Response assessment in oncology: Limitations of anatomic response criteria in the era of tailored treatments

Quarterly Journal of Nuclear Medicine and Molecular Imaging

Volumn 55, Issue 6, 2011, Pages 589-602

  Carnaghi, C ^a,c   Sclafani, F ^b   Basilico, V ^c   Doherty, M ^b  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

^c Humanitas Mater Domini   (Italy)

Author keywords

Diagnostic imaging; Graft vs. tumor effect; Positron Emission tomography

Indexed keywords

FLUORODEOXYGLUCOSE F 18;

CANCER RESEARCH; CELL PROLIFERATION; CLINICAL DECISION MAKING; DIAGNOSTIC IMAGING; HUMAN; METHODOLOGY; MOLECULAR BIOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATIENT IDENTIFICATION; PERSONALIZED MEDICINE; POSITRON EMISSION TOMOGRAPHY; PRACTICE GUIDELINE; PREOPERATIVE TREATMENT; REVIEW; SURVIVAL RATE; TREATMENT OUTCOME; TREATMENT PLANNING; TREATMENT RESPONSE; TUMOR GROWTH; TUMOR VOLUME;

HUMANS; MOLECULAR IMAGING; NEOPLASMS; OUTCOME ASSESSMENT (HEALTH CARE); PATIENT-CENTERED CARE; SUBTRACTION TECHNIQUE; TREATMENT OUTCOME;

EID: 84857523143     PISSN: 18244785     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (80)

