The management of early breast carcinoma before and after the introduction of clinical practice guidelines

The Management of Early Breast Carcinoma beforeand after the Introduction of Clinical PracticeGuidelines

Victoria White, Ph.D.1

Myee Pruden, Dip.Rad1

Graham Giles, Ph.D.2

John Collins, M.B.B.S.3

Konrad Jamrozik, D.Phil.4,5

Graeme Inglis, M.Appl.Sc. (Stats)1

John Boyages, Ph.D.6

David Hill, Ph.D.1

1 Centre for Behavioural Research in Cancer, TheCancer Council Victoria, Carlton, Victoria, Australia.

2 Cancer Epidemiology Centre, The Cancer CouncilVictoria, Carlton, Victoria. Australia.

3 Department of Surgery, Royal Melbourne Hospi-tal, University of Melbourne, Melbourne, Victoria,Australia.

4 Centre for Primary Care and Social Medicine,ICSM Charing Cross Campus, London, United King-dom.

5 Department of Public Health, University of West-ern Australia, Perth, Western Australia.

6 New South Wales Breast Cancer Institute, West-mead Hospital, Sydney, New South Wales, Austra-lia.

Funded through research grants from the NationalBreast Cancer Foundation and by the VictorianHealth Promotion Foundation (VicHealth). The Na-tional Breast Cancer Centre funded the 1995study.

Address for reprints: Victoria White, Ph.D., Centrefor Behavioural Research in Cancer, Cancer Con-trol Research Institute, The Cancer Council Victo-ria, 1 Rathdowne Street, Carlton, Victoria 3053Australia; Fax: (011) 61-3-9635 5380; E-mail:[email protected]

Received March 2, 2004; revision received April23, 2004; accepted May 3, 2004.

BACKGROUND. Clinical practice guidelines for the management of breast carci-

noma were introduced in Australia in October, 1995. This article describes the

management of early-stage breast carcinoma both before and after the introduc-

tion of these guidelines.

METHODS. All cases of early breast carcinoma that were diagnosed over the same

6-month period in 1995 and 1999 and registered with a state-based cancer registry

were identified. Treating surgeons completed a survey assessing tumor character-

istics and primary treatment. In 1995, 95% of 188 surgeons who were approached

participated and 96% of the surveys were returned. In 1999, 92% of 159 surgeons

who were approached participated and 91% of the surveys were returned. Analyses

are based on 1066 cases from 1995 and 1001 cases from 1999.

RESULTS. The pathologic disease stage of the patients was similar in both study

years. The proportion of patients who underwent breast-conserving therapy (BCT)

increased from 54% in 1995 to 69% in 1999. This increase was noted across most

levels of disease characteristics but was not evident among those patients treated

by the least active surgeons. The proportion of patients treated with BCT who

received radiotherapy increased from 59% in 1995 to 80% in 1999. This trend was

observed across most levels of tumor characteristics and surgeon caseload. The

proportion of women with receptor-positive tumors who were treated with endo-

crine therapy increased, whereas the proportion of patients with receptor-negative

tumors who received this therapy decreased from 39% in 1995 to 17% in 1999.

CONCLUSIONS. The management of early breast carcinoma in the state of Victoria

appeared to change between 1995 and 1999 in the direction expected if the

national guidelines had been incorporated into the practice patterns of surgeons

treating breast carcinoma patients. Cancer 2004;101:476 – 85.

© 2004 American Cancer Society.

KEYWORDS: breast, clinical practice guidelines, management, population-based.

Evidence-based clinical practice guidelines (CPGs) are advocated asa way to ensure that patients receive treatment based on the best

available evidence and that this will improve health outcomes.1 InAustralia, guidelines for the management of early breast carcinomawere first released in October 19952 and disseminated to all relevantclinicians (surgeons, medical and radiation oncologists) and profes-sional groups. Approximately 80% of surgeons working in the areawere aware of the guidelines within 1 year after their release and themajority believed that the guidelines would improve the managementof breast carcinoma.3,4 A lay version of the guidelines also was pro-duced and disseminated.5

Because clinical practice guidelines can only improve patient care

476

© 2004 American Cancer SocietyDOI 10.1002/cncr.20401Published online 21 June 2004 in Wiley InterScience (www.interscience.wiley.com).

and health outcomes if they are incorporated intoclinicians’ usual practice, there is a need to determinethe extent to which this happens by examining clini-cians’ actual practice patterns. Although several stud-ies to date have examined the treatment women withbreast carcinoma received after publication ofCPGs,6 –9 to our knowledge most reports have not in-cluded a comparison of practice prior to the release ofthe guidelines or examined practice at a populationlevel. For example, Craft et al.6 examined the manage-ment practices for early breast carcinoma among 19specialists after the release of the Australian CPGs.Only 46% of cases were treated with breast-conservingtherapy (BCT) and 98% of these women received ad-juvant radiotherapy. A much larger study that exam-ined the management of early breast carcinoma in theU.S. 2 years after the release of guidelines, suggestedthat the treatment of 80% of patients adhered to 16 of21 guidelines.9 However, because there were no dataregarding practice prior to the release of the guidelinesand because only 42% of the hospitals approachedparticipated in the study, it is not possible to deter-mine whether practice changed as a result of theguidelines’ release or whether uptake of the guidelineswas widespread. Ray-Coquard et al.8 conducted a pre-guidelines and post guidelines comparison of breastcarcinoma treatment in one center in France usinginformation from medical records and demonstratedthat a significantly greater proportion of patients weretreated according to guideline recommendations aftertheir introduction.

