Emerging evidence on the pathobiology of mucositis

Supportive Care in Cancer

Volumn 21, Issue 7, 2013, Pages 2075-2083

  Al Dasooqi, Noor ^a   Sonis, Stephen T ^b   Bowen, Joanne M ^a   Bateman, Emma ^a   Blijlevens, Nicole ^c   Gibson, Rachel J ^a   Logan, Richard M ^a   Nair, Raj G ^d   Stringer, Andrea M ^e   Yazbeck, Roger ^e   Elad, Sharon ^f   Lalla, Rajesh V ^g  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d QUEENSLAND HEALTH   (Australia)

^e UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^f UNIVERSITY OF ROCHESTER   (United States)

^g UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Alimentary tract; Cancer therapy; Mucosal injury; Pharmacogenetics; Targeted drugs; Toxicity

Indexed keywords

ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR; PACLITAXEL; PROTEIN TYROSINE KINASE INHIBITOR; TRASTUZUMAB;

ABDOMINAL PAIN; DIARRHEA; GASTROINTESTINAL SYMPTOM; GENETIC POLYMORPHISM; HUMAN; INFLAMMATION; MICROBIOME; MUCOSA INFLAMMATION; PATHOLOGY; PHARMACOGENOMICS; PREDICTION; PRIORITY JOURNAL; QUALITY OF LIFE; REVIEW; RISK FACTOR; TISSUE STRUCTURE; VOMITING;

HUMANS; MUCOSITIS; NEOPLASMS;

EID: 84878678617     PISSN: 09414355     EISSN: 14337339     Source Type: Journal    
DOI: 10.1007/s00520-013-1810-y     Document Type: Review

References (105)

