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How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) – A systematic literature review
Radiography xxx (2016) 1e5
Contents lists available at ScienceDirect
Radiography journal homepage: www.elsevier.com/locate/radi
Review article
How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review J. Curran a, b, c, * a b c
London South Bank University, 103 Borough Rd, London SE1 0AA, UK Kings College Hospital, Denmark Hill, London SE5 9RS, UK Breast Test Wales, 18 Cathedral Road, Cardiff CF11 9LJ, UK
a r t i c l e i n f o
a b s t r a c t
Article history: Received 22 November 2015 Received in revised form 18 January 2016 Accepted 2 February 2016 Available online xxx
Breast Conservation Therapy (BCT) is now seen as the treatment of choice for early-stage breast cancer, leading to a rising demand for post-operative surveillance. Ongoing mammographic surveillance of the post-operative breast is necessary to minimise the morbidity risk from recurrence. This review evaluates the diagnostic value of mammography following BCT, and identifies the possible challenges with mammography regarding imaging, interpretation and test performance when investigating the treated breast. Relevant literature was reviewed and critically analysed. Three studies reported that surveillance mammography provided a significant survival advantage through early detection of recurrence. Five studies recognised the diagnostic challenges of surveillance mammography following BCT, reporting reduced sensitivity after breast surgery. The need for a more tailored screening strategy after treatment for breast cancer was highlighted in four studies. Although overall mammographic sensitivity is reduced after BCT, it is still proven to be effective in detecting recurrences, therefore remains an important surveillance tool. © 2016 The College of Radiographers. Published by Elsevier Ltd. All rights reserved.
Keywords: Mammography Surveillance Breast Conservation Therapy Diagnostic accuracy Breast cancer recurrence
Introduction Statistical data has shown that female death rates from breast cancer have fallen by around one fifth in the past ten years and survival rates have steadily increased over the past forty years.1e4 This may be attributed to earlier detection following the introduction of the National Health Service Breast Screening Programme (NHSBSP) in 1988 and improved treatments including the widespread use of tamoxifen since 1992.5 With more breast cancer survivors comes the need for more long-term surveillance, and it is estimated that by 2020 there will be a 48% increase in the need for breast cancer follow-up services post breast cancer treatment.6,7 Breast Conservation Therapy (BCT) has replaced radical mastectomy as the treatment of choice for early breast cancer. Studies have shown equivocal survival rates for both treatments, with BCT also allowing some preservation of the unaffected breast tissue.8,9 BCT involves the surgical excision of a malignant tumour with a
* 28 Nantcarn Road, Cwmcarn, Newport, Gwent, South Wales, NP11 7EU, UK. E-mail addresses: [email protected], [email protected].
margin of microscopically normal breast tissue, usually followed by radiotherapy and or chemotherapy.9,10 The goal is to remove the tumour while minimising chances of breast cancer recurrence (BCR).5 Ongoing surveillance is necessary as post-operative recurrence and metastases are the leading cause of breast cancer associated mortality, with approximately one in four patients who develop local recurrence dying as a result.8 The risk of a second primary breast cancer remains significantly elevated for up to twenty years post operatively with around 15% of breast cancer survivors developing a second breast malignancy within ten years of their initial treatment.11 Early detection is key to long term recovery, a five year survival rate of between 80% and 90% for ladies with asymptomatic loco-regional recurrences detected through clinical screening has been reported, compared with 25% for those detected at later stages with distant metastases.12 Current follow-up guidelines recommended by the National Institute for Health and Care Excellence (2014)13 and by the Royal College of Radiologists (2010),14 suggest that patients should receive annual mammography until they enter the NHSBSP age bracket, or for five years following treatment if already eligible for screening. These
http://dx.doi.org/10.1016/j.radi.2016.02.001 1078-8174/© 2016 The College of Radiographers. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Curran J, How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.001
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recommendations are based mainly on expert opinion only as there is little quality evidence on the accuracy of mammography for ladies with a history of BCT.15 The post-operative breast represents an increasing diagnostic challenge in mammographic interpretation, as alterations to the breast following BCT can often mimic or disguise early signs of BCR, delaying diagnosis and may lead to a reduced prognosis for the patient.10,16 The aim of this study is to review current literature to evaluate the diagnostic value of mammography following BCT, and to identify the possible challenges with mammography regarding imaging, interpretation and test performance when investigating the treated breast. Methodology Relevant literature from the years 2009e2015 was retrieved using electronic databases including OVID, EMBASE and Science Direct. In order to ensure that relevant information was not missed, search terms were kept broad and relevant key words were combined to refine my searches. The literature was then reviewed and critically analysed to determine the strength of each article and therefore the weight it had in my discussion. Please see Supplementary material online demonstrating research strategy. Findings/results Challenges of post-operative mammography Chansakul et al. recognised the difficulties in distinguishing between normal post-operative alterations and BCR.16 They suggest that in order to minimise unnecessary recall and permit earlier detection of recurrence, the reader must review mammograms in light of previous imaging and have an awareness of the of timing and morphology of expected normal mammographic appearances post-surgery. A subsequent study suggests that any change in image appearance after the stability of post-operative alterations, is suggestive of a possible recurrence.9 The authors advise that postoperative mammography is often of suboptimal quality due to difficulty positioning the breast after surgical disfigurement, limited compressibility and an overall increase in breast density.16 Although much of this evidence is based on expert opinion, some of the points raised have been echoed in other more empirical literature within this review. An increase in breast density due to surgical scarring can limit the interpretation of BCR on mammography by masking subtle abnormalities.17 Mammographic density (MD) is thought to be one of the strongest risk factors of breast cancer, and is linked with lower prognosis due to later detection.18 In a retrospective study by Cil et al., it was found that the risk of local recurrence after BCT was much higher in the high MD group (21% at 10 years).17 Risk was highest for women who did not receive radiotherapy and were in the high breast density group (40% risk at 10 years). The authors concluded that although there was a notable link between MD and local recurrence, there was no effect on distant recurrence or death. In a larger study by Eriksson et al., similar findings were reported, where women in the highest MD group had a three-fold increased risk of local recurrence than those in the lowest MD group.18 Again no link was found between breast density and risk of distant recurrence and survival. Limited compressibility after BCT was investigated by Groot et al., who reported that women having a mammogram following BCT were five times more likely to experience severe pain compared to those with untreated breasts, owing to an approximate 30% reduction in elasticity.19 The study investigated the use of a sensor to calculate optimal pressure to apply to the treated breast.
