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Epidemiology of treatment-associated mucosal injury after treatment with newer regimens for lymphoma, breast, lung, or colorectal cancer

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Abstract

Goals of work: Oral and gastrointestinal (GI) mucositis are frequent complications of chemotherapy and radiotherapy for cancer, contributing to not only the morbidity of treatment but its cost as well. The risk associated with specific chemotherapeutic agents, alone and in combination, has been characterized previously. In the current study, we sought to estimate the risk associated with newer regimens for the treatment of non-Hodgkin’s lymphoma (NHL) and common solid tumors. Methods: We reviewed published studies reporting phase II and III clinical trials of dose-dense regimens for breast cancer and NHL, TAC (docetaxel, adriamycin, cyclophosphamide) chemotherapy for breast cancer, and infusional 5-fluorouracil-based regimens for colorectal cancer. Platinum-, gemcitabine-, and taxane-based regimens for lung cancer, either alone or in combination with radiotherapy, were also considered. Using modified meta-analysis methods, we calculated quality-adjusted estimates of the risk for oral and GI mucositis by tumor type and regimen. Case reports are used to emphasize the relevance of the findings for patient care. Main results: Our findings demonstrate that mucosal toxicity remains an important complication of cancer treatment. Moreover, innovations in drug combinations, scheduling, or mode of administration significantly modulate the risk for both oral and GI mucositis. Conclusions: Ongoing review of the clinical trial experience will remain important as newer, targeted agents enter standard clinical practice.

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References

  1. Arriagada R, Bergman B, Dunant A, Le Chevalier T, Pignon JP, Vansteenkiste J (2004) Cisplatin-based adjuvant chemotherapy in patients with completely resected non-small-cell lung cancer. N Engl J Med 350:351–360

    Article  PubMed  Google Scholar 

  2. Avritscher EB, Cooksley CD, Elting LS (2004) Scope and epidemiology of cancer therapy-induced oral and gastrointestinal mucositis. Semin Oncol Nurs 20:3–10

    Article  PubMed  Google Scholar 

  3. Bajetta E, Stani SC, De Candis D, Zaffaroni N, Zilembo N, Cortinovis D, Aglione S, Mariani L, Formisano B, Bidoli P (2003) Preclinical and clinical evaluation of four gemcitabine plus carboplatin schedules as front-line treatment for stage IV non-small-cell lung cancer. Ann Oncol 14:242–247

    Article  PubMed  CAS  Google Scholar 

  4. Benson AB 3rd, Schrag D, Somerfield MR, Cohen AM, Figueredo AT, Flynn PJ, Krzyzanowska MK, Maroun J, McAllister P, Van Cutsem E, Brouwers M, Charette M, Haller DG (2004) American Society of Clinical Oncology recommendations on adjuvant chemotherapy for stage II colon cancer. J Clin Oncol 22:3408–3419

    Article  PubMed  Google Scholar 

  5. Bhatia S, Hanna N, Ansari R, Einhorn L, Sandler A (2002) Carboplatin plus paclitaxel and sequential radiation followed by consolidation carboplatin and paclitaxel in patients with previously untreated locally advanced NSCLC. A Hoosier Oncology Group (HOG) phase II study. Lung Cancer 38:85–89

    Article  PubMed  Google Scholar 

  6. Blayney DW, LeBlanc ML, Grogan T, Gaynor ER, Chapman RA, Spiridonidis CH, Taylor SA, Bearman SI, Miller TP, Fisher RI (2003) Dose-intense chemotherapy every 2 weeks with dose-intense cyclophosphamide, doxorubicin, vincristine, and prednisone may improve survival in intermediate- and high-grade lymphoma: a phase II study of the Southwest Oncology Group (SWOG 9349). J Clin Oncol 21:2466–2473

    Article  PubMed  CAS  Google Scholar 

  7. Burtness B, Windsor S, Holston B, DiStasio S, Staugaard-Hahn C, Abrantes J, Kneuper-Hall R, Farber L, Orell J, Bober-Sorcinelli K, Haffty BG, Reiss M (1999) Adjuvant sequential dose-dense doxorubicin, paclitaxel, and cyclophosphamide (ATC) for high-risk breast cancer is feasible in the community setting. Cancer J Sci Am 5:224–229

    PubMed  CAS  Google Scholar 

  8. Chen YM, Perng RP, Lee YC, Shih JF, Lee CS, Tsai CM, Whang-Peng J (2002) Paclitaxel plus carboplatin, compared with paclitaxel plus gemcitabine, shows similar efficacy while more cost-effective: a randomized phase II study of combination chemotherapy against inoperable non-small-cell lung cancer previously untreated. Ann Oncol 13:108–115

    Article  PubMed  CAS  Google Scholar 

  9. Citron ML, Berry DA, Cirrincione C, Hudis C, Winer EP, Gradishar WJ, Davidson NE, Martino S, Livingston R, Ingle JN, Perez EA, Carpenter J, Hurd D, Holland JF, Smith BL, Sartor CI, Leung EH, Abrams J, Schilsky RL, Muss HB, Norton L (2003) Randomized trial of dose-dense versus conventionally scheduled and sequential versus concurrent combination chemotherapy as postoperative adjuvant treatment of node-positive primary breast cancer: first report of Intergroup Trial C9741/Cancer and Leukemia Group B Trial 9741. J Clin Oncol 21:1431–1439