1. Elting L et al (2003) The burdens of cancer therapy: clinical and economic outcomes of chemotherapy-induced mucositis. Cancer 98:1531-1539
2. Sonis S et al (2004) Perspectives on cancer therapy-induced mucosal injury: pathogenesis, measurement, epidemiology, and consequences for patients. Cancer 100:1995-2025
3. Capp A et al (2009) Is there more than one proctitis syndrome? A revisitation using data from the TROG 96.01 trial. Radiother Oncol 90:400-407
4. Keefe D et al (2007) Updated clinical practice guidelines for the prevention and treatment of mucositis. Cancer 109:820-831
5. Aprile G et al (2008) Application of distance matrices to define associations between acute toxicities in colorectal cancer patients receiving chemotherapy. Cancer 112:284-292
6. Murphy B (2007) Clinical and economic consequences of mucositis induced by chemotherapy and/or radiation therapy. J Support Oncol 5:13-21
7. Sonis S (2004) The pathobiology of mucositis. Nat Rev Cancer 4:277-284
8. Sonis S et al (2002) The gene expression sequence of radiated mucosa in an animal mucositis model. Cell Prolif 35:s92-s102
9. Sonis S et al (1990) An animal model for mucositis induced by cancer chemotherapy. Oral Surg, Oral Med, Oral Pathol 69:437-443
10. Paris F et al (2001) Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science 293:293-297
11. Logan R et al (2009) Is the pathobiology of chemotherapy-induced alimentary tract mucositis influenced by the type of mucotoxic drug administered? Cancer Chemother Pharmacol 63:239-251
12. Sonis S et al (2000) Defining mechanisms of action of interleukin-11 on the progression of radiation-induced oral mucositis in hamsters. Oral Oncol 36:373-381
13. Yeoh A et al (2005) Nuclear factor κB (NFκB) and cyclooxygenase-2 (COX-2) expression in the irradiated colorectum is associated with subsequent histopathological changes. Int J Radiat Oncol Biol Phys 63:1295-1303
14. Manzano M et al (2007) Intestinal toxicity induced by 5-fluorouracil in pigs: a new preclinical model. Chemotherapy 53:344-355
15. Stringer A et al (2009) Irinotecan-induced mucositis manifesting as diarrhoea corresponds with an amended intestinal flora and mucin profile. Int J Exp Pathol 90:489-499
16. Stringer A et al (2009) Chemotherapy-induced changes to microflora: evidence and implications of change. Curr Drug Metab 10:79-83
17. Stringer A et al (2007) Chemotherapy-induced diarrhea is associated with changes in the luminal environment in the DA rat. Exp Biol Med 232:96-106
18. Al-Dasooqi N et al (2011) Irinotecan-induced alterations in intestinal cell kinetics and extracellular matrix component expression in the dark agouti rat. Int J Exp Pathol 92:357-365
19. Al-Dasooqi N et al (2010) Matrix metalloproteinases are possible mediators for the development of alimentary tract mucositis in the DA rat. Exp Biol Med 235:1244-1256
20. Anthony L et al (2007) New thoughts on the pathobiology of regimen-related mucosal injury. Support Care Cancer 14:516-518
21. Hannum Y (1997) Apoptosis and the dilemma of cancer chemotherapy. Blood 89:1845-1853
22. Kerr J, Winterford C, Harmon B (1994) Apoptosis: its significant in cancer and cancer therapy. Cancer 73:2013-2026
23. Gibson R et al (2005) Relationship between dose of methotrexate, apoptosis, p53/p21 expression and intestinal crypt proliferation in the rat. Clin Exp Med 4:188-195
24. Bowen J et al (2005) Cytotoxic chemotherapy up-regulates pro-apoptotic Bax and Bak in the small intestine of rats and humans. Pathology 37:56-62
25. Keefe D (2000) Chemotherapy for cancer causes apoptosis that precedes hypoplasia in crypts of the small intestine in humans. Gut 47:632-637
26. Sonis S et al (1992) Effect of epidermal gorwth factor on ulcerative mucositis in hamsters that receive chemotherapy. Oral Surg, Oral Med, Oral Pathol 74:749-755
27. Gibson R et al (2007) Establishment of a single-dose irinotecan model of gastrointestinal mucositis. Chemotherapy 53:360-369
28. Gibson R et al (2006) Apoptosis occurs early in the basal layer of the oral mucosa following cancer chemotherapy. Asia Pac J Clin Oncol 2:39-49
29. Li C et al (2011) The correlation between the severity of radiotherapy-induced glossitis and endothelial cell injury in local tissues in a rat model. Med Oral Pathol Oral Cir Bucal 16:e711-e715
