: 407-411. (Pubitemid 19088782)
7. Bjarnason I, Hayllar J, MacPherson AJ, Russell AS, (1993). Side effects of nonsteroidal anti-inflammatory drugs on the small and large intestine in humans. Gastroenterology 104: 1832-1847. (Pubitemid 23235480)
8. Claria J, Serhan CN, (1995). Aspirin triggers previously unrecognized bioactive eicosanoids in human endothelial cell-leukocyte interactions. Proc Natl Acad Sci U S A 92: 9475-9479.
9. Cryer B, Bhatt DL, Lanza FL, Dong JF, Lichtenberger LM, Marathi UK, (2011). Low-dose aspirin-induced ulceration is attenuated by aspirin-phosphatidylcholine: a randomized clinical trial. Am J Gastroenterol 106: 272-277.
10. Davies NM, Røseth AG, Appleyard CB, McKnight W, Del Soldato P, Calignano A, et al,. (1997a). NO-naproxen vs. naproxen: ulcerogenic, analgesic and anti-inflammatory effects. Aliment Pharmacol Ther 11: 69-79. (Pubitemid 27067336)
11. Davies NM, Sharkey KA, ASFAHA S, MacNaughton WK, Wallace JL, (1997b). Aspirin induces a rapid up-regulation of cyclooxygenase-2 expression in the rat stomach. Aliment Pharmacol Ther 11: 1101-1108.
12. Douthwaite AH, Lintott SAM, (1938). Gastroscopic observation of the effect of aspirin and certain other substances on the stomach. Lancet 2: 1222-1225.
13. Estes LL, Fuhs DW, Heaton AH, Butwinick CS, (1993). Gastric ulcer perforation, associated with the use of injectable ketorolac. Ann Pharmacother 27: 42-43. (Pubitemid 23024807)
14. 4 increases gastric resistance to aspirin-induced damage. Gastroenterology 123: 1598-1606. (Pubitemid 35231659)
15. Fiorucci S, Santucci L, Wallace JL, Sardina M, Fransioli R, Romano M, et al,. (2003). Interaction of COX-2 inhibitor with aspirin and NO-aspirin in the human gastric mucosa: evidence for a protective role of nitric oxide. Proc Natl Acad Sci U S A 100: 10937-10941. (Pubitemid 37140131)
16. Fiorucci S, Antonelli E, Distrutti E, Rizzo G, Mencarelli A, Orlandi S, et al,. (2005). Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology 129: 1210-1224. (Pubitemid 41446861)
17. Fujimora S, Gudis K, Takahashi Y, Seo T, Yamada Y, Ehara A, et al,. (2010). Distribution of small intestinal mucosal injuries as a result of NSAID administration. Eur J Clin Invest 40: 504-510.
18. Fujimori S, Seo T, Ehara A, Kobayashi T, Mitsui K, Yonezawa M, et al,. (2009). Prevention of nonsteroidal anti-inflammatory drug-induced small-intestinal injury by prostaglandin: a pilot randomized controlled trial evaluated by capsule endoscopy. Gastrointest Endosc 69: 1339-1346.
