NSAID-induced enteropathy: the current state of the problem


Cite item

Full Text

Abstract

The review analyzes the main etiological and pathogenetic mechanisms of the development of NSAID-enteropathy. Particular attention is paid to the role of intestinal microbiota in the manifestation and progression of NSAID-enteropathy. The special role of probiotics in the prevention and treatment of NSAIDs enteropathy is considered.

About the authors

A A Svistunov

I.M. Sechenov First Moscow State Medical University, Ministry of Health of Russia (Sechenov University)

Email: svistunov@sechenov.ru
д.м.н., проф., член-корр. РАН, первый проректор Первого МГМУ им. И.М. Сеченова; ORCID: 0000-0003-1592-5703 Moscow, Russia

M A Osadchuk

I.M. Sechenov First Moscow State Medical University, Ministry of Health of Russia (Sechenov University)

Email: osadchuk.mikhail@yandex.ru
д.м.н., проф., зав. каф. поликлинической терапии лечебного фак-та Первого МГМУ им. И.М. Сеченова; ORCID: 0000-0003-0485-6802 Moscow, Russia

N V Kireeva

I.M. Sechenov First Moscow State Medical University, Ministry of Health of Russia (Sechenov University)

Email: kireeva_nat@inbox.ru
к.м.н., доц. каф. поликлинической терапии лечебного фак-та Первого МГМУ им. И.М. Сеченова; ORCID: 0000-0002-3467-886X Moscow, Russia

A A Hudarova

I.M. Sechenov First Moscow State Medical University, Ministry of Health of Russia (Sechenov University)

клинический врач-ординатор каф. поликлинической терапии лечебного фак-та Первого МГМУ им. И.М. Сеченова; тел.:+7(926)457-43-45; ORCID: 0000-0002-0689-7934 Moscow, Russia

E E Achkasov

I.M. Sechenov First Moscow State Medical University, Ministry of Health of Russia (Sechenov University)

д.м.н., профессор, зав. каф. спортивной медицины и медицинской реабилитации лечебного фак-та Первого МГМУ им. И.М. Сеченова; тел.: +7(903)733-07-76; ORCID: 0000-0001-9964-5199 Moscow, Russia