30. Carneiro-Filho B et al (2004) Intestinal barrier function and secretion in methotrexate-induced rat intestinal mucositis. Dig Dis Sci 49:65-72
31. Chen P et al (2011) Role of AMP-18 in oral mucositis. Oral Oncol 47:831-839
32. Huang T et al (2009) Minocycline attenuates 5-fluorouracil-induced small intestinal mucositis in mouse model. Biochem Biophys Res Commun 389:634-639
33. Meredith J, Fazeli B, Schwartz M (1993) The extracellular matrix as a cell survival factor. Mol Biol Cell 4:953-961
34. Afshar S, Phelan K, O'Donnell C, Bragdon C, Castro D, Sonis S (2002) A new in vivo model for the study of mucosal disease. International Association for Dental Research Meeting Abstract 16220
35. Phelan S, Afshar S, O'Donnell C, Bragdon C, Castro D, Shklar G, Sonis S (2002) A mucosal graft model to evaluate radiation induced injury. International Association for Dental Research Meeting Abstract 0221
36. Beutheu Youmba S et al (2012) Methotrexate modulates tight junctions through NFkB, MEK, and JNK pathways. J Pediatric Gastroenterol Nutr 54:463-470
37. Hamada K et al (2010) Zonula Occluden-1 alterations and enhances intestinal permeability in methotrexate-treated rats. Cancer Chemother Pharmacol 66:1031-1038
38. Al-Sadi R et al (2010) IL-1beta-induced increase in intestinal epithelial tight junction permeability is mediated by MEKK-1 activation of canonical NF-kappaB pathway. Am J Pathol 177:2310-2322
39. Al-Sadi R et al (2008) Mechanism of IL-1beta-induced increase in intestinal epithelial tight junction permeability. J Immunol 180:5653-5661
40. Ma T et al (2004) TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 286:G367-G376
41. Han X, Fink M, Delude R (2003) Proinflammatory cytokines cause NO*-dependent and -independent changes in expression and localization of tight junction proteins in intestinal epithelial cells. Shock 19:229-237
42. Melichar B et al (2005) Intestinal permeability in the assessment of intestinal toxicity of cytotoxic agents. Chemotherapy 51:336-338
43. Logan R et al (2008) Characterisation of mucosal changes in the alimentary tract following administration of irinotecan: implications for the pathobiology of mucositis. Cancer Chemother Pharmacol 62:33-41
44. Sonis S (2002) The biologic role for nuclear factor-kappaB in disease and its potential involvement in mucosal injury associated with anti-neoplastic therapy. Crit Rev Oral BiolMed 13:380-389
45. Sonis S (2004) A biological approach to mucositis. J Support Oncol 2:21-32
46. Sonis S et al (2004) The relationship between mucosal cyclooxygenase-2 (COX-2) expression and experimental radiation-induced mucositis. Oral Oncol 40:170-176
47. Logan R et al (2007) Nuclear factor-kB (NFkB) and cyclooxygenase-2 expression in the oral mucosa following cancer chemotherapy. Oral Oncol 43:395-401
48. Haagen J et al (2009) Effect of selective inhibitors of inflammation on oral mucositis: preclinical studies. Radiother Oncol 92:472-476
49. Ong Z et al (2010) Pro-inflammatory cytokines play a key role in the development of radiotherapy-induced gastrointestinal mucositis. Radiat Oncol 16:22
50. Logan R et al (2007) The role of pro-inflammatory cytokines in cancer treatment-induced alimentary tract mucositis: pathobiology, animal models and cytotoxic drugs. Cancer Treat Rev 33:448-460
51. Logan R et al (2008) Serum levels of NFkappaB and pro-inflammatory cytokines following administration of mucotoxic drugs. Cancer Biol Ther 7:1139-1145
52. Lima V et al (2005) Effects of tumour necrosis factor-alpha inhibitors pentoxifylline and thalidomide in short-term experimental oral mucositis in hamsters. Eur J Oral Sci 113:210-217
53. Melo M et al (2008) Role of cytokines (TNF-alpha, IL-1beta and KC) in the pathogenesis of CPT-11-induced intestinal mucositis in mice: effect of pentoxifylline and thalidomide. Cancer Chemother Pharmacol 61:775-784
54. Fiochhi C (1998) Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 115:182-205
55. de Koning B et al (2006) Contributions of mucosal immune cells to methotrexate-induced mucositis. Int Immunol 18:941-949
56. Bultzingslowen I et al (2006) Growth factors and cytokines in the prevention and treatment of oral and gastrointestinal mucositis. Support Care Cancer 14:519-527