19. Goldstein JL, Eisen GM, Lewis B, Gralnek IM, Zlotnick S, Fort JG, (2005). Video capsule endoscopy to prospectively assess small bowel injury with celecoxib, naproxen plus omeprazole, and placebo. Clin Gastroenterol Hepatol 3: 133-141. (Pubitemid 40220308)
20. Graham DY, Smith JL, Holmes GI, Davies RO, (1985). Nonsteroidal anti-inflammatory effect of sulindac sulfoxide and sulfide on gastric mucosa. Clin Pharmacol Ther 38: 65-70. (Pubitemid 15242202)
21. Graham DY, White RH, Moreland LW, Schubert TT, KATZ R, Jaszewski R, et al,. (1993). Duodenal and gastric ulcer prevention with misoprostol in arthritis patients taking NSAIDs. Misoprostol Study Group. Ann Intern Med 119: 257-262. (Pubitemid 23319880)
22. Graham DY, Opekun AR, Willingham FF, Qureshi WA, (2005). Visible small-intestinal mucosal injury in chronic NSAID users. Clin Gastroenterol Hepatol 3: 55-59. (Pubitemid 40092944)
23. Green FW, Kaplan MM, Curtis LE, Levine PH, (1978). Effect of acid and pepsin on blood coagulation and platelet aggregation. A possible contributor prolonged gastroduodenal mucosal hemorrhage. Gastroenterology 74: 38-43. (Pubitemid 8248881)
24. Hagiwara M, Kataoka K, Arimochi H, Kuwahara T, Ohnishi Y, (2004). Role of unbalanced growth of Gram-negative bacteria in ileal ulcer formation in rats treated with a nonsteroidal anti-inflammatory drug. J Med Invest 51: 43-51. (Pubitemid 38899321)
25. Hawkey CJ, Jones JI, Atherton CT, Skelly MM, Bebb JR, Fagerholm U, et al,. (2003). Gastrointestinal safety of AZD3582, a cyclooxygenase inhibiting nitric oxide donator: proof of concept study in humans. Gut 52: 1537-1542. (Pubitemid 37363434)
26. Henry D, Dobson A, Turner C, (1993). Variability in the risk of major gastrointestinal complications from nonaspirin nonsteroidal anti-inflammatory drugs. Gastroenterology 10: 1078-1088. (Pubitemid 23281496)
27. Hunt RH, Lanas A, Stichtenoth DO, Scarpignato C, (2009). Myths and facts in the use of anti-inflammatory drugs. Ann Med 8: 1-16.
28. Ito T, Jensen RT, (2010). Association of long-term proton pump inhibitor therapy with bone fractures and effects on absorption of calcium, vitamin B12, iron, and magnesium. Curr Gastroenterol Rep 12: 448-457.
29. Kearney PM, Baigent C, Godwin J, Halls H, Emberson JR, Patrono C, (2006). Do selective cyclo-oxygenase-2 inhibitors and traditional non-steroidal anti-inflammatory drugs increase the risk of atherothrombosis? Meta-analysis of randomised trials. BMJ 332: 1302-1308.
30. Kent TH, Cardelli RM, Stamler FW, (1969). Small intestinal ulcers and intestinal flora in rats given indomethacin. Am J Pathol 54: 237-245.
31. Konaka A, Kato S, Tanaka A, Kunikata T, Korolkiewicz R, Takeuchi K, (1999). Roles of enterobacteria, nitric oxide and neutrophil in pathogenesis of indomethacin-induced small intestinal lesions in rats. Pharmacol Res 40: 517-524.
32. Kubes P, Suzuki M, Granger DN, (1991). Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci U S A 88: 4651-4655. (Pubitemid 21914599)
33. Laine L, Connors LG, Reicin A, Hawkey CJ, Burgos-Vargas R, Schnitzer TJ, et al,. (2003a). Serious lower gastrointestinal adverse clinical events with non-selective NSAID or coxib use. Gastroenterology 124: 288-292. (Pubitemid 36169245)
34. Laine L, Maller ES, Yu C, Quan H, Simon T, (2003b). Ulcer formation with low-dose enteric-coated aspirin and the effect of COX-2-selective inhibition: a double-blind trial. Gastroenterology 127: 395-402. (Pubitemid 39091887)
35. Lanas A, Scarpignato C, (2006). Microbial flora in NSAID-induced intestinal damage: a role for antibiotics? Digestion 73 (Suppl. 1): 136-150.
36. Lanas A, Baron JA, Sandler RS, Horgan K, Bolognese J, Oxenius B, et al,. (2007). Peptic ulcer and bleeding events associated with rofecoxib in a 3-year colorectal adenoma chemoprevention trial. Gastroenterology 132: 490-497. (Pubitemid 46274654)
37. Lanza FL, Marathi UK, Anand BS, Lichtenberger LM, (2008). Clinical trial: comparison of ibuprofen-phosphatidycholine and ibuprofen on the gastrointestinal safety and analgesic efficacy in osteoarthritis patients. Aliment Pharmacol Ther 28: 431-442. (Pubitemid 352033288)
38. Lichtenberger LM, (2001). 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 61: 631-637. (Pubitemid 32239415)
39. Lichtenberger LM, Barron M, Marathi U, (2009). Association of phosphatidylcholine and NSAIDs as a novel strategy to reduce gastrointestinal toxicity. Drugs Today (Barc) 45: 877-890.
40. Lombardo L, Foti M, Ruggia O, Chiecchio A, (2010). Increased incidence of small intestinal bacterial overgrowth during proton pump inhibitor therapy. Clin Gastroenterol Hepatol 8: 504-508.
41. Ma L, del Soldato P, Wallace JL, (2002). Divergent effects of new cyclooxygenase inhibitors on gastric ulcer healing: shifting the angiogenic balance. Proc Natl Acad Sci U S A 99: 13243-13247.
42. MacNaughton WK, Cirino G, Wallace JL, (1989). Endothelium-derived relaxing factor (nitric oxide) has protective actions in the stomach. Life Sci 45: 1869-1876. (Pubitemid 19284677)
43. Maiden L, Thjodleifsson B, Theodors A, Gonzalez J, Bjarnason I, (2005). A quantitative analysis of NSAID-induced small bowel pathology by capsule endoscopy. Gastroenterology 128: 1172-1178.
44. McCafferty DM, Granger DN, Wallace JL, (1995). Indomethacin-induced gastric injury and leukocyte adherence in arthritic versus healthy rats. Gastroenterology 109: 1173-1180.
45. McCarthy DM, (2009). GI bleeding: problems that persist. Gastrointest Endosc 70: 225-228.
46. McCarthy DM, (2010). Adverse effects of proton pump inhibitor drugs: clues and conclusions. Curr Opin Gastroenterol 26: 624-631.
47. Mizuno H, Sakamoto C, Matsuda K, Wada K, Uchida T, Noguchi H, et al,. (1997). Induction of cyclooxygenase 2 in gastric mucosal lesions and its inhibition by the specific antagonist delays healing in mice. Gastroenterology 112: 387-397. (Pubitemid 27078825)
48. Pirmohamed M, James S, Meakin S, Green C, Scott AK, Walley TJ, et al,. (2004). Adverse drug reactions as cause of admission to hospital: prospective analysis of 18 820 patients. Br Med J 329: 15-19. (Pubitemid 38869995)
49. Rainsford KD, Willis C, (1982). Relationship of gastric mucosal damage induced in pigs by antiinflammatory drugs to their effects on prostaglandin production. Dig Dis Sci 27: 624-635. (Pubitemid 12075492)
50. Reuter BK, Cirino G, Wallace JL, (1994). Markedly reduced intestinal toxicity of a diclofenac derivative. Life Sci 55: PL1-PL8. (Pubitemid 24185770)
51. Reuter BK, Asfaha S, Buret A, Sharkey KA, Wallace JL, (1996). Exacerbation of inflammation-associated colonic injury in rat through inhibition of cyclooxygenase-2. J Clin Invest 98: 2076-2085. (Pubitemid 26376296)
52. Reuter BK, Davies NM, Wallace JL, (1997). Nonsteroidal anti-inflammatory drug enteropathy in rats: role of permeability, bacteria, and enterohepatic circulation. Gastroenterology 112: 109-117. (Pubitemid 27008992)
53. Robert A, Asano T, (1977). Resistance of germ free rats to indomethacin-induced lesions. Prostaglandins 14: 331-341.
54. Robert A, Nezamis JE, Lancaster C, Hanchar AJ, (1979). Cytoprotection by prostaglandins in rats. Prevention of gastric necrosis produced by alcohol, HCl, NaOH, hypertonic NaCl, and thermal injury. Gastroenterology 77: 433-443. (Pubitemid 10132046)
55. Santucci L, Fiorucci S, Giansanti M, Brunori PM, Di Matteo FM, Morelli A, (1994). Pentoxifylline prevents indomethacin induced acute gastric mucosal damage in rats: role of tumour necrosis factor alpha. Gut 35: 909-915. (Pubitemid 24202720)
56. Scarpignato C, Hunt RH, (2010). Nonsteroidal anti-inflammatory drug-related injury to the gastrointestinal tract: clinical picture, pathogenesis, and prevention. Gastroenterol Clin North Am 39: 433-464.
57. Scheiman JM, Yeomans ND, Talley NJ, VAKIL N, Chan FK, Tulassay Z, et al,. (2006). Prevention of ulcers by esomeprazole in at-risk patients using non-selective NSAIDs and COX-2 inhibitors. Am J Gastroenterol 101: 701-710.
58. Serhan CN, Oliw E, (2001). Unorthodox routes to prostanoid formation: new twists in cyclooxygenase-initiated pathways. J Clin Invest 107: 1481-1489. (Pubitemid 32574630)
59. Serhan CN, Brain SD, Buckley CD, Gilroy DW, Haslett C, O'Neill LA, et al,. (2007). Resolution of inflammation: state of the art, definitions and terms. FASEB J 21: 325-332. (Pubitemid 46213480)
60. Shindo K, Machida M, Fukumura M, Koide K, Yamazaki R, (1998). Omeprazole induces altered bile acid metabolism. Gut 42: 266-271. (Pubitemid 28212183)
61. Somasundaram S, Sigthorsson G, Simpson RJ, Watts J, Jacob M, Tavares IA, et al,. (2000). Uncoupling of intestinal mitochondrial oxidative phosphorylation and inhibition of cyclooxygenase are required for the development of NSAID-enteropathy in the rat. Aliment Pharmacol Ther 14: 639-650. (Pubitemid 30240758)
62. Souza MHLP, Menezes de Lima O, Zamuner SR, Fiorucci S, Wallace JL, (2003). Gastritis increases resistance to aspirin-induced mucosal injury via COX-2-mediated lipoxin synthesis. Am J Physiol Gastrointest Liver Physiol 285: G54-G61. (Pubitemid 36736388)
63. Taha AS, Hudson N, Hawkey CJ, Swannell AJ, Trye PN, Cottrell J, et al,. (1996). Famotidine for the prevention of gastric and duodenal ulcers caused by nonsteroidal antiinflammatory drugs. N Engl J Med 334: 1435-1439. (Pubitemid 26157439)
64. Tanaka A, Hase S, Miyazawa T, Takeuchi K, (2002). Up-regulation of cyclooxygenase-2 by inhibition of cyclooxygenase-1: a key to nonsteroidal anti-inflammatory drug-induced intestinal damage. J Pharmacol Exp Ther 300: 754-761. (Pubitemid 34164976)
65. Uejima M, Kinouchi T, Kataoka K, Hiraokam I, Ohnishi Y, (1996). Role of intestinal bacteria in ileal ulcer formation in rats treated with a nonsteroidal anti-inflammatory drug. Microbiol Immunol 40: 553-560. (Pubitemid 26282108)
66. Wallace JL, (1993). Gastric ulceration: critical events at the neutrophil-endothelium interface. Can J Physiol Pharmacol 71: 98-102. (Pubitemid 23172130)
67. Wallace JL, (2007). Hydrogen sulfide-releasing anti-inflammatory drugs. Trends Pharmacol Sci 28: 501-505. (Pubitemid 47488507)
68. Wallace JL, (2008). Prostaglandins, NSAIDs, and gastric mucosal protection: why doesn't the stomach digest itself? Physiol Rev 88: 1547-1565.
69. Wallace JL, Devchand PR, (2005). Emerging roles for cyclooxygenase-2 in gastrointestinal mucosal defense. Br J Pharmacol 145: 275-282. (Pubitemid 40896072)
70. Wallace JL, Ferraz JG, (2010). New pharmacological therapies in gastrointestinal disease. Gastroenterol Clin North Am 39: 709-720.
71. Wallace JL, McKnight GW, (1990). The mucoid cap over superficial gastric damage in the rat. A high-pH microenvironment dissipated by nonsteroidal antiinflammatory drugs and endothelin. Gastroenterology 99: 295-304. (Pubitemid 20219083)
72. Wallace JL, McKnight GW, (1993). Characterization of a simple animal model for nonsteroidal anti-inflammatory drug induced antral ulcer. Can J Physiol Pharmacol 71: 447-452. (Pubitemid 23325436)
73. Wallace JL, Keenan CM, Granger DN, (1990). Gastric ulceration induced by nonsteroidal anti-inflammatory drugs is a neutrophil-dependent process. Am J Physiol 259: G462-G467. (Pubitemid 20317856)
74. Wallace JL, Arfors K-E, McKnight GW, (1991). A monoclonal antibody against the CD18 leukocyte adhesion molecule prevents indomethacin-induced gastric damage in the rabbit. Gastroenterology 100: 878-883.
75. Wallace JL, McKnight W, Miyasaka M, Tamatani T, Paulson J, Anderson DC, et al,. (1993). Role of endothelial adhesion molecules in NSAID-induced gastric mucosal injury. Am J Physiol 265: C993-C998.
76. Wallace JL, Reuter B, Cicala C, McKnight W, Grisham MB, Cirino G, (1994). Novel nonsteroidal anti-inflammatory drug derivatives with markedly reduced ulcerogenic properties in the rat. Gastroenterology 107: 173-179. (Pubitemid 24195359)
77. Wallace JL, McKnight W, Reuter BK, Vergnolle N, (2000). NSAID-induced gastric damage in rats: requirement of inhibition of both cyclooxygenase 1 and 2. Gastroenterology 119: 706-714.
78. Wallace JL, Caliendo G, Santagada V, CIRINO G, Fiorucci S, (2007). Gastrointestinal safety and anti-inflammatory effects of a hydrogen sulphide-releasing diclofenac derivative in the rat. Gastroenterology 132: 261-271. (Pubitemid 46108763)
79. Wallace JL, Caliendo G, Santagada V, Cirino G, (2010). Markedly reduced toxicity of a hydrogen sulfide-releasing derivative of naproxen (ATB-346). Br J Pharmacol 159: 1236-1246.
80. Wallace JL, Denou E, Vong L, Syer S, McKnight W, Jury J, et al,. (2011). Proton pump inhibitors and low-dose aspirin markedly exacerbate NSAID-induced small intestinal injury: link to dysbiosis? Gastroenterology 140: S-87.
81. Watanabe T, Higuchi K, Kobata H, Tanigawa T, Shiba M, Tominaga K, et al,. (2008). Non-steroidal anti-inflammatory drug-induced small intestinal damage is Toll-like receptor 4 dependent. Gut 57: 181-187. (Pubitemid 351158044)
82. Whittle BJ, (1981). Temporal relationship between cyclooxygenase inhibition, as measured by prostacyclin biosynthesis, and the gastrointestinal damage induced by indomethacin in the rat. Gastroenterology 80: 94-98. (Pubitemid 11213294)
83. Williams C, McColl KE, (2006). Review article: proton pump inhibitors and bacterial overgrowth. Aliment Pharmacol Ther 23: 3-10. (Pubitemid 43381161)
84. Yeomans ND, Tulassay Z, Juhasz L, Racz I, Howard JM, van Rensburg CJ, et al,. (1998). A comparison of omeprazole with ranitidine for ulcers associated with nonsteroidal anti-inflammatory drugs. Acid Suppression Trial: Ranitidine versus Omeprazole for NSAID-associated Ulcer Treatment (ASTRONAUT) Study Group. N Engl J Med 338: 719-726.
85. Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL, (2006). Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 20: 2118-2120.
86. Zhou Y, Dial EJ, Doyen R, Lichtenberger LM, (2010). Effect of indomethacin on bile acid-phospholipid interactions: implication for small intestinal injury induced by nonsteroidal anti-inflammatory drugs. Am J Physiol Gastrointest Liver Physiol 298: G722-G731.