1,488
Views
64
CrossRef citations to date
0
Altmetric
Review Article

Late Radiation Injury of the Small Intestine Clinical, pathophysiologic and radiobiologic aspects: A review

Pages 401-415 | Accepted 22 May 1989, Published online: 08 Jul 2009

References

  • Bloomer W D, Hellman S. Normal tissue response to radiation therapy. N Engl J Med 1975; 293: 80–3
  • Galland R B, Spencer J. Surgical management of radiation enteritis. Surgery 1986; 99: 133–9
  • Kinsella T J, Bloomer W D. Tolerance of the intestine to radiation therapy. Surg Gynecol Obstet 1980; 151: 273–84
  • Walsh D. Deep traumatism from roentgen ray exposure. Br Med J July, 1897; 31: 273–374
  • Bories-Aseau A, Dayan L. Les radiolesions du grele. Ann Chir 1979; 33: 299–306
  • DeCosse J J, Rhodes R S, Wentz W B, Reagan J W, Dworken H J, Holden W D. The natural history and management of radiation induced injury to the gastrointestinal tract. Ann Surg 1969; 120: 369–84
  • Localio S A, Pachter H L, Gouge T H. The radiation-injured bowel. Surg Ann 1979; 11: 181–95
  • Berthrong M, Fajardo L F. Radiation injury in surgical pathology. Part II. Alimentary tract. Am J Surg Pathol 1981; 5: 153–78
  • Gallez-Marchal D, Foyalle M, Henry-Amar M, LeBurgeois J P, Rougier P, Cosset J M. Radiation injury of the gastrointestinal tract in Hodgkin's disease: The role of exploratory laparotomy and fractionation. Radiat Oncol 1984; 2: 93–9
  • Dirksen P K, Matolo N M, Trelford J D. Complications following operation in the previously irradiated abdominopelvic cavity. Am Surg 1977; 43: 234–41
  • Morgenstern L, Hart M, Lugo D, Friedman N B. Changing aspects of radiation enteropathy. Arch Surg 1985; 120: 1225–8
  • Cram A E, Pearlman N W, Jochimsen P R. Surgical management of complications of radiation-injured gut. Am J Surg 1977; 133: 551–3
  • Donaldson S S, Jundt S, Ricour C, Sarrazin D, Lemerle J, Schweisguth O. Radiation enteritis in children. Cancer 1975; 35: 1167–78
  • Strockbine M F, Hancock J E, Fletcher G H. Complications in 831 patients with squamous cell carcinoma of the intact uterine cervix treated with 3000 rads or more whole pelvis irradiation. AJR 1970; 108: 293–304
  • Wharton J T, Jones H W, Day T G, Rutledge F N, Fletcher G H. Preirradiation celiotomy and extended field irradiation for invasive carcinoma of the cervix. Obstet Gynecol 1977; 49: 333–8
  • Withers H R, Romsdahl M M. Post-operative radiotherapy for adenocarcinoma of the rectum and rectosigmoid. Int J Radiat Oncol Biol Phys 1977; 2: 1069–74
  • LoIudice T, Baxter D OD, Balint J. Effects of abdominal surgery on the development of radiation enteropathy. Gastroenterology 1977; 73: 1093–7
  • Potish R A. Prediction of radiation-related small-bowel damage. Radiology 1980; 135: 219–21
  • Potish R A, Jones T K, Levitt S H. Factors predisposing to radiation-related small bowel damage. Radiology 1979; 132: 479–82
  • Danjoux C E, Catton G E. Delayed complications in colorectal carcinoma treated by combination radiotherapy and 5-fluorouracil. Eastern cooperative oncology group (ECOG) pilot study. Int J Radiat Oncol Biol Phys 1979; 5: 311–5
  • Indran M, Boyle F C, Carr K E. Simulation with pharmacological agents of radiation damage to small intestinal villi. Scanning Electron Microsc 1985; 3: 1165–75
  • Walker R I, Brook I, Casterton J W, MacVittie T M, Myhal M L. Possible association of mucous blanket integrity with postirradiation colonization resistance. Radiat Res 1985; 104: 346–57
  • Devik F. A study of the local roentgen reaction on the skin of mice, with special reference to the vascular effects. Acta Radiol 1955, Suppl 119
  • Hagemann R F, Sigdestad C P, Lesher S. Intestinal crypt survival and total and per crypt levels of proliferative cellularity following irradiation: Single X-ray exposures. Radiat Res 1971; 46: 533–46
  • Hendry J H, Potten C S, Roberts N P. The gastrointestinal syndrome and mucosal clonogenic cells: Relationship between target cell sensitivities, LD50 and cell survival, and their modification by antibiotics. Radiat Res 1983; 96: 100–12
  • Trier J S, Browning T H, Foroozan P. The effects of X-ray therapy on the mucosa of the human small intestine. Gastrointestinal radiation injury, M F Sullivan. Excerpta Medica Foundation, Amsterdam 1968; 57–72
  • Wiernik G. Muscosal cell kinetics in patients exposed to abdominal irradiation. Gastrointestinal radiation injury, M F Sullivan. Excerpta Medica Foundation, Amsterdam 1968; 167–74
  • Poulakos L, Osborne J W. The kinetics of cellular recovery in locally X-irradiated rat ileum. Radiat Res 1973; 53: 402–13
  • Wiernik G, Creamer B, Shorter R G. Recovery of the intestinal mucosa in the rat after X-irradiation of the exteriorized intestine. Radiat Res 1966; 27: 264–71
  • Devik F. Intestinal cell kinetics in irradiated mice. Acta Radiol Oncol 1971; 10: 129–49
  • Daburon F, Chomette G, Remy J, et al. La restauration de l'intestine chez le pore irradie a forte dose. Biol Gastroenterol 1975; 8: 321–38
  • Michalowski A. Effects of radiation on normal tissues: Hypothetical mechanisms and limitations of in situ assays of clonogenicity. Radiat Environ Biophys 1981; 19: 157–72
  • Withers H R, Peters L J, Kogelnik H D. The pathobiology of late effects of irradiation. Radiation biology in cancer research, R E Meyn, H R Withers. Raven Press, New York 1980; 439–48
  • Hasleton P S, Carr N, Schofield P F. Vascular changes in radiation bowel disease. Histopathol 1985; 9: 517–34
  • Law M P. Radiation-induced vascular injury and its relation to late effects in normal tissue. Adv Radiat Biol 1981; 9: 37–73
  • Law M P. Vascular permeability and late radiation fibrosis in mouse lung. Radiat Res 1985; 103: 60–76
  • Hopewell J W. The importance of vascular damage in the development of late radiation effects in normal tissues. Radiation biology in cancer research, R E Meyn, H R Withers. Raven Press, New York 1980; 449–59
  • Efskind L. Experimentelle Untersuchungen ueber die Biologie des Peritoneums. I. Die morphologische Reaktion des Peritoneums auf Reize. Oslo 1940, (Thesis)
  • Efskind L. Experimentelle Untersuchungen ueber die Biologie des Peritoneums. II. Die peritoneale Aufsaugung. Oslo 1940, (Thesis)
  • McBride W H, Mason K A, Davis C, Withers H R, Smathers J B. Adhesion formation in experimental chronic radiation enteropathy. Int J Radiat Oncol Biol Phys 1989; 16: 737–43
  • McBride W H, Mason K, Withers H R, Davis C. Effects of Interleukin 1, inflammation, and surgery on the incidence of adhesion formation and death after abdominal irradiation in mice. Cancer Res 1989; 49: 169–73
  • Hauer-Jensen M, Carlsen E, Nygaard K. Tynntarmskade etter straaleterapi. (Injury to the small intestine following radiation therapy). Tidsskr Nor Laegeforen 1983; 103: 133–5
  • Newman A, Katsari J, Blendis L M, Charlesworth M, Walter L H. Small-intestinal injury in women who have had pelvic radiotherapy. Lancet 1973; 2: 1471–3
  • Swan R W. Stagnant loop syndrome resulting from small-bowel irradiation injury and intestinal bypass. Gynecol Oncol 1974; 2: 441–5
  • Wellwood J M, Jackson B T. The intestinal complications of radiotherapy. Br J Surg 1973; 60: 814–8
  • Stryker J A, Hepner G W, Mortel R. The effect of pelvic irradiation on ileal function. Radiology 1977; 124: 213–6
  • Andersson H, Bosaeus I, Nyström C. Bile salt malabsorption in the radiation syndrome. Acta Radiol Oncol 1978; 17: 312–8
  • Cosnes J, Laurent-Puig P, Baumer P, Bellanger J, Gendre J P, Le Quintrec Y. La denutrition de l'enterite radique chronique. Etude de cent malades. Ann Gastroenterol Hepatol (Paris) 1988; 24: 7–12
  • Mendelson R H, Nolan D J. The radiological features of chronic radiation enteritis. Clin Radiol 1985; 36: 141–8
  • Dencker H, Holmdahl K H, Lunderquist A, Olivecrona H, Tylen U. Mesenteric angiography in patients with radiation injury of the bowel after pelvic irradiation. AJR 1972; 114: 476–81
  • Hauer-Jensen M, Skar V, Husebye E, Selbekk B. 14-C-D-Xylose breath test in the diagnosis of radiation induced malabsorption. Abstracts from the 37th Annual Meeting of the Radiation Research Society. 1989, 81
  • Zentler-Munro P L, Bessell E M. Medical management of radiation enteritis -an algorithmic guide. Clin Radiol 1987; 38: 291–4
  • den Hartog Jager F CA, van Haaster M, Batterman J J, Tytgat G NJ. The endoscopic spectrum of late radiation damage of the rectosigmoid colon. Endoscopy 1985; 17: 214–6
  • Rosen I B, Shapiro B J. Radiation enteropathy of the small bowel. Can Med Assoc J 1964; 91: 681–8
  • Haddad H, Bounous G, Tahan W T, Devroede G, Beadry R, Lafond R. Long-term nutrition with an elemental diet following intensive abdominal irradiation. Dis Colon Rectum 1974; 17: 373–6
  • Goldstein F, Khoury J, Thornton J J. Treatment of chronic radiation enteritis and colitis with salicylazosulfapyridine and systemic corticosteroids. Am J Gastroenterol 1976; 65: 201–8
  • Kochhar R, Sharma S C, Gupta B B, Mehta S K. Rectal sucralfate in radiation proctitis. Lancet 1988; 2: 400–1
  • Bounos G. Elemental diets in the prophylaxis and therapy for intestinal lesions: An update. Surgery 1989; 105: 571–5
  • Fischer L, Kimose H H, Spjeldnaes N, Wara P. Late radiation injuries of the small intestine—management and outcome. Acta Chir Scand 1989; 155: 47–51
  • Harling H, Balslev I. Radical surgical approach to radiation injury of the small bowel. Dis Colon Rectum 1986; 29: 371–3
  • Makela J, Nevasaari K, Kairaluoma M I. Surgical treatment of intestinal radiation injury. J Surg Oncol 1987; 36: 93–7
  • Deveney C W, Lewis F R, Schrock T R. Surgical management of radiation injury of the small and large intestine. Dis Colon Rectum 1976; 19: 25–9
  • Johansson K, Ahn H, Herder A, Lindhagen J. Assessment of gastrointestinal blood flow with laser doppler flowmetry in patients with chronic radiation injury. Acta Chir Scand 1988; 154: 291–6
  • Meese D L, Bubrick M P, Paulson G L, et al. Safety of low anterior resection in the presence of chronic radiation changes in dogs. Dis Colon Rectum 1986; 29: 22–6
  • Miholic J, Schlappack O, Klepetko W, Kolbl H, Szepesi T, Moeschl P. Surgical therapy of radiation-induced small bowel lesions. Arch Surg 1987; 122: 923–6
  • Miholic J, Schwarz C, Moeschl P. Surgical therapy of radiation-induced lesions of the colon and rectum. Am J Surg 1988; 155: 761–4
  • Russel J C, Welch J P. Operative management of radiation injuries of the intestinal tract. Am J Surg 1979; 137: 433–42
  • Galland R B, Spencer J. The natural history of clinically established radiation enteritis. Lancet 1985; 1: 1257–8
  • Harling H, Balslev I. Long-term prognosis of patients with severe radiation enteritis. Am J Surg 1988; 155: 517–9
  • Bounous G. The use of elemental diets during cancer therapy. Anticancer Res 1983; 3: 299–304
  • Bounous G, Bel E L, Shuster J, Gold P, Tahan W T, Bastin E. Dietary protection during radiation therapy. Strahlentherapie 1975; 149: 476–83
  • McArdle A H, Wittnich C, Freeman C R, Duguid W P. Elemental diet as prophylaxis against radiation injury. Arch Surg 1985; 120: 1026–32
  • Bosaeus I, Andersson H, Nyström C. Effect of a low-fat diet on bile salt excretion and diarrhoea in the gastrointestinal radiation syndrome. Acta Radiol Oncol 1979; 18: 460–4
  • Franzen L, Hellsing U, Henriksson R, Littbrand B. Managing side-effects in radiotherapy with regard to the gastrointestinal tract. Recent Results Cancer Res 1988; 108: 127–33
  • Chary S, Thomson D H. A clinical trial evaluating cholestyramine to prevent diarrhea in patients maintained on low-fat diets during pelvic radiation therapy. Int J Radiat Oncol Biol Phys 1984; 10: 1885–90
  • Salminen E, Elomaa I, Minkkinen J, Vapaatalo H, Salminen S. Preservation of intestinal integrity during radiotherapy using live Lactobacillus acidopheles cultures. Clin Radiol 1988; 39: 435–7
  • Mennie A T, Dalley V M, Dinneen L C, Collier H OJ. Treatment of radiation-induced gastrointestinal distress with acetylsalicylate. Lancet 1975; 2: 942–3
  • Ludgate C M. Preliminary report: Acetylsalicylic acid therapy in the treatment of complications following abdominal radiation. J Can Assoc Radiol 1985; 36: 138–40
  • Stryker J A, Chung C K, Layser J D. Colestipol hydrochloride prophylaxis of diarrhea during pelvic radiotherapy. Int J Radiat Oncol Biol Phys 1983; 9: 185–90
  • Henriksson R, Franzen L, Littbrand B. Does sucralfate reduce radiation-induced diarrhea. Act Oncol 1987; 26: 76–7
  • Devereux D F, Chandler J J, Eisenstat T, Zinkin L. Efficacy of an absorbable mesh in keeping the small bowel out of the human pelvis following surgery. Dis Colon Rectum 1988; 31: 17–21
  • Plowman O N, Shand W S, Jackson D B. Use of absorbable mesh to displace bowel and avoid radiation enteropathy during therapy of pelvic Ewing's sarcoma. Hum Toxicol 1984; 3: 229–37
  • Feldman M I, Kavanah M T, Devereux D E, Choe S. New surgical method to prevent pelvic radiation enteropathy. Am J Clin Oncol 1988; 11: 25–33
  • Deutsch A A, Stern H S. Technique of insertion of pelvic vicryl mesh sling to avoid postradiation enteritis. Dis Colon Rectum 1989; 32: 628–30
  • DeLuca F R, Ragins H. Construction of an omental envelope as a method of excluding the small intestine from the field of postoperative irradiation to the pelvis. Surg Gynecol Obstet 1985; 160: 365–6
  • Petit J Y, Lacour J, Margulis A, Reed W P. Indications and results of omental pedicle grafts in oncology. Cancer 1979; 44: 2343–8
  • Russ J E, Smoron G L, Gagnon J D. 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
  • Freund H, Gunderson L, Krause R, Fischer J E. Prevention of radiation enteritis after abdominoperineal resection and radiotherapy. Surg Gynecol Obstet 1979; 149: 206–8
  • Allen P IM, Fielding J WL, Middleton M D, Priestman T J. Rectal carcinoma: a new technique to allow safer postoperative irradiation of the pelvis. Eur J Surg Oncol 1987; 13: 21–5
  • Durig M, Steenblock U, Heberer M. Prevention of radiation injuries to the small intestine. Surg Gynecol Obstet 1984; 159: 162–3
  • Sugarbaker P H. Intrapelvic prosthesis to prevent injury of the small intestine with high dosage pelvic irradiation. Surg Gynecol Obstet 1983; 157: 269–71
  • Green N. The avoidance of small intestinal injury in gynecologic cancer. Int J Radiat Oncol 1983; 9: 1385–90
  • Green N, Iba G, Smith W R. Measures to minimize small intestinal injury in the irradiated pelvis. Cancer 1975; 35: 1633–40
  • Schraub S, Monnier A, Poulin G. Preventions des complications tardives du grele par l'irradiation en position de Trendelenbourg. J Radiol Electrol 1978; 59: 347–52
  • Phelps T A, Blacket N M. Protection of intestinal damage by pretreatment with cytarabine (Cytosine arabinoside). Int J Radiat Oncol Biol Phys 1979; 5: 1617–20
  • Tseng V LY, Bybee J W, Osborne J W. Intestinal crypt survival after X-irradiation of the rat small intestine under conditions of radioprotection. Radiat Res 1978; 74: 129–38
  • Ito H, Meistrich M L, Barkley T, Thames H D, Milas L. Protection of acute and late radiation damage of the gastrointestinal tract by WR-2721. Int J Radiat Oncol Biol Phys 1986; 12: 211–9
  • Geraci J P, Jackson K L, Mariano M S. Effect of pseudomonas contamination or antibotic decontamination of the GI tract on acute radiation lethality after neutron or gamma irradiation. Radiat Res 1985; 104: 395–405
  • Mastromarino A J, Wilson R. Antibiotic radioprotection of mice exposed to supralethal whole-body irradiation independent of antibacterial activity. Radiat Res 1976; 68: 329–38
  • Morgenstern L, Patin C S, Krohn H L, Hiatt N. Prolongation of survival in lethally irradiated dogs. Arch Surg 1970; 101: 586–9
  • Sokol A B, Lipson L W, Morgenstern L, Hiatt N. Protection against lethal irradiation injury by pancreatic enzyme exclusion. Surg Forum 1967; 18: 387–9
  • Hauer-Jensen M, Sauer T, Berstad T, Nygaard K. Influence of pancreatic secretion on late radiation enteropathy in the rat. Acta Radiol Oncol 1985; 24: 555–60
  • Forsberg J O. Transient ischemia for radioprotection. University of Uppsala, UppsalaSweden 1978, (Academic thesis)
  • Lote K. Temporary intestinal ischemia for radiation protection. University of Bergen, BergenNorway 1983, (Academic thesis)
  • Steckel R J, Snow H D, Collins J D, Barenfus M, Patin T. Successful radiation protection of the normal intestinal tract in the dog. Radiology 1974; 111: 451–5
  • Chadwick K H, Leenhouts H P. The molecular theory of radiation biology. Springer-Verlag, Berlin 1981
  • Duncan W, Nias A HW. Clinical radiobiology. Churchill Livingstone, Edinburgh 1977
  • Sandler R S, Sandler D P. Radiation-induced cancers of the colon and rectum: Assessing the risk. Gastroenterology 1983; 84: 51–7
  • Rotmensch S, Avigad I, Soffer E E, et al. Carcinoma of the large bowel after a single massive dose of radiation in healthy teenagers. Cancer 1986; 57: 728–31
  • Denman D L, Kirchner F R, Osborne J W. Induction of colonic adenocarcinoma in the rat by x-irradiation. Cancer Res 1978; 38: 1899–905
  • Osborne J W, Nicholson D P, Prasad K N. Induction of intestinal carcinoma in the rat by x-irradiation of the small intestine. Radiat Res 1963; 18: 76–85
  • Hauer-Jensen M, Sauer T, Devik F, Nygaard K. Late changes following single dose roentgen irradiation of rat small intestine. Acta Radiol Oncol 1983; 22: 299–303
  • Borek C, Hall E. Transformation of mammalian cells in vitro by low doses of X-rays. Nature 1973; 243: 450–3
  • Hauer-Jensen M, Sauer T, Devik F, Nygaard K. Effects of dose fractionation on late roentgen radiation damage of rat small intestine. Acta Radiol Oncol 1983; 22: 381–4
  • Stark W. Specimen septem historias et dissectiones dysentericorum exhibens. Leiden 1766, (Thesis)
  • Wayte D M, Helwig E B. Colitis cystica profunda. Am J Clin Pathol 1967; 48: 159–69
  • Eriksson B, Johnson L, Rubio C. A semiquantitative histological method to estimate acute and chronic radiation injury in the small intestine of the cat. Scand J Gastroenterol 1982; 17: 1017–24
  • Rubio C A, Eriksson B, Johnson L. Ectopic intestinal glands after segmental small bowel irradiation in the cat. Acta Radiol Oncol 1983; 22: 473–5
  • Gardiner G W, McAuliffe N, Murray D. Colitis cystica profunda occuring in a radiation-induced colonic stricture. Hum Pathol 1984; 15: 259–68
  • Hubmann F H. Proctitis cystica profunda and radiation fibrosis in the rectum of the female Wistar rat after X-irradiation: A histopathological study. J Pathol 1982; 138: 193–204
  • Valiulis A P, Gardiner G W, Mahoney L J. Adenocarcinoma and colitis cystica profunda in a radiation-induced colonic stricture. Dis Colon Rectum 1985; 28: 128–31
  • Martin J K, Culp C E, Weiland L H. Colitis cystica profunda. Dis Colon Rectum 1980; 23: 488–91
  • Osborne J W, Prasad K N, Zimmerman G R. Changes in the rat intestine after X-irradiation of exteriorized short segments of ileum. Radiat Res 1970; 43: 131–42
  • Reinhold H S. Structural changes in blood vessels. Curr Topics Radiat Res Quarterly 1974; 10: 58–74
  • Fonkalsrud E W, Sanchez M, Zerubavel R, Mahoney A. Serial changes in arterial structure following radiation therapy. Surg Gynecol Obstet 1977; 145: 395–400
  • Steaner S P, Devine R L, Christian E JB. Late changes in the irradiated microvasculature: An electron microscopy study of the effects of fission neutrons. Radiat Res 1976; 65: 351–70
  • Bosniak M A, Hardy M A, Quint J, Ghossein N A. Demonstration of the effect of irradiation of eanine bowel using in vivo photographic magnification angiography. Radiology 1969; 93: 1361–8
  • Carr N D, Pullen B R, Hasleton P S, Schofield P F. Microvascular studies in human radiation bowel disease. Gut 1984; 25: 448–54
  • Eriksson B. Microangiographic pattern in the small intestine of the cat after irradiation. Scand J Gastroenterol 1982; 17: 887–95
  • Cockerham L G, Doyle T F, Trumbo R B, Nold J B. Acute post-irradiation canine intestinal blood flow. Int J Radiat Biol 1984; 45: 65–72
  • Watters C, Gerber G B. Regional blood flow in rats exposed to supralethal doses of whole body X-irradiation. Radiat Environ Biophys 1975; 12: 303–13
  • Kudrjavcev V D, Suskevic L N. Der Mechanismus der Zirkulationsstoerungen in der Duenndarmwand und ihre Rolle bei der Entwicklung des Darmsyndroms. Radiobiol Radiother 1980; 21: 771–7
  • Eriksson B, Johnson L. Capillary filtration in the small intestine after irradiation. Scand J Gastroenterol 1983; 18: 209–15
  • Eriksson B, Johnson L, Lundquist P G. Ultrastructural aspects of capillary function in irradiated bowel. An experimental study in the cat. Scand J Gastroenterol 1983; 18: 473–80
  • Altman K I, Gerber G B. The effect of ionizing radiation on connective tissue. Adv Radiat Biol, J T Lett, U K Ehmann, A B Cox. Academic Press, San Diego 1983; 237–304
  • Gerber G B, Altman K I. Biochemical effects of ionizing radiation on connective tissue. Nukleonika 1980; 25: 725–52
  • Rantanen J. Radiation injury of connective tissue. A biochemical investigation with experimental granuloma. Acta Radiol 1973, Suppl 330
  • Ward W F, Shih-Hoellwarth A, Tuttle R D. Collagen accumulation in irradiated rat lung: modification by D-penicillamine. Radiology 1983; 146: 533–7
  • Parker F G, Barnes E N, Kaye G I. The pericryptal fiberoblast sheath. IV. Replication, migration, and differentiation of the subepithelial fibroblasts of the crypts and villus of the rabbit jejunum. Gastroenterology 1974; 67: 601–21
  • Fajardo L F, Berthrong M. Radiation injury in surgical pathology. Am J Surg Pathol 1978; 12: 159–99
  • Tsao C, Ward W F. Plasminogen activator activity in lung and alveolar macrophages of rats exposed to graded single doses of gamma rays to the right hemithorax. Radiat Res 1985; 103: 393–402
  • Zweifach B W, Kivy-Rosenberg E. Microcirculatory effects of whole-body X-irradiation and radiomimetic procedures. Am J Physiol 1965; 208: 492–8
  • Kalima T V, Saloniemi H, Rahko T. Experimental regional enteritis in pigs. Scand J Gastroenterol 1976; 11: 353–62
  • Black W C, Gomez L S, Yuhas J M, Kligerman M M. Quantitation of the late effects of X-radiation on the large intestine. Cancer 1980; 45: 444–51
  • Greenberger N J, Isselbacher K J. Malabsorption following radiation injury to the gastrointestinal tract. Am J Med 1964; 36: 450–6
  • Engeset A. Irradiation of lymph nodes and vessels. Universitetsforlaget, Oslo 1964
  • Van den Brenk H AS. The effect of ionizing radiation on the regeneration and behaviour of mammalian lymphatics. AJR 1957; 78: 837–49
  • Bond V P, Swift M N, Allen A C, Fishler M C. Sensitivity of abdomen of rat to X-irradiation. Am J Physiol 1950; 161: 323–30
  • Dewit L, Oussoren Y, Bartelink H, Stewart F A. Differences in the acute intestinal syndrome after partial and total abdominal irradiation in mice. Int J Radiat Biol 1985; 48: 745–52
  • Sullivan M F, Marks S, Hackett P L, Thompson R C. X-irradiation of the exteriorized or in situ intestine of the rat. Radiat Res 1959; 11: 653–66
  • Jervis H R, Donati R M, Stromberg L R, Sprinz H. Effect of exposure conditions on the production of radiation lesions in the rat small intestine. Proc Soc Exp Med Biol 1968; 127: 948–52
  • Peck J W, Gibbs F A, Dethlefsen L A. Localized hyperthermia and X-irradiation of murine jejunum in situ: a new method. Int J Hyperthermia 1986; 2: 227–98
  • Hauer-Jensen M, Poulakos L, Osborne J W. Effects of accelerated fractionation on radiation injury of the small intestine: A new rat model. Int J Radiat Oncol Biol Phys 1988; 14: 1205–12
  • Withers H R, Elkind M M. Radiosensitivity and fractionation response of crypt cells of mouse jejunum. Radiat Res 1969; 38: 598–613
  • Withers H R, Elkind M M. Microcolony survival assay for cells of mouse intestinal mucosa exposed to radiation. Int J Radiat Biol 1970; 17: 261–7
  • Sebes J I, Zaldivar R, Vogel H H. Histopathologic changes induced in rats by localized x-irradiation of an exteriorized segment of the small intestine. Strahlentherapie 1975; 150: 403–10
  • Reynaud A, Travis E L. Late effects of irradiation in mouse jejunum. Int J Radiat Biol 1984; 46: 125–34
  • Hauer-Jensen M, Sauer T, Sletten K, Reitan J B, Nygaard K. Value of hydroxyproline measurements in the assessment of late radiation enteropathy. Acta Radiol Oncol 1986; 25: 137–42
  • Mulholland M V, Levitt S H, Song C W, Potish R A, Delancy J R. The role of luminal contents in radiation enteritis. Cancer 1984; 54: 2396–402
  • Hauer-Jensen M, Sauer T, Reitan J B, Nygaard K. Late radiation enteropathy following split-dose irradiation of rat small intestine. Acta Radiol Oncol 1986; 25: 203–6
  • Hauer-Jensen M, Poulakos L, Osborne J W. Intestinal complications following accelerated fractionated x-irradiation. An experimental study in the rat. Acta Oncol 1990; 29: 229–34
  • Poulakos L, Elwell J H, Osborne J W, et al. The prevalence and severity of late effects in normal rat duodenum following intraoperative irradiation. Int J Radiat Oncol Biol Phys
  • Fowler J F. Fractionated radiation therapy after Strandqvist. Acta Radiol Oncol 1984; 23: 209–16
  • Thames H D, Withers H R, Peters L J, Fletcher G H. Changes in early and late radiation responses with altered dose fractionation: Implications for dose-survival relationships. Int J Radiat Oncol Biol Phys 1982; 8: 219–26
  • Turesson I, Notter G. The influence of fraction size in radiotherapy on the late normal tissue reaction. I: Comparison of the effects of daily and once-a-week fractionation on human skin. Int J Radiat Oncol Biol Phys 1984; 10: 593–8
  • Denekamp J. Cell kinetics and radiation biology. Int J Radiat Biol 1986; 49: 357–80
  • Zeman E M, Bedford J S. Changes in early and late effects with dose-per-fraction: alpha, beta, redistribution and repair. Int J Radiat Oncol Biol Phys 1984; 10: 1039–47
  • Barendsen G W. Dose fractionation, dose rate, and iso-effect relationships for normal tissue response. Int J Radiat Oncol Biol Phys 1982; 8: 1981–97
  • Kiszel Z, Spiethoff A, Trott K R. Large bowel stenosis in rats after fractionated local irradiation. Radiother Oncol 1984; 2: 247–54
  • Terry N HA, Denekamp J. RBE values and repair characteristics for colorectal injury after caesium-137 gamma-ray and neutron-irradiation. II. Fractionation up to ten doses. Br J Radiol 1984; 57: 617–29
  • Peck J W, Gibbs F A. Therapeutic implications of thermal radiosensitization and alpha-beta analysis of intestinal fibrosis. Abstracts of papers for the 36th annual meeting of the Radiation Research Society. 1988, 155
  • van der Kogel A J, Jarrett K A, Paciotti M A, Raju M R. Radiation tolerance of the rat rectum to fractionated X-rays and pi-mesons. Radiother Oncol 1988; 12: 225–32
  • Field S B, Hornsey S, Kutsutani Y. Effects of fractionated irradiation on mouse lung and a phenomenon of slow repair. Br J Radiol 1976; 49: 700–7
  • Bryant P E. Decrease in sensitivity of cells after split-dose recovery: Evidence for the involvement of protein synthesis. Int J Radiat Biol 1975; 27: 95–102
  • Reinhold H S, Buisman G H. Repair of radiation damage to capillary endothelium. Br J Radiol 1975; 48: 727–31
  • Trott K R, Kiszel Z. Dependence of radiation-induced large bowel stenosis in rats on dose fractionation. Radiat Res 1981; 87: 459
  • Hornsey S, Field S B. Slow repair and residual injury. Radiation biology in cancer research, R E Mey, H R Withers. Raven Press, New York 1980; 489–90
  • Wheldon T E, Michalowski A S, Kirk J. The effect of irradiation on function in self-renewing normal tissues with differing proliferative organisation. Br J Radiol 1982; 55: 759–66
  • Arcangeli G, Mauro F, Morelli D, Nervi C. Multiple daily fractionation in radiotherapy: Biological rationale and preliminary clinical experience. Eur J Cancer 1979; 15: 1077–83
  • Saunders M I, Dische S, Fowler J F, et al. Radiotherapy employing three fractions on each of twelve consecutive days. Acta Oncol 1988; 27: 163–7
  • Peters L J, Ang K K, Thames H D, Jr. Accelerated fractionation in the radiation treatment of head and neck cancer. Acta Oncol 1988; 27: 185–94
  • Turesson I, Notter G. Accelerated versus conventional fractionation. Acta Oncol 1988; 27: 169–79
  • Thames H D, Peters L J, Withers H R, Fletcher G H. Accelerated fractionation vs. hyperfractionation: Rationales for several treatments per day. Int J Radiat Oncol Biol Phys 1983; 9: 127–38
  • Withers H R. Biologic basis for altered fractionation schemes. Cancer 1985; 55: 2086–95
  • Turesson I, Notter G. The influence of the overall treatment time in radiotherapy on the acute reaction: Comparison of the effects of daily and twice-a-week fractionation on human skin. Int J Radiat Oncol Biol Phys 1984; 10: 607–18
  • Elkind M M. DNA repair and cell repair. Are they related. Int J Radiat Oncol Biol Phys 1979; 5: 1089–94
  • Hiatt N, Warner N E. Influence of intestinal content on radiation lesions of the small intestine. Proc Soc Exp Biol Med 1967; 124: 937–9
  • Morgenstern L, Hiatt N. Injurious effect of pancreatic secretions on postradiation enteropathy. Gastroenterology 1967; 53: 923–9
  • Quastler H. The nature of intestinal radiation death. Radiat Res 1956; 4: 303–20
  • Krause P, Ziegler K. Experimentelle Untersuchungen ueber die Einwirkung der Roentgenstrahlen auf tierische Gewebe. A. Uebersicht ueber die in der Litteratur niedergelegten Angaben ueber die Wirkung der Roentgenstrahlen auf innere Organe. Fortschr a d Geb d Roentgenstr 1906; 10: 126–82
  • Bealmear P M, Holtermann O A, Mirand E A. Radiation pathology and treatment. The germ-free animal in biomedical research, M E Coates, B E Gustafsson. Laboratory Animals Ltd, London 1984; 413–34
  • Wilson R, Bealmear P, Matsuzawa T. Acute intestinal radiation death in germfree and conventional mice. Gastrointestinal radiation injury, M F Sullivan. Excerpta Medica Foundation, Amsterdam 1968; 148–58
  • Mastromarino A J, Wilson R. Increased intestinal mucosal turnover and radiosensitivity to supralethal whole-body irradiation resulting from cholic acid-induced alterations of the microecology of germfree CFW mice. Radiat Res 1976; 66: 393–400
  • Osborne J W, Bryan H S, Quastler H, Rhoades H E. X-irradiation and bacteremia. Studies on roentgen death in mice, IV. Am J Physiol 1952; 170: 414–7
  • Spratt J S, Heinbecker P, Saltzstein S L. The influence of succinylsulphathiazole (Sulfasuxidine) upon the response of canine small intestine to irradiation. Cancer 1961; 14: 862–74
  • Toorop-Bouma A G, Van der Waaij D. The effect of selective decontamination of the GI-tract of mice on the survival of intestinal mucosa during X-irradiation. Germfree research, B S Wostmann. Alan R Liss Inc, New York 1985; 271–3
  • Fry R JM, Kisielski W E, Kraft B, Staffeldt E, Sullivan M F. Cell renewal in the intestine of the bile duct cannulated rat. Gastrointestinal radiation injury, M F Sullivan. Excerpta Medica Foundation, Amsterdam 1968; 142–7
  • Jackson K L, Entenman C. The role of bile secretion in the gastrointestinal radiation syndrome. Radiat Res 1959; 10: 67–79
  • Sullivan M F, Hulse E V, Mole R H. The mucus-depleting action of bile in the small intestine of the irradiated rat. Br J Exp Pathol 1965; 46: 235–44
  • Rachootin S, Shapiro S, Yamakawa T, Goldman L, Patin S, Morgenstern L. Potent anti-protease from Ascaris lumbricoides: Efficacy in amelioration of post-radiation enteropathy. Gastroenterology 1972; 62: 796
  • Weser E, Drummond A, Tawil T. Effect of diverting bile and pancreatic secretions into the ileum on small bowel mucosa in rats fed a liquid formula diet. JPEN 1982; 6: 39–42

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.