    Article  PubMed  CAS  Google Scholar 

  10. Danesi R, Fogli S, Gennari A, Conte P, Del Tacca M (2002) Pharmacokinetic–pharmacodynamic relationships of the anthracycline anticancer drugs. Clin Pharmacokinet 41:431–444

    Article  PubMed  CAS  Google Scholar 

  11. Danson S, Middleton MR, O’Byrne KJ, Clemons M, Ranson M, Hassan J, Anderson H, Burt PA, Fairve-Finn C, Stout R, Dowd I, Ashcroft L, Beresford C, Thatcher N (2003) Phase III trial of gemcitabine and carboplatin versus mitomycin, ifosfamide, and cisplatin or mitomycin, vinblastine, and cisplatin in patients with advanced nonsmall cell lung carcinoma. Cancer 98:542–553

    Article  PubMed  CAS  Google Scholar 

  12. De Candis D, Stani SC, Bidoli P, Bedini VA, Potepan P, Navarria P, Aglione S, Bajetta E (2003) Induction chemotherapy with carboplatin/paclitaxel followed by surgery or standard radiotherapy and concurrent daily low-dose cisplatin for locally advanced non-small cell lung cancer (NSCLC). Am J Clin Oncol 26:265–269

    Article  PubMed  Google Scholar 

  13. Douillard JY, Peschel C, Shepherd F, Paz-Ares L, Arnold A, Davis M, Tonato M, Smylie M, Tu D, Voi M, Humphrey J, Ottaway J, Young K, Vreckem AV, Seymour L (2004) Randomized phase II feasibility study of combining the matrix metalloproteinase inhibitor BMS-275291 with paclitaxel plus carboplatin in advanced non-small cell lung cancer. Lung Cancer 46:361–368

    Article  PubMed  Google Scholar 

  14. Edelman MJ, Clark JI, Chansky K, Albain K, Bhoopalam N, Weiss GR, Giguere JK, Kelly K, Crowley J, Gandara DR (2004) Randomized phase II trial of sequential chemotherapy in advanced non-small cell lung cancer (SWOG 9806): carboplatin/gemcitabine followed by paclitaxel or cisplatin/vinorelbine followed by docetaxel. Clin Cancer Res 10:5022–5026

    Article  PubMed  CAS  Google Scholar 

  15. Edelman MJ, Gandara DR, Lau DH, Lara P, Lauder IJ, Tracy D (2001) Sequential combination chemotherapy in patients with advanced nonsmall cell lung carcinoma: carboplatin and gemcitabine followed by paclitaxel. Cancer 92:146–152

    Article  PubMed  CAS  Google Scholar 

  16. Ellis GK, Livingston RB, Gralow JR, Green SJ, Thompson T (2002) Dose-dense anthracycline-based chemotherapy for node-positive breast cancer. J Clin Oncol 20:3637–3643

    Article  PubMed  CAS  Google Scholar 

  17. Elting LS, Cooksley C, Chambers M, Cantor SB, Manzullo E, Rubenstein EB (2003) The burdens of cancer therapy. Clinical and economic outcomes of chemotherapy-induced mucositis. Cancer 98:1531–1539

    Article  PubMed  Google Scholar 

  18. Engstrom PF, Benson AB 3rd, Chen YJ, Choti MA, Dilawari RA, Enke CA, Fakih MG, Fuchs C, Kiel K, Knol JA, Leong LA, Ludwig KA, Martin EW Jr, Rao S, Saif MW, Saltz L, Skibber JM, Venook AP, Yeatman TJ (2005) Colon cancer clinical practice guidelines in oncology. J Natl Compr Canc Netw 3:468–491

    PubMed  Google Scholar 

  19. Falcone A, Masi G, Allegrini G, Danesi R, Pfanner E, Brunetti IM, Di Paolo A, Cupini S, Del Tacca M, Conte P (2002) Biweekly chemotherapy with oxaliplatin, irinotecan, infusional fluorouracil, and leucovorin: a pilot study in patients with metastatic colorectal cancer. J Clin Oncol 20:4006–4014

    Article  PubMed  CAS  Google Scholar 

  20. Fisher B (1992) The evolution of paradigms for the management of breast cancer: a personal perspective. [erratum appears in Cancer Res 1992 Jun 15; 52(12):3512]. Cancer Res 52:2371–2383

    PubMed  CAS  Google Scholar 

  21. Fisher RI, Gaynor ER, Dahlberg S, Oken MM, Grogan TM, Mize EM, Glick JH, Coltman CA Jr, Miller TP (1994) A phase III comparison of CHOP vs. m-BACOD vs. ProMACE-CytaBOM vs. MACOP-B in patients with intermediate- or high-grade non-Hodgkin’s lymphoma: results of SWOG-8516 (Intergroup 0067), the National High-Priority Lymphoma Study. Ann Oncol 2(5 Suppl):91–95

