Systematic review of the benefits and risks of neoadjuvant chemoradiation for oesophageal cancer

British Journal of Surgery

Volumn 97, Issue 10, 2010, Pages 1482-1496

  Courrech Staal, E F W ^a   Aleman, B M P ^a   Boot, H ^a   Van Velthuysen, M L F ^a   Van Tinteren, H ^a   Van Sandick, J W ^a  

^a ANTONI VAN LEEUWENHOEK HOSPITAL   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT;

ADENOCARCINOMA; ADJUVANT CHEMOTHERAPY; ADJUVANT THERAPY; EPIDEMIOLOGY; ESOPHAGUS TUMOR; HUMAN; META ANALYSIS; METHODOLOGY; QUALITY OF LIFE; RADIATION DOSE; REVIEW; SQUAMOUS CELL CARCINOMA; SURVIVAL; TREATMENT OUTCOME; TUMOR RECURRENCE;

ADENOCARCINOMA; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CARCINOMA, SQUAMOUS CELL; CHEMOTHERAPY, ADJUVANT; EPIDEMIOLOGIC METHODS; ESOPHAGEAL NEOPLASMS; HUMANS; NEOPLASM RECURRENCE, LOCAL; QUALITY OF LIFE; RADIOTHERAPY DOSAGE; RADIOTHERAPY, ADJUVANT; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 77957014982     PISSN: 00071323     EISSN: 13652168     Source Type: Journal    
DOI: 10.1002/bjs.7175     Document Type: Review

References (86)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55: 74-108.
2. Steiger Z, Franklin R, Wilson RF, Leichman L, Seydel H, Loh JJ et al. Eradication and palliation of squamous cell carcinoma of the esophagus with chemotherapy, radiotherapy, and surgical therapy. J Thorac Cardiovasc Surg 1981; 82: 713-719. (Pubitemid 11031761)
3. Franklin R, Steiger Z, Vaishampayan G, Asfaw I, Rosenberg J, Loh J et al. Combined modality therapy for esophageal squamous cell carcinoma. Cancer 1983; 51: 1062-1071.
4. Leichman L, Steiger Z, Seydel HG, Vaitkevicius VK. Combined preoperative chemotherapy and radiation therapy for cancer of the esophagus: the Wayne State University, Southwest Oncology Group and Radiation Therapy Oncology Group experience. Semin Oncol 1984; 11: 178-185.
5. Arnott SJ, Duncan W, Gignoux M, Hansen HS, Launois B, Nygaard K et al. Preoperative radiotherapy for esophageal carcinoma. Cochrane Database Syst Rev 2005; (4)CD001799.
6. Tannock IF. Treatment of cancer with radiation and drugs. J Clin Oncol 1996; 14: 3156-3174.
7. Hennequin C, Favaudon V. Biological basis for chemo-radiotherapy interactions. Eur J Cancer 2002; 38: 223-230.
8. Nygaard K, Hagen S, Hansen HS, Hatlevoll R, Hultborn R, Jakobsen A et al. Pre-operative radiotherapy prolongs survival in operable esophageal carcinoma: a randomized, multicenter study of pre-operative radiotherapy and chemotherapy. The second Scandinavian trial in esophageal cancer. World J Surg 1992; 16: 1104-1109.
9. Le Prise E, Etienne PL, Meunier B, Maddern G, Ben Hassel M, Gedouin D et al. A randomized study of chemotherapy, radiation therapy, and surgery versus surgery for localized squamous cell carcinoma of the esophagus. Cancer 1994; 73: 1779-1784.
10. Apinop C, Puttisak P, Preecha N. A prospective study of combined therapy in esophageal cancer. Hepatogastroenterology 1994; 41: 391-393.
11. Walsh TN, Noonan N, Hollywood D, Kelly A, Keeling N, Hennessy TP. A comparison of multimodal therapy and surgery for esophageal adenocarcinoma. N Engl JMed 1996; 335: 462-467.
