Berry

De Koning

Gigerenzer

Horak

IARC

Jørgensen

Koscielny

Miller

Mittra

Okonkwo Lamberts

Otto

Parkin

Rijnsburger

Schopper

Woloshin

Koning, H.J. (Harry) de

Erasmus University Digital Repository

LETTER TO THE EDITORAre Low- and Middle-Income Countries Becoming theVictim of Western Debates About Breast Screening?To the Editor:Recently, two important initiatives took place tofurther increase quality of breast cancer (BC) screen-ing and treatment, also in other than high-incomecountries. In Batumi, Georgia, the 1st InternationalBlack Sea Conference on cervical and BC screeningwas held on 10th and 11th September 2009 withparticipants from Armenia, Azerbaijan, Bulgaria,Georgia, Moldova, Romania, Turkey, and Ukraine.By exchanging experiences, ideas and the scientificevidence available, plans to further improve imple-mentation of breast (and cervical) cancer screeningwere debated and formed.From 24–27 October 2009, the 15th Annual Multi-disciplinary Symposium on Breast Disease was held inCairo with a special summit on health care disparitiesin developing countries. With thousands of peoplerunning the ‘‘race for cure’’ at the Giza pyramids,around 600 participants at the symposium, the pres-ence of ambassador Nancy Brinker of the Susan GKoomen For The Cure and her interview for CNN,the importance of BC prevention got international andhigh profile attention again. Not least to say, due tothe excellent organization and programme directed byShahla Masood, the editor of The Breast Journal.The programme reflected nicely the integratedapproach in BC care: primary prevention, screeningand treatment, and palliative care, with excellentspeakers from high-, middle- and low-income coun-tries. However, the evidence on and fact sheet aboutBC screening seemed overwhelmed, again, by negativesounds, either called critical issues, challenges orcontroversies, as was aired recently again both on thisand the other side of the Atlantic (1–3).Screening has always been highly controversial,partly because the procedure is for seemingly healthypeople, for whom the benefit should be clear. Evi-dence of this benefit is, however, for the group as awhole. At the individual level, prediction of who willbenefit and who will suffer more harm than good isimpossible. The balance between favorable and unfa-vorable effects is delicate (4).Of course, it is not likely to involve large-scalemammography as a screening test in low-resourcescountries, but the debate about mammography screen-ing in Western countries seemed to question and leadto disbelief about the benefits of BC screening in gen-eral. That is simply wrong.Whether earlier detection and treatment of BCresult in health benefits was hypothesized in the 1960s(5). Large clinical series then showed that for womenextensively treated but with relatively large tumors thechance of distant metastases was significantly highereven 25 years after primary treatment (6). Horakshowed the biological concept of this: with growth ofthe tumor, angiogenesis increases with increasingchances of tumor spread to lymph nodes and beyond(7). Removal of the tumor before such critical pointsof angiogenesis might then mean a higher cure rate.Randomised controlled trials on mammographyscreening during 1960–1980 confirmed the benefits ofearlier detection and treatment by showing a 25%reduction in BC mortality in invited women aged 50and over compared to a control group (8). Also, inpractice, numerous case–control studies showed thatscreened women have a 30–40% reduced risk in dyingfrom the disease (9), although case–control studies ofscreening may be biased by the fact that womenwho have been screened may have been self-selected(showing a favorable outcome independent of screen-ing). This hampers standard evaluations when large-scale breast screen programmes are running, but weAddress correspondence and reprint requests to: Harry J. de Koning,MD, PhD, Professor of Screening Evaluation, Department of Public