    Google Scholar 

  22. Fornier MN, Seidman AD, Theodoulou M, Moynahan ME, Currie V, Moasser M, Sklarin N, Gilewski T, D’Andrea G, Salvaggio R, Panageas KS, Norton L, Hudis C (2001) Doxorubicin followed by sequential paclitaxel and cyclophosphamide versus concurrent paclitaxel and cyclophosphamide: 5-year results of a phase II randomized trial of adjuvant dose-dense chemotherapy for women with node-positive breast carcinoma. Clin Cancer Res 7:3934–3941

    PubMed  CAS  Google Scholar 

  23. Fridrik MA, Greil R, Hausmaninger H, Krieger O, Oppitz P, Stoger M, Klocker J, Neubauer M, Helm W, Pont J, Fazeny B, Hudec M, Simonitsch I, Radaszkiewicz T (1997) Randomized open label phase III trial of CEOP/IMVP-Dexa alternating chemotherapy and filgrastim versus CEOP/IMVP-Dexa alternating chemotherapy for aggressive non-Hodgkin’s lymphoma (NHL). A multicenter trial by the Austrian Working Group for Medical Tumor Therapy. Ann Hematol 75:135–140

    Article  PubMed  CAS  Google Scholar 

  24. Fridrik MA, Hausmaninger H, Linkesch W, Stoger M, Sill H, Neubauer M, Seewann HL, Klocker J, Haidinger R, Schiller L, Pont J, Raudaschl G, Falk M, Radaszkiewicz T (1996) CEOP-IMVP-Dexa in the treatment of aggressive lymphomas: an Austrian multicenter trial. J Clin Oncol 14:227–232

    PubMed  CAS  Google Scholar 

  25. Giannakakis T, Kakolyris S, Theodoropoulos E, Kouroussis C, Michailakis E, Papadouris S, Tsitoura M, Kalbakis K, Souglakos J, Agelaki S, Vardakis N, Georgoulias V (2002) A multicenter phase II study of docetaxel and carboplatin combination as front-line treatment in advanced non-small cell lung cancer. Anticancer Res 22:3743–3748

    PubMed  CAS  Google Scholar 

  26. Goldberg RM, Sargent DJ, Morton RF, Fuchs CS, Ramanathan RK, Williamson SK, Findlay BP, Pitot HC, Alberts SR (2004) A randomized controlled trial of fluorouracil plus leucovorin, irinotecan, and oxaliplatin combinations in patients with previously untreated metastatic colorectal cancer. J Clin Oncol 22:23–30

    Article  PubMed  CAS  Google Scholar 

  27. Goldberg SL, Chiang L, Selina N, Hamarman S (2004) Patient perceptions about chemotherapy-induced oral mucositis: implications for primary/secondary prophylaxis strategies. Support Care Cancer 12:526–530

    Article  PubMed  Google Scholar 

  28. Goldstein D, Mitchell P, Michael M, Beale P, Friedlander M, Zalcberg J, White S, Clarke S (2005) Australian experience of a modified schedule of FOLFOX with high activity and tolerability and improved convenience in untreated metastatic colorectal cancer patients. Br J Cancer 92:832–837

    Article  PubMed  CAS  Google Scholar 

  29. Greco FA, Gray JR Jr, Thompson DS, Burris HA 3rd, Erland JB, Barton JH Jr, Litchy S, Houston GA, Butts JA, Webb C, Scott C, Hainsworth JD (2002) Prospective randomized study of four novel chemotherapy regimens in patients with advanced nonsmall cell lung carcinoma: a minnie pearl cancer research network trial. Cancer 95:1279–1285

    Article  PubMed  CAS  Google Scholar 

  30. Gregory SA, Case DC Jr, Bosserman L, Litwak DL, Berry WR, Kalman LA, Belt RJ, Saven A (2003) Fourteen-day CHOP supported with granulocyte colony-stimulating factor in patients with aggressive non-Hodgkin’s lymphoma: results of a phase II study. Clin Lymphoma 4:93–98

    Article  PubMed  Google Scholar 

  31. Hainsworth JD, Gray JR, Litchy S, Bearden JD, Shaffer DW, Houston GA, Greco FA (2004) A phase II trial of preoperative concurrent radiation therapy and weekly paclitaxel/carboplatin for patients with locally advanced non-small-cell lung cancer. Clin Lung Cancer 6:33–42

    PubMed  CAS  Google Scholar 

  32. Hainsworth JD, Gray JR, Morrissey LH, Kalman LA, Hon JK, Greco FA (2002) Long-term follow-up of patients treated with paclitaxel/carboplatin-based chemotherapy for advanced non-small-cell lung cancer: sequential phase II trials of the Minnie Pearl Cancer Research Network. J Clin Oncol 20:2937–2942

    Article  PubMed  CAS  Google Scholar 

  33. Herbst RS, Giaccone G, Schiller JH, Natale RB, Miller V, Manegold C, Scagliotti G, Rosell R, Oliff I, Reeves JA, Wolf MK, Krebs AD, Averbuch SD, Ochs JS, Grous J, Fandi A, Johnson DH (2004) Gefitinib in combination with paclitaxel and carboplatin in advanced non-small-cell lung cancer: a phase III trial-INTACT 2. J Clin Oncol 22:785–794

