DOI:10.2214/AJR.07.2875
AJR 2008; 190:886-891
© American Roentgen Ray Society
Improved Detection of Small Lung Cancers with Dual-Energy Subtraction Chest Radiography
Feng Li1,
Roger Engelmann1,
Kunio Doi1 and
Heber MacMahon1
1 All authors: Kurt Rossmann Laboratories for Radiologic Image Research and the
Department of Radiology, The University of Chicago, 5841 S Maryland Ave.,
MC-2026, Chicago, IL 60637.
Received July 16, 2007;
accepted after revision October 9, 2007.
This work was supported in part by USPHS grants CA61625, CA09119, and
EB00341 and by a research grant from Riverain Medical.
CAD technologies developed in the Kurt Rossmann Laboratories for Radiologic
Image Research have been licensed to R2 Technology, Deus Technologies,
Riverain Medical, Mitsubishi Space Software Co., Median Technologies, GE
Healthcare Corporation, and Toshiba Corporation.
K. Doi and H. MacMahon are shareholders of R2 Technology, Sunnyvale, CA,
and are consultants for Riverain Medical, Dayton, OH.
Presented at the 2006 annual meeting of the Radiological Society of North
America, Chicago, IL.
Address correspondence to F. Li
(feng{at}uchicago.edu).
Abstract
OBJECTIVE. The objective of our study was to retrospectively
evaluate whether the use of dual-energy subtraction chest radiographs can
improve radiologists' performance for the detection of small previously missed
lung cancers.
MATERIALS AND METHODS. Dual-energy subtraction chest radiographs of
19 patients with previously missed nodular cancers, in which the radiology
report did not mention a nodule that was visible in retrospect, were selected.
Dual-energy subtraction radiographs of 19 patients with cancer and 16 patients
without cancer were used for an observer study. Six radiologists indicated
their confidence level regarding the presence of a lung cancer and, if they
thought a cancer was present, also marked the most likely position for each
lung, first using standard posteroanterior and lateral chest radiographs and
then using both soft-tissue and bone dual-energy subtraction images along with
standard radiographs. Receiver operating characteristic (ROC) curves were used
to evaluate the observers' performance. The indicated locations of cancers and
false-positives were also analyzed.
RESULTS. The average area under the ROC curve
(Az) value for the six radiologists was improved from
0.718 to 0.816, a statistically significant amount (p = 0.004), and
the average sensitivity (correct localizations) for 19 previously missed
cancers was also significantly improved from 40% to 59% (p = 0.008)
with the aid of dual-energy subtraction images. The average number of
false-positive (incorrect) localizations on 70 lungs was 10 without and nine
with dual-energy subtraction images (p = 0.785).
CONCLUSION. Dual-energy subtraction chest radiography has the
potential to improve radiologists' performance for the detection of small
missed lung cancers.
Keywords: diagnostic radiology • digital radiography • dual-energy subtraction radiography • lung neoplasms • observer performance study
Introduction
With the evolution from film-based to digital systems, there have been many
remarkable advances in projection chest imaging
[1,
2]. Dual-energy subtraction
techniques can distinguish bone from soft tissue
[3,
4], and dual-energy subtraction
chest radiography has been shown by several observer performance studies to
improve the observers' ability to detect and characterize lung nodules
[5–7].
Dual-energy subtraction chest radiography has been used routinely for more
than 10 years in our institution. We recently studied lung cancers previously
missed by radiologists on chest radiographs in 34 patients
[8], over half of whom also had
dual-energy subtraction images. We noted that many of these lung cancers were
very subtle on the standard radiographs but were relatively obvious on the
soft-tissue images. We suspect that the radiologists did not review the
dual-energy subtraction images in many such cases either because they were
unaware that dual-energy subtraction images were available or because the
dual-energy subtraction images were not easily available for viewing due to
technical issues at that time. The purpose of our observer study was to
evaluate whether dual-energy subtraction chest radiographs can improve
radiologists' performance for the detection of small lung cancers.
Materials and Methods
Institutional review board approval was obtained, and the requirement for
informed patient consent was waived. Our study was compliant with HIPAA.
