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Breast Imaging |
1 From the Department of Radiology, Breast Imaging Center, Ullevaal University Hospital, Kirkeveien 166, N-0407 Oslo, Norway. From the 2001 RSNA scientific assembly. Received September 12, 2002; revision requested November 22; final revision received June 6, 2003; accepted July 15. Address correspondence to P.S. (e-mail: per.skaane@ulleval.no).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Full-field digital and screen-film mammography were performed in 3,683 women aged 50–69 years. Two standard views of each breast were acquired with each modality. Images underwent independent double reading with use of a five-point rating scale for probability of cancer. Recall rates and positive predictive values were calculated. Cancer detection rates determined with both modalities were compared by using the McNemar test for paired proportions. Retrospective side-by-side analysis for conspicuity of cancers was performed by an external independent radiologist group with experience in both modalities.
RESULTS: In 3,683 cases, 31 cancers were detected. Screen-film mammography depicted 28 (0.76%) malignancies, and full-field digital mammography depicted 23 (0.62%) malignancies. The difference between cancer detection rates was not significant (P = .23). The recall rate for full-field digital mammography (4.6%; 168 of 3,683 cases) was slightly higher than that for screen-film mammography (3.5%; 128 of 3,683 cases). The positive predictive value based on needle biopsy results was 46% for screen-film mammography and 39% for full-field digital mammography. Side-by-side image comparison for cancer conspicuity led to classification of 19 cancers as equal for probability of malignancy, six cancers as slightly better demonstrated at screen-film mammography, and six cancers as slightly better demonstrated at full-field digital mammography.
CONCLUSION: There was no statistically significant difference in cancer detection rate between screen-film and full-field digital mammography. Cancer conspicuity was equal with both modalities. Full-field digital mammography with soft-copy reading is comparable to screen-film mammography in population-based screening.
© RSNA, 2003
Index terms: Breast neoplasms, radiography, 00.112, 00.1215 • Breast radiography, comparative studies, 00.112, 00.1215 • Cancer screening • Radiography, digital, 00.1215
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Mammography screening programs could benefit greatly from implementation of digital imaging technologies if practical, effective, and economical digital imaging techniques could be applied in routine clinical practice. The main advantage of digital mammography is that the processes of image acquisition, display, and storage are decoupled. Consequently, with a digital mammography imaging system, each of these processes is performed independently, allowing each step to be optimized individually. Digital technology has the potential to offer several advantages in future screening programs. The true flexibility and the true benefit of digital technology are realized primarily in a soft-copy display of the images and consequently in soft-copy reading.
So far, only a few experimental or retrospective studies on the comparison of screen-film and full-field digital mammography with soft-copy reading have been reported (3–6). These studies have focused mainly on investigation of the two modalities in symptomatic women. To our knowledge, only one study has been published on the comparison of screen-film and full-field digital mammography in asymptomatic women in a screening situation (7). Thus, the aim of our study was to compare screen-film and full-field digital mammography with soft-copy reading in a population-based mammography screening program.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Imaging
The 3,683 women (mean age, 58.2 years) that represented the study population underwent both analog screen-film mammography and full-field direct digital mammography. The screen-film images were all acquired with one of two Mammomat 300 systems (Siemens Medical Systems, Erlangen, Germany) with Min-R 2000 film and Min-R 2190 screens (Eastman Kodak, Rochester, NY) in standard and large formats. Molybdenum-molybdenum and 29 kV were always used. Full-field digital images were acquired with a Senographe 2000D system (GE Medical Systems, Milwaukee, Wis). The unit is equipped with an automatic mode (automatic optimization of parameters), in which anode-filter combination and kilovolts are selected automatically after analysis of a short preexposure image. The automatic optimization of parameters was used according to the manufacturer’s recommendations. The area of the image detector was 19 x 23 cm. Mammograms of both imaging modalities included two standard views (craniocaudal and mediolateral oblique) of each breast.
Image Interpretation
The images were interpreted the following day in the breast imaging center. Eight radiologists, each with more than 4 years of experience with screening mammography, participated in the image interpretation. Before the project started, each radiologist had to interpret 400 full-field digital mammography images by using soft copies. The eight readers were divided into two teams: One team interpreted screen-film images, and the other team interpreted full-field digital images for 1 week. The teams of four radiologists each alternated weekly between screen-film and full-field digital image interpretations. The images were interpreted independently by two radiologists. Mammograms from prior screening rounds were not offered for interpretation sessions, since a view box placed next to the monitors might have influenced the detection of abnormalities at full-field digital mammography and consequently caused an interpretation bias.
The screen-film images were viewed on two standard motorized mammography alternators. A magnifying glass was always offered for screen-film reading, but its use was optional. The full-field digital images were interpreted as soft copies on the review workstation (GE Medical Systems), which included two high-resolution 2,000 x 2,500-pixel monitors and a dedicated keypad. The recommended display protocol for full-field digital image reading included three steps: (a) presentation of all four images, with two craniocaudal views back-to-back on one monitor and two mediolateral oblique views back-to-back on the other monitor; (b) presentation of both craniocaudal views, with one on each monitor ("full size"); and (c) presentation of both mediolateral oblique views, with one on each monitor ("full size"). This protocol, as well as further postprocessing (window-level adjustments, zooming, inversion) of the images, was optional. Postprocessing was strongly recommended for all cases, however, especially for the two mediolateral oblique full-size views, since, in general, most of the breast parenchyma is shown on these images.
The interpretations of screen-film and full-field digital images were recorded directly into the central database of the Norwegian Cancer Registry (QBE Vision; Sysdeco Technology, Oslo, Norway) by the radiologist with use of either a light pen (bar code technology) or a mouse connected to a personal computer that was placed next to the alternator for screen-film examinations or next to the viewing station for full-field digital examinations. A five-point rating scale for probability of cancer was used for both screen-film and full-field digital mammography: 1 = normal or definitely benign, 2 = probably benign, 3 = indeterminate finding, 4 = probably malignant, and 5 = malignant. If at least one of the two readers categorized the mammographic finding as 2 or higher, the case was automatically selected for the consensus meeting. The other two modes of selection for the consensus meetings were clinical symptoms (especially a palpable lump) and technically insufficient examination. Information about clinical findings, if present, was written on an envelope or information sheet by the radiographers in the screening center. This information was always placed next to the alternator or the viewing station during the image interpretation sessions. There was no time limit for image interpretation with either modality.
There were separate consensus meetings for interpretation of screen-film and full-field digital mammography images twice weekly. Mammograms from the previous screening rounds were, if available, offered at both screen-film and full-field digital mammography consensus meetings. The two radiologists that interpreted the screen-film images together with the two other radiologists from the screen-film team were responsible for the screen-film consensus meeting, and the two radiologists that interpreted full-field digital mammograms together with the other two readers on the full-field digital mammography team were responsible for the full-field digital mammography consensus meeting. A flow chart that shows the study design of the project is presented in Figure 1.
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Diagnostic Work-up
The diagnostic work-up of women who were recalled was performed in the breast imaging center, usually 1–2 weeks after the consensus meeting. The imaging work-up included spot-compression and magnification views, ultrasonography (US), and magnetic resonance imaging if needed. Fine-needle aspiration cytology was the standard technique for our percutaneous biopsies. The imaging-guided biopsies were performed with US guidance whenever possible; otherwise, stereotactic biopsy was performed or the perforated compression plate was used. All cytologic and histologic examinations were performed in the pathology department. All cancers (including breast malignancies) in Norway are reported to the Norwegian Cancer Registry, and this cancer file is linked to the file of the Norwegian Breast Cancer Screening Program. Thus, an absolute surveillance of patients included in our mammography screening program is given.
External Readings
After ending the study, two independent radiologists well experienced in both screen-film and full-field digital mammography with soft-copy reading performed a side-by-side analysis for cancer conspicuity of the proved malignancies detected in the study population. These two readers had 18 and 4 years of experience with screen-film mammography and 3 years of experience each with full-field digital mammography. The radiologists were informed about the presence of cancer; otherwise, no information about the interpretations by the Oslo radiologists, the side or localization of the cancer, or the histologic findings of the tumors were given.
The conspicuity for cancer was scored by means of consensus as equal or slightly better or better with one of the two modalities if the radiologists found that a cancer conspicuity difference was present. Furthermore, they were asked to evaluate if the cancer conspicuity of full-field digital mammography was increased by using extensive postprocessing beyond the full-size image presentation and the three predefined window levels—that is, quadrant zooming or free continuous zooming (by using the mouse), free continuous windowing (by using the mouse), and inversion.
Statistical Analysis
Medical audit parameters for mammography screening programs, including recall rate, cancer detection rate, and positive predictive value (PPV), were calculated with both modalities, as well as for the 6,249 women in the nonstudy population. The recall rate is the percentage of patients for whom further imaging work-up is recommended at the consensus meeting. PPV1 is the percentage of all screening mammography cases that result in a diagnosis of cancer based on an abnormal screening interpretation (score of 2 or higher on the five-point rating scale by at least one of the two readers). PPV2 is the percentage of examinations that result in a diagnosis of cancer in patients who underwent fine-needle aspiration cytology. The McNemar test for paired proportions (with P < .05 considered to indicate a statistically significant difference) was used to compare the cancer detection rates of the two modalities.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The median tumor size of the invasive cancers was 11.0 mm, which is comparable to the size of cancers detected with screen-film mammography in the previous round (Table 1). Twenty-eight of the 31 cancers in the study population were depicted on screen-film images (detection rate, 0.76%), compared with 23 cancers (detection rate, 0.62%) depicted on full-field digital images (Fig 2), with "positive" findings defined as a rating score of 2 or higher by at least one of the two independent readers. Thus, 20 cancers were considered positive with both modalities, whereas eight cancers were considered positive only on screen-film images and three cancers only on full-field digital images. The PPV based on an abnormal mammographic finding (PPV1) was 20% (26 cancers among the 128 recalled cases) with screen-film mammography compared with 12% (20 cancers among the 168 recalled cases) with full-field digital mammography (Table 1). PPV2 was 46% (26 cancers in 57 patients that underwent fine-needle aspiration cytology) for screen-film mammography and 39% (20 cancers in 52 patients that underwent fine-needle aspiration cytology) for full-field digital mammography.
In a 2 x 2 table analysis, the difference between the cancer detection rates was not significant (McNemar test, P = .23; discordant pairs 8 and 3). Two of the 20 cancers were discarded in the screen-film consensus meeting (screen-film image scores [for two readers] of 2–1 and 2–1 and full-field digital mammography scores of 3–1 and 3–2 in the reading sessions), and three cancers were discarded in the full-field digital mammography consensus meeting (screen-film image scores of 2–1, 3–1, and 3–3 and full-field digital mammography scores of 2–1, 2–1, and 3–1 in the reading sessions). Thus, 15 cancers were recalled for further diagnostic work-up in both screen-film and full-field digital mammography consensus meetings separately, and 11 cancers were recalled only in the screen-film consensus meeting compared with five cancers recalled only in the full-field digital consensus meeting. Again, this difference was not significant (McNemar test, P = .21; discordant pairs 11 and 5). The recall rate, cancer detection rate, PPV1, and median tumor size of the invasive cancers in the first two mammography screening rounds in Oslo compared with the third round (screen-film and full-field digital mammography of the study population) are summarized in Table 1.
The side-by-side analysis for cancer conspicuity performed by the independent external radiologists showed that 19 (61%) of the 31 tumors had equal conspicuity for malignancy (Fig 3). Six cancers had a higher score for conspicuity of malignancy on screen-film images, and six cancers were better demonstrated on full-field digital mammograms (Fig 3). One of the two cancers scored as "better" on screen-film images was located outside the images on the full-field digital mammograms and consequently represented a technical (positioning) failure at full-field digital mammography. This tumor was well demonstrated at full-field digital mammography during diagnostic work-up. One cancer depicted at full-field digital mammography was not seen by the external readers on either screen-film or full-field digital mammograms. The mammographic abnormality seen at full-field digital image interpretation turned out to be a simple cyst. During diagnostic work-up, an irregularity in the cystic wall was found at US, which histologic findings demonstrated to be an infiltration from an adjacent cancer. This tumor should be considered an incidental finding and is included in Figure 3 as having equal conspicuity with the two modalities. These two cases excluded, the comparison of the false-negative findings on screen-film and full-field digital mammograms, the results of side-by-side analysis for cancer conspicuity, and the mammographic features of the missed cancers are summarized in Table 2.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The advantage of soft-copy display is its flexibility, but disadvantages have mainly been poor user interface and limited resolution for currently available monitors (consequently with the need for "roam and zoom" functions). The design of efficient workstations has been considered one of the most important challenges of digital technology in mammography screening. The reading protocols used for image display would most likely be crucial to the success of full-field digital mammography with soft-copy reading.
To our knowledge, only one study has been reported (7) on the comparison of screen-film and full-field digital mammography with soft-copy reading in an asymptomatic population. That study, conducted at two institutions, included a total of 4,945 paired examinations of which 1,055 women were enrolled twice (7). No difference in cancer detection rate was found. Of the 31 cancers detected at screening and the four interval cancers detected in the study of Lewin et al (35 cancers total), screen-film mammography depicted 22 (63%), and full-field digital mammography depicted 21 (60%) (7). It is noteworthy that of the 31 cancers detected at screening, 12 (39%) were found with both modalities. The only significant result of the study of Lewin et al was a lower recall rate of full-field digital mammography (7).
The results of our study diverge somewhat from those of Lewin et al. First, our study results do not confirm the significantly lower recall rate of full-field digital mammography. On the contrary, 7% of cases were categorized as abnormal by at least one reader on screen-film images, compared with 12% on full-field digital images. After discussion in the consensus meetings, the recall rate for full-field digital mammography (4.6%) was still higher than that for screen-film mammography (3.5%) and that in the nonstudy population (2.6%) and was also higher than that for the two previous screening rounds. The higher recall rate with full-field digital mammography in our study could be explained by a learning curve effect, since the radiologists might have wanted to have a second opinion and diagnostic work-up for some of the lesions that were "probably benign" with the new modality.
The cancer detection rate was remarkably high for both screen-film mammography (0.76%) and full-field digital mammography (0.62%) in the study population, taking into account that the women were invited to a subsequent (third) screening round. The higher cancer detection rate in our project compared with that in the study of Lewin et al might partly be explained by the independent double reading in our study, whereas a single reading was performed for each modality in the study of Lewin et al (7). Although full-field digital mammography showed a high cancer detection rate, the PPV of abnormal screening mammograms was lower for full-field digital mammography compared with that of screen-film mammography because of the higher recall rate. The high cancer detection rate for the study population (0.84%) compared with that of the nonstudy population (0.40%) is remarkable. We are not aware of any bias that can fully explain this noticeable difference. This difference in cancer detection rate is, however, of no importance with regard to the aim of the study, which was to compare screen-film and full-field digital mammography with soft-copy reading in the study population.
Principal differences in eligible population and study design may also partly explain our diverging results compared with those of the study of Lewin et al. We included only women aged 50–69 years, compared with women older than 40 years in the study of Lewin et al (7). For a subject in the study of Lewin et al, one radiologist interpreted the screen-film images and another interpreted the full-field digital images, compared with independent double reading of both modalities in our study (7). Our five-point rating scale is somewhat different from the Breast Imaging Reporting and Data System, and we never require short-term follow-up of "probably benign" lesions. In the study of Lewin et al, a side-by-side review was performed for findings recalled for additional evaluation with only one of the two modalities, and the discarded findings were still considered positive in calculations of recall and sensitivity (7).
We had separate consensus meetings for screen-film and full-field digital mammograms for all cases selected by one or both readers, and discarded lesions were not included in our overall performance measures. The discarded findings were, however, counted as positive in the calculations of performance for the individual radiologists as presented in a separate report. It is noteworthy that a total of three cancers selected by one of the two independent readers on full-field digital images and two cancers selected by one of the radiologists on screen-film images were discarded in the consensus meetings in our study.
The results of our side-by-side analysis for cancer conspicuity confirm the results in phantom studies and clinical experimental settings, which have shown that full-field digital mammography is comparable to screen-film mammography in the detectability and characterization of microcalcifications and low-contrast objects (4,5,8,9). In our analysis, six of the nine cases of DCIS with the appearance of microcalcifications were grouped as equal, one case of DCIS had a higher conspicuity score on screen-film images, and two cases of DCIS had a higher conspicuity score on full-field digital mammograms. A comparison of false-negative mammographic interpretations (score of 1 by both independent readers), results of side-by-side analysis, and mammographic features of missed cancers are presented in Table 2. It is noteworthy that the three cases of DCIS missed on full-field digital mammograms were rated as equal for cancer conspicuity in the side-by-side image analysis. One case of grade I DCIS with an equal score for cancer conspicuity in the side-by-side image analysis was considered to be better demonstrated on full-field digital mammograms by using extensive postprocessing (zooming beyond the quadrant zooming and free windowing with the mouse).
Our results of the side-by-side conspicuity analysis indicate that little additional information is achieved by applying postprocessing (zooming) beyond the suggested quadrant zooming. Of the 19 cancers with equal cancer conspicuity in the side-by-side image analysis, two cancers (one invasive ductal carcinoma with the appearance of an ill-defined mass with accompanying microcalcification from DCIS and one pure DCIS) were better demonstrated by using extensive zooming and free windowing. One cancer (an ill-defined mass due to an invasive ductal carcinoma) was even considered to have a lower cancer conspicuity by using extensive zooming. In a previous study, no significant overall difference in lesion conspicuity was found between analog hard-copy mammograms, hard-copy digital mammograms, and enlarged soft-copy display in early cancers, but the mean conspicuity score for nonenlarged soft-copy display was substantially lower (3). These results are not comparable to those of our study, however, since different types of equipment with different pixel sizes were used, and we compared the quadrant zooming (suggested default setting in the interpretation session) and extensive postprocessing (zooming) beyond the quadrant enlargement.
Since our conspicuity analysis was not a blinded study, a certain amount of subjective bias may have occurred. The number of cases is also too small to draw final conclusions. Nevertheless, our results indicate that the discordant cancer cases represent detection or characterization errors by the readers and not failure of the imaging system, thus confirming the big issue of reader variability in mammography screening (10,11).
Considering the equal scores for cancer conspicuity of screen-film and full-field digital mammography in the side-by-side analysis, the question arises why some obvious cancers were missed at soft-copy reading. In retrospect, there seems to be no reason why some obvious cancers should be missed at full-field digital mammography. We believe that it is unlikely that the pixel size was of importance for the full-field digital mammography detection failure of cancers in our project. Results of a previous investigation have shown that images acquired with 50-µm pixel size did not show significantly improved lesion detection over those acquired with 100-µm pixel size (9).
Two primary weaknesses of our study might have favored screen-film compared with full-field digital mammography: insufficient experience of the radiologists in soft-copy reading and a suboptimal reading environment. Although all readers were highly experienced in screen-film screening, they were not trained with the same level of familiarity with digital soft-copy reading before the project started. Four readers had only the minimum experience of the 100 full-field digital mammography test cases with soft-copy display in the training session. The second weakness was the lack of a "dedicated" quiet room with minimal extraneous light for the soft-copy reading during our study. Display monitors should be located in a dark room because the brightness output is not as high as the brightness coming through film on a view box, which is one of several important factors that influences human perception in soft-copy reading (12).
Furthermore, the readers had to handle the radiology information system, or RIS, monitor (by using a mouse or a light pen with bar code technology) of the Norwegian Cancer Registry for the recording of interpretation results in addition to the two monitors of the full-field digital mammography soft-copy workstation. This somewhat troublesome user interface might have drawn attention away from the image analysis and thus influenced the perception of small mammographic abnormalities. The missed cancers on full-field digital mammograms, which were easily visible in retrospect, could support this assumption.
In conclusion, our results indicate that full-field digital mammography with soft-copy reading is suitable for a population-based mammography screening program. Cancer conspicuity was equal for screen-film and full-field digital mammography in the limited number of malignant tumors in this study. There was no statistically significant difference in cancer detection rates between screen-film and full-field digital mammography. The small number of cancer cases in this study limits the ability to detect true differences between the two imaging modalities. Some additional missed cancers at full-field digital mammography are most likely caused by factors other than image quality. The slightly lower diagnostic performance for full-field digital mammography might be due to a learning curve effect and suboptimal reading environment for soft-copy reading during the study and indicates that close attention must be paid to reader training and reading environments in full-field digital mammography with soft-copy display.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, P.S.; study concepts and design, P.S., A.S.; literature research, P.S., K.Y.; clinical studies, P.S., K.Y., A.S.; data acquisition and analysis/interpretation, P.S., K.Y., A.S.; statistical analysis, P.S.; manuscript preparation, definition of intellectual content, and editing, P.S., K.Y., A.S.; manuscript revision/review, P.S., A.S.; manuscript final version approval, P.S.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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P. Skaane, C. Balleyguier, F. Diekmann, S. Diekmann, J.-C. Piguet, K. Young, and L. T. Niklason Breast Lesion Detection and Classification: Comparison of Screen-Film Mammography and Full-Field Digital Mammography with Soft-copy Reading--Observer Performance Study Radiology, October 1, 2005; 237(1): 37 - 44. [Abstract] [Full Text] [PDF]
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E. D. Pisano, C. A. Gatsonis, M. J. Yaffe, R. E. Hendrick, A. N. A. Tosteson, D. G. Fryback, L. W. Bassett, J. K. Baum, E. F. Conant, R. A. Jong, et al. American College of Radiology Imaging Network Digital Mammographic Imaging Screening Trial: Objectives and Methodology Radiology, August 1, 2005; 236(2): 404 - 412. [Abstract] [Full Text] [PDF]
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 J. G. Elmore, K. Armstrong, C. D. Lehman, and S. W. Fletcher Screening for Breast Cancer JAMA, March 9, 2005; 293(10): 1245 - 1256. [Abstract] [Full Text] [PDF]
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D. Gur Technology and Practice Assessment: In Search of a "Desirable" Statement Radiology, March 1, 2005; 234(3): 659 - 660. [Full Text] [PDF]
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E. D. Pisano and M. J. Yaffe Digital Mammography Radiology, February 1, 2005; 234(2): 353 - 362. [Abstract] [Full Text] [PDF]
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 S. H. Taplin, L. Ichikawa, M. U. Yood, M. M. Manos, A. M. Geiger, S. Weinmann, J. Gilbert, J. Mouchawar, W. A. Leyden, R. Altaras, et al. Reason for Late-Stage Breast Cancer: Absence of Screening or Detection, or Breakdown in Follow-up? J Natl Cancer Inst, October 20, 2004; 96(20): 1518 - 1527. [Abstract] [Full Text] [PDF]
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P. Skaane and A. Skjennald Screen-Film Mammography versus Full-Field Digital Mammography with Soft-Copy Reading: Randomized Trial in a Population-based Screening Program--The Oslo II Study Radiology, July 1, 2004; 232(1): 197 - 204. [Abstract] [Full Text] [PDF]
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