Breast Cancer Screening
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2 IARC Handbooks of Cancer Prevention Volume 7 Breast Cancer Screening
3 IARC Handbooks of Cancer Prevention Programme Head: Harri Vainio Volume 7: Breast Cancer Screening Editors: Technical editor: Bibliographic assistance: Photographic assistance: Layout: Printed by: Publisher: Harri Vainio, M.D., Ph.D. Franca Bianchini, Ph.D Elisabeth Heseltine, M.Sc. Agnes Meneghel Brigitte Kajo Georges Mollon/Pascale Rousson Josephine Thévenoux LIPS, Lyon, France larcpress International Agency for Research on Cancer 150 cours Albert Thomas, Lyon, France Tel Fax
4 WORLD HEALTH ORGANIZATION INTERNATIONAL AGENCY FOR RESEARCH ON CANCER IARC Handbooks of Cancer Prevention Volume 7 Breast Cancer Screening IARCPress Lyon, 2002
5 Published by the International Agency for Research on Cancer, 150 cours Albert Thomas, F Lyon cedex 08, France International Agency for Research on Cancer, 2002 Distributed by Oxford University Press, Walton Street, Oxford, 0X2 6DP, UK (Fax: i ) and in the USA by Oxford University Press, 2001 Evans Road, Carey, NC 27513, USA (Fax: ). All IARC publications can also be ordered directly from larcpress (Fax: i ; press@iarc.fr) and in the USA from larcpress, WHO Office, Suite 480, 1775 K Street, Washington DC, Publications of the World Health Organization enjoy copyright protection in accordance with the provisions of Protocol 2 of the Universal Copyright Convention. All rights reserved. The designations used and the presentation of the material in this publication do not imply the expression of any opinion whatsoever on the part of the Secretariat of the World Health Organization concerning the legal status of any country, territory, city, or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. The mention of specific companies or of certain manufacturers' products does not imply that they are endorsed or recommended by the World Health Organization in preference to others of a similar nature that are not mentioned. Errors and omissions excepted, the names of proprietary products are distinguished by initial capital letters. The authors alone are responsible for the views expressed in this publication. The International Agency for Research on Cancer welcomes requests for permission to reproduce or translate its publications, in part or in full. Applications and enquiries should be addressed to the Communications Unit, International Agency for Research on Cancer, which will be glad to provide the latest information on any changes made to the text, plans for new editions, and reprints and translations already available. IARC Library Cataloguing in Publication Data Breast Cancer Screening! IARC Working Group on the Evaluation of Cancer-Preventive Strategies (2002 : Lyon, France) (IARC handbooks of cancer prevention ; 7) 1. Breast Neoplasms - prevention & control 2. Mass Screening I, IARC Working Group on the Evaluation of Cancer-Preventive Strategies II. Series ISBN ISSN (NLM Classification: Wi) Printed in France
6 International Agency For Research On Cancer The International Agency for Research on Cancer (IARC) was established in 1965 by the World Health Assembly, as an independently financed organization within the framework of the World Health Organization. The headquarters of the Agency are in Lyon, France. The Agency conducts a programme of research concentrating particularly on the epidemiology of cancer and the study of potential carcinogens in the human environment. Its field studies are supplemented by biological and chemical research carried out in the Agency's laboratories in Lyon and, through collaborative research agreements, in national research institutions in many countries. The Agency also conducts a programme for the education and training of personnel for cancer research. The publications of the Agency contribute to the dissemination of authoritative information on different aspects of cancer research. Information about IARC publications, and how to order them, is available via the Internet at: This publication represents the views and opinions of an IARC Working Group on the Evaluation of Cancer-Preventive Strategies which met in Lyon, France, 5-12 March 2002 Participants and members of the secretariat: First row from left: T. Kuroishi, M. Blettner, F. Bianchini, M. Hakama, P. Dean, B. Armstrong, P. Pisani, S. Robles, J. Thévenoux. Middle row: E. Suonio, K. Straif, C. Partensky, S. Taplin, E. Heseltine, C. Baines, J. Hall, I. Andersson, G. Welsch, D. Thomas, N. Segnan, A. B. Miller, A. Kricker, H. Sancho-Gamier, S. Redman, L. NystrOm. Back row: H. Vainio, S. Narod, H. de Koning, A. Ullrich, J. Tyczynski, E. Weiderpass-Vainio, N. Day, L. Irwig. (Participants missing from photo: V. Beral, I. Ellis and R. Blanks)
7 Note to the Reader Anyone who is aware of published data that may influence any consideration in these Handbooks is encouraged to make the information available to the Unit of Chemoprevention, International Agency for Research on Cancer, 150 Cours Albert Thomas, Lyon Cedex 08, France Although all efforts are made to prepare the Handbooks as accurately as possible, mistakes may occur. Readers are requested to communicate any errors to the Unit of Chemoprevention, so that corrections can be reported in future volumes. Acknowledgements We would like to acknowledge generous support from the Foundation for Promotion of Cancer Research, Japan (2nd Term Comprehensive 10-Year Strategy for Cancer Control), and from the German Federal Ministry for Health.