An average reduction in pain by 26%, and severe pain by 77% was achieved when this technology was used. This study was based on a relatively small sample size (n ¼ 58) and the main outcomes are based on model estimates. Mathers et al., conducted a unique study into the experiences of women attending follow-up mammography appointments after breast disease, in which women described mammography as uncomfortable or extremely painful. Women reported increased anxiety due to tenderness, and some believed that this would impact on their ability to stay still during the examination.20 It could be assumed that this may have a detrimental effect on resultant image quality through increased likelihood of image blurring, although this is not specified within the paper. Overall women valued the reassurance gained from having follow-up mammography and felt that this outweighed concerns of potential increased pain. This was a relatively small study with a possible selection bias, therefore may not be representative of the UK as a whole. Mammographic surveillance after BCT A cross-sectional study by Greenwood-Haigh, revealed a marked difference in the post-operative mammographic follow-up protocols used between centres in the UK.21 The majority of centres (56%) adhered to the current recommendations, performing annual mammography for five years after surgery, before discharging eligible patients to NHSBSP. Some patients however had been discharged immediately, with others receiving annual screening for up to ten years depending on geographic location. Although the authors admit that some generalisations have been made in the study, it generated an excellent response rate and highlights the lack of evidence available to determine the optimal frequency for followup after BCT. A recent study compared recurrence outcomes of those having biannual compared to annual mammographic surveillance.22 It was found that recurrences detected six months post-treatment were significantly less advanced, smaller and node negative compared to those detected at annual intervals. It was suggested that biannual mammography for 5 years post-treatment could derive a significant survival benefit. This large scale study is thought to be the first to provide direct evidence comparing the effect of surveillance intervals on recurrence outcomes in the same populations. The validity of the study was questioned by Dershaw et al., who suggested that an overestimation of the real significance between the two groups had been made, as the smaller tumour size noted in the biannual mammographic surveillance cohort did not reach statistical significance.23 Arasu et al., defended the significance of the findings stating that although tumour size did not reach maximum statistical significance, it had clinical significance as it separated smaller cancers from larger cancers, and noted that the prognosis for invasive cancers measuring 1 cm or less was around 90% survival at twenty years.24 Houssami et al., have also reported a survival benefit from earlier detection of breast cancer in their retrospective study.25 It was found that early detection of asymptomatic BCR improved survival by up to 47% compared with those detected symptomatically. The study found that asymptomatic cancers were smaller and more likely to be early stage, compared with symptomatic BCR. Mammography was reported to be more sensitive than clinical examination (CE) for detecting asymptomatic cancers, 87% versus 57% retrospectively. Although methods were used to minimise biases in this study, it is limited by its non-randomised design and does not report absolute survival. Similarly Lu et al., reported better overall survival for recurrences detected asymptomatically by mammography rather than CE, reporting an absolute reduction in
Please cite this article in press as: Curran J, How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.001
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mortality of 17%e28% if loco-regional recurrences are detected early.6 Accuracy of mammography following BCT A large study was conducted to determine whether mammographic interpretation was hindered by tissue characteristics of previous breast surgery. This was measured using interval cancer figures, i.e. the number of cancers detected after a prior negative screening result, which presented before the next planned screening within a two year interval.26 Screening sensitivity was found to be significantly lower in women with previous breast surgery (63.5%) compared with those without (73.5%). Interval cancers were found to have more pronounced post-operative alterations in the breast segment where the cancer was detected compared to screen-detected cancers. This study was based on screen-film mammography (SFM) images only, therefore may be difficult to directly compare with full-field digital mammography (FFDM). Similar findings were presented in a study by Houssami et al., which found that mammography sensitivity was lower for those with previous history of breast cancer (PHBC), (65%) compared to those without (76%), despite having higher additional evaluation rates.15 Of those with PHBC, screening sensitivity was higher for early stage, in-situ cancers (78%) compared with invasive cancers (61%). Higher mammographic sensitivity was noted in women who did not receive systemic therapy, for whom underlying cancer rates were higher. Overall those with PHBC displayed higher rates of cancer detection, and a significantly higher proportion of these were interval cancers. The authors conclude that there is a need for a more tailored screening strategy based on risk. This was a large comprehensive study, in which screening accuracy was based on final assessment. An earlier study also focused around the need for a more individualised screening strategy, based on risk of recurrence.27 It was demonstrated that 1/3 of recurrences and primary cancers were not screen-detected. Although mammography demonstrates low sensitivity in women with dense breasts and generates high false positive rates, it remains the only proven test to reduce cancer related death.28 The need for a personalised approach was suggested again, where it was proposed that age, risk and MD should be considered to provide the optimal screening strategy. A systematic review found that the average sensitivity for surveillance mammography in detecting ipsilateral BCR was 71% and 63% specificity across four studies.29 The results showed that around 50% of local recurrences were detected by mammography, with the rest being detected by CE or reported by the patient. Ten percent of palpable tumours were not clearly seen on mammography. This paper highlighted the need for further research on surveillance mammography and diagnostic tests for patients following BCT. A similar review reported that surveillance mammography following BCT detected 8e50% of ipsilateral recurrences, and 18e80% of contralateral recurrence.11 The lower cancer detection rates noted in the ipsilateral breast may be evidence of the reduced sensitivity of mammography to BCR after surgical intervention. Screening sensitivity of FFDM was increased from 60% to 94%, and specificity increased from 20.7% to 74% when digital breast tomosynthesis (DBT) was applied in a study by Mansour et al.30 Operative bed recurrence could be more confidently excluded from scarring, which reduced the number of indeterminate findings by proving either a definite benign or malignant diagnosis. DBT allowed unnecessary biopsy to be avoided in 37.3% of patients. Although the study was not directly focused on breast cancer recurrence after BCT, these findings demonstrate relevance in this area.