    Article  PubMed  CAS  Google Scholar 

  34. Hirabayashi M, Endoh K, Teramachi M, Okuda M, Yamaguchi K, Fukuda K, Tokuhisa H, Kagioka H, Nakai N, Nakade M (2004) Phase II study of carboplatin and weekly paclitaxel combination chemotherapy in advanced non-small cell lung cancer: a Kansai Clinical Oncology Group study. Lung Cancer 44:355–362

    Article  PubMed  Google Scholar 

  35. Hudis C, Seidman A, Baselga J, Raptis G, Lebwohl D, Gilewski T, Moynahan M, Sklarin N, Fennelly D, Crown JP, Surbone A, Uhlenhopp M, Riedel E, Yao TJ, Norton L (1999) Sequential dose-dense doxorubicin, paclitaxel, and cyclophosphamide for resectable high-risk breast cancer: feasibility and efficacy. J Clin Oncol 17:93–100

    PubMed  CAS  Google Scholar 

  36. Hudis CA, Schmitz N (2004) Dose-dense chemotherapy in breast cancer and lymphoma. Semin Oncol 31:19–26

    Article  PubMed  CAS  Google Scholar 

  37. Illiano A, Barletta E, De Marino V, Battiloro C, Barzelloni M, Scognamiglio F, Rossi N, Zampa G, De Bellis M, Gridelli C (2000) New triplet chemotherapy combination with carboplatin, paclitaxel and gemcitabine plus amifostine support in advanced non small cell lung cancer: a phase II study. Anticancer Res 20:3999–4003

    PubMed  CAS  Google Scholar 

  38. Itoh K, Ohtsu T, Fukuda H, Sasaki Y, Ogura M, Morishima Y, Chou T, Aikawa K, Uike N, Mizorogi F, Ohno T, Ikeda S, Sai T, Taniwaki M, Kawano F, Niimi M, Hotta T, Shimoyama M, Tobinai K (2002) Randomized phase II study of biweekly CHOP and dose-escalated CHOP with prophylactic use of lenograstim (glycosylated G-CSF) in aggressive non-Hodgkin’s lymphoma: Japan Clinical Oncology Group Study 9505. Ann Oncol 13:1347–1355

    Article  PubMed  CAS  Google Scholar 

  39. Jatoi A, Stella PJ, Hillman S, Mailliard JA, Vanone S, Perez EA, Cannon MW, Geyer S, Wiesenfeld M, Jett JR (2003) Weekly carboplatin and paclitaxel in elderly non-small-cell lung cancer patients (> or =65 years of age): a phase II North Central Cancer Treatment Group study. Am J Clin Oncol 26:441–447

    Article  PubMed  CAS  Google Scholar 

  40. Jeremic B, Milicic B, Acimovic L, Milisavljevic S (2005) Concurrent hyperfractionated radiotherapy and low-dose daily carboplatin and paclitaxel in patients with stage III non-small-cell lung cancer: long-term results of a phase II study. J Clin Oncol 23:1144–1151

    Article  PubMed  CAS  Google Scholar 

  41. Johnson DH, Fehrenbacher L, Novotny WF, Herbst RS, Nemunaitis JJ, Jablons DM, Langer CJ, DeVore RF 3rd, Gaudreault J, Damico LA, Holmgren E, Kabbinavar F (2004) Randomized phase II trial comparing bevacizumab plus carboplatin and paclitaxel with carboplatin and paclitaxel alone in previously untreated locally advanced or metastatic non-small-cell lung cancer. J Clin Oncol 22:2184–2191

    Article  PubMed  CAS  Google Scholar 

  42. Kaplan B, Altynbas M, Eroglu C, Karahacioglu E, Er O, Ozkan M, Bilgin M, Canoz O, Gulmez I, Gulec M (2004) Preliminary results of a phase II study of weekly paclitaxel (PTX) and carboplatin (CBDCA) administered concurrently with thoracic radiation therapy (TRT) followed by consolidation chemotherapy with PTX/CBDCA for stage III unresectable non-small-cell lung cancer (NSCLC). Am J Clin Oncol 27:603–610

    Article  PubMed  CAS  Google Scholar 

  43. Kortsik C, Albrecht P, Elmer A (2003) Gemcitabine and carboplatin in patients with locally advanced or metastatic non-small cell lung cancer: a prospective phase II study. Lung Cancer 40:85–90

    Article  PubMed  CAS  Google Scholar 

  44. Kuten A, Anacak Y, Abdah-Bortnyak R, Chetver L, Zen Al Deen I, Daoud K, Nijem R, Billan S, Best L (2003) Neoadjuvant radiotherapy concurrent with weekly paclitaxel and carboplatin and followed by surgery in locally advanced non-small-cell lung cancer. Am J Clin Oncol 26:184–187

    Article  PubMed  CAS  Google Scholar 

  45. Lalisang RI, Voest EE, Wils JA, Nortier JW, Erdkamp FL, Hillen HF, Wals J, Schouten HC, Blijham GH (2000) Dose-dense epirubicin and paclitaxel with G-CSF: a study of decreasing intervals in metastatic breast cancer. Br J Cancer 82:1914–1919