8 Contents List of participants Preface 1. Breast cancer and screening The world-wide burden of breast cancer...1 Breast cancer biology, pathology and natural history as related to screening... 4 Barriers to understanding of early cancers... 5 Benign breast disease... 5 Carcinoma in situ... 6 Invasive carcinoma... 9 Can a patient be 'cured' of breast cancer '2 16 Diagnosis and treatment Screening for breast cancer: Conceptual considerations...17 General definitions Positive predictive value, specificity and the issue of over-diagnosis Cancers detected at screening, interval cancers and distribution of lead time and sojourn time Period screening: Length bias and the unbiased set A more complex view of cancer Evaluation of screening for breast cancer Screening techniques Screening mammography X-ray equipment Radiation dose Quality control Sensitivity and specificity Host factors that affect sensitivity One versus two views Double reading xi xiii Other and emerging imaging techniques Digital mammography Ultrasonography Magnetic resonance imaging Positron emission tomography Scintimammography Electrical impedance imaging Other techniques Clinical breast examination Technique Training Maintenance of standards Costs and potential harms Other issues Breast self-examination Technique Training Maintenance of standards Mechanisms for improving breast self-examination. 45 Costs and potential harms Other issues Use of breast cancer screening Delivery and uptake of screening Europe Americas...54 Oceania and Asia Behavioural factors and the longer-term success of screening Information and understanding Psychological consequences of participation in screening...74 Encouraging participation in screening vii
9 Table of contents 4. Efficacy of screening Methodological and analytical issues in assessing efficacy...87 Issues in evaluating the efficacy of screening. 87 Use of randomized controlled trials in evaluation of screening Use of cohort (observational) and case control studies in evaluating screening Efficacy of screening by conventional mammography Randomized trials...91 Cohort and nested case control studies Quasi-experimental study Efficacy of screening by clinical breast examination Efficacy of screening by breast selfexamination Randomized trials Cohort studies Case control studies Studies of survival Studies of extent of disease at diagnosis Efficacy of screening women at high risk Radiation sensitivity Tumour factors Family history BRCA1 and BRCA Magnetic resonance imaging Effectiveness of screening Has screening been implemented in accordance with the results of screening trials" Methods of invitation Screening processes Age range Screening interval Mammography Clinical breast examination Breast self examination Indicators for monitoring and evaluating the effectiveness of screening programmes Origins of indicators of effectiveness of screening. 122 Performance indicators Mortality from and screening for breast cancer in different countries Alternative measures of effect on mortality Balance between false-positive and false-negative results Conclusion Hazards (risks) of screening Occurrence and consequences of false-positive results in mammography Overdiagnosis Reservoir of potentially detectable breast cancer Ductal carcinoma in situ Early mortality from breast cancer Risk for breast cancer induced by radiation Cost effectiveness of population-based breast cancer screening Cost-effectiveness analysis: What and why? Published analyses Application of strict rules Elements of cost effectiveness Effectiveness Unfavourable effects Costs Discounting effects and costs Modelling for policy decisions Policy decisions on age categories to be screened 164 Policy decisions on screening interval Policy decisions on high-risk groups Policy decisions on recall or referral Participation Cost effectiveness in practice Quality of life Cost Cost effectiveness...168