12. Bosset JF, Gignoux M, Triboulet JP, Tiret E, Mantion G, Elias D et al. Chemoradiotherapy followed by surgery compared with surgery alone in squamous-cell cancer of the esophagus. N Engl JMed 1997; 337: 161-167.
13. Malthaner RA, Collin S, Fenlon D. Preoperative chemotherapy for resectable thoracic esophageal cancer. Cochrane Database Syst Rev 2006; (3)CD001556.
14. Fiorica F, Di Bona D, Schepis F, Licata A, Shahied L, Venturi A et al. Preoperative chemoradiotherapy for oesophageal cancer: a systematic review and meta-analysis. Gut 2004; 53: 925-930.
15. Malthaner RA, Wong RK, Rumble RB, Zuraw L; Members of the Gastrointestinal Cancer Disease Site Group of Cancer Care Ontario's Program in Evidence-based Care. Neoadjuvant or adjuvant therapy for resectable esophageal cancer: a systematic review and meta-analysis. BMC Med 2004; 2: 35.
16. Kaklamanos IG,Walker GR, Ferry K, Franceschi D, Livingstone AS. Neoadjuvant treatment for resectable cancer of the esophagus and the gastroesophageal junction: a meta-analysis of randomized clinical trials. Ann Surg Oncol 2003; 10: 754-761.
17. Urschel JD, Vasan H. A meta-analysis of randomized controlled trials that compared neoadjuvant chemoradiation and surgery to surgery alone for resectable esophageal cancer. Am J Surg 2003; 185: 538-543.
18. Greer SE, Goodney PP, Sutton JE, Birkmeyer JD. Neoadjuvant chemoradiotherapy for esophageal carcinoma: a meta-analysis. Surgery 2005; 137: 172-177.
19. Gebski V, Burmeister B, Smithers BM, Foo K, Zalcberg J, Simes J et al. Survival benefits from neoadjuvant chemoradiotherapy or chemotherapy in oesophageal carcinoma: a meta-analysis. Lancet Oncol 2007; 8: 226-234.
20. Geh JI, Crellin AM, Glynne-Jones R. Preoperative (neoadjuvant) chemoradiotherapy in oesophageal cancer. Br J Surg 2001; 88: 338-356.
21. Kim JH, Choi EK, Kim SB, Park SI, Kim DK, Song HY et al. Preoperative hyperfractionated radiotherapy with concurrent chemotherapy in resectable esophageal cancer. Int J Radiat Oncol Biol Phys 2001; 50: 1-12.
22. Vermund H, PoriesWJ, Hillard J, Wiley AL, Youngblood R. Neoadjuvant chemoradiation therapy in patients with surgically treated esophageal cancer. Acta Oncol 2001; 40: 558-565.
23. Hagry O, CoosemansW, De Leyn P, Nafteux P, Van Raemdonck D, Van Cutsem E et al. Effects of preoperative chemoradiotherapy on postsurgical morbidity and mortality in cT3-4 +/- cM1 lymph cancer of the oesophagus and gastro-oesophageal junction. Eur J Cardiothorac Surg 2003; 24: 179-186.
24. Meluch AA, Greco FA, Gray JR, Thomas M, Sutton VM, Davis JL et al. Preoperative therapy with concurrent paclitaxel/carboplatin/infusional 5-FU and radiation therapy in locoregional esophageal cancer: final results of a Minnie Pearl Cancer Research Network phase II trial. Cancer J 2003; 9: 251-260.
25. Donington JS, Miller DL, Allen MS, Deschamps C, Nichols FC III, Pairolero PC. Tumor response to induction chemoradiation: influence on survival after esophagectomy. Eur J Cardiothorac Surg 2003; 24: 631-636.
26. Urba SG, Orringer MB, Ianettonni M, Hayman JA, Satoru H. Concurrent cisplatin, paclitaxel, and radiotherapy as preoperative treatment for patients with locoregional esophageal carcinoma. Cancer 2003; 98: 2177-2183.
27. Imdahl A, Schüffel U, Ruf G. Impact of neoadjuvant therapy of perioperative morbidity in patients with esophageal cancer. Am J Surg 2004; 187: 64-68.
