BMJ                                 2011;                                                                  343:d6894                                                                  doi: 10.1136/bmj.d6894                                                                                                           (Published                                                                  25 October 2011)                                                                                                         Cite this as:                                                                                                            BMJ                                     2011;                                                                        343:d6894                                   

• Observations

• Breast Cancer Screening

The NHS breast screening programme needs independent reviewSusan Bewley, professor of complex obstetrics, Division of Women's Health, King's College Londonsusan.bewley@kcl.ac.ukThe BMJ has published several articles over the past few years raising concerns about the accuracy and transparency of information                                 provided to women about the benefits and harms of mammography screening for breast cancer (BMJ 2006;332:538, doi:10.1136/bmj.332.7540.538; 2009;338:b86, doi:10.1136/bmj.b86; 2010;340:c3106, doi:10.1136/bmj.c3106). Last month the professor of complex obstetrics Susan Bewley sent us for publication an open letter to England's cancer tsar. Here we publish the letter and Mike Richards's response (BMJ 2011;343:d6843, doi:10.1136/bmj.d6843)                              Dear MikePersonal reasons propelled me into the debate on breast cancer screening. As a house officer (in the early 1980s) working for two surgeons-one still performing "frozen section, query proceed to radical (Halsted) mastectomy" and the other promulgating the perceived heretical practice of breast conservation by lumpectomy-we dealt with what seemed an inevitably fatal disease. After my sister's discovery in 2006 of a malignant lump when in her mid-40s I was impressed by the intervening improvements in diagnosis, treatment, care, and prognosis, which were based on a continuing programme of research evidence. Approaching 50, with a family history of the cancer (grandmother, aunt, and sister) and risk factors (late childbearing, low parity, obesity), I had to consider screening mammography for myself. It is natural to fear cancer and its treatments and understandable to think "better safe than sorry"-that the promise of early detection could offer me a much better chance of life and health.I declined screening when it was offered, as the NHS breast screening programme was not telling the whole truth. As a non-expert                              in the subject, I found myself examining the evidence for breast screening with increasing doubts. I compared the NHS and                              Nordic Cochrane Centre leaflets1 and found that the NHS leaflets exaggerated benefits and did not spell out the risks.2 Journals showed a reputable and growing body of international opinion acknowledging that breast cancer screening was not                              as good as used to be thought. The distress of overdiagnosis and decision making when finding lesions that might (or might                              not) be cancer that might (or might not) require mutilating surgery is increasingly being exposed.3 The oft repeated statement that "1400 lives a year are saved" has not been subjected to proper scrutiny.4 Even cancer charities use lower estimates.5 I expressed my misgivings to you "behind the scenes" as a work colleague. You replied in a personal email "that the large majority of experts in this country disagrees with the methodology used in the Cochrane Centre reviews of breast screening."                           It is extraordinary to be told that methodology is contentious so many years into the national programme. Many people believe that "evidence based medicine" has rightly succeeded "eminence based medicine," so it was disappointing that such a senior, successful, and respected medical professional apparently disagreed with the open, highly defensible, peer reviewed Cochrane methodology without suggesting something better. That more people support one side of an argument does not make it right. Large groups of well educated, well intentioned, and kind people can be wrong. The fact that British experts see it one way holds no sway, as many do indeed support the Cochrane Centre's viewpoint.6 Experts simply disagreeing with the Nordic methodology is not enough: it is necessary to know what their expertise is, what their vested interests are (financial, academic, reputation, and so on), how they came to their conclusions, and why they disagreed. Your argument-that our (British) experts are better than their (Nordic) experts-is inadequate and unpersuasive.                           There is a science behind the numbers and a duty to debate the facts, question the assumptions, and agree-or at least explain systematically-where the areas of dispute and uncertainty lie. How information is delivered must be explicit so that the ethical imperative for women to come to a free and fully informed decision is supported. The usefulness of screening diminishes with development of better treatments. In recent decades, breast cancer treatments improved unambiguously, so the risk:benefit ratio of screening inevitably changed as the "window of opportunity" narrowed. Evidence questioning the purported size of the benefits of screening continues to accumulate. 7 8 9 10 11 12 It seems that the biology of breast cancer is not fully understood.13 14 15 Predictions of its behaviour from microscopic examination remain elusive. Earlier is not necessarily better: the increasing literature concerning overdiagnosis suggests that many "cancers" detected through screening have been revealed "too early" in their unpredictable lives. Surgery may even accelerate cancer.16 Fixed thinking also means that research opportunities and discoveries arising from new understandings will be delayed.                           Women should be reassured that the NHS treats breast cancer more successfully now, but screening is only of marginal benefit,                              at best. The medical profession needs to find ways to cope with the complex issues. Trust is at stake if the public is not                              told the full story. In the past few years British women have not been told about the genuine doubts. Those millions of women                              passing through the breast screening treadmill have been unaware of the problems, criticism, and real numerical risks they                              face. The new leaflet17 is still not good enough and contrasts with the excellent NHS screening information for men regarding prostate specific antigen                              testing.18 Whether for historical reasons, the NHS breast screening programme reports to you as cancer director. Accountability to the UK National Screening Committee might merit more professional confidence. It's uncomfortable to change set beliefs in the face of changing evidence but unforgivable not to. I am not convinced that you have challenged your experts competently and mercilessly, rather than hidden behind them.19 Thus I support the calls for an independent review of the evidence20 21-a real, unbiased review that will not be kicked into the long grass, whose findings will be widely and properly disseminated, and that will adjust screening policy appropriately and will lead to proper pursuit of the research implications.                           