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Discussion The information obtained in this review presents varied findings as to the effectiveness of mammography in detecting breast cancer recurrence after BCT. Three studies of high validity demonstrated that a significant survival advantage by up to 47%, could be achieved by earlier detection of asymptomatic recurrences through surveillance mammography.6,22,25 One of these studies recommended that biannual mammography follow-up intervals for five years post-surgery would improve prognosis of recurrence as cancers were generally smaller and node negative.22 While these findings seem promising, it may be argued that consideration needs to made to the possible increased volume of false positive rates generated through increased mammography screening, and the negative effect this has been shown to have on the patient.20,28 It has been suggested that offering surveillance mammography more frequently than NHSBSP should be limited to those for which benefit outweighs risk.21 The findings from this review have highlighted some inherent diagnostic challenges of surveillance mammography following BCT. The distortion of the remaining breast tissue can lead to problems with initial positioning of the mammogram, reduced toleration of compression due to increased pain sensation and suboptimal quality of the resultant image. It would seem that the sensitivity of mammography is reduced for this group of patients who are at higher risk of breast disease. Five studies reported on the sensitivity of mammography to breast disease after breast surgery, all of which suggested that diagnostic accuracy was reduced as a result.15,26e29 Quantitative data to support these arguments is provided in four of these studies reporting an average of 10% reduction in sensitivity. Two studies reported increased interval cancer rates after BCT,15,26 however it is not clear if this was due to the inherent increased risk of recurrence after primary breast cancer, or due to inability to detect recurrence in the first instance due to suboptimal image quality. It was interesting to note that Smallenberg et al.,26 found interval cancers demonstrated more noticeable surgical disfigurement in the breast segment where the cancer was detected, compared to cancers detected through screening. Conversely, one study reported higher screening sensitivity for those with PHBC compared to those without in detecting early stage breast cancers,15 perhaps owing to more frequent screening. Similarly screening sensitivity was higher in women who did not receive systemic therapy, for whom underlying cancer rates were also higher.15 Cil et al.17 reported that those who did not receive radiotherapy had higher mammographic screening sensitivity, yet a doubled risk of recurrence. Radiotherapy treatment was thought to reduce mammographic sensitivity as it leads to increased MD, and therefore higher risk of masking recurrences. There is a clear compromise between providing adequate risk reduction treatment and limiting alterations to the breast which can conceal recurrences. Four studies in this review described the need for a more tailored screening strategy, based on individual risk of recurrence.15,21,27,28 Perhaps due to the lack of evidence-based national guidance there is discordance in the follow-up protocols used across the country, varying in duration and frequency of mammographic surveillance provided.21 Current guidelines for surveillance recommendations which are thought to be employed by the majority of screening centres in the UK, may be considered too broad and do not factor for heterogeneity of the population. It has been suggested that age, stage of initial diagnosis, treatment type, and MD should be considered important factors in developing a strategy based on risk stratification for more individualised care. This method could help target appropriate mammographic surveillance
Please cite this article in press as: Curran J, How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.001
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to those who would benefit, and exploit the survival advantage of early detection. Many of the papers reviewed did not specify if they had used SFM or FFDM which may have had an impact on the sensitivity and specificity values recorded. A recent study however reported similar sensitivities and interval cancer rates for SFM and FFDM.7 Advancements in FFDM technology may further improve sensitivity of mammography to breast cancer recurrence after BCT, an example of such technology is DBT which demonstrated a significant increase in sensitivity and specificity of the screening mammogram and allowed surgical scarring to be effectively differentiated from cancer recurrence in a study by Mansour et al.30 Due to the restrictions of this study, other digital advancements could not be investigated in detail. Future studies may focus on comparisons between FFDM and other modalities/technologies in the detection of breast cancer recurrence. Most of the primary research obtained in this review was retrospective in design, therefore perhaps holds less weight than findings from that of clinical trials. There seemed to be a lack of empirical research which was acknowledged by some of the authors of the literature obtained, however some suggested that clinical trials were infeasible in this subject area due to ethical implications. Despite this, a large randomised controlled trial (MAMMO-50) is currently under way at Warwick Medical School which will generate information from a large number of UK based breast departments over a 30 year period. This trial will compare annual to biennial mammography for