References

  1. Wallace J.L. Mechanisms, prevention and clinical implications of non - steroidal anti - inflammatory drug - enteropathy. World J Gastroenterol. 2013 Mar 28;19(12):1861-1876. doi: 10.3748/wjg.v19.i12.1861
  2. Smecuol E, Sanchez M, Suarez A, et al. Low - dose aspirin affects the small bowel mucosa: results of a pilot study with a multidimensional assessment. Clin Gastroenterol Hepatol. 2009 May;7(5):524-529. doi: 10.1016/j.cgh.2008.12.019
  3. Fortun P.J, Hawkey C.J. Nonsteroidal antiinflammatory drugs and the small intestine. Curr Opin Gastroenterol. 2007 Mar;23(2):134-141.
  4. 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 misoprostal: a pilot study. Clin Gastroenterol Hepatol. 2008 Nov;6(11):1279-1282. doi: 10.1016/j.cgh.2008.06.021
  5. Endo H, Hosono K, Inamori M, Kato S, Nozaki Y, Yoneda K, Akiyama T, Fujita K, Takahashi H, Yoneda M, Abe Y, Kirikoshi H, Kobayashi N, Kubota K, Saito S, Matsuhashi N, Nakajima A. Incidence of small bowel injury induced by low - dose aspirin: a crossover study using capsule endoscopy in healthy volunteers. Digestion. 2009;79(1):44-51. doi: 10.1159/000204465
  6. Bjarnason I, Hayllar J, Mac Pherson A.J, Russell A.S. Side effects of nonsteroidal anti - inflammatory drugs on the small and large intestine in humans. Gastroenterology. 1993;104:1832-1847.
  7. Utzeri E, Usai P. Role of non - steroidal anti - inflammatory drugs on intestinal permeability and nonalcoholic fatty liver disease. World J Gastroenterol. 2017 Jun 14;23(22):3954-3963. doi: 10.3748/wjg.v2 3.i22.3954
  8. Lanas A, Sopeña F. Nonsteroidal anti - inflammatory drugs and lower gastrointestinal complications. Gastroenterol Clin North Am. 2009 Jun;38(2):333-352. doi: 10.1016/j.gtc.2009.03.007
  9. Wallace J.L. NSAID gastropathy and enteropathy: distinct pathogenesis likely necessitates distinct prevention strategies. Br J Pharmacol. 2012 Jan;165(1):67-74. doi: 10.1111/j.1476-5381.2011.01509.x
  10. Goldstein J.L, Eisen G.M, Lewis B, et al. Video capsule endoscopy to prospectively assess small bowel injury with celecoxib, naproxen plus omperpazole, and placebo. Clin Gastroenterol Hepatol. 2005;3:133-141.
  11. Lengeling R, Mitros F, Brennan J, et al. Ulcerative enteritis encountered at ileo - colonoscopy: likely role of nonsteroidal agents. Clin Gastroenterol Hepatol. 2003;1(3):1160-1169. doi: 10.1016/S1542-3565 (03)70031-7
  12. Nagar A.B, Proctor D.D. NSAID-induced ulceration of the small intestine: diagnosis. In: Feldman M, Friedman L.S, Brandt L.J, eds. Sleisenger and Fordtran's gastrointestinal and liver disease. 8th ed. Philadelphia: Saunders Elsevier; 2006. P. 2590.
  13. Scarpignato C, Dolak W, Lanas A, Matzneller P, Renzulli C, Grimaldi M, Zeitlinger M, Bjarnason I. Rifaximin Reduces the Number and Severity of Intestinal Lesions Associated With Use of Nonsteroidal Anti-Inflammatory Drugs in Humans. Gastroenterology. 2017 Apr;152(5): 980-982.e3. doi: 10.1053/j.gastro.2016.12.007
  14. Wallace J.L, Syer S, Denou E, de Palma G, Vong L, Mc Knight W, Jury J, Bolla M, Bercik P, Collins S.M, et al. Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology. 2011;141:1314-1322, 1322.e1-5. doi: 10.1053/j.gastro.2011.06.075
  15. Tanaka A, Hase S, Miyazawa T, Takeuchi K. Up - regulation of cyclooxygenase-2 by inhibition of cyclooxygenase-1: a key to nonsteroidal anti - inflammatory drug - induced intestinal damage. J Pharmacol Exp Ther. 2002;300:754-761.
  16. Bayer Quick Release Crystals. (Accessed August 24, 2009). Available from: http://www.wonderdrug.com/products/es/es_crystals.htm
  17. Scheiman J.M, Yeomans N.D, Talley N.J, Vakil N, Chan F.K, Tulassay Z, et al. Prevention of ulcers by esomeprazole in at - risk patients using non - selective NSAIDs and COX-2 inhibitors. Am J Gastroenterol. 2006;101:701-710.
  18. Zhao Y, Encinosa W. Hospitalizations for Gastrointestinal Bleeding in 1998 and 2006: Statistical Brief #65. Healthcare Cost and Utilization Project (HCUP) Statistical Briefs [Internet]. Rockville (MD): Agency for Healthcare Research and Quality (US); 2006 Feb-.2008 Dec.