Health,Erasmus MC, University Medical Center Rotterdam, PO Box 2040, 3000 CARotterdam, the Netherlands, or e-mail: h.dekoning@erasmusmc.nl.DOI: 10.1111/j.1524-4741.2010.00926.xª 2010 Wiley Periodicals, Inc., 1075-122X/10The Breast Journal, Volume 16 Number 4, 2010 442–444elegantly showed that in the Netherlands the start ofscreening in the municipality changed the annualincrease in BC mortality from 0.3 per 100,000increase per year towards a 1.7 per 100,000 decreaseper year (10; Fig. 1). Model exercises showed thatroughly 50% of the decline in BC mortality in the USwas likely to be due to the mammography dissemina-tion between 1975 and 2000 (11).So, there should be no doubt that high quality mam-mography screening (followed by treatment of earlystage cancer) substantially reduces BC mortality in apopulation. Unfortunately, trials on teaching breast selfexamination have failed to show a beneficial effect onBC mortality (8). For low- and middle-income coun-tries clinical breast examination (CBE) may be anappropriate alternative to mammography. There isonly one randomised controlled trial reported, theCanadian National Breast Screening Study that invitedrandomised women for clinical breast exams per-formed by highly trained nurses and the other groupfor clinical breast exams and mammography (12).Since the trial did not have a control arm withoutscreening tests offered, one has to estimate to what thestages (and stage shift) produced by the clinical breastexams compares to. By detailed mathematical model-ing Rijnsburger estimated the CBEs might have pro-duced a 20.5% BC mortality difference compared to a(nonobserved) control situation without screening (13).In many middle-income countries BC incidence issteadily increasing due to aging of the population anda remarkable change in risk factors (14). At the sametime, BC is often diagnosed at a late stage. So itmeans that two prerequisites of considering screeningand earlier detection are met.Especially this worse clinical stage distributionmay be one of the main reasons why breast screen-ing, e.g., by clinical exams may still be cost-effectivein low-resource and low-incidence countries. Theshift attainable by screening may result in importantFigure 1. Relative rates of breast cancer by year since introduction of screening in municipalities for age groups 55–74 years in the Neth-erlands (Otto et al., Initiation of population-based mammography screening in Dutch municipalities and effect on breast-cancer mortality: asystematic review. Lancet 2003;361(9367):1411–17; reproduced with permission from Elsevier).Figure 2. Differential costs and effects of breast cancer screeningprograms, discounted at 3% per year (based on Okonkwo et al.,JNCI 2009). The dashed line indicates a cost-effectiveness ratio ofInt.$1000 per life year saved, and the solid line indicates the effi-cient frontier. The numbers refer to the programs in the originalpaper (Okonkwo et al., JNCI 2009).letter to the editor • 443health benefits, if high quality early treatment isavailable. For India, we found that screening byclinical breast exams every 2 years for women aged40–60 might lead to a 16.3% reduction in BC mor-tality at 6.6 million Int.$ cost (15). Although there isnot one guideline applicable to all countries, CBEscreening should seriously be considered in manycountries. Figure 2 shows the so-called efficient fron-tier of breast screen scenarios in India. It shows thatprogrammes with clinical breast exams are cost-effec-tive. This does not mean advising inferior technologyfor low-income countries; this means achievingimportant health benefits for the resources available.Of course, the mortality results in the running Indiatrial are eagerly awaited (16), but in the mean timepilot studies performing CBE screening could begradually implemented. Any new feasible technologyor policy changes could perhaps be built on that.Many steps have to be taken still, both in break-ing cultural barriers, in