Patient Database and Reference Standard
The records of the cancer registry at the University of Chicago Hospitals
were reviewed to identify all patients diagnosed with lung cancer from January
2001 to November 2004 (n = 821). All patients with chest radiographs
on file before treatment were reviewed, and the relevant radiographs and
reports were analyzed (n = 314). From the 314 patients, 34 standard
posteroanterior (PA) digital radiographs of 34 patients were identified in
which a nodular cancer was present on the standard PA image in retrospect, but
had not been mentioned in the initial report. The location of each missed
cancer on the 34 standard PA chest radiographs was identified by consensus of
two radiologists, with all confirmed by CT. All of the cancers were confirmed
using biopsy or surgery as the reference standard. The two radiologists had 15
and 30 years of experience, respectively, in interpreting chest radiographs.
Analysis of the 34 missed lung cancers on 34 standard PA chest radiographs has
been reported previously in a study of computer-aided detection (CAD)
[8].
Dual-Energy Subtraction Chest Radiographs for Observer Study
Among the 34 patients with missed lung cancers, 21 had dual-energy
subtraction radiographs, of which 19 were available for review. All of these
missed cancers were visible in retrospect on the standard PA images by
consensus of the two radiologists, and all were visible on the dual-energy
subtraction images as well. Among these 19 patients, three had two primary
cancers in different lungs. One patient had two lung cancers, both of which
were identifiable on the soft-tissue image, but only one of which was
identifiable on the standard image. Two patients had a small nodular cancer
(< 20 mm) that had been mentioned in the report in addition to the missed
cancer. These two detected cancers and the one that was identifiable only on
the dual-energy subtraction image were excluded from the analysis of observer
results, although the images were included in the observer test.
In total, 19 patients with missed lung cancers on standard
(Fig. 1) or dual-energy
subtraction radiographs (or both) were used in our observer study. The 19
patients with missed cancers included 12 men and seven women with a mean age
of 69 years (range, 58–87 years). The mean interval between CT and
corresponding dual-energy subtraction radiography for the 19 patients was 11
months (five within 1 month, six at 2–12 months, five at 13–24
months, and three at 25–32 months). Eight lung cancers were located in
the right lung (four in the right upper lobe, one in the right middle lobe,
and three in the right lower lobe), and 11 were located in the left lung
(seven in the left upper lobe and four in the left lower lobe). The pathologic
diagnoses for the 19 cancers included 17 non–small cell carcinomas
(including seven adenocarcinomas, seven squamous cell carcinomas, and three
unspecified non–small cell carcinomas) and two small cell
carcinomas.
Before the observer study, the 19 missed cancers were graded for subtlety
(from extremely subtle to extremely obvious on a 1–10 scale) on the
standard images by the same two radiologists independently, and their numeric
ratings were averaged. The cases consisted of 12 with ratings of 1 to 3
(extremely to very subtle) and seven with ratings of 3.5 to 6.5 (subtle to
relatively obvious). The mean diameter (average of the length and width) of
the 19 identifiable lung cancers was 15.6 mm (range, 7–22 mm) on
standard images as measured by one radiologist.
Sixteen control subjects (mean age, 66 years; range, 50–79 years; 11
men and five women) without cancer on standard and dual-energy subtraction
radiographs were selected by approximate matching of age and sex to the 19
patients with cancer, and their examinations were performed on the same
radiography system as the subjects with cancer. Some of the 16 dual-energy
subtraction radiographs without missed lung cancers included incidental
abnormal findings (other than cancer) similar to those seen in the selected
cancer patients, including diffuse lung diseases, pleural abnormalities, and
very small calcified benign nodules; the results were confirmed by CT.
All radiographs with and without missed cancers used in our observer study
were obtained with a single-exposure dual-energy subtraction computed
radiography system (FCR 5501ES, Fuji Medical Systems) using 110 kVp and
2.5–16 mAs, according to patient size.