10 Breast cancer and screening Limitations of cost effectiveness analysis Practical limitations Gaps in knowledge New developments Summary Breast cancer and screening World-wide burden Biology, pathology and natural history Conceptual considerations Screening techniques Screening mammography Other and emerging imaging techniques Clinical breast examination Breast self-examination Overall evaluation Effect of screening with mammography on mortality from breast cancer Influence of inter-screening interval on effect of screening by mammography Effect of breast screening by clinical breast examination on mortality from breast cancer Effect of breast screening by breast selfexamination on mortality from breast cancer Effectiveness in practice of breast cancer screening with mammography Adverse effects of breast screening Cost effectiveness of a programme of screening with mammography Implications for public health Recommendations Use of breast cancer screening Delivery and uptake of screening Behavioural considerations in screening participation Efficacy of screening Methodological and analytical issues in assessing efficacy Conventional screening mammography Clinical breast examination Breast self-examination Women at high-risk Effectiveness of population-based screening Implementation of population-based screening in accordance with results of screening trials Indicators of the effectiveness of population-based screening programmes Hazards of screening Research recommendations Improving conventional mammography Implementing mammographic screening programmes Accuracy of mammographic screening Clinical breast examination Breast self-examination Consequences of diagnosis of breast cancer Biology of breast tumours in relation to screening 184 New techniques Women at high risk Public health recommendations Information systems Implementation of mammographic screening programmes References Glossary Cost-effectiveness of population-based screening Working Procedures Evaluation Sources of figures Evaluation of the efficacy of breast cancer screening...179
11 List of participants I. Andersson Department of Diagnostic Radiology Malmö University Hospital Malmö Sweden B. Armstrong (Chairman) Edward Ford Building A27 University of Sydney Sydney NSW 2006 Australia C. Baines Department of Public Health Sciences University of Toronto Toronto Ontario M5S 1A8 Canada V. Beral Imperial Cancer Research Fund Cancer Epidemiology Unit University of Oxford Gibson Building Radcliffe Infirmary Oxford 0X2 6HE United Kingdom R. Blanks Institute of Cancer Research Royal Cancer Hospital Cancer Screening Evaluation Unit Sutton Surrey 5M2 5NG United Kingdom M. Blettner Department of Epidemiology and Medical Statistics School of Public Health Bielefeld Germany N. Day Strangeways Research Laboratory University of Cambridge Cambridge CB1 8RN United Kingdom R Dean Department of Diagnostic Radiology University of Turku Turku Finland N.J. de Koning Department of Public Health Erasmus University Rotterdam 3000 DR Rotterdam Netherlands I. Ellis Faculty of Medicine and Health Sciences Division of Histopathology Nottingham City Hospital NHS Trust Nottingham NG5 1 PB United Kingdom S. Fletcher* Harvard Medical School Harvard Pilgrim Health Care Boston Massachusetts USA M. Hakama (Vice-Chairman) University of Tampere School of Public Health Tampere Finland L. Irwig Screening and Test Evaluation Program (STEP) Department of Public Health and Community Medicine University of Sydney Sydney NSW 2006 Australia A. Kricker NHMRC National Breast Cancer Centre Kings Cross Sydney NSW Australia T. Kuroishi Division of Epidemiology & Prevention Aichi Cancer Center Research Institute Nagoya Japan A.B. Miller Division of Clinical Epidemiology German Cancer Research Center Heidelberg Germany *Unable to attend
12 IARC Handbooks of Cancer Prevention, Volume 7: Breast Cancer Screening S. Narod H. Sancho-Gamier The Centre for Research in Women's EPIDAURE Health Centre Val d'aurelle Toronto M5G 1N8 Parc Euromédicine Canada Montpellier France C. Nichols* Office of Science Planning and N. Segnan Assessment CPO Piemonte National Cancer Institute Cancer Prevention Centre Bethesda Unit of Epidemiology Maryland Torino USA Italy L. Nyström Department of Public Health and Clinical Medicine Unit of Epidemiology Umei University Umeâ Sweden S. Redman NHMRC National Breast Cancer Centre Kings Cross NSW Australia S. Robles Pan American Health Organization Regional Office of the World Health Organization HCP/HCN Washington DC USA S. Taplin Group Health Cooperative Center for Health Studies Seattle Washington USA D.B. Thomas Fred Hutchinson Cancer Research Center Seattle Washington USA H.G. Welch Department of Medicine and Community and Family Medicine Dartmouth Medical School Hanover New Hampshire USA Observer A. Ullrich WHO Geneva Switzerland Secretariat F. Bianchini J. Cheney J. Hall E. Heseltine (Lajarthe, St Léon-sur-Vézère, France) C. Partensky D.M. Parkin P. Pisani A. Sasco K. Straif L. Stayner E. Suonio J. Tyczynski H. Vainio E. Weiderpass-Vainio Technical assistance B. Kajo J. Mitchell C. Mogenet J. Thévenoux * Unable to attend xu