28. Brücher BL, Stein HJ, Zimmermann F,Werner M, Sarbia M, Busch R et al. Responders benefit from neoadjuvant radiochemotherapy in esophageal squamous cell carcinoma: results of a prospective phase-II trial. Eur J Surg Oncol 2004; 30: 963-971.
29. Kelley ST, Coppola D, Karl RC. Neoadjuvant chemoradiotherapy is not associated with a higher complication rate vs. surgery alone in patients undergoing esophagectomy. J Gastrointest Surg 2004; 8: 227-231.
30. Liao Z, Zhang Z, Jin J, Ajani JA, Swisher SG, Stevens CW et al. Esophagectomy after concurrent chemoradiotherapy improves locoregional control in clinical stage II or III esophageal cancer patients. Int J Radiat Oncol Biol Phys 2004; 60: 1484-1493.
31. Kesler KA, Helft PR,Werner EA, Jain NP, Brooks JA, DeWitt JM et al. A retrospective analysis of locally advanced esophageal cancer patients treated with neoadjuvant chemoradiation therapy followed by surgery or surgery alone. Ann Thorac Surg 2005; 79: 1116-1121.
32. Zhang X,Watson DI, Jamieson GG, Bessell JR, Devitt PG. Neoadjuvant chemoradiotherapy for esophageal carcinoma. Dis Esophagus 2005; 18: 104-108.
33. Burmeister BH, Smithers BM, Gebski V, Fitzgerald L, Simes RJ, Devitt P et al. Surgery alone versus chemoradiotherapy followed by surgery for resectable cancer of the oesophagus: a randomised controlled phase III trial. Lancet Oncol 2005; 6: 659-668.
34. de Manzoni G, Pedrazzani C, Laterza E, Pasini F, Grandinetti A, Bernini M et al. Induction chemoradiotherapy for squamous cell carcinoma of the thoracic esophagus: impact of increased dosage on long-term results. Ann Thorac Surg 2005; 80: 1176-1183.
35. Berger AC, ScottWJ, Freedman G, Konski A, Weiner L, Cheng JD et al. Morbidity and mortality are not increased after induction chemoradiotherapy followed by esophagectomy in patients with esophageal cancer. Semin Oncol 2005; 32(Suppl 9): S16-S20.
36. Berger AC, Farma J, ScottWJ, Freedman G,Weiner L, Cheng JD et al. Complete response to neoadjuvant chemoradiotherapy in esophageal carcinoma is associated with significantly improved survival. J Clin Oncol 2005; 23: 4330-4337.
37. Gaca JG, Petersen RP, Peterson BL, Harpole DH Jr, D'Amico TA, Pappas TN et al. Pathologic nodal status predicts disease-free survival after neoadjuvant chemoradiation for gastroesophageal junction carcinoma. Ann Surg Oncol 2006; 13: 340-346.
38. Reynolds JV, McLaughlin R, Moore J, Rowley S, Ravi N, Byrne PJ. Prospective evaluation of quality of life in patients with localized oesophageal cancer treated by multimodality therapy or surgery alone. Br J Surg 2006; 93: 1084-1090.
39. Bonnetain F, Bouché O, Michel P, Mariette C, Conroy T, Pezet D et al. A comparative longitudinal quality of life study using the Spitzer quality of life index in a randomized multicenter phase III trial (FFCD 9102): chemoradiation followed by surgery compared with chemoradiation alone in locally advanced squamous resectable thoracic esophageal cancer. Ann Oncol 2006; 17: 827-834.
40. van Meerten E, Muller K, Tilanus HW, Siersema PD, Eijkenboom WM, van Dekken H et al. Neoadjuvant concurrent chemoradiation with weekly paclitaxel and carboplatin for patients with oesophageal cancer: a phase II study. Br J Cancer 2006; 94: 1389-1394.
41. Law S, Kwong DL,Wong KH, Kwok KF,Wong J. The effects of neoadjuvant chemoradiation on pTNM staging and its prognostic significance in esophageal cancer. J Gastrointest Surg 2006; 10: 1301-1311.