ladies treated with BCT or every three years for patients treated with mastectomy. The results will provide a solid evidence base to determine optimal screening frequency and duration for ladies fifty years or over following BCT.31 It should be noted that due to the lack of literature available surrounding this subject area it was difficult to refine my study to focus on either long term or short term surveillance, instead a more generalised overview is given. Although an extensive range of databases, and library catalogues were searched, all relevant information may not have been located. Furthermore, as a single reviewer my research may be assumed to be of less strength than that of a Cochrane-style systematic review. The evidence gathered in this review may help to give health professionals a better appreciation of some challenges of mammographic surveillance after BCT, and the sensitivity and test performance of the modality in detecting breast cancer recurrences in this patient group. Due to the insufficiency of empirical research available there are still many areas surrounding the subject that remain uncertain. This emphasises the need for future studies to provide a solid evidence base for practice in areas such as; the use of FFDM in detecting breast cancer recurrences, comparative studies to determine the optimal modality for breast cancer recurrence, and investigating alternative surveillance follow-up strategies based on risk of recurrence in individual patients. Implications for practice e conclusion Regular mammographic surveillance following BCT has been shown to facilitate early detection of asymptomatic breast cancer recurrences, which can provide a significant survival advantage to the patient. This is despite the fact that image quality is thought to be compromised to varying degrees due to surgical disfigurement, scar tissue overlay, increased breast density and limited compressibility of the breast. Although overall mammographic sensitivity is reduced after BCT, it is still proven to be effective in detecting recurrences in the ipsilateral and contralateral breast, and therefore remains an important surveillance tool. It is important to consider also that although ladies with a history of BCT will
generally feel more pain from follow-up mammograms, surveillance screening is still welcomed by these women due to the reassurance it provides. Technological developments in FFDM including DBT may further improve sensitivity in imaging the postsurgical breast, however more research is needed in this area. There is evidence to suggest that a more individualistic structure to mammographic surveillance would be beneficial, regarding frequency and duration of follow-up procedures. Anticipated future findings from the ongoing Mammo-50 trial will be hugely influential in providing a solid evidence-base from which decisions can be made to optimise screening strategy for ladies with a history of BCT. This could potentially maximise the survival advantage of early detection and minimise the adverse effects of unnecessary mammography and false positive results. With the rising demand for post-operative surveillance after treatment for early breast cancer, this strategy could elicit better use of breast screening services, improving efficiencies with a more patient centred approach and ultimately further improve long-term survival after BCT. Conflict of interest statement None declared. Acknowledgements
Joshua Rogers-Evans Zebby Rees Noel Curran Jayne Skillen Gillian Rogers Danielle Moakes Melanie Button Isobelle Puscus Katie Pyne
Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.radi.2016.02.001. References 1. Autier P, Boniol M, LaVecchia C, Vatten L, Gavin A, Hery C, et al. Disparities in breast cancer mortality rates between 30 European countries: retrospective trend analysis of WHO mortality database. Br Med J 2010;341(c3620):1e7. Available from: http://www.bmj.com/content/341/bmj.c3620.full.pdfþhtml [accessed 10.01.15]. 2. Northern Ireland Statistics and Research Agency. Publications and statistics. 2013. Available from: http://www.nisra.gov.uk/publications/default.asp.htm [accessed 10.01.15]. 3. National Records of Scotland. Statistics and data. 2014. Available from: http:// www.gro-scotland.gov.uk/statistics-and-data [accessed 10.01.15]. 4. Office of National Statistics. All releases of mortality statistics: deaths registered in England and Wales. 2014. Available from: http://www.ons.gov.uk/ons/ publications/all-releases.html?definition¼tcm:77-27475 [accessed 10.01.15]. 5. Neal CH, Yilmaz ZN, Noroozian M, Klein KA, Sundaram B, Kazerooni EA, et al. Imaging of breast cancer-related changes after surgical therapy. Am J Roentgenol 2014;202(2):262e72. Available from: http://www.ajronline.org/doi/pdf/ 10.2214/AJR.13.11517 [accessed 10.01.15]. 6. Lu WL, Jansen L, Post WJ, Bonnema J, Van de Velde JC, De Bock GH. Impact on survival of early detection of isolated breast recurrences after the primary treatment for breast cancer: a meta-analysis. Breast Cancer Res Treat 2009;114(3):403e12. Available from: http://link.springer.com/article/10.1007/ s10549-008-0023-4#page-1 [accessed 10.01.15]. 7. Nederend J, Duijm LEM, Louwman MWJ, Coebergh JW, Roumen RMH, Lohle PL, et al. Impact of the transition from screen-film to digital screening mammography on the interval cancer characteristics and treatment e a population based study from the Netherlands. Eur J Cancer 2014;50(1):31e9. Available from: http://www.ejcancer.com/article/S0959-8049(13)00893-9/pdf [accessed 15.02.15]. 8. Association of Breast Surgery at BASO. Surgical guidelines for the management of breast cancer. London: Elsevier Ltd.; 2009. Available from: http://www.
