Recent advances in NSAIDs-induced enteropathy therapeutics: New options, new challenges

Gastroenterology Research and Practice

Volumn 2013, Issue , 2013, Pages

  Lim, Yun Jeong ^a   Chun, Hoon Jai ^b  

^a Dongguk University Ilsan Hospital   (South Korea)

^b Korea University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; CELECOXIB; DICLOFENAC; ESOMEPRAZOLE; FAMOTIDINE; HYDROGEN SULFIDE; IBUPROFEN; INDOMETACIN; LANSOPRAZOLE; MISOPROSTOL; NAPROXEN; NITRIC OXIDE; NONSTEROID ANTIINFLAMMATORY AGENT; OMEPRAZOLE; PROBIOTIC AGENT; PROSTAGLANDIN DERIVATIVE; PROTON PUMP INHIBITOR; REBAMIPIDE; REVAPRAZAN; TEPRENONE;

ABDOMINAL PAIN; ANTIINFLAMMATORY ACTIVITY; BIFIDOBACTERIUM ADOLESCENTIS; CAPSULE ENDOSCOPY; CHEMOPROPHYLAXIS; DIARRHEA; DYSPEPSIA; ENZYME INHIBITION; FRACTURE; GASTRITIS; HUMAN; INTESTINE INJURY; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS CASEI; LOW DRUG DOSE; MALABSORPTION; NAUSEA; NONHUMAN; OSTEOPENIA; PROSTAGLANDIN SYNTHESIS; REVIEW;

EID: 84885357653     PISSN: 16876121     EISSN: 1687630X     Source Type: Journal    
DOI: 10.1155/2013/761060     Document Type: Review

References (62)

1. Graham D. Y., Opekun A. R., Willingham F. F., Qureshi W. A., Visible small-intestinal mucosal injury in chronic NSAID users. Clinical Gastroenterology and Hepatology 2005 3 1 55 59 2-s2.0-11844272068 10.1016/S1542-3565(04)00603-2 (Pubitemid 40092944)
2. Maiden L., Thjodleifsson B., Theodors A., Gonzalez J., Bjarnason I., A quantitative analysis of NSAID-induced small bowel pathology by capsule enteroscopy. Gastroenterology 2005 128 5 1172 1178 2-s2.0-19044396444 10.1053/j.gastro.2005.03.020
3. Tibble J. A., Sigthorsson G., Foster R., Scott D., Fagerhol M. K., Roseth A., Bjarnason I., High prevalence of NSAID enteropathy as shown by a simple faecal test. Gut 1999 45 3 362 366 2-s2.0-0032786449 (Pubitemid 29400711)
4. Fujimori S., Gudis K., Takahashi Y., Seo T., Yamada Y., Ehara A., Kobayashi T., Mitsui K., Yonezawa M., Tanaka S., Tatsuguchi A., Sakamoto C., Distribution of small intestinal mucosal injuries as a result of NSAID administration. European Journal of Clinical Investigation 2010 40 6 504 510 2-s2.0-77952174383 10.1111/j.1365-2362.2010.02290.x
5. Matsumoto T., Kudo T., Esaki M., Yano T., Yamamoto H., Sakamoto C., Goto H., Nakase H., Tanaka S., Matsui T., Sugano K., Iida M., Prevalence of non-steroidal anti-inflammatory drug-induced enteropathy determined by double-balloon endoscopy: a Japanese multicenter study. Scandinavian Journal of Gastroenterology 2008 43 4 490 496 2-s2.0-41349106207 10.1080/00365520701794121 (Pubitemid 351450993)
6. Maiden L., Capsule endoscopic diagnosis of nonsteroidal antiinflammatory drug-induced enteropathy. Journal of Gastroenterology 2009 44 19 64 71 2-s2.0-58849140520 10.1007/s00535-008-2248-8
7. Smale S., Tibble J., Sigthorsson G., Bjarnason I., Epidemiology and differential diagnosis of NSAID-induced injury to the mucosa of the small intestine. Best Practice and Research: Clinical Gastroenterology 2001 15 5 723 738 2-s2.0-0034764858 10.1053/bega.2001.0231 (Pubitemid 32982362)
8. Zuccaro G., Epidemiology of lower gastrointestinal bleeding. Best Practice and Research: Clinical Gastroenterology 2008 22 2 225 232 2-s2.0-40649103166 10.1016/j.bpg.2007.10.009 (Pubitemid 351372993)