  19. 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):e35196. doi: 10.1371/journal.pone.0035196. Epub 2012 Apr 9.
  20. Satoh H, Amagase K, Takeuchi K. Exacerbation of nonsteroidal anti - inflammatory drug - induced small intestinal lesions by antisecretory drugs in rats: the role of intestinal motility. J Pharmacol Exp Ther. 2012 Nov;343(2):270-277. doi: 10.1124/jpet.112.197475
  21. Watanabe T, Tanigawa T, Nadatani Y, Nagami Y, Sugimori S, Okazaki H, Yamagami H, Watanabe K, Tominaga K, Fujiwara Y, Koike T, Arakawa T. Risk factors for severe nonsteroidal anti - inflammatory drug - induced small intestinal damage. Dig Liver Dis. 2013 May;45(5): 390-395. doi: 10.1016/j.dld.2012.12.005
  22. Fujimori S. What are the effects of proton pump inhibitors on the small intestine? World J Gastroenterol. 2015 Jun 14;21(22):6817-6819. doi: 10.3748/wjg.v21.i22.6817
  23. Wallace J.L, Caliendo G, Santagada V, Cirino G, Fiorucci S. Gastrointestinal safety and anti - inflammatory effects of a hydrogen sulphide - releasing diclofenac derivative in the rat. Gastroenterology. 2007;132:261-271 doi: 10.1053/j.gastro.2006.11.042
  24. Flannigan K.L, Ferraz J.G, Wang R, Wallace J.L. Enhanced synthesis and diminished degradation of hydrogen sulfide in experimental colitis: a site - specific, pro - resolution mechanism. PLoS One. 2013 Aug 5;8(8):e71962. doi: 10.1371/journal.pone.0071962. Print 2013.
  25. Fiorucci S, Orlandi S, Mencarelli A, Caliendo G, Santagada V, Distrutti E, Santucci L, Cirino G, Wallace JL. Enhanced activity of a hydrogen sulphide - releasing derivative of mesalamine (ATB-429) in a mouse model of colitis. Br J Pharmacol. 2007 Apr;150(8):996-1002. Epub 2007 Mar 5.
  26. Somasundaram S, Rafi S, Hayllar J, Sigthorsson G, Jacob M, Price A.B, et al. Mitochondrial damage: a possible mechanism of the ‘topical’ phase of NSAID induced injury to the rat intestine. Gut. 1997;41:344-353.
  27. 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;112:109-117.
  28. Hofmann A.F. The continuing importance of bile acids in liver and intestinal disease. Arch Intern Med. 1999;159:2647-2658.
  29. Martinez-Augustin O, Sanchez de Medina F. Intestinal bile acid physiology and pathophysiology. World J Gastroenterol. 2008;14:5630-5640. doi: 10.3748/wjg.14.5630
  30. Saitta K.S, Zhang C, Lee K.K, Fujimoto K, Redinbo M.R, Boelsterli U.A. Bacterial β - glucuronidase inhibition protects mice against enteropathy induced by indomethacin, ketoprofen or diclofenac: mode of action and pharmacokinetics. Xenobiotica. 2014;44:28-35. doi: 10.3109/ 00498254.2013.811314
  31. Wax J, Clinger W.A, Varner P, Bass P, Winder C.V. Relationship of the enterohepatic cycle to ulcerogenesis in the rat small bowel with flufenamic acid. Gastroenterology. 1970;58:772-780.
  32. Elliott S.N, Buret A, Mc Knight W, Miller M.J, Wallace J.L. Bacteria rapidly colonize and modulate healing of gastric ulcers in rats. Am J Physiol. 1998 Sep;275(3 Pt 1):G425-G432.
  33. Yamada T, Deitch E, Specian R.D, Perry M.A, Sartor R.B, Grisham M.B. Mechanisms of acute and chronic intestinal inflammation induced by indomethacin. Inflammation. 1993 Dec;17(6):641-662.
  34. Mujagic Z, de Vos P, Boekschoten M.V, Govers C, Pieters H.H, de Wit N.J, et al. The effects of Lactobacillus plantarum on small intestinal barrier function and mucosal gene transcription; a randomized double - blind placebo controlled trial. Sci Rep. 2017;7:40128. doi: 10.1038/srep 40128
  35. Kim H.J, Kim Y.J, Lee S.H, Yu J, Jeong S.K, Hong S.J. Effects of Lactobacillus rhamnosus on allergic march model by suppressing Th2, Th17, and TSLP responses via CD4(+)CD25(+)Foxp3(+) Tregs. Clin Immunol. 2014;153(1):178-186. doi: 10.1016/j.clim.2014.04.008
  36. Smelt M.J, de Haan B.J, Bron P.A, van Swam I, Meijerink M, Wells J.M, et al. The impact of Lactobacillus plantarum WCFS1 teichoic acid D-alanylation on the generation of effector and regulatory T-cells in healthy mice. PLoS One. 2013;8(4):e63099. doi: 10.1371/journal. pone.0063099/
  37. Yaqoob P. Ageing, immunity and influenza: a role for probiotics. Proc Nutr Soc. 2014;73(2):309-317. doi: 10.1017/S0029665113003777