    Article  PubMed  CAS  Google Scholar 

  46. Leighl NB, Paz-Ares L, Douillard JY, Peschel C, Arnold A, Depierre A, Santoro A, Betticher DC, Gatzemeier U, Jassem J, Crawford J, Tu D, Bezjak A, Humphrey JS, Voi M, Galbraith S, Hann K, Seymour L, Shepherd FA (2005) Randomized phase III study of matrix metalloproteinase inhibitor BMS-275291 in combination with paclitaxel and carboplatin in advanced non-small-cell lung cancer: National Cancer Institute of Canada—Clinical Trials Group Study BR.18. J Clin Oncol 23:2831–2839

    Article  PubMed  CAS  Google Scholar 

  47. Lombardi D, Crivellari D, Scuderi C, Magri MD, Spazzapan S, Sorio R, Di Lauro V, Scalone S, Veronesi A (2004) Long-term, weekly one-hour infusion of paclitaxel in patients with metastatic breast cancer: a phase II monoinstitutional study. Tumori 90:285–288

    PubMed  CAS  Google Scholar 

  48. Maindrault-Goebel F, de Gramont A, Louvet C, Andre T, Carola E, Mabro M, Artru P, Gilles V, Lotz JP, Izrael V (2001) High-dose intensity oxaliplatin added to the simplified bimonthly leucovorin and 5-fluorouracil regimen as second-line therapy for metastatic colorectal cancer (FOLFOX 7). Eur J Cancer 37:1000–1005

    Article  PubMed  CAS  Google Scholar 

  49. Maindrault-Goebel F, Louvet C, Andre T, Carola E, Lotz JP, Molitor JL, Garcia ML, Gilles-Amar V, Izrael V, Krulik M (1999) Oxaliplatin added to the simplified bimonthly leucovorin and 5-fluorouracil regimen as second-line therapy for metastatic colorectal cancer (FOLFOX6). Eur J Cancer 35:1338–1342

    Article  PubMed  CAS  Google Scholar 

  50. Marsland TA, Garfield DH, Khan MM, Look RM, Boehm KA, Asmar L (2005) Sequential versus concurrent paclitaxel and carboplatin for the treatment of advanced non-small cell lung cancer in elderly patients and patients with poor performance status: results of two Phase II, multicenter trials. Lung Cancer 47:111–120

    Article  PubMed  CAS  Google Scholar 

  51. Martin M (2005) Adjuvant docetaxel for node-positive breast cancer. N Engl J Med 352:2302–2313

    Article  PubMed  CAS  Google Scholar 

  52. Masotti A, Zannini G, Gentile A, Morandini G (2002) Activity of gemcitabine and carboplatin in advanced non-small cell lung cancer: a phase II trial. Lung Cancer 36:99–103

    Article  PubMed  Google Scholar 

  53. Mazzanti P, Massacesi C, Rocchi MB, Mattioli R, Lippe P, Trivisonne R, Buzzi F, De Signoribus G, Tuveri G, Rossi G, Di Lullo L, Sturba F, Morale D, Catanzani S, Pilone A, Bonsignori M, Battelli T (2003) Randomized, multicenter, phase II study of gemcitabine plus cisplatin versus gemcitabine plus carboplatin in patients with advanced non-small cell lung cancer. Lung Cancer 41:81–89

    Article  PubMed  Google Scholar 

  54. Miller KD, McCaskill-Stevens W, Sisk J, Loesch DM, Monaco F, Seshadri R, Sledge GW Jr (1999) Combination versus sequential doxorubicin and docetaxel as primary chemotherapy for breast cancer: a randomized pilot trial of the Hoosier Oncology Group. J Clin Oncol 17:3033–3037

    PubMed  CAS  Google Scholar 

  55. Mott FE, Cable CT, Sharma N (2003) Phase II study of an alternate carboplatin and gemcitabine dosing schedule in advanced non-small-cell lung cancer. Clin Lung Cancer 5:174–176

    Article  PubMed  CAS  Google Scholar 

  56. Nabholtz JM, Cantin J, Chang J, Guevin R, Patel R, Tkaczuk K, Vodvarka P, Lindsay MA, Reese D, Riva A, Mackey J (2002) Phase III trial comparing granulocyte colony-stimulating factor to leridistim in the prevention of neutropenic complications in breast cancer patients treated with docetaxel/doxorubicin/cyclophosphamide: results of the BCIRG 004 trial. Clin Breast Cancer 3:268–275

    Article  PubMed  CAS  Google Scholar 

  57. Nabholtz JM, Mackey J, Smylie M, Tonkin K (1998) Taxane-based three-drug combination in metastatic and adjuvant treatment of breast cancer. Semin Oncol 25:27–31

    PubMed  CAS  Google Scholar 

  58. Nabholtz JM, Mackey JR, Smylie M, Paterson A, Noel DR, Al-Tweigeri T, Tonkin K, North S, Azli N, Riva A (2001) Phase II study of docetaxel, doxorubicin, and cyclophosphamide as first-line chemotherapy for metastatic breast cancer. J Clin Oncol 19:314–321

    PubMed  CAS  Google Scholar 

  59. Nabholtz JM, Smylie M, Mackey JR, Noel D, Paterson AH, al-Tweigeri T, Au D, Sansregret E, Delorme F, Riva A (1997) Docetaxel/doxorubicin/cyclophosphamide in the treatment of metastatic breast cancer. Oncology (Williston Park) 11:37–41

