SPECIAL ARTICLE |
New Guidelines to Evaluate the Response to Treatment in Solid Tumors
Patrick Therasse,
Susan G. Arbuck,
Elizabeth A. Eisenhauer,
Jantien Wanders,
Richard S. Kaplan,
Larry Rubinstein,
Jaap Verweij,
Martine Van Glabbeke,
Allan T. van Oosterom,
Michaele C. Christian,
Steve G. Gwyther
Affiliations of authors: P. Therasse, J. Verweij, M. Van
Glabbeke, A. T. van Oosterom, European Organization for Research and
Treatment of Cancer, Brussels, Belgium; S. G. Arbuck, R. S. Kaplan, L.
Rubinstein, M. C. Christian, National Cancer Institute, Bethesda, MD;
E. A. Eisenhauer, National Cancer Institute of Canada Clinical Trials
Group, Kingston, ON, Canada; J. Wanders, New Drug Development Office
Oncology, Amsterdam, The Netherlands; S. G. Gwyther, East Surrey
Healthcare National Health Service Trust, Redhill, U.K.
Correspondence to:
Patrick
Therasse, M.D., European Organization for Research and Treatment of Cancer Data Center,
Avenue
Mounier 83/11, 1200 Brussels, Belgium (e-mail: pth{at}eortc.be).
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ABSTRACT
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Anticancer cytotoxic agents go through a process by which their antitumor activityon the
basis
of the amount of tumor shrinkage they could generatehas been investigated. In the late
1970s,
the International Union Against Cancer and the World Health Organization introduced specific
criteria
for the codification of tumor response evaluation. In 1994, several organizations involved in
clinical
research combined forces to tackle the review of these criteria on the basis of the experience and
knowledge acquired since then. After several years of intensive discussions, a new set of
guidelines is
ready that will supersede the former criteria. In parallel to this initiative, one of the participating
groups
developed a model by which response rates could be derived from unidimensional measurement of
tumor lesions instead of the usual bidimensional approach. This new concept has been largely
validated
by the Response Evaluation Criteria in Solid Tumors Group and integrated into the present
guidelines.
This special article also provides some philosophic background to clarify the various purposes of
response evaluation. It proposes a model by which a combined assessment of all existing lesions,
characterized by target lesions (to be measured) and nontarget lesions, is used to extrapolate an
overall
response to treatment. Methods of assessing tumor lesions are better codified, briefly within the
guidelines and in more detail in Appendix I. All other aspects of response evaluation have been
discussed, reviewed, and amended whenever appropriate.
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A. PREAMBLE
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Early attempts to define the objective response of
a tumor to an anticancer agent were made in the early 1960s
(1,2). In the mid- to late 1970s, the definitions of objective
tumor response were widely disseminated and adopted when it became
apparent that a common language would be necessary to report the
results of cancer treatment in a consistent manner.
The World Health Organization (WHO) definitions published in the 1979 WHO
Handbook (3) and by Miller et al. (4) in 1981
have been the criteria most commonly
used by investigators around the globe. However, some problems have developed with the use of
WHO criteria: 1) The methods for integrating into response assessments the change in size of
measurable and "evaluable" lesions as defined by WHO vary among research
groups, 2)
the minimum lesion size and number of lesions to be recorded also vary, 3) the definitions of
progressive disease are related to change in a single lesion by some and to a change in the overall
tumor
load (sum of the measurements of all lesions) by others, and 4) the arrival of new technologies
(computed tomography [CT] and magnetic resonance imaging [MRI]) has
led
to some confusion about how to integrate three-dimensional measures into response assessment.
These issues and others have led to a number of different modifications or clarifications to the
WHO criteria, resulting in a situation where response criteria are no longer comparable among
research
organizationsthe very circumstance that the WHO publication had set out to avoid. This
situation led to an initiative undertaken by representatives of several research groups to review the
response definitions in use and to create a revision of the WHO criteria that, as far as possible,
addressed areas of conflict and inconsistency.
In so doing, a number of principles were identified:
1) Despite the fact that "novel" therapies are being developed that may
work by
mechanisms unlikely to cause tumor regression, there remains an important need to continue to
describe
objective change in tumor size in solid tumors for the foreseeable future. Thus, the four categories
of
complete response, partial response, stable disease, and progressive disease, as originally
categorized
in the WHO Handbook (3), should be retained in any new
revision.
2) Because of the need to retain some ability to compare favorable results of future
therapies with
those currently available, it was agreed that no major discrepancy in the meaning and the concept
of
partial response should exist between the old and the new guidelines, although measurement
criteria
would be different.
3) In some institutions, the technology now exists to determine changes in tumor volume
or
changes in tumor metabolism that may herald shrinkage. However, these techniques are not yet
widely
available, and many have not been validated. Furthermore, it was recognized that the utility of
response
criteria to date had not been related to precision of measurement. The definition of a partial
response, in
particular, is an arbitrary conventionthere is no inherent meaning for an individual patient
of a
50% decrease in overall tumor load. It was not thought that increased precision of
measurement
of tumor volume was an important goal for its own sake. Rather, standardization and
simplification of
methodology were desirable. Nevertheless, the guidelines proposed in this document are not
meant to
discourage the development of new tools that may provide more reliable surrogate end points
than
objective tumor response for predicting a potential therapeutic benefit for cancer patients.
4) Concerns regarding the ease with which a patient may be considered mistakenly to
have
disease progression by the current WHO criteria (primarily because of measurement error) have
already led some groups such as the Southwest Oncology Group to adopt criteria that require a
greater
increase in size of the tumor to consider a patient to have progressive disease (5). These concerns have led to a similar change within these revised WHO criteria (see Appendix II).
5) These criteria have not addressed several other areas of recent concern, but it is
anticipated
that this process will continue and the following will be considered in the future:
Measures of antitumor activity, other than tumor shrinkage, that
may appropriately allow investigation of cytostatic agents in phase II
trials;
Definitions of serum marker response and recommended methodology for their validation;
and
Specific tumors or anatomic sites presenting unique complexities.
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B. BACKGROUND
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These guidelines are the result of a large, international
collaboration. In 1994, the European Organization for Research and
Treatment of Cancer (EORTC), the National Cancer Institute (NCI) of the
United States, and the National Cancer Institute of Canada Clinical
Trials Group set up a task force (see Appendix III) with the
main objective of reviewing the existing sets of criteria used to
evaluate response to treatment in solid tumors. After 3 years of
regular meetings and exchange of ideas within the task force, a draft
revised version of the WHO criteria was produced and widely circulated
(see Appendix IV). Comments received (response rate, 95%)
were compiled and discussed within the task force before a second
version of the document integrating relevant comments was issued. This
second version of the document was again circulated to external
reviewers who were also invited to participate in a consensus meeting
(on behalf of the organization that they represented) to discuss and
finalize unresolved problems (October 1998). The list of participants
to this consensus meeting is shown in Appendix IV and included
representatives from academia, industry, and regulatory authorities.
