Objective response rate assessment in oncology: Current situation and future expectations

Nuri Faruk Aykan, Tahsin Özatlı, Nuri Faruk Aykan, Tahsin Özatlı

Abstract

The tumor objective response rate (ORR) is an important parameter to demonstrate the efficacy of a treatment in oncology. The ORR is valuable for clinical decision making in routine practice and a significant end-point for reporting the results of clinical trials. World Health Organization and Response Evaluation Criteria in Solid Tumors (RECIST) are anatomic response criteria developed mainly for cytotoxic chemotherapy. These criteria are based on the visual assessment of tumor size in morphological images provided by computed tomography (CT) or magnetic resonance imaging. Anatomic response criteria may not be optimal for biologic agents, some disease sites, and some regional therapies. Consequently, modifications of RECIST, Choi criteria and Morphologic response criteria were developed based on the concept of the evaluation of viable tumors. Despite its limitations, RECIST v1.1 is validated in prospective studies, is widely accepted by regulatory agencies and has recently shown good performance for targeted cancer agents. Finally, some alternatives of RECIST were developed as immune-specific response criteria for checkpoint inhibitors. Immune RECIST criteria are based essentially on defining true progressive disease after a confirmatory imaging. Some graphical methods may be useful to show longitudinal change in the tumor burden over time. Tumor tissue is a tridimensional heterogenous mass, and tumor shrinkage is not always symmetrical; thus, metabolic response assessments using positron emission tomography (PET) or PET/CT may reflect the viability of cancer cells or functional changes evolving after anticancer treatments. The metabolic response can show the benefit of a treatment earlier than anatomic shrinkage, possibly preventing delays in drug approval. Computer-assisted automated volumetric assessments, quantitative multimodality imaging in radiology, new tracers in nuclear medicine and finally artificial intelligence have great potential in future evaluations.

Keywords: Depth of response; Early tumor shrinkage; Immune Response Evaluation Criteria in Solid Tumors criteria; Objective response rate; Response Evaluation Criteria in Solid Tumors; Spider plot; Swimmer plot; Tumor shrinkage; Waterfall plot; World Health Organization criteria.

Conflict of interest statement

Conflict-of-interest statement: The authors have no conflicts of interest to declare.

©The Author(s) 2019. Published by Baishideng Publishing Group Inc. All rights reserved.

Figures

Figure 1
Figure 1
Different cut-off levels of E of early tumor shrinkage at first tumor response assessment (6 or 8 wk). A: ≥ -10% (5 cases); B: ≥ -20% (4 cases); C: ≥ -30% (3 cases). CR: Complete response; PR: Partial response; SD: Stable disease.
Figure 2
Figure 2
Two hypothetical examples of tumor shrinkage. Example 1: Spheroid mass, symmetric (proportional) shrinkage; Example 2: Irregular mass, asymmetric shrinkage. t0: Time point baseline; t1: Time point-1; t2: Time point-2; A, B, C: Spheroid mass; X, Y, Z: Irregular mass.
Figure 3
Figure 3
Pseudoprogression. t0: Time point baseline; t1: Time point-1; t2: Time point-2; NK: Natural killer.
Figure 4
Figure 4
Waterfall, spider (spaghetti) and swimmer plot for 12 hypothetical cases. A: Waterfall; B: Spider (spaghetti); C: Swimmer. Case 8 (blue arrow with cycle) represents pseudoprogression at the 4th week. RR: Response rate; CR: Complete response; PR: Partial response; SD: Stable disease; PD: Progressive disease.

References

    1. Karnofsky DA. Meaningful clinical classification of therapeutic responses to anticancer drugs. Clin Pharmacol Ther. 1961;2:709–712.
    1. Moertel CG, Hanley JA. The effect of measuring error on the results of therapeutic trials in advanced cancer. Cancer. 1976;38:388–394.
    1. Levin VA, Crafts DC, Norman DM, Hoffer PB, Spire JP, Wilson CB. Criteria for evaluating patients undergoing chemotherapy for malignant brain tumors. J Neurosurg. 1977;47:329–335.
    1. Macdonald DR, Cascino TL, Schold SC, Jr, Cairncross JG. Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol. 1990;8:1277–1280.
    1. World Health Organization. WHO Handbook for Reporting Results of Cancer Treatment. World Health Organization Offset Publication No. 48; Geneva (Switzerland), 1979.
    1. Miller AB, Hoogstraten B, Staquet M, Winkler A. Reporting results of cancer treatment. Cancer. 1981;47:207–214.
    1. Thiesse P, Ollivier L, Di Stefano-Louineau D, Négrier S, Savary J, Pignard K, Lasset C, Escudier B. Response rate accuracy in oncology trials: reasons for interobserver variability. Groupe Français d'Immunothérapie of the Fédération Nationale des Centres de Lutte Contre le Cancer. J Clin Oncol. 1997;15:3507–3514.
    1. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC, Gwyther SG. 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;92:205–216.
    1. Burzykowski T, Buyse M, Piccart-Gebhart MJ, Sledge G, Carmichael J, Lück HJ, Mackey JR, Nabholtz JM, Paridaens R, Biganzoli L, Jassem J, Bontenbal M, Bonneterre J, Chan S, Basaran GA, Therasse P. Evaluation of tumor response, disease control, progression-free survival, and time to progression as potential surrogate end points in metastatic breast cancer. J Clin Oncol. 2008;26:1987–1992.
    1. Borcoman E, Nandikolla A, Long G, Goel S, Le Tourneau C. Patterns of Response and Progression to Immunotherapy. Am Soc Clin Oncol Educ Book. 2018;38:169–178.
    1. 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. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1) Eur J Cancer. 2009;45:228–247.
    1. Choi JH, Ahn MJ, Rhim HC, Kim JW, Lee GH, Lee YY, Kim IS. Comparison of WHO and RECIST criteria for response in metastatic colorectal carcinoma. Cancer Res Treat. 2005;37:290–293.
    1. Zacharia TT, Saini S, Halpern EF, Sumner JE. CT of colon cancer metastases to the liver using modified RECIST criteria: determining the ideal number of target lesions to measure. AJR Am J Roentgenol. 2006;186:1067–1070.
    1. Kim HS, Kim JH, Yang I. Tumor response assessment by measuring the single largest lesion per organ in patients with advanced non-small cell lung cancer. Lung Cancer. 2014;85:385–389.
    1. Kim HS, Kim JW, Kim JH, Choi DR, Han AR, Kim MJ, Kim BC, Zang DY. Single-lesion measurement per organ for assessing tumor response in advanced gastric cancer. Oncology. 2015;88:69–75.
    1. Kim HS, Kim JH. Ideal number of target lesions per organ to measure in metastatic colorectal cancer. Oncol Lett. 2014;8:1896–1900.
    1. Jang HJ, Cho JW, Park B, Choi HC, Kim HS, Kim JH. The assessment of tumor response by measuring the single largest lesion per organ in metastatic tumors: a pooled analysis of previously reported data. J Cancer. 2015;6:169–176.
    1. Lencioni R, Llovet JM. Modified RECIST (mRECIST) assessment for hepatocellular carcinoma. Semin Liver Dis. 2010;30:52–60.
    1. European Association for the Study of the Liver. EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. J Hepatol. 2018;69:182–236.
    1. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, Schwartz M, Porta C, Zeuzem S, Bolondi L, Greten TF, Galle PR, Seitz JF, Borbath I, Häussinger D, Giannaris T, Shan M, Moscovici M, Voliotis D, Bruix J SHARP Investigators Study Group. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008;359:378–390.
    1. Forner A, Ayuso C, Varela M, Rimola J, Hessheimer AJ, de Lope CR, Reig M, Bianchi L, Llovet JM, Bruix J. Evaluation of tumor response after locoregional therapies in hepatocellular carcinoma: are response evaluation criteria in solid tumors reliable? Cancer. 2009;115:616–623.
    1. Kantarci M, Pirimoglu B. Radiological Response to the Locoregional Treatment in Hepatocellular Carcinoma: RECIST, mRECIST, and Others. J Gastrointest Cancer. 2017;48:282–285.
    1. Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK, Christensen E, Pagliaro L, Colombo M, Rodés J. EASL Panel of Experts on HCC. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol. 2001;35:421–430.
    1. Zhao Y, Duran R, Bai W, Sahu S, Wang W, Kabus S, Lin M, Han G, Geschwind JF. Which Criteria Applied in Multi-Phasic CT Can Predict Early Tumor Response in Patients with Hepatocellular Carcinoma Treated Using Conventional TACE: RECIST, mRECIST, EASL or qEASL? Cardiovasc Intervent Radiol. 2018;41:433–442.
    1. Lin M, Pellerin O, Bhagat N, Rao PP, Loffroy R, Ardon R, Mory B, Reyes DK, Geschwind JF. Quantitative and volumetric European Association for the Study of the Liver and Response Evaluation Criteria in Solid Tumors measurements: feasibility of a semiautomated software method to assess tumor response after transcatheter arterial chemoembolization. J Vasc Interv Radiol. 2012;23:1629–1637.
    1. Byrne MJ, Nowak AK. Modified RECIST criteria for assessment of response in malignant pleural mesothelioma. Ann Oncol. 2004;15:257–260.
    1. Labby ZE, Armato SG, 3rd, Kindler HL, Dignam JJ, Hasani A, Nowak AK. Optimization of response classification criteria for patients with malignant pleural mesothelioma. J Thorac Oncol. 2012;7:1728–1734.
    1. Choi H, Charnsangavej C, Faria SC, Macapinlac HA, Burgess MA, Patel SR, Chen LL, Podoloff DA, Benjamin RS. 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;25:1753–1759.
    1. Benjamin RS, Choi H, Macapinlac HA, Burgess MA, Patel SR, Chen LL, Podoloff DA, Charnsangavej C. We should desist using RECIST, at least in GIST. J Clin Oncol. 2007;25:1760–1764.
    1. Choi H. Response evaluation of gastrointestinal stromal tumors. Oncologist. 2008;13 Suppl 2:4–7.
    1. Saltz LB, Clarke S, Díaz-Rubio E, Scheithauer W, Figer A, Wong R, Koski S, Lichinitser M, Yang TS, Rivera F, Couture F, Sirzén F, Cassidy J. Bevacizumab in combination with oxaliplatin-based chemotherapy as first-line therapy in metastatic colorectal cancer: a randomized phase III study. J Clin Oncol. 2008;26:2013–2019.
    1. Vera R, Gomez Dorronsoro M, Lopez-Ben S, Viudez A, Queralt B, Hernandez I, Ortiz-Duran MR, Zazpe C, Soriano J, Amat I, Herrera Cabezón J, Diaz E, Codina-Barreras A, Hernandez-Yagüe X, Quera A, Figueras J. Retrospective analysis of pathological response in colorectal cancer liver metastases following treatment with bevacizumab. Clin Transl Oncol. 2014;16:739–745.
    1. Ribero D, Wang H, Donadon M, Zorzi D, Thomas MB, Eng C, Chang DZ, Curley SA, Abdalla EK, Ellis LM, Vauthey JN. Bevacizumab improves pathologic response and protects against hepatic injury in patients treated with oxaliplatin-based chemotherapy for colorectal liver metastases. Cancer. 2007;110:2761–2767.
    1. Blazer DG 3rd, Kishi Y, Maru DM, Kopetz S, Chun YS, Overman MJ, Fogelman D, Eng C, Chang DZ, Wang H, Zorzi D, Ribero D, Ellis LM, Glover KY, Wolff RA, Curley SA, Abdalla EK, Vauthey JN. Pathologic response to preoperative chemotherapy: a new outcome end point after resection of hepatic colorectal metastases. J Clin Oncol. 2008;26:5344–5351.
    1. Klinger M, Tamandl D, Eipeldauer S, Hacker S, Herberger B, Kaczirek K, Dorfmeister M, Gruenberger B, Gruenberger T. Bevacizumab improves pathological response of colorectal cancer liver metastases treated with XELOX/FOLFOX. Ann Surg Oncol. 2010;17:2059–2065.
    1. Stremitzer S, Stift J, Singh J, Starlinger P, Gruenberger B, Tamandl D, Gruenberger T. Histological response, pattern of tumor destruction and clinical outcome after neoadjuvant chemotherapy including bevacizumab or cetuximab in patients undergoing liver resection for colorectal liver metastases. Eur J Surg Oncol. 2015;41:868–874.
    1. Adam R, Wicherts DA, de Haas RJ, Aloia T, Lévi F, Paule B, Guettier C, Kunstlinger F, Delvart V, Azoulay D, Castaing D. Complete pathologic response after preoperative chemotherapy for colorectal liver metastases: myth or reality? J Clin Oncol. 2008;26:1635–1641.
    1. Rubbia-Brandt L, Giostra E, Brezault C, Roth AD, Andres A, Audard V, Sartoretti P, Dousset B, Majno PE, Soubrane O, Chaussade S, Mentha G, Terris B. Importance of histological tumor response assessment in predicting the outcome in patients with colorectal liver metastases treated with neo-adjuvant chemotherapy followed by liver surgery. Ann Oncol. 2007;18:299–304.
    1. Gruenberger T, Arnold D, Rubbia-Brandt L. Pathologic response to bevacizumab-containing chemotherapy in patients with colorectal liver metastases and its correlation with survival. Surg Oncol. 2012;21:309–315.
    1. Chun YS, Vauthey JN, Boonsirikamchai P, Maru DM, Kopetz S, Palavecino M, Curley SA, Abdalla EK, Kaur H, Charnsangavej C, Loyer EM. Association of computed tomography morphologic criteria with pathologic response and survival in patients treated with bevacizumab for colorectal liver metastases. JAMA. 2009;302:2338–2344.
    1. Shindoh J, Loyer EM, Kopetz S, Boonsirikamchai P, Maru DM, Chun YS, Zimmitti G, Curley SA, Charnsangavej C, Aloia TA, Vauthey JN. Optimal morphologic response to preoperative chemotherapy: an alternate outcome end point before resection of hepatic colorectal metastases. J Clin Oncol. 2012;30:4566–4572.
    1. Nishioka Y, Shindoh J, Yoshioka R, Gonoi W, Abe H, Okura N, Yoshida S, Oba M, Hashimoto M, Watanabe G, Hasegawa K, Kokudo N. Radiological Morphology of Colorectal Liver Metastases after Preoperative Chemotherapy Predicts Tumor Viability and Postoperative Outcomes. J Gastrointest Surg. 2015;19:1653–1661.
    1. Pan W, Huang S, Zhang J, Zhao B, Wang H, Liu F, Jin K, Mou X. Heterogeneity-related anticancer therapy response differences in metastatic colon carcinoma: new hints to tumor-site-based personalized cancer therapy. Hepatogastroenterology. 2013;60:1927–1934.
    1. Smith NR, Wedge SR, Pommier A, Barry ST. Mechanisms that influence tumour response to VEGF-pathway inhibitors. Biochem Soc Trans. 2014;42:1601–1607.
    1. Heinemann V, von Weikersthal LF, Decker T, Kiani A, Vehling-Kaiser U, Al-Batran SE, Heintges T, Lerchenmüller C, Kahl C, Seipelt G, Kullmann F, Stauch M, Scheithauer W, Hielscher J, Scholz M, Müller S, Link H, Niederle N, Rost A, Höffkes HG, Moehler M, Lindig RU, Modest DP, Rossius L, Kirchner T, Jung A, Stintzing S. FOLFIRI plus cetuximab versus FOLFIRI plus bevacizumab as first-line treatment for patients with metastatic colorectal cancer (FIRE-3): a randomised, open-label, phase 3 trial. Lancet Oncol. 2014;15:1065–1075.
    1. Sclafani F, Cunningham D. Cetuximab or bevacizumab in metastatic colorectal cancer? Lancet Oncol. 2014;15:1040–1041.
    1. Pietrantonio F, Iacovelli R, Di Bartolomeo M, de Braud F. FOLFIRI with cetuximab or bevacizumab: FIRE-3. Lancet Oncol. 2014;15:e581.
    1. Stintzing S, Modest DP, Fischer von Weikersthal L, Decker T, Kiani A, Vehling-Kaiser U, Al-Batran S, Heintges T, Lerchenmueller C, Kahl C, Seipelt G, Kullmann F, Scheithauer W, Held S, Giessen C, Moehler M, Jagenburg A, Jung A, Kirchner T, Heinemann V. Independent radiological evaluation of objective response, early tumor shrinkage, and depth of response in FIRE-3 (AIO KRK-0306) in the final RAS evaluable population. Ann Oncol. 2014;25:1–41.
    1. Heinemann V, Stintzing S. FOLFIRI with cetuximab or bevacizumab: FIRE-3-authors' reply. Lancet Oncol. 2014;15:e583–e584.
    1. Heinemann V, Stintzing S, Modest DP, Giessen-Jung C, Michl M, Mansmann UR. Early tumour shrinkage (ETS) and depth of response (DpR) in the treatment of patients with metastatic colorectal cancer (mCRC) Eur J Cancer. 2015;51:1927–1936.
    1. Modest DP, Laubender RP, Stintzing S, Giessen C, Schulz C, Haas M, Mansmann U, Heinemann V. Early tumor shrinkage in patients with metastatic colorectal cancer receiving first-line treatment with cetuximab combined with either CAPIRI or CAPOX: an analysis of the German AIO KRK 0104 trial. Acta Oncol. 2013;52:956–962.
    1. Piessevaux H, Buyse M, Schlichting M, Van Cutsem E, Bokemeyer C, Heeger S, Tejpar S. Use of early tumor shrinkage to predict long-term outcome in metastatic colorectal cancer treated with cetuximab. J Clin Oncol. 2013;31:3764–3775.
    1. Piessevaux H, Buyse M, De Roock W, Prenen H, Schlichting M, Van Cutsem E, Tejpar S. 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;20:1375–1382.
    1. Petrelli F, Pietrantonio F, Cremolini C, Di Bartolomeo M, Coinu A, Lonati V, de Braud F, Barni S. Early tumour shrinkage as a prognostic factor and surrogate end-point in colorectal cancer: a systematic review and pooled-analysis. Eur J Cancer. 2015;51:800–807.
    1. Karoui M, Penna C, Amin-Hashem M, Mitry E, Benoist S, Franc B, Rougier P, Nordlinger B. Influence of preoperative chemotherapy on the risk of major hepatectomy for colorectal liver metastases. Ann Surg. 2006;243:1–7.
    1. Douillard JY, Siena S, Peeters M, Koukakis R, Terwey JH, Tabernero J. Impact of early tumour shrinkage and resection on outcomes in patients with wild-type RAS metastatic colorectal cancer. Eur J Cancer. 2015;51:1231–1242.
    1. Douillard JY, Siena S, Cassidy J, Tabernero J, Burkes R, Barugel M, Humblet Y, Bodoky G, Cunningham D, Jassem J, Rivera F, Kocákova I, Ruff P, Błasińska-Morawiec M, Šmakal M, Canon JL, Rother M, Oliner KS, Wolf M, Gansert J. Randomized, phase III trial of panitumumab with infusional fluorouracil, leucovorin, and oxaliplatin (FOLFOX4) versus FOLFOX4 alone as first-line treatment in patients with previously untreated metastatic colorectal cancer: the PRIME study. J Clin Oncol. 2010;28:4697–4705.
    1. Douillard JY, Oliner KS, Siena S, Tabernero J, Burkes R, Barugel M, Humblet Y, Bodoky G, Cunningham D, Jassem J, Rivera F, Kocákova I, Ruff P, Błasińska-Morawiec M, Šmakal M, Canon JL, Rother M, Williams R, Rong A, Wiezorek J, Sidhu R, Patterson SD. Panitumumab-FOLFOX4 treatment and RAS mutations in colorectal cancer. N Engl J Med. 2013;369:1023–1034.
    1. Douillard JY, Siena S, Cassidy J, Tabernero J, Burkes R, Barugel M, Humblet Y, Bodoky G, Cunningham D, Jassem J, Rivera F, Kocákova I, Ruff P, Błasińska-Morawiec M, Smakal M, Canon JL, Rother M, Oliner KS, Tian Y, Xu F, Sidhu R. Final results from PRIME: randomized phase III study of panitumumab with FOLFOX4 for first-line treatment of metastatic colorectal cancer. Ann Oncol. 2014;25:1346–1355.
    1. Masuishi T, Taniguchi H, Eto T, Komori A, Mitani S, Hasegawa H, Narita Y, Ishihara M, Tanaka T, Kadowaki S, Ura T, Ando M, Tajika M, Nomura M, Sato Y, Mishima H, Muro K. Morphologic Response and Tumor Shrinkage as Early Predictive Markers in Unresectable Colorectal Liver Metastases. Anticancer Res. 2018;38:6501–6506.
    1. Aykan NF, Onat H, Uskent N. The virtual comparison of size-based tumor shrinkage methods and the effect of tumor heterogeneity. Proceedings of the Conference: Cell Symposia Hallmarks of Cancer; 2016 Dec 12; Ghent, Belgium. Abstract: 0065; Available from: .
    1. Chiou VL, Burotto M. Pseudoprogression and Immune-Related Response in Solid Tumors. J Clin Oncol. 2015;33:3541–3543.
    1. Seymour L, Bogaerts J, Perrone A, Ford R, Schwartz LH, Mandrekar S, Lin NU, Litière S, Dancey J, Chen A, Hodi FS, Therasse P, Hoekstra OS, Shankar LK, Wolchok JD, Ballinger M, Caramella C, de Vries EGE RECIST working group. iRECIST: guidelines for response criteria for use in trials testing immunotherapeutics. Lancet Oncol. 2017;18:e143–e152.
    1. Wolchok JD, Hoos A, O'Day S, Weber JS, Hamid O, Lebbé C, Maio M, Binder M, Bohnsack O, Nichol G, Humphrey R, Hodi FS. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009;15:7412–7420.
    1. Nishino M, Giobbie-Hurder A, Gargano M, Suda M, Ramaiya NH, Hodi FS. Developing a common language for tumor response to immunotherapy: immune-related response criteria using unidimensional measurements. Clin Cancer Res. 2013;19:3936–3943.
    1. Hodi FS, Ballinger M, Lyons B, Soria JC, Nishino M, Tabernero J, Powles T, Smith D, Hoos A, McKenna C, Beyer U, Rhee I, Fine G, Winslow N, Chen DS, Wolchok JD. Immune-Modified Response Evaluation Criteria In Solid Tumors (imRECIST): Refining Guidelines to Assess the Clinical Benefit of Cancer Immunotherapy. J Clin Oncol. 2018;36:850–858.
    1. Shen Y, Anderson A, Sinha R, Li Y. Joint modeling tumor burden and time to event data in oncology trials. Pharm Stat. 2014;13:286–293.
    1. LoRusso PM, Anderson AB, Boerner SA, Averbuch SD. Making the investigational oncology pipeline more efficient and effective: are we headed in the right direction? Clin Cancer Res. 2010;16:5956–5962.
    1. Gillespie TW. Understanding waterfall plots. J Adv Pract Oncol. 2012;3:106–111.
    1. Tsimberidou AM, Levit LA, Schilsky RL, Averbuch SD, Chen D, Kirkwood JM, McShane LM, Sharon E, Mileham KF, Postow MA. Trial Reporting in Immuno-Oncology (TRIO): An American Society of Clinical Oncology-Society for Immunotherapy of Cancer Statement. J Clin Oncol. 2019;37:72–80.
    1. Johnston S, Puhalla S, Wheatley D, Ring A, Barry P, Holcombe C, Boileau JF, Provencher L, Robidoux A, Rimawi M, McIntosh SA, Shalaby I, Stein RC, Thirlwell M, Dolling D, Morden J, Snowdon C, Perry S, Cornman C, Batten LM, Jeffs LK, Dodson A, Martins V, Modi A, Osborne CK, Pogue-Geile KL, Cheang MCU, Wolmark N, Julian TB, Fisher K, MacKenzie M, Wilcox M, Huang Bartlett C, Koehler M, Dowsett M, Bliss JM, Jacobs SA. Randomized Phase II Study Evaluating Palbociclib in Addition to Letrozole as Neoadjuvant Therapy in Estrogen Receptor-Positive Early Breast Cancer: PALLET Trial. J Clin Oncol. 2019;37:178–189.
    1. Shao T, Wang L, Templeton AJ, Jang R, Vera-Badillo FW, McNamara MG, Margolis M, Kim TK, Sinaei M, Shoushtari H, Tannock IF. Use and misuse of waterfall plots. J Natl Cancer Inst. 2014;106
    1. Booth CM, Calvert AH, Giaccone G, Lobbezoo MW, Eisenhauer EA, Seymour LK. Design and conduct of phase II studies of targeted anticancer therapy: recommendations from the task force on methodology for the development of innovative cancer therapies (MDICT) Eur J Cancer. 2008;44:25–29.
    1. Stroobants S, Goeminne J, Seegers M, Dimitrijevic S, Dupont P, Nuyts J, Martens M, van den Borne B, Cole P, Sciot R, Dumez H, Silberman S, Mortelmans L, van Oosterom A. 18FDG-Positron emission tomography for the early prediction of response in advanced soft tissue sarcoma treated with imatinib mesylate (Glivec) Eur J Cancer. 2003;39:2012–2020.
    1. Warburg O, Posener K, Negelein E. The metabolism of cancer cells. Biochem Zeitschr. 1924;152:319–344.
    1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57–70.
    1. Vallabhajosula S. (18)F-labeled positron emission tomographic radiopharmaceuticals in oncology: an overview of radiochemistry and mechanisms of tumor localization. Semin Nucl Med. 2007;37:400–419.
    1. Wahl RL, Jacene H, Kasamon Y, Lodge MA. From RECIST to PERCIST: Evolving Considerations for PET response criteria in solid tumors. J Nucl Med. 2009;50 Suppl 1:122S–150S.
    1. Pietrantonio F, Orlandi A, Inno A, Da Prat V, Spada D, Iaculli A, Di Bartolomeo M, Morosi C, de Braud F. Bevacizumab-based neoadjuvant chemotherapy for colorectal cancer liver metastases: Pitfalls and helpful tricks in a review for clinicians. Crit Rev Oncol Hematol. 2015;95:272–281.
    1. O JH, Lodge MA, Wahl RL. Practical PERCIST: A Simplified Guide to PET Response Criteria in Solid Tumors 1.0. Radiology. 2016;280:576–584.
    1. Young H, Baum R, Cremerius U, Herholz K, Hoekstra O, Lammertsma AA, Pruim J, Price P. Measurement of clinical and subclinical tumour response using [18F]-fluorodeoxyglucose and positron emission tomography: review and 1999 EORTC recommendations. European Organization for Research and Treatment of Cancer (EORTC) PET Study Group. Eur J Cancer. 1999;35:1773–1782.
    1. Pinker K, Riedl C, Weber WA. Evaluating tumor response with FDG PET: updates on PERCIST, comparison with EORTC criteria and clues to future developments. Eur J Nucl Med Mol Imaging. 2017;44:55–66.
    1. Kim JH, Kim BJ, Jang HJ, Kim HS. Comparison of the RECIST and EORTC PET criteria in the tumor response assessment: a pooled analysis and review. Cancer Chemother Pharmacol. 2017;80:729–735.
    1. Goldfarb L, Duchemann B, Chouahnia K, Zelek L, Soussan M. Monitoring anti-PD-1-based immunotherapy in non-small cell lung cancer with FDG PET: introduction of iPERCIST. EJNMMI Res. 2019;9:8.
    1. Gallamini A, Fiore F, Sorasio R, Meignan M. Interim positron emission tomography scan in Hodgkin lymphoma: definitions, interpretation rules, and clinical validation. Leuk Lymphoma. 2009;50:1761–1764.
    1. Meignan M, Gallamini A, Meignan M, Gallamini A, Haioun C. Report on the First International Workshop on Interim-PET-Scan in Lymphoma. Leuk Lymphoma. 2009;50:1257–1260.
    1. Barrington SF, Mikhaeel NG, Kostakoglu L, Meignan M, Hutchings M, Müeller SP, Schwartz LH, Zucca E, Fisher RI, Trotman J, Hoekstra OS, Hicks RJ, O'Doherty MJ, Hustinx R, Biggi A, Cheson BD. Role of imaging in the staging and response assessment of lymphoma: consensus of the International Conference on Malignant Lymphomas Imaging Working Group. J Clin Oncol. 2014;32:3048–3058.
    1. Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, Zucca E, Lister TA Alliance, Australasian Leukaemia and Lymphoma Group; Eastern Cooperative Oncology Group; European Mantle Cell Lymphoma Consortium; Italian Lymphoma Foundation; European Organisation for Research; Treatment of Cancer/Dutch Hemato-Oncology Group; Grupo Español de Médula Ósea; German High-Grade Lymphoma Study Group; German Hodgkin's Study Group; Japanese Lymphorra Study Group; Lymphoma Study Association; NCIC Clinical Trials Group; Nordic Lymphoma Study Group; Southwest Oncology Group; United Kingdom National Cancer Research Institute. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014;32:3059–3068.
    1. James K, Eisenhauer E, Christian M, Terenziani M, Vena D, Muldal A, Therasse P. Measuring response in solid tumors: unidimensional versus bidimensional measurement. J Natl Cancer Inst. 1999;91:523–528.
    1. Hav M, Libbrecht L, Geboes K, Ferdinande L, Boterberg T, Ceelen W, Pattyn P, Cuvelier C. Prognostic value of tumor shrinkage versus fragmentation following radiochemotherapy and surgery for rectal cancer. Virchows Arch. 2015;466:517–523.
    1. King BL, Butler WM, Merrick GS, Kurko BS, Reed JL, Murray BC, Wallner KE. Electromagnetic transponders indicate prostate size increase followed by decrease during the course of external beam radiation therapy. Int J Radiat Oncol Biol Phys. 2011;79:1350–1357.
    1. Therasse P, Eisenhauer EA, Verweij J. RECIST revisited: a review of validation studies on tumour assessment. Eur J Cancer. 2006;42:1031–1039.
    1. Liu Y, Litière S, de Vries EG, Sargent D, Shankar L, Bogaerts J, Seymour L. The role of response evaluation criteria in solid tumour in anticancer treatment evaluation: results of a survey in the oncology community. Eur J Cancer. 2014;50:260–266.
    1. Litière S, Isaac G, De Vries EGE, Bogaerts J, Chen A, Dancey J, Ford R, Gwyther S, Hoekstra O, Huang E, Lin N, Liu Y, Mandrekar S, Schwartz LH, Shankar L, Therasse P, Seymour L RECIST Working Group. RECIST 1.1 for Response Evaluation Apply Not Only to Chemotherapy-Treated Patients But Also to Targeted Cancer Agents: A Pooled Database Analysis. J Clin Oncol. 2019;37:1102–1110.
    1. Inno A, Lo Russo G, Salgarello M, Corrao G, Casolino R, Galli G, Modena A, Romano L, Pusceddu S, Greco FG, Garassino MC, Gori S. The evolving landscape of criteria for evaluating tumor response in the era of cancer immunotherapy: From Karnofsky to iRECIST. Tumori. 2018;104:88–95.
    1. Queirolo P, Spagnolo F. Atypical responses in patients with advanced melanoma, lung cancer, renal-cell carcinoma and other solid tumors treated with anti-PD-1 drugs: A systematic review. Cancer Treat Rev. 2017;59:71–78.
    1. Rowe SP, Tran PT, Fishman EK, Johnson PT. Oligoprogression: What Radiologists Need to Know About This Emerging Concept in Cancer Therapeutic Decision-making. Acad Radiol. 2017;24:898–900.
    1. Cheung P. Stereotactic body radiotherapy for oligoprogressive cancer. Br J Radiol. 2016;89:20160251.
    1. Blumenthal GM, Pazdur R. Response Rate as an Approval End Point in Oncology: Back to the Future. JAMA Oncol. 2016;2:780–781.
    1. Oxnard GR, Wilcox KH, Gonen M, Polotsky M, Hirsch BR, Schwartz LH. Response Rate as a Regulatory End Point in Single-Arm Studies of Advanced Solid Tumors. JAMA Oncol. 2016;2:772–779.
    1. Hamaoka T, Costelloe CM, Madewell JE, Liu P, Berry DA, Islam R, Theriault RL, Hortobagyi GN, Ueno NT. Tumour response interpretation with new tumour response criteria vs the World Health Organisation criteria in patients with bone-only metastatic breast cancer. Br J Cancer. 2010;102:651–657.
    1. Wen PY, Chang SM, Van den Bent MJ, Vogelbaum MA, Macdonald DR, Lee EQ. Response Assessment in Neuro-Oncology Clinical Trials. J Clin Oncol. 2017;35:2439–2449.
    1. Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, Degroot J, Wick W, Gilbert MR, Lassman AB, Tsien C, Mikkelsen T, Wong ET, Chamberlain MC, Stupp R, Lamborn KR, Vogelbaum MA, van den Bent MJ, Chang SM. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol. 2010;28:1963–1972.
    1. Hopper KD, Kasales CJ, Eggli KD, TenHave TR, Belman NM, Potok PS, Van Slyke MA, Olt GJ, Close P, Lipton A, Harvey HA, Hartzel JS. The impact of 2D versus 3D quantitation of tumor bulk determination on current methods of assessing response to treatment. J Comput Assist Tomogr. 1996;20:930–937.
    1. Van Hoe L, Van Cutsem E, Vergote I, Baert AL, Bellon E, Dupont P, Marchal G. Size quantification of liver metastases in patients undergoing cancer treatment: reproducibility of one-, two-, and three-dimensional measurements determined with spiral CT. Radiology. 1997;202:671–675.
    1. Sohaib SA, Turner B, Hanson JA, Farquharson M, Oliver RT, Reznek RH. CT assessment of tumour response to treatment: comparison of linear, cross-sectional and volumetric measures of tumour size. Br J Radiol. 2000;73:1178–1184.
    1. Dachman AH, MacEneaney PM, Adedipe A, Carlin M, Schumm LP. Tumor size on computed tomography scans: is one measurement enough? Cancer. 2001;91:555–560.
    1. Werner-Wasik M, Xiao Y, Pequignot 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 Biol Phys. 2001;51:56–61.
    1. Warren KE, Patronas N, Aikin AA, Albert PS, Balis FM. Comparison of one-, two-, and three-dimensional measurements of childhood brain tumors. J Natl Cancer Inst. 2001;93:1401–1405.
    1. Prasad SR, Jhaveri KS, Saini S, Hahn PF, Halpern EF, Sumner JE. CT tumor measurement for therapeutic response assessment: comparison of unidimensional, bidimensional, and volumetric techniques initial observations. Radiology. 2002;225:416–419.
    1. Wormanns D, Kohl G, Klotz E, Marheine A, Beyer F, Heindel W, Diederich S. Volumetric measurements of pulmonary nodules at multi-row detector CT: in vivo reproducibility. Eur Radiol. 2004;14:86–92.
    1. Tran LN, Brown MS, Goldin JG, Yan X, Pais RC, McNitt-Gray MF, Gjertson D, Rogers SR, Aberle DR. Comparison of treatment response classifications between unidimensional, bidimensional, and volumetric measurements of metastatic lung lesions on chest computed tomography. Acad Radiol. 2004;11:1355–1360.
    1. Shah GD, Kesari S, Xu R, Batchelor TT, O'Neill AM, Hochberg FH, Levy B, Bradshaw J, Wen PY. Comparison of linear and volumetric criteria in assessing tumor response in adult high-grade gliomas. Neuro Oncol. 2006;8:38–46.
    1. Marten K, Auer F, Schmidt S, Kohl G, Rummeny EJ, Engelke C. Inadequacy of manual measurements compared to automated CT volumetry in assessment of treatment response of pulmonary metastases using RECIST criteria. Eur Radiol. 2006;16:781–790.
    1. Galanis E, Buckner JC, Maurer MJ, Sykora R, Castillo R, Ballman KV, Erickson BJ. Validation of neuroradiologic response assessment in gliomas: measurement by RECIST, two-dimensional, computer-assisted tumor area, and computer-assisted tumor volume methods. Neuro Oncol. 2006;8:156–165.
    1. Fabel M, von Tengg-Kobligk H, Giesel FL, Bornemann L, Dicken V, Kopp-Schneider A, Moser C, Delorme S, Kauczor HU. Semi-automated volumetric analysis of lymph node metastases in patients with malignant melanoma stage III/IV--a feasibility study. Eur Radiol. 2008;18:1114–1122.
    1. Ertl-Wagner BB, Blume JD, Peck D, Udupa JK, Herman B, Levering A, Schmalfuss IM Members of the American College of Radiology Imaging Network 6662 Study Group. 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. 2009;19:599–609.
    1. Krueger DA, Care MM, Holland K, Agricola K, Tudor C, Mangeshkar P, Wilson KA, Byars A, Sahmoud T, Franz DN. Everolimus for subependymal giant-cell astrocytomas in tuberous sclerosis. N Engl J Med. 2010;363:1801–1811.
    1. Lubner MG, Stabo N, Lubner SJ, Del Rio AM, Song C, Pickhardt PJ. Volumetric Versus Unidimensional Measures of Metastatic Colorectal Cancer in Assessing Disease Response. Clin Colorectal Cancer. 2017;16:324–333.e1.
    1. Quivey JM, Castro JR, Chen GT, Moss A, Marks WM. Computerized tomography in the quantitative assessment of tumour response. Br J Cancer Suppl. 1980;4:30–34.
    1. Breiman RS, Beck JW, Korobkin M, Glenny R, Akwari OE, Heaston DK, Moore AV, Ram PC. Volume determinations using computed tomography. AJR Am J Roentgenol. 1982;138:329–333.
    1. Nawaratne S, Fabiny R, Brien JE, Zalcberg J, Cosolo W, Whan A, Morgan DJ. Accuracy of volume measurement using helical CT. J Comput Assist Tomogr. 1997;21:481–486.
    1. De Robertis R, Tinazzi Martini P, Demozzi E, Puntel G, Ortolani S, Cingarlini S, Ruzzenente A, Guglielmi A, Tortora G, Bassi C, Pederzoli P, D'Onofrio M. Prognostication and response assessment in liver and pancreatic tumors: The new imaging. World J Gastroenterol. 2015;21:6794–6808.
    1. Yankeelov TE, Abramson RG, Quarles CC. Quantitative multimodality imaging in cancer research and therapy. Nat Rev Clin Oncol. 2014;11:670–680.
    1. RadiologyInfo. org. How much dose do I get from different imaging procedures? 2018 May 15 [cited 19 March 2019] Available from: .
    1. Salvatori M, Rizzo A, Rovera G, Indovina L, Schillaci O. Radiation dose in nuclear medicine: the hybrid imaging. Radiol Med. 2019;124:768–776.
    1. Cha KH, Hadjiiski L, Chan HP, Weizer AZ, Alva A, Cohan RH, Caoili EM, Paramagul C, Samala RK. Bladder Cancer Treatment Response Assessment in CT using Radiomics with Deep-Learning. Sci Rep. 2017;7:8738.
    1. Hosny A, Parmar C, Quackenbush J, Schwartz LH, Aerts HJWL. Artificial intelligence in radiology. Nat Rev Cancer. 2018;18:500–510.

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