Surprisingly, because a surgeon’s breast carci-noma caseload has been found to predict the type oftreatment women with early breast carcinoma re-ceive10,11 and their survival,12,13 to our knowledge, therelation between surgeon caseload and the uptake ofCPGs has not been investigated to date. CPGs mightbe more likely to be incorporated into the practice ofsurgeons with small patient caseloads because theymight value the specification of treatment standards.Alternatively, surgeons with heavier caseloads mightbe more likely to incorporate the CPGs into their rou-tine care because they might be more familiar with theliterature on which the guidelines are based.

In the current study, we analyzed data from twosurveys (one before and one after the release of CPGs)to determine the extent to which women in one Aus-tralian state (Victoria) were being treated according tothe best available evidence. Unlike previous surveys,we adopted a population-based approach and usedthe state-based central cancer registry to identify allcases of early breast carcinoma diagnosed over a6-month period. We then surveyed the treating sur-geon (identified from the cancer registry) concerning

the management of each patient. This approach al-lowed us to include inpatients treated at differentinstitutions, and thereby measure the impact of CPGson the entire community.

The CPGs, which were released in Australia in1995, made a number of clear recommendations,which are shown in Table 1. In this article, we focus ondetermining changes in the proportion of patientstreated according to the following guidelines: 1) theuse of BCT; 2) the inclusion of radiotherapy in womenundergoing BCT; 3) including endocrine therapy inthe treatment of women; and 4) using chemotherapyand endocrine therapy in the treatment of women age� 50 years. Although to our knowledge the 1995 CPGscontained no specific guidelines regarding investiga-tions to be conducted to obtain a preoperative diag-nosis, they do recommend that more that one diag-nostic modality be used and indicate that thecombination of clinical examination, mammography,ultrasonography, and fine-needle aspiration providethe highest diagnostic accuracy. In the current study,we investigated the use of these diagnostic modalitiesin 1995 and 1999.

MATERIALS AND METHODSProcedureThe study years were 1995 and 1999. Methods of iden-tifying cases and ascertaining management were thesame in both surveys. All cases of early invasive breastcarcinoma (UICC pathologic Stage 0, I, or II tumors)diagnosed between April 1 and September 30 andregistered with the Victorian Cancer Registry (VCR)were identified. Women presenting with more thanone breast tumor during the study period and thosewho did not undergo surgery as their primary therapywere excluded from the study. Questionnaires werecompleted retrospectively of the woman’s treatment.For each patient, the relevant surgeon was identifiedand sent a questionnaire assessing treatment for thatpatient. Only data recorded in this surgeon’s question-naire are reported here. Completed questionnaireswere returned to VCR, at which point all identifyinginformation was removed. Surgeons who had not re-turned their questionnaire within 2 months were con-tacted and offered assistance from a data manager ifthey were unable to complete their questionnaires.In those cases where this offer was accepted, thedata manager extracted information regarding thepatient’s treatment from the surgeon’s records. Signif-icantly more surgeons completed questionnaires inthe 1995 survey (73%) than in the 1999 survey (52%)(chi-square test (df � 2) � 99; P � 0.01). However, inboth survey years the reported disease characteristicsfor women whose surveys were completed by the

Management of Early Breast Ca/White et al. 477

treating surgeon or another person (e.g., data manageror surgical registrar) did not differ. Ethical approval forboth studies was obtained from the appropriate insti-tutional ethics committees.

QuestionnairesThe questionnaire was based on survey instrumentsused previously.10,14,15 Using a closed-item format, thequestionnaires assessed menopausal status; referralsource; preoperative investigations; clinical character-istics of the tumor (size, location, lymph node involve-ment, etc); type of definitive surgery; reasons for thechoice of surgical therapy; pathologic tumor staging;hormone receptor status; referral to a radiation and/ormedical oncologist; and the use of radiotherapy, che-motherapy, and hormonal therapy.

Morphologic tumor type using International Clas-sification of Diseases for Oncology (second revision)tumor codes, histologic grade, hormone receptor sta-tus, lymph node involvement, laterality, and previousbreast carcinoma history were obtained from the pa-thology report available through the VCR and added tothe data file by the study manager.

Statistical AnalysisWe used the chi-square test to examine differences inproportions and constructed multivariate logistic re-gression models to establish the independent associ-ations between various factors and the use of BCT andthe use of local radiotherapy to the breast after BCT.When examining associations between different treat-ment modalities and characteristics of the women andthe tumor, standard errors were adjusted for cluster-ing of cases by treating surgeon. Caseload was deter-mined by calculating the number of newly diagnosedcases of early breast carcinoma in our data set thatwere treated by each surgeon. To determine the an-nual caseload, this number was doubled. Because thisestimate uses information only from returned surveys,the caseload may be underestimated if surgeons didnot return questionnaires for patients treated duringthe study period or if they were absent from clinicalpractice for any time during the study period. How-ever, given the high response to the survey, any un-derestimation is likely to be small and should not biasthe findings of the study.

Response and Sample Characteristics—1995For the 1995 sample, data concerning all 1316 breastcarcinoma incident tumors registered during the6-month study period were collected. Completed sur-veys were returned for 1261 cases, giving a response of96%. Of these tumors, 88% were classified as “early”breast carcinoma (pathologic Stage I, Stage IIA, and

TABLE 1Summary of Clinical Practice Guidelines, 1995

GuidelinesLevel ofevidence✦

Counselling and support1. Appropriate counselling has the potential to improve quality of life. II*Multidisciplinary support2. *The survival of patients with breast and other cancers is better if they

are treated by a specialist who also treats a large number of similarpatients, and who has access to the full range of treatment options in amultidisciplinary setting.

