Downstaging and Tumor Regression in Rectal Cancer Following Neo-Adjuvant Chemoradiotherapy_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

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王林 , 顧晉

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直腸癌; 新輔助放化療; 降期; 腫瘤消退

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Citation： 王林,顧晉. Downstaging and Tumor Regression in Rectal Cancer Following Neo-Adjuvant Chemoradiotherapy. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2011, 18(11): 1147-1150. doi: Copy

1.	Clinical pactice gidlines of rectal cancer 2011v1 [Z]. Available at http://www.nccn.org/professionals/physician_gls/PDF/rectal.pdf.
2.	BeetsTan RG. MRI in rectal cancer: the T stage and circumferential resection margin [J]. Colorectal Dis, 2003, 5(5): 392395.
3.	Brown G, Kirkham A, Williams GT, et al. Highresolution MRI of the anatomy important in total mesorectal excision of the rectum [J]. AJR Am J Roentgenol, 2004, 182(2): 431439.
4.	Brown G, Daniels IR. Preoperative staging of rectal cancer: the MERCURY research project [J]. Recent Results Cancer Res, 2005, 165: 5874.
5.	Salerno G, Daniels IR, Moran BJ, et al. Clarifying margins in the multidisciplinary management of rectal cancer: the MERCURY experience [J]. Clin Radiol, 2006, 61(11): 916923.
6.	Guo M, Gao C, Li D, et al. MRI anatomy of the anal region[J]. Dis Colon Rectum, 2010, 53(11): 15421548.
7.	Sauer R, Becker H, Hohenberger W, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer [J]. N Engl J Med, 2004, 351(17): 17311740.
8.	Larsen SG, Wiig JN, Emblemsvaag HL, et al. Extended total mesorectal excision in locally advanced rectal cancer (T4a) and the clinical role of MRIevaluated neoadjuvant downstaging [J]. Colorectal Dis, 2009, 11(7): 759767.
9.	Das P, Skibber JM, RodriguezBigas MA, et al. Predictors of tumor response and downstaging in patients who receive preoperative chemoradiation for rectal cancer [J]. Cancer, 2007, 109(9): 17501755.
10.	Kim NK, Baik SH, Seong JS, et al. Oncologic outcomes after neoadjuvant chemoradiation followed by curative resection with tumorspecific mesorectal excision for fixed locally advanced rectal cancer: Impact of postirradiated pathologic downstaging on local recurrence and survival [J]. Ann Surg, 2006, 244(6): 10241030.
11.	Theodoropoulos G, Wise WE, Padmanabhan A, et al. Tlevel downstaging and complete pathologic response after preoperative chemoradiation for advanced rectal cancer result in decreased recurrence and improved diseasefree survival [J]. Dis Colon Rectum, 2002, 45(7): 895903.
12.	Francois Y, Nemoz CJ, Baulieux J, et al. Influence of the interval between preoperative radiation therapy and surgery on downstaging and on the rate of sphinctersparing surgery for rectal cancer: the Lyon R9001 randomized trial [J]. J Clin Oncol, 1999, 17(8): 2396.
13.	Hiotis SP, Weber SM, Cohen AM, et al. Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients [J]. J Am Coll Surg, 2002, 194(2): 131135.
14.	Guillem JG, Chessin DB, Cohen AM, et al. Longterm oncologic outcome following preoperative combined modality therapy and total mesorectal excision of locally advanced rectal cancer [J]. Ann Surg, 2005, 241(5): 829836.
15.	Hughes R, GlynneJones R, Grainger J, et al. Can pathological complete response in the primary tumour following preoperative pelvic chemoradiotherapy for T3T4 rectal cancer predict for sterilisation of pelvic lymph nodes, a low risk of local recurrence and the appropriateness of local excision? [J]. Int J Colorectal Dis, 2006, 21(1): 1117.