    CAS  Google Scholar 

  60. NCI (2005) Oral Complications of Chemotherapy and Head/Neck Radiation (PDQ): Health Professional Version

  61. Neubauer M, Heaven R, Olivares J, Otsuka A, Paschold E, Sirridge C, Ilegbodu D, Tuttle T, Asmar L (2004) Results of a Phase II study of carboplatin plus gemcitabine in patients with untreated extensive small cell lung cancer. Lung Cancer 46:369–375

    Article  PubMed  Google Scholar 

  62. Ng EW, Sandler AB, Robinson L, Einhorn LH (1999) A phase II study of carboplatin plus gemcitabine in advanced non-small-cell lung cancer (NSCLC): a Hoosier Oncology Group study. Am J Clin Oncol 22:550–553

    Article  PubMed  CAS  Google Scholar 

  63. Norton L (1997) Evolving concepts in the systemic drug therapy of breast cancer. Semin Oncol 24:S10-13-S10-10

    Google Scholar 

  64. O’Brien ME, Splinter T, Smit EF, Biesma B, Krzakowski M, Tjan-Heijnen VC, Van Bochove A, Stigt J, Smid-Geirnaerdt MJ, Debruyne C, Legrand C, Giaccone G (2003) Carboplatin and paclitaxol (Taxol) as an induction regimen for patients with biopsy-proven stage IIIA N2 non-small cell lung cancer: an EORTC phase II study (EORTC 08958). Eur J Cancer 39:1416–1422

    Article  PubMed  CAS  Google Scholar 

  65. Osby E, Hagberg H, Kvaloy S, Teerenhovi L, Anderson H, Cavallin-Stahl E, Holte H, Myhre J, Pertovaara H, Bjorkholm M (2003) CHOP is superior to CNOP in elderly patients with aggressive lymphoma while outcome is unaffected by filgrastim treatment: results of a Nordic Lymphoma Group randomized trial. Blood 101:3840–3848

    Article  PubMed  CAS  Google Scholar 

  66. Pfreundschuh M, Trumper L, Kloess M, Schmits R, Feller AC, Rube C, Rudolph C, Reiser M, Hossfeld DK, Eimermacher H, Hasenclever D, Schmitz N, Loeffler M (2004) Two-weekly or 3-weekly CHOP chemotherapy with or without etoposide for the treatment of elderly patients with aggressive lymphomas: results of the NHL-B2 trial of the DSHNHL. Blood 104:634–641

    Article  PubMed  CAS  Google Scholar 

  67. Pfreundschuh M, Trumper L, Kloess M, Schmits R, Feller AC, Rudolph C, Reiser M, Hossfeld DK, Metzner B, Hasenclever D, Schmitz N, Glass B, Rube C, Loeffler M (2004) Two-weekly or 3-weekly CHOP chemotherapy with or without etoposide for the treatment of young patients with good-prognosis (normal LDH) aggressive lymphomas: results of the NHL-B1 trial of the DSHNHL. Blood 104:626–633

    Article  PubMed  CAS  Google Scholar 

  68. Portlock CS, Qin J, Schaindlin P, Roistacher N, Myers J, Filippa D, Louie D, Zelenetz AD, O’Brien JP, Moskowitz C, Norton L, Yahalom J, Straus DJ, Bertino JR (2004) The NHL-15 protocol for aggressive non-Hodgkin’s lymphomas: a sequential dose-dense, dose-intense regimen of doxorubicin, vincristine and high-dose cyclophosphamide. Ann Oncol 15:1495–1503

    Article  PubMed  CAS  Google Scholar 

  69. Pronzato P, Lionetto R, Botto F, Pensa F, Tognoni A (1998) High-dose intensity cyclophosphamide, epidoxorubicin, vincristine and prednisone by shortened intervals and granulocyte colony-stimulating factor in non-Hodgkin’s lymphoma: a phase II study. Br J Cancer 78:777–780

    PubMed  CAS  Google Scholar 

  70. Razis E, Dimopoulos AM, Bafaloukos D, Papadimitriou C, Kalogera-Fountzila A, Kalofonos H, Briassoulis E, Samantas E, Keramopoulos A, Pavlidis N, Kosmidis P, Fountzilas G (2001) Dose-dense sequential chemotherapy with epirubicin and paclitaxel in advanced breast cancer. Cancer Invest 19:137–144

    Article  PubMed  CAS  Google Scholar 

  71. Recchia F, Saggio G, Nuzzo A, Lalli A, Lullo LD, Cesta A, Rea S (2004) Multicentre phase II study of bifractionated CPT-11 with bimonthly leucovorin and 5-fluorouracil in patients with metastatic colorectal cancer pretreated with FOLFOX. Br J Cancer 91:1442–1446

    PubMed  CAS  Google Scholar 

  72. Rosell R, Gatzemeier U, Betticher DC, Keppler U, Macha HN, Pirker R, Berthet P, Breau JL, Lianes P, Nicholson M, Ardizzoni A, Chemaissani A, Bogaerts J, Gallant G (2002) Phase III randomised trial comparing paclitaxel/carboplatin with paclitaxel/cisplatin in patients with advanced non-small-cell lung cancer: a cooperative multinational trial. Ann Oncol 13:1539–1549