II*

Surgery for invasive breast cancer3. †Surgical treatment of cancers detected by mammographic screening is

beneficial.II

4. †Total mastectomy and either axillary dissection or axillary radiotherapyachieves results similar to those achieved by the Halsted radicalmastectomy.

II

5. There is no difference in the rate of survival or distant metastasisbetween women having mastectomy and those having breast conservingsurgery where appropriate.

II*

6. †Not all women with nodal disease on axillary sampling develop clinicallymph node metastases.

II

Radiotherapy7. †Survival rates are not decreased by delaying radiotherapy to the axilla,

although local control is less likely.II

8. Radiotherapy after lumpectomy significantly reduces the risk of localrecurrence.

II*

9. The omission of radiotherapy, even in carefully selected patients, leadsto an increased risk of local recurrence.

II*

10. †Overall, the routine addition of radiotherapy to surgery causes nosignificant change in mortality in the first 10 years, but an excess latemortality.

I

11. †The excess in cardiac deaths is offset by a reduction in breast cancerdeaths in recent trials.

I

12. †In older studies which no longer apply, there is a nonsignificantincrease in late cardiac deaths in women who have had adjuvantradiotherapy.

I

13. †There is a nonsignificant increase in the probability of a secondmalignancy in women who have had adjuvant radiotherapy. When site-specific associations are excluded, this risk becomes negligible.

II

Systemic adjuvant therapy14. *Tamoxifen, multiagent chemotherapy and ovarian ablation all reduce

annual risk of recurrence and death after treatment for women under 50with node-positive and node-negative breast cancer.

I

15. *Optimal dose intensity is important to outcome in adjuvantchemotherapy.

II

16. Cytotoxic regimens of several months duration are more effective thanthose lasting one month.

I

17. *A three month anthracycline-based regimen may be equivalent to sixmonths of CMF.

II*

18. *Tamoxifen significantly improves recurrence free survival at all ages. I19. Tamoxifen reduces the incidence of contralateral breast cancer. I20. *Side effects of tamoxifen include endometrial cancer, hot flushes and

vaginal dryness and discharge, but not excessive weight gain.II

21. †Women with ER-negative tumors have a poorer prognosis than thosewith ER-positive tumors.

II

Follow-up22. Intensive follow-up confers no survival benefit over a minimalist

schedule.II

* Changed in 1999 Guidelines.† Omitted in 1999 Guidelines.

✦Level of evidence is as follows:

I: evidence obtained from systematic reviews.

II: evidence from at least one properly designed randomized controlled trial.

Reprinted from: National Health and Medical Research Council. Clinical practice guidelines for the

management of early breast cancer. Canberra, Australian Capital Territory, Australia: Australian Gov-

ernment Publishing Service, 1995. Rescinded March 2003 (after publication of 2nd edition, 2001).

Copyright Commonwealth of Australia, reproduced by permission.

478 CANCER August 1, 2004 / Volume 101 / Number 3

Stage IIB). One hundred seventy-nine of the 188 sur-geons approached (95%) returned the questionnaires.

We omitted from analysis 14 women with bilateralbreast carcinoma and 13 women age � 90 years, leav-ing 1066 cases.

Response and Sample Characteristics—1999For the 1999 study, 1181 cases of early breast carci-noma (excluding bilateral tumors) were registeredover the 6-month study period, and 96% (n � 1134)had identifiable treating surgeons. Completed surveyswere returned for 1031 cases, for a coverage of 91%.The 1134 patients were treated by 159 surgeons, 146 ofwhom (92%) returned questionnaires. Twenty-fourpatients did not undergo surgery as their primary ther-apy and 6 patients were age � 90 years. These patientswere excluded, resulting in a final sample of 1001patients.

CaseloadIn 1995, 63% of the surgeons surveyed treated between1–9 cases of breast carcinoma each year, 21% treatedbetween 10 –19 cases, 10% treated between 20 –39cases, and 6% treated � 40 cases each year. The pro-portions had changed little by 1999, with 63% of sur-geons treating 1–9 cases of breast carcinoma, 19%treating 10 –19 cases, 9% treating 2039 cases, and 9%treating � 40 cases of breast carcinoma each year.

RESULTSTable 2 shows for each survey year the distribution ofcases by patient characteristics (age, place of resi-dence), the tumor (site, size, clinical and pathologicstage, lymph node involvement), detection throughthe national screening program, and surgeon case-load. Although the tumor site was similar, tumorsappeared to be smaller in 1999 compared with 1995(chi-square test (df � 1) � 8.7; P � 0.01). Women in1999 were younger (chi-square test (df � 3) � 15.53; P� 0.01) and more likely to reside in metropolitan areas(chi-square test (df � 1) � 5.66; P � 0.05) than in 1995.The proportion of cases diagnosed through the na-tional breast cancer screening program increasedfrom 32% in 1995 to 38% in 1999 (chi-square test (df �1) � 6.1; P � 0.05). Surgeons managing � 40 cases peryear treated nearly half of the cases (48%) in 1999,compared with approximately one-third (35%) in 1995(chi-square test (df � 3) � 35.56; P � 0.01).