  38. Meijerink M, van Hemert S, Taverne N, Wels M, de Vos P, Bron P.A, et al. Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS One. 2010;5(5):e10632. doi: 10.1371/journal. pone.0010632
  39. Seddik H.A, Bendali F, Gancel F, Fliss I, Spano G, Drider D. Lactobacillus plantarum and its probiotic and food potentialities. Probiotics Antimicrob Proteins. 2017;9:111-122.10.doi: 1007/s12602-017-9264-z
  40. Otani K, Tanigawa T, Watanabe T, Shimada S, Nadatani Y, Nagami Y, Tanaka F, Kamata N, Yamagami H, Shiba M, Tominaga K, Fujiwara Y, Arakawa T. Microbiota Plays a Key Role in Non-Steroidal Anti-Inflammatory Drug-Induced Small Intestinal Damage. Digestion. 2017;95(1):22-28. doi: 10.1159/000452356
  41. Scarpignato C, Lanas A, Bjarnason I. Reply. Gastroenterology. 2017 Aug;153(2):612-613. doi: 10.1053/j.gastro.2017.06.047
  42. Syer S.D, Blackler R.W, Martin R, de Palma G, Rossi L, Verdu E, Bercik P, Surette M.G, Aucouturier A, Langella P, Wallace J.L. NSAID enteropathy and bacteria: a complicated relationship. J Gastroenterol. 2015 Apr;50(4):387-393. doi: 10.1007/s00535-014-1032-1
  43. De Vos P, Mujagic Z, de Haan B.J, Siezen R.J, Bron P.A, Meijerink M, Wells J.M, Masclee A.A.M, Boekschoten M.V, Faas M.M, Troost F.J. Lactobacillus plantarum Strains Can Enhance Human Mucosal and Systemic Immunity and Prevent Non - steroidal Anti - inflammatory Drug Induced Reduction in T Regulatory Cells. Front Immunol. 2017 Aug 23;8:1000. doi: 10.3389/fimmu.2017.01000. eCollection 2017.
  44. Byun S.J, Lim T.J, Lim Y.J, Seo J.G, Chung M.J. In vivo effects of s - pantoprazole, polaprenzinc, and probiotic blend on chronic small intestinal injury induced by indomethacin. Benef Microbes. 2016 Nov 30;7(5):731-737. doi: 10.3920/BM2016.0029. Epub 2016 Nov 8.
  45. Bai K. On the mechanism of cereobiogen readjustment to dysbiosis. Prog Clin Biol Res. 1985;181:169-170.
  46. Kanareykina S.K, Misautova A.A, Zlatkina A.R, Levina E.N. Proteus dysbioses in patients with ulcerative colitis. Nahrung. 1987;31:557-561.
  47. Knoke M, Bernhardt H. Clinical significance of changes of flora in the upper digestive tract. Infection. 1989;17:255-258.
  48. Tamboli C.P, Neut C, Desreumaux P, Colombel J.F. Dysbiosis in inflammatory bowel disease. Gut. 2004;53:1-4.
  49. Tilg H, Moschen A.R. Microbiota and diabetes: an evolving relationship. Gut. 2014;63:1513-1521. doi: 10.1136/gutjnl-2014-306928
  50. Henao-Mejia J, Elinav E, Jin C, Hao L, Mehal W.Z, Strowig T, Thaiss C.A, Kau A.L, Eisenbarth S.C, Jurczak M.J, et al. Inflammasome - mediated dysbiosis regulates progression of NAFLD and obesity. Nature. 2012;482:179-185. doi: 10.1038/nature10809
  51. Mc Lean M.H, Dieguez D, Miller L.M, Young H.A. Does the microbiota play a role in the pathogenesis of autoimmune diseases? Gut. 2015;64:332-341. doi: 10.1136/gutjnl-2014-308514
  52. Vernazza C.L, Gibson G.R, Rastall R.A. Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium. J Appl Microbiol. 2006;100:846-853. doi: 10.1111/j.1365-2672.2006.02832.x
  53. Matsumoto M, Ohishi H, Benno Y. H+-ATPase activity in Bifidobacterium with special reference to acid tolerance. Int J Food Microbiol. 2004;93:109-113. doi: 10.1016/j.ijfoodmicro.2003.10.009
  54. De Vrese M. The probiotic effects of LA-5 and BB-12 - an overview. Chr Hansen Monograph, June 2003.
  55. Осадчук М.А., Осадчук М.М. Синдром раздраженного кишечника и микробиота: пути оптимизации терапии. Врач. 2015;(5):47-51.
  56. Осадчук М.А., Осадчук М.М. Синдром перекреста функциональной диспепсии, гастроэзофагеальной рефлюксной болезни и синдрома раздраженного кишечника: оптимизация терапии. Русский медицинский журнал. 2015;23(28):1690-1692.
  57. Commane D.M, Shortt C.T, Silvi S, Cresci A, Hughes R.M, Rowland I.R. Effects of fermentation products of pro - and prebiotics on trans - epithelial electrical resistance in an in vitro model of the colon. Nutr Cancer. 2005;51:102-109. doi: 10.1207/s15327914nc5101_14

Copyright (c) 2018 Consilium Medicum

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
 
 


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies