Skip to main content

Advertisement

SpringerLink
Log in

Radiation Enteritis

  • Small Intestine (J Sellin, Section Editor)
  • Published:
Current Gastroenterology Reports Aims and scope Submit manuscript

Abstract

Radiation enteritis continues to be a major health concern in recipients of radiation therapy. The incidence of radiation enteritis is expected to continue to rise during the coming years paralleling the unprecedented use of radiotherapy in pelvic cancers. Radiation enteritis can present as either an acute or chronic syndrome. The acute form presents within hours to days of radiation exposure and typically resolves within few weeks. The chronic form may present as early as 2 months or as long as 30 years after exposure. Risk factors can be divided into patient and treatment-related factors. Chronic radiation enteritis is characterized by progressive obliterative endarteritis with exaggerated submucosal fibrosis and can manifest by stricturing, formation of fistulae, local abscesses, perforation, and bleeding. In the right clinical context, diagnosis can be confirmed by cross-sectional imaging, flexible or video capsule endoscopy. Present treatment strategies are directed primarily towards symptom relief and management of emerging complications. Recently, however, there has been a shift towards rational drug design based on improved understanding of the molecular basis of disease in an effort to limit the fibrotic process and prevent organ damage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Walsh D. Deep tissue traumatism from roentgen ray exposure. Br Med J. 1897;2:272–3.

    PubMed Central  PubMed  CAS  Google Scholar 

  2. Grubbe EH. The origin and birth of x-ray therapy. Urol Cutan Rev. 1947;51:375–9.

    PubMed  CAS  Google Scholar 

  3. Goldstein HI. The discovery of the roentgen rays; the contribution of Wilhelm Konrad Roentgen to science. J Int Coll Surg. 1946;9:688–93.

    PubMed  CAS  Google Scholar 

  4. Warren SL, Whipple GH. Roentgen Ray intoxication: Iv. Intestinal lesions and acute intoxication produced by radiation in a variety of animals. J Exp Med. 1923;38:741–52.

    PubMed Central  PubMed  CAS  Google Scholar 

  5. Shadad AK, Sullivan FJ, Martin JD, Egan LJ. Gastrointestinal radiation injury: prevention and treatment. World J Gastroenterol. 2013;19:199–208.

    PubMed Central  PubMed  Google Scholar 

  6. Andreyev HJ. Gastrointestinal problems after pelvic radiotherapy: the past, the present and the future. Clin Oncol. 2007;19:790–9.

    CAS  Google Scholar 

  7. Zimmerer T, Bocker U, Wenz F, Singer MV. Medical prevention and treatment of acute and chronic radiation induced enteritis–is there any proven therapy? A short review. Z Gastroenterol. 2008;46:441–8.

    PubMed  CAS  Google Scholar 

  8. Gerard JP, Conroy T, Bonnetain F, et al. Preoperative radiotherapy with or without concurrent fluorouracil and leucovorin in T3-4 rectal cancers: results of FFCD 9203. J Clin Oncol Off J Am Soc Clin Oncol. 2006;24:4620–5.

    Google Scholar 

  9. Zhu Y, Zhou J, Tao G. Molecular aspects of chronic radiation enteritis. Clin Investig Med Med Clin Exp. 2011;34:E119–24.

    CAS  Google Scholar 

  10. Abayomi JC, Kirwan J, Hackett AF. Coping mechanisms used by women in an attempt to avoid symptoms of chronic radiation enteritis. J Hum Nutr Diet Off J Br Diet Assoc. 2009;22:310–6.

    CAS  Google Scholar 

  11. Hungness ES, Fischer JE. Radiation enteritis: sometimes the treatment is worse than the disease. Curr Surg. 2000;57:573–7.

    PubMed  Google Scholar 

  12. Seal M, Naito Y, Barreto R, Lorenzetti A, Safran P, Marotta F. Experimental radiotherapy-induced enteritis: a probiotic interventional study. J Dig Dis. 2007;8:143–7.

    PubMed  Google Scholar 

  13. Waddell BE, Rodriguez-Bigas MA, Lee RJ, Weber TK, Petrelli NJ. Prevention of chronic radiation enteritis. J Am Coll Surg. 1999;189:611–24.

    PubMed  CAS  Google Scholar 

  14. Sher ME, Bauer J. Radiation-induced enteropathy. Am J Gastroenterol. 1990;85:121–8.

    PubMed  CAS  Google Scholar 

  15. Andreyev HJ, Vlavianos P, Blake P, Dearnaley D, Norman AR, Tait D. Gastrointestinal symptoms after pelvic radiotherapy: role for the gastroenterologist? Int J Radiat Oncol Biol Phys. 2005;62:1464–71.

    PubMed  Google Scholar 

  16. Cox JD, Byhardt RW, Wilson JF, Haas JS, Komaki R, Olson LE. Complications of radiation therapy and factors in their prevention. World J Surg. 1986;10:171–88.

    PubMed  CAS  Google Scholar 

  17. Hauer-Jensen M, Wang J, Denham JW. Bowel injury: current and evolving management strategies. Semin Radiat Oncol. 2003;13:357–71.

    PubMed  Google Scholar 

  18. Theis VS, Sripadam R, Ramani V, Lal S. Chronic radiation enteritis. Clin Oncol. 2010;22:70–83.

    CAS  Google Scholar 

  19. Ooi BS, Tjandra JJ, Green MD. Morbidities of adjuvant chemotherapy and radiotherapy for resectable rectal cancer: an overview. Dis Colon Rectum. 1999;42:403–18.

    PubMed  CAS  Google Scholar 

  20. Langley RE, Bump EA, Quartuccio SG, Medeiros D, Braunhut SJ. Radiation-induced apoptosis in microvascular endothelial cells. Br J Cancer. 1997;75:666–72.

    PubMed Central  PubMed  CAS  Google Scholar 

  21. Leadon SA. Repair of DNA damage produced by ionizing radiation: a minireview. Semin Radiat Oncol. 1996;6:295–305.

    PubMed  Google Scholar 

  22. Clarke AR, Gledhill S, Hooper ML, Bird CC, Wyllie AH. p53 dependence of early apoptotic and proliferative responses within the mouse intestinal epithelium following gamma-irradiation. Oncogene. 1994;9:1767–73.

    PubMed  CAS  Google Scholar 

  23. Potten CS, Booth C. The role of radiation-induced and spontaneous apoptosis in the homeostasis of the gastrointestinal epithelium: a brief review. Comp Biochem Physiol B Biochem Mol Biol. 1997;118:473–8.

    PubMed  CAS  Google Scholar 

  24. Dublineau I, Grison S, Grandcolas L, et al. Effects of chronic 137Cs ingestion on barrier properties of jejunal epithelium in rats. J Toxicol Environ Health Part A. 2007;70:810–9.

    PubMed  CAS  Google Scholar 

  25. Guzman-Stein G, Bonsack M, Liberty J, Delaney JP. Abdominal radiation causes bacterial translocation. J Surg Res. 1989;46:104–7.

    PubMed  CAS  Google Scholar 

  26. Baker DG, Krochak RJ. The response of the microvascular system to radiation: a review. Cancer Investig. 1989;7:287–94.

    CAS  Google Scholar 

  27. Hopewell JW, Calvo W, Jaenke R, Reinhold HS, Robbins ME, Whitehouse EM. Microvasculature and radiation damage. Recent Results Cancer Res Fortschr Krebsforschung Progres Rech Cancer. 1993;130:1–16.

    CAS  Google Scholar 

  28. Paris F, Fuks Z, Kang A, et al. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science. 2001;293:293–7.

    PubMed  CAS  Google Scholar 

  29. Wang J, Zheng H, Ou X, Fink LM, Hauer-Jensen M. Deficiency of microvascular thrombomodulin and up-regulation of protease-activated receptor-1 in irradiated rat intestine: possible link between endothelial dysfunction and chronic radiation fibrosis. Am J Pathol. 2002;160:2063–72.

    PubMed Central  PubMed  CAS  Google Scholar 

  30. Verheij M, Dewit LG, Boomgaard MN, Brinkman HJ, van Mourik JA. Ionizing radiation enhances platelet adhesion to the extracellular matrix of human endothelial cells by an increase in the release of von Willebrand factor. Radiat Res. 1994;137:202–7.

    PubMed  CAS  Google Scholar 

  31. Dunn MM, Drab EA, Rubin DB. Effects of irradiation on endothelial cell-polymorphonuclear leukocyte interactions. J Appl Physiol. 1986;60:1932–7.

    PubMed  CAS  Google Scholar 

  32. Wang J, Boerma M, Fu Q, Hauer-Jensen M. Significance of endothelial dysfunction in the pathogenesis of early and delayed radiation enteropathy. World J Gastroenterol. 2007;13:3047–55.

    PubMed  CAS  Google Scholar 

  33. Denham JW, Hauer-Jensen M. The radiotherapeutic injury–a complex ‘wound’. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2002;63:129–45.

    Google Scholar 

  34. Lebrun F, Francois A, Vergnet M, Lebaron-Jacobs L, Gourmelon P, Griffiths NM. Ionizing radiation stimulates muscarinic regulation of rat intestinal mucosal function. Am J Physiol. 1998;275:G1333–40.

    PubMed  CAS  Google Scholar 

  35. Classen J, Belka C, Paulsen F, Budach W, Hoffmann W, Bamberg M. Radiation-induced gastrointestinal toxicity. Pathophysiology, approaches to treatment and prophylaxis. Strahlenther Onkol Organ Deutsch Rontgengesellschaft. 1998;174 Suppl 3:82–4.

    Google Scholar 

  36. Wedlake L, Thomas K, McGough C, Andreyev HJ. Small bowel bacterial overgrowth and lactose intolerance during radical pelvic radiotherapy: An observational study. Eur J Cancer. 2008;44:2212–7.

    PubMed  CAS  Google Scholar 

  37. Sandle GI. Salt and water absorption in the human colon: a modern appraisal. Gut. 1998;43:294–9.

    PubMed Central  PubMed  CAS  Google Scholar 

  38. Konishi T, Watanabe T, Nagawa H. Treatment of local ischaemia: another promising approach for gastrointestinal complications of pelvic radiotherapy. Gut. 2006;55:1209.

    PubMed Central  PubMed  CAS  Google Scholar 

  39. Yarnold J, Brotons MC. Pathogenetic mechanisms in radiation fibrosis. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2010;97:149–61.

    CAS  Google Scholar 

  40. Gervaz P, Morel P, Vozenin-Brotons MC. Molecular aspects of intestinal radiation-induced fibrosis. Curr Mol Med. 2009;9:273–80.

    PubMed  CAS  Google Scholar 

  41. Haydont V, Vozenin-Brotons MC. Maintenance of radiation-induced intestinal fibrosis: cellular and molecular features. World J Gastroenterol. 2007;13:2675–83.

    PubMed  CAS  Google Scholar 

  42. Thompson JS, Saxena SK, Sharp JG. Regulation of intestinal regeneration: new insights. Microsc Res Tech. 2000;51:129–37.

    PubMed  CAS  Google Scholar 

  43. Kennedy GD, Heise CP. Radiation colitis and proctitis. Clin Colon Rectal Surg. 2007;20:64–72.

    PubMed Central  PubMed  Google Scholar 

  44. Coia LR, Myerson RJ, Tepper JE. Late effects of radiation therapy on the gastrointestinal tract. Int J Radiat Oncol Biol Phys. 1995;31:1213–36.

    PubMed  CAS  Google Scholar 

  45. Otterson MF. Effects of radiation upon gastrointestinal motility. World J Gastroenterol. 2007;13:2684–92.

    PubMed  Google Scholar 

  46. Overgaard J, Matsui M. Effect of radiation on glucose absorption in the mouse jejunum in vivo. Radiother Oncol J Eur Soc Ther Radiol Oncol. 1990;18:71–7.

    CAS  Google Scholar 

  47. Packey CD, Ciorba MA. Microbial influences on the small intestinal response to radiation injury. Curr Opin Gastroenterol. 2010;26:88–94.

    PubMed  Google Scholar 

  48. Ciorba MA, Stenson WF. Probiotic therapy in radiation-induced intestinal injury and repair. Ann N Y Acad Sci. 2009;1165:190–4.

    PubMed  Google Scholar 

  49. Crawford PA, Gordon JI. Microbial regulation of intestinal radiosensitivity. Proc Natl Acad Sci U S A. 2005;102:13254–9.

    PubMed Central  PubMed  CAS  Google Scholar 

  50. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263–74.

    PubMed  CAS  Google Scholar 

  51. Willett CG, Ooi CJ, Zietman AL, et al. Acute and late toxicity of patients with inflammatory bowel disease undergoing irradiation for abdominal and pelvic neoplasms. Int J Radiat Oncol Biol Phys. 2000;46:995–8.

    PubMed  CAS  Google Scholar 

  52. Manichanh C, Varela E, Martinez C, et al. The gut microbiota predispose to the pathophysiology of acute postradiotherapy diarrhea. Am J Gastroenterol. 2008;103:1754–61.

    PubMed  CAS  Google Scholar 

  53. Algin O, Turkbey B, Ozmen E, Algin E. Magnetic resonance enterography findings of chronic radiation enteritis. Cancer Imaging Off Publ Int Cancer Imaging Soc. 2011;11:189–94.

    Google Scholar 

  54. Cronin CG, Lohan DG, Browne AM, Alhajeri AN, Roche C, Murphy JM. MR enterography in the evaluation of small bowel dilation. Clin Radiol. 2009;64:1026–34.

    PubMed  CAS  Google Scholar 

  55. Khalid U, Norman AR, Andreyev HJ. Elevated C-reactive protein levels are not a feature of uncomplicated radiation-induced bowel injury. Eur J Cancer Care. 2007;16:346–50.

    CAS  Google Scholar 

  56. Hille A, Schmidt-Giese E, Hermann RM, et al. A prospective study of faecal calprotectin and lactoferrin in the monitoring of acute radiation proctitis in prostate cancer treatment. Scand J Gastroenterol. 2008;43:52–8.

    PubMed  CAS  Google Scholar 

  57. Wedlake L, McGough C, Hackett C, et al. Can biological markers act as non-invasive, sensitive indicators of radiation-induced effects in the gastrointestinal mucosa? Aliment Pharmacol Ther. 2008;27:980–7.

    PubMed  CAS  Google Scholar 

  58. Lutgens L, Lambin P. Biomarkers for radiation-induced small bowel epithelial damage: an emerging role for plasma Citrulline. World J Gastroenterol. 2007;13:3033–42.

    PubMed  CAS  Google Scholar 

  59. Lutgens LC, Blijlevens NM, Deutz NE, Donnelly JP, Lambin P, de Pauw BE. Monitoring myeloablative therapy-induced small bowel toxicity by serum citrulline concentration: a comparison with sugar permeability tests. Cancer. 2005;103:191–9.

    PubMed  Google Scholar 

  60. Lutgens LC, Deutz NE, Gueulette J, et al. Citrulline: a physiologic marker enabling quantitation and monitoring of epithelial radiation-induced small bowel damage. Int J Radiat Oncol Biol Phys. 2003;57:1067–74.

    PubMed  CAS  Google Scholar 

  61. Kopelman Y, Groissman G, Fireman Z. Radiation enteritis diagnosed by capsule endoscopy. Gastrointest Endosc. 2007;66:599. discussion.

    PubMed  Google Scholar 

  62. Sidhu R, Sanders DS, Morris AJ, McAlindon ME. Guidelines on small bowel enteroscopy and capsule endoscopy in adults. Gut. 2008;57:125–36.

    PubMed  CAS  Google Scholar 

  63. Kim HM, Kim YJ, Kim HJ, Park SW, Bang S, Song SY. A pilot study of capsule endoscopy for the diagnosis of radiation enteritis. Hepato-gastroenterology. 2011;58:459–64.

    PubMed  Google Scholar 

  64. Caunedo-Alvarez A, Romero-Vazquez J, Herrerias-Gutierrez JM. Patency and Agile capsules. World J Gastroenterol. 2008;14:5269–73.

    PubMed Central  PubMed  Google Scholar 

  65. Spada C, Riccioni ME, Costamagna G. The new, dissolving patency capsule: a safe and effective tool to avoid the complication of retained video capsules. J Clin Gastroenterol. 2008;42:761–2.

    PubMed  Google Scholar 

  66. Ludgate SM, Merrick MV. The pathogenesis of post-irradiation chronic diarrhoea: measurement of SeHCAT and B12 absorption for differential diagnosis determines treatment. Clin Radiol. 1985;36:275–8.

    PubMed  CAS  Google Scholar 

  67. Danielsson A, Nyhlin H, Persson H, Stendahl U, Stenling R, Suhr O. Chronic diarrhoea after radiotherapy for gynaecological cancer: occurrence and aetiology. Gut. 1991;32:1180–7.

    PubMed Central  PubMed  CAS  Google Scholar 

  68. Yeoh EK, Horowitz M, Russo A, Muecke T, Robb T, Chatterton BE. Gastrointestinal function in chronic radiation enteritis–effects of loperamide-N-oxide. Gut. 1993;34:476–82.

    PubMed Central  PubMed  CAS  Google Scholar 

  69. Rossel P, Sortsoe Jensen H, Qvist P, Arveschoug A. Prognosis of adult-onset idiopathic bile acid malabsorption. Scand J Gastroenterol. 1999;34:587–90.

    PubMed  CAS  Google Scholar 

  70. Gasbarrini A, Lauritano EC, Gabrielli M, et al. Small intestinal bacterial overgrowth: diagnosis and treatment. Dig Dis. 2007;25:237–40.

    PubMed  Google Scholar 

  71. Beer WH, Fan A, Halsted CH. Clinical and nutritional implications of radiation enteritis. Am J Clin Nutr. 1985;41:85–91.

    PubMed  CAS  Google Scholar 

  72. Green N, Iba G, Smith WR. Measures to minimize small intestine injury in the irradiated pelvis. Cancer. 1975;35:1633–40.

    PubMed  CAS  Google Scholar 

  73. Gunderson LL, Russell AH, Llewellyn HJ, Doppke KP, Tepper JE. Treatment planning for colorectal cancer: radiation and surgical techniques and value of small-bowel films. Int J Radiat Oncol Biol Phys. 1985;11:1379–93.

    PubMed  CAS  Google Scholar 

  74. Herbert SH, Solin LJ, Hoffman JP, et al. Volumetric analysis of small bowel displacement from radiation portals with the use of a pelvic tissue expander. Int J Radiat Oncol Biol Phys. 1993;25:885–93.

    PubMed  CAS  Google Scholar 

  75. Shanahan TG, Mehta MP, Bertelrud KL, et al. Minimization of small bowel volume within treatment fields utilizing customized “belly boards”. Int J Radiat Oncol Biol Phys. 1990;19:469–76.

    PubMed  CAS  Google Scholar 

  76. Russ JE, Smoron GL, Gagnon JD. Omental transposition flap in colorectal carcinoma: adjunctive use in prevention and treatment of radiation complications. Int J Radiat Oncol Biol Phys. 1984;10:55–62.

    PubMed  CAS  Google Scholar 

  77. Lechner P, Cesnik H. Abdominopelvic omentopexy: preparatory procedure for radiotherapy in rectal cancer. Dis Colon Rectum. 1992;35:1157–60.

    PubMed  CAS  Google Scholar 

  78. Devereux DF, Kavanah MT, Feldman MI, et al. Small bowel exclusion from the pelvis by a polyglycolic acid mesh sling. J Surg Oncol. 1984;26:107–12.

    PubMed  CAS  Google Scholar 

  79. Rodier JF, Janser JC, Rodier D, et al. Prevention of radiation enteritis by an absorbable polyglycolic acid mesh sling. A 60-case multicentric study. Cancer. 1991;68:2545–9.

    PubMed  CAS  Google Scholar 

  80. Beitler A, Rodriguez-Bigas MA, Weber TK, Lee RJ, Cuenca R, Petrelli NJ. Complications of absorbable pelvic mesh slings following surgery for rectal carcinoma. Dis Colon Rectum. 1997;40:1336–41.

    PubMed  CAS  Google Scholar 

  81. Hoffman JP, Sigurdson ER, Eisenberg BL. Use of saline-filled tissue expanders to protect the small bowel from radiation. Oncology. 1998;12:51–4. discussion 4, 60, 2, passim.

    PubMed  CAS  Google Scholar 

  82. Sugarbaker PH. Intrapelvic prosthesis to prevent injury of the small intestine with high dosage pelvic irradiation. Surg Gynecol Obstet. 1983;157:269–71.

    PubMed  CAS  Google Scholar 

  83. Freund H, Gunderson L, Krause R, Fischer JE. Prevention of radiation enteritis after abdominoperineal resection and radiotherapy. Surg Gynecol Obstet. 1979;149:206–8.

    PubMed  CAS  Google Scholar 

  84. Jia D, Koonce NA, Griffin RJ, Jackson C, Corry PM. Prevention and mitigation of acute death of mice after abdominal irradiation by the antioxidant N-acetyl-cysteine (NAC). Radiat Res. 2010;173:579–89.

    PubMed Central  PubMed  CAS  Google Scholar 

  85. Tannehill SP, Mehta MP, Larson M, et al. Effect of amifostine on toxicities associated with sequential chemotherapy and radiation therapy for unresectable non-small-cell lung cancer: results of a phase II trial. J Clin Oncol Off J Am Soc Clin Oncol. 1997;15:2850–7.

    CAS  Google Scholar 

  86. Athanassiou H, Antonadou D, Coliarakis N, et al. Protective effect of amifostine during fractionated radiotherapy in patients with pelvic carcinomas: results of a randomized trial. Int J Radiat Oncol Biol Phys. 2003;56:1154–60.

    PubMed  CAS  Google Scholar 

  87. Akpolat M, Gulle K, Topcu-Tarladacalisir Y, et al. Protection by L-carnitine against radiation-induced ileal mucosal injury in the rat: pattern of oxidative stress, apoptosis and cytokines. Int J Radiat Biol. 2013;89:732–40.

    PubMed  CAS  Google Scholar 

  88. Sekhon S. Chronic radiation enteritis: women’s food tolerances after radiation treatment for gynecologic cancer. J Am Diet Assoc. 2000;100:941–3.

    PubMed  CAS  Google Scholar 

  89. McGough C, Baldwin C, Frost G, Andreyev HJ. Role of nutritional intervention in patients treated with radiotherapy for pelvic malignancy. Br J Cancer. 2004;90:2278–87.

    PubMed Central  PubMed  CAS  Google Scholar 

  90. Arlow FL, Dekovich AA, Priest RJ, Beher WT. Bile acids in radiation-induced diarrhea. South Med J. 1987;80:1259–61.

    PubMed  CAS  Google Scholar 

  91. Walters JR, Pattni SS. Managing bile acid diarrhoea. Ther Adv Gastroenterol. 2010;3:349–57.

    Google Scholar 

  92. Jenkins C, Carmody TJ, Rush AJ. Depression in radiation oncology patients: a preliminary evaluation. J Affect Disord. 1998;50:17–21.

    PubMed  CAS  Google Scholar 

  93. Abayomi J, Kirwan J, Hackett A, Bagnall G. A study to investigate women’s experiences of radiation enteritis following radiotherapy for cervical cancer. J Hum Nutr Diet Off J Br Diet Assoc. 2005;18:353–63.

    CAS  Google Scholar 

  94. Bories C, Messing B, Lacourt J, Bernier JJ. Evaluation of the use of parenteral nutrition in chronic and severe radiation enterocolitis. Gastroenterol Clin Biol. 1987;11:142–7.

    PubMed  CAS  Google Scholar 

  95. Thompson JS, Weseman R, Rochling F, et al. Radiation therapy increases the risk of hepatobiliary complications in short bowel syndrome. Nutr Clin Pract Off Publ Am Soc Parenter Enter Nutr. 2011;26:474–8.

    Google Scholar 

  96. Dietz DW, Remzi FH, Fazio VW. Strictureplasty for obstructing small-bowel lesions in diffuse radiation enteritis–successful outcome in five patients. Dis Colon Rectum. 2001;44:1772–7.

    PubMed  CAS  Google Scholar 

  97. Regimbeau JM, Panis Y, Gouzi JL, Fagniez PL, French University Association for Surgical R. Operative and long term results after surgery for chronic radiation enteritis. Am J Surg. 2001;182:237–42.

    PubMed  CAS  Google Scholar 

  98. Galland RB, Spencer J. Surgical management of radiation enteritis. Surgery. 1986;99:133–9.

    PubMed  CAS  Google Scholar 

  99. Swan RW, Fowler Jr WC, Boronow RC. Surgical management of radiation injury to the small intestine. Surg Gynecol Obstet. 1976;142:325–7.

    PubMed  CAS  Google Scholar 

  100. Amiot A, Joly F, Lefevre JH, et al. Long-term outcome after extensive intestinal resection for chronic radiation enteritis. Dig Liver Dis Off J Ital Soc Gastroenterol Ital Assoc Study Liver. 2013;45:110–4.

    Google Scholar 

  101. Onodera H, Nagayama S, Mori A, Fujimoto A, Tachibana T, Yonenaga Y. Reappraisal of surgical treatment for radiation enteritis. World J Surg. 2005;29:459–63.

    PubMed  Google Scholar 

  102. Spyropoulos BG, Misiakos EP, Fotiadis C, Stoidis CN. Antioxidant properties of probiotics and their protective effects in the pathogenesis of radiation-induced enteritis and colitis. Dig Dis Sci. 2011;56:285–94.

    PubMed  Google Scholar 

  103. Han W, Mercenier A, Ait-Belgnaoui A, et al. Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutase. Inflamm Bowel Dis. 2006;12:1044–52.

    PubMed  Google Scholar 

  104. Carroll IM, Andrus JM, Bruno-Barcena JM, Klaenhammer TR, Hassan HM, Threadgill DS. Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am Jo Physiol Gastrointest Liver Physiol. 2007;293:G729–38.

    CAS  Google Scholar 

  105. Kullisaar T, Zilmer M, Mikelsaar M, et al. Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol. 2002;72:215–24.

    PubMed  CAS  Google Scholar 

  106. Chang SK, Hassan HM. Characterization of superoxide dismutase in Streptococcus thermophilus. Appl Environ Microbiol. 1997;63:3732–5.

    PubMed Central  PubMed  CAS  Google Scholar 

  107. Molla M, Gironella M, Salas A, et al. Protective effect of superoxide dismutase in radiation-induced intestinal inflammation. Int J Radiat Oncol Biol Phys. 2005;61:1159–66.

    PubMed  CAS  Google Scholar 

  108. Loguercio C, D’Argenio G, Delle Cave M, et al. Glutathione supplementation improves oxidative damage in experimental colitis. Dig Liver Dis Off J Ital Soc Gastroenterol Ital Assoc Study Liver. 2003;35:635–41.

    CAS  Google Scholar 

  109. Sengul N, Aslim B, Ucar G, et al. Effects of exopolysaccharide-producing probiotic strains on experimental colitis in rats. Dis Colon Rectum. 2006;49:250–8.

    PubMed  Google Scholar 

  110. Delia P, Sansotta G, Donato V, et al. Use of probiotics for prevention of radiation-induced diarrhea. World J Gastroenterol. 2007;13:912–5.

    PubMed  CAS  Google Scholar 

  111. Urbancsek H, Kazar T, Mezes I, Neumann K. Results of a double-blind, randomized study to evaluate the efficacy and safety of Antibiophilus in patients with radiation-induced diarrhoea. Eur J Gastroenterol Hepatol. 2001;13:391–6.

    PubMed  CAS  Google Scholar 

  112. Floch MH, Walker WA, Guandalini S, et al. Recommendations for probiotic use–2008. J Clin Gastroenterol. 2008;42 Suppl 2:S104–8.

    PubMed  Google Scholar 

  113. Hille A, Christiansen H, Pradier O, et al. Effect of pentoxifylline and tocopherol on radiation proctitis/enteritis. Strahlenther Onkol Organ Deutsch Rontgengesellschaft. 2005;181:606–14.

    Google Scholar 

  114. Gothard L, Cornes P, Brooker S, et al. Phase II study of vitamin E and pentoxifylline in patients with late side effects of pelvic radiotherapy. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2005;75:334–41.

    CAS  Google Scholar 

  115. Delanian S, Lefaix JL. Current management for late normal tissue injury: radiation-induced fibrosis and necrosis. Semin Radiat Oncol. 2007;17:99–107.

    PubMed  Google Scholar 

  116. Hamama S, Gilbert-Sirieix M, Vozenin MC, Delanian S. Radiation-induced enteropathy: molecular basis of pentoxifylline-vitamin E anti-fibrotic effect involved TGF-beta1 cascade inhibition. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2012;105:305–12.

    CAS  Google Scholar 

  117. Kilic D, Egehan I, Ozenirler S, Dursun A. Double-blinded, randomized, placebo-controlled study to evaluate the effectiveness of sulphasalazine in preventing acute gastrointestinal complications due to radiotherapy. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2000;57:125–9.

    CAS  Google Scholar 

  118. Loiudice TA, Lang JA. Treatment of radiation enteritis: a comparison study. Am J Gastroenterol. 1983;78:481–7.

    PubMed  CAS  Google Scholar 

  119. Marshall GT, Thirlby RC, Bredfeldt JE, Hampson NB. Treatment of gastrointestinal radiation injury with hyperbaric oxygen. Undersea Hyperb Med J Undersea Hyperb Med Soc Inc. 2007;34:35–42.

    CAS  Google Scholar 

  120. Olgac V, Erbil Y, Barbaros U, et al. The efficacy of octreotide in pancreatic and intestinal changes: radiation-induced enteritis in animals. Dig Dis Sci. 2006;51:227–32.

    PubMed  CAS  Google Scholar 

  121. Rocourt DV, Mehta VB, Besner GE. Heparin-binding EGF-like growth factor decreases inflammatory cytokine expression after intestinal ischemia/reperfusion injury. J Surg Res. 2007;139:269–73.

    PubMed Central  PubMed  CAS  Google Scholar 

  122. Kuhn MA, Xia G, Mehta VB, Glenn S, Michalsky MP, Besner GE. Heparin-binding EGF-like growth factor (HB-EGF) decreases oxygen free radical production in vitro and in vivo. Antioxid Redox Signal. 2002;4:639–46.

    PubMed  CAS  Google Scholar 

  123. Matthews MA, Watkins D, Darbyshire A, Carson WE, Besner GE. Heparin-binding EGF-like growth factor (HB-EGF) protects the intestines from radiation therapy-induced intestinal injury. J Pediatr Surg. 2013;48:1316–22.

    PubMed  Google Scholar 

  124. Williams JP, Hernady E, Johnston CJ, et al. Effect of administration of lovastatin on the development of late pulmonary effects after whole-lung irradiation in a murine model. Radiat Res. 2004;161:560–7.

    PubMed  CAS  Google Scholar 

  125. Haydont V, Bourgier C, Pocard M, et al. Pravastatin Inhibits the Rho/CCN2/extracellular matrix cascade in human fibrosis explants and improves radiation-induced intestinal fibrosis in rats. Clin Cancer Res Off J Am Assoc Cancer Res. 2007;13:5331–40.

    CAS  Google Scholar 

  126. Yamashita M, Otsuka F, Mukai T, et al. Simvastatin antagonizes tumor necrosis factor-alpha inhibition of bone morphogenetic proteins-2-induced osteoblast differentiation by regulating Smad signaling and Ras/Rho-mitogen-activated protein kinase pathway. J Endocrinol. 2008;196:601–13.

    PubMed  CAS  Google Scholar 

  127. Keskek M, Gocmen E, Kilic M, et al. Increased expression of cyclooxygenase-2 (COX-2) in radiation-induced small bowel injury in rats. J Surg Res. 2006;135:76–84.

    PubMed  CAS  Google Scholar 

  128. Wang J, Zheng H, Ou X, et al. Hirudin ameliorates intestinal radiation toxicity in the rat: support for thrombin inhibition as strategy to minimize side-effects after radiation therapy and as countermeasure against radiation exposure. J Thromb Haemost. 2004;2:2027–35.

    PubMed  CAS  Google Scholar 

  129. Wang J, Albertson CM, Zheng H, Fink LM, Herbert JM, Hauer-Jensen M. Short-term inhibition of ADP-induced platelet aggregation by clopidogrel ameliorates radiation-induced toxicity in rat small intestine. Thromb Haemost. 2002;87:122–8.

    PubMed  CAS  Google Scholar 

  130. Wang J, Zheng H, Qiu X, Kulkarni A, Fink LM, Hauer-Jensen M. Modulation of the intestinal response to ionizing radiation by anticoagulant and non-anticoagulant heparins. Thromb Haemost. 2005;94:1054–9.

    PubMed  CAS  Google Scholar 

  131. De Cristofaro R, De Candia E, Landolfi R. Effect of high- and low-molecular-weight heparins on thrombin-thrombomodulin interaction and protein C activation. Circulation. 1998;98:1297–301.

    PubMed  Google Scholar 

  132. Mohri M, Gonda Y, Oka M, et al. The antithrombotic effects of recombinant human soluble thrombomodulin (rhsTM) on tissue factor-induced disseminated intravascular coagulation in crab-eating monkeys (Macaca fascicularis). Blood Coagul Fibrinolysis Int J Haemost Thromb. 1997;8:274–83.

    CAS  Google Scholar 

  133. Solis MM, Vitti M, Cook J, et al. Recombinant soluble human thrombomodulin: a randomized, blinded assessment of prevention of venous thrombosis and effects on hemostatic parameters in a rat model. Thromb Res. 1994;73:385–94.

    PubMed  CAS  Google Scholar 

  134. Bernard GR, Vincent JL, Laterre PF, et al. Efficacy and safety of recombinant human activated protein C for severe sepsis. New Engl J Med. 2001;344:699–709.

    PubMed  CAS  Google Scholar 

  135. Andrade-Gordon P, Maryanoff BE, Derian CK, et al. Design, synthesis, and biological characterization of a peptide-mimetic antagonist for a tethered-ligand receptor. Proc Natl Acad Sci U S A. 1999;96:12257–62.

    PubMed Central  PubMed  CAS  Google Scholar 

  136. Nguyen NP, Antoine JE, Dutta S, Karlsson U, Sallah S. Current concepts in radiation enteritis and implications for future clinical trials. Cancer. 2002;95:1151–63.

    PubMed  Google Scholar 

  137. Rose DM, Hochwald SN, Harrison LE, Burt M. Selective glutathione repletion with oral oxothiazolidine carboxylate (OTZ) in the radiated tumor-bearing rat. J Surg Res. 1996;62:224–8.

    PubMed  CAS  Google Scholar 

  138. Graca BM, Freire PA, Brito JB, Ilharco JM, Carvalheiro VM, Caseiro-Alves F. Gastroenterologic and radiologic approach to obscure gastrointestinal bleeding: how, why, and when? Radiogr Rev Publ Radiol Soc N Am Inc. 2010;30:235–52.

    Google Scholar 

Download references

Compliance with Ethics Guidelines

Conflict of Interest

Ala Sharara, Ali Harb, and C. Abou Fadel disclose no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors [137].

Author information

Authors and Affiliations

  1. Division of Gastroenterology, Department of Internal Medicine, American University of Beirut Medical Center, Beirut, Lebanon

    Ali H. Harb, Carla Abou Fadel & Ala I. Sharara

  2. Division of Gastroenterology, American University of Beirut Medical Center, P.O. Box 11-0236/16-B, Beirut, Lebanon

    Ala I. Sharara

Authors
  1. Ali H. Harb
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carla Abou Fadel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ala I. Sharara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ala I. Sharara.

Additional information

This article is part of the Topical Collection on Small Intestine

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harb, A.H., Abou Fadel, C. & Sharara, A.I. Radiation Enteritis. Curr Gastroenterol Rep 16, 383 (2014). https://doi.org/10.1007/s11894-014-0383-3

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s11894-014-0383-3

Keywords

Search

Navigation