16.	Onaitis MW, Noone RB, Fields R, et al. Complete response to neoadjuvant chemoradiation for rectal cancer does not influence survival [J]. Ann Surg Oncol, 2001, 8(10): 801806.
17.	Carlo C, Vincenzo V, Luca C, et al. Prognostic value of pathologic complete response after neoadjuvant therapy in locally advanced rectal cancer: longterm analysis of 566 ypCR patients [J]. Int J Radiat Oncol Biol Phys, 2008, 72(1): 99107.
18.	Stipa F, Chessin DB, Shia J, et al. A pathologic complete response of rectal cancer to preoperative combinedmodality therapy results in improved oncological outcome compared with those who achieve no downstaging on the basis of preoperative endorectal ultrasonography [J]. Ann Surg Oncol, 2006, 13(8): 10471053.
19.	Engelen SM, BeetsTan RG, Lahaye MJ, et al. MRI after chemoradiotherapy of rectal cancer: a useful tool to select patients for local excision[J]. Dis Colon Rectum, 2010, 53(7): 979986.
20.	Yeo SG, Kim DY, Kim TH, et al. Local excision following preoperative chemoradiotherapyinduced downstaging for selected cT3 distal rectal cancer [J]. Jpn J Clin Oncol, 2010, 40(8): 754760.
21.	Vincenzo V, Claudio C, Aurelio P, et al. Does downstaging predict improved outcome after preoperative chemoradiation for extraperitoneal locally advanced rectal cancer? A longterm analysis of 165 patients [J]. Int J Radiat Oncol Biol Phys, 2002, 53(3): 664674.
22.	Huh JW, Kim HR. Postoperative chemotherapy after neoadjuvant chemoradiation and surgery for rectal cancer: is it essential for patients with ypT02N0?[J]. J Surg Oncol, 2009, 100(5): 387391.
23.	Fietkau R, Barten M, Klautke G, et al. Postoperative chemotherapy may not be necessary for patients with ypN0category after neoadjuvant chemoradiotherapy of rectal cancer [J]. Dis Colon Rectum, 2006, 49(9): 12841292.
24.	Pasetto LM, Basso U, Sinigaglia G, et al. Rectal cancer adjuvant chemotherapy: when is more useful? [J]. Anticancer Res, 2008, 28(3B): 18051812.
25.	CamposLobato CL, Stocchi L, da Luz MA, et al. Downstaging without complete pathologic response after neoadjuvant treatment improves cancer outcomes for cⅢ but not cⅡ rectal cancers [J]. Ann Surg Oncol, 2010, 17(7): 17581766.
26.	Rullier A, Laurent C, Vendrely V, et al. Impact of colloid response on survival after preoperative radiotherapy in locally advanced rectal carcinoma [J]. Am J Surg Pathol, 2005, 29(5): 602606.
27.	Kalady MF, de CamposLobato LF, Stocchi L, et al. Predictive factors of pathologic complete response after neoadjuvant chemoradiation for rectal cancer [J]. Ann Surg, 2009, 250(4): 582589.
28.	Moore HG, Gittleman AE, Minsky BD, et al. Rate of pathologic complete response with increased interval between preoperative combined modality therapy and rectal cancer resection [J]. Dis Colon Rectum, 2004, 47(3): 279286.
29.	Tulchinsky H, Shmueli E, Figer A, et al. An interval >7 weeks between neoadjuvant therapy and surgery improves pathologic complete response and diseasefree survival in patients with locally advanced rectal cancer [J]. Ann Surg Oncol, 2008, 15(10): 26612667.
30.	HabrGama A, Perez RO, Proscurshim I, et al. Interval between surgery and neoadjuvant chemoradiation therapy for distal rectal cancer: does delayed surgery have an impact on outcome? [J]. Int J Radiat Oncol Biol Phys, 2008, 71(4): 11811188.
31.	Lim SB, Choi HS, Jeong SY, et al. Optimal surgery time after preoperative chemoradiotherapy for locally advanced rectal cancers [J]. Ann Surg, 2008, 248(2): 243251.