Next SectionNotesCite this as: BMJ 2011;343:d6894                              Previous Section References↵Nordic Cochrane Centre. Screening for breast cancer with mammography. www.cochrane.dk/screening/index-en.htm.                                       ↵Baum M, McCartney M, Thornton H, Vaidya JS, Barrat A, and 19 others. Breast cancer screening peril: negative consequences                                             of the breast cancer screening programme. Times2009 Feb 19..↵Prinjha S, Evans J, Ziebland S, McPherson A. "A mastectomy for something that wasn't even truly invasive cancer." Women's understandings of having a mastectomy for screen-detected DCIS: a qualitative study. J Med Screen2011;18:34-40.[Abstract/FREE Full text]↵Jørgensen KJ, Gøtzsche PC. Who evaluates public health programmes? A review of the NHS Breast Screening Programme. J R Soc Med2010;103:14-20.[FREE Full text]↵Cancer Research UK. Mammograms in breast screening. http://cancerhelp.cancerresearchuk.org/type/breast-cancer/about/screening/mammograms-in-breast-screening.                                       ↵Baum M, Thornton H, Gøtzsche C (on behalf of 24 others). Breast cancer awareness month: still awaiting screening facts (letter).                                             BMJ2010;341:c6152.[FREE Full text]↵Moss SM, Cuckle H, Evans A, Johns L, Waller M, Bobrow L. Effect of mammographic screening from age 40 years on breast cancer mortality at 10 years' follow-up: a randomised controlled trial. Lancet2006;368:2053-60.[CrossRef][Medline][Web of Science]↵Gøtzsche PC, Nielsen M. Screening for breast cancer with mammography. Cochrane Database Syst Rev2011;(1):CD001877.↵Kalager M, Zelen M, Langmark F, Adami HO. Effect of screening mammography on breast-cancer mortality in Norway. N Engl J Med2010;363:1203-10.[CrossRef][Medline]↵Welch HG. Screening mammography: a long run for a short slide? N Engl J Med2010;363:13.[CrossRef]↵Jørgensen KJ, Zahl PH, Gøtzsche PC. Breast cancer mortality in organised mammography screening in Denmark: comparative study.                                             BMJ2010;340:c1241.[Abstract/FREE Full text]↵Autier P, Boniol M, Gavin A, Vatten LJ. Breast cancer mortality in neighbouring European countries with different levels of                                             screening but similar access to treatment: trend analysis of WHO mortality database. BMJ2011;343:d4411.[Abstract/FREE Full text]↵Baum M, Chaplain MAJ, Anderson ARA, Douek M, Vaidya JS. Does breast cancer exist in a state of chaos? Eur J Cancer1999;35:886-91.[CrossRef][Medline][Web of Science]↵Baum M, Demicheli R, Hrushesky W, Retsky M. Does surgery unfavourably perturb the "natural history" of early breast cancer by accelerating the appearance of distant metastases? Eur J Cancer2005;41:508-15.[CrossRef][Medline][Web of Science]↵Retsky MW, Demicheli R, Hurshesky WJM, Baum M, Gukas ID. Dormancy and surgery-driven escape from dormancy help explain some                                             clinical features of breast cancer. APMIS2008;116:730-41.[CrossRef][Medline][Web of Science]↵Badwe RA, Vaidya JS. Haematogenous dissemination of prostate epithelial cells during surgery. Lancet1996;347:325-6.[Medline]↵NHS Cancer Screening Programmes. NHS breast screening. www.cancerscreening.nhs.uk/breastscreen/publications/nhsbsp.pdf.                                       ↵NHS Cancer Screening Programmes. PSA (prostate screening antigen) testing for prostate cancer: an information sheet for men                                          considering a PSA test. www.cancerscreening.nhs.uk/prostate/prostate-patient-info-sheet.pdf.                                       ↵Gøtzsche PC, Jørgensen KJ. The breast screening programme and misinforming the public. J R Soc Med2011;104:361-9.[Abstract/FREE Full text]↵McPherson K. Screening for breast cancer: balancing the debate. BMJ2010;340:c3106.[FREE Full text]↵Godlee F. Breast screening and other fights. BMJ2010;341:c4096.[FREE Full text]CiteULikeComploreConnoteaDeliciousDiggFacebookGoogle+MendeleyRedditStumbleUponTechnoratiTwitterWhat's this?Relevant Articles: Karsten Juhl Jørgensen, Peter C Gøtzsche[Extract][Full text][PDF][Further details]Peter C Gøtzsche, Ole J Hartling, Margrethe Nielsen, John Brodersen, Karsten Juhl Jørgensen[Extract][Full text][Supplementary material]Klim McPherson[Extract][Full text]Mike Richards[Extract][Full text][PDF]Nigel Hawkes[Extract][Full text][PDF]Analysis and Comment: Public health: Content of invitations for publicly funded screening mammography BMJ 2006;332:538-541 doi:10.1136/bmj.332.7540.538 (Published 2 March 2006)Analysis: Breast screening: the facts-or maybe not BMJ 2009;338:doi:10.1136/bmj.b86 (Published 27 January 2009)Analysis: Screening for breast cancer-balancing the debate BMJ 2010;340:doi:10.1136/bmj.c3106 (Published 24 June 2010)Observations: Breast Cancer Screening: An independent review is under way BMJ 2011;343:doi:10.1136/bmj.d6843 (Published 25 October 2011)News: Breast cancer screening is to be reviewed, cancer tsar announces BMJ 2011;343:doi:10.1136/bmj.d6905 (Published 26 October 2011)Relevant ArticlesResearch: Breast cancer mortality in neighbouring European countries with different levels of screening but similar access to treatment:                                       trend analysis of WHO mortality database Philippe Autier, Mathieu Boniol, Anna Gavin, Lars J Vatten BMJ 2011;343:doi:10.1136/bmj.d4411 (Published 28 July 2011)[Abstract][Full text][PDF]  Letter: Breast cancer awareness month: Still awaiting screening facts Michael Baum, Hazel Thornton, Peter C Gøtzsche, on behalf of Susan Bewley, Karsten Juhl Jørgensen, Alexandra Barratt, Nick Ross, Steven Woloshin, Lisa Schwartz, Toni Musiello,                                             Mitzi Blennerhassett, Maryann Napoli, Cornelia J Baines, Jayant S Vaidya, Norman Williams, Daphne Havercroft, Per-Henrik Zahl,                                             Michael Retsky, Robert M Kaplan, Mary Dixon-Woods Donald A Berry, Keith Isaacson, Diana Brahams, Miriam Pryke, Gillian Tindall,                                             David A Bender, Tom Marshall. BMJ 2010;341:doi:10.1136/bmj.c6152 (Published 2 November 2010)[Extract][Full text]Editor's Choice: Breast screening and other fights Fiona Godlee BMJ 2010;341:doi:10.1136/bmj.c4096 (Published 29 July 2010)[Extract][Full text]Research: Breast cancer mortality in organised mammography screening in Denmark: comparative study Karsten Juhl Jørgensen, Per-Henrik Zahl, Peter C Gøtzsche BMJ 2010;340:doi:10.1136/bmj.c1241 (Published 23 March 2010)[Abstract][Full text][PDF][Web Extra]  This Article

I'd like to learn more about an "innocuous" breast cancer.  What do you suppose that is?

Cathy

I don't understand the British stuff.  "Earlier is not necessarily better."  I think early detection is always good.  Do doctors ever tell their patients, "I'm sorry, we caught your breast cancer too early"?  And "Surgery may even accelerate cancer".  I have heard this before, but thought it was a myth.  How could surgery accelerate cancer?  The  one part I do agree with is "It seems the biology of breast cancer is not fully understood".  

I often wonder if articles like this and others give fuel to the Insurance companies to not cover certain tests and exams. Then Insurance companies make it difficult or refuse to cover cost for a test IMO and doctors are less likely to order it. In some instances the test may be beneficial for "some" patients but the doctors refuse to waste time with the insurance companies --- so the insurance companies are dictating medicine without a medical degree. There are so many women who have posted about missed cancers (beyond stage 1) which may have been caught by US or MRI but it was never ordered. I read so many posts of women who were previously treated and then find another breast cancer because it was previously missed.  I certainly wish mine were caught earlier to have avoided 8 rounds of Chemo.

I think women should be able to get mammos whenever they wish.   But with billions of dollars spent on research, we need to be able to offer women more than this old and unreliable diagnostic tool.

This controversy has been going on way back.  I know when I turned 40 a deacde ago,  it was also  being contested.  As one who had two tumors that were not detected by mammogram, and it fact one tumor not detected by ultrasound either, I think the statement that mammograms are oversold is accurate. 

The article questions whether it saves lives.  We have believed that the earlier a tumor is found, the better.  I think some of those beliefs may be changing, and that we're finding its the biology of the tumor and how good is our treatment for  that type of tumor, rather than the exact timing of when it was found. 

I read a second article about this study and it said we should focus on prevention rather than screening.  You know, tell women to exercise, not smoke, not gain weight, not drink excessively.  I thought, oh there's another venture that's going to fail women like me.  My BMI has never been abnormal, I never smoked, I drank maybe 8 drinks a year, exercised and I eat all the things you read that you are supposed to eat.  I never dreamed I would have cancer of any kind.  You know what, I have cancer. 

My conclusion, we have to muddle through while the debate goes on and I do wish they would work on treatments that will help everyone with any kind of tumor instead of simply telling us mammograms will save your life.  I don't think anyone should have to give up mammograms, just yet, but let's not focus on mammograms as the end all be all.   

Fearless... All my mammograms including my diagnostic one missed my tumor.

I was two months shy of my annual screening mammo and ultrasound. Had dense lumpy breasts. Went annually beginning at 40. My mammos were unreadable. At my annual ob/gyn visit, my doctor's magic fingers felt a lump. I went for a diagnostic mammo that missed it. The accompanying ultrasound found it. MRI found "a drop" of DCIS.

In Australia we have a free government run screening program - free annual mammos if you are over 45. If I did not have this service, I hate to think the situation I would be in now 2 years later. Agressive (HER2+ve), barely palpable, sneaky ILC. I thank my lucky stars it showed up on the mammogram before it had grown so big and spread to the nodes!!!

Gardengumby,

You make some very good, and very important, points.  This is my very first post on these boards; your post compelled me to write this.  I am copying and pasting your statements below, so that people who may have missed your comments see them.

FROM GARDENGUMBY:

" . . . I had a screening mammogram that found DCIS, LCIS and invasive.  They say mine was "slow growing", and I was religious about getting yearly mammograms, but nonetheless the area affected by DCIS was approximately 6 cm, the largest invasive was 13 mm and it had moved into my lymph [nodes].  Sooooo, it follows that the cancer was almost undoubtedly missed at least once and probably 2 or even 3 times.  If the "new" guidelines go into effect, someone like me is much more likely to be at state IV before the cancer if found.

I find it very sad that saving money is more important than saving lives."

I agree with the bullets elimar presented. The bottom line is we all need better screening methodology at reasonable cost. If MRI were more cost effective many doctors might order them instead of "watching" with repeat mammograms.  In addition, as patients I strongly feel we have the RIGHT to KNOW the detailed results if we so request it. This is especially true for those of us who had "something" seen and some medical professional decided to watch it without our knowledge. This is not meant to cause more stress to the patient but IMO to help us better in monitoring any concerns. The current scanning methods still miss a significant number of breast cancers. This IMO is detrimental if it now beyond stage 1 and adding much more complex treatments with chemo or involved surgeries.  I would think insurance companies would be on board for better improved screening as more cost effective then extensive treatments for more advanced dx. 

So often there is news of a new methodology already proven to be better than current methods and then that's all you hear about it.  It drops in that black hole again. 

The same goes for the drugs but I suspect that is big business with mega profit margins at stake.

I am getting off topic as usual but in the news not so long ago was the problem with critical drug shortages. There is now an ongoing FBI investigation where a third party was using the FDA drug shortage list to identify critical drugs. They were buying them up in bulk to hoard and resell back to the hospitals at 600% profit for the critical care patients.

Yes, so very true about the over-inflated value of mammograms.  So many women walk away with their yearly letter thinking they are all clear.  You will have to explain the 5th bullet as I looked up the site and see a medical school named after someone.  But I'm clueless and have no idea who that person is. 

How about a sixth thought....Someone like Larry Norton, MD coming out and saying something bold like his British counterpart that the controversy has gone on for too long and it's time for an answer.  Then we can move on to find preventions and better treatments and dare I say, a cure.  Until someone in the United States stands up, we'll still be having all of this controversy.  And if I see one more radiology association debunking those who question screening...without offering up a better answer and SOLUTION....well....hmmm....

Gardengumby, well said.  We are not close to a cure, or prevention, so right now early detection is all we have.  And you bring up a good point, how can we determine who is high risk?  Even though there were several in your family with breast cancer, you were not considered high risk.  

Just a thought--all these studies which followed women for many years to determine how many lives were saved with screening mammograms--were the mammograms analog or digital?  Wonder if it would make a difference.

Also, even if screening mammograms were reduced, what would guarantee that the money saved would go directly towards research for a cure?  There is already a lot of money going towards a cure.  I don't think reducing mammograms will pave the way for a cure.