1. Wu W, Shi Q, Sargent DJ. Statistical considerations for the next generation of clinical trials. Semin Oncol 2011;38:598-604
2. Rubistein LV. Therapeutic studies. Hematol Oncol Clin North Am 2000;14:849-76.
3. Miller AB, Hoogstraten B, Staquet M, Winkler A. Reporting results of cancer treatment. Cancer 1981;47:207-14. (Pubitemid 11167383)
4. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 2000;92:205-16.
5. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D et al. New response evaluation criteria in solid tumours: Revised RECIST guideline (version 1.1). Eur J Cancer 2009;45:228-47.
6. Weber WA. Assessing tumor response to therapy. J Nucl Med 2009;50(Suppl 1):1S-10S.
7. Curran SD, Muellner AU, Schwartz LH. Imaging response assessment in oncology. Cancer Imaging 2006;6:126-30.
8. Harry VN, Semple SI, Parkin DE, Gilbert FJ. Use of new imaging techniques to predict tumour response to therapy. Lancet Oncol 2010;11.92-102.
9. Park JO, Lee SI, Song SY, Kim K, Kim WS, Jung CW et al. Measuring response in solid tumors: comparison of RECIST and WHO response criteria. Jpn J Clin Oncol 2003;33:533-5.
10. James K, Eisenhauer E, Christian M, Terenziani M, Vena D, Muldal A et al. Measuring response in solid tumors: unidimensional versus bidimensional measurement. J Natl Cancer Inst 1999;91:523-8. (Pubitemid 29157060)
11. Erasmus JJ, Gladish GW, Broemeling L, Sabloff BS, Truong MT, Herbst RS et al. Interobserver and intraobserver variability in measurement of non-small-cell carcinoma lung lesions: implications for assessment of tumor response. J Clin Oncol 2003;21:2574-82. (Pubitemid 46606340)
12. McNitt-Gray MF, Bidaut LM, Armato SG, Meyer CR, Gavrielides MA, Fenimore C et al. Computed tomography assessment of response to therapy: tumor volume change measurement, truth, data, and error. Transi Oncol 2009;2:216-22.
13. Schwartz LH, Mazumdar M, Wang L, Smith A, Marion S, Panicek DM et al. Response assessment classification in patients with advanced renal cell carcinoma treated on clinical trials. Cancer 2003;98:1611-9. (Pubitemid 37238616)
14. Therasse P. Measuring the clinical response. What does it mean? Eur J Cancer 2002;38:1817-23. (Pubitemid 35256090)
15. Therasse P, Eisenhauer EA, Verweij J. RECIST revisited: a review of validation studies on tumour assessment. Eur J Cancer 2006;42:1031-9.
16. Schwartz LH, Colville JA, Ginsberg MS, Wang L, Mazumdar M, Kalaigian J et al. Measuring tumor response and shape change on CT: esophageal cancer as a paradigm. Ann Oncol 2006;17:1018-23. (Pubitemid 43778997)
17. Scher HI, Morris MJ, Kelly WK, Schwartz LH, Heller G. Prostate cancer clinical trial end points: RECISTing a step backwards. Clin Cancer Res 2005;11:5223-32. (Pubitemid 41003710)
18. Gehan EA, Tefft MC. Will there be resistance to the RECIST (Response Evaluation Criteria in Solid Tumors)? J NatlCancer Inst 2000;92:179-81. (Pubitemid 30099776)
19. Nishino M, Jackman DM, Hatabu H, Yeap BY, Cioffredi LA, Yap JT et al. New response evaluation criteria in solid tumors (RECIST) guidelines for advanced non-small cell lung cancer: comparison with original RECIST and impact on assessment of tumor response to targeted therapy. AJR Am J Roentgenol 2010;195:W221-8.
20. Moertel CG, Hanley JA. The effect of measuring error on the results of therapeutic trials in advanced cancer. Cancer 1976;38:388-94.
21. Ford R, Schwartz L, Dancey J, Dodd LE, Eisenhauer EA, Gwyther S et al. Lessons learned from independent central review. Eur J Cancer 2009;45:268-74.
22. Van de Steene J, Linthout N, de Mey J, Vinh-Hung V, Claassens C, Noppen M et al. Definition of gross tumor volume in lung cancer: inter-observer variability. Radiother Oncol 2002;62:37-49.
23. Desar IME, van Herpen CML, van Laarhoven HWM, Barentsz JO, Oyen WJG, van der Graaf WTA. Beyond RECIST: Molecular and functional imaging techniques for evaluation of response to targeted therapy. Cancer Treatment Reviews 2009;35:309-21.