32.	Marijnen CA, Nagtegaal ID, Klein Kranenbarg E, et al. No downstaging after shortterm preoperative radiotherapy in rectal cancer patients[J]. J Clin Oncol, 2001, 19(7): 19761984.
33.	Bosset JF, Calais G, Mineur L, et al. Enhanced tumorocidal effect of chemotherapy with preoperative radiotherapy for rectal cancer: preliminary resultsEORTC 22921 [J]. J Clin Oncol, 2005, 23(24): 56205627.
34.	Mandard AM, Dalibard F, Mandard JC, et al. Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma. Clinicopathologic correlations [J]. Cancer, 1994, 73(11): 26802686.
35.	Vecchio FM, Vincenzo V, Minsky BD, et al. The relationship of pathologic tumor regression grade (TRG) and outcomes after preoperative therapy in rectal cancer [J]. Int J Radiat Oncol Biol Phys, 2005, 62(3): 752760.
36.	Vironen J, Juhola M, Kairaluoma M, et al. Tumour regression grading in the evaluation of tumour response after different preoperative radiotherapy treatments for rectal carcinoma [J]. Int J Colorectal Dis, 2005, 20(5): 440445.
37.	Twu CM, Wang HM, Chen JB, et al. Neoadjuvant concurrent chemoradiotherapy in treating locally advanced rectal cancer [J]. J Chin Med Assoc, 2009, 72(4): 179182.
38.	Wheeler JM, Dodds E, Warren BF, et al. Preoperative chemoradiotherapy and total mesorectal excision surgery for locally advanced rectal cancer: correlation with rectal cancer regression grade [J]. Dis Colon Rectum, 2004, 47(12): 20252031.
39.	Ryan R, Gibbons D, Hyland JM, et al. Pathological response following longcourse neoadjuvant chemoradiotherapy for locally advanced rectal cancer [J].Histopathology, 2005, 47(2): 141146.
40.	Dworak O, Keilholz L, Hoffmann A. Pathological features of rectal cancer after preoperative radiochemotherapy [J]. Int J Colorectal Dis, 1997, 12(1): 1923.
41.	Wheeler JM, Warren BF, Mortensen NJ, et al. Quantification of histologic regression of rectal cancer after irradiation: a proposal for a modified staging system [J]. Dis Colon Rectum, 2002, 45(8): 10511056.
42.	Bateman AC, Jaynes E, Bateman AR. Rectal cancer staging post neoadjuvant therapy—how should the changes be assessed? [J]. Histopathology, 2009, 54(6): 713721.
43.	American Joint Committee on Cancer. AJCC cancer staging handbook [Z]. 7th ed. New York: Springer， 2010： 718.
44.	Nagtegaal ID, van de Velde CJ, van der Worp E, et al. Macroscopic evaluation of rectal cancer resection specimen: clinical significance of the pathologist in quality control [J]. J Clin Oncol, 2002, 20(7): 17291734.
45.	Wibe A, Rendedal PR, Svensson E, et al. Prognostic significance of the circumferential resection margin following total mesorectal excision for rectal cancer [J]. Br J Surg, 2002, 89(3): 327334.
46.	SebagMontefiore D, Stephens RJ, Steele R, et al. Preoperative radiotherapy versus selective postoperative chemoradiotherapy in patients with rectal cancer (MRC CR07 and NCICCTG C016): a multicentre, randomised trial [J]. Lancet, 2009, 373(9666): 811820.
47.	Marijnen CA, Nagtegaal ID, Kapiteijn E, et al. Radiotherapy does not compensate for positive resection margins in rectal cancer patients: report of a multicenter randomized trial [J]. Int J Radiat Oncol Biol Phys, 2003, 55(5): 13111320.
