RECIST revised: implications for the radiologist. A review article on the modified RECIST guideline

World Health Organization (1979) WHO Handbook for reporting results of cancer treatment. WHO Publication No. 48, Geneva Miller AB, Hoogstraten B, Staquet M, Winkler A (1981) Reporting results of cancer treatment. Cancer 47:207–214 Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, Van Oosterom AT, Christian MC, Gwyther SG (2000) New guidelines to evaluate the response to treatment in solid tumors. J Natl Cancer Inst 92:205–216 Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M, Rubinstein L, Shankar L, Dodd L, Kaplan R, Lacombe D, Verweij J (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45:228–247. doi:10.1016/j.ejca.2008.10.026 Cheson BD, Pfistner B, Juweid ME, Gascoyne RD, Specht L, Horning SJ, Coiffier B, Fisher RI, Hagenbeek A, Zucca E, Rosen ST, Stroobants S, Lister TA, Hoppe RT, Dreyling M, Tobinai K, Vose JM, Connors JM, Federico M, Diehl V (2007) Revised response criteria for malignant lymphoma. J Clin Oncol 25:579–586. doi:10.1200/JCO.2006.09.2403 Bogaerts J, Ford R, Sargent D, Schwartz LH, Rubinstein L, Lacombe D, Eisenhauer E, Verweij J, Therasse P (2009) Individual patient data analysis to assess modifications of the RECIST criteria. Eur J Cancer 45:248–260. doi:10.1016/j.ejca.2008.10.027 Moskowitz CS, Jia X, Schwartz LH, Gönen M (2009) A simulation study to evaluate the impact of the number of lesions measured on response assessment. Eur J Cancer 45:300–310. doi:10.1016/j.ejca.2008.11.010 Schwartz LH, Mazumdar M, Brown W, Smith A, Panicek DM (2003) Variability in response assessment in solid tumors: effect of number of lesions chosen for measurement. Clin Cancer Res 9:4318–4323 Watanabe H, Kunitoh H, Yamamoto S, Kawasaki S, Inoue A, Hotta K, Shiomi K, Kusumoto M, Sugimura K, Saijo N (2006) Effect of the introduction of minimum lesion size on interobserver reproducibility using RECIST guidelines in non-small cell lung cancer patients. Cancer Sci 97:214–218 van Klaveren RJ, Aerts JGJV, de Bruin H, Giaccone G, Manegold C, van Meerbeeck JP (2004) Inadequacy of the RECIST criteria for response evaluation in patients with malignant pleural mesothelioma. Lung Cancer 43:63–69. doi:10.1016/S0169-5002(3)00292-7 Byrne MJ, Nowak AK (2004) Modified RECIST criteria for assessment of response in malignant pleural mesothelioma. Ann Oncol 15:257–260. doi:10.1093/annonc/mdh059 Plathow Ch, Klopp M, Thieke Ch, Herth F, Thomas A, Schmaehl A, Zuna I, Kauczor H-U (2008) Therapy response in malignant pleural mesothelioma - role of MRI using RECIST, modified RECIST and volumetric approaches in comparison with CT. Eur Radiol 18:1635–1643. doi:10.1007/s00330-008-0918-9 James K, Eisenhauer E, Christian M, Terenziani M, Vena D, Muldal A, Therasse P (1999) Measuring response in solid tumors: unidimensional versus bidimensional measurement. J Natl Cancer Inst 91:523–528 Trillet-Lenoir V, Freyer G, Kaemmerlen P, Fond A, Pellet O, Lombard-Bohas C, Gaudin JL, Lledo G, Mackiewicz R, Gouttebel MC, Moindrot H, Boyer JD, Chassignol L, Stremsdoerfer N, Desseigne F, Moreau JM, Hedelius F, Moraillon A, Chapuis F, Bleuse JP, Barbier Y, Heilmann MO, Valette PJ (2002) Assessment of tumour response to chemotherapy for metastatic colorectal cancer: accuracy of the RECIST criteria. Br J Radiol 75:903–908 Cortes J, Rodriguez J, Diaz-Gonzalez JA, Garzon C, Gurpide A, Arbea L, Gil-Bazo I, Navarro V, Cambeiro M, Nicolas AI, Martin-Algarra S, Garcia-Foncillas J, Calvo E (2002) Comparison of unidimensional and bidimensional measurements in metastatic non-small cell lung cancer. Br J Cancer 87:158–160. doi:10.1038/sj.bjc.6600449 Prasad SR, Saini S, Sumner JE, Hahn PF, Sahani D, Boland GW (2003) Radiological measurement of breast cancer metastases to lung and liver: comparison between WHO (bidimensional) and RECIST (unidimensional) guidelines. J Comp Ass Tom 27:380–384 Mazumdar M, Smith A, Schwartz LH (2004) A statistical simulation study finds discordance between WHO criteria and RECIST guideline. J Clin Epid 57:358–365. doi:10.1016/j.jclinepi.2003.07.015 Schwartz LH, Colville JAC, Ginsberg MS, Wang L, Mazumdar M, Kalaigian J, Hricak H, Ilson D, Schwartz GK (2006) Measuring tumor response and shape change on CT: esophageal cancer as a paradigm. Ann Oncol 17:1018–1023. doi:10.1093/annonc/mdl058 Belton AL, Saini S, Liebermann K, Boland GW, Halpern EF (2003) Tumour size measurement in an oncology clinical trial: comparison between off-site and on-site measurements. Clin Radiol 58:311–314. doi:10.1016/S0009-9260(02)00577-9 Hopper KD, Kasales CJ, Van Slyke MA, Schwartz TA, TenHave TR, Jozefiak JA (1996) Analysis of interobserver and intraobserver variability in CT tumor measurements. AJR Am J Roentgenol 167:851–854 Erasmus JJ, Gladish GW, Broemeling L, Sabloff BS, Truong MT, Herbst RS, Munden RF (2003) Interobserver and intraobserver variability in measurement of non-small-cell carcinoma lung lesions: implications for assessment of tumor response. J Clin Oncol 21:2574–2582. doi:10.1200/JCO.2003.01.144 Wormanns D, Kohl G, Klotz E, Marheine A, Beyer F, Heindel W, Diederich S (2004) Volumetric measurements of pulmonary nodules at multi-row detector CT: in vivo reproducibility. Eur Radiol 14:86–92. doi:10.1007/s00330-003-2132-0 Gietema HA, Schaefer-Prokop CM, Mali WPTM, Groenewegen G, Prokop M (2007) Pulmonary nodules: interscan variability of semiautomated volume measurements with multisection CT—influence of inspiration level, nodule size, and segmentation performance. Radiology 245:888–894 Marten K, Auer F, Schmidt S, Kohl G, Rummey EJ, Engelke C (2006) Inadequacy of manual measurements compared to automated CT volumetry in assessment of treatment response of pulmonary metastases using RECIST criteria. Eur Radiol 16:781–790. doi:10.1007/s00330-005-0036-x Keil S, Behrendt FF, Stanzel S, Sühling M, Koch A, Bubenzer J, Mühlenbruch G, Mahnken AH, Günther RW, Das M (2008) Semi-automated measurement of hyperdense, hypodense and heterogeneous hepatic metastasis on standard MDCT slices. Comparison of semi-automated and manual measurement of RECIST and WHO criteria. Eur Radiol 18:2456–2465. doi:10.1007/s00330-008-1050-6 Fabel M, von Tengg-Kobligk H, Giesel FL, Bornemann L, Dicken V, Kopp-Schneider A, Moser C, Delorme S, Kauczor H-U (2008) Semi-automated volumetric analysis of lymph nod metastases in patients with malignant melanoma stage III/IV—a feasibility study. Eur Radiol 18:1114–1122. doi:10.1007/s00330-008-0866-4 Ertl-Wagner BB, Blume JD, Peck D, Udupa JK, Herman B, Levering A, Schmalfuss IM (2009) Reliability of tumor volume estimation from MR images in patients with malignant glioma. Results from the American College of Radiology Imaging Network (ACRIN) 6662 trial. Eur Radiol 19:599–609. doi:10.1007/s00330-008-1191-7 Sargent DJ, Rubinstein L, Schwartz L, Dancey JE, Gatsonis G, Dodd LE, Shankar LK (2009) Validation of novel imaging methodologies for use as cancer clinical trial end-points. Eur J Cancer 45:290–299. doi:10.1016/j.ejca.2008.10.030 McHugh K, Kao S (2003) Response evaluation criteria in solid tumours (RECIST): problems and need for modifications in paediatric oncology? Br J Radiol 76:433–436. doi:10.1259/bjr/15521966 Therasse P, Eisenhauer EA, Verweij J (2006) RECIST revisited: a review of validation studies on tumour assessment. Eur J Cancer 42:1031–1039. doi:10.1016/j.ejca.2006.01.026 Husband JE, Schwartz LH, Spencer J, Ollivier L, King DM, Johnson R, Reznik R (2004) Evaluation of the response to treatment of solid tumours—a consensus statement of the International Cancer Imaging Society. Br J Cancer 90:2256–2260 Glazer GM, Gross BH, Quint LE, Francis IR, Bookstein FL, Orringer MB (1985) Normal mediastinal lymph nodes: number and size according to American Thoracic Society Mapping. AJR Am J Roentgenol 144:261–265 Matsuoka H, Masaki T, Sugiyama M, Atomi Y, Ohkura Y, Sakamoto A (2007) Morphological characteristics of lateral pelvic lymph nodes in rectal carcinoma. Langenbecks Arch Surg 392:543–547. doi:10.1007/s00423-007-0181-6 Schwartz LH, Bogaerts J, Ford R, Shankar L, Therasse P, Gwyther S, Eisenhauer EA (2009) Evaluation of lymph nodes with RECIST 1.1. Eur J Cancer 45:261–267. doi:10.1016/j.ejca.2008.10.028 Dorfman RE, Alpern MB, Gross BH, Sandler MA (1991) Upper abdominal lymph nodes: criteria for normal size determined with CT. Radiology 180:310–322 McLoud TC, Bourgouin PM, Greenberg RW, Kosiuk JP, Templeton PA, Shepard JAO, Moore EH, Wain JC, Mathisen DJ, Grillo HC (1992) Bronchogenic carcinoma: analysis of staging in the mediastinum with CT by correlative lymph node mapping and sampling. Radiology 182:319–323 Tombal B, Rezazadeh A, Therasse P, Van Cangh PJ, Vandeberg B, Lecouvet FE (2005) Magnetic resonance imaging of the axial skeleton enables objective measurement of tumor response on prostate cancer bone metastases. Prostate 65:178–187. doi:10.1002/pros.20280 Ratain MJ, Eisen T, Stadler WM, Flaherty KT, Kaye SB, Rosner GL, Gore M, Desai AA, Patnaik A, Xiong HQ, Rowinksy E, Abbruzzese JL, Xia C, Simantov R, Schwartz B, O’Dwyer PJ (2006) Phase II placebo-controlled randomized discontinuation trial of Sorafenib in patients with metastatic renal cell carcinoma. J Clin Oncol 24:2505–2512. doi:10.1200/JCO.2005.03.6723 Pennell NA, Daniels GH, Haddad RI, Ross DS, Evans T, Wirth LJ, Fidias PH, Temel JS, Gurubhagavatula S, Suk Heist R, Clark JR Lynch TJ (2008) A phase II study of Gefitinib in patients with advanced thyroid cancer. Thyroid 18:317–323. doi:10.1089/thy.2007.0120 Shephard FA, Rodrigues Pereira J, Ciuleanu T, Huat Tan E, Hirsch V, Thongprasert S, Campos D, Maoleekoonpiroj S, Smylie M, Martins R, van Kooten M, Dediu M, Findlay B, Tu D, Johnston D, Bezjak A, Clark G, Santabárbara P, Seymour L, for the National Cancer Institute of Canada Clinical Trials Group (2005) Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med 353:123–132 Hudes G, Carducci M, Tomczak P, Dutcher J, Figlin R, Kapoor A, Staroslawska E, Sosman J, McDermott D, Bodrogi I, Kovacevic Z, Lesovoy V, Schmidt-Wolf IGH, Barbarash O, Gokmen E, O’Toole T, Lustgarten S, Moore L, Motzer RJ, for the Global ARCC Trial (2007) Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma. N Engl J Med 356:2271–2281 Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, Berlin J, Baron A, Griffing S, Holmgren E, Ferrara N, Fyfe G, Rogers B, Ross R, Kabbinavar F (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 350:2335–2342 Llovet JM, Di Bisceglie AM, Bruix J, Kramer BS, Lencioni R, Zhu AZ, Sherman M, Schwartz M, Lotze M, Talwalkar J, Gores GJ (2008) Design and endpoints of clinical trials in hepatocellular carcinoma. J Natl Cancer Inst 100:698–711. doi:10.1093/jnci/djn134 Choi H, Charnsangavej C, Faria SC, Macapinlac HA, Burgess MA, Patel SR, Chen LL, Podoloff DA, Benjamin RS (2007) 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 25:1753–1759. doi:10.1200/JCO.2006.07.3049 Benjamin RS, Choi H, Macapinlac HA, Burgess MA, Patel SR, Chen LL, Podoloff DA Charnsangavej C (2007) We should desist using RECIST, at least in GIST. J Clin Oncol 25:1760–1764. doi:10.1200/JCO.2006.07.3411 Kawamoto S, Permpongkosol S, Bluemke DA, Fishman EK, Solomon SB (2007) Sequential changes after radiofrequency ablation and cryoablation of renal neoplasms: role of CT and MR imaging. Radiographics 27:343–355. doi:10.1148/rg.272065119 Kim Y-S, Rhim H, Lim HK (2009) Imaging after radiofrequency ablation of hepatic tumors. Semin Ultrasound CT MRI 30:49–66. doi:10.1053/j.sult.2008.12.004 Weber WA (2009) Assessing tumor response to therapy. J Nucl Med 50:1S–10S. doi:10.2967/jnumed.108.057174 Hutchings M, Barrington SF (2009) PET/CT for therapy response assessment in lymphoma. J Nucl Med 50:21S–30S. doi:10.2967/jnumed.108.057190 Hicks RJ (2009) Role of F-FDG PET in assessment of response in non-small cell lung cancer. J Nucl Med 50:31S–42S. doi:10.2967/jnumed.108.057216 de Geus-Oei L-F, Vriens D, van Laarhoven HWM, van der Graaf WTA, Oyen WJG (2009) Monitoring and predicting response to therapy with 18F-FDG PET in colorectal cancer: a systematic review. J Nucl Med 50:43S–54S. doi:10.2967/jnumed.108.057224 Avril N, Sassen S, Roylance R (2009) Response to therapy in breast cancer. J Nucl Med 50:55S–63S. doi:10.2967/JNUMED.108.057240 Boellaard R (2009) Standards for PET image acquisition and quantitative data analysis. J Nucl Med 50:11S–20S. doi:10.2967/jnumed.108.057182 Wahl RL, Jacene H, Kasamon Y, Lodge MA (2009) From RECIST to PERCIST: evolving considerations for PET response criteria in solid tumors. J Nucl Med 50:122S–150S. doi:10.2967/jnumed.108.057307 Galbraith SM, Rustin GJS, Lodge MA, Taylor J, Stirling JJ, Jameson M, Thompson P, Hough D, Gumbrell L, Padhani AR (2002) Effects of 5,6-dimethylxanthenone-4-acetic acid on human tumor microcirculation assessed by dynamic contrast-enhanced magnetic resonance imaging. J Clin Oncol 20:3826–3840. doi:10.1200/JCO.2002.09.144 van Rijswijk CSP, Geirnaerdt MJA, Hogendoorn PCW, Peterse JL, van Coevorden F, Taminiau AHM, Tollenaar RAEM, Kroon BBR, Bloem JL (2003) Dynamic contrast-enhanced MR imaging in monitoring response to isolated limb perfusion in high-grade soft tissue sarcoma: initial results. Eur Radiol 13:1849–1858. doi:10.1007/s00330-002-1785-4 O’Connor JPB, Jackson A, Parker GJM, Jayson GC (2007) DCE-MRI biomarkers in the clinical evaluation of antiangiogenic and vascular disrupting agents. Br J Cancer 96:189–195. doi:10.1038/sj.bjc.6603515 Yankeelov TE, Lepage M, Chakravarthy A, Broome EE, Niermann KJ, Kelley MC, Meszoely I, Mayer IA, Herman CR, McManns K, Price RR, Gore JC (2007) Integration of quantitative DCE-MRI and ADC mapping to monitor treatment response in human breast cancer: initial results. Magn Res Imag 25:1–13. doi:10.1016/j.mri.2006.09.006 Padhani AR, Liu G, Mu-Koh D, Chenevert TL, Thoeny HC, Takahara T, Dzik-Jurasz A, Ross BD, Van Cauteren M, Collins D, Hammond DA, Rustin GJS, Taouli B, Choyke PL (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:102–125. doi:10.1593/neo.81328 Kan Z, Phongkitkarun S, Kobayashi S, Tang Y, Ellis LM, Lee TY, Charnsangavej C (2005) Functional CT for quantifying tumor perfusion in antiangiogenic therapy in a rat model. Radiology 237:151–158. doi:10.1148/radiol.2363041293 Meijerink MR, van Cruijsen H, Hoekman K, Kater M, van Schaik C, van Waesberghe JHTM, Giaccone G, Manuliu RA (2007) The use of perfusion CT for the evaluation of therapy combining AZD2171 with gefitinib in cancer patients. Eur Radiol 17:1700–1713. doi:10.1007/s00330-006-0425-9 Kambadakone AR, Sahani DV (2009) Body perfusion CT: technique, clinical applications and advances. Radiol Clin N Am 47:161–178. doi:10.1016/j.rcl.2008.11.003