13 Preface Why a Handbook on breast cancer screening? The scientific process of acquiring information about the efficacy of breast cancer screening was initiated in 1963, when Sam Shapiro and coworkers introduced the Health Insurance Plan study (Shapiro etal., 1988a) in New York, USA, the first randomized controlled trial of the effect of mammography and clinical breast examination in reducing mortality from breast cancer. This study opened the era of randomized controlled trials for evaluation of screening techniques. Cancer screening techniques used before that, such as the Papanicolau (Pap) smear, never underwent proper evaluation in randomized trials before their introduction as a means for population screening. Randomized controlled trials have been criticized many times as expensive and slow to provide results. The Breast Cancer Detection Demonstration Project (Baker, 1982) in the USA was initiated to provide data on the efficacy of breast cancer screening rapidly, and the first results appeared in 1979, 3 years before publication of the results of the Health Insurance Plan study. Three more studies - in MalmO, Sweden (Andersson et al., 1988), Edinburgh, Scotland (Roberts et al., 1990) and in two Swedish counties (Tabár et al., 1985) - were initiated years after the beginning of the Health Insurance Plan study, and another three studies were initiated in , in Canada (Miller et al., 1 992a,b) and in Stockholm (Frisell et al., 1986) and Goteborg, Sweden (Bjurstam etal., 1997). Thus, a number of randomized controlled trials, initiated in five different countries over a 20-year period, provide the basis for evidence in the field of mammographic screening. Mammography was first officially introduced in a population-wide, organized screening programme in Iceland and in several districts in Sweden in The Netherlands and several regions of Canada followed in 1988, and Finland in In 1988, the American Cancer Society and the Preventive Services Task Force established policies in favour of screening for breast cancer in the USA (US Preventive Task Force, 1996). In contrast to the policies in other countries, that in the USA emphasized a triple approach, involving breast self-examination, clinical breast examination and mammography. The Europe Against Cancer programme simultaneously initiated a series of pilot screening programmes in several countries in Europe (Commission of the European Communities, 1996) in order to develop expertise in planning and running high-quality population-based screening programmes before their incorporation into national policy. In the early 1990s, national screening programmes were initiated in Australia and the United Kingdom, and these were followed by organized programmes in several states of the USA, in Israel and, later, in France. Germany and Switzerland were among the last western countries to join the international trend, with plans to introduce national screening at the beginning of the twentyfirst century. Experience in large-scale mammographic screening by the mid-1 990s, and the availability of data on more recent follow-up from the trials, led to discussion about the value of mammographic screening for women under the age of 50. Even on the basis of the same scientific evidence, few countries have established the same breast cancer screening policy. The policies differ with respect to the target age group to be screened, the frequency of screening, the number of mammographic views to be taken and the screening modalities. In Japan, the policy was based on clinical breast examination until recently, when it was decided to add mammography. In spite of the vast amount of information available from several randomized trials, some doubt has recently been cast on the value of breast cancer screening in reducing mortality from breast cancer (Gotzsche & Olsen, 2000; Olsen & Gotzsche, 2001). In this volume, the relevant published studies are thoroughly reassessed, together with the newest data, either recently published or in press, according to the procedures and guidelines followed in the Handbooks (see pp. 223)
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