48.	Gérard JP, Azria D, GourgouBourgade S, et al. Comparison of two neoadjuvant chemoradiotherapy regimens for locally advanced rectal cancer: results of the phase Ⅲ trial ACCORD 12/0405Prodige 2 [J]. J Clin Oncol, 2010, 28(10): 16381644.

1. Clinical pactice gidlines of rectal cancer 2011v1 [Z]. Available at http://www.nccn.org/professionals/physician_gls/PDF/rectal.pdf.
2. BeetsTan RG. MRI in rectal cancer: the T stage and circumferential resection margin [J]. Colorectal Dis, 2003, 5(5): 392395.
3. Brown G, Kirkham A, Williams GT, et al. Highresolution MRI of the anatomy important in total mesorectal excision of the rectum [J]. AJR Am J Roentgenol, 2004, 182(2): 431439.
4. Brown G, Daniels IR. Preoperative staging of rectal cancer: the MERCURY research project [J]. Recent Results Cancer Res, 2005, 165: 5874.
5. Salerno G, Daniels IR, Moran BJ, et al. Clarifying margins in the multidisciplinary management of rectal cancer: the MERCURY experience [J]. Clin Radiol, 2006, 61(11): 916923.
6. Guo M, Gao C, Li D, et al. MRI anatomy of the anal region[J]. Dis Colon Rectum, 2010, 53(11): 15421548.
7. Sauer R, Becker H, Hohenberger W, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer [J]. N Engl J Med, 2004, 351(17): 17311740.
8. Larsen SG, Wiig JN, Emblemsvaag HL, et al. Extended total mesorectal excision in locally advanced rectal cancer (T4a) and the clinical role of MRIevaluated neoadjuvant downstaging [J]. Colorectal Dis, 2009, 11(7): 759767.
9. Das P, Skibber JM, RodriguezBigas MA, et al. Predictors of tumor response and downstaging in patients who receive preoperative chemoradiation for rectal cancer [J]. Cancer, 2007, 109(9): 17501755.
10. Kim NK, Baik SH, Seong JS, et al. Oncologic outcomes after neoadjuvant chemoradiation followed by curative resection with tumorspecific mesorectal excision for fixed locally advanced rectal cancer: Impact of postirradiated pathologic downstaging on local recurrence and survival [J]. Ann Surg, 2006, 244(6): 10241030.
11. Theodoropoulos G, Wise WE, Padmanabhan A, et al. Tlevel downstaging and complete pathologic response after preoperative chemoradiation for advanced rectal cancer result in decreased recurrence and improved diseasefree survival [J]. Dis Colon Rectum, 2002, 45(7): 895903.
12. Francois Y, Nemoz CJ, Baulieux J, et al. Influence of the interval between preoperative radiation therapy and surgery on downstaging and on the rate of sphinctersparing surgery for rectal cancer: the Lyon R9001 randomized trial [J]. J Clin Oncol, 1999, 17(8): 2396.
13. Hiotis SP, Weber SM, Cohen AM, et al. Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients [J]. J Am Coll Surg, 2002, 194(2): 131135.
14. Guillem JG, Chessin DB, Cohen AM, et al. Longterm oncologic outcome following preoperative combined modality therapy and total mesorectal excision of locally advanced rectal cancer [J]. Ann Surg, 2005, 241(5): 829836.
15. Hughes R, GlynneJones R, Grainger J, et al. Can pathological complete response in the primary tumour following preoperative pelvic chemoradiotherapy for T3T4 rectal cancer predict for sterilisation of pelvic lymph nodes, a low risk of local recurrence and the appropriateness of local excision? [J]. Int J Colorectal Dis, 2006, 21(1): 1117.
16. Onaitis MW, Noone RB, Fields R, et al. Complete response to neoadjuvant chemoradiation for rectal cancer does not influence survival [J]. Ann Surg Oncol, 2001, 8(10): 801806.
17. Carlo C, Vincenzo V, Luca C, et al. Prognostic value of pathologic complete response after neoadjuvant therapy in locally advanced rectal cancer: longterm analysis of 566 ypCR patients [J]. Int J Radiat Oncol Biol Phys, 2008, 72(1): 99107.
18. Stipa F, Chessin DB, Shia J, et al. A pathologic complete response of rectal cancer to preoperative combinedmodality therapy results in improved oncological outcome compared with those who achieve no downstaging on the basis of preoperative endorectal ultrasonography [J]. Ann Surg Oncol, 2006, 13(8): 10471053.
19. Engelen SM, BeetsTan RG, Lahaye MJ, et al. MRI after chemoradiotherapy of rectal cancer: a useful tool to select patients for local excision[J]. Dis Colon Rectum, 2010, 53(7): 979986.
20. Yeo SG, Kim DY, Kim TH, et al. Local excision following preoperative chemoradiotherapyinduced downstaging for selected cT3 distal rectal cancer [J]. Jpn J Clin Oncol, 2010, 40(8): 754760.
21. Vincenzo V, Claudio C, Aurelio P, et al. Does downstaging predict improved outcome after preoperative chemoradiation for extraperitoneal locally advanced rectal cancer? A longterm analysis of 165 patients [J]. Int J Radiat Oncol Biol Phys, 2002, 53(3): 664674.
22. Huh JW, Kim HR. Postoperative chemotherapy after neoadjuvant chemoradiation and surgery for rectal cancer: is it essential for patients with ypT02N0?[J]. J Surg Oncol, 2009, 100(5): 387391.
23. Fietkau R, Barten M, Klautke G, et al. Postoperative chemotherapy may not be necessary for patients with ypN0category after neoadjuvant chemoradiotherapy of rectal cancer [J]. Dis Colon Rectum, 2006, 49(9): 12841292.
24. Pasetto LM, Basso U, Sinigaglia G, et al. Rectal cancer adjuvant chemotherapy: when is more useful? [J]. Anticancer Res, 2008, 28(3B): 18051812.
25. CamposLobato CL, Stocchi L, da Luz MA, et al. Downstaging without complete pathologic response after neoadjuvant treatment improves cancer outcomes for cⅢ but not cⅡ rectal cancers [J]. Ann Surg Oncol, 2010, 17(7): 17581766.
26. Rullier A, Laurent C, Vendrely V, et al. Impact of colloid response on survival after preoperative radiotherapy in locally advanced rectal carcinoma [J]. Am J Surg Pathol, 2005, 29(5): 602606.
27. Kalady MF, de CamposLobato LF, Stocchi L, et al. Predictive factors of pathologic complete response after neoadjuvant chemoradiation for rectal cancer [J]. Ann Surg, 2009, 250(4): 582589.
28. Moore HG, Gittleman AE, Minsky BD, et al. Rate of pathologic complete response with increased interval between preoperative combined modality therapy and rectal cancer resection [J]. Dis Colon Rectum, 2004, 47(3): 279286.
29. Tulchinsky H, Shmueli E, Figer A, et al. An interval >7 weeks between neoadjuvant therapy and surgery improves pathologic complete response and diseasefree survival in patients with locally advanced rectal cancer [J]. Ann Surg Oncol, 2008, 15(10): 26612667.
30. HabrGama A, Perez RO, Proscurshim I, et al. Interval between surgery and neoadjuvant chemoradiation therapy for distal rectal cancer: does delayed surgery have an impact on outcome? [J]. Int J Radiat Oncol Biol Phys, 2008, 71(4): 11811188.
31. Lim SB, Choi HS, Jeong SY, et al. Optimal surgery time after preoperative chemoradiotherapy for locally advanced rectal cancers [J]. Ann Surg, 2008, 248(2): 243251.
32. Marijnen CA, Nagtegaal ID, Klein Kranenbarg E, et al. No downstaging after shortterm preoperative radiotherapy in rectal cancer patients[J]. J Clin Oncol, 2001, 19(7): 19761984.
33. Bosset JF, Calais G, Mineur L, et al. Enhanced tumorocidal effect of chemotherapy with preoperative radiotherapy for rectal cancer: preliminary resultsEORTC 22921 [J]. J Clin Oncol, 2005, 23(24): 56205627.
34. Mandard AM, Dalibard F, Mandard JC, et al. Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma. Clinicopathologic correlations [J]. Cancer, 1994, 73(11): 26802686.
35. Vecchio FM, Vincenzo V, Minsky BD, et al. The relationship of pathologic tumor regression grade (TRG) and outcomes after preoperative therapy in rectal cancer [J]. Int J Radiat Oncol Biol Phys, 2005, 62(3): 752760.
36. Vironen J, Juhola M, Kairaluoma M, et al. Tumour regression grading in the evaluation of tumour response after different preoperative radiotherapy treatments for rectal carcinoma [J]. Int J Colorectal Dis, 2005, 20(5): 440445.
37. Twu CM, Wang HM, Chen JB, et al. Neoadjuvant concurrent chemoradiotherapy in treating locally advanced rectal cancer [J]. J Chin Med Assoc, 2009, 72(4): 179182.
38. Wheeler JM, Dodds E, Warren BF, et al. Preoperative chemoradiotherapy and total mesorectal excision surgery for locally advanced rectal cancer: correlation with rectal cancer regression grade [J]. Dis Colon Rectum, 2004, 47(12): 20252031.
39. Ryan R, Gibbons D, Hyland JM, et al. Pathological response following longcourse neoadjuvant chemoradiotherapy for locally advanced rectal cancer [J].Histopathology, 2005, 47(2): 141146.
40. Dworak O, Keilholz L, Hoffmann A. Pathological features of rectal cancer after preoperative radiochemotherapy [J]. Int J Colorectal Dis, 1997, 12(1): 1923.
41. Wheeler JM, Warren BF, Mortensen NJ, et al. Quantification of histologic regression of rectal cancer after irradiation: a proposal for a modified staging system [J]. Dis Colon Rectum, 2002, 45(8): 10511056.
42. Bateman AC, Jaynes E, Bateman AR. Rectal cancer staging post neoadjuvant therapy—how should the changes be assessed? [J]. Histopathology, 2009, 54(6): 713721.
43. American Joint Committee on Cancer. AJCC cancer staging handbook [Z]. 7th ed. New York: Springer， 2010： 718.
44. Nagtegaal ID, van de Velde CJ, van der Worp E, et al. Macroscopic evaluation of rectal cancer resection specimen: clinical significance of the pathologist in quality control [J]. J Clin Oncol, 2002, 20(7): 17291734.
45. Wibe A, Rendedal PR, Svensson E, et al. Prognostic significance of the circumferential resection margin following total mesorectal excision for rectal cancer [J]. Br J Surg, 2002, 89(3): 327334.
46. SebagMontefiore D, Stephens RJ, Steele R, et al. Preoperative radiotherapy versus selective postoperative chemoradiotherapy in patients with rectal cancer (MRC CR07 and NCICCTG C016): a multicentre, randomised trial [J]. Lancet, 2009, 373(9666): 811820.
47. Marijnen CA, Nagtegaal ID, Kapiteijn E, et al. Radiotherapy does not compensate for positive resection margins in rectal cancer patients: report of a multicenter randomized trial [J]. Int J Radiat Oncol Biol Phys, 2003, 55(5): 13111320.
48. Gérard JP, Azria D, GourgouBourgade S, et al. Comparison of two neoadjuvant chemoradiotherapy regimens for locally advanced rectal cancer: results of the phase Ⅲ trial ACCORD 12/0405Prodige 2 [J]. J Clin Oncol, 2010, 28(10): 16381644.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Downstaging and Tumor Regression in Rectal Cancer Following Neo-Adjuvant Chemoradiotherapy

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