Investigations Conducted before Definitive DiagnosisThe proportion of women undergoing the recom-mended individual investigations increased between1995 and 1999 (Table 3). For example, more womenwere undergoing fine-needle aspiration cytology

(FNAC) as part of their diagnostic workup in 1999(84%) compared with 1995 (72%) (chi-square test (df� 1) � 9; P � 0.01). Although more women in 1999(77%) were undergoing mammography and FNAC incombination as part of their diagnostic work-up com-pared with women in 1995 (72%), this difference wasnot found to be significant. Fewer women underwentinvestigations that tested for advanced disease in 1999compared with 1995. For example, the proportion ofpatients undergoing bone scans fell from 34% to 21%(chi-square test � 6; P � 0.05). Overall, the average

TABLE 2Characteristics of Women, Tumors, and Treating Surgeons in the1995 and 1999 Studies

% of patientsa

Effect of yearP value1995 1999

Sample size (no.) (1066) (1001)Age (yrs)� 50 22 2650–59 27 2760–69 24 2570� 29 22 � 0.01UICC Clinical stageI 76 76II 18 18 NSTumor dimension (cm)� 1 24 22� 1 to � 2 37 432 13 11� 2 25 24 � 0.05Axillary lymph node invasionYes 9 7 NSPathology stageI 66 63II 33 37 NSTumor siteUpper outer 52 53Upper inner 11 12Lower outer 11 11Lower inner 6 6Central 14 12Other 7 5 NSDisease detected through national screening programb

Yes 32 38 � 0.05Patient’s place of residenceMetropolitan 73 78 � 0.05Surgeon’s annual activity level1–9 patients 23 1910–19 patients 24 1820–39 patients 18 1640� patients 35 48 � 0.01

NS: not significant; UICC: International Union Against Cancer.a Percentage of valid patient responses.b Free public sector mammography screening service for women age � 40 years (only women age � 50

years were actively recruited)


number of preoperative investigations did not appearto change between survey years.

Surgical Treatment in 1995 and 1999Table 4 shows that significantly more women withearly breast carcinoma were managed with BCT in1999 (69%) compared with 1995 (54%). This increasewas evident regardless of the woman’s age, whetherthe tumor was detected at a screening center, andacross nearly all levels of disease characteristics, butwas not apparent among surgeons who treated fewerthan 10 new patients per year (chi-square test (df � 1)� 0.07; P � 0.79). However, the association betweensurgeon caseload and BCT changed between 1995 and1999. In 1995, surgeon caseload was not found to besignificantly associated with BCT, whereas in 1999women treated by surgeons seeing � 10 new cases ayear were more likely to receive BCT than thosetreated by less active surgeons. The multivariate anal-yses shown in Table 4 confirmed that, in both 1995and 1999, BCT was significantly less likely when tu-mors measured � 2 cm in size, when tumors werepathologic Stage II, and when women resided in rurallocations.

Surgeons were asked for the reasons behind the

surgeries performed. In both 1995 and 1999, themain reasons for choosing BCT were that the tumorwas small enough, the breast was large enough, andthe patient was keen to conserve the breast. In bothyears, the main reasons cited by surgeons who per-formed a mastectomy were the patient’s concernregarding the risk of recurrence and the tumor beinglarge.

Use of Adjuvant Radiotherapy in 1995 and 1999As can be seen in Table 5, more women managed withBCT in 1999 (80%) received radiotherapy than in 1995(59%), and this trend was observed across most levelsof tumor characteristics, patients’ characteristics, andsurgeon caseload. In the main, multivariate analysesdemonstrated that the factors associated with the useof radiotherapy after BCT in 1995 and 1999 were sim-ilar. For example, in both years, receiving radiotherapywas found to have an inverse association with age buta positive association with tumor size. Although in1995 there was no significant association noted be-tween pathologic stage and radiotherapy, by 1999 asignificant relation had emerged, such that womenwith pathologic Stage II tumors were 3 times morelikely to receive radiotherapy than those with Stage Itumors (odds ratio [OR] � 3.05; 95% confidence inter-val [95% CI], 1.63–5.72). In 1995, women residing inrural areas were significantly less likely to receive ra-diotherapy after BCT (OR � 0.54; 95% CI, 0.34 – 0.89).However, in 1999, women from rural areas were al-most as likely as women from metropolitan areas toreceive radiotherapy after BCT. Although in 1995,women being treated by surgeons with the highestcaseloads were least likely to receive radiotherapy af-ter BCT (OR � 0.32; 95% CI, 0.13– 0.82), by 1999 therewas no apparent significant association noted be-tween surgeon caseload and radiotherapy after BCT.

Use of Adjuvant Systemic Therapies in 1995 and 1999Table 6 shows changes in the use of endocrine therapyand chemotherapy between 1995 and 1999. The pro-portion of women with early breast carcinoma receiv-ing endocrine therapy increased from 62% in 1995 to73% in 1999 (chi-square test (df � 1) � 15.1; P � 0.01),largely because of the increase in the use of this treat-ment among women age � 50 who had estrogen re-ceptor (ER)-positive tumors. At the same time, therewas a sharp decrease in the use of such treatment forall women whose tumors were ER negative (39% in1995 and 17% in 1999; chi-square test (df � 1) � 17.3;P � 0.01).