Following the recommendations discussed during the consensus meeting, a
third version of the document was produced, presented publicly to the
scientific community (American Society for Clinical Oncology, 1999),
and submitted to the Journal of the National Cancer Institute
in June 1999 for official publication.
Data from collaborative studies, including more than 4000 patients assessed for tumor
response,
support the simplification of response evaluation through the use of unidimensional measurements
and
the sum of the longest diameters instead of the conventional method using two measurements and
the
sum of the products. The results of the different retrospective analyses (comparing both
approaches)
performed by use of these different databases are described in Appendix V. This new approach,
which
has been implemented in the following guidelines, is based on the model proposed by James et al.
(6).
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C. RESPONSE EVALUATION CRITERIA IN SOLID
TUMORS (RECIST) GUIDELINES
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1. Introduction
The introduction explores the definitions, assumptions, and purposes
of tumor response criteria. Below, guidelines that are offered may lead
to more uniform reporting of outcomes of clinical trials. Note that,
although single investigational agents are discussed, the principles
are the same for drug combinations, noninvestigational agents, or
approaches that do not involve drugs.
Tumor response associated with the administration of anticancer agents can be evaluated for
at
least three important purposes that are conceptually distinct:
- Tumor response as a prospective end point in early clinical trials.
In this situation, objective tumor response is employed to determine
whether the agent/regimen demonstrates sufficiently encouraging results
to warrant further testing. These trials are typically phase II trials
of investigational agents/regimens (see section 1.2), and it
is for use in this precise context that these guidelines have been
developed.
- Tumor response as a prospective end point in more definitive
clinical trials designed to provide an estimate of benefit for a
specific cohort of patients. These trials are often randomized
comparative trials or single-arm comparisons of combinations of agents
with historical control subjects. In this setting, objective tumor
response is used as a surrogate end point for other measures of
clinical benefit, including time to event (death or disease
progression) and symptom control (see section 1.3).
- Tumor response as a guide for the clinician and patient or study
subject in decisions about continuation of current therapy. This
purpose is applicable both to clinical trials and to routine practice
(see section 1.1), but use in the context of decisions
regarding continuation of therapy is not the primary focus of this
document.
However, in day-to-day usage, the distinction among these
uses of the term "tumor response" can easily be missed, unless an
effort is made to be explicit. When these differences are ignored,
inappropriate methodology may be used and incorrect conclusions may result.
1.1. Response Outcomes in Daily Clinical Practice of Oncology
The evaluation of tumor response in the daily clinical practice of
oncology may not be performed according to predefined criteria. It may,
rather, be based on a subjective medical judgment that results from
clinical and laboratory data that are used to assess the treatment
benefit for the patient. The defined criteria developed further in this
document are not necessarily applicable or complete in such a context.
It might be appropriate to make a distinction between "clinical
improvement" and "objective tumor response" in routine patient
management outside the context of a clinical trial.
1.2. Response Outcomes in Uncontrolled Trials as a Guide to Further Testing of a New
Therapy
"Observed response rate" is often employed in single-arm studies
as a "screen" for new anticancer agents that warrant further
testing. Related outcomes, such as response duration or proportion of
patients with complete responses, are sometimes employed in a similar
fashion. The utilization of a response rate in this way is not
encumbered by an implied assumption about the therapeutic benefit of
such responses but rather implies some degree of biologic antitumor
activity of the investigated agent.
For certain types of agents (i.e., cytotoxic drugs and hormones), experience has demonstrated
that
objective antitumor responses observed at a rate higher than would have been expected to occur
spontaneously can be useful in selecting anticancer agents for further study. Some agents selected
in this
way have eventually proven to be clinically useful. Furthermore, criteria for
"screening"
new agents in this way can be modified by accumulated experience and eventually validated in
terms of
the efficiency by which agents so screened are shown to be of clinical value by later, more
definitive,
trials.
In most circumstances, however, a new agent achieving a response rate determined a
priori to be sufficiently interesting to warrant further testing may not prove to be an effective
treatment
for the studied disease in subsequent randomized phase III trials. Random variables and selection
biases, both known and unknown, can have an overwhelming effect in small, uncontrolled trials.
These
trials are an efficient and economic step for initial evaluation of the activity of a new agent or
combination in a given disease setting. However, many such trials are performed, and the
proportion
that will provide false-positive results is necessarily substantial. In many circumstances, it would
be
appropriate to perform a second small confirmatory trial before initiating large resource-intensive
phase
III trials.
Sometimes, several new therapeutic approaches are studied in a randomized phase II trial.
The
purpose of randomization in this setting, as in phase III studies, is to minimize the impact of
random
imbalances in prognostic variables. However, randomized phase II studies are, by definition, not
intended to provide an adequately powered comparison between arms (regimens). Rather, the
goal is
simply to identify one or more arms for further testing, and the sample size is chosen so to provide
reasonable confidence that a truly inferior arm is not likely to be selected. Therefore, reporting the
results of such randomized phase II trials should not imply statistical comparisons between
treatment
arms.
1.3. Response Outcomes in Clinical Trials as a Surrogate for Palliative Effect
1.3.1. Use in nonrandomized clinical trials. The only
circumstance in which objective responses in a nonrandomized trial can
permit a tentative assumption of a palliative effect (i.e., beyond a
purely clinical measure of benefit) is when there is an actual or
implied comparison with historical series of similar patients. This
assumption is strongest when the prospectively determined statistical
analysis plan provides for matching of relevant prognostic variables
between case subjects and a defined series of control subjects.
Otherwise, there must be, at the very least, prospectively determined
statistical criteria that provide a very strong justification for
assumptions about the response rate that would have been expected in
the appropriate "control" population (untreated or treated with
conventional therapy, as fits the clinical setting). However, even
under these circumstances, a high rate of observed objective response
does not constitute proof or confirmation of clinical therapeutic
benefit. Because of unavoidable and nonquantifiable biases inherent in
nonrandomized trials, proof of benefit still requires eventual
confirmation in a prospectively randomized, controlled trial of
adequate size. The appropriate end points of therapeutic benefit for
such a trial are survival, progression-free survival, or symptom
control (including quality of life).