57. Gibson R et al (2002) Effect of interleukin-11 on ameliorating intestinal damage after methotrexate treatment of breast cancer in rats. Dig Dis Sci 47:2751-2757
58. Antin J et al (2002) A phase I/II double-blind, placebo-controlled study of recombinant human interleukin-11 for mucositis and acute GVHD prevention in allogeneic stem cell transplantation. Bone Marrow Transplant 29:373-377
59. Zhao J et al (2004) Oral RDP58 allows CPT-11 dose intensification for enhanced tumor response by decreasing gastrointestinal toxicity. Clin Cancer Res 10:2851-2859
60. Frei E et al (1965) The nature and control of infections in patients with acute leukemia. Cancer Res 25:1511-1515
61. Dreizen S, Bodey G, Brown L (1974) Opportunistic gram-negative bacillary infections in leukemia. Oral manifestations during myelosuppression. Post Med 55:133-139
62. Stringer A et al (2008) Faecal microflora and β-glucuronidase expression are altered in an irinotecan-induced diarrhoea model in rats. Cancer Biol Ther 7:1919-1925
63. Stringer A et al (2009) Gastrointestinal microflora and mucins play a role in the development of 5-fluorouracil-induced gastrointestinal mucositis in rats. Exp Biol Med 234:430-441
64. Shao Z et al (2011) Effects of intensity-modulated radiotherapy on human oral microflora. J Radiat Res 52:834-839
65. Napenas J et al (2010) Molecular methodology to assess the impact of cancer chemotherapy on the oral bacterial flora: a pilot study. Oral Surg, Oral Med, Oral Pathol, Oral Radiol Endodentics 109:554-560
66. van Vliet M et al. (2010) The role of intestinal microbiota in the development and severity of chemotherapy-induced mucositis. PLoS Pathog 6(5): e1000879
67. Martin M, van Saene H (1992) The role of oral microorganisms in cancer therapy. Curr Opin Dent 2:81-84
68. Bochud P et al (1994) Bacteremia due to viridans streptococcus in neutropenic patients with cancer: clinical spectrum and risk factors. Clin Infect Dis 18:25-31
69. Ruescher T et al (1998) The impact of mucositis on alpha-hemolytic streptococcal infection in patients undergoing autologous bone marrow transplantation for hematologic malignancies. Cancer 82:2275-2281
70. Soga Y et al (2011) Bacterial substitution of coagulase-negative staphylococci for streptococci on the oral mucosa after hematopoietic cell transplantation. Support Care Cancer 19:995-1000
71. van der Velden W, Donnelly J, Blijlevens N (2012) Lymphocyte subsets, granulocyte-colony-stimulating factor responsiveness and post-stem cell transplantation infections: mucositis is the underestimated confounder? Cytotherapy 14:381-383
72. Sonis S (2009) Mucositis: the impact, biology and therapeutic opportunities of oral mucositis. Oral Oncol 45:1015-1020
73. Barasch A et al (2006) Antimicrobials, mucosal coating agents, anesthetics, analgesics, and nutritional supplements for alimentary tract mucositis. Support Care Cancer 14:528-532
74. Blijlevens N, Donnelly J, DePauw B (2000) Mucosal barrier injury: biology, pathology, clinical counterparts and consequences of intensive treatment for haematological malignancy: an overview. Bone Marrow Transplant 25:1269-1278
75. Prisciandaro L et al (2011) Probiotic factors partially improve parameters of 5-fluorouracil-induced intestinal mucositis in rats. Cancer Biol Ther 11:671-677
76. Gibson R et al. (2013) Systematic review of agents for the management of gastrointestinal mucositis in cancer patients. Supportive Care Cancer 21(1):313-26
77. Blijlevens N, Donnelly J (2011) Mucosal barrier injury and infections. In: Safdar A (ed) Principles and practice of cancer infectious diseases, current clinical oncology. Springer Science, New York
78. Wisplinghoff H et al (2003) Current trends in the epidemiology of nosocomial bloodstream infections in patients with hematological malignancies and solid neoplasms in hospitals in the United States. Clin Infect Dis 36:1103-1110
79. Keefe D, Bateman E (2011) Tumor control versus adverse events with targeted anticancer therapies. Nat Rev Clin Oncol 9:98-109
80. Sonis S et al (2010) Preliminary characterization of oral lesions associated with inhibitors of mammalian target of rapamycin in cancer patients. Cancer 116:210-215
81. Toi M et al (2009) Lapatinib monotherapy in patients with relapsed, advanced, or metastatic breast cancer: efficacy, safety, and biomarker results from Japanese patients phase II studies. Br J Cancer 101(10):1676-1682