There was a general increase in the proportion ofwomen with early breast carcinoma who were receiv-ing chemotherapy, from 26% in 1995 to 40% in 1999

TABLE 3Proportion of Early Breast Carcinoma Patients in 1995 and 1999 whoUnderwent Different Preoperative Investigations and the ProportionUndergoing the Preoperative Investigations Recommended in the1995 Clinical Practice Guidelines

1995% patients

1999% patients

Screening mammogram 36 43a

Diagnostic mammogram 56 53Ultrasound 21 48b

FNAC 72 84b

Needle/carbon surgical biopsy 13 9Incisional biopsy 8 5Excisional biopsy 20 13b

Full blood examination (CBC) 64 53Bone scan 34 21a

Chest X-ray 62 49Liver scan/ultrasound 11 11Liver function test 51 43Serum creatinine 41 39Serum calcium 26 22Recommended testsMammogram (diagnostic or screening) 86 90a

Needle biopsies 81 84a

Best practice (mammogram and FNAC) 72 77Average no. of tests 5.2 5.2

FNAC: fine-needle aspiration cytology.a P � 0.05.b P � 0.01.


(chi-square test (df � 1) � 35.8; P � 0.01), which wasfound to be greatest, in relative terms, among olderwomen with ER-negative tumors. More women hadtissue submitted for assays of hormone receptors in1999 (99%) than in 1995 (90%) (chi-square (df � 1)� 36.4,;P � 0.01).

Surgeon’s Practice by Caseload in 1995 and 1999Table 7 shows surgeons’ management practices for var-ious caseloads in 1995 and 1999. There was little changenoted with regard to the average number of prior inves-tigations conducted by surgeons with different caseloadsbetween 1995 and 1999. The proportion of cases in

TABLE 4Bivariate and Multivariate Association between Characteristics of the Patients, Tumors and the Treating Surgeons and BCT for Early BreastCarcinoma

Conservativesurgery,% of patients Effect

of yearP valuea

1995Multivariate resultsb

1999Multivariate resultsb

1995 1999 OR 95% CI OR 95% CI

Overall (no.) (1066) (1001) � 0.01% BCT 54 69Age (yrs)� 50 54 63 � 0.05 1 150–59 57 70 � 0.01 0.98 0.67–1.43 1.14 0.78–1.6660–69 52 71 � 0.01 0.83 0.55–1.24 0.92 0.60–1.4270� 55 69 � 0.01 1.00 0.67–1.51 1.22 0.75–2.00UICC Clinical stageI 60 74 � 0.01 1 1II 36 50 � 0.05 1.13 0.72–1.78 1.00 0.57–1.77Tumor dimension (cm)� 1 71 74 NS 1 1� 1 to � 2 61 79 � 0.01 0.69 0.47–1.01 1.66 1.05–2.612 58 65 NS 0.72 0.42–1.22 0.91 0.53–1.58� 2 31 48 � 0.01 0.27 0.17–0.42 0.55 0.30–0.99Axillary lymph node involvementYes 28 48 � 0.01 1 1No 57 70 � 0.01 1.98 1.09–3.61 1.85 0.96–3.58Pathology stageI 62 76 � 0.01 1 1II 40 56 � 0.01 0.61 0.44–0.85 0.62 0.43–0.91Tumor siteUpper outer 60 72 � 0.01 1 1Upper inner 53 80 � 0.01 0.67 0.46–0.98 1.82 1.00–3.28Lower outer 55 63 NS 0.89 0.59–1.36 0.71 0.43–1.17Lower inner 64 72 NS 1.37 0.75–2.49 1.03 0.49–2.16Central 37 53 � 0.05 0.47 0.30–0.75 0.42 0.29–0.60Other 39 53 NS 0.43 0.25–0.73 0.58 0.34–0.99Disease detected through National Screening Programc

Yes 61 78 � 0.01 1 1No 52 63 � 0.01 0.92 0.62–1.37 0.68 0.46–1.01Patient’s place of residenceMetropolitan 59 72 � 0.01 1 1Rural 43 57 � 0.05 0.57 0.39–0.84 0.58 0.37–0.90Surgeon’s annual activity level1–9 patients 49 50 NS 1 110–19 patients 48 67 � 0.01 0.97 0.61–1.54 2.51 1.32–4.7820–39 patients 52 73 � 0.01 0.92 0.51–1.66 2.55 1.39–3.9740� patients 64 75 � 0.05 1.48 0.89–2.46 2.74 1.49–5.08

BCT: breast-conserving therapy; OR: odds ratio; 95% CI: 95% confidence interval; NS: not significant; UICC: International Union Against Cancer.a P value was determined based on chi-square test.b Odds ratios were adjusted for all variables shown in the table.c Free public sector manmography screening service for women age � 40 years (only women age � 50 years were actively recruited into the program.


which a radiation oncologist or a medical oncologist wasconsulted and the use of adjuvant chemotherapy in-creased among all levels of surgeon activity. The onlysignificant increase in the proportion of cases receivingendocrine therapy was found among patients treated bysurgeons with the heaviest caseloads of newly diagnosedcases (chi-square (df � 1) � 7.81; P � 0.01). In both

years, more active surgeons tended to enroll a largerproportion of patients into clinical trials, but this fractionhad increased in all strata of caseloads.