42. Roof KS, Coen J, Lynch TJ,Wright C, Fidias P,Willett CG et al. Concurrent cisplatin, 5-FU, paclitaxel, and radiation therapy in patients with locally advanced esophageal cancer. Int J Radiat Oncol Biol Phys 2006; 65: 1120-1128.
43. Mariette C, Piessen G, Lamblin A, Mirabel X, Adenis A, Triboulet JP. Impact of preoperative radiochemotherapy on postoperative course and survival in patients with locally advanced squamous cell oesophageal carcinoma. Br J Surg 2006; 93: 1077-1083.
44. Lin CC, Hsu CH, Cheng JC, Wang HP, Lee JM, Yeh KH et al. Concurrent chemoradiotherapy with twice weekly paclitaxel and cisplatin followed by esophagectomy for locally advanced esophageal cancer. Ann Oncol 2007; 18: 93-98.
45. Rizk NP, Venkatraman E, Bains MS, Park B, Flores R, Tang L et al. American Joint Committee on Cancer staging system does not accurately predict survival in patients receiving multimodality therapy for esophageal adenocarcinoma. J Clin Oncol 2007; 25: 507-512.
46. Bedenne L, Michel P, Bouché O, Milan C, Mariette C, Conroy T et al. Chemoradiation followed by surgery compared with chemoradiation alone in squamous cancer of the esophagus: FFCD 9102. J Clin Oncol 2007; 25: 1160-1168.
47. Reynolds JV, Muldoon C, Hollywood D, Ravi N, Rowley S, O'Byrne K et al. Long-term outcomes following neoadjuvant chemoradiotherapy for esophageal cancer. Ann Surg 2007; 245: 707-716.
48. Walshe L, Rowley S, Coffey M, Hollywood D, Kennedy MJ, Gillham C et al. Comparison of two fractionation regimens in the multimodal therapy of cancer of the esophagus. Dis Esophagus 2007; 20: 217-224.
49. Kelsey CR, Chino JP,Willett CG, Clough RW, Hurwitz HI, Morse MA et al. Paclitaxel-based chemoradiotherapy in the treatment of patients with operable esophageal cancer. Int J Radiat Oncol Biol Phys 2007; 69: 770-776.
50. Rizk NP, Seshan VE, Bains MS, Ilson DH, Minsky BD, Tang L et al. Prognostic factors after combined modality treatment of squamous cell carcinoma of the esophagus. J Thorac Oncol 2007; 2: 1117-1123.
51. Luu TD, Gaur P, Force SD, Staley CA, Mansour KA, Miller JI Jr et al. Neoadjuvant chemoradiation versus chemotherapy for patients undergoing esophagectomy for esophageal cancer. Ann Thorac Surg 2008; 85: 1217-1223.
52. Hsu FM, Lin CC, Lee JM, Chang YL, Hsu CH, Tsai YC et al. Improved local control by surgery and paclitaxel-based chemoradiation for esophageal squamous cell carcinoma: results of a retrospective non-randomized study. J Surg Oncol 2008; 98: 34-41.
53. McLoughlin JM, Melis M, Siegel EM, Dean EM, Weber JM, Chern J et al. Are patients with esophageal cancer who become PET negative after neoadjuvant chemoradiation free of cancer? J Am Coll Surg 2008; 206: 879-886.
54. Rizzetto C, DeMeester SR, Hagen JA, Peyre CG, Lipham JC, DeMeester TR. En bloc esophagectomy reduces local recurrence and improves survival compared with transhiatal resection after neoadjuvant therapy for esophageal adenocarcinoma. J Thorac Cardiovasc Surg 2008; 135: 1228-1236.
55. van Meerten E, van der Gaast A, Looman CW, Tilanus HW, Muller K, Essink-Bot ML. Quality of life during neoadjuvant treatment and after surgery for resectable esophageal carcinoma. Int J Radiat Oncol Biol Phys 2008; 71: 160-166.
56. Barbour AP, Jones M, Gonen M, Gotley DC, Thomas J, Thomson DB et al. Refining esophageal cancer staging after neoadjuvant therapy: importance of treatment response. Ann Surg Oncol 2008; 15: 2894-2902.