24. Forner A, Ayuso C, Varela M, Rimola J, Hessheimer AJ, de Lope CR et al. Evaluation of tumor response after locoregional therapies in hepatocellular carcinoma: are response evaluation criteria in solid tumors reliable? Cancer 2009;115:616-23.
25. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008;359:378-90.
26. Vossen JA, Buijs M, Kamel IR. Assessment of tumor response on MR imaging after locoregional therapy. Tech Vasc Interv Radiol 2006;9:125-32. (Pubitemid 46875018)
27. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
28. Levine ZH, Galloway BR, Peskin AP, Heussel CP, Chen JJ. Tumor volume measurement errors of RECIST studied with ellipsoids. Med Phys 2011;38:2552-7.
29. Steger S, Franco F, Sverzellati N, Chiari G, Colomer R. 3D assessment of lymph nodes vs. RECIST 1.1. Acad Radiol 2011;18:391-4.
30. Tran LN, Brown MS, Goldin JG, Heussel CP, Chen JJ. Comparison of treatment response classifications between unidimensional, bidimensional, and volumetric measurements of metastatic lung lesions on chest computed tomography. Acad Radiol 2004;11:1355-60. (Pubitemid 39642822)
31. Prasad SR, Jhaveri KS, Saini S, Hahn PF, Halpern EF, Sumner J. CT tumor measurement for therapeutic response assessment: comparison of unidimensional, bidimensional, and volumetric techniques initial observations. Radiology 2002;225:416-9. (Pubitemid 35239241)
32. Werner-Wasik M, Xiao Y, Peguignot E, Curran WJ, Hauck W. Assessment of lung cancer response after nonoperative therapy: tumor diameter, bidimensional product, and volume. A serial CT scan-based study. Int J Radiat Oncol Phys 2001;51:56-61. (Pubitemid 32758861)
33. Shah GD, Kesari S, Xu R, Batchelor TT, O'Neill AM, Hochberg FH et al. Comparison of linear and volumetric criteria in assessing tumor response in adult high-grade gliomas. Neuro Oncol 2006;8:38-46. (Pubitemid 43154449)
34. Plathow C, Kloop M, Thieke C, Herth F, Thomas A, Schmaehl A et al. Therapy response in malignant pleural mesothelioma-role of MRI using RECIST, modified RECIST and volumetric approaches in comparison with CT. Eur Radiol 2008;18:1635-43.
35. Birchard KR, Hoang JK, Herndon JE Jr, Patz EF Jr. Early changes in tumor size in patients treated for advanced stage nonsmall cell lung cancer do not correlate with survival. Cancer 2009;115:581-6.
36. Zhao B, Oxnard GR, Moskowitz CS, Kris MG, Pao W, Guo P et al. A pilot study of volume measurement as a method of tumor response evaluation to aid biomarker development. Clin Cancer Res 2010;16:4647-53.
37. Frauenfelder T, Tutic M, Weder W, Götti RP, Stahel RA, Seifert B et al. Volumetry: an alternative to assess therapy response for malignant pleural mesothelioma? Eur Respir J 2011;38:162-8.
38. Ak G, Metintas M, Metintas S, Yildirim H, Ozkan R, Ozden H. Three-dimensional evaluation of chemotherapy response in malignant pleural mesothelioma. Eur J Radiol 2010;74:130-5.
39. Liu F, Zhao B, Krug LM, Ishill NM, Lim RC, Guo P et al. Assessment of therapy responses and prediction of survival in malignant pleural mesothelioma through computer-aided volumetric measurement on computed tomography scans. J Thorac Oncol 2010;5:879-84.
40. Ceresoli GL, Chiti A, Zucali PA, Cappuzzo F, De Vincenzo F, Cavina R et al. Assessment of tumor response in malignant pleural mesothelioma. Cancer Treat Rev 2007;33:533-41. (Pubitemid 47355343)
41. Van Klaveren RJ, Aerts JG, de Bruin H, Giaccone G, Manegold C, van Meerbeeck JP. Inadequacy of the RECIST criteria for response evaluation in patients with malignant pleural mesothelioma. Lung Cancer 2004;43:63-9. (Pubitemid 38096293)
42. Mehrara E, Forssell-Aronsson E, Bernhardt P. Objective assessment of tumour response to therapy based on tumour growth kinetics. Br J Cancer 2011;105:682-6.
43. Piessevaux H, Buyse M, De Roock W, Prenen H, Schlichting M, Van Cutsem E et al. Radiological tumor size decrease at week 6 is a potent predictor of outcome in chemorefractory metastatic colorectal cancer treated with cetuximab (BOND trial). Ann Oncol 2009;20:1375-82.