DISCUSSIONThere was high awareness of the CPGs for early breastcarcinoma noted among Australian surgeons working

TABLE 5Bivariate and Multivariate Associations between the Characteristics of the Patients, Tumors, and the Treating Surgeons and ReceivingRadiotherapy after BCT

Radiotherapyafter BCT% of patients Effect

of yearP valuea

1995 Multivariateresultsb

1999 Multivariateresultsb

1995 1999 OR 95% CI OR 95% CI

Overall (no.) (581) (683) � 0.01% receiving radiotherapy 59 80Age (yrs)� 50 74 91 � 0.05 1 150–59 65 92 � 0.01 0.71 0.41–1.23 0.92 0.54–1.5960–69 67 78 � 0.05 0.86 0.54–1.37 0.30 0.17–0.5570� 35 55 � 0.02 0.16 0.09–0.28 0.10 0.04–0.22UICC Clinical stageI 58 80 � 0.01 1 1II 69 83 � 0.05 1.38 0.62–3.09 0.41 0.15–1.11Tumor dimension (cm)� 1 49 64 � 0.01 1 1� 1 to � 2 61 84 � 0.01 1.84 1.13–3.93 2.33 1.30–4.172 69 86 � 0.03 2.45 1.14–5.26 3.05 1.26–7.35� 2 68 86 � 0.01 2.34 1.07–5.10 2.52 1.04–6.11Axillary lymph node involvementNo 59 80 � 0.01 1 1Yes 67 83 NS 1.16 0.34–3.93 1.53 0.32–7.29Pathology stageI 55 76 � 0.01 1 1II 72 90 � 0.01 1.62 0.96–2.76 3.05 1.63–5.72Tumor siteUpper outer 60 80 � 0.01 1 1Upper inner 65 82 NS 1.69 0.86–3.33 1.40 0.81–2.42Lower outer 50 79 � 0.01 0.69 0.40–1.17 0.73 0.35–1.53Lower inner 71 79 NS 1.82 0.75–4.38 1.12 0.41–3.05Central 55 77 � 0.05 0.79 0.39–1.59 1.11 0.62–1.97Other 52 83 � 0.04 0.58 0.23–1.47 1.02 0.38–2.75Disease detected through national screening programc

Yes 53 79 � 0.01 1 1No 63 80 � 0.01 0.93 0.54–1.61 0.56 0.34–0.94Patient’s place of residenceMetropolitan 61 81 � 0.01 1 1Rural 51 78 � 0.01 0.54 0.34–0.89 0.79 0.41–1.50Surgeon’s annual activity level1–9 patients 66 80 NS 1 110–19 patients 67 88 � 0.01 1.26 0.58–2.71 1.88 0.79–4.5120–39 patients 65 75 NS 0.70 0.26–1.87 0.50 0.21–1.1640� patients 49 79 � 0.03 0.32 0.13–0.82 0.65 0.20–2.15

BCT: breast-conserving therapy; OR: odds ratio; 95% CI: 95% confidence interval; NS: not significant; UICC: International Union Against Cancer.a P value determined by the chi-square test.b Odds ratios were adjusted for all the variables shown in the tables.c Free public sector mammography screening service for women age � 40 years (only women age � 50 years were actively recruited into the program).


in the area of breast carcinoma.3,4 Using the samemethods for case ascertainment and data collection,we compared the primary treatment of early breastcarcinoma in one State jurisdiction in Australia (Vic-toria) before and after the release of the CPGs. Similarto other studies in this area,6 –9 we found that after therelease of the CPGs, more women were being treatedwith BCT and more of these women received adjuvantradiotherapy. The use of adjuvant medical therapiesalso converged as the CPGs recommended.

Unlike other studies in this area,6 –9 we took apopulation-based approach and examined the treat-ment practices of surgeons working in all treatmentcenters across Victoria. The high participation by sur-

geons and the high coverage of patients in both sur-veys (� 90% for both) ensure that selection bias wasminimal and that the results can be taken as repre-senting practice patterns for all surgeons working inVictoria.

The 1995 CPGs recommended the use of mam-mography, either with or without ultrasound, and FNAcytology or core needle biopsy to confirm a diagnosisof breast carcinoma. We found that the proportion ofpatients undergoing FNA cytology increased from 72%in 1995 to 84% in 1999, with a corresponding decreasein both excisional and incisional biopsies. We alsofound that the proportion of women undergoing amammogram as part of their preoperative investiga-

TABLE 6Adjuvant Systemic Therapy Related to ER Status, Age, and Year.

ER positive status% patients

ER negative status% patients

Total% patients

1995 1999 P valuea 1995 1999 P valuea 1995 1999 P valuea

All womenReceived endocrine therapyb 69 90 � 0.01 39 17 � 0.01 62 73 � 0.01Received adjuvant chemotherapyc 25 33 � 0.01 39 67 � 0.01 26 40 � 0.01Women age � 50 yrsReceived endocrine therapyb 29 81 � 0.01 18 5 NS 25 61 � 0.01Received adjuvant chemotherapyc 56 65 NS 65 89 � 0.01 57 72 � 0.01Women age � 50 yrsReceived endocrine therapyb 79 92 � 0.01 47 22 � 0.01 72 78 NSReceived adjuvant chemotherapyc 17 22 � 0.05 32 56 � 0.01 17 29 � 0.01

ER: estrogen receptor; NS: not significant.a P value was determined using the chi-square test.b In both 1999 and 1995 tamoxifen was the endocrine therapy of choice (96% of patients receiving endocrine therapy received tamoxifen).c In both 1995 and 1999, the most common chemotherapy regimens used were cyclophosphamide, methotrexate, and 5-fluorouracil (40%); doxorubicin/epirubicin and cyclophosphamide (33%), or a combination

of both regimens (15%).

