Jessica M Winfield1,2, Nina Tunariu1,2, Mihaela Rata1,2, Keiko Miyazaki1,2, Neil P Jerome1,2, Michael Germuska1,2,3, Matthew D Blackledge1,2, David J Collins1,2, Johann S de Bono4,5, Timothy A Yap4,5, Nandita M deSouza1,2, Simon J Doran1,2, Dow-Mu Koh1,2, Martin O Leach1,2, Christina Messiou1,2, and Matthew R Orton1,2
1Cancer Research UK Cancer Imaging Centre, The Institute of Cancer Research, London, United Kingdom, 2MRI Unit, The Royal Marsden NHS Foundation Trust, Sutton, United Kingdom, 3Cardiff University Brain Research Imaging Centre (CUBRIC), School of Psychology, Cardiff University, Cardiff, United Kingdom, 4Drug Development Unit, The Royal Marsden NHS Foundation Trust, Sutton, United Kingdom, 5Division of Clinical Studies, The Institute of Cancer Research, London, United Kingdom
Synopsis
Repeatability of ADC estimates from ten diffusion-weighted MRI studies in extra-cranial soft tissues (nine patient studies and one healthy volunteer study, with a total of 111 subjects) were analysed in combination using the Radiological Society of North America (RSNA) Quantitative Imaging Biomarkers Alliance (QIBA) framework for assessment of technical performance of imaging biomarkers, in order to investigate factors affecting ADC repeatability. Coefficient of variation was between 2 and 7% for all studies, with no marked differences between imaging protocols or study populations, and better repeatability in large tumours compared with smaller tumours, indicating that ADC is a robust imaging metric with excellent repeatability in extra-cranial soft-tissue tumours.
Background
Body diffusion-weighted-MRI (DW-MRI) is established as a qualitative and
quantitative technique in oncology.1 Post-treatment changes in the
apparent diffusion coefficient (ADC) have been shown to be indicative of
response to chemotherapy and other treatments in a wide range of tumour types. The
minimum significant change in ADC that can be detected after treatment is
determined by the repeatability of the measurement. Double-baseline
examinations are often incorporated into clinical trials in order to estimate
ADC repeatability but conducting a second baseline examination is an additional
burden on patients and resources. It is desirable to make use of repeatability
estimates from previous studies, but this is hindered by variations in imaging
protocols, tumour types, and patient cohorts, as well as variations in
reporting ADC repeatability. The Radiological Society of North America (RSNA)
Quantitative Imaging Biomarkers Alliance (QIBA) framework for assessment of
technical performance of imaging biomarkers was developed to encourage consistency
in assessment of technical performance, including repeatability, and is applied
in this study.2Purpose
To assess ADC
repeatability in a wide variety of DW-MRI studies of extra-cranial soft-tissue
tumours and healthy organs, using methods proposed in the QIBA framework2,
across a wide range of imaging protocols, tumour sites, tumour sizes, and
patient populations.Methods
Nine patient studies and one healthy volunteer study were included in
this analysis, with Research Ethics Committee approval and written consent.
Study cohorts and imaging protocols are described in Figure 1; example images
from two patients are shown in Figure 2. A total of 141 tumours/healthy organs
were each imaged twice. For each tumour/organ, a volume of interest (VOI) was
defined by outlining the whole area of the tumour/organ on at least 3 central
slices. Median and mean ADC estimates (ADCmedian, ADCmean)
were calculated for each VOI. ADC repeatability was assessed using the within-subject
standard deviation (sw), within-subject coefficient of variation
(CoV), limits of agreement (LoA), repeatability coefficient (RC), and
intraclass correlation coefficient (ICC), with 95% confidence intervals
estimated for all quantities.2
Levene’s test for equality of variance (Matlab2016a) was used to assess
whether ADC repeatability differed between studies. Pearson’s linear correlation
coefficient (Matlab2016a) was used to assess correlation between CoV and the
year the study started, number of VOIs in the study, and the median volume of VOIs
in the study.
After analysis of each study separately, VOIs were further grouped into
small, medium, and large volumes (Figure 4), and ADC repeatability assessed for
the three groups. Tumours were also grouped by site (liver lesions, pelvic
masses, abdominal masses) and ADC repeatability assessed for these sub-groups.
Levene’s test was used to assess whether ADC repeatability differed between
sizes and between sites.
Results
Repeatability of ADCmedian
and ADCmean was good with CoVs between 1.7% and 6.5% for all studies
(Figure 3). Repeatability of ADCmean was similar to repeatability of
ADCmedian in each study (Figure 3). Levene’s test showed a
significant difference in repeatability between studies (p<0.05), which did
not persist after excluding the study with the lowest CoV (study B, which
included many large tumours). No correlation was observed between the CoV and
the year the study started nor the number of VOIs in each study. Weak
correlation was observed between the CoV and the median volume of VOIs in the
study (r=-0.5, p=0.1). There was a significant difference in ADC repeatability
between small, medium, and large volumes with the smallest CoV for large VOIs
(Figure 4, Levene’s test p<0.05). There was no difference in ADC
repeatability between liver lesions, pelvic masses and abdominal masses (Figure
5, Levene’s test p=0.5). The upper 95% LoA was 20% or lower in all studies,
with LoA of 12% for all VOIs analysed together. Discussion
The excellent
repeatability in all of the studies included in this analysis demonstrates that
ADC is a robust metric in clinical practice in oncology. Good repeatability was
observed across a wide variety of imaging protocol variations, with no marked
differences between study populations (phase 1 trial patients, paediatric
patients, and healthy adult volunteers) or tumour sites. However, the fact that
all studies were performed on single-vendor 1.5T scanners at the same
institution remains a limitation. The significant difference in repeatability
between small, medium and large tumours/organs, suggests that tumour
size is an important factor in ADC repeatability. A post-treatment increase in
ADC of 20% or more would be outside the LoA in all studies included in this
analysis.Conclusions
In a single-centre
setting, ADC is a robust imaging
metric with excellent repeatability in extra-cranial soft-tissue tumours across
a wide range of patient populations, tumour sites, sizes, and imaging protocol
variations.Acknowledgements
We
acknowledge CRUK and EPSRC support to the Cancer Imaging Centre at ICR and
RMH in association with MRC and Department of Health C1060/A10334, C1060/A16464
and NHS funding to the NIHR Biomedical Research Centre and the Clinical
Research Facility in Imaging. MOL
is an Emeritus NIHR Senior Investigator.
For
specific studies included in this work, we acknowledge funding from CRUK BIDD
grants C7273/A12064 and C1353/A12762; CRUK and EPSRC Cancer Imaging Programme at the
Children’s Cancer and Leukaemia Group (CCLG) in association with the MRC and
Department of Health (England) (C7809/A10342); an Experimental Cancer Medicine Centre
Network award (joint initiative, CRUK and UK Department of Health) grants
C51/A7401 and C12540/A15573; EPSRC Platform Grant EP/H046526/1; Experimental Cancer
Medicine Centre (ECMC) Network funding for support to early clinical trials; and the support of
the National Institute for Health Research through the Cancer Research Network.
Some of these studies
were supported by AstraZeneca, Merck, Basilea, ArQule, and Genentech. MRO was
funded by AstraZeneca.
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