1.3.2. Use in randomized trials. Even in the context of prospectively randomized
phase III
comparative trials, "observed response rate" should not be the sole, or major, end
point.
The trial should be large enough that differences in response rate can be validated by association
with
more definitive end points reflecting therapeutic benefit, such as survival, progression-free
survival,
reduction in symptoms, or improvement (or maintenance) of quality of life.
2. Measurability of Tumor Lesions at Baseline
2.1. Definitions
At baseline, tumor lesions will be categorized as follows:
measurable (lesions that can be accurately measured in at least one
dimension [longest diameter to be recorded] as
20 mm with
conventional techniques or as
10 mm with spiral CT scan
[see section 2.2]) or nonmeasurable (all other lesions,
including small lesions [longest diameter <20 mm with conventional
techniques or <10 mm with spiral CT scan] and truly nonmeasurable
lesions).
The term "evaluable" in reference to measurability is not recommended and will
not
be used because it does not provide additional meaning or accuracy.
All measurements should be recorded in metric notation by use of a ruler or calipers. All
baseline
evaluations should be performed as closely as possible to the beginning of treatment and never
more
than 4 weeks before the beginning of treatment.
Lesions considered to be truly nonmeasurable include the following: bone lesions,
leptomeningeal
disease, ascites, pleural/pericardial effusion, inflammatory breast disease, lymphangitis
cutis/pulmonis,
abdominal masses that are not confirmed and followed by imaging techniques, and cystic lesions.
(Note: Tumor lesions that are situated in a previously irradiated area might or might
not be
considered measurable, and the conditions under which such lesions should be considered must be
defined in the protocol when appropriate.)
2.2. Specifications by Methods of Measurements
The same method of assessment and the same technique should be used
to characterize each identified and reported lesion at baseline and
during follow-up. Imaging-based evaluation is preferred to evaluation
by clinical examination when both methods have been used to assess the
antitumor effect of a treatment.
2.2.1. Clinical examination. Clinically detected lesions will only be considered
measurable
when they are superficial (e.g., skin nodules and palpable lymph nodes). For the case of skin
lesions,
documentation by color photographyincluding a ruler to estimate the size of the
lesionis recommended.
2.2.2. Chest x-ray. Lesions on chest x-ray are acceptable as measurable lesions when
they are clearly defined and surrounded by aerated lung. However, CT is preferable. More details
concerning the use of this method of assessment for objective tumor response evaluation are
provided
in Appendix I.
2.2.3. CT and MRI. CT and MRI are the best currently available and most
reproducible
methods for measuring target lesions selected for response assessment. Conventional CT and MRI
should be performed with contiguous cuts of 10 mm or less in slice thickness. Spiral CT should be
performed by use of a 5-mm contiguous reconstruction algorithm; this specification applies to the
tumors of the chest, abdomen, and pelvis, while head and neck tumors and those of the
extremities
usually require specific protocols. More details concerning the use of these methods of assessment
for
objective tumor response evaluation are provided in Appendix I.
2.2.4. Ultrasound. When the primary end point of the study is objective response
evaluation, ultrasound should not be used to measure tumor lesions that are clinically not easily
accessible. It may be used as a possible alternative to clinical measurements for superficial
palpable
lymph nodes, subcutaneous lesions, and thyroid nodules. Ultrasound might also be useful to
confirm the
complete disappearance of superficial lesions usually assessed by clinical examination.
Justifications for
not using ultrasound to measure tumor lesions for objective response evaluation are provided in
Appendix I.
2.2.5. Endoscopy and laparoscopy. The utilization of these techniques for objective
tumor
evaluation has not yet been fully or widely validated. Their uses in this specific context require
sophisticated equipment and a high level of expertise that may be available only in some centers.
Therefore, utilization of such techniques for objective tumor response should be restricted to
validation
purposes in specialized centers. However, such techniques can be useful in confirming complete
histopathologic response when biopsy specimens are obtained.
2.2.6. Tumor markers. Tumor markers alone cannot be used to assess response.
However, if markers are initially above the upper normal limit, they must return to normal levels
for a
patient to be considered in complete clinical response when all tumor lesions have disappeared.
Specific additional criteria for standardized usage of prostate-specific antigen and CA (cancer
antigen)
125 response in support of clinical trials are being validated.
2.2.7. Cytology and histology. Cytologic and histologic techniques can be used to
differentiate between partial response and complete response in rare cases (e.g., after treatment to
differentiate between residual benign lesions and residual malignant lesions in tumor types such as
germ
cell tumors). Cytologic confirmation of the neoplastic nature of any effusion that appears or
worsens
during treatment is required when the measurable tumor has met criteria for response or stable
disease.
Under such circumstances, the cytologic examination of the fluid collected will permit
differentiation
between response or stable disease (an effusion may be a side effect of the treatment) and
progressive
disease (if the neoplastic origin of the fluid is confirmed). New techniques to better establish
objective
tumor response will be integrated into these criteria when they are fully validated to be used in the
context of tumor response evaluation.
3. Tumor Response Evaluation
3.1. Baseline Evaluation
3.1.1. Assessment of overall tumor burden and measurable
disease. To assess objective response, it is necessary to estimate
the overall tumor burden at baseline to which subsequent measurements
will be compared. Only patients with measurable disease at baseline
should be included in protocols where objective tumor response is the
primary end point. Measurable disease is defined by the presence of at
least one measurable lesion (as defined in section 2.1). If the
measurable disease is restricted to a solitary lesion, its neoplastic
nature should be confirmed by cytology/histology.
3.1.2. Baseline documentation of "target" and "nontarget"
lesions. All measurable lesions up to a maximum of five lesions per organ and 10 lesions in
total,
representative of all involved organs, should be identified as target lesions and recorded and
measured
at baseline. Target lesions should be selected on the basis of their size (those with the longest
diameter)
and their suitability for accurate repeated measurements (either by imaging techniques or
clinically). A
sum of the longest diameter for all target lesions will be calculated and reported as the baseline
sum
longest diameter. The baseline sum longest diameter will be used as the reference by which to
characterize the objective tumor response.
All other lesions (or sites of disease) should be identified as nontarget lesions and should also
be
recorded at baseline. Measurements of these lesions are not required, but the presence or absence
of
each should be noted throughout follow-up.
