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rganized Breast Cancer Screeningn British Columbia: The Screening

ammography Program of British Columbiainda J. Warren Burhenne, MD, FRCPC, Andrew J. Coldman, PhD, and Lisa Kan, MSc

The first organized breast cancer service screening program in Canada was established in1988 in British Columbia. The pilot project was successful in showing that screening couldbe conducted at a unit cost of US$38; now US$41. Screening is conducted in dedicatedcenters and diagnostic work-ups done in the community. The current annual volume is235,000. Stepwise expansion is ongoing and is determined by community specific servicerequirements. Prognostic factors of cancers detected consistently exceed internationallyrecommended targets. Since the inception of the program the age standardized breastcancer mortality rate per 100,000 has dropped in British Columbia from the highest to thelowest in Canada for provinces with similar populations.Semin Breast Dis 10:83-88 © 2007 Elsevier Inc. All rights reserved.

KEYWORDS mammography, screening program organization, screening cost analysis, servicescreening, screening performance indicators

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n 1988, the first breast cancer service screening program inCanada, the Screening Mammography Program of British

olumbia, was established.By that time, earliest results of the Health Insurance Plan of

ew York1,2 and the results from the Swedish Two Countyrial3 had been published. As well, there were reports of

ow-cost screening programs in Sweden, the Netherlands,nd North America.4-9

The Program began as a pilot project funded by the Min-stry of Health of British Columbia to examine 7000 womenn 1 year. The primary goals were: (1) to determine the unitost of screening mammography; (2) to study data collection,nalysis, and quality control; and (3) to study compliancend acceptance of the project by women. This report com-rises data and analyses compiled up to and including 2003.There are now 34 screening centers, 78 mobile destina-

ions, and 63 program screeners.

epartment of Radiology, University of British Columbia, BC CancerAgency, Vancouver, British Columbia.

ddress reprint requests to Linda J. Warren Burhenne, MD, FRCPC,Department of Radiology, University of British Columbia, 505-750W. Broadway, Vancouver, B.C. Canada, V5Z 1H4. E-mail: lwarren@

evancouverbreastcentre.com

092-4450/07/$-see front matter © 2007 Elsevier Inc. All rights reserved.oi:10.1053/j.sembd.2007.09.005

rogram Organizationhe program continues to be funded by the Ministry ofealth of British Columbia as one of the screening programsf the British Columbia Cancer Agency.Any asymptomatic British Columbia woman aged 40 to 80

s welcome to participate in the program. High-risk womennder age 40 are accepted individually by consultation withhe Chief Screener and the referring family doctor.

creening andiagnostic Procedures

elf-referred women undergo a telephone interview toetermine eligibility and complete a brief questionnaire onegistration. Two-view mammography is conducted with noadiologist on site; and films mounted on an alternatingulti-viewer are interpreted in batches.Work-ups of screen detected abnormalities are conducted

t various diagnostic facilities. Once the referral is made, theiagnostic radiologist coordinates and supervises all imagingtudies.

A recent innovation, “fast-track,” or “facilitated referral”llows family doctors to designate a diagnostic facility oracilities of choice. Under this policy, abnormal screening

xams are forwarded directly to diagnostic facilities. Staff

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84 L.J. Warren Burhenne, A.J. Coldman, and L. Kan

hen contact women directly to arrange for diagnostic work-p. This policy has been shown to reduce the time to diag-osis from 23 to 6 days if a biopsy is not required.The results of diagnostic studies are collected either

hrough the Ministry of Health data bank or directly fromhysicians. Diagnostic follow-up information is thus avail-ble for analysis on 95.5% of women with abnormal screen-ng mammograms. Most of the remaining 4.5% were onomen who did not consent to the release of diagnostic

nformation for data analysis.Data are analyzed at Head Office and for annual and other

eportings. Early results have been published in 1992,10 latern 1995,11 and the 10-year study in 2000.12

articipationetween 1997 and 2002, overall participation increased from3% to 49%. However, the goal of the program is to ensure0% participation.A total of 234,890 examinations were provided in the year

