Severity scoring systems for radiation-induced GI injury – prioritization for use of GI-ARS medical countermeasures

References

• Abderrahmani R, François A, Buard V, Benderitter M, Sabourin JC, Crandall DL, Milliat F. 2009. Effects of pharmacological inhibition and genetic deficiency of plasminogen activator inhibitor-1 in radiation-induced intestinal injury. Int J Radiat Oncol Biol Phys. 74(3):942–948.
   PubMed Web of Science ®Google Scholar
• Armed Forces Radiobiology Research Institute (AFRRI). 2022. AFRRI Biodosimetry Worksheet, AFRRI Form 331. [accessed 2022 25 Nov]. https://afrri.usuhs.edu/sites/default/files/2022-03/AFRRI_Form_331_v2022_fillable_0.pdf.
   Google Scholar
• Accardi MV, Donini O, Rumage A, Ascah A, Haruna J, Pouliot M, Bujold K, Huang H, Wierzbicki W, Stamatopoulos J, et al. 2020. Characterization of a partial-body irradiation model with oral cavity shielding in nonhuman primates. Int J Radiat Biol. 96(1):100–111.
   PubMed Web of Science ®Google Scholar
• Blakely WF, King GL, Ossetrova NI, Port M. 2011. Molecular biomarkers of acute radiation syndrome and radiation injury. In: Blakely WF, Janiak MK, Edwards K, Duffy F, editors. Radiation bioeffects and countermeasures. Technical Report, North Atlantic Treaty Organization, Research and Technology Organization, Human Factors and Medicine-099 RTO-TR-HFM-099, AC/323(HFM-099)TP/356, Neuilly-sur-Seine. France: RTO. Chapter 5, p 5–1 to 5–22. http://www.rto.nato.int—Use the Publications drop-down menu to select RTO-TR Technial Reports. Enter "Blakely" into Author(s) field, then click Search. Click "Radiation Bioeffects and Countermeasures".
   Google Scholar
• Bujold K, Hauer-Jensen M, Donini O, Rumage A, Hartman D, Hendrickson HP, Stamatopoulos J, Naraghi H, Pouliot M, Ascah A, et al. 2016. Citrulline as a biomarker for gastrointestinal-acute radiation syndrome: Species differences and experimental condition effects. Radiat Res. 186(1):71–78.
   PubMed Web of Science ®Google Scholar
• Cai WB, Roberts SA, Bowley E, Hendry JH, Potten CS. 1997. Differential survival of murine small and large intestinal crypts following ionizing radiation. Int J Radiat Biol. 71(2):145–155.
   PubMed Web of Science ®Google Scholar
• Centers of Disease Control (CDC). 2022. Acute radiation syndrome: a fact sheet for clinicians. [accessed 2022 Nov 15]. https://www.cdc.gov/nceh/radiation/emergencies/arsphysicianfactsheet.htm.
   Google Scholar
• Cella L, D'Avino V, Liuzzi R, Conson M, Doria F, Faiella A, Loffredo F, Salvatore M, Pacelli R. 2013. Multivariate normal tissue complication probability modeling of gastrointestinal toxicity after external beam radiotherapy for localized prostate cancer. Radiat Oncol. 8:221.
   PubMed Web of Science ®Google Scholar
• Cox JD, Stetz J, Pajak TF. 1995. Toxicity criteria of the Radiation Therapy Oncology Group (RTOG) and the European Organization for Research and Treatment of Cancer (EORTC). Int J Radiat Oncol Biol Phys. 31(5):1341–1346.
   PubMed Web of Science ®Google Scholar
• Deng W, Kimura Y, Gududuru V, Wu W, Balogh A, Szabo E, Thompson E, Yates K, Balazs CR, Johnson L, et al. 2015. Mitigation of the hematopoietic and gastrointestinal acute radiation syndrome by octadecenyl thiophosphate, a small molecule mimic of lysophosphatidic acid. Radiat Res. 183(4):465–475.
   PubMed Web of Science ®Google Scholar
• Farese A, Cohen M, Katz B, Smith C, Jackson W III, Cohen D, MacVittie T. 2012. A nonhuman primate model of the hematopoietic acute radiation syndrome plus medical management. Health Phys. 103(4):367–382.
   PubMed Web of Science ®Google Scholar
• Farese A, Cohen M, Katz B, Smith C, Gibbs A, Cohen D, MacVittie T. 2013. Filgrastim improves survival in lethally irradiated nonhuman primates. Radiat Res. 179(1):89–100.
   PubMed Web of Science ®Google Scholar
• Farese AM, MacVittie TJ. 2015. Filgrastim for the treatment of hematopoietic acute radiation syndrome. Drugs Today. 51(9):537–548.
   PubMed Web of Science ®Google Scholar
• Farese AM, Bennett AW, Gibbs AM, Hankey KG, Prado K, Jackson W III, MacVittie TJ. 2019. Efficacy of Neulasta or Neupogen on H-ARS and GI-ARS mortality and hematopoietic recovery in nonhuman primates after 10-Gy irradiation with 2.5% bone marrow sparing. Health Phys. 116(3):339–353.
   PubMed Web of Science ®Google Scholar
• Felemovicius I, Bonsack MEM, Baptista L, Delaney JP. 1995. Intestinal radioprotection by vitamin E (alpha-tocopherol). Ann Surg. 222(4):504–510.
   PubMed Web of Science ®Google Scholar
• Friesecke I, Beyrer K, Fliedner TM. 2001. How to cope with radiation accidents: the medical management. Br J Radiol. 74(878):121–122.
   PubMed Web of Science ®Google Scholar
• Macià I Garau M, Lucas Calduch A, López EC. 2011. Radiobiology of the acute radiation syndrome. Rep Pract Oncol Radiother. 16(4):123–130.
   PubMedGoogle Scholar
• Gasperetti T, Miller T, Gao F, Narayanan J, Jacobs ER, Szabo A, Cox GN, Orschell CM, Fish BL, Medhora M. 2021. Polypharmacy to mitigate acute and delayed radiation syndromes. Front Pharmacol. 12:634477.
   PubMed Web of Science ®Google Scholar
• Hamilton E. 1977. Differences in survival of mouse colon crypts after whole- or partial-body irradiation. Int J Radiat Biol Relat Stud Phys Chem Med. 31(4):341–347.
   PubMed Web of Science ®Google Scholar
• Hauer-Jensen M, Wang J, Boerma M, Fu Q, Denham JW. 2007. Radiation damage to the gastrointestinal tract: mechanisms, diagnosis, and management. Curr Opin Support Palliat Care. 1(1):23–29.
   PubMedGoogle Scholar
• Hick JL, Bader JL, Coleman CN, Ansari AJ, Chang A, Salame-Alfie A, Hanfling D, Koerner JF. 2018. Proposed “exposure and symptom triage” (EAST) tool to assess radiation exposure after a nuclear detonation. Disaster Med Public Health Prep. 12(3):386–395.
   PubMed Web of Science ®Google Scholar
• Jones JW, Bennett A, Carter CL, Tudor G, Hankey KG, Farese AM, Booth C, MacVittie TJ, Kane MA. 2015. Citrulline as a biomarker in the non-human primate total- and partial-body irradiation models: correlation of circulating citrulline to acute and prolonged gastrointestinal injury. Health Phys. 109(5):440–451.
   PubMed Web of Science ®Google Scholar
• Jones JW, Tudor G, Li F, Tong Y, Katz B, Farese AM, MacVittie TJ, Booth C, Kane MA. 2015. Citrulline as a biomarker in the murine total-body irradiation model: correlation of circulating and tissue citrulline to small intestine epithelial histopathology. Health Phys. 109(5):452–465.
   PubMed Web of Science ®Google Scholar
• Kaur A, Ten Have GAM, Hritzo B, Deutz NEP, Olsen C, Moroni M. 2020. Morphological and functional impairment in the gut in a partial body irradiation minipig model of GI-ARS. Int J Radiat Biol. 96(1):112–128.
   PubMed Web of Science ®Google Scholar
• Kiang JG, Olabisi AO. 2019. Radiation: a poly-traumatic hit leading to multi-organ injury. Cell Biosci. 9:25.
   PubMed Web of Science ®Google Scholar
• Kiang JG, Cannon G, Olson MG, Zhai M, Woods AK, Lin B, Li X, Hull L, Xu F, Cui W, et al. 2023. Ciprofloxacin enhances Neulasta efficacy in mitigating the radiation-induced brain, bone marrow, ileum and spleen injury and mortality: Increases in P-akt and tight junction, and decreases in P-p38, C3/IL-18, and MiR-34a. Bethesda (MD): Armed Forces Radiobiology Research Institute, Uniformed Services University of the Health Sciences. https://mhsrs.amedd.army.mil/.
   Google Scholar
• King GL, Sandgren DJ, Mitchell JM, Bolduc DL, Blakely WF. 2018. System for scoring severity of acute radiation syndrome response in rhesus macaques (Macaca mulatta). Comp Med. 68(6):474–488.
   PubMed Web of Science ®Google Scholar
• Koch A, Gulani J, King G, Hieber K, Chappell M, Ossetrova N. 2016. Establishment of early endpoints in mouse total-body irradiation model. PLOS One. 11(8):e0161079.
   PubMed Web of Science ®Google Scholar
• Lutgens LCHW, Deutz NEP, Gueulette J, Cleutjens JPM, Berger MPF, Wouters BG, von Meyenfeldt MF, Lambin P. 2003. Citrulline: a physiologic marker enabling quantitation and monitoring of epithelial radiation-induced small bowel damage. Int J Radiat Oncol Biol Phys. 57(4):1067–1074.
   PubMed Web of Science ®Google Scholar
• Lutgens LC, Deutz N, Granzier-Peeters M, Beets-Tan R, De Ruysscher D, Gueulette J, Cleutjens J, Berger M, Wouters B, von Meyenfeldt M, et al. 2004. Plasma citrulline concentration: a surrogate end point for radiation-induced mucosal atrophy of the small bowel. A feasibility study in 23 patients. Int J Radiat Oncol Biol Phys. 60(1):275–285.
   PubMed Web of Science ®Google Scholar
• Lutgens L, Lambin P. 2007. Biomarkers for radiation-induced small bowel epithelial damage: an emerging role for plasma citrulline. World J Gastroenterol. 13(22):3033–3042.
   PubMed Web of Science ®Google Scholar
• MacVittie TJ, Farese AM, Jackson W. 2005. Defining the full therapeutic potential of recombinant growth factors in the post radiation-accident environment: the effect of supportive care plus administration of G-CSF. Health Phys. 89(5):546–555.
   PubMed Web of Science ®Google Scholar
• MacVittie TJ, Farese AM, Bennett A, Gelfond D, Shea-Donohue T, Tudor G, Booth C, McFarland E, Jackson W. 2012. The acute gastrointestinal subsyndrome of the acute radiation syndrome: a rhesus macaque model. Health Phys. 103(4):411–426.
   PubMed Web of Science ®Google Scholar
• MacVittie TJ, Farese AM, Parker GA, Jackson W, Booth C, Tudor GL, Hankey KG, Potten CS. 2019. The gastrointestinal subsyndrome of the acute radiation syndrome in rhesus macaques: a systematic review of the lethal dose-response relationship with and without medical management. Health Phys. 116(3):305–338.
   PubMed Web of Science ®Google Scholar
• MacVittie TJ, Jackson W III. 2020. Acute radiation-induced GI-ARS and H-ARS in a canine model of mixed neutron/gamma relative to reference Co-60 gamma radiation: a retrospective study. Health Phys. 119(3):351–357.
   PubMed Web of Science ®Google Scholar
• MacVittie TJ, Bennett AW, Farese AM, Taylor-Howell C, Smith CP, Gibbs AM, Prado K, Jackson W. 3rd. 2015. The effect of radiation dose and variation in Neupogen® initiation schedule on the mitigation of myelosuppression during the concomitant GI-ARS and H-ARS in a nonhuman primate model of high-dose exposure with marrow sparing. Health Phys. 109(5):427–439.
   PubMed Web of Science ®Google Scholar
• Measey TJ, Pouliot M, Wierzbicki W, Swanson C, Brown D, Authier S, Donini O. 2018. Pilot study of radiation-induced gastrointestinal injury in a hemi-body shielded Gottingen minipig model. Health Phys. 114(1):43–57.
   PubMed Web of Science ®Google Scholar
• Medhora M, Gao F, Gasperetti T, Narayanan J, Khan AH, Jacobs ER, Fish BL. 2019. Delayed effects of acute radiation exposure (DEARE) in juvenile and old rats: mitigation by lisinopril. Health Phys. 116(4):529–545.
   PubMed Web of Science ®Google Scholar
• Miousse IR, Ewing LE, Skinner CM, Pathak R, Garg S, Kutanzi KR, Melnyk S, Hauer-Jensen M, Koturbash I. 2020. Methionine dietary supplementation potentiates ionizing radiation-induced gastrointestinal syndrome. Am J Physiol Gastrointest Liver Physiol. 318(3):G439–G450.
   PubMed Web of Science ®Google Scholar
• MyBiosource.com. 2022. Human citrulline ELISA Kit. [accessed 2022 Nov 25]. https://www.mybiosource.com/human-elisa-kits/citrulline/2601236.
   Google Scholar
• Ossetrova NI, Blakely WF, Nagy V, McGann C, Ney PH, Christensen CL, Koch AL, Gulani J, Sigal GB, Glezer EN, et al. 2016. Non-human primate total-body irradiation model with limited and full medical supportive care including filgrastim for biodosimetry and injury assessment. Radiat Prot Dosimetry. 172(1-3):174–191.
   PubMed Web of Science ®Google Scholar
• Nunamaker EA, Artwohl JE, Anderson RJ, Fortman JD. 2013. Endpoint refinement for total body irradiation of C57BL/6 mice. Comp Med. 63(1):22–28.
   PubMed Web of Science ®Google Scholar
• Okunieff P, Chen Y, Maguire DJ, Huser AK. 2008. Molecular markers of radiation-related normal tissue toxicity. Cancer Metastasis Rev. 27(3):363–374.
   PubMed Web of Science ®Google Scholar
• Patil R, Szabó R, Fells JI, Balogh A, Fujiwara KG, Norman Y, Lee DD, Balazs S-C, Thomas L, Patil F, et al. 2015. Combined mitigation of the gastrointestinal and hematopoietic acute radiation syndromes by an LPA2 receptor-specific nonlipid agonist. Chem Biol. 22(2):206–216.
   PubMedGoogle Scholar
• Polistena A, Johnson LB, Röme A, Wittgren L, Bäck S, Osman N, Molin G, Adawi D, Jeppsson B. 2011. Matrilysin expression related to radiation and microflora changes in murine bowel. J Surg Res. 167(2):e137–e143.
   PubMed Web of Science ®Google Scholar
• Romesser PB, Kim AS, Jeong J, Mayle A, Dow LE, Lowe SW. 2019. Preclinical murine platform to evaluate therapeutic countermeasures against radiation-induced gastrointestinal syndrome. Proc Natl Acad Sci U S A. 116(41):20672–20678.
   PubMed Web of Science ®Google Scholar
• Shadad AK, Sullivan FJ, Martin JD, Egan LJ. 2013. Gastrointestinal radiation injury: prevention and treatment. World J Gastroenterol. 19(2):199–208.
   PubMed Web of Science ®Google Scholar
• Shea-Donohue T, Fasano A, Zhao A, Notari L, Yan S, Sun R, Bohl JA, Desai N, Tudor G, Morimoto M, et al. 2016. Mechanisms involved in the development of the chronic gastrointestinal syndrome in nonhuman primates after total-body irradiation with bone marrow shielding. Radiat Res. 185(6):591–603.
   PubMed Web of Science ®Google Scholar
• Shim S, Jang WS, Lee SJ, Jin S, Kim J, Lee SS, Bang HY, Jeon BS, Park S. 2014. Development of a new minipig model to study radiation-induced gastrointestinal syndrome and its application in clinical research. Radiat Res. 181(4):387–395.
   PubMed Web of Science ®Google Scholar
• Somosy Z, Horváth G, Telbisz A, Réz G, Pálfia Z. 2002. Morphological aspects of ionizing radiation response of small intestine. Micron. 33(2):167–178.
   PubMed Web of Science ®Google Scholar
• Thompson KE, Ray RM, Alli S, Ge W, Boler A, Shannon McCool W, Meena AS, Shukla PK, Rao R, Johnson LR, et al. 2018. Prevention and treatment of secretory diarrhea by the lysophosphatidic acid analog Rx100. Exp Biol Med. 243(13):1056–1065.
   Web of Science ®Google Scholar
• Tigyi GJ, Johnson LR, Lee SC, Norman DD, Szabo E, Balogh A, Thompson K, Boler A, McCool WS., 2019. Lysophosphatidic acid type 2 receptor agonists in targeted drug development offer broad therapeutic potential. J Lipid Res. 60(3):464–474.
   PubMed Web of Science ®Google Scholar
• Vigneulle RM, Vriesendorp HM, Taylor P, Burns W, Pelkey T. 1989. Survival after total-body irradiation. I. Effects of partial small bowel shielding. Radiat Res. 119(2):313–324.
   PubMed Web of Science ®Google Scholar
• Wang J, Boerma M, Fu Q, Kulkarni A, Fink LM, Hauer-Jensen M., 2007. Simvastatin ameliorates radiation enteropathy development after localized, fractionated irradiation by a protein C-independent mechanism. Int J Radiat Oncol Biol Phys. 68(5):1483–1490.
   PubMed Web of Science ®Google Scholar
• Waselenko JK, MacVittie TJ, Blakely WF, Pesik N, Wiley AL, Dickerson WE, Tsu H, Confer DL, Coleman CN, Seed T, et al. 2004. Medical management of the acute radiation syndrome: recommendations of the Strategic National Stockpile Radiation Working Group. Ann Intern Med. 140(12):1037–1051.
   PubMed Web of Science ®Google Scholar
• West CM, Davidson SE. 2009. Measurement tools for gastrointestinal symptoms in radiation oncology. Curr Opin Support Palliat Care. 3(1):36–40.
   PubMedGoogle Scholar
• Ye F, Ning J, Fardous Z, Katsube T, Li Q, Wang B. 2020. Citrulline, a potential biomarker of radiation-induced small intestine damage. Dose Response. 18(3):1559325820962341.
   Web of Science ®Google Scholar
• Zheng J, Wang J, Pouliot M, Authier S, Zhou D, Loose DS, Hauer-Jensen M. 2015. Gene expression profiling in non-human primate jejunum, ileum and colon after total-body irradiation: a comparative study of segment-specific molecular and cellular responses. BMC Genomics. 16:984.
   PubMed Web of Science ®Google Scholar