3.2. Response Criteria
3.2.1. Evaluation of target lesions. This section provides
the definitions of the criteria used to determine objective tumor
response for target lesions. The criteria have been adapted from the
original WHO Handbook (3), taking into account the
measurement
of the longest diameter only for all target lesions: complete
responsethe disappearance of all target lesions; partial responseat
least a 30% decrease in the sum of the longest diameter of target
lesions, taking as reference the baseline sum longest diameter;
progressive diseaseat least a 20% increase in the sum of the longest
diameter of target lesions, taking as reference the smallest sum
longest diameter recorded since the treatment started or the appearance
of one or more new lesions; stable diseaseneither sufficient
shrinkage to qualify for partial response nor sufficient increase to
qualify for progressive disease, taking as reference the smallest sum
longest diameter since the treatment started.
3.2.2. Evaluation of nontarget lesions. This section provides the definitions of the
criteria
used to determine the objective tumor response for nontarget lesions: complete
responsethe
disappearance of all nontarget lesions and normalization of tumor marker level; incomplete
response/stable diseasethe persistence of one or more nontarget lesion(s) and/or the
maintenance of tumor marker level above the normal limits; and progressive diseasethe
appearance of one or more new lesions and/or unequivocal progression of existing nontarget
lesions (1).
(Note: Although a clear progression of "nontarget" lesions only is
exceptional, in such circumstances, the opinion of the treating physician should prevail and the
progression status should be confirmed later by the review panel [or study chair]).
3.2.3. Evaluation of best overall response. The best overall response is the best
response
recorded from the start of treatment until disease progression/recurrence (taking as reference for
progressive disease the smallest measurements recorded since the treatment started). In general,
the
patient's best response assignment will depend on the achievement of both measurement
and
confirmation criteria (see section 3.3.1). Table 1
provides overall
responses for all possible combinations of tumor responses in target and nontarget lesions with or
without the appearance of new lesions.
View this table:
[in this window]
[in a new window]
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Table 1. Overall responses for all possible combinations of
tumor
responses in target and nontarget lesions with or without the appearance of new lesions*
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(Notes:
- Patients with a global deterioration of health status requiring
discontinuation of treatment without objective evidence of disease
progression at that time should be classified as having "symptomatic
deterioration." Every effort should be made to document the objective
disease progression, even after discontinuation of treatment.
- Conditions that may define early progression, early death, and
inevaluability are study specific and should be clearly defined in each
protocol (depending on treatment duration and treatment periodicity).
- In some circumstances, it may be difficult to distinguish residual
disease from normal tissue. When the evaluation of complete response
depends on this determination, it is recommended that the residual
lesion be investigated (fine-needle aspiration/biopsy) before
confirming the complete response status.)
3.2.4. Frequency of tumor re-evaluation. Frequency
of tumor re-evaluation while on treatment should be protocol specific
and adapted to the type and schedule of treatment. However, in the
context of phase II studies where the beneficial effect of therapy is
not known, follow-up of every other cycle (i.e., 6-8 weeks) seems a
reasonable norm. Smaller or greater time intervals than these could be
justified in specific regimens or circumstances.
After the end of the treatment, the need for repetitive tumor evaluations depends on whether
the
phase II trial has, as a goal, the response rate or the time to an event (disease progression/death).
If
time to an event is the main end point of the study, then routine re-evaluation is warranted of
those
patients who went off the study for reasons other than the expected event at frequencies to be
determined by the protocol. Intervals between evaluations twice as long as on study are often
used, but
no strict rule can be made.
3.3. Confirmatory Measurement/Duration of Response
3.3.1. Confirmation. The main goal of confirmation of
objective response in clinical trials is to avoid overestimating the
response rate observed. This aspect of response evaluation is
particularly important in nonrandomized trials where response is the
primary end point. In this setting, to be assigned a status of partial
response or complete response, changes in tumor measurements must be
confirmed by repeat assessments that should be performed no less than 4
weeks after the criteria for response are first met. Longer intervals
as determined by the study protocol may also be appropriate.
In the case of stable disease, measurements must have met the stable disease criteria at least
once
after study entry at a minimum interval (in general, not less than 6-8 weeks) that is defined in the
study
protocol (see section 3.3.3).
(Note: Repeat studies to confirm changes in tumor size may not always be feasible or
may
not be part of the standard practice in protocols where progression-free survival and overall
survival
are the key end points. In such cases, patients will not have "confirmed response."
This
distinction should be made clear when reporting the outcome of such studies.)
3.3.2. Duration of overall response. The duration of overall response is measured
from
the time that measurement criteria are met for complete response or partial response (whichever
status
is recorded first) until the first date that recurrent or progressive disease is objectively
documented
(taking as reference for progressive disease the smallest measurements recorded since the
treatment
started). The duration of overall complete response is measured from the time measurement
criteria are
first met for complete response until the first date that recurrent disease is objectively
documented.
3.3.3. Duration of stable disease. Stable disease is measured from the start of the
treatment until the criteria for disease progression is met (taking as reference the smallest
measurements
recorded since the treatment started). The clinical relevance of the duration of stable disease
varies for
different tumor types and grades. Therefore, it is highly recommended that the protocol specify
the
minimal time interval required between two measurements for determination of stable disease.
This time
interval should take into account the expected clinical benefit that such a status may bring to the
population under study.
(Note: The duration of response or stable disease as well as the progression-free
survival
are influenced by the frequency of follow-up after baseline evaluation. It is not in the scope of this
guideline to define a standard follow-up frequency that should take into account many parameters,
including disease types and stages, treatment periodicity, and standard practice. However, these
limitations to the precision of the measured end point should be taken into account if comparisons
among trials are to be made.)
3.4. Progression-Free Survival/Time to Progression
This document focuses primarily on the use of objective response end
points. In some circumstances (e.g., brain tumors or investigation of
noncytoreductive anticancer agents), response evaluation may not be the
optimal method to assess the potential anticancer activity of new
agents/regimens. In such cases, progression-free survival/time to
progression can be considered valuable alternatives to provide an
initial estimate of biologic effect of new agents that may work by a
noncytotoxic mechanism. It is clear though that, in an uncontrolled
trial proposing to utilize progession-free survival/time to
progression, it will be necessary to document with care the basis for
estimating what magnitude of progression-free survival/time to
progression would be expected in the absence of a treatment effect. It
is also recommended that the analysis be quite conservative in
recognition of the likelihood of confounding biases, e.g., with regard
to selection and ascertainment. Uncontrolled trials using
progression-free survival or time to progression as a primary end point
should be considered on a case-by-case basis, and the methodology to be
applied should be thoroughly described in the protocol.
4. Response Review
For trials where the response rate is the primary end point, it is
strongly recommended that all responses be reviewed by an expert or
experts independent of the study at the study's completion.
Simultaneous review of the patients' files and radiologic images is
the best approach.