    Article  PubMed  CAS  Google Scholar 

  73. Rudd RM, Gower NH, Spiro SG, Eisen TG, Harper PG, Littler JA, Hatton M, Johnson PW, Martin WM, Rankin EM, James LE, Gregory WM, Qian W, Lee SM (2005) Gemcitabine plus carboplatin versus mitomycin, ifosfamide, and cisplatin in patients with stage IIIB or IV non-small-cell lung cancer: a phase III randomized study of the London Lung Cancer Group. J Clin Oncol 23:142–153

    Article  PubMed  CAS  Google Scholar 

  74. Scagliotti GV, De Marinis F, Rinaldi M, Crino L, Gridelli C, Ricci S, Matano E, Boni C, Marangolo M, Failla G, Altavilla G, Adamo V, Ceribelli A, Clerici M, Di Costanzo F, Frontini L, Tonato M (2002) Phase III randomized trial comparing three platinum-based doublets in advanced non-small-cell lung cancer. J Clin Oncol 20:4285–4291

    Article  PubMed  CAS  Google Scholar 

  75. Schiller JH, Harrington D, Belani CP, Langer C, Sandler A, Krook J, Zhu J, Johnson DH (2002) Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N Engl J Med 346:92–98

    Article  PubMed  CAS  Google Scholar 

  76. Sederholm C (2002) Gemcitabine versus gemcitabine/carboplatin in advanced non-small cell lung cancer: preliminary findings in a phase III trial of the Swedish Lung Cancer Study Group. Semin Oncol 29:50–54

    Article  PubMed  CAS  Google Scholar 

  77. Seidman AD, Hudis CA, Albanel J, Tong W, Tepler I, Currie V, Moynahan ME, Theodoulou M, Gollub M, Baselga J, Norton L (1998) Dose-dense therapy with weekly 1-hour paclitaxel infusions in the treatment of metastatic breast cancer. J Clin Oncol 16:3353–3361

    PubMed  CAS  Google Scholar 

  78. Smith GM, Child JA, Cullen MH, Bailey NP, Woodruffe CM, Fletcher J, Earl H, Barnard D (1996) A phase I trial to assess the value of recombinant human granulocyte colony stimulating factor (R-MeTHuG-CSF, filgrastim) in accelerating the dose rate of chemotherapy for intermediate and high-grade non-Hodgkin’s lymphoma (NHL). The Central Lymphoma Group. Hematol Oncol 14:193–201

    Article  PubMed  CAS  Google Scholar 

  79. Smith RE, Anderson SJ, Brown A, Scholnik AP, Desai AM, Kardinal CG, Lembersky BC, Mamounas EP (2002) Phase II trial of doxorubicin/docetaxel/cyclophosphamide for locally advanced and metastatic breast cancer: results from NSABP trial BP-58. Clin Breast Cancer 3:333–340

    PubMed  CAS  Google Scholar 

  80. Socinski MA, Schell MJ, Peterman A, Bakri K, Yates S, Gitten R, Unger P, Lee J, Lee JH, Tynan M, Moore M, Kies MS (2002) Phase III trial comparing a defined duration of therapy versus continuous therapy followed by second-line therapy in advanced-stage IIIB/IV non-small-cell lung cancer. J Clin Oncol 20:1335–1343

    Article  PubMed  CAS  Google Scholar 

  81. Sonis ST, Elting LS, Keefe D, Peterson DE, Schubert M, Hauer-Jensen M, Bekele BN, Raber-Durlacher J, Donnelly JP, Rubenstein EB (2004) Perspectives on cancer therapy-induced mucosal injury: pathogenesis, measurement, epidemiology, and consequences for patients. Cancer 100:1995–2025

    Article  PubMed  Google Scholar 

  82. Sonis ST, Oster G, Fuchs H, Bellm L, Bradford WZ, Edelsberg J, Hayden V, Eilers J, Epstein JB, LeVeque FG, Miller C, Peterson DE, Schubert MM, Spijkervet FK, Horowitz M (2001) Oral mucositis and the clinical and economic outcomes of hematopoietic stem-cell transplantation. J Clin Oncol 19:2201–2205

    PubMed  CAS  Google Scholar 

  83. Souglakos J, Mavroudis D, Kakolyris S, Kourousis C, Vardakis N, Androulakis N, Agelaki S, Kalbakis K, Tsetis D, Athanasiadis N, Samonis G, Georgoulias V (2002) Triplet combination with irinotecan plus oxaliplatin plus continuous-infusion fluorouracil and leucovorin as first-line treatment in metastatic colorectal cancer: a multicenter phase II trial. J Clin Oncol 20:2651–2657

    Article  PubMed  CAS  Google Scholar 

  84. Stathopoulos GP, Veslemes M, Georgatou N, Antoniou D, Giamboudakis P, Katis K, Tsavdaridis D, Rigatos SK, Dimitroulis I, Bastani S, Loukides S, Vergos K, Marossis K, Grigoratou T, Kalatzi E, Charalambatou M, Paspalli A, Michalopoulou P, Stoka M, Gerogianni A (2004) Front-line paclitaxel-vinorelbine versus paclitaxel-carboplatin in patients with advanced non-small-cell lung cancer: a randomized phase III trial. Ann Oncol 15:1048–1055

    Article  PubMed  CAS  Google Scholar 

  85. Steele JP (2001) Gemcitabine/carboplatin versus cisplatin/etoposide for patients with poor-prognosis small cell lung cancer: a phase III randomized trial with quality-of-life evaluation. Semin Oncol 28:15–18

    Article  PubMed  CAS  Google Scholar 

  86. Taieb J, Artru P, Paye F, Louvet C, Perez N, Andre T, Gayet B, Hebbar M, Goebel FM, Tournigand C, Parc R, de Gramont A (2005) Intensive systemic chemotherapy combined with surgery for metastatic colorectal cancer: results of a phase II study. J Clin Oncol 23:502–509

    Article  PubMed  CAS  Google Scholar 

  87. Tanosaki R, Okamoto S, Akatsuka N, Ishida A, Michikawa N, Masuda Y, Uchida H, Murata M, Kizaki M, Ikeda Y (1994) Dose escalation of biweekly cyclophosphamide, doxorubicin, vincristine, and prednisolone using recombinant human granulocyte colony stimulating factor in non-Hodgkin’s lymphoma. Cancer 74:1939–1944

    Article  PubMed  CAS  Google Scholar 

  88. Tassinari D, Fochessati F, Arcangeli V, Sartori S, Agostini V, Fantini M, Genestreti G, Grassia S, Ioli G, Imola M, Iorio D, Mianulli AM, Monticelli G, Oliverio G, Panzini I, Papi M, Poggi B, Polselli A, Pulini S, Tamburini E, Fattori PP, Ravaioli A (2004) Carboplatin and gemcitabine in the palliative treatment of stage IV non-small cell lung cancer: definitive results of a phase II trial. Tumori 90:54–59

    PubMed  CAS  Google Scholar 

  89. Tsurumi H, Yamada T, Sawada M, Kasahara S, Kanemura N, Kojima Y, Fukuno K, Hara T, Saio M, Takahashi T, Oyama M, Ozawa K, Takami T, Moriwaki H (2004) Biweekly CHOP or THP-COP regimens in the treatment of newly diagnosed aggressive non-Hodgkin’s lymphoma. A comparison of doxorubicin and pirarubicin: a randomized phase II study. J Cancer Res Clin Oncol 130:107–113

    Article  PubMed  CAS  Google Scholar 

  90. Winton T, Livingston R, Johnson D, Rigas J, Johnston M, Butts C, Cormier Y, Goss G, Inculet R, Vallieres E, Fry W, Bethune D, Ayoub J, Ding K, Seymour L, Graham B, Tsao MS, Gandara D, Kesler K, Demmy T, Shepherd F (2005) Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med 352:2589–2597

    Article  PubMed  CAS  Google Scholar 

  91. Younes A (2004) New treatment strategies for aggressive lymphoma. Semin Oncol 31:10–13

    Article  PubMed  CAS  Google Scholar 

  92. Zatloukal P, Petruzelka L, Zemanova M, Kolek V, Skrickova J, Pesek M, Fojtu H, Grygarkova I, Sixtova D, Roubec J, Horenkova E, Havel L, Prusa P, Novakova L, Skacel T, Kuta M (2003) Gemcitabine plus cisplatin vs. gemcitabine plus carboplatin in stage IIIb and IV non-small cell lung cancer: a phase III randomized trial. Lung Cancer 41:321–331

    Article  PubMed  Google Scholar 

  93. Zujewski JA, Eng-Wong J, O’Shaughnessy J, Venzon D, Chow C, Danforth D, Kohler DR, Cusack G, Riseberg D, Cowan KH (2003) A pilot study of dose intense doxorubicin and cyclophosphamide followed by infusional paclitaxel in high-risk primary breast cancer. Breast Cancer Res Treat 81:41–51

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

Ronald Hutchins, Senior Librarian at the UTMDACC Research Medical Library, provided invaluable assistance in conducting the literature searches. We also thank Kelly Johnson for her able administrative coordination of the review process and assistance with data entry.

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Authors and Affiliations

  1. Section of Health Services Research, Department of Biostatistics, The University of Texas M. D. Anderson Cancer Center, Houston, TX, USA

    Jeffrey A. Jones, Elenir B. C. Avritscher, Catherine D. Cooksley & Linda S. Elting

  2. FUNDALEU (Foundation for the Fight Against Leukemia), Buenos Aires, Argentina

    Marisol Michelet

  3. Department of Biostatistics and Applied Mathematics, The University of Texas M. D. Anderson Cancer Center, Houston, TX, USA

    B. Nebiyou Bekele

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  1. Jeffrey A. Jones
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  2. Elenir B. C. Avritscher
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  5. B. Nebiyou Bekele
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  6. Linda S. Elting
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Correspondence to Jeffrey A. Jones.

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Jones, J.A., Avritscher, E.B.C., Cooksley, C.D. et al. Epidemiology of treatment-associated mucosal injury after treatment with newer regimens for lymphoma, breast, lung, or colorectal cancer. Support Care Cancer 14, 505–515 (2006). https://doi.org/10.1007/s00520-006-0055-4

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