Observer Study
Two 2-megapixel monochrome LCD monitors (MDL 2004A, Totoku Electric),
similar to those used in our clinical reading area, were used in the observer
study. Observers were advised that cases in the study might show no cancers,
unilateral cancers, or bilateral cancers. However, observers were not informed
of the number of patients with or the number of patients without cancers or
that some of the cancers had been missed on the initial reading. Each case was
scored first without review of the dual-energy subtraction images and then
with the dual-energy subtraction images. Confidence bars were shown, one under
each lung, both without and with dual-energy subtraction. Radiologists
indicated their confidence level regarding the presence of a lung cancer, and
if they thought a cancer was present, also marked the most likely position for
each lung, first by use of standard PA and lateral chest radiographs and then
with dual-energy subtraction images (soft-tissue and bone images). Windowing
values were controlled manually by the radiologists, and a magnification tool
was available. Two clinical parameters (patient age and sex) were provided on
one of the monitors.
The six radiologists who participated in the observer study consisted of
one chest radiologist (26 years of experience), three general radiologists
(mean experience, 14 years; range, 10–16 years), and two radiology
residents (third and fourth year). Radiologists were instructed regarding the
nature of the task and appropriate use of the confidence rating scales. We
provided a training session before the test with five cases that were not used
in the study so that radiologists could learn how to operate the interface.
The five cases included two representative examples with a nodular cancer and
three without cancer.
Data Analysis
The confidence level ratings from each observer for 35 patients (70 lungs)
were analyzed using receiver operating characteristic (ROC) methodology, and a
quasi-maximum-likelihood estimation of the binormal distribution was fitted to
the radiologists' confidence ratings
[9]. The statistical
significance of the difference in Az values (area under
the ROC curve) between observers' readings without and with dual-energy
subtraction images was tested using the Dorfman-Berbaum-Metz method
[10], which included both
reader variation and case sample variation by means of an analysis-of-variance
approach. The quantity Az represents the area under an ROC
curve that has been fit by use of the conventional binormal model. Because ROC
curve area can be interpreted as sensitivity averaged over all specificities,
larger values of Az indicate greater diagnostic accuracy
[11,
12].
A marked location on an image was determined to be a correct localization
(used to calculate sensitivity) if the mark point was located within the
cancer boundary. Any marked locations that did not satisfy this criterion were
considered to be incorrect localizations (false-positives). The sensitivity
and number of false-positives were defined on the basis of the number of
localizations by the observers regardless of the confidence level ratings. The
statistical significance of the difference in correct or incorrect
localizations between radiologists without and with the dual-energy
subtraction images was estimated by use of the paired Student's t
test for the six radiologists.
Results
Evaluation by ROC Analysis
The average Az value for the six radiologists was
improved from 0.718 to 0.816, a statistically significant degree (p =
0.004) with the aid of dual-energy subtraction images
(Table 1 and
Fig. 2).
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TABLE 1: Areas Under the Receiver Operating Characteristic Curve
(Az) for the Detection of 19 Missed Cancers with Six
Observers
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Fig. 2 —Receiver operating characteristic (ROC) curves for detection
of cancers on chest radiographs with six radiologists. Average area under ROC
curve (Az) value was improved significantly from 0.718 to
0.816 with aid of dual-energy subtraction (ES) images.
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Evaluation by Analysis of Localization
The average sensitivity (based on correct localizations) for 19 missed
cancers with six radiologists was also significantly improved from 40% to 59%
(p = 0.008) with dual-energy subtraction images
(Table 2 and
Fig. 3). The average number of
false-positive (incorrect) localizations on 70 lungs was 10 without and nine
with dual-energy subtraction images (p = 0.785)
(Table 3).
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Fig. 3 —Bar graph shows number of correct localizations for 19
cancers by six radiologists with dual-energy subtraction images (gray
bars) and without dual-energy subtraction images (white bars).
For nine of 19 cancers (index numbers 4–6, 9–11, 14, 15, and 17),
dual-energy subtraction image had beneficial effect for one or more
radiologists. Dual-energy subtraction image had detrimental effect for only
one cancer (number 12).
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The six radiologists marked a total of 46 cancer locations on the standard
PA images and 67 cancer locations on the soft-tissue images. The radiologists
also marked a total of 60 false-positive locations on the standard PA images
and 53 false-positive locations on the soft-tissue images. Among these
false-positives, three pulmonary vessels (one in the periphery and two in the
hilum) were marked by two radiologists on both standard and soft-tissue
images; one nipple was marked by five radiologists on the standard image and
by four radiologists on the soft-tissue image; one bone lesion was marked by
four radiologists only on the standard image; one peripheral vessel, one
nipple, and one artifact were marked by two or three radiologists only on the
soft-tissue image; and each of the remaining 81 false-positives was marked by
only one radiologist on either the standard (n = 45) or the
soft-tissue (n = 36) images.
Examples of Images in Observer Study
Many of the missed lung cancers were very subtle on the standard
radiographs but were relatively obvious on the soft-tissue dual-energy
subtraction images, and most radiologists detected these cancers with the
dual-energy subtraction images (Figs.
4A,
4B,
5A,
5B, and
5C). Review of the dual-energy
subtraction image had a detrimental effect for the detection of only one
cancer (Figs. 6A and
6B).
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Fig. 4A —Dual-energy subtraction radiograph in 60-year-old woman
(number 5 in Fig. 3) with
previously missed bronchoalveolar carcinoma in left lung. Missed cancer
(arrows) is very subtle on standard posteroanterior image (A)
but is relatively obvious on soft-tissue image (B). Note that no
radiologists detected missed cancer without dual-energy subtraction and five
radiologists detected it with dual-energy subtraction in this observer
study.
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Fig. 4B —Dual-energy subtraction radiograph in 60-year-old woman
(number 5 in Fig. 3) with
previously missed bronchoalveolar carcinoma in left lung. Missed cancer
(arrows) is very subtle on standard posteroanterior image (A)
but is relatively obvious on soft-tissue image (B). Note that no
radiologists detected missed cancer without dual-energy subtraction and five
radiologists detected it with dual-energy subtraction in this observer
study.
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Fig. 5A —Dual-energy subtraction radiographs in 66-year-old woman
(number 10 in Fig. 3) with
missed squamous cell carcinoma in left upper lobe. Standard posteroanterior
image shows cancer (black arrow) and another nodular lesion
(white arrow).
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Fig. 5B —Dual-energy subtraction radiographs in 66-year-old woman
(number 10 in Fig. 3) with
missed squamous cell carcinoma in left upper lobe. Soft-tissue image
(B) clearly shows missed cancer (arrow, B) and bone
image (C) shows that other lesion is a fracture callus (arrow,
C). Note that two radiologists detected cancer without dual-energy
subtraction image, whereas five radiologists (three more) detected it with
dual-energy subtraction image in this observer study.
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Fig. 5C —Dual-energy subtraction radiographs in 66-year-old woman
(number 10 in Fig. 3) with
missed squamous cell carcinoma in left upper lobe. Soft-tissue image
(B) clearly shows missed cancer (arrow, B) and bone
image (C) shows that other lesion is a fracture callus (arrow,
C). Note that two radiologists detected cancer without dual-energy
subtraction image, whereas five radiologists (three more) detected it with
dual-energy subtraction image in this observer study.
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Fig. 6A —Dual-energy subtraction radiographs in 61-year-old woman
(number 12 in Fig. 3) with
primary adenocarcinoma in left lower lobe. Cropped views of left lung show
missed cancers (arrows) on standard posteroanterior image (A)
and soft-tissue image (B). Note that three radiologists detected cancer
without dual-energy subtraction image, but none confirmed it with dual-energy
subtraction (detrimental effect). This was probably because nodule appears to
represent confluence of vessels on dual-energy subtraction soft-tissue
image.
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Fig. 6B —Dual-energy subtraction radiographs in 61-year-old woman
(number 12 in Fig. 3) with
primary adenocarcinoma in left lower lobe. Cropped views of left lung show
missed cancers (arrows) on standard posteroanterior image (A)
and soft-tissue image (B). Note that three radiologists detected cancer
without dual-energy subtraction image, but none confirmed it with dual-energy
subtraction (detrimental effect). This was probably because nodule appears to
represent confluence of vessels on dual-energy subtraction soft-tissue
image.
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Discussion
Recent advances in chest radiography, including image processing, temporal
subtraction, dual-energy subtraction imaging, and CAD, have been shown to
enhance lung nodule detection
[1–7,
13–22].
However, it is important that available techniques are used appropriately in
clinical practice to obtain maximum benefit. The lung cancers used in our
observer study were previously missed by radiologists during routine
interpretation even when dual-energy subtraction images were available. The
observer study indicates that radiologists' performance for the detection of
these cancers could have been improved by the use of dual-energy subtraction
images, as indicated by the higher sensitivity, a similar number of
false-positives, and improved ROC curves as compared with the use of the
standard images alone. However, radiologists apparently did not review the
dual-energy subtraction images in at least some instances, probably because
they were not aware that dual-energy subtraction images were available.
Dual-energy subtraction images are now displayed easily on our PACS, and
review of these images requires only clicking on an icon or scrolling the
mouse wheel to reveal them. At the time that many of these images were
obtained, viewing dual-energy subtraction images required opening a separate
application, and these images were viewed only selectively when the
radiologist suspected an abnormality.
Studies have found that small nodular lung cancers are frequently missed on
conventional chest radiographs by radiologists in clinical practice
[23–30].
Shah et al. [28] reported a
missed cancer series with 40 cancers, in which 26 (65%) were obscured by two
or three bones, nine (22%) were obscured by a clavicle or one or more ribs,
and 12 (30%) were obscured by one bone. A similar incidence of obscuration by
bone was apparent in another missed cancer series that we performed
[8]. For those patients with
dual-energy subtraction images, many of the cancers were very subtle on the
standard radiographs but were relatively obvious on the soft-tissue
dual-energy subtraction images. The radiologists' performance for the
detection of missed cancers in our series was significantly improved
(Az values improved from 0.718 to 0.816; detection rates,
from 40% to 59%), and we believe soft-tissue images were responsible for the
improvement because they minimize obscuration by bones.
Ide et al. [31] performed a
study using 77 consecutive lung cancers and 77 healthy subjects without regard
to "missed" or "visible" criteria and reported that
Az values with five observers were increased from 0.46 to
0.53 for nonsolid, 0.72 to 0.82 for partly solid, and 0.97 to 0.99 for solid
cancers with dual-energy subtraction images. The three cancer patterns were
confirmed on thin-section CT performed at approximately the same time as the
dual-energy subtraction studies. Their results suggest that some of these
cancers were probably not visible on the radiograph, because the
Az values were approximately 0.5 without and with
dual-energy subtraction images for nonsolid cancers, and no localizations (to
determine detection rate) were requested of observers in that study
[31]. Our observer performance
study used missed cancers that were identified in retrospect as visible on
chest radiographs, although the CT studies used for confirmation were not
always obtained at the same time as the dual-energy subtraction radiographs.
In addition, we obtained the observers' localizations for cancers and
false-positives, whereas the previous study did not.
A limitation of our study was that it was a retrospective observer study of
a small number of patients with nodular cancers. Patients were identified from
the University of Chicago Cancer Registry, and inclusion was based on the
existence of an energy subtraction chest radiograph in which a peripheral
cancer was visible in retrospect that had not been mentioned in the radiology
report. Central hilar cancers were not included.
As with most observer tests, the results were influenced by the high
incidence of cancers as compared with routine clinical practice and by the
small number of cases. It is likely that the sensitivity was higher (increased
detection rate of subtle cancers) and the specificity lower (increased
false-positives) on both standard and dual-energy subtraction images in the
observer study because observers were more focused on the specific task of
detecting lung cancers than they might be in routine clinical practice.
Although the detection rate of missed cancers in our series was significantly
improved from 40% to 59% by use of dual-energy subtraction images in the
observer study, approximately 40% of these small cancers were still missed
because many were extremely subtle and difficult to detect.
In the observer performance study, we found the use of dual-energy
subtraction images yielded an improvement in sensitivity and did not produce a
detrimental effect for observers in terms of false-positive detections. We
conclude that dual-energy subtraction chest radiography can substantially
improve radiologists' ability to detect small lung cancers, and we believe
that dual-energy subtraction images should be viewed routinely, rather than
selectively, to derive maximum benefit.
Acknowledgments
We are grateful to Hiroyuki Abe, Jarvis Chen, Philip Caligiuri, Rodney
Corby, Christopher Straus, and Yonglin Pu for participating as observers.
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Abstract
Introduction