increasing knowledge andfighting misconceptions. There are unfortunatelynumerous misconceptions: some think the breast is avital organ and some think cancer is a contagiousdisease. There are cultural barriers, e.g., in the cos-tumes and clothing hiding any clear visible abnormal-ities, in the fear women will loose their husbandswhen loosing their breast and therefore income,women feeling not being a woman anymore and inpractical issues like transportation to a screening cen-ter as a woman. Unfortunately, also some health careproviders are still not equipped both physically norknowledgeable.It will be far from easy to start breast screening byclinical breast exams in low-resource countries. It willbe challenging to use the culture positively. Tailoredout-reach community services, one-stop clinics andemphasis on both public education and health careprofessionals education will be crucial to ‘‘win therace’’. These initiatives are crucial to pave the roads.And let developing countries not make the same mis-take to be confused and stopped in their progress byWestern debates about the benefits of breast screening.When you don’t know where you are going,every road will take you there (adapted from Alice inWonderland).Harry J. de Koning, MD, PhDDepartment of Public Health,Erasmus MC, University Medical Center Rotterdam,PO Box 2040, 3000 CA Rotterdam, the NetherlandsREFERENCES1. Jørgensen KJ, Gøtzsche PC. Overdiagnosis in publicly organ-ised mammography screening programmes: systematic review ofincidence trends. Br Med J 2009;339:b2587.2. Woloshin S, Schwartz LM. Numbers needed to decide [Edito-rial]. J Natl Cancer Inst 2009;101:1163–65.3. Gigerenzer G, Mata J, Frank M. Public knowledge of benefitsof breast and prostate cancer screening in Europe. J Natl CancerInst 2009;101:1216–20.4. de Koning HJ. Assessment of nationwide cancer-screeningprogrammes. Lancet 2000;355:80–1.5. Ingleby H, Gershon-Cohon J, eds. Comparative Anatomy,Pathology and Roentgenology of The Breast. Philadelphia: Univer-sity of Pennsylvania, 1960.6. Koscielny S, Tubiana M, Leˆ MG, et al. Breast cancer: rela-tionship between the size of the primary tumour and the probabilityof metastatic dissemination. Br J Cancer 1984;49:709–15.7. Horak ER, Leek R, Klenk N, et al. Angiogenesis, assessed byplatelet ⁄ endothelial cell adhesion molecule antibodies, as indicatorof node metastases and survival in breast cancer. Lancet1992;340:1120–24.8. IARC. Handbooks of Cancer Prevention. Vol. 7: Breast Can-cer Screening. Lyon, France: IARC, 2002, p. 248.9. Schopper D, de Wolf C. How effective are breast cancerscreening programmes by mammography? Review of the current evi-dence. Eur J Cancer 2009;45:1916–23.10. Otto SJ, Fracheboud J, Looman CW, et al. Initiation of pop-ulation-based mammography screening in Dutch municipalities andeffect on breast-cancer mortality: a systematic review. Lancet2003;361:1411–17.11. Berry DA, Inoue L, Shen Y, et al. Modeling the impact oftreatment and screening on U.S. breast cancer mortality: a Bayesianapproach. J Natl Cancer Inst Monogr 2006;36:30–6.12. Miller AB, To T, Baines CJ, Wall C. Canadian NationalBreast Screening Study-2: 13-year results of a randomized trial inwomen age 50–59 years. J Natl Cancer Inst 2000;92:1490–99.13. Rijnsburger AJ, van Oortmarssen GJ, Boer R, et al.Mammography benefit in the Canadian National Breast ScreeningStudy-2: a model evaluation. Int J Cancer 2004;110:756–62.14. Parkin DM, Sitas F, Chirenje M, Stein L, Abratt L, WabingaH. Part I: Cancer in Indigenous Africans—burden, distribution, andtrends. Lancet Oncol 2008;9:683–92.15. Okonkwo Lamberts Q, Draisma G, der Kinderen A, BrownM, de Koning HJ. Breast cancer screening policies in developingcountries: a cost-effectiveness analysis for India. J Natl Cancer Inst2008;100:1290–300.16. Mittra I, Baum M, Thornton H, Houghton J. Is clinicalbreast examination an acceptable alternative to mammographicscreening? Br Med J 2000;321:1071–73.444 • letter to the editor