57. Roedl JB, Colen RR, Holalkere NS, Fischman AJ, Choi NC, Blake MA. Adenocarcinomas of the esophagus: response to chemoradiotherapy is associated with decrease of metabolic tumor volume as measured on PET-CT. Comparison to histopathologic and clinical response evaluation. Radiother Oncol 2008; 89: 278-286.
58. Schneider PM, Metzger R, Schaefer H, Baumgarten F, Vallbohmer D, Brabender J et al. Response evaluation by endoscopy, rebiopsy, and endoscopic ultrasound does not accurately predict histopathologic regression after neoadjuvant chemoradiation for esophageal cancer. Ann Surg 2008; 248: 902-908.
59. Mandard AM, Dalibard F, Mandard JC, Marnay J, Henry-Amar M, Petiot JF et al. Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma. Clinicopathologic correlations. Cancer 1994; 73: 2680-2686.
60. Junker K, Thomas M, Schulmann K, Klinke F, Bosse U, Müller KM. Tumour regression in non-small-cell lung cancer following neoadjuvant therapy. Histological assessment. J Cancer Res Clin Oncol 1997; 123: 469-477.
61. Bruce J, Krukowski ZH, Al Khairy G, Russell EM, Park KG. Systematic review of the definition and measurement of anastomotic leak after gastrointestinal surgery. Br J Surg 2001; 88: 1157-1168.
62. Aaronson NK, Ahmedzai S, Bergman B, Bullinger M, Cull A, Duez NJ et al. The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst 1993; 85: 365-376.
63. Blazeby JM, Conroy T, Hammerlid E, Fayers P, Sezer O, Koller M et al. Clinical and psychometric validation of an EORTC questionnaire module, the EORTC QLQ-OES18, to assess quality of life in patients with oesophageal cancer. Eur J Cancer 2003; 39: 1384-1394.
64. Blazeby JM, Alderson D,Winstone K, Steyn R, Hammerlid E, Arraras J et al. Development of an EORTC questionnaire module to be used in quality of life assessment for patients with oesophageal cancer. The EORTC Quality of Life Study Group. Eur J Cancer 1996; 32A: 1912-1917.
65. Shrier I, Boivin JF, Steele RJ, Platt RW, Furlan A, Kakuma R et al. Should meta-analyses of interventions include observational studies in addition to randomized controlled trials? A critical examination of underlying principles. Am J Epidemiol 2007; 166: 1203-1209.
66. Urba SG, Orringer MB, Turrisi A, Iannettoni M, Forastiere A, Strawderman M. Randomized trial of preoperative chemoradiation versus surgery alone in patients with locoregional esophageal carcinoma. J Clin Oncol 2001; 19: 305-313.
67. Lee JL, Park SI, Kim SB, Jung HY, Lee GH, Kim JH et al. A single institutional phase III trial of preoperative chemotherapy with hyperfractionation radiotherapy plus surgery versus surgery alone for resectable esophageal squamous cell carcinoma. Ann Oncol 2004; 15: 947-954.
68. Tepper J, Krasna MJ, Niedzwiecki D, Hollis D, Reed CE, Goldberg R et al. Phase III trial of trimodality therapy with cisplatin, fluorouracil, radiotherapy, and surgery compared with surgery alone for esophageal cancer: CALGB 9781. J Clin Oncol 2008; 26: 1086-1092.
69. National Cancer Institute Cancer Therapy Evaluation Program (CTEP). http://ctep.cancer.gov/protocolDevelopment/electronic-applications/ctc.htm [accessed 15 October 2009].
70. Lerut T, CoosemansW, Decker G, De Leyn P, Moons J, Nafteux P et al. Diagnosis and therapy in advanced cancer of the esophagus and the gastroesophageal junction. Curr Opin Gastroenterol 2006; 22: 437-441.
71. Zuccaro G Jr, Rice TW, Goldblum J, Medendorp SV, Becker M, Pimentel R et al. Endoscopic ultrasound cannot determine suitability for esophagectomy after aggressive chemoradiotherapy for esophageal cancer. Am J Gastroenterol 1999; 94: 906-912.
72. Mulligan ED, Dunne B, Griffin M, Keeling N, Reynolds JV. Margin involvement and outcome in oesophageal carcinoma: a 10-year experience in a specialist unit. Eur J Surg Oncol 2004; 30: 313-317.
73. Hulscher JB, van Sandick JW, de Boer AG, Wijnhoven BP, Tijssen JG, Fockens P et al. Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the esophagus. N Engl JMed 2002; 347: 1662-1669.
74. Sagar PM, Johnston D, McMahon MJ, Dixon MF, Quirke P. Significance of circumferential resection margin involvement after oesophagectomy for cancer. Br J Surg 1993; 80: 1386-1388.
75. Birbeck KF, Macklin CP, Tiffin NJ, Parsons W, Dixon MF, Mapstone NP et al. Rates of circumferential resection margin involvement vary between surgeons and predict outcomes in rectal cancer surgery. Ann Surg 2002; 235: 449-457.
76. Luna-Peréz P, Bustos-Cholico E, Alvarado I, Maffuz A, Rodríguez-Ramírez S, Gutierrez de la Barrera M et al. Prognostic significance of circumferential margin involvement in rectal adenocarcinoma treated with preoperative chemoradiotherapy and low anterior resection. J Surg Oncol 2005; 90: 20-25.
77. Geh JI, Bond SJ, Bentzen SM, Glynne-Jones R. Systematic overview of preoperative (neoadjuvant) chemoradiotherapy trials in oesophageal cancer: evidence of a radiation and chemotherapy dose response. Radiother Oncol 2006; 78: 236-244.
78. Kerr SF, Norton S, Glynne-Jones R. Delaying surgery after neoadjuvant chemoradiotherapy for rectal cancer may reduce postoperative morbidity without compromising prognosis. Br J Surg 2008; 95: 1534-1540.
79. Moore HG, Gittleman AE, Minsky BD, Wong D, Paty PB, Weiser M et al. Rate of pathologic complete response with increased interval between preoperative combined modality therapy and rectal cancer resection. Dis Colon Rectum 2004; 47: 279-286.
80. Bujko K, Nowacki MP, Kepka L, Oledzki J, Bebenek M, Kryj M. Postoperative complications in patients irradiated pre-operatively for rectal cancer: report of a randomised trial comparing short-term radiotherapy vs chemoradiation. Colorectal Dis 2005; 7: 410-416.
81. van Heijl M, van Lanschot JJ, Koppert LB, Berge Henegouwen MI, Muller K, Steyerberg EWet al. Neoadjuvant chemoradiation followed by surgery versus surgery alone for patients with adenocarcinoma or squamous cell carcinoma of the esophagus (CROSS). BMC Surg 2008; 8: 21.
82. Conroy T, Marchal F, Blazeby JM. Quality of life in patients with oesophageal and gastric cancer: an overview. Oncology 2006; 70: 391-402.
83. Stahl M, Stuschke M, Lehmann N, Meyer HJ, Walz MK, Seeber S et al. Chemoradiation with and without surgery in patients with locally advanced squamous cell carcinoma of the esophagus. J Clin Oncol 2005; 23: 2310-2317.
84. Luthra R, Wu TT, Luthra MG, Izzo J, Lopez-Alvarez E, Zhang L et al. Gene expression profiling of localized esophageal carcinomas: association with pathologic response to preoperative chemoradiation. J Clin Oncol 2006; 24: 259-267.
85. Luthra MG, Ajani JA, Izzo J, Ensor J,Wu TT, Rashid A et al. Decreased expression of gene cluster at chromosome 1q21 defines molecular subgroups of chemoradiotherapy response in esophageal cancers. Clin Cancer Res 2007; 13: 912-919.
86. Ashida A, Boku N, Aoyagi K, Sato H, Tsubosa Y, Minashi K et al. Expression profiling of esophageal squamous cell carcinoma patients treated with definitive chemoradiotherapy: clinical implications. Int J Oncol 2006; 28: 1345-1352.