44. Pietras K, Ostman A, Sjoquist M, Buchdunger E, Reed RK, Heldin CH et al. Inhibition of platelet-derived growth factor receptors reduces interstitial hypertension and increases transcapillary transport in tumors. Cancer Res 2001;61:2929-34. (Pubitemid 32691937)
45. Demetri GD, von Mehren M, Blanke CD, Van den Abbeele AD, Eisenberg B, Roberts PJ et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 2002;347:472-80. (Pubitemid 34879334)
46. Antoch G, Kanja J, Bauer S, Kuehl H, Renzing-Koehler K, Schuette J et al. Comparison of PET, CT, and dual-modality PET/CT imaging for monitoring of imatinib (STI-571) therapy in patients with gastrointestinal stromal tumors. J Nucl Med 2004;45:357-65. (Pubitemid 47618607)
47. Choi H, Charnsangavej C, Faria SC, Macapinlac HA, Burgess MA, Patel SR et al. Correlation of computed tomography and positron emission tomography in patients with metastatic gastrointestinal stromal tumor treated at a single institution with imatinib mesylate: proposal of new computed tomography response criteria. J Clin Oncol 2007;25:1753-9. (Pubitemid 46797957)
48. Benjamin RS, Choi H, Macapinlac HA, Burgess MA, Patel SR, Chen LL et al. We should desist using RECIST, at least in GIST. J Clin Oncol 2007;25:1760-4. (Pubitemid 46797958)
49. Bradbury P, Seymour L. Tumor shrinkage and objective response rates: gold standard for oncology efficacy screening trials, or an outdated endpoint? Cancer J 2009;15:354-60.
50. Dhani N, Tu D, Sargent DJ, Seymour L, Moore MJ. Alternate endpoints for screening phase II studies. Clin Caner Res 2009;15:1873-82.
51. Lara P, Redman M, Kelly K, Edelman MJ, Williamson SK, Crowley JJ et at. Disease control rate at 8 weeks predicts clinical benefit in advanced non-small cell lung cancer: results from Southwest Oncology Group randomized trials. J Clin Oncol 2008;26:463-7. (Pubitemid 351171700)
52. Heun JM, Grothey A, Branda ME, Goldberg RM, Sargent DJ. Tumor status at 12 weeks predicts survival in advanced colorectal cancer: findings from NCCTG N9741. Oncologist 2011;16.859-67.
53. An MW, Mandrekar SJ, Branda ME, Hillman SL, Adjei AA, Pitot HC et al. Comparison of continuous versus categorical tumor measurement-based metrics to predict overall survival in cancer treatment trials. Clin Cancer Res 2011;17:6592-9.
54. Sirohi B, Ashley S, Norton A, Popat S, Hughes S, Papadopoulos P et at. Early response to platinum-based first-line chemotherapy in non-small cell lung cancer may predict survival. J Thorac Oncol 2007;2:735-40. (Pubitemid 47357528)
55. Pisters KM, Kris MG, Gralla RJ, Zaman MB, Heelan RT, Martini N. Pathologic complete response in advanced non-small-cell lung cancer following preoperative chemotherapy: implications for the design of future non-small-cell lung cancer combined modality trials. J Clin Oncol 1993;11:1757-62. (Pubitemid 23277329)
56. Albain KS, Rusch VW, Crowley JJ, Rice TW, Turrisi AT 3rd, Weick JK et al. Concurrent cisplatin/etoposide plus chest radiotherapy followed by surgery for stages IIIA (N2) and IIIB non-smallcell lung cancer: mature results of Southwest Oncology Group phase II study 8805. J Clin Oncol 1995;13:1880-92.
57. Bepler G, Sommers KE, Cantor A, Li X, Sharma A, Williams C et al. Clinical efficacy and predictive molecular markers of neoadjuvant gemcitabine and pemetrexed in resectable non-small cell lung cancer. J Thorac Oncol 2008;3:1112-8.
58. He L, Teng Y, Jin B, Zhao M, Yu P, Hu X et al. Initial partial response and stable disease according to RECIST indicate similar survival for chemotherapeutical patients with advanced non-small cell lung cancer. BMC Cancer 2010;14:681.
59. Sekine I, Kubota K, Nishiwaki Y, Sasaki Y, Tamura T, Saijo N. Response rate as an endpoint for evaluating new cytotoxic agents in phase II trials of non-smallcell lung cancer. Ann Oncol 1998;9:1079-84. (Pubitemid 28518145)
60. Yabuuchi H, Hatakenaka M, Takayama K, Matsuo Y, Sunami S, Kamitani T et al. Non-small cell lung cancer: detection of early response to chemotherapy by using contrast-enhanced dynamic and diffusion-weighted MR imaging. Radiology 2011;261:598-604.
61. Zander T, Scheffler M, Nogova L, Kobe C, Engel-Riedel W, Hellmich M et al. Early prediction of nonprogression in advanced non-small-cell lung cancer treated with erlotinib by using [18F] Fluorodeoxyglucose and [18F]Fluorothymidine positron emission tomography. J Clin Oncol 2011;29:1701-8.
62. Sauer R, Becker H, Hohenberger W, Rödel C, Wittekind C, Fietkau R et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med 2004;351:1731-40.
63. Glynne-Jones R, Mawdsley S, Pearce T, Buyse M. Alternative clinical end points in rectal cancer - are we getting closer? Ann Oncol 2006,17:1239-48. (Pubitemid 44288215)
64. Patel UB, Taylor F, Blomqvist L, George C, Evans H, Tekkis P et al. Magnetic resonance imaging - detected tumor response for locally advanced rectal cancer predicts survival outcomes: MERCURY experience. J Clin Oncol 2011;29:3753-60.
65. Kim YC, Lim JS, Keum KC, Kim KA, Myoung S, Shin SJ et al. Comparison of diffusion-weighted mri and mr volumetry in the evaluation of early treatment outcomes after preoperative chemoradiotherapy for locally advanced rectal cancer. J Magn Reson Imaging 2011 [Epub ahead of print].
66. Sun YS, Zhang XP, Tang L, Ji JF, Gu J, Cai Y et al. Locally advanced rectal carcinoma treated with preoperative chemotherapy and radiation therapy: preliminary analysis of diffusion-weighted MR imaging for early detection of tumor histopathologic downstaging. Radiology 2010;254:170-8.
67. Lambrecht M, Vandecaveve V, De Keyzer F, Roels S, Penninckx F, Van Cutsem E et al. Value of diffusion-weighted magnetic resonance imaging for prediction and early assessment of response to neoadjuvant radiochemotherapy in rectal cancer: preliminary results. Int J Radiat Oncol Biol Phys 2011 [Epub ahead of print].
68. Macdonald D, Cascino T, Schold SJ, Cairncross J. Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 1990;8:1277-80. (Pubitemid 20195640)
69. Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 2010;28:1963-72.
70. Wen PY, Norden AD, Drappatz J, Quant E. Response assessment challenges in clinical trials of gliomas. Current Oncol Rep 2010;12:68-75.
71. Quant EC, Wen PY. Response assessment in neuro-oncology. Curr Oncol Rep 2011;13:50-6.
72. Van den Bent MJ, Vogelbaum MA, When PY, Macdonald DR, Chang SM. End point assessment in gliomas: novel treatments limit usefulness of classical Macdonald's Criteria. J Clin Oncol 2009;27:2905-8.
73. Brandes AA, Franceschi E, Tosoni, A Blatt V, Pession A, Tallini G et al. MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J Clin Oncol 2008;26:2192-7.
74. Brandes AA, Tosoni A, Spagnolli F, Frezza G, Leonardi M, Calbucci F et al. Disease progression or pseudoprogression after concomitant radiochemotherapy treatment: pitfalls in neurooncology. Neuro Oncol 2008;10:361-7.
75. Brandsma D, Stalpers L, Taal W, Sminia P, van den Bent MJ. Clinical features, mechanisms, and management of pseudoprogression in malignant gliomas. Lancet Oncol 2008;9:453-61. (Pubitemid 351597795)
76. Gerstner ER, McNamara MB, Norden AD, Lafrankie D, Wen PY. Effect of adding temozolomide to radiation therapy on the incidence of pseudoprogression. J Neurooncol 2009;94:97-101.
77. Vredenburgh JJ, Desjardins A, Herndon JE 2nd, Marcello J, Reardon DA, Quinn JA et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol 2007;25:4722-9. (Pubitemid 350086473)
78. Friedman HS, Prados MD, Wen PY, Mikkelsen T, Schiff D, Abrey LE et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol 2009;27:4733-40.
79. Kreisl TN, Kim L, Moore K, Duic P, Royce C, Stroud I et al. Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol 2009;27:740-5.
80. Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001;35:421-30. (Pubitemid 32844200)