002, and 1,090,623 were performed between 1998 and002. Thirty-five percent of all women attending are 40 to 49ears old, 32% are 50 to 59 years, and 19.6% are age 60 to 69

able 1 Histological Features of Breast Cancers Detected by

40-49 50-59

umber of exams 386,185 336,81835.4% 30.9

umber of cancers 730 133416.1% 29.5

bnormal call rate 7.6% 7.1on first screens 12.2% 12.7on subsequent screens 5.6% 5.8ancer Detection Rate (per

1000)1.9 4.0

on first screens 2.5 5.7on subsequent screens 1.6 3.5CIS Detection Rate (per

1000)0.6 1.1

ositive predictive value ofscreening mammography

2.6% 5.8

iopsy yield ratio 22.0% 36.1Benign:malignant 3.5:1 1.8:1

interval cancer rate (per1000)

to 12 months 0.59 0.8on first screens 0.48 0.6on subsequent screens 0.64 0.9

3 to 24 months 0.39 1.0ensitivity (ie, 1 - false

negative rate)�76.0% 82.3

pecificity (ie, 1 - falsepositive rate)�

92.6% 93.1

otes:NM staging was determined by using mammographic measuremen

by assuming N0 whenever nodes were not assessed, and M0 uargets: >50% invasive tumors <15 mm; <30% invasive tumors w

ears old (Table 1). (

erformancendicators: Cumulative0-Year Age Group Data

he cumulative abnormal call rate is 7.0% and varies littlemong the age decades from 7.6% in the 40s to 6.7% in the0s.By contrast, the cancer detection rate is 4.2 per 1000 over-

ll, and rates range from 1.9 per 1000 in the 40s to 7.8 per000 in the 80s. The biopsy yield ratio is 39% overall, and

ncreases from 22% in the 40s to 61% in the 80s. These lattererformance indicators are related to prior probability. How-ver, overall 16% of all cancers are detected in women inheir 40s and 29.5% for women in their 50s (Table 2).

Sensitivity and specificity have remained relatively stableith time. Between 1998 and 2001, sensitivity ranged from5% to 86%, specificity from 94% to 93% (Table 1).

iagnostic Proceduresn the year 2002, 88% of women with abnormal results had aiagnostic mammogram, 49% ultrasound, 7% fine needlespiration, 5% core biopsy, and 19% surgical biopsy

C Years: Cumulative To and Including 2001

e at Exam

All60-69 70-79 80�

221,670 137,021 7018 1,090,62320.3% 12.6% 0.6%

1357 1049 55 452730.0% 23.2% 1.2%

6.4% 5.9% 6.7% 7.0%11.6% 11.3% 11.0% 12.1%5.4% 5.0% 5.1% 5.5%6.1 7.7 7.8 4.2

9.3 12.8 12.1 5.35.5 6.8 6.3 3.81.4 1.6 1.0 1.0

10.1% 13.8% 13.0% 6.3%

48.9% 57.8% 60.6% 38.6%1.0:1 0.7:1 0.7:1 1.6:1

0.66 0.77 0.35 0.700.59 0.79 0.59 0.570.67 0.76 0.25 0.751.10 1.26 1.74 0.87

90.1% 90.8% 95.6% 85.3%

94.1% 94.8% 94.0% 93.3%

never pathologic measurement of the tumor was not available, andtherwise informed.itive nodes; >30% grade 3 tumors <15 mm.