Are low- and middle-income countries becoming the victim of Western debates about breast screening?

de Koning, Harry

EUR Research Repository

LETTER TO THE EDITORAre Low- and Middle-Income Countries Becoming theVictim of Western Debates About Breast Screening?To the Editor:Recently, two important initiatives took place tofurther increase quality of breast cancer (BC) screen-ing and treatment, also in other than high-incomecountries. In Batumi, Georgia, the 1st InternationalBlack Sea Conference on cervical and BC screeningwas held on 10th and 11th September 2009 withparticipants from Armenia, Azerbaijan, Bulgaria,Georgia, Moldova, Romania, Turkey, and Ukraine.By exchanging experiences, ideas and the scientificevidence available, plans to further improve imple-mentation of breast (and cervical) cancer screeningwere debated and formed.From 24–27 October 2009, the 15th Annual Multi-disciplinary Symposium on Breast Disease was held inCairo with a special summit on health care disparitiesin developing countries. With thousands of peoplerunning the ‘‘race for cure’’ at the Giza pyramids,around 600 participants at the symposium, the pres-ence of ambassador Nancy Brinker of the Susan GKoomen For The Cure and her interview for CNN,the importance of BC prevention got international andhigh profile attention again. Not least to say, due tothe excellent organization and programme directed byShahla Masood, the editor of The Breast Journal.The programme reflected nicely the integratedapproach in BC care: primary prevention, screeningand treatment, and palliative care, with excellentspeakers from high-, middle- and low-income coun-tries. However, the evidence on and fact sheet aboutBC screening seemed overwhelmed, again, by negativesounds, either called critical issues, challenges orcontroversies, as was aired recently again both on thisand the other side of the Atlantic (1–3).Screening has always been highly controversial,partly because the procedure is for seemingly healthypeople, for whom the benefit should be clear. Evi-dence of this benefit is, however, for the group as awhole. At the individual level, prediction of who willbenefit and who will suffer more harm than good isimpossible. The balance between favorable and unfa-vorable effects is delicate (4).Of course, it is not likely to involve large-scalemammography as a screening test in low-resourcescountries, but the debate about mammography screen-ing in Western countries seemed to question and leadto disbelief about the benefits of BC screening in gen-eral. That is simply wrong.Whether earlier detection and treatment of BCresult in health benefits was hypothesized in the 1960s(5). Large clinical series then showed that for womenextensively treated but with relatively large tumors thechance of distant metastases was significantly highereven 25 years after primary treatment (6). Horakshowed the biological concept of this: with growth ofthe tumor, angiogenesis increases with increasingchances of tumor spread to lymph nodes and beyond(7). Removal of the tumor before such critical pointsof angiogenesis might then mean a higher cure rate.Randomised controlled trials on mammographyscreening during 1960–1980 confirmed the benefits ofearlier detection and treatment by showing a 25%reduction in BC mortality in invited women aged 50and over compared to a control group (8). Also, inpractice, numerous case–control studies showed thatscreened women have a 30–40% reduced risk in dyingfrom the disease (9), although case–control studies ofscreening may be biased by the fact that womenwho have been screened may have been self-selected(showing a favorable outcome independent of screen-ing). This hampers standard evaluations when large-scale breast screen programmes are running, but weAddress correspondence and reprint requests to: Harry J. de Koning,MD, PhD, Professor of Screening Evaluation, Department of Public Health,Erasmus MC, University Medical Center Rotterdam, PO Box 2040, 3000 CARotterdam, the Netherlands, or e-mail: h.dekoning@erasmusmc.nl.DOI: 10.1111/j.1524-4741.2010.00926.xª 2010 Wiley Periodicals, Inc., 1075-122X/10The Breast Journal, Volume 16 Number 4, 2010 442–444elegantly showed that in the Netherlands the start ofscreening in the municipality changed the annualincrease in BC mortality from 0.3 per 100,000increase per year towards a 1.7 per 100,000 decreaseper year (10; Fig. 1). Model exercises showed thatroughly 50% of the decline in BC mortality in the USwas likely to be due to the mammography dissemina-tion between 1975 and 2000 (11).So, there should be no doubt that high quality mam-mography screening (followed by treatment of earlystage cancer) substantially reduces BC mortality in apopulation. Unfortunately, trials on teaching breast selfexamination have failed to show a beneficial effect onBC mortality (8). For low- and middle-income coun-tries clinical breast examination (CBE) may be anappropriate alternative to mammography. There isonly one randomised controlled trial reported, theCanadian National Breast Screening Study that invitedrandomised women for clinical breast exams per-formed by highly trained nurses and the other groupfor clinical breast exams and mammography (12).Since the trial did not have a control arm withoutscreening tests offered, one has to estimate to what thestages (and stage shift) produced by the clinical breastexams compares to. By detailed mathematical model-ing Rijnsburger estimated the CBEs might have pro-duced a 20.5% BC mortality difference compared to a(nonobserved) control situation without screening (13).In many middle-income countries BC incidence issteadily increasing due to aging of the population anda remarkable change in risk factors (14). At the sametime, BC is often diagnosed at a late stage. So itmeans that two prerequisites of considering screeningand earlier detection are met.Especially this worse clinical stage distributionmay be one of the main reasons why breast screen-ing, e.g., by clinical exams may still be cost-effectivein low-resource and low-incidence countries. Theshift attainable by screening may result in importantFigure 1. Relative rates of breast cancer by year since introduction of screening in municipalities for age groups 55–74 years in the Neth-erlands (Otto et al., Initiation of population-based mammography screening in Dutch municipalities and effect on breast-cancer mortality: asystematic review. Lancet 2003;361(9367):1411–17; reproduced with permission from Elsevier).Figure 2. Differential costs and effects of breast cancer screeningprograms, discounted at 3% per year (based on Okonkwo et al.,JNCI 2009). The dashed line indicates a cost-effectiveness ratio ofInt.