82. Sawaki M et al (2004) Efficacy and safety of trastuzumab as a single agent in heavily pretreated patients with HER-2/neu-overexpressing metastatic breast cancer. Tumori 90(1):40-43
83. Keefe D, Gibson R (2007) Mucosal injury from targeted anticancer therapy. Support Care Cancer 15:483-490
84. Burris H (2004) Dual kinase inhibition in the treatment of breast cancer: initial experience with the EGFR/ErbB-2 inhibitor lapatinib. Oncologist 9:10-15
85. Geyer CE et al (2006) Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 355(26):2733-2743
86. Al-Dasooqi N et al (2008) Trastuzumab induces gastrointestinal side effects in HER2-overexpressing breast cancer patients. Investig New Drugs 27:173-178
87. Fountzilas G et al (2001) Weekly paclitaxel as first-line chemotherapy and trastuzumab in patients with advanced breast cancer. A Hellenic Cooperative Oncology Group phase II study. Ann Oncol 12:1545-1551
88. Bartsch R et al (2007) Capecitabine and trastuzumab in heavily pretreated metastatic breast cancer. J Clin Oncol 25:3853-3858
89. Ruiz M et al (2008) Phase-II study of weekly schedule of trastuzumab, paclitaxel, and carboplatin followed by a week off every 28 days for HER2+ metastatic breast cancer. Cancer Chemother Pharmacol 62:1085-1090
90. Bowen J et al (2012) Development of a rat model of oral small molecule receptor tyrosine kinase inhibitor-induced diarrhoea. Cancer Biol Ther 13(13):1269-75
91. Peterson D, Keefe D, Sonis S (2012) New frontiers in mucositis. ASCO Educational Book. American Society of Clinical Oncology, Alexandria, pp. 545-61
92. Keefe D (1998) The effect of cytotoxic chemotherapy on the mucosa of the small intestine. Department of Medicine University of Adelaide, Adelaide
93. Pico J, Avila-Garavito A, Naccache P (1998) Mucositis: its occurence, consequences and treatment in the oncology setting. The Oncologist volume 3:p446-451
94. Sloan J et al (2002) Women experience greater toxicity with fluorouracil-based chemotherapy for colorectal cancer. J Clin Oncol 20:1491-1498
95. Pratesi N et al (2011) Association between single nucleotide polymorphisms in XRCC1 and RAD51 genes and clinical radiosensitivity in head and neck cancer. Radiother Oncol 99:356-362
96. West C, Dunning A, Rosenstein (2012) Genome-wide association studies and prediction of normal tissue toxicity. Sem Radiat Oncol 22:91-99
97. Thomas F et al (2011) Methylenetetrahydrofolate reductase genetic polymorphisms and toxicity to 5-FU-based chemoradiation in rectal cancer. Br J Cancer 105:1654-1662
98. Werbrouck J et al (2009) Acute normal tissue reactions in head-and-neck cancer patients treated with IMRT: influence of dose and association with genetic polymorphisms in DNA DSB repair genes. Int J Radiat Oncol Biol Phys 73:1187-1195
99. Schwab M et al (2008) Role of genetic and nongenetic factors for fluorouracil treatment-related severe toxicity: a prospective clinical trial by the German 5-FU Toxicity Study Group. J Clin Oncol 26:2131-2138
100. Cho H et al (2010) Glutathione-S-transferase genotypes influence the risk of chemotherapy-related toxicities and prognosis in Korean patients with diffuse large B-cell lymphoma. Cancer CGenet Cytogenet 198:40-46
101. Hahn T et al (2010) A deletion polymorphism in glutathione-S-transferase mu (GSTM1) and/or theta (GSTT1) is associated with an increased risk of toxicity after autologous blood and marrow transplantation. Biol Blood Marrow Transplant 16:801-808
102. Alterovitz G et al (2011) Personalized medicine for mucositis: bayesian networks identify unique gene clusters which predict the response to gamma-D-glutamyl-L-tryptophan (SCV-07) for the attenuation of chemoradiation-induced oral mucositis. Oral Oncol 47:951-955
103. Roseth A (2003) Determination of faecal calprotectin, a novel marker of organic gastrointestinal disorders. Dig Liver Dis 35:607-609
104. Lutgens L et al. (2005) Monitoring myeloablative therapy-induced small bowel toxicity by serum citrulline concentration: a comparison with sugar permeability tests. Cancer 103(1):191-9
105. Xanthinaki A et al (2008) Apoptosis and inflammation markers in oral mucositis in head and neck cancer patients receiving radiotherapy: preliminary report. Support Care Cancer 16:1025-1033