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umulativeancer Characteristics

uring the 14 years from 1988 to 2002, 6812 cancers wereetected, 23% of which were DCIS, the remainder invasive.he prevalence to expected incidence ratio for women aged0 to 70 years was also stable through the 1998-2001 timeeriod, ranging from 3.2 to 4.0.For histologic features of detected cancers, complete cu-ulative data are available up until 2001 (Table 4).Pertinent results include: (1) Cancers staged 0 � 1,

0%; invasive cancers with positive lymph nodes, 19%;nvasive lesions less than 15 mm, 65%, and lesions gradeII and less than 15 mm, 50%; and (2) median tumor size,3 mm. All of these results exceed internationally recom-ended targets.

able 2 SMPBC Outcome Indicators by 10-Year Age Group Y

<40 40-49

umber of exams 339 83,161 70.1% 35.4%

umber of first screens 293 20,6390.9% 60.9%

umber of cancers 1 1620.1% 15.9%

bnormal call rate 6.2% 7.5%on first screens 6.1% 12.8%on subsequent screens 6.5% 5.8%verall cancer detection rate

(per 1000)2.9 1.9

on first screens 3.4 2.5on subsequent screens 0.0 1.8CIS detection rate (per 1000) 0.0 0.6ositive predictive value of

screening mammography5.0% 2.7%

iopsy yield ratio - 25.5%Benign:Malignant - 2.9:1

otes:ut of 15,953 cases called ôabnormal,ö there were 17 lobular carcin

is still to be determined.verall cancer includes ductal carcinoma in situ (DCIS).ee glossary in the Appendix for definitions of terms.

able 3 Diagnostic Procedures Received by SMPBC Particip

Procedure <40 40-49

iagnostic mammogram 80% 88%ltrasound 40% 50%ine needle aspiration 5% 6%ore biopsy 5% 4%urgical biopsy 10% 8%with localization 10% 7%umber of cases* 20 6009

Diagnostic assessment information available.

rogram Costshe current cost per screen for 2002 is Cdn $56; US $41. Thereatest proportion, $30 Cdn is attributable to operatingosts; $10 to central services. The cost per screen detectedancer is $13,264 Cdn (Table 5).13

ecurrence and Survivaln 1999, we performed a comparison of prognostic factorsnd disease-free survival between women with cancer whottended the Screening Program and those who did not. Pro-ram attenders had more favorable outcomes than nonat-enders. The 7-year survival for program attenders was 83%s compared with 69% for nonattenders.14

002)

ge at Exam

All9 60-69 70-79 80�

46,800 28,990 1257 234,890.7% 19.9% 12.3% 0.5%

3278 1316 200 33,871.0% 9.7% 3.9% 0.6%

315 227 12 1019.6% 30.9% 22.3% 1.2%.8% 6.2% 5.7% 7.0% 6.8%.0% 13.8% 13.3% 11.5% 13.1%.9% 5.6% 5.3% 6.1% 5.7%.1 6.7 7.8 9.5 4.3

.6 13.4 13.7 5.0 4.8

.9 6.2 7.6 10.4 4.3

.9 1.5 1.6 0.8 1.0

.2% 11.2% 14.4% 14.5% 6.6%

.2% 51.1% 60.1% 50.0% 41.4%1 1.0:1 0.7:1 1.0:1 1.4:1

situ cases and 589 outcomes unknown. The final number of cancers

ith “Abnormal” Screening Mammograms Year: 2002

ge at Exam

All60-69 70-79 80�

89% 89% 94% 88%48% 47% 47% 49%7% 8% 10% 7%6% 7% 7% 5%

15% 17% 19% 11%13% 15% 17% 10%

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86 L.J. Warren Burhenne, A.J. Coldman, and L. Kan

nique Program Featurestandardized Interpretation Test

ince 1989, the Program has had in place a standardizednterpretation test for radiologist screening candidates.

Acceptable sensitivity and specificity performance is re-uired, and these criteria are based on the distribution of resultsor the group of incumbent screeners. Those who do not achieveatisfactory performance are advised to take additional trainingnd are required to pass the test before they can begin screening.

ocumentation of Individualesults and Standardized Ratiosach screener is presented with an annual confidential reportackage which includes volume statistics, outcome indica-ors, graphs of selected statistics for all screeners, a personalist of screen detected cancers, as well as postscreen cancersiagnosed within 36 months of the preceding screen.In 2000, Standardized Detection Ratios, including the Stan-

ardized Abnormal Call Ratio (SACR) and Standard Cancer De-ection Ratio (SCDR), were developed.15 These ratios are used to

able 4 Histologic Features of Breast Cancers Detected by S

40-49 50-59

umber of cancers 147 276in situ 40 27% 78 28%invasive 107 73% 198 72%umber of invasive cancers

with staging information88 162

NM stagingI 48 55% 102 63%II 39 44% 49 30%III� 1 1% 10 6%(no. unknown) (0) (1)

nvasive tumor size<5 mm 7 8% 15 9%6-10 mm 19 22% 39 24%11-15 mm 21 24% 44 27%16-20 mm 14 16% 27 17%>20 mm 27 31% 36 22%(no. unknown) (0) (1)<15 mm 47 53% 98 60%median tumour size 15 mm 14 mmode involvementno nodes sampled 0 0% 8 5%no 60 68% 112 69%yes 28 32% 42 26%(no. unknown) (0) (0)istologic grade1: well differentiated 31 36% 66 42%2: moderately

differentiated36 41% 62 39%

3: poorly differentiated 20 23% 30 19%(no. unknown) (1) (4)grade 3 tumor <15 mm 9 45% 19 63%

argets: >50% invasive tumors <15 mm <30% invasive tumors wi

ompare individual reader performance with the standard per- N

ormance after adjusting for age and screening history. A mini-um of 2500 interpretations per year were associated with

ower abnormal interpretation rates and average or better canceretection rates. This criterion has been accepted as the mini-um annual volume for program screeners.

nterval Cancer Review Processhis review process has been in operation since 1989 and in-olves both blind and retrospective reviews to document, clas-ify, and analyze interval cancers. In the original context, theefinition of interval cancers for our Program included “all can-ers detected within twelve months of a normal screening mam-ogram.” The new protocol for reminders at 2-year intervals foromen over age 50 has now been integrated. Interval cancers

an be accurately documented in British Columbia as all breastancers must be registered with the BC Cancer Registry. TheMPBC obtains monthly listings of all newly diagnosed breastancers from the BC Cancer Registry.

The program developed a simple classification after reviewf the scientific literature: (1) True Interval Cancers: Thosehich are not visible in the blind review process; (2) False

Year: 2001

ge at Exam

Age 40�0-69 70-79 80�

263 213 10 90922% 45 21% 1 10% 222 24%78% 168 79% 9 90% 687 76%

144 108 5 507

66% 67 63% 2 50% 314 62%29% 22 21% 2 50% 153 30%5% 5 5% 0 0% 23 5%

(1) (1) (4)

10% 9 8% 0 0% 45 9%26% 29 27% 0 0% 124 25%31% 38 35% 0 0% 147 29%13% 20 19% 3 75% 82 16%21% 12 11% 1 25% 106 21%

(0) (1) (3)66% 76 70% 0 0% 316 63%

2 mm 12 mm 18.5 mm 13 mm

9% 15 14% 2 40% 38 7%75% 74 69% 2 40% 356 70%16% 19 18% 1 20% 113 22%

(0) (0) (0)

44% 48 45% 1 25% 209 42%41% 43 40% 2 50% 201 40%

15% 16 15% 1 25% 89 18%(1) (1) (8)

50% 9 56% 0 48 54%

tive nodes >30% grade 3 tumors <15 mm.

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Screening mammography program of British Columbia 87

r more of the review team; and (3) Technical Interval Can-ers are those due to errors in positioning and exposure.

The classification review scheme involves an independentlind review by each of 3 experienced screeners conductedonthly. The 100 case series includes 10 to 20 interval can-

ers. Joint reviews are held 4 to 6 times per year to allowonfirmation and correlation of any questionable calls atlind reviews as well as providing a forum for analysis of

nterval cancers diagnosed after a longer delay.

ecent Results10-year analysis documented 513 twelve-month interval

ancers in 794,000 screening examinations.16 The 12-monthnterval cancer rate from 1992 to 1997 varied from 0.5 to 0.7er 1000 and is currently 0.6. During this project period, theensitivity varied from 84% to 86%, and specificity from 93%o 94%. A total of 40% of interval cancers were in the Falseegative category, the remaining 60% were True. A very

mall proportion are classified as due to technical errors. Ofhe cancers which could be seen in retrospect, the majority79%) were observed by 1 or 2 of the screening team, theemainder by all 3.

The current analysis has revealed that breast density isssociated with higher interval cancer rates in all age groups,nd that interval cancer rates and prognostic factors do notary with age.

For screening programs or studies with recommended-year screening intervals, the SMPBC interval cancer rate of.6 per 1000 compares favorably with 0.78 for the Breastancer Detection Demonstration Project17 and 0.92 for theealth Insurance Plan of New York study.1 Interval cancer

able 5 Cost Comparison by Fiscal Year

1997/98 1998/99

umber of screens 175,916 202,352umber of cancers

detected734 892

otal cost $8,228,305 $9,486,600otal cost/screen $46.77 $46.88Central services $9.40 $9.51Other operating costs $29.23 $27.98Professional reading

fee$5.88 $6.08

Capital allocation $2.27 $3.31ost per cancer

detected$11,210 $10,635

umbers of cancers detected in 2002/2003 and cost per cancer ishe cost per screen in 2002/2003 includes $0.99 retroactive paym

payments of 6.2% of the reading fee for the period April 1-Oct2001-March 31, 2002)

otal cost includes amortization of capital assets purchased througapital Allocation includes: (1) capital differential allocated to p

amortization of equipment purchased through BCCA; does nohospitals.

rofessional reading fee was $8 per screen prior to December 2000,

ates must be carefully compared with other studies with c

imilar intervals as the interval cancer rates are documentedo increase exponentially after 6 months.

Interval cancer rates as expressed in this context clearlyomprise a very small proportion of diagnosed cancers asompared with the screen-detected cancer volume. However,hat is very important to screeners is that it is possible, basedn the review process, to establish the proportion of false-egative interval cancers for each individual screener. A lowroportion of false-negative cancers could confer a high ef-ective sensitivity, and the converse: if all interval cancers or aarge proportion of them were deemed to be false negatives,his would confer a less favorable effective sensitivity. There-ore, such specific information can be very helpful to screen-rs who may need to improve their interpretive skills.

ummaryhe focus of the original Pilot Project was to establish quality

ndicators and operate at low cost. These goals have beeneached.

The subsequent objective results have shown that quality sus-ained in the service can result in improved prognosis, recur-ence, and survival rates for women attending for screening.

A review of the estimated age standardized breast cancerortality rate (per 100,000 population) for 1996 and 2000

hows that, in British Columbia, mortality was 2518 and is now3,19 and is the lowest in Canada for provinces of similar size.Tabar and coworkers have shown in 2001 that in Sweden

t was possible to reduce mortality by 63% for women aged0 to 69 who attended for screening.20

The Screening Mammography Program of British Colum-ia aspires to such favorable results, which if realized, wouldean nearly 400 fewer deaths per year as the result of breast

/2000 2000/2001 2001/2002 2002/2003

19,994 224,917 225,064 232,951884 827 966 1000

99,642 $11,358,867 $12,335,692 $13,262,184$46.82 $50.50 $54.81 $56.93$9.88 $9.35 $9.84 $9.61

$28.45 $29.17 $30.41 $30.82$6.12 $9.36 $12.00 $13.39

$2.37 $2.62 $2.56 $2.1311,651 $13,735 $12,770 $13,264

ted, because the final number of cancers is not determined yet.professional fee increase for the fiscal year 2001/02 (Lump sum

1, 2001 and 11.6% of the reading fee for the period November 1,

A (2001/2002: $278,019, 2002/2003: $230,363).administered centres in their annual operating budget and (2)

de capital expenditures capitalized and amortized through host

fective December 2000, and $13.39 per screen effective April 2002.

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88 L.J. Warren Burhenne, A.J. Coldman, and L. Kan

However, although the British Columbia Program is mod-led in many ways after the successful Two County study inweden, the remarkable compliance to screening which waschieved in Sweden has not yet been realized here. Efforts tochieve this goal will be the focus of our work in the comingecade.

eferences1. Shaprio S, Strax P: Evidence of screening for breast cancer from a

Randomized trial. Cancer 39:2772-2782, 1987 (suppl 6)2. Shaprio S, Strax P, Venet L, et al: Changes in five year breast cancer

Mortality in a breast screening program, in 7th National Cancer Con-ference Proceedings. Philadelphia, PA, American Cancer Society, 1973,pp 653-678

3. Tabar L, Gad A, Holmberg LH, et al: Reduction in mortality from breastcancer after mass screening with mammography: randomized trial fromthe Breast Screening Workshop Group of the Swedish National Boardof Health and Welfare. Lancet 1:829-832, 1985

4. Day NE, Chamberlain J: Screening for breast cancer: workshop report.Eur J Cancer Clin Oncol 24:55-59, 1988

5. Moskowtiz M: Costs of screening for breast cancer. Radiol Clin NorthAm 25:1031-1037, 1987

6. Sickles EA, Weber W, Glavin HB, et al: Mammographic Screening: howto operate successfully at low cost. Radiology 160:95-97, 1986

7. Sickles EA: Impact of low cost mammography screening on nearbymammography practices. Radiology 168:59-61, 1988

8. Bird RE, McLelland R: How to initiate and operate a low cost screeningmammography centre. Radiology 161:43-47, 1986

9. Bird RE: Low cost screening mammography: report on finances andreview of 21,716 consecutive cases. Radiology 171:87-90, 1989

0. Warren Burhenne LJ, Hislop TG, Burhenne HJ: The British Columbia

mammography screening program: evaluation of the first 15 months.AJR Am J Roentgenol 58:45-49, 1992

1. Warren Burhenne LJ, Burhenne HJ, Kan L: Quality-oriented massmammography screening. Radiology 194:185-188, 1995

2. Olivotto IA, Kan L, d’Yachkova Y, et al: Ten years of breast screening inthe Screening Mammography Program of British Columbia, 1988-97.J Med Screen 7:152-159, 2000

3. Screening Mammography Program of British Columbia: Annual Report6-20, 2002/2003

4. Olivotto IA, Mates D, Kan L, et al: Prognosis, treatment, and recurrenceof breast cancer for women attending or not attending the ScreeningMammography Program of British Columbia. Breast Cancer Res Treat54:73-81, 1999

5. Kan L, Olivotto IA, Warren Burhenne LJ, et al: Standardized abnormalInterpretation and cancer detection ratios to assess reading volume andreader performance in a breast screening program. Radiology 215:563-567, 2000

6. Warren Burhenne L, Kan L, Olivotto I: A new analysis of intervalcancers in the screening mammography program of British Columbia(SMPBC) based on five year age groupings. Radiology 215(P):315,2000

7. Seidman H, Gelb SK, Silverberg E, et al: Survival experience in theBreast Cancer Detection Demonstration Project. CA Cancer J Clin 37:258-290, 1987

8. Canadian Cancer Society, National Cancer Institute of Canada, Statis-tics Canada, Provincial/Territorial Cancer Registries, Health Canada.Canadian Cancer Statistics 1986, p 24

9. Canadian Cancer Society, national Cancer Institute of Canada, Statis-tics Canada, Provincial/Territorial Cancer Registries, Health Canada.Canadian Cancer Statistics 2002, p 29

0. Tabar L, Vitak B, Chen HHT, et al: Beyond randomized controlled

trials. Cancer 91:1724-1731, 2001