$1000 per life year saved, and the solid line indicates the effi-cient frontier. The numbers refer to the programs in the originalpaper (Okonkwo et al., JNCI 2009).letter to the editor • 443health benefits, if high quality early treatment isavailable. For India, we found that screening byclinical breast exams every 2 years for women aged40–60 might lead to a 16.3% reduction in BC mor-tality at 6.6 million Int.$ cost (15). Although there isnot one guideline applicable to all countries, CBEscreening should seriously be considered in manycountries. Figure 2 shows the so-called efficient fron-tier of breast screen scenarios in India. It shows thatprogrammes with clinical breast exams are cost-effec-tive. This does not mean advising inferior technologyfor low-income countries; this means achievingimportant health benefits for the resources available.Of course, the mortality results in the running Indiatrial are eagerly awaited (16), but in the mean timepilot studies performing CBE screening could begradually implemented. Any new feasible technologyor policy changes could perhaps be built on that.Many steps have to be taken still, both in break-ing cultural barriers, in increasing knowledge andfighting misconceptions. There are unfortunatelynumerous misconceptions: some think the breast is avital organ and some think cancer is a contagiousdisease. There are cultural barriers, e.g., in the cos-tumes and clothing hiding any clear visible abnormal-ities, in the fear women will loose their husbandswhen loosing their breast and therefore income,women feeling not being a woman anymore and inpractical issues like transportation to a screening cen-ter as a woman. Unfortunately, also some health careproviders are still not equipped both physically norknowledgeable.It will be far from easy to start breast screening byclinical breast exams in low-resource countries. It willbe challenging to use the culture positively. Tailoredout-reach community services, one-stop clinics andemphasis on both public education and health careprofessionals education will be crucial to ‘‘win therace’’. These initiatives are crucial to pave the roads.And let developing countries not make the same mis-take to be confused and stopped in their progress byWestern debates about the benefits of breast screening.When you don’t know where you are going,every road will take you there (adapted from Alice inWonderland).Harry J. de Koning, MD, PhDDepartment of Public Health,Erasmus MC, University Medical Center Rotterdam,PO Box 2040, 3000 CA Rotterdam, the NetherlandsREFERENCES1. Jørgensen KJ, Gøtzsche PC. Overdiagnosis in publicly organ-ised mammography screening programmes: systematic review ofincidence trends. Br Med J 2009;339:b2587.2. Woloshin S, Schwartz LM. Numbers needed to decide [Edito-rial]. J Natl Cancer Inst 2009;101:1163–65.3. Gigerenzer G, Mata J, Frank M. Public knowledge of benefitsof breast and prostate cancer screening in Europe. J Natl CancerInst 2009;101:1216–20.4. de Koning HJ. Assessment of nationwide cancer-screeningprogrammes. Lancet 2000;355:80–1.5. Ingleby H, Gershon-Cohon J, eds. Comparative Anatomy,Pathology and Roentgenology of The Breast. Philadelphia: Univer-sity of Pennsylvania, 1960.6. Koscielny S, Tubiana M, Lê MG, et al. Breast cancer: rela-tionship between the size of the primary tumour and the probabilityof metastatic dissemination. Br J Cancer 1984;49:709–15.7. Horak ER, Leek R, Klenk N, et al. Angiogenesis, assessed byplatelet ⁄ endothelial cell adhesion molecule antibodies, as indicatorof node metastases and survival in breast cancer. Lancet1992;340:1120–24.8. IARC. Handbooks of Cancer Prevention. Vol. 7: Breast Can-cer Screening. Lyon, France: IARC, 2002, p. 248.9. Schopper D, de Wolf C. How effective are breast cancerscreening programmes by mammography? Review of the current evi-dence. Eur J Cancer 2009;45:1916–23.10. Otto SJ, Fracheboud J, Looman CW, et al. Initiation of pop-ulation-based mammography screening in Dutch municipalities andeffect on breast-cancer mortality: a systematic review. Lancet2003;361:1411–17.11. Berry DA, Inoue L, Shen Y, et al. Modeling the impact oftreatment and screening on U.S. breast cancer mortality: a Bayesianapproach. J Natl Cancer Inst Monogr 2006;36:30–6.12. Miller AB, To T, Baines CJ, Wall C. Canadian NationalBreast Screening Study-2: 13-year results of a randomized trial inwomen age 50–59 years. J Natl Cancer Inst 2000;92:1490–99.13. Rijnsburger AJ, van Oortmarssen GJ, Boer R, et al.Mammography benefit in the Canadian National Breast ScreeningStudy-2: a model evaluation. Int J Cancer 2004;110:756–62.14. Parkin DM, Sitas F, Chirenje M, Stein L, Abratt L, WabingaH. Part I: Cancer in Indigenous Africans—burden, distribution, andtrends. Lancet Oncol 2008;9:683–92.15. Okonkwo Lamberts Q, Draisma G, der Kinderen A, BrownM, de Koning HJ. Breast cancer screening policies in developingcountries: a cost-effectiveness analysis for India. J Natl Cancer Inst2008;100:1290–300.16. Mittra I, Baum M, Thornton H, Houghton J. Is clinicalbreast examination an acceptable alternative to mammographicscreening? Br Med J 2000;321:1071–73.444 • letter to the editor

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Are low- and middle-income countries becoming the victim of Western debates about breast screening?

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