Please cite this article in press as: Curran J, How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.001
J. Curran / Radiography xxx (2016) 1e5
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
associationofbreastsurgery.org.uk/media/4565/surgical_guidelines_for_the_ management_of_breast_cancer.pdf [accessed 10.01.15]. Chansakul T, Lai KC, Slanetz PJ. The postconservation breast: part 2, imaging findings of tumor recurrence and other long-term sequelae. Am J Roentgenol 2012b;198(2):331e43. Available from: http://www.ajronline.org/doi/pdf/10. 2214/AJR.11.6881 [accessed 15.12.14]. Guitierrez R, Horst KC, Dirbas FM, Ikeda DM. Breast imaging following breast conservation therapy. In: Dirbas FM, Scott-Conner CFH, editors. Breast surgical techniques and interdisciplinary management. Washington: Springer; 2011. p. 975e95. Schneble EJ, Graham LJ, Shupe MP, Flynt FI, Banks KP, Kirkpatrick AD, et al. Current approaches and challenges in early detection of breast cancer recurrence. J Cancer 2014;5(4):281e90. Available from: http://www.jcancer.org/ v05p0281.pdf [accessed 10.01.15]. Puglisi F, Fontanella C, Numico G, Sini V, Evangelista L, Monetti F, et al. Followup of patients with early breast cancer: is it time to rewrite the story? Crit Rev Oncol Hematol 2014;91(2):130e41. Available from: http://ac.els-cdn.com/ S104084281400050X/1-s2.0-S104084281400050X-main.pdf?_tid¼0cf33aba0317-11e5-8761-00000aacb35d&acdnat¼1432583504_ 6419301dcb1ee4eaa382ffc72f218317 [accessed 15.12.14]. National Institute for Health and Care Excellence. Early and locally advanced breast cancer: diagnosis and treatment. London: National Institute for Health and Care Excellence; 2014. Available from: http://www.nice.org.uk/guidance/ cg80/resources/guidance-early-and-locally-advanced-breast-cancer-pdf [accessed 10.11.14]. Royal College of Radiologists. Guidance on screening and symptomatic breast imaging. London: Royal College of Radiologists; 2010. Available from: https:// www.rcr.ac.uk/sites/default/files/publication/BFCR%2813%295_breast.pdf [accessed 10.12.14]. Houssami N, Abraham LA, Miglioretti DL, Sickles EA, Kerlikowske K, Buist DSM, et al. Accuracy and outcomes of screening mammography in women with a personal history of early-stage breast cancer. J Am Med Assoc 2011;305(8): 790e9. Available from: http://jama.jamanetwork.com/article.aspx? articleid¼645792 [accessed 15.12.14]. Chansakul T, Lai KC, Slanetz PJ. The postconservation breast: part 1, expected imaging findings. Am J Roentgenol 2012a;198(2):321e30. Available from: http://www.ajronline.org/doi/pdf/10.2214/AJR.10.7298 [accessed 15.12.14]. Cil T, Fishell E, Hanna W, Sun P, Rawlinson E, Narod SA, et al. Mammographic density and the risk of breast cancer recurrence after breast conserving surgery. Cancer 2009;115(24):5781e7. Available from: http://onlinelibrary.wiley. com/doi/10.1002/cncr.24638/epdf [accessed 10.01.15]. Eriksson L, Czene K, Rosenberg L, Humphreys K, Hall P. Possible influence of mammographic density on local and locoregional recurrence of breast cancer. Breast Cancer Res 2013;15(4):1e9. Available from: http://breast-cancerresearch.com/content/pdf/bcr3450.pdf [accessed 10.01.15]. Groot JE, Broeders MJM, Branderhorst W, Den Heeten GJ, Grimbergen CA. Mammographic compression after breast conserving therapy: controlling pressure instead of force. Med Phys 2014;41(2). pp. 023501e1-023501023501-8. Available from: http://scitation.aip.org/docserver/fulltext/aapm/ journal/medphys/41/2/1.4862512.pdf?expires¼1432312517&id¼id&accname ¼guest&checksum¼BDA6BB2B6ECB2B53A3FA48BB5FA95013 [accessed 26.10.14].
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20. Mathers SA, Graham AM, Robertson EM. ‘It was daunting’ experience of women with a diagnosis of breast cancer attending for breast imaging. Radiography 2013;19(2):156e63. 21. Greenwood-Haigh L. Mammographic surveillance in the follow-up of early breast cancer in england: a cross-sectional survey. Radiography 2009;15(3): 220e7. Available from: http://www.radiographyonline.com/article/S10788174(08)00093-X/pdf [accessed 10.01.15]. 22. Arasu VA, Joe BN, Lvoff NM, Leung JWT, Brenner RJ, Flowers CI, et al. Benefit of semiannual ipsilateral mammographic surveillance following breast conservation therapy. Radiology 2012;264(2):371e7. Available from: http://www.ncbi. nlm.nih.gov/pmc/articles/PMC3401347/pdf/111458.pdf [accessed 10.01.15]. 23. Dershaw DD, Lee CH, Morris EA. Letters to the editor. Radiology 2013;266(2): 685. Available from: http://pubs.rsna.org/doi/pdf/10.1148/radiol.12121630 [accessed 10.01.15]. 24. Arasu VA, Joe BN, Lvoff NM, Leung JWT, Brenner RJ, Flowers CI, et al. Letter to the editor. Radiology 2013;266(2):685e6. Available from: http://pubs.rsna.org/ doi/pdf/10.1148/radiol.12121630 [accessed 10.01.15]. 25. Houssami N, Ciatto S, Martinello F, Bonardi R, Duffy SW. Early detection of second breast cancers improves prognosis in breast cancer survivors. Ann Oncol 2009;20(9):1505e10. Available from: http://annonc.oxfordjournals.org/ content/20/9/1505.full.pdfþhtml [accessed 15.12.14]. 26. Smallenburg VVB, Duijm LEM, Voogd AC, Jansen FH, Louwman WJ. Mammographic changes from benign breast surgery impair breast cancer detection at screening mammography. Eur J Cancer 2012;48(14):2097e103. Available from: http://0-ac.els-cdn.com.lispac.lsbu.ac.uk/S0959804912002663/1-s2.0-S09598 04912002663-main.pdf?_tid¼ab15b020-0573-11e5-bf93-00000aab0f26&ac dnat¼1432843185_839ab1e97a4e7c0539d021a1f3666707 [accessed 10.01.15]. 27. Buist DSM, Abraham LA, Barlow WE, Krishnaraj A, Holdridge RC, Sickles EA, et al. Diagnosis of second breast cancer events after initial diagnosis of early stage breast cancer. Breast Cancer Res Treat 2010;124(3):863e73. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2976764/pdf/nihms233 153.pdf [accessed 15.12.14]. 28. Drukteinis JS, Mooney BP, Flowers CI, Gatenby RA. Beyond mammography: new frontiers in breast cancer screening. Am J Med 2013;126(6):472e9. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4010151/pdf/ nihms571320.pdf [accessed 10.01.15]. 29. Robertson C, Ragupathy SKA, Boachie C, Fraser C, Heys SD, MacLennan G, et al. Surveillance mammography for detecting ipsilateral breast tumour recurrence and metachronous contralateral breast cancer: a systematic review. Eur Radiol 2011;21(12):2484e91. Available from: http://www.ncbi.nlm.nih.gov/pmc/ articles/PMC3217137/pdf/330_2011_Article_2226.pdf [accessed 10.01.15]. 30. Mansour S, Adel L, Mokhtar O, Sherif Omar O. Comparative study between breast tomosynthesis and classic digital mammography in the evaluation of different breast lesions. Egypt J Radiol Nucl Med 2014;45(3):1053e61. Available from: http://ac.els-cdn.com/S0378603X14000539/1-s2.0-S0378603X14000 539-main.pdf?_tid¼5810f9d4-0569-11e5-b8e000000aab0f6c&acdnat¼1432838751_21659c39dd6f49117b4b305d7579aeaa [accessed 10.02.15]. 31. Warwick Medical School. Mammo- 50 mammographic surveillance in breast cancer patients aged 50 years or older. 2015. Available from: http://www2. warwick.ac.uk/fac/med/research/hscience/ctu/trials/cancer/mammo50/ [accessed 16.01.16].
Please cite this article in press as: Curran J, How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.001
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Review article
How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review J. Curran a, b, c, * a b c
London South Bank University, 103 Borough Rd, London SE1 0AA, UK Kings College Hospital, Denmark Hill, London SE5 9RS, UK Breast Test Wales, 18 Cathedral Road, Cardiff CF11 9LJ, UK
a r t i c l e i n f o
a b s t r a c t
Article history: Received 22 November 2015 Received in revised form 18 January 2016 Accepted 2 February 2016 Available online xxx
Breast Conservation Therapy (BCT) is now seen as the treatment of choice for early-stage breast cancer, leading to a rising demand for post-operative surveillance. Ongoing mammographic surveillance of the post-operative breast is necessary to minimise the morbidity risk from recurrence. This review evaluates the diagnostic value of mammography following BCT, and identifies the possible challenges with mammography regarding imaging, interpretation and test performance when investigating the treated breast. Relevant literature was reviewed and critically analysed. Three studies reported that surveillance mammography provided a significant survival advantage through early detection of recurrence. Five studies recognised the diagnostic challenges of surveillance mammography following BCT, reporting reduced sensitivity after breast surgery. The need for a more tailored screening strategy after treatment for breast cancer was highlighted in four studies. Although overall mammographic sensitivity is reduced after BCT, it is still proven to be effective in detecting recurrences, therefore remains an important surveillance tool. © 2016 The College of Radiographers. Published by Elsevier Ltd. All rights reserved.
Keywords: Mammography Surveillance Breast Conservation Therapy Diagnostic accuracy Breast cancer recurrence
Introduction Statistical data has shown that female death rates from breast cancer have fallen by around one fifth in the past ten years and survival rates have steadily increased over the past forty years.1e4 This may be attributed to earlier detection following the introduction of the National Health Service Breast Screening Programme (NHSBSP) in 1988 and improved treatments including the widespread use of tamoxifen since 1992.5 With more breast cancer survivors comes the need for more long-term surveillance, and it is estimated that by 2020 there will be a 48% increase in the need for breast cancer follow-up services post breast cancer treatment.6,7 Breast Conservation Therapy (BCT) has replaced radical mastectomy as the treatment of choice for early breast cancer. Studies have shown equivocal survival rates for both treatments, with BCT also allowing some preservation of the unaffected breast tissue.8,9 BCT involves the surgical excision of a malignant tumour with a
* 28 Nantcarn Road, Cwmcarn, Newport, Gwent, South Wales, NP11 7EU, UK. E-mail addresses: [email protected], [email protected].
margin of microscopically normal breast tissue, usually followed by radiotherapy and or chemotherapy.9,10 The goal is to remove the tumour while minimising chances of breast cancer recurrence (BCR).5 Ongoing surveillance is necessary as post-operative recurrence and metastases are the leading cause of breast cancer associated mortality, with approximately one in four patients who develop local recurrence dying as a result.8 The risk of a second primary breast cancer remains significantly elevated for up to twenty years post operatively with around 15% of breast cancer survivors developing a second breast malignancy within ten years of their initial treatment.11 Early detection is key to long term recovery, a five year survival rate of between 80% and 90% for ladies with asymptomatic loco-regional recurrences detected through clinical screening has been reported, compared with 25% for those detected at later stages with distant metastases.12 Current follow-up guidelines recommended by the National Institute for Health and Care Excellence (2014)13 and by the Royal College of Radiologists (2010),14 suggest that patients should receive annual mammography until they enter the NHSBSP age bracket, or for five years following treatment if already eligible for screening. These
http://dx.doi.org/10.1016/j.radi.2016.02.001 1078-8174/© 2016 The College of Radiographers. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Curran J, How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.001
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recommendations are based mainly on expert opinion only as there is little quality evidence on the accuracy of mammography for ladies with a history of BCT.15 The post-operative breast represents an increasing diagnostic challenge in mammographic interpretation, as alterations to the breast following BCT can often mimic or disguise early signs of BCR, delaying diagnosis and may lead to a reduced prognosis for the patient.10,16 The aim of this study is to review current literature to evaluate the diagnostic value of mammography following BCT, and to identify the possible challenges with mammography regarding imaging, interpretation and test performance when investigating the treated breast. Methodology Relevant literature from the years 2009e2015 was retrieved using electronic databases including OVID, EMBASE and Science Direct. In order to ensure that relevant information was not missed, search terms were kept broad and relevant key words were combined to refine my searches. The literature was then reviewed and critically analysed to determine the strength of each article and therefore the weight it had in my discussion. Please see Supplementary material online demonstrating research strategy. Findings/results Challenges of post-operative mammography Chansakul et al. recognised the difficulties in distinguishing between normal post-operative alterations and BCR.16 They suggest that in order to minimise unnecessary recall and permit earlier detection of recurrence, the reader must review mammograms in light of previous imaging and have an awareness of the of timing and morphology of expected normal mammographic appearances post-surgery. A subsequent study suggests that any change in image appearance after the stability of post-operative alterations, is suggestive of a possible recurrence.9 The authors advise that postoperative mammography is often of suboptimal quality due to difficulty positioning the breast after surgical disfigurement, limited compressibility and an overall increase in breast density.16 Although much of this evidence is based on expert opinion, some of the points raised have been echoed in other more empirical literature within this review. An increase in breast density due to surgical scarring can limit the interpretation of BCR on mammography by masking subtle abnormalities.17 Mammographic density (MD) is thought to be one of the strongest risk factors of breast cancer, and is linked with lower prognosis due to later detection.18 In a retrospective study by Cil et al., it was found that the risk of local recurrence after BCT was much higher in the high MD group (21% at 10 years).17 Risk was highest for women who did not receive radiotherapy and were in the high breast density group (40% risk at 10 years). The authors concluded that although there was a notable link between MD and local recurrence, there was no effect on distant recurrence or death. In a larger study by Eriksson et al., similar findings were reported, where women in the highest MD group had a three-fold increased risk of local recurrence than those in the lowest MD group.18 Again no link was found between breast density and risk of distant recurrence and survival. Limited compressibility after BCT was investigated by Groot et al., who reported that women having a mammogram following BCT were five times more likely to experience severe pain compared to those with untreated breasts, owing to an approximate 30% reduction in elasticity.19 The study investigated the use of a sensor to calculate optimal pressure to apply to the treated breast.
An average reduction in pain by 26%, and severe pain by 77% was achieved when this technology was used. This study was based on a relatively small sample size (n ¼ 58) and the main outcomes are based on model estimates. Mathers et al., conducted a unique study into the experiences of women attending follow-up mammography appointments after breast disease, in which women described mammography as uncomfortable or extremely painful. Women reported increased anxiety due to tenderness, and some believed that this would impact on their ability to stay still during the examination.20 It could be assumed that this may have a detrimental effect on resultant image quality through increased likelihood of image blurring, although this is not specified within the paper. Overall women valued the reassurance gained from having follow-up mammography and felt that this outweighed concerns of potential increased pain. This was a relatively small study with a possible selection bias, therefore may not be representative of the UK as a whole. Mammographic surveillance after BCT A cross-sectional study by Greenwood-Haigh, revealed a marked difference in the post-operative mammographic follow-up protocols used between centres in the UK.21 The majority of centres (56%) adhered to the current recommendations, performing annual mammography for five years after surgery, before discharging eligible patients to NHSBSP. Some patients however had been discharged immediately, with others receiving annual screening for up to ten years depending on geographic location. Although the authors admit that some generalisations have been made in the study, it generated an excellent response rate and highlights the lack of evidence available to determine the optimal frequency for followup after BCT. A recent study compared recurrence outcomes of those having biannual compared to annual mammographic surveillance.22 It was found that recurrences detected six months post-treatment were significantly less advanced, smaller and node negative compared to those detected at annual intervals. It was suggested that biannual mammography for 5 years post-treatment could derive a significant survival benefit. This large scale study is thought to be the first to provide direct evidence comparing the effect of surveillance intervals on recurrence outcomes in the same populations. The validity of the study was questioned by Dershaw et al., who suggested that an overestimation of the real significance between the two groups had been made, as the smaller tumour size noted in the biannual mammographic surveillance cohort did not reach statistical significance.23 Arasu et al., defended the significance of the findings stating that although tumour size did not reach maximum statistical significance, it had clinical significance as it separated smaller cancers from larger cancers, and noted that the prognosis for invasive cancers measuring 1 cm or less was around 90% survival at twenty years.24 Houssami et al., have also reported a survival benefit from earlier detection of breast cancer in their retrospective study.25 It was found that early detection of asymptomatic BCR improved survival by up to 47% compared with those detected symptomatically. The study found that asymptomatic cancers were smaller and more likely to be early stage, compared with symptomatic BCR. Mammography was reported to be more sensitive than clinical examination (CE) for detecting asymptomatic cancers, 87% versus 57% retrospectively. Although methods were used to minimise biases in this study, it is limited by its non-randomised design and does not report absolute survival. Similarly Lu et al., reported better overall survival for recurrences detected asymptomatically by mammography rather than CE, reporting an absolute reduction in
Please cite this article in press as: Curran J, How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.001
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mortality of 17%e28% if loco-regional recurrences are detected early.6 Accuracy of mammography following BCT A large study was conducted to determine whether mammographic interpretation was hindered by tissue characteristics of previous breast surgery. This was measured using interval cancer figures, i.e. the number of cancers detected after a prior negative screening result, which presented before the next planned screening within a two year interval.26 Screening sensitivity was found to be significantly lower in women with previous breast surgery (63.5%) compared with those without (73.5%). Interval cancers were found to have more pronounced post-operative alterations in the breast segment where the cancer was detected compared to screen-detected cancers. This study was based on screen-film mammography (SFM) images only, therefore may be difficult to directly compare with full-field digital mammography (FFDM). Similar findings were presented in a study by Houssami et al., which found that mammography sensitivity was lower for those with previous history of breast cancer (PHBC), (65%) compared to those without (76%), despite having higher additional evaluation rates.15 Of those with PHBC, screening sensitivity was higher for early stage, in-situ cancers (78%) compared with invasive cancers (61%). Higher mammographic sensitivity was noted in women who did not receive systemic therapy, for whom underlying cancer rates were higher. Overall those with PHBC displayed higher rates of cancer detection, and a significantly higher proportion of these were interval cancers. The authors conclude that there is a need for a more tailored screening strategy based on risk. This was a large comprehensive study, in which screening accuracy was based on final assessment. An earlier study also focused around the need for a more individualised screening strategy, based on risk of recurrence.27 It was demonstrated that 1/3 of recurrences and primary cancers were not screen-detected. Although mammography demonstrates low sensitivity in women with dense breasts and generates high false positive rates, it remains the only proven test to reduce cancer related death.28 The need for a personalised approach was suggested again, where it was proposed that age, risk and MD should be considered to provide the optimal screening strategy. A systematic review found that the average sensitivity for surveillance mammography in detecting ipsilateral BCR was 71% and 63% specificity across four studies.29 The results showed that around 50% of local recurrences were detected by mammography, with the rest being detected by CE or reported by the patient. Ten percent of palpable tumours were not clearly seen on mammography. This paper highlighted the need for further research on surveillance mammography and diagnostic tests for patients following BCT. A similar review reported that surveillance mammography following BCT detected 8e50% of ipsilateral recurrences, and 18e80% of contralateral recurrence.11 The lower cancer detection rates noted in the ipsilateral breast may be evidence of the reduced sensitivity of mammography to BCR after surgical intervention. Screening sensitivity of FFDM was increased from 60% to 94%, and specificity increased from 20.7% to 74% when digital breast tomosynthesis (DBT) was applied in a study by Mansour et al.30 Operative bed recurrence could be more confidently excluded from scarring, which reduced the number of indeterminate findings by proving either a definite benign or malignant diagnosis. DBT allowed unnecessary biopsy to be avoided in 37.3% of patients. Although the study was not directly focused on breast cancer recurrence after BCT, these findings demonstrate relevance in this area.
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Discussion The information obtained in this review presents varied findings as to the effectiveness of mammography in detecting breast cancer recurrence after BCT. Three studies of high validity demonstrated that a significant survival advantage by up to 47%, could be achieved by earlier detection of asymptomatic recurrences through surveillance mammography.6,22,25 One of these studies recommended that biannual mammography follow-up intervals for five years post-surgery would improve prognosis of recurrence as cancers were generally smaller and node negative.22 While these findings seem promising, it may be argued that consideration needs to made to the possible increased volume of false positive rates generated through increased mammography screening, and the negative effect this has been shown to have on the patient.20,28 It has been suggested that offering surveillance mammography more frequently than NHSBSP should be limited to those for which benefit outweighs risk.21 The findings from this review have highlighted some inherent diagnostic challenges of surveillance mammography following BCT. The distortion of the remaining breast tissue can lead to problems with initial positioning of the mammogram, reduced toleration of compression due to increased pain sensation and suboptimal quality of the resultant image. It would seem that the sensitivity of mammography is reduced for this group of patients who are at higher risk of breast disease. Five studies reported on the sensitivity of mammography to breast disease after breast surgery, all of which suggested that diagnostic accuracy was reduced as a result.15,26e29 Quantitative data to support these arguments is provided in four of these studies reporting an average of 10% reduction in sensitivity. Two studies reported increased interval cancer rates after BCT,15,26 however it is not clear if this was due to the inherent increased risk of recurrence after primary breast cancer, or due to inability to detect recