Full-Field Digital versus Screen- Film Mammography - … · Full-Field Digital versus Screen-Film...

Full-Field Digital versus Screen-Film Mammography: Comparisonwithin the UK Breast ScreeningProgram and Systematic Review ofPublished Data1

Sarah Vinnicombe, MRCP, FRCRSnehal M. Pinto Pereira, MScValerie A. McCormack, MSc, PhDSusan Shiel, BScNick Perry, MDIsabel M. dos Santos Silva, MD, PhD

Purpose: To (a) compare the performance of full-field digital mam-mography (FFDM), using hard-copy image reading, withthat of screen-film mammography (SFM) within a UKscreening program (screening once every 3 years) forwomen aged 50 years or older and (b) conduct a meta-analysis of published findings along with the UK data.

Materials andMethods:

The study complied with the UK National Health ServiceCentral Office for Research Ethics Committee guidelines;informed patient consent was not required, since analysiswas carried out retrospectively after data anonymization.Between January 2006 and June 2007, a London popula-tion-based screening center performed 8478 FFDM and31 720 SFM screening examinations, with modality deter-mined by the type of machine available at the screeningsite. Logistic regression was used to assess whether breastcancer detection rates and recall rates differed betweenscreening modalities. For the meta-analysis, random-ef-fects models were used to combine study-specific esti-mates, if appropriate.

Results: A total of 263 breast cancers were detected. After adjust-ment for age, ethnicity, area of residence, and type ofreferral, there was no evidence of differences betweenFFDM and SFM in terms of detection rates (0.68 [95%confidence interval {CI}: 0.47, 0.89] vs 0.72 [95% CI:0.58, 0.85], respectively, per 100 screening mammo-grams; P � .74), recall rates (3.2% [95% CI: 2.8, 3.6] vs3.4% [95% CI: 3.1, 3.6]; P � .44), positive predictivevalue (PPV) of an abnormal mammogram, or characteris-tics of detected tumors. Meta-analysis of data from eightstudies showed a slightly higher detection rate for FFDM,particularly at 60 years of age or younger (pooled FFDM-SFM difference: 0.11 [95% CI: 0.04, 0.18] per 100 screen-ing mammograms), but no clear modality differences inrecall rates or PPVs.

Conclusion: Within a routine screening program, FFDM with hard-copy image reading performed as well as SFM in terms ofprocess indicators; the meta-analysis was consistent withFFDM yielding detection rates at least as high as those forSFM.

� RSNA, 2009

1 From the Breast Unit, St Bartholomew’s Hospital, Bartsand The London NHS Trust, West Smithfield, LondonEC1A 7BE, England (S.V., S.S., N.P.); and Cancer Re-search UK Epidemiology and Genetics Group, LondonSchool of Hygiene and Tropical Medicine, London, En-gland (S.M.P.P., V.A.M., I.M.d.S.S.). From the 2007 RSNAAnnual Meeting. Received July 15, 2008; revision re-quested August 19; revision received October 14; ac-cepted November 5; final version accepted December 11.Address correspondence to S.V. (e-mail: [email protected] ).

� RSNA, 2009

ORIGINALRESEARCH

�BREAST

IMAGING

Radiology: Volume 251: Number 2—May 2009 ▪ radiology.rsnajnls.org 347

Note: This copy is for your personal, non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, use the Radiology Reprints form at the end of this article.

Randomized controlled trials haveshown that screening mammogra-phy reduces breast cancer mortal-

ity, largely through its ability to depictsubtle soft-tissue masses and microcalci-fications that may represent early breastcancer (1,2). These trials were based onthe use of screen-film mammography(SFM). Mortality has not been assessedfor other screening modalities; rather, re-liance has been placed on surrogate endpoints such as breast cancer detectionrates, recall rates, and tumor character-istics (eg, size and stage) at diagnosis.

Full-field digital mammography(FFDM) was approved by the U.S. Foodand Drug Administration in 2000, but itsincorporation into screening mammogra-phy programs has been slow. Fewer than10% of mammography units in the UnitedStates were digital in 2006 (3) and in theUnited Kingdom, where most mammo-graphic screening takes place within theNational Health Service Breast ScreeningProgramme (NHSBSP), the move toFFDM has been even slower. Major ob-stacles to FFDM include the high cost ofthe units and of archiving facilities and thelogistics of converting from analogue todigital systems. In the United Kingdom,most screening takes place in mobileunits that move around catchment areas,with film being developed and imagesread at the base hospital.

Authors of previous studies have at-tempted to compare FFDM to SFM, butfew have done so within an operationalnational screening program. The newpurpose-built Breast Unit at St Bar-tholomew Hospital (London, England),which houses the Central and East Lon-don Breast Screening Service (CELBSS),was the first NHSBSP unit in the UnitedKingdom to be equipped with FFDMunits in 2005, although thus far it has notbeen possible to implement soft-copy im-age reading in the screening setting.

The aim of our study was to comparethe performance of FFDM, using hard-copy image reading, with that of conven-tional SFM within the context of a UKmammography screening program forwomen aged 50 years or older (two-viewmammograms obtained once every 3years). In addition, a systematic literaturereview on the performance of FFDM rel-ative to that of SMF, along with the newUK data, was conducted to summarizethe available evidence.

Materials and Methods

CELBSS StudyThe CELBSS is covered by the generalethical approval of the NHSBSP. Ourstudy complied with the UK NationalHealth Service Central Office for Re-search Ethics Committee guidelines.Informed patient consent was not con-sidered necessary as this retrospec-tive analysis was carried out after dataanonymization.

The NHSBSP is a population-basedscreening program that began in 1988 andoffers two-view mammography once every3 years to women aged 50–70 years.Women older than 70 years can self-referevery 3 years. The CELBSS, one of the re-gional NHSBSP centers, has an eligible pop-ulation of 120 000 women. The program is

quality assured according to NHSBSPguidelines (4), with an average standard-ized detection ratio of 1.25 in 2006–2007.Uptake is, however, relatively low acrossthis deprived urban inner-city area (uptakeis 50% compared with the national mini-mum target of 70%).

A total of 40 198 screening examina-tions in 39 651 women were performedby the CELBSS between January 1, 2005,when FFDM was first implemented, andJune 30, 2007. The majority of screeningexaminations were performed in two mo-bile units, each equipped with an M-IVmammography unit (Lorad, London, En-gland). The remainder of the screeningexaminations were conducted in a staticunit at St Bartholomew’s Hospital, whichhas four FFDM units: three SenographeDS units (GE Healthcare, Slough, En-gland) and one Selenia unit (Lorad). Thescreening location, and thus modality,was mainly influenced by residential area,since women are invited for screening ac-cording to the location of their generalpractitioner’s practice. A small percent-age of women (eg, those with specialneeds or implants) are preferentially in-vited for screening at St Bartholomew’sBreast Unit, and those working nearbycan request to be screened in this unit.

Published online10.1148/radiol.2512081235

Radiology 2009; 251:347–358

Abbreviations:BI-RADS � Breast Imaging Reporting and Data SystemCELBSS � Central and East London Breast Screening

ServiceCI � confidence intervalFFDM � full-field digital mammographyNHSBSP � National Health Service Breast Screening

ProgrammePPV � positive predictive valueSFM � screen-film mammography

Author contributions:Guarantors of integrity of entire study, S.V., I.M.d.S.S.;study concepts/study design or data acquisition or dataanalysis/interpretation, all authors; manuscript drafting ormanuscript revision for important intellectual content, allauthors; approval of final version of submitted manu-script, all authors; literature research, S.V., S.M.P.P.,I.M.d.S.S.; clinical studies, S.V., N.P.; statistical analysis,S.M.P.P., V.A.M., I.M.d.S.S.; and manuscript editing, S.V.,S.M.P.P., V.A.M., I.M.d.S.S.

Authors stated no financial relationship to disclose.

Advances in Knowledge

� In a UK routine population-basedscreening program for womenaged 50 years or older (screeningevery 3 years), full-field digitalmammography (FFDM) usinghard-copy reading performed aswell as screen-film mammography(SFM) in terms of breast cancerdetection rates, recall rates, andpositive predictive value (PPV) ofan abnormal mammogram.

� A meta-analysis of data fromseven published studies, togetherwith those from our UK study,was consistent with FFDM havingdetection rates at least as high asthose for SFM, with no clear mo-dality differences in recall rates orPPVs.

Implication for Patient Care

� Digital mammography with hard-copy reading performs, in termsof process measures, at least aswell as conventional screen-filmmammography for breast cancerscreening.

BREAST IMAGING: Full-Field Digital versus Screen-Film Mammography Vinnicombe et al

348 radiology.rsnajnls.org ▪ Radiology: Volume 251: Number 2—May 2009

All mammography units have compa-rable focal spot size and grid and are sub-jected to rigorous quality control proce-dures as specified in the NHSBSP (4) andEuropean quality assurance guidelines(5). Images obtained at the mobile unitswere processed at the base unit. Readingof the SFM film images and hard-copyreading of the FFDM images took placewith the same multiloaders and with thesame viewing conditions. For the first 18months, the optimized postprocessed im-ages (“Premium View” from SenographeDS units; GE Healthcare) could not beprinted, but a software upgrade renderedthis possible starting in June 2006. Thus,the unoptimized images were read for thefirst 18 months. Images from the FFDMscreening examinations were printedwith an 8900 laser hard-copy unit(Kodak, Hemel Hempstead, England)(38.75-�m laser spot size, 650 dpi reso-lution).

Each SFM and FFDM image was readby two of six radiologists (a pool of six pos-sible readers: S.V., N.P., and four nonau-thors), all but one of whom had more than10 years of experience in breast screening,reading a minimum of 5000 screening

Table 1

Characteristics of Study Subjects by Screening Modality

CharacteristicNo. of SFMExaminations*

No. of FFDMExaminations* Difference†

Total no. of screening examinations 31 720 (100.0)‡ 8478 (100.0)‡

Type of screening or referral 10.1 (9.3, 10.9)§

Routine recall 21 547 (67.9) 4305 (50.8)Prevalent round 8352 (26.3) 2831 (33.4)General practitioner referral 147 (0.46) 37 (0.4)Self-referral 1674 (5.28) 1305 (15.4)

Age (y) 2.3 (1.2, 3.5)�60 18 939 (59.7) 5263 (62.1)�60 12 781 (40.3) 3215 (37.9)

Ethnicity 4.5 (5.7, 3.3)Caucasian 17 828 (64.6) 4945 (69.1)Non-Caucasian 9770 (35.4) 2212 (30.9)Missing data 4122 (13.0) 1321 (15.6)

No. of recalls 1404 (4.43) 406 (4.79) 0.36 (�0.15, 0.87)No. of detected breast cancers 205 (0.65) 58 (0.68) 0.04 (�0.16, 0.23)

* Data in parentheses are percentages.† Data in parentheses are 95% CIs.‡ Numbers of screening examinations among 31 271 (SFM) and 8380 (FFDM) women.§ Difference between FFDM and SFM in percentage of screening examinations that were routine recall or prevalent as opposedto referrals.

Table 2

Cancer Detection Rates, Recall Rates, and PPVs of an Abnormal Mammogram by Screening Modality

Age at Screening (y) SFM FFDMRelative Risk for FFDM vs SFM

Crude Crude P Value* Adjusted† Adjusted P Value*

Cancer Detection Rates per 100 Screening Mammograms (n � 40 198‡ and 34 755§ in crude and adjusted analyses, respectively)�60 0.52 (0.42, 0.62) 0.61 (0.40, 0.82) 1.18 (0.71, 1.64) .43 1.05 (0.59, 1.51) .83�60 0.84 (0.68, 1.00) 0.81 (0.50, 1.12) 0.97 (0.55, 1.38) .87 0.86 (0.48, 1.25) .52All ages 0.65 (0.56, 0.73) 0.68 (0.51, 0.86) 1.06 (0.75, 1.37) .70 0.95 (0.65, 1.25) .74

Recall Rates per 100 Screening Mammograms (n � 40 198‡ and 34 755§ in crude and adjusted analyses, respectively)�60 5.03 (4.72, 5.34) 5.23 (4.62, 5.83) 1.04 (0.90, 1.18) .56 0.93 (0.79, 1.06) .31�60 3.54 (3.22, 3.86) 4.08 (3.39, 4.76) 1.15 (0.93, 1.37) .15 1.01 (0.80, 1.23) .91All ages 4.43 (4.20, 4.65) 4.79 (4.33, 5.24) 1.08 (0.97, 1.20) .15 0.95 (0.84, 1.07) .44

PPV of Breast Cancers among Recalls (%) (n � 1810� and 1516# in crude and adjusted analyses, respectively)�60 10.29 (8.36, 12.22) 11.64 (7.85, 15.43) 1.13 (0.71, 1.56) .52 1.07 (0.65, 1.49) .72�60 23.67 (19.75, 27.59) 19.85 (13.02, 26.68) 0.84 (0.52, 1.16) .36 0.84 (0.51, 1.18) .39All ages 14.60 (12.75, 16.45) 14.29 (10.88, 17.69) 0.98 (0.71, 1.24) .87 0.95 (0.68, 1.23) .75

Note.—Numbers in parentheses are 95% CIs. Interactions between screening modality and age at screening were not statistically significant (P � .54, .49, and .37 for adjusted detection rates,recall rates, and PPVs, respectively).

* P value for comparison between SFM and FFDM.† Adjusted for age, ethnicity, type of referral, and area of residence.‡ 31 720 SFM and 8478 FFDM screening examinations.§ Smaller numbers due to missing information on ethnicity (27 598 SFM and 7157 FFDM screening examinations).� 1404 SFM and 406 FFDM positive screening mammograms.# Smaller numbers due to missing information on ethnicity (1182 SFM and 334 FFDM recalls).



mammogramsper year. The second readerwas aware of the first reader’s opinion; anydisagreementwas arbitrated independentlyby a third reader. These procedures fol-lowed NHSBSP guidelines (4) and were notspecifically implemented for the purpose ofour study.

Data routinely collected at the time ofeach screening examination included age,ethnicity, area of residence, type of refer-ral, screening round, and, for all malignan-cies, type (invasive vs noninvasive), size,andhistologic grade. For the purpose of ourstudy, the screening mammograms for alldetected breast cancer cases were re-evaluated by a radiologist (S.V.) blinded tothe findings at the original assessment andpathologic evaluation. The following wereassessed: mammographic density (BreastImaging Reporting and Data System [BI-RADS] classification [6]); location, type,and size of lesion; radiologic characteristicsof lesion; and degree of radiologic suspicion(R1 � normal; R2 � benign; R3 � atypical;R4 � suspicious; R5 � highly suggestive ofmalignancy). In UK and European practice,theR3 categoryprompts assessment ratherthan early recall (5).

Standard logistic regression models (7)were fitted to assess the association ofscreening modality with the probability ofdetecting breast cancer while adjusting forage, ethnicity, area of residence, and typeof referral. To account for within-womancorrelations, observations from a singlewoman were treated as a cluster, with 95%confidence intervals (CIs) computed by us-ing robust standard errors and Wald testsused to assess associations. Similar logisticregression models were used to comparerecall rates, positive predictive values(PPVs) of an abnormal mammogram, andbinary tumor characteristics between thetwo screening modalities (the latter re-stricted to cases). Tests for interactionwere performed to investigate whether theeffect of screening modality on cancer de-tection, recall, and PPV differed by age atscreening or screening round. Analyseswere conducted by using statistical soft-ware (Stata, version 10; Stata, College Sta-tion, Tex).

Systematic ReviewA computerized search was conducted byusing PubMed, MEDLINE, and EMBASE to

Table 3

Characteristics of Mammographically Detected Cancers by Screening Modality

Characteristic SFM FFDM P Value*

Mammograms with BI-RADS 3�

(heterogeneous or extremely dense) 64/205 (31.2) 15/58 (25.9) .31Mammographic lesion visible on both standard

views 165/201 (82.1) 46/54 (85.2) .86Location of mammographic lesion

Upper quadrants 127/181 (70.2) 35/51 (68.6) .98Lower quadrants 38/181 (21.0) 11/51 (21.6)Other (eg, upper and lower) 16/181 (8.8) 5/51 (9.8)

Type of mammographic lesionMass 120/201 (59.7) 32/54 (59.3) .97Calcification 73/201 (36.3) 16/54 (29.6) .27Architectural distortion 67/201 (33.3) 16/54 (29.6) .29Asymmetric density 32/201 (15.9) 7/54 (13.0) .94

Radiologic characteristics of mass lesionsMean size (mm)†‡ 15.8 (14.3, 17.2) 15.3 (12.6, 18.1) .59Ovoid shape 68/99 (68.7) 17/26 (65.4) .87Microlobulate/lobulate border 9/55 (16.4) 2/14 (14.3) .40Halo 1/120 (0.8) 2/32 (6.3) .10Multiple lesions 8/119 (6.7) 1/32 (3.1) .46

Radiologic characteristics of calcificationsPresent jointly with a mass 18/69 (26.1) 1/15 (6.7) .26Nature .67

Punctuate 23/70 (32.9) 6/16 (37.5)Variable 16/70 (22.9) 4/16 (25.0)Linear branching/pleomorphic 31/70 (44.2) 6/16 (37.5)

Distribution .57Cluster 26/71 (36.6) 7/15 (46.7)Linear 19/71 (26.8) 2/15 (13.3)Segmental/regional 24/71 (33.8) 6/15 (4.0)

Extent (mm)†§ 33.4 (24.6, 42.2) 31.0 (12.2, 49.8) .80Density of individual particles .16

High 32/72 (44.4) 10/16 (62.5)Moderate 20/72 (27.8) 5/16 (31.3)Low 20/72 (27.8) 1/16 (6.3)

Cluster conspicuity .12High 13/69 (18.8) 9/14 (64.3)Moderate 28/69 (40.6) 5/14 (35.7)Low 28/69 (40.6) 0/14

With high density in surrounding breast area 32/72 (44.4) 10/16 (62.5) .15Radiologic characteristics of architectural

distortionIsolated 6/67 (9.0) 3/16 (18.8) .16With mass/asymmetric density 6/67 (9.0) 1/16 (6.3) .89

Degree of malignancy suspicionR3 (atypical) 54/205 (26.3) 14/57 (24.6) .87R4 (suspicious) 68/205 (33.2) 17/57 (29.8)R5 (highly suggestive) 83/205 (4.5) 26/57 (45.6)

Histologic characteristicsInvasive 159/205 (77.6) 45/58 (77.6) .74Grade of invasive tumors .24

1 39/156 (25.0) 8/42 (19.1)2 78/156 (50.0) 18/42 (42.9)3 39/156 (25.0) 16/42 (38.1)

(Table 3 continues)



identify studies published in English-lan-guage journals between January 1, 2000,andFebruary29, 2008 (inclusive) that com-pared FFDM to SFM in terms of their pro-cess indicators by using as search terms“digital” and “mammogra*” in the title.Studies were eligible if they reported esti-mates of detection rates, recall rates, orPPVs of an abnormal mammogram accord-ing to screening modality. Reference lists

within relevant articles and reviews weresearched to identify further publications.Each publication was checked to see if itwas a reanalysis or a subset of another eli-gible study and, if so, only the larger study,or constituent studies, where the data weredisplayedmost appropriatelywere includedto avoid duplication.

Each eligible publication was inde-pendently reviewed by two of the authors

(S.M.P.P., statistician; I.M.d.S.S., epide-miologist). Study-specific modality differ-ences (with 95% CIs) in process indica-tors were estimated if not provided in theoriginal publication; differences in PPVfrom paired studies were calculated byusing the methods outlined by Moskowitzand Pepe (8). Researchers from two stud-ies (9,10) were contacted to obtain addi-tional data, but additional data could nolonger be retrieved for one of these stud-ies (9). Forest plots were used to visualizestudy-specific estimates. Heterogeneitybetween studies was assessed by using a�2 statistic (Q) with inverse varianceweights. The percentage of total variationbetween studies that was caused by het-erogeneity rather than chance was quan-tified as I2 (11). Random effects modelswere used, if appropriate, to combinestudy-specific estimates (12) overall andstratified by study type and prespecifiedage groups (�60 and �60 years, or asclose to these as possible). Study size ef-fects were assessed by using funnel plotsand the Egger test (12).

Results

CELBSS StudyA total of 39 651womenunderwent 40 198screening examinations (546 women un-derwentmore than one screening examina-tion because of their moves between gen-eral practitioner practices). The medianage at screening was 58.0 years (inter-quartile range: 53.5, 63.5 years). Rela-tive to women in the SFM group, thosein the FFDM group were more likely tobe younger, Caucasian, and self-refer-rals (Table 1).

A total of 263 cancers were detectedin the study population (0.65 per 100screening mammograms). The crudedetection rate was slightly higher forFFDM than for SMF (0.68 vs 0.65 per100 screening mammograms, respec-tively), but after adjustment for age,ethnicity, type of referral, and area ofresidence there was no evidence of anydifference in detection rates betweenthe two screening modalities (Table 2).Similarly, there were no differences indetection rates between FFDM andSFM in analyses stratified by age at

Figure 1

Figure 1: Flow diagram illustrates the selection of studies included in the meta-analysis.

Table 3 (continued)

Characteristics of Mammographically Detected Cancers by Screening Modality

Characteristic SFM FFDM P Value*

Invasive tumor size (mm)†� 14.4 (12.8, 15.9) 17.01 (14.1, 19.9) .054

Note.—Except where noted, data are numbers of mammographically detected cancers with a given characteristic out ofrelevant SFM or FFDM tumors with no missing information, and numbers in parentheses are percentages.

* P value for difference in percentages between SFM and FFDM after adjustment for age, ethnicity, type of referral, and areaof residence.† Data are means, with 95% CIs in parentheses.‡ Among 120 (SFM) and 32 (FFDM) lesions measured.§ Among 73 (SFM) and 16 (FFDM) calcifications measured.� Among 159 (SFM) and 45 (FFDM) tumores measured.



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screening and no evidence that thesecomparisons varied by age (P � .54 forinteraction; Table 2) or screening round(ie, incident vs prevalent; P � .60 forinteraction).

The overall recall rate was 4.5% anddid not differ by screening modality, ei-

ther before or after adjustment for po-tential confounders (Table 2). Therewas also no evidence that the effect ofscreening modality on recall rates var-ied according to age at screening (P �.49 for interaction).

In total, 1810 women were recalled

for further assessment and 263 cancerswere detected and histologically con-firmed, yielding an overall PPV for anabnormal screening mammogram of14.5%. There was no difference in PPVby screening modality, either before orafter adjustment for potential confound-

Figure 2

Figure 2: Detection rates by screening modality. (a) Study-specific detection rates forSFM (black) and FFDM (gray), overall and by age at screening (when available), by studydesign. PM � pre- or perimenopausal. (b) Study-specific and pooled modality differences indetection rates, by study design. (c) Study-specific and pooled modality differences in detec-tion rates, by age at screening. No estimates were available for Yamada et al (9), as no cancerswere diagnosed. For Skaane et al (10), 2005, cancer detection rates are based on initial read-ing sessions and number of cancers diagnosed in the initial round, interval, and subsequentscreening round. For Pisano et al (19,23) data are also presented for certain population sub-groups defined by age, menopausal status, and breast density. Area of black squares in b andc is inversely proportional to the variance (on the log scale).



ers (Table 2). The effect of screeningmodality on PPVs did not differ by ageat screening (P � .37 for interaction).

Review of the original screeningmammograms for the 263 detected can-cers showed no associations betweenscreening modality and BI-RADS mam-mographic density (Table 3). Therewere also no associations betweenscreening modality and type of mammo-graphic lesion, likelihood of it being vis-ible on both standard views, its location,or radiologic characteristics. There wasno difference between the two modalitiesin the proportion of detected tumors thatwere invasive or in the distribution oftheir histologic grades. The average inva-sive tumor size was slightly larger for tu-mors detected with FFDM, but after ad-justment for potential confounders, thedifference was only of borderline statisti-cal significance (difference of 3.45 mm[95% CI: �0.07 mm, 6.97 mm]; P �.054).

Systematic ReviewThe search identified 189 publications(Fig 1); 124 were on digital mammogra-phy only and 52 were not eligible. Of theremaining 13 publications, one was on astudy performed in a diagnostic popula-tion (13) and in four (14–17), the studypopulation overlapped with that inother eligible publications. Thus, datafrom seven studies extracted from eightpublications (9,10,18–23), along withour UK study, were included in the re-view (Fig 1; Table 4). Four studies(9,10,18,19) had a paired design, thatis, the same group of women underwentscreening with both modalities, onestudy (20) was a randomized controlledtrial, and two studies (21,22)—plus ourstudy—had a cohort design (althoughsome included only baseline data intheir analyses). All studies, except one(9), used two standard views of eachbreast with each screening modality.Only our study and two others (9,19)used FFDM with hard-copy image read-ing, although this was only partial forone of the studies (19) (Table 4). Twostudies (18,19) used single reading, fivestudies (9,10,20,22), including ours,used double reading (three with consen-sus [10,20,22] and one with arbitration

by a third reader [our study]), and onestudy (21) used double reading with sin-gle-reader recall; however, in the latterstudy (21), as in our study, the tworeadings were not independent. In somestudies, prior mammograms and historydetails were available either at the ini-tial reading (18,21) or at the consensusmeetings (10,20,22). The length of fol-low-up varied, with two studies (10,20)including interval cancers as well as can-cers detected in the subsequent screen-ing round, while some cohort studiesincluded only baseline data.

Figure 2a shows study-specific de-tection rates for SFM and FFDM at allages, and by age group whenever avail-able in the original publication. Detec-tion rates tended to be lower in the twoU.S. studies and, as expected, in theyounger age groups. Figure 2b shows

study-specific and pooled modality dif-ferences in detection rates; there wasno evidence of study size effects (Eggerfunnel plot asymmetry test, P � .85).The overall pooled estimate was consis-tent with FFDM having a higher detec-tion rate than SFM (pooled FFDM-SFMdifference, 0.04 [95% CI: �0.03, 0.11]per 100 screening mammograms, equiva-lent to FFDM depicting an extra fourcases of breast cancer per every 10 000screening mammograms), but withevidence of some heterogeneity be-tween study types (I2 � 40%) (Fig 2b).Analyses stratified by age showedhigher FFDM detection rates at 60years or younger (equivalent to FFDMdepicting an extra 11 [95% CI: 4, 18]breast cancer cases per every 10 000screening mammograms) with no be-tween-study type heterogeneity (I2 �

Figure 3

Figure 3: Study-specific recall rates by screening modality (black � SFM, gray � FFDM) by study de-sign. For Pisano et al (19), recall rates are those reported for the BI-RADS scale.



0%) (Fig 2c). Pooled estimates at olderages were more difficult to interpret ow-ing to fewer and smaller studies. Theonly study (19,23) to have comparedthe two modalities simultaneously byage, menopausal status, and breast den-sity did not find any differences exceptthat FFDM yielded higher detectionrates among pre- and perimenopausalwomen younger than 50 years withdense breasts, whereas SFM yieldedslightly higher detection rates amongwomen older than 64 years with fatty(nondense) breasts (Fig 2a).

Recall rates varied greatly between

studies, with much higher rates in theUnited States than in the European andJapanese studies (Fig 3). There wasmarkedbetween-studyheterogeneity in dif-ferences in recall rates between modalities(I2 � 94%), with some studies showing sig-nificantly lower and others significantlyhigher recall rates for FFDM; thus, pooledestimates could not be calculated. Similarly,there was marked between-study type het-erogeneity in modality differences in thePPV of an abnormal mammogram (I2 �100%), with only cohort studies showing ahigher PPV for FFDM (Fig 4) and, hence,no pooled estimates were calculated. Some

studies (9,18–21) presented various recalland PPV estimates for different definitionsof abnormal mammograms (eg, before orafter consensus meetings) and detectedcancers (eg, at initial screening only or dur-ing follow-up), but these alternative esti-mates did not affect the findings shown inFigures 3 and 4.

Discussion

We found similar cancer detection ratesfor SFM and FFDM using hard-copy im-age reading; meta-analysis of publisheddata, along with our UK study findings,showed that FFDM performed, in termsof process measures, at least as well asconventional SFM.

Only two other published studies toour knowledge have compared FFDMwith SFM within the context of the dailypractice of a routine screening program(21,22). Del Turco et al (21) comparedFFDM and SFM within a local popula-tion-based program in Italy and found aslightly higher cancer detection rate forFFDM, which was particularly markedfor cancers that manifested as clusteredcalcifications (0.26% for FFDM vs0.12% for SFM; P � .007). Vigelandet al (22) conducted their study withinthe Norwegian national screening pro-gram and reported a higher detectionrate for FFDM, which was particularlymarked for ductal carcinoma in situ(0.21% for FFDM vs 0.11% for SFM;P � .001).

To our knowledge, our study is theonly one to have examined cancer de-tection rates for FFDM by using hard-copy image reading. Although Yamadaet al (9) used hard-copy reading, detec-tion rates could not be estimated, be-cause no cancers occurred during thefollow-up period. Pisano et al (19) alsoused hard-copy images for some of theirFFDM systems but these were not ana-lyzed separately. The use of hard-copyimage reading in our study was a matterof necessity rather than choice, becauseat the time, FFDM was still undergoingevaluation by the NHSBSP, and thusFFDM with soft-copy reading had notbeen incorporated into routine screen-ing. It did, however, obviate some of thedifficulties reported by authors of

Figure 4

Figure 4: Study-specific PPVs of an abnormal mammogram by screening modality (black � SFM, gray �FFDM), by study design and age. For Skaane et al (10), 2005, PPVs are based on all cancers diagnosed ininitial round, interval, and subsequent screening round among those with SFM or FFDM positive screeningmammograms at initial reading (prior to consensus meetings). For Pisano et al (19,23), PPVs are those re-ported for the BI-RADS scale. For Skaane et al (20), 2007, PPVs are based on number of cancers diagnosed ininitial round, interval, and subsequent screening round among those recalled (after consensus meetings). ForPisano et al (19,23) data are also presented for certain population subgroups defined by age, menopausalstatus (PM � pre- or perimenopausal), and breast density.



other studies, such as use of prototypesoft-copy workstations (18), subopti-mal viewing conditions, and learningcurve effect (15). In our study allscreening mammograms, whether fromSFM or FFDM, were viewed with iden-tical conditions. For the first 18 monthsof the study, it was not possible to printhard copy of the optimally postpro-cessed GE Healthcare images (“Pre-mium View”), and FFDM screening im-ages obtained during this period resem-bled analogue film images. Thus, somecancers may have been missed at FFDMin this group. This did not apply to thehard-copy images from screening mam-mograms obtained with the Selenia unit(Lorad), which were indistinguishablefrom the soft-copy images. Very fewstudies have compared hard-copy andsoft-copy reading, but in one analysis of60 tumors (31 benign, 29 malignant),there was little difference in sensitivitybetween the two modes, although threeof the four readers improved their spec-ificity and PPV with soft-copy imagereading (24). If true, these findingswould suggest that hard-copy readingmight not have affected the observedcancer detection rates for FFDM but itmight have decreased the specificity andPPV of this screening modality, thusleading to an increase in its recall rate(15,19).

The overall recall rate of 4.5% inour study was well below the NHSBSPtarget of less than 7% for prevalentscreening examinations and 5% for inci-dent screening examinations (4). Recallrates were significantly higher in theFFDM group than the SFM group in two(20,21) of the three studies (20–22)that found higher FFDM detectionrates, whereas recall rates in our studywere very similar for the two modali-ties. It is possible that the lack of FFDM-SFM difference in detection rates in ourstudy may be partly due to the fact thatrecall rates were similar for the two mo-dalities. Skaane et al (20) commented intheir article that their SFM recall ratewas too low; this might have led to anoverestimation of the FFDM-SFM dif-ference in detection rates in their study.

Meta-analyses provide an opportu-nity to identify sources of between-

study heterogeneity and, when appro-priate, to combine study-specific effectsto estimate an overall summary effectacross the various studies. Our meta-analysis was consistent with FFDM per-forming at least as well as conventionalSFM. Subgroup analyses by age pro-vided some evidence of FFDM having aslightly higher detection rate than SFMat age 60 years or younger, equivalentto an extra 11 breast cancer cases de-tected at FFDM per every 10 000screening examinations, but this findingneeds to be confirmed in future studies.Cohort studies, such as ours, are moreprone to be affected by confoundingthan paired studies or large randomizedtrials. In cohort studies, distinct groupsof women underwent FFDM and SFM,with the allocation to screening modal-ity being determined nonrandomly bythe women themselves or by the screen-ing program. Thus, women who under-went FFDM might have differed fromthose who underwent SFM in relation tofactors that influence detection rates.Although attempts were made to mini-mize confounding at the design andanalysis stages, one cannot exclude thepossibility that the findings from cohortstudies might have been affected by re-sidual or unknown confounding. Reas-suringly, the meta-analyses found noclear evidence of heterogeneity by studydesign, particularly in analyses stratifiedby age. Although meta-analyses areprone to small size effects, includingpublication bias, the data did not pro-vide any evidence to support this.

In summary, the findings from ourUK study and the meta-analysis are con-sistent with FFDM performing at leastas well as conventional SFM for breastcancer screening. Further research is,however, required to assess the eco-nomic costs of FFDM and identify thebest clinical and cost-effective ways ofimplementing it. �

References1. Humphrey LL, Helfand M, Chan BKS, Woolf

SH. Breast cancer screening: a summary ofthe evidence for the US Preventive ServicesTask Force. Ann Intern Med 2002;137:347–360.

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3. Dershaw DD. Status of mammography afterthe Digital Mammography Imaging Screen-ing Trial: digital versus film. Breast J 2006;12:99–102.

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5. Perry N, Broeders M, de Wolf C, et al, eds.European guidelines for quality assurance inbreast cancer screening and diagnosis. 4thed. Luxembourg: European Communities,2006.

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10. Skaane P, Skjennald A, Young K, et al. Fol-low-up and final results of the Oslo I studycomparing screen-film mammography andfull-field digital mammography with soft-copy reading. Acta Radiol 2005;46:679–689.

11. Higgins JP, Thompson SG, Deeks JJ, AltmanDG. Measuring inconsistency in meta-analy-ses. BMJ 2003;327:557–560.

12. Sutton AJ. Methods for meta-analysis inmedical research. Wiley Series in Probabil-ity and Statistics. New York, NY: Wiley,2000.

13. Venta LA, Hendrick RE, Adler YT, et al.Rates and causes of disagreement in inter-pretation of full-field digital mammographyand film-screen mammography in a diagnos-tic setting. AJR Am J Roentgenol 2001;176:1241–1248.

14. Lewin JM, Hendrik RE, D’Orsi CJ, et al.Comparison of full-field digital mammogra-phy with screen-film mammography for can-cer detection: results of 4,945 paired exami-nations. Radiology 2001;218:873–880.

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mammography with soft-copy reading—OsloI Study. Radiology 2003;229:877–884.

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mography and screen-film mammographyfor detection of breast cancer. AJR Am JRoentgenol 2002;179:671–677.

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Invoice or Credit Card InformationInvoice Address Please Print ClearlyPlease complete Invoice address as it appears on credit card statementName ____________________________________________Institution ________________________________________Department _______________________________________Street ____________________________________________City ________________________ State _____ Zip _______Country ___________________________________________Phone _____________________ Fax _________________E-mail Address _____________________________________

Cadmus will process credit cards and Cadmus Journal Services will appear on the credit card statement.

If you don’t mail your order form, you may fax it to 410-820-9765 with your credit card information.

Signature __________________________________________ Date _______________________________________Signature is required. By signing this form, the author agrees to accept the responsibility for the payment of reprints and/or all charges described in this document.

Reprint order forms and purchase orders or prepayments must be received 72 hours after receipt of form either by mail or by fax at 410-820-9765. It is the policy of Cadmus Reprints to issue one invoice per order.

Please print clearly.

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Radiology 2009Black and White Reprint Prices

Domestic (USA only)# of

Pages50 100 200 300 400 500

1-4 $239 $260 $285 $303 $323 $3405-8 $379 $420 $455 $491 $534 $5729-12 $507 $560 $651 $684 $748 $814

13-16 $627 $698 $784 $868 $954 $1,03817-20 $755 $845 $947 $1,064 $1,166 $1,27221-24 $878 $985 $1,115 $1,250 $1,377 $1,51825-28 $1,003 $1,136 $1,294 $1,446 $1,607 $1,75729-32 $1,128 $1,281 $1,459 $1,632 $1,819 $2,002

Covers $149 $164 $219 $275 $335 $393

International (includes Canada and Mexico)# of

Pages50 100 200 300 400 500

1-4 $299 $314 $367 $429 $484 $5465-8 $470 $502 $616 $722 $838 $9499-12 $637 $687 $852 $1,031 $1,190 $1,369

13-16 $794 $861 $1,088 $1,313 $1,540 $1,76517-20 $963 $1,051 $1,324 $1,619 $1,892 $2,16821-24 $1,114 $1,222 $1,560 $1,906 $2,244 $2,58825-28 $1,287 $1,412 $1,801 $2,198 $2,607 $2,99829-32 $1,441 $1,586 $2,045 $2,499 $2,959 $3,418

Covers $211 $224 $324 $444 $558 $672

Minimum order is 50 copies. For orders larger than 500 copies, please consult Cadmus Reprints at 800-407-9190.

Reprint CoverCover prices are listed above. The cover will include the publication title, article title, and author name in black.

ShippingShipping costs are included in the reprint prices. Do mesticorders are shipped via FedEx Ground service. Foreign orders are shipped via a proof of delivery air service.

Multiple ShipmentsOrders can be shipped to more than one location. Please be aware that it will cost $32 for each additional location.

DeliveryYour order will be shipped within 2 weeks of the journal print date. Allow extra time for delivery.

Color Reprint PricesDomestic (USA only)

# of Pages

50 100 200 300 400 500

1-4 $247 $267 $385 $515 $650 $7805-8 $297 $435 $655 $923 $1194 $14679-12 $445 $563 $926 $1,339 $1,748 $2,162

13-16 $587 $710 $1,201 $1,748 $2,297 $2,84317-20 $738 $858 $1,474 $2,167 $2,846 $3,53221-24 $888 $1,005 $1,750 $2,575 $3,400 $4,23025-28 $1,035 $1,164 $2,034 $2,986 $3,957 $4,91229-32 $1,186 $1,311 $2,302 $3,402 $4,509 $5,612

Covers $149 $164 $219 $275 $335 $393

International (includes Canada and Mexico))# of

Pages50 100 200 300 400 500

1-4 $306 $321 $467 $642 $811 $9865-8 $387 $517 $816 $1,154 $1,498 $1,8449-12 $574 $689 $1,157 $1,686 $2,190 $2,717

13-16 $754 $874 $1,506 $2,193 $2,883 $3,57017-20 $710 $1,063 $1,852 $2,722 $3,572 $4,42821-24 $1,124 $1,242 $2,195 $3,231 $4,267 $5,30025-28 $1,320 $1,440 $2,541 $3,738 $4,957 $6,15329-32 $1,498 $1,616 $2,888 $4,269 $5,649 $7028

Covers $211 $224 $324 $444 $558 $672

Tax DueResidents of Virginia, Maryland, Pennsylvania, and the District of Columbia are required to add the appropriate sales tax to each reprint order. For orders shipped to Canada, please add 7% Canadian GST unless exemption is claimed.

OrderingReprint order forms and purchase order or prepayment is required to process your order. Please reference journal name and reprint number or manuscript number on anycorrespondence. You may use the reverse side of this form as a proforma invoice. Please return your order form and prepayment to:

Cadmus ReprintsP.O. Box 751903Charlotte, NC 28275-1903

Note: Do not send express packages to this location, PO Box.FEIN #:541274108

Please direct all inquiries to:

Rose A. Baynard800-407-9190 (toll free number)410-819-3966 (direct number)410-820-9765 (FAX number)[email protected] (e-mail)

Reprint Order Forms and purchase order or prepayments must be received 72 hours after receipt of form.

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