(Note: When a review of the radiologic images is to take place, it is also
recommended
that images be free of marks that might obscure the lesions or bias the evaluation of the
reviewer[s]).
5. Reporting of Results
All patients included in the study must be assessed for response to
treatment, even if there are major protocol treatment deviations or if
they are ineligible. Each patient will be assigned one of the following
categories: 1) complete response, 2) partial response, 3) stable
disease, 4) progressive disease, 5) early death from malignant disease,
6) early death from toxicity, 7) early death because of other cause, or
9) unknown (not assessable, insufficient data). (Note: By
arbitrary convention, category 9 usually designates the "unknown"
status of any type of data in a clinical database.)
All of the patients who met the eligibility criteria should be included in the main analysis of the
response rate. Patients in response categories 4-9 should be considered as failing to respond to
treatment (disease progression). Thus, an incorrect treatment schedule or drug administration
does not
result in exclusion from the analysis of the response rate. Precise definitions for categories 4-9 will
be
protocol specific.
All conclusions should be based on all eligible patients.
Subanalyses may then be performed on the basis of a subset of patients, excluding those for
whom
major protocol deviations have been identified (e.g., early death due to other reasons, early
discontinuation of treatment, major protocol violations, etc). However, these subanalyses may not
serve
as the basis for drawing conclusions concerning treatment efficacy, and the reasons for excluding
patients from the analysis should be clearly reported. The 95% confidence intervals should
be
provided.
6. Response Evaluation in Randomized Phase III Trials
Response evaluation in phase III trials may be an indicator of the
relative antitumor activity of the treatments evaluated but may usually
not solely predict the real therapeutic benefit for the population
studied. If objective response is selected as a primary end point for a
phase III study (only in circumstances where a direct relationship
between objective tumor response and a real therapeutic benefit can be
unambiguously demonstrated for the population studied), the same criteria as
those applicable to phase II trials (RECIST guidelines) should be used.
On the other hand, some of the guidelines presented in this special article might not be
required in
trials, such as phase III trials, in which objective response is not the primary end point.
For
example, in such trials, it might not be necessary to measure as many as 10 target lesions or to
confirm
response with a follow-up assessment after 4 weeks or more. Protocols should be written clearly
with
respect to planned response evaluation and whether confirmation is required so as to avoid post-hoc decisions affecting patient evaluability.
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APPENDIX I. SPECIFICATIONS FOR RADIOLOGIC IMAGING
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These notes are recommendations for use in clinical studies and,
as such, these protocols for computed tomography (CT) and magnetic
resonance imaging (MRI) scanning may differ from those employed in
clinical practice at various institutions. The use of standardized
protocols allows comparability both within and between different
studies, irrespective of where the examination has been undertaken.
Specific Notes
For chest x-ray, not only should the film be performed
in full inspiration in the posteroanterior projection, but also the
film to tube distance should remain constant between examinations.
However, patients in trials with advanced disease may not be well
enough to fulfill these criteria, and such situations should be
reported together with the measurements.
Lesions bordering the thoracic wall are not suitable for measurements by chest x-ray, since a
slight
change in position of the patients can cause considerable differences in the plane in which the
lesion is
projected and may appear to cause a change that is actually an artifact. These lesions should be
followed by a CT or an MRI. Similarly, lesions bordering or involving the mediastinum should be
documented on CT or MRI.
CT scans of the thorax, abdomen, and pelvis should be contiguous
throughout the anatomic
region of interest. As a rule of thumb, the minimum size of the lesion should be no less than
double the
slice thickness. Lesions smaller than this are subject to substantial "partial volume"
effects (i.e., size is underestimated because of the distance of the cut from the longest diameter;
such a
lesion may appear to have responded or progressed on subsequent examinations, when, in fact,
they
remain the same size [Fig. 1
]). This minimum lesion size for a
given
slice thickness at baseline ensures that any lesion appearing smaller on subsequent examinations
will
truly be decreasing in size. The longest diameter of each target lesion should be selected in the
axial
plane only.




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Fig 1. A) Computed tomography (CT)
"scannogram" of the thorax with a simulated 20-mm lesion in the
right mid-zone. B) CT "scannogram" of the thorax with
contiguous slices of 10-mm thickness. Each volume within the slice
thickness is scanned, and the average attenuation coefficient (i.e.,
density of multiple small cubes [voxels]) is represented spatially in
two dimensions (pixels) as a cross-sectional image on a gray scale. It
is important to note each line on the figure is a spatial
representation of the average density for the structures that pass
through that slice thickness, and the line does not represent a thin
"cut" through it at that level. Therefore, a lesion of at least 20
mm will appear about its true diameter on at least one image because
sufficient volume of the lesion is present so as not
to average it down substantially. C) CT scannogram performed at
15-mm intervals. Depending on how much of the tumor is within the slice
thickness, the average density may be substantially underestimated, as
in the upper of the two lesions, or it may approximate the true tumor
diameter, lower lesion. This is an oversimplification of the process
but illustrates the point without going into the physics of CT
reconstruction. D) CT scannogram performed at 24-mm intervals
and of 10-mm thickness. The lesion may be imaged through its diameter,
it may be partially imaged, or it may not be imaged at all. This is the
equivalent of imaging a very small lesion and trying to determine
whether its true diameter has changed from one examination to the next.
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|
The type of CT scanner is important regarding the slice thickness and minimum-sized lesion.
For
spiral (helical) CT scanners, the minimum size of any given lesion at baseline may be 10 mm,
provided
the images are reconstructed contiguously at 5-mm intervals. For conventional CT scanners, the
minimum-sized lesion should be 20 mm by use of a contiguous slice thickness of 10 mm.
The fundamental difference between spiral and conventional CT is that conventional CT
acquires
the information only for the particular slice thickness scanned, which is then expressed as a
two-dimensional representation of that thickness or volume as a gray scale image. The next slice
thickness needs to be scanned before it can be imaged and so on. Spiral CT acquires the data for
the
whole volume imaged, typically the whole of the thorax or upper abdomen in a single breath hold
of
about 20-30 seconds. To view the images, a suitable reconstruction algorithm is selected, by the
machine, so the data are appropriately imaged. As suggested above, for spiral CT, 5-mm
reconstructions can be made, thereby allowing a minimum-sized lesion of 10 mm.
Spiral CT is now the standard in most hospitals involved in cancer management in the United
States, Europe, and Japan, so the above comments related to spiral CT are pertinent. However,
some
institutions involved in clinical trials will have conventional CT, but the number of these scanners
will
decline as they are replaced by spiral CT.
Other body parts, where CT scans are of different slice thickness (such as the neck, which is
typically 5-mm thickness), or in the young pediatric population, where the slice thickness may be
different, the minimum-sized lesion allowable for measurability of the lesion may be different.
However,
it should be double the slice thickness. The slice thickness and the minimum-sized lesion should be
specified in the study protocol.
In patients in whom the abdomen and pelvis have been imaged, oral contrast agents should be
given to accentuate the bowel against other soft-tissue masses. This procedure is almost
universally
undertaken on a routine basis.
Intravenous contrast agents should also be given, unless contraindicated for medical reasons
such
as allergy. This is to accentuate vascular structures from adjacent lymph node masses and to help
enhance liver and other visceral metastases. Although, in clinical practice, its use may add little, in
the
context of a clinical study where objective response rate based on measurable disease is the end
point,
unless an intravenous contrast agent is given, a substantial number of otherwise measurable
lesions will
not be measurable. The use of intravenous contrast agents may sometimes seem unnecessary to
monitor
the evolution of specific disease sites (e.g., in patients in whom the disease is apparently restricted
to the
periphery of the lungs). However, the aim of a clinical study is to ensure that lesions are truly
resolving,
and there is no evidence of new disease at other sites scanned (e.g., small metastases in the liver)
that
may be more easily demonstrated with the use of intravenous contrast agent that should,
therefore, also
be considered in this context.
The method of administration of intravenous contrast agents is variable. Rather than try to
institute
rigid rules regarding methods for administering contrast agents and the volume injected, it is
appropriate
to suggest that an adequate volume of a suitable contrast agent should be given so that the
metastases
are demonstrated to best effect and a consistent method is used on subsequent examinations for
any
given patient.
All images from each examination should be included and not "selected"
images of
the apparent lesion. This distinction is intended to ensure that, if a review is undertaken, the
reviewer
can satisfy himself/herself that no other abnormalities coexist. All window settings should be
included,
particularly in the thorax, where the lung and soft-tissue windows should be considered.
Lesions should be measured on the same window setting on each examination. It is not
acceptable
to measure a lesion on lung windows on one examination and on soft-tissue settings on the next
(Fig. 2
). In the lung, it does not really matter whether lung or soft-tissue
windows are
used for intraparenchymal lesions, provided a thorough assessment of nodal and parenchymal
disease
has been undertaken and the target lesions are measured as appropriate by use of the same
window
settings for repeated examinations throughout the study.


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Fig 2. A) Computed tomography (CT) scan of the
thorax at the level of the carina on "soft-tissue" windows. Two
lesions have been measured with calipers. The intraparenchymal lesion
has been measured bidimensionally, using the greatest diameter and the
greatest perpendicular distance. Unidimensional measurements require
only the greatest diameter to be measured. The anterior-carinal lymph
node has been measured using unidimensional criteria. B) The
same image as above imaged on "lung" windows, with
the calipers remaining as they were for the soft-tissue measurements.
The size of the lung lesion appears different. The anterior-carinal
lymph node cannot be measured on these windows. The same windows should
be used on subsequent examinations to measure any lesions. Some favor
soft-tissue windows, so paratracheal, anterior, and subcarinal lesions
may be followed on the same settings as intraparenchymal lesions.
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Use of MRI is a complex issue. MRI is entirely acceptable and capable
of providing images
in different anatomic planes. It is, therefore, important that, when MRI is used, lesions must be
measured in the same anatomic plane by use of the same imaging sequences on subsequent
examinations. MRI scanners vary in the images produced. Some of the factors involved include
the
magnet strength (high-field magnets require shorter scan times, typically 2-5 minutes), the coil
design,
and patient cooperation. Wherever possible, the same scanner should be used. For instance, the
images
provided by a 1.5-Tesla scanner will differ from those provided by a 0.5-Tesla scanner. Although
comparisons can be made between images from different scanners, such comparisons are not
ideal.
Moreover, many patients with advanced malignancy are in pain, so their ability to remain still for
the
duration of a scan sequenceon the order of 2-5 minutesis limited. Any
movement
during the scan time leads to motion artifacts and degradation of image quality, so that the
examination
will probably be useless. For these reasons, CT is, at this point in time, the imaging modality of
choice.
Ultrasound examinations should not be used in clinical trials to measure
tumor regression or
progression of lesions that are not superficial because the examination is necessarily subjective.
Entire
examinations cannot be reproduced for independent review at a later date, and it must be
assumed,
whether or not it is the case, that the hard-copy films available represent a true and accurate
reflection
of events (Fig. 3
). Furthermore, if, for example, the only measurable
lesion is in
the para-aortic region of the abdomen and if gas in the bowel overlies the lesion, the lesion will
not be
detected because the ultrasound beam cannot penetrate the gas. Accordingly, the disease staging
(or
restaging for treatment evaluation) for this patient will not be accurate.


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Fig 3. A) Ultrasound scan of a normal structure,
the right kidney, which has been measured as 93 mm with the use of
callipers. B) Ultrasound scan of the same kidney taken a few
minutes later when it measures 108 mm. It appears to have increased in
size by 16%. The difference is due to foreshortening of the
kidney in panel A. The lack of anatomic landmarks
makes accurate measurement in the same plane on subsequent examinations
difficult. One has to hope that the measurements given on the hard copy
film are a true and accurate reflection of events.
|
|
The same imaging modality must be used throughout the study to measure disease. Different
imaging techniques have differing sensitivities, so any given lesion may have different dimensions
at any
given time if measured with different modalities. It is, therefore, not acceptable to interchange
different
modalities throughout a trial and use these measurements. It must be the same technique
throughout.
It is desirable to try to standardize the imaging modalities without adding undue constraints so
that
patients are not unnecessarily excluded from clinical trials.
 |
APPENDIX II. RELATIONSHIP BETWEEN CHANGE IN DIAMETER, PRODUCT, AND VOLUME
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 |
APPENDIX III. RESPONSE EVALUATION CRITERIA IN SOLID TUMORS (RECIST) WORKING GROUP AND SPECIAL ACKNOWLEDGMENTS
|
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RECIST Working Group
P. Therasse (Chair), J. Verweij, M. Van Glabbeke, A. T. van
Oosterom, European Organization for Research and Treatment of Cancer
(Brussels, Belgium); S. G. Arbuck, R. S. Kaplan, M. C. Christian,
National Cancer Institute, United States (Bethesda, MD); E. Eisenhauer,
National Cancer Institute of Canada Clinical Trials Group (Kingston);
S. Gwyther, East Surrey Hospital (Redhill, U.K.); and J. Wanders, New
Drug Development Office Oncology (Amsterdam, The Netherlands).
Retrospective Analyses
L. A. Rubinstein, National Cancer Institute, United States; B. K.
James, A. Muldal, W. Walsh, National Cancer Institute of Canada
Clinical Trials Group; S. Green, Southwest Oncology Group (Seattle,
WA); M. Terenziani, National Cancer Institute (Milan, Italy); D. Vena,
Emmes Corporation (Rockville, MD); R. Canetta, J. Burroughs,
Bristol-Myers Squibb (Wallingford, CT); A. Riva, M. Murawsky,
Rhone-Poulenc Rorer Pharmaceuticals Inc. (Paris, France).
 |
APPENDIX IV. PARTICIPANTS IN THE OCTOBER 1998
WORKSHOP TO DEVELOP THE FINAL RESPONSE
EVALUATION CRITERIA IN SOLID TUMORS
(RECIST)
DOCUMENT AND FURTHER ACKNOWLEDGMENTS
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Participants
S. C. S. Kao, Children's Cancer Study Group (Iowa City, IA); D.
Grinblatt, Cancer and Leukemia Group B (CALGB) (Chicago, IL); B.
Giantonio, Eastern Cooperative Oncology Group (ECOG) (Philadelphia,
PA); F. B. Stehman, Gynecologic Oncology Group (GOG) (Indianapolis,
IN); A. Trotti, Radiation Therapy Oncology Group (Tampa, FL); C. A.
Coltman, Southwest Oncology Group (SWOG) (San Antonio, TX); R. E.
Smith, National Surgical Adjuvant Breast and Bowel Project (Pittsburgh,
PA); J. Zalcberg, Peter MacCallum Cancer Institute (Melbourne),
Australia; N. Saijo, National Cancer Center Hospital (Tokyo, Japan); Y.
Fujiwara, National Institute of Health Sciences (Tokyo); G.
Schwartsmann, Hospital de Clinicas de Porto Alegre (Brazil); A. Klein,
Health Canada, Bureau of Pharmaceutical Assessment (Ottawa, ON); B.
Weinerman, National Cancer Institute of Canada Clinical Trials Group
(Kingston, ON); D. Warr, Ontario Cancer Institute/Princess Margaret
Hospital (Toronto); P. Liati, South Europe New Drugs Organization
(Milan, Italy); S. Einstein, Bio-Imaging Technologies (West Trenton,
NJ); S. Négrier, L. Ollivier, Fédération Nationale
des Centres de Lutte contre le Cancer (Paris, France); M. Marty,
International Cancer Cooperative Group/French Drug Agency (Paris); H.
Anderson, A. R. Hanauske, European Organization for Research and
Treatment of Cancer (EORTC) (Brussels, Belgium); M. R. Mirza, Odense
University Hospital (Denmark); J. Ersboll, The European Agency for the
Evaluation of Medicinal Products (Bronshoj, Denmark); C. Pagonis,
Cancer Research Campaign (London, U.K.); S. Hatty, Eli Lilly and Co.,
(Surrey, U.K.); A. Riva, Rhone-Poulenc Rorer Pharmaceuticals Inc.
(Paris); C. Royce, GlaxoWellcome (Middlesex, U.K.); G. Burke, Novartis
Pharma AG (Basel, Switzerland); I. Horak, Janssen Research Foundation
(Beerse, Belgium); G. Hoctin-Boes, Zeneca (Macclesfield Cheshire,
U.K.); C. Weil, Bristol-Myers Squibb (Waterloo, Belgium); M. G. Zurlo,
Pharmacia & Upjohn (Milan); S. Z. Fields, SmithKline Beecham
Pharmaceuticals (Collegeville, PA); B. Osterwalder, Hoffmann-La Roche
Inc. (Basel); Y. Shimamura, Taiho Pharmaceutical Co. Ltd. (Tokyo); and
M. Okabe, Kyowa-Hakko-Kogyo Co. Ltd. (Tokyo).
Additional comments were received from the following:
A. Hamilton, R. De Wit, E. Van Cutsem, J. Wils, J.-L.
Lefèbvre, I. Vergote, M. S. Aapro, J.-F. Bosset, M.
Hernandez-Bronchud, D. Lacombe, H. J. Schmoll, E. Van Limbergen, P.
Fumoleau, A. Bowman, U. Bruntsch, EORTC (Brussels); B. Escudier, P.
Thiesse, N. Tournemaine, P. Troufleau, C. Lasset, F. Gomez,
Fédération Nationale des Centres de Lutte contre le Cancer
(Paris); G. Rustin, Mount Vernon Hospital (Northwood Middlesex, U.K.);
S. B. Kaye, Western Infirmary (Glasgow, U.K.); A. Goldhirsch, F.
Nolè, G. Zampino, F. De Braud, M. Colleoni, E. Munzone, T. De
Pas, International Breast Cancer Study Group and Istituto Europeo di
Oncologia (Milan); M. Castiglione, J. F. Delaloye, A. Roth, C. Sessa,
D. Hess, B. Thürlimann, C. Böhme, T. Cerny, U. Hess,
Schweizer Arbeitsgemeinschaft für Klinische Krebsforschung (Bern,
Switzerland); H. J. Stewart, Scottish Cancer Therapy Network
(Edinburgh, U.K.); A. Howell, J. F. R. Robertson, United Kingdom
Coordinating Committee on Cancer Research (Nottingham); K. Noever,
Bio-Imaging Technologies (Monheim, Germany); M. Kurihara, Toyosu
Hospital, SHOWA University (Tokyo); L. Seymour, J. Pater, J. Rusthoven,
F. Shepherd, J. Maroun, G. Cairncross, D. Stewart, K. Pritchard,
National Cancer Institute of Canada Clinical Trials Group (Kingston);
T. Uscinowicz, Health Canada, Bureau of Pharmaceutical Assessment
(Ottawa); I. Tannock, Princess Margaret Hospital (Toronto); M. Azab,
QLT Phototherapeutics (Vancouver, Canada); V. H. C. Bramwell, Canadian
Sarcoma Group (London); P. O'Dwyer, ECOG (Philadelphia); A. Martin, S.
Ellenberg, U.S. Food and Drug Administration (Rockville, MD); C. Chow,
D. Sullivan, A. Murgo, A. Dwyer, J. Tatum, National Cancer Institute
(Bethesda, MD); R. Schilsky, CALGB (Chicago, IL); J. Crowley, S. Green,
SWOG (Seattle, WA); R. Park, GOG (Philadelphia, PA); V. Land, B. D.
Fletcher, Pediatric Oncology Group (Chicago, IL); B. Hillman,
University of Virginia (Charlottesville); F. Muggia, New York
University Medical Center (New York); C. Erlichman, Mayo Clinic
(Rochester, MN); L. H. Schwartz, Memorial Sloan-Kettering Cancer Center
(New York, NY); S. P. Balcerzak, Ohio State University Health Sciences
Center (Columbus); G. Fleming, CALGB (Chicago); G. Sorensen, Harvard
University (Cambridge, MA); H. Levy, Thomas Jefferson University
(Philadelphia); N. Patz, Duke University (Durham, NC); C.
Visseren-Grul, Eli Lilly Nederland BV (Nieuwegein, The Netherlands)/J.
Walling, Lilly Research Laboratories (Indianapolis); P. Hellemans,
Janssen Research Foundation (Beerse, Belgium); L. Finke, Merck
(Darmstadt, Germany); A. Man, N. Barbet, Novartis Pharma AG (Basel); G.
Massimini, Pharmacia & Upjohn (Milan); J, Jimeno, Pharma Mar (Madrid,
Spain); I. Hudson, SmithKline Beecham Pharmaceuticals (Essex, U.K.);
and J. Krebs, R. A. Beckman, S. Lane, D. Fitts, SmithKline Beecham
Pharmaceuticals (Collegeville).
 |
APPENDIX V. RETROSPECTIVE COMPARISON OF
RESPONSE/DISEASE PROGRESSION RATES
OBTAINED WITH THE WORLD HEALTH ORGANIZATION (WHO)/SOUTHWEST
ONCOLOGY GROUP CRITERIA AND THE NEW
RESPONSE EVALUATION CRITERIA IN
SOLID TUMORS (RECIST) CRITERIA
|
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To evaluate the hypothesis by which unidimensional measurement of
tumor lesions may substitute for the usual bidimensional approach, a
number of retrospective analyses have been undertaken. The results of
these analysis are given below in this section.
1. Comparison of Response and Disease Progression Rates by Use of WHO (or
Modified
WHO) or RECIST Methods
1.1. Trials Evaluated
No specific selection criteria were employed except that trial
data had to include serial (repeated) records of tumor measurements.
Several groups evaluated their own data on one or more such studies
(National Institute of Canada Clinical Trials Group, Kingston, ON; U.S.
National Cancer Institute, Bethesda, MD; and Rhone-Poulenc Rorer
Pharmaceuticals Inc., Paris, France) or made data available for
evaluation to the U.S. National Cancer Institute (Southwest Oncology
Group and Bristol-Myers Squibb, Wallingford, CT)
1.2. Response Criteria Evaluated
Not all databases were assessed for all response outcomes. At the
outset of this process, the most interest was in the assessment of
complete plus partial response rate comparisons by both the WHO and new
RECIST criteria. Once these data suggested no impact of using the new
criteria on the response rate, several more databases were analyzed for
the impact of the use of the new criteria not only on complete response
plus partial response but also on stable disease and progressive
disease rates (see Appendix V, Table 4
) and on time to disease
progression (see Appendix V, Table 5
).
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|
Appendix V, Table 4. Comparison of RECIST (unidimensional)
and
WHO (bidimensional) criteria in the same patients recruited in 14 different trials*
|
|
1.3. Methods of Comparison
For each patient in each study, baseline sums were calculated (sum
of products of the two longest diameters in perpendicular dimensions
for WHO and sum of longest diameters for RECIST). After each
assessment, when new tumor measures were available, the sums were
recalculated. Patients were assigned complete response, partial
response, stable disease, and progressive disease as their "best"
response on the basis of achieving the measurement criteria as
indicated in Appendix V, Table 3
. For both WHO and RECIST, a
minimum
interval of 4 weeks was required to consider complete response and
partial response confirmed. Each patient could, therefore, be assigned
a best response according to each of the two criteria. The overall
response and disease progression rates could be calculated for the
population studied for each trial or dataset examined.
(Note: For WHO progressive disease, as is the convention in most groups, an
increase in
sums of products was required, not an increase in only one lesion.)
1.4. Results
2. Evaluation of Time to Disease Progression
Time to disease progression was evaluated, comparing WHO criteria
with RECIST in a dataset provided by the Southwest Oncology Group
(SWOG). Since SWOG criteria (5) for disease progression is a
50% increase in the sum of the products, or new disease, or an
absolute increase of 10 cm2 in the sum of the products, this
dataset provided the means of assessing the impact of time to disease
progression differences between a 25% increase in the sum of the
products and a 20% increase in the sum of the longest diameters
(equivalent to approximately a 44% increase in the product sum).
2.1. Dataset Evaluated
The dataset includes 234 patients with progressive disease as
defined by the SWOG (5). All patients had baseline measurable
disease followed by the same technique(s) until disease progression.
The tumor types included were melanoma and colorectal, lung, and
breast cancers.
 |
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(2005). Study of the Biologic Effects of Lapatinib, a Reversible Inhibitor of ErbB1 and ErbB2 Tyrosine Kinases, on Tumor Growth and Survival Pathways in Patients With Advanced Malignancies. J Clin Oncol
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(2004). A Phase II Clinical and Pharmacodynamic Study of E7070 in Patients with Metastatic, Recurrent, or Refractory Squamous Cell Carcinoma of the Head and Neck: Modulation of Retinoblastoma Protein Phosphorylation by a Novel Chloroindolyl Sulfonamide Cell Cycle Inhibitor. Clin Cancer Res
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Correspondence about this Article
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CORRESPONDENCE
Ignace Vergote, Gordon J. S. Rustin, Elisabeth A. Eisenhauer, Gunnar B. Kristensen, Eric Pujade-Lauraine, Mahesh K. B. Parmar, Michael Friedlander, Anders Jakobsen, and Jan B. Vermorken
Re: New Guidelines to Evaluate the Response to Treatment in Solid Tumors [Ovarian Cancer]
J Natl Cancer Inst
2000;
92:
1534-1535.
[Extract]
[Full Text]
[PDF]
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CORRESPONDENCE
Gordon J. S. Rustin, Michael Quinn, Tate Thigpen, Andreas du Bois, Eric Pujade-Lauraine, Anders Jakobsen, Elizabeth Eisenhauer, Satoru Sagae, Kathryn Greven, Ignace Vergote, Andres Cervantes, and Jan Vermorken
Re: New Guidelines to Evaluate the Response to Treatment in Solid Tumors (Ovarian Cancer)
J Natl Cancer Inst
2004;
96:
487-488.
[Extract]
[Full Text]
[PDF]