TABLE 7Management of Operable Breast Carcinoma Based on the Surgeon’s Activity Level (% of patients in each year)

No. of patients per annum (% in each year)

1–9 patients 10–19 patients 20–39 patients 40� patients

1995 1999 1995 1999 1995 1999 1995 1999

Mean no. of prior investigations 4.7 5.2 5.3 4.9a 5.5 5.1 5.4 5.3Radiation oncologist consulted 49 52 46 69b 41 64b 38 68b

Medical oncologist consulted 58 68b 48 65b 36 59b 40 51b

Received chemotherapyc 26 42b 26 42b 25 37b 26 39b

Received endocrine therapyd 59 70a 65 68 60 72a 63 77b

Entered into clinical trial 2 3 2 6 5 8 7 8

a P � 0.05.b P � 0.01.c In both 1995 and 1999, the most common chemotherapy regimens used were cyclophosphamide, methotrexate, and 5-fluorouracil (40%); doxorubicin/epirubicin and cyclophosphamide (33%); or a combination

of both regimens (15%).d In both 1995 and 1999, tamoxifen was the endocrine therapy of choice (96% of patients who received endocrine therapy received tamoxifen.


tions increased only slightly from 86% to 90%, largelybecause of the rise in the proportion of cases beingdetected by screening mammogram. Although thenumber of women undergoing the recommended in-vestigations increased, the average number of preop-erative investigations per woman did not appear tochange between 1995 and 1999. This suggests that theincrease in the number of women undergoing therecommended investigations coincided with a de-crease in the number of women having tests designedto detect “occult” metastases. However, in 1999, 53%of women with early disease were still undergoing fullblood examinations, 49% were undergoing chest X-rays, and slightly greater than 40% were undergoingliver function tests. These tests have a low diagnosticyield and the guidelines recommend their use onlywhen clinically indicated. Their use should be mini-mal in the case of early breast carcinoma, except thatsurgeons may perceive that anesthesiologists will in-sist on full blood examinations and chest X-rays.

In 1999, 69% of patients with early breast carci-noma were treated with BCT. This was a significantincrease from the 54% of patients in Victoria under-going BCT in 1995 and was higher than the rate of 46%found in a smaller Australian study in 1997–1998.6 Italso is a significant increase from the rate of BCTfound for Victorian women with breast carcinoma in1990 (44%)10 and 1986 (22%),14 indicating a continuedincreasing trend toward using this treatment optionamong both surgeons treating breast carcinoma andthe women with breast carcinoma. We noted also thatthe proportion of patients receiving BCT in Victoria in1995 was higher than that reported for women in theU.S. in 1994 (42%), 2 years after guidelines were re-leased.9 The increase in the proportion of womenreceiving BCT in Victoria was found regardless of thewoman’s age, tumor pathologic stage, where the tu-mor was detected (screening center or not), and wherethe woman lived (urban or rural). However, womenfrom rural areas were still less likely to be treated withBCT than were women from metropolitan areas in1999. In 1999, rural women undergoing BCT were aslikely to receive radiotherapy as women from metro-politan regions, suggesting that access to radiotherapyfacilities is an unlikely reason for the significantlyhigher use of mastectomy among these rural women.This conclusion is supported by surgeons’ responsesto a separate question asking why women were treatedwith mastectomy. Distance to a radiotherapy centerwas only indicated as an issue for 4% of cases.

To our knowledge, the current study is the first toexamine whether caseload influenced surgeons’ up-take of CPGs. The results suggest that, for the mostpart, the recommendations contained in the guide-

lines were incorporated into the practice patterns ofall surgeons, regardless of caseload. The exception tothis was the use of BCT and consulting with radiationoncologists among surgeons seeing fewer than 10 newcases of breast carcinoma per year. This was the onlygroup of surgeons in which the proportion of patientstreated with BCT did not increase between 1995 and1999 and, perhaps correspondingly, in which therehad not been an increase in the proportion of cases inwhich a radiation oncologist was consulted. The rea-sons for the lack of change in the use of BCT amongthis group of surgeons require further investigation. Incontrast to these results for surgeons with the lowestcaseload, surgeons with the highest caseloads in-creased the proportion of patients treated with BCT,increased their consultations with radiation oncolo-gists, and correspondingly increased their use of ra-diotherapy among BCT patients. The results of thecurrent study suggest that CPGs can lead to improve-ments in the use of adjuvant therapies and breast-conserving surgery, particularly among surgeons withheavier breast carcinoma caseloads. Although theseresults might suggest that CPGs are less effective atchanging the clinical practice of surgeons with thelowest annual breast cancer caseloads, we note thatthese surgeons were more likely to consult with amedical oncologist and to use adjuvant chemotherapyand endocrine therapy in 1999 than in 1995. We be-lieve the current study’s results indicate that CPGsmay be effective in promoting at least some changesto the clinical practice of all surgeons working in thearea of breast cancer.

Between 1995 and 1999, there was an increase inthe proportion of women with early breast carcinomawho were receiving radiotherapy after BCT. This in-crease was in accordance with CPGs and was foundfor patients living in both urban and rural regions,patients with pathologic Stage I and Stage II tumors,and regardless of whether the tumor was detected at ascreening center. It is important to note that, in 1999,there was no longer an apparent association betweensurgeon caseload and receiving radiotherapy afterBCT, largely because there was an increase in the useof this therapy among surgeons with the heaviest ca-seloads between 1995 and 1999. However, despite thisincrease, the proportion of patients treated with BCTwho were receiving radiotherapy in Victoria in 1999was less than that reported for American women withearly breast carcinoma in 1994,9 in which 86% ofwomen treated with BCT received adjuvant radiother-apy. Although the low response achieved by this U.S.study (only 42% of the hospitals approached partici-pated) suggests that this proportion may not be ashigh among the general population of breast carci-


noma patients, it does suggest that the practice ofVictorian surgeons with regard to the utilization ofradiotherapy after BCT could still improve.

Although the 1995 CPGs2 indicated that the effectof tamoxifen on recurrence-free and overall survivalwas greatest for women with ER-positive tumors, theyalso indicated that tamoxifen had a significant positivebenefit in women with ER-negative tumors. With thepublication of data from the Early Breast Cancer Tri-alists’ Collaborative Group in 199816 showing that themain benefit of tamoxifen was noted in women withER-positive tumors, recommendations regarding theuse of tamoxifen in the updated CPGs published in200117 became more specific for women with ER-pos-itive tumors. The pattern of practice with regard toprescribing endocrine therapy in 1999 anticipated thatchange and is likely to reflect the impact of the 1998publication. Over the study period, there was an over-all increase of 11% in the proportion of women receiv-ing endocrine therapy, but also evidence that endo-crine therapy was used more appropriately in 1999than in 1995. Because the current study data suggestthat medical oncologists were more frequently in-volved in the management of early breast carcinomapatients in 1999 than in 1995, we speculate that themore routine involvement of medical oncologists mayhave led to these changes.

Overall, the current study shows that the manage-ment of early breast carcinoma in Victoria changedbetween 1995 and 1999 in the direction expected if thenational guidelines had been incorporated into thepractice of surgeons treating breast carcinoma. Ofcourse, because we did not have a control group ofsurgeons who did not receive the guidelines, we can-not conclude that the change in practice reportedherein was the direct outcome of the release of theCPGs. We note that the results of several reports ex-amining the use of adjuvant radiotherapy,18 chemo-therapy,19 and endocrine therapy16 in the manage-ment of breast carcinoma were published after therelease of the CPGs, and these publications would beexpected to have an impact on the way surgeons man-age breast carcinoma. Indeed, the findings of the cur-rent study regarding the decrease in the use of endo-crine therapy for ER-negative tumors providesevidence for this suggestion. However, because theresults of the current study are similar to those ofother studies examining the impact of guidelines onthe management of breast carcinoma, we suggest thatthe dissemination of guidelines is an effective meansof promoting the uptake of information regarding bestpractices for the management of breast carcinoma.

REFERENCES1. Smith T, Hillner B. Ensuring quality cancer care by the use

of clinical practice guidelines and critical pathways. J ClinOncol. 2001;19:2886 –2897.

2. National Health and Medical Research Council. Clinicalpractice guidelines for the management of early breast can-cer [rescinded in March 2003, after publication of the 2ndedition in 2001]. Canberra, Australian Capital Territory, Aus-tralia: Australian Government Publishing Service, 1995.

3. Carrick S, Bonevski B, Redman S, et al. Surgeons’ opinionsabout the NHMRC clinical practice guidelines for the manage-ment of early breast cancer. Med J Aust. 1998;169:300–305.

4. Ward J, Boyages J, Gupta L. Local impact of the NHMRCearly breast cancer guidelines: where to from here? Med JAust. 1997;167:362–365.

5. National Health and Medical Research Council. Early breastcancer: a consumer’s guide. Canberra, Australian CapitalTerritory, Australia: Australian Government Publishing Ser-vice, 1995.

6. Craft P, Zhang Y, Brogan J, et al. Implementing clinicalpractice guidelines: a community-based audit of breast can-cer treatment. Med J Aust. 2000;172:213–216.

7. Balasubramanian S, Murrow S, Holt S, et al. Audit of com-pliance to adjuvant chemotherapy and radiotherapy guide-lines in breast cancer in a cancer network. Breast. 2003;12:136 –141.

8. Ray-Coquard I, Phillip T, Lehmann M, et al. Impact of aclinical guidelines program for breast and colon cancer in aFrench cancer center. JAMA. 1997;278:1591–1595.

9. White J, Morrow M, Moughan J, et al. Compliance withbreast-conservation standards for patients with early-stagebreast carcinoma. Cancer. 2003;97:893–904.

10. Hill D, White V, Giles G, et al. Changes in the investigationand management of primary operable breast cancer in Vic-toria. Med J Aust. 1994;161:110 –122.

11. Taylor R, Stubbs J, Langlands A, et al. Predictors of mastec-tomy for women with breast cancer in greater western re-gion of Sydney. Breast J. 1999;5:116 –121.

12. Sainsbury R, Haward B, Rider L, et al. Influence of clinicianworkload and patterns of treatment on survival from breastcancer. Lancet. 1995;345:1265–1270.

13. Kingsmore D, Ssemwogerere A, Hole D, et al. Specialisationand breast cancer survival in the screening era. Br J Cancer.2003;88:1708 –1712.

14. Hill D, Giles G, Russell I, et al. Management of primary oper-able breast cancer in Victoria. Med J Aust. 1990;152:67–72.

15. Hill D, Jamrozik K, White V, et al. Surgical management ofbreast cancer in Australia in 1995. Sydney, New SouthWales, Australia: NHMRC National Breast Cancer Centre,1999.

16. Early Breast Cancer Trialists’ Collaborative Group. Tamox-ifen for early breast cancer: an overview of the randomisedtrials. Lancet. 1998;351:1451–1467.

17. National Breast Cancer Centre. Clinical practice guidelinesfor the management of early breast cancer. 2nd edition.Canberra, Australian Capital Territory, Australia: NationalHealth and Medical Research Council, 2001.

18. Peto R, Clarke M, Collins R, et al. Facts and figures from themeta-analyses in breast cancer. Eur J Cancer. 1998;34:S88.

19. Early Breast Cancer Trialists’ Collaborative Group. Polyche-motherapy for early breast cancer: an overview of random-ised trials. Lancet. 1998;352:930 –942.


Documents

The management of early breast carcinoma before and after the introduction of clinical practice guidelines