9. Lanas A., Sopeña F., Nonsteroidal anti-inflammatory drugs and lower gastrointestinal complications. Gastroenterology Clinics of North America 2009 38 2 333 352 2-s2.0-65549161937 10.1016/j.gtc.2009.03.007
10. Scarpignato C., Hunt R. H., Nonsteroidal antiinflammatory drug-related injury to the gastrointestinal tract: clinical picture, pathogenesis, and prevention. Gastroenterology Clinics of North America 2010 39 3 433 464 2-s2.0-77957892163 10.1016/j.gtc.2010.08.010
11. Keum B., Chun H. J., Capsule endoscopy and double balloon enteroscopy for obscure gastrointestinal bleeding: which is better? Journal of Gastroenterology and Hepatology 2011 26 5 794 795 2-s2.0-79954565962 10.1111/j.1440-1746.2011. 06708.x
12. Lee B. J., Chun H. J., Koo J. S., Keum B., Park S. H., Kim D. R., Kwon Y. D., Kim Y. S., Jean Y. T., Lee H. S., Um S. H., Lee S. W., Choi J. H., Kim C. D., Ryu H. S., Analysis of the factors that affect the diagnostic yield of capsule endoscopy in patients with obscure gastrointestinal bleeding. The Korean Journal of Gastroenterology 2007 49 2 79 84 2-s2.0-53749102153
13. Park S. C., Chun H. J., Kang C. D., Sul D., Prevention and management of non-steroidal anti-inflammatory drugs-induced small intestinal injury. World Journal of Gastroenterology 2011 17 42 4647 4653 2-s2.0-82555204542 10.3748/wjg.v17.i42.4647
14. Lim Y. J., Yang C. H., Non-steroidal anti-inflammatory drug-induced enteropathy. Clinical Endoscopy 2012 45 2 138 144 10.5946/ce.2012.45.2.138
15. Arakawa T., Watanabe T., Tanigawa T., Tominaga K., Otani K., Nadatani Y., Fujiwara Y., Small intestinal injury caused by NSAIDs/aspirin: finding new from old. Current Medicinal Chemistry 2012 19 1 77 81 2-s2.0-84857581497
16. Wallace J. L., Ferraz J. G. P., New pharmacologic therapies in gastrointestinal disease. Gastroenterology Clinics of North America 2010 39 3 709 720 2-s2.0-77957927410 10.1016/j.gtc.2010.08.020
17. Goel G. A., Deshpande A., Lopez R., Hall G. S., van Duin D., Carey W. D., Increased rate of spontaneous bacterial peritonitis among cirrhotic patients receiving pharmacologic acid suppression. Clinical Gastroenterology and Hepatology 2012 10 4 422 427 2-s2.0-84858703547 10.1016/j.cgh.2011.11.019
18. Kim J. W., Lee K. L., Jeong J. B., Kim B. G., Shin S., Kim J. S., Jung H. C., Song I. S., Proton pump inhibitors as a risk factor for recurrence of Clostridium-difficile -associated diarrhea. World Journal of Gastroenterology 2010 16 28 3573 3577 2-s2.0-77955112230 10.3748/wjg.v16.i28.3573
19. Targownik L. E., Leslie W. D., Davison K. S., Goltzman D., Jamal S. A., Kreiger N., Josse R. G., Kaiser S. M., Kovacs C. S., Prior J. C., Zhou W., The relationship between proton pump inhibitor use and longitudinal change in bone mineral density: a population-based study [corrected] from the Canadian multicentre osteoporosis study (CaMos). The American Journal of Gastroenterology 2012 107 9 1361 1369 10.1038/ajg.2012.200
20. Hagiwara T., Mukaisho K., Nakayama T., Sugihara H., Hattori T., Long-term proton pump inhibitor administration worsens atrophic corpus gastritis and promotes adenocarcinoma development in Mongolian gerbils infected with Helicobacter pylori. Gut 2011 60 5 624 630 2-s2.0-79953732352 10.1136/gut.2010.207662
21. Wallace J. L., Syer S., Denou E., De Palma G., Vong L., McKnight W., Jury J., Bolla M., Bercik P., Collins S. M., Verdu E., Ongini E., Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology 2011 141 4 1314.e5 1322.e5 2-s2.0-80053596796 10.1053/j.gastro.2011.06.075
22. Lim Y. J., Phan T. M., Dial E. J., Graham D. Y., Lichtenberger L. M., In vitro and in vivo protection against indomethacin-induced small intestinal injury by proton pump inhibitors, acid pump antagonists, or indomethacin- phosphatidylcholine. Digestion 2012 86 2 171 177 10.1159/000339882
23. Yoda Y., Amagase K., Kato S., Tokioka S., Murano M., Kakimoto K., Nishio H., Umegaki E., Takeuchi K., Higuchi K., Prevention by lansoprazole, a proton pump inhibitor, of indomethacin-induced small intestinal ulceration in rats through induction of heme oxygenase-1. Journal of Physiology and Pharmacology 2010 61 3 287 294 2-s2.0-77957063789
24. Takeuchi K., Tanaka A., Kato S., Amagase K., Satoh H., Roles of COX inhibition in pathogenesis of NSAID-induced small intestinal damage. Clinica Chimica Acta 2010 411 7-8 459 466 2-s2.0-77649192712 10.1016/j.cca.2009.12.026
25. Laine L., Curtis S. P., Langman M., Jensen D. M., Cryer B., Kaur A., Cannon C. P., Lower gastrointestinal events in a double-blind trial of the cyclo-oxygenase-2 selective inhibitor etoricoxib and the traditional nonsteroidal anti-inflammatory drug diclofenac. Gastroenterology 2008 135 5 1517 1525 2-s2.0-55249118829 10.1053/j.gastro.2008.07.067
26. Goldstein J. L., Eisen G. M., Lewis B., Gralnek I. M., Zlotnick S., Fort J. G., Video capsule endoscopy to prospectively assess small bowel injury with celecoxib, naproxen plus omeprazole, and placebo. Clinical Gastroenterology and Hepatology 2005 3 2 133 141 2-s2.0-13544272038 10.1016/S1542-3565(04)00619-6 (Pubitemid 40220308)
27. Maiden L., Thjodleifsson B., Seigal A., Bjarnason I. I., Scott D., Birgisson S., Bjarnason I., Long-term effects of nonsteroidal anti-inflammatory drugs and cyclooxygenase-2 selective agents on the small bowel: a cross-sectional capsule enteroscopy study. Clinical Gastroenterology and Hepatology 2007 5 9 1040 1045 2-s2.0-35748970752 10.1016/j.cgh.2007.04.031
28. Laine L., Maller E. S., Yu C., Quan H., Simon T., Ulcer formation with low-dose enteric-coated aspirin and the effect of COX-2 selective inhibition: a double-blind trial. Gastroenterology 2004 127 2 395 402 2-s2.0-4143087071 10.1053/j.gastro.2004.05.001 (Pubitemid 39091887)
29. Watson D. J., Harper S. E., Zhao P. L., Quan H., Bolognese J. A., Simon T. J., Gastrointestinal tolerability of the selective cyclooxygenase-2 (COX-2) inhibitor rofecoxib compared with nonselective COX-1 and COX-2 inhibitors in osteoarthritis. Archives of Internal Medicine 2000 160 19 2998 3003 2-s2.0-0034706411 (Pubitemid 32009059)
30. Chan F. K. L., Lanas A., Scheiman J., Berger M. F., Nguyen H., Goldstein J. L., Celecoxib versus omeprazole and diclofenac in patients with osteoarthritis and rheumatoid arthritis (CONDOR): a randomised trial. The Lancet 2010 376 9736 173 179 2-s2.0-77955049924 10.1016/S0140-6736(10)60673-3
31. Fujimori S., Seo T., Gudis K., Ehara A., Kobayashi T., Mitsui K., Yonezawa M., Tanaka S., Tatsuguchi A., Sakamoto C., Prevention of nonsteroidal anti-inflammatory drug-induced small-intestinal injury by prostaglandin: a pilot randomized controlled trial evaluated by capsule endoscopy. Gastrointestinal Endoscopy 2009 69 7 1339 1346 2-s2.0-65749102226 10.1016/j.gie.2008.08.017
32. Watanabe T., Sugimori S., Kameda N., Machida H., Okazaki H., Tanigawa T., Watanabe K., Tominaga K., Fujiwara Y., Oshitani N., Higuchi K., Arakawa T., Small bowel injury by low-dose enteric-coated aspirin and treatment with misoprostol: a pilot study. Clinical Gastroenterology and Hepatology 2008 6 11 1279 1282 2-s2.0-55149116313 10.1016/j.cgh.2008.06.021
33. Niwa Y., Nakamura M., Ohmiya N., Maeda O., Ando T., Itoh A., Hirooka Y., Goto H., Efficacy of rebamipide for diclofenac-induced small-intestinal mucosal injuries in healthy subjects: a prospective, randomized, double-blinded, placebo-controlled, cross-over study. Journal of Gastroenterology 2008 43 4 270 276 2-s2.0-43249114126 10.1007/s00535-007-2155-4 (Pubitemid 351650037)
34. Fujimori S., Takahashi Y., Gudis K., Seo T., Ehara A., Kobayashi T., Mitsui K., Yonezawa M., Tanaka S., Tatsuguchi A., Sakamoto C., Rebamipide has the potential to reduce the intensity of NSAID-induced small intestinal injury: a double-blind, randomized, controlled trial evaluated by capsule endoscopy. Journal of Gastroenterology 2011 46 1 57 64 2-s2.0-78651477419 10.1007/s00535-010-0332-3
35. Mizukami K., Murakami K., Abe T., Inoue K., Uchida M., Okimoto T., Kodama M., Fujioka T., Aspirin-induced small bowel injuries and the preventive effect of rebamipide. World Journal of Gastroenterology 2011 17 46 5117 5122 2-s2.0-83155184052 10.3748/wjg.v17.i46.5117
36. Niwa Y., Nakamura M., Miyahara R., Ohmiya N., Watanabe O., Ando T., Kawashima H., Itoh A., Hirooka Y., Goto H., Geranylgeranylacetone protects against diclofenac-induced gastric and small intestinal mucosal injuries in healthy subjects: a prospective randomized placebo-controlled double-blind cross-over study. Digestion 2009 80 4 260 266 2-s2.0-70350059067 10.1159/000236032
37. Endo H., Higurashi T., Hosono K., Sakai E., Sekino Y., Iida H., Sakamoto Y., Koide T., Takahashi H., Yoneda M., Tokoro C., Inamori M., Abe Y., Nakajima A., Efficacy of Lactobacillus casei treatment on small bowel injury in chronic low-dose aspirin users: a pilot randomized controlled study. Journal of Gastroenterology 2011 46 7 894 905 2-s2.0-79960307847 10.1007/s00535-011-0410-1
38. Bjarnason I., Hayllar J., MacPherson A. J., Russell A. S., Side effects of nonsteroidal anti-inflammatory drugs on the small and large intestine in humans. Gastroenterology 1993 104 6 1832 1847 2-s2.0-0027244454 (Pubitemid 23235480)
39. Higuchi K., Umegaki E., Watanabe T., Yoda Y., Morita E., Murano M., Tokioka S., Arakawa T., Present status and strategy of NSAIDs-induced small bowel injury. Journal of Gastroenterology 2009 44 9 879 888 2-s2.0-70349651858 10.1007/s00535-009-0102-2
40. Wallace J. L., NSAID gastropathy and enteropathy: distinct pathogenesis likely necessitates distinct prevention strategies. The British Journal of Pharmacology 2012 165 1 67 74 2-s2.0-82955184551 10.1111/j.1476-5381.2011.01509. x
41. Konaka A., Kato S., Tanaka A., Kunikata T., Korolkiewicz R., Takeuchi K., Roles of enterobacteria, nitric oxide and neutrophil in pathogenesis of indomethacin-induced small intestinal lesions in rats. Pharmacological Research 1999 40 6 517 524 2-s2.0-0032763157 10.1006/phrs.1999.0550
42. Kent T. H., Cardelli R. M., Stamler F. W., Small intestinal ulcers and intestinal flora in rats given indomethacin. The American Journal of Pathology 1969 54 2 237 249 2-s2.0-0014468568
43. Uejima M., Kinouchi T., Kataoka K., Hiraoka I., Ohnishi Y., Role of intestinal bacteria in ileal ulcer formation in rats treated with a nonsteroidal antiinflammatory drug. Microbiology and Immunology 1996 40 8 553 560 2-s2.0-0029787769 (Pubitemid 26282108)
44. Watanabe T., Higuchi K., Kobata A., Nishio H., Tanigawa T., Shiba M., Tominaga K., Fujiwara Y., Oshitani N., Asahara T., Nomoto K., Takeuchi K., Arakawa T., Non-steroidal anti-inflammatory drug-induced small intestinal damage is toll-like receptor 4 dependent. Gut 2008 57 2 181 187 2-s2.0-38549158018 10.1136/gut.2007.125963 (Pubitemid 351158044)
45. Bjarnason I., Hayllar J., Smethurst P., Price A., Gumpel M. J., Metronidazole reduces intestinal inflammation and blood loss in non-steroidal anti-inflammatory drug induced enteropathy. Gut 1992 33 9 1204 1208 2-s2.0-0026785849
46. Reuter B. K., Davies N. M., Wallace J. L., Nonsteroidal anti-inflammatory drug enteropathy in rats: role of permeability, bacteria, and enterohepatic circulation. Gastroenterology 1997 112 1 109 117 2-s2.0-0031014088 (Pubitemid 27008992)
47. Zhou Y., Dial E. J., Doyen R., Lichtenberger L. M., Effect of indomethacin on bile acid-phospholipid interactions: implication for small intestinal injury induced by nonsteroidal anti-inflammatory drugs. The American Journal of Physiology-Gastrointestinal and Liver Physiology 2010 298 5 G722 G731 2-s2.0-77951447882 10.1152/ajpgi.00387.2009
48. Barrios J. M., Lichtenberger L. M., Role of biliary phosphatidylcholine in bile acid protection and nsaid injury of the lleal mucosa in rats. Gastroenterology 2000 118 6 1179 1186 2-s2.0-0034128638 (Pubitemid 30346995)
49. Lichtenberger L. M., Barron M., Marathi U., Association of phosphatidylcholine and nsaids as a novel strategy to reduce gastrointestinal toxicity. Drugs of Today 2009 45 12 877 890 2-s2.0-77949413862 1396674/dot.2009.45.12.1441075
50. Lichtenberger L. M., Wang Z. M., Romero J. J., Ulloa C., Perez J. C., Giraud-M. N., Barreto J. C., Non-steroidal anti-inflammatory drugs (NSAIDs) associate with zwitterionic phospholipids: insight into the mechanism and reversal of NSAID-induced gastrointestinal injury. Nature Medicine 1995 1 2 154 158 2-s2.0-0028939954
51. Lichtenberger L. M., Zhou Y., Jayaraman V., Doyen J. R., O'Neil R. G., Dial E. J., Volk D. E., Gorenstein D. G., Boggara M. B., Krishnamoorti R., Insight into NSAID-induced membrane alterations, pathogenesis and therapeutics: characterization of interaction of NSAIDs with phosphatidylcholine. Biochimica et Biophysica Acta 2012 1821 7 994 1002 10.1016/j.bbalip.2012.04.002
52. Lanza F. L., Marathi U. K., Anand B. S., Lichtenberger L. M., Clinical trial: comparison of ibuprofen-phosphatidylcholine and ibuprofen on the gastrointestinal safety and analgesic efficacy in osteoarthritic patients. Alimentary Pharmacology and Therapeutics 2008 28 4 431 442 2-s2.0-47749083511 10.1111/j.1365-2036.2008.03765.x (Pubitemid 352033288)
53. Lim Y. J., Lee J. S., Ku Y. S., Hahm K. B., Rescue strategies against non-steroidal anti-inflammatory drug-induced gastroduodenal damage. Journal of Gastroenterology and Hepatology 2009 24 7 1169 1178 2-s2.0-68749085157 10.1111/j.1440-1746.2009.05929.x
54. Wallace J. L., Del Soldato P., The therapeutic potential of NO-NSAIDs. Fundamental and Clinical Pharmacology 2003 17 1 11 20 2-s2.0-0037323905 10.1046/j.1472-8206.2003.00125.x (Pubitemid 36241449)
55. Blackler R., Syer S., Bolla M., Ongini E., Wallace J. L., Gastrointestinal-sparing effects of novel nsaids in rats with compromised mucosal defence. PLoS ONE 2012 7 4 2-s2.0-84859509888 10.1371/journal.pone. 0035196 e35196
56. Fiorucci S., Antonelli E., Distrutti E., Rizzo G., Mencarelli A., Orlandi S., Zanardo R., Renga B., Di Sante M., Morelli A., Cirino G., Wallace J. L., Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology 2005 129 4 1210 1224 2-s2.0-26844568431 10.1053/j.gastro.2005.07.060 (Pubitemid 41446861)
57. Wallace J. L., Hydrogen sulfide-releasing anti-inflammatory drugs. Trends in Pharmacological Sciences 2007 28 10 501 505 2-s2.0-34748841476 10.1016/j.tips.2007.09.003 (Pubitemid 47488507)
58. Montalto M., Maggiano N., Ricci R., Curigliano V., Santoro L., Di Nicuolo F., Vecchio F. M., Gasbarrini A., Gasbarrini G., Lactobacillus acidophilus protects tight junctions from aspirin damage in HT-29 cells. Digestion 2004 69 4 225 228 2-s2.0-4344653745 10.1159/000079152 (Pubitemid 39140468)
59. Kamil R., Geier M. S., Butler R. N., Howarth G. S., Lactobacillus rhamnosus GG exacerbates intestinal ulceration in a model of indomethacin-induced enteropathy. Digestive Diseases and Sciences 2007 52 5 1247 1252 2-s2.0-34247221616 10.1007/s10620-006-9443-3 (Pubitemid 46626177)
60. Gotteland M., Cruchet S., Verbeke S., Effect of Lactobacillus ingestion on the gastrointestinal mucosal barrier alterations induced by indometacin in humans. Alimentary Pharmacology and Therapeutics 2001 15 1 11 17 2-s2.0-0035182040 10.1046/j.1365-2036.2001.00898.x (Pubitemid 32055581)
61. Montalto M., Gallo A., Curigliano V., D'Onofrio F., Santoro L., Covino M., Dalvai S., Gasbarrini A., Gasbarrini G., Clinical trial: the effects of a probiotic mixture on non-steroidal anti-inflammatory drug enteropathy-a randomized, double-blind, cross-over, placebo-controlled study. Alimentary Pharmacology and Therapeutics 2010 32 2 209 214 2-s2.0-77953792873 10.1111/j.1365-2036.2010.04324.x
62. Lanas A., García-Rodríguez L. A., Polo-Tomás M., Ponce M., Alonso-Abreu I., Perez-Aisa M. A., Perez-Gisbert J., Bujanda L., Castro M., Muñoz M., Rodrigo L., Calvet X., Del-Pino D., Garcia S., Time trends and impact of upper and lower gastrointestinal bleeding and perforation in clinical practice. The American Journal of Gastroenterology 2009 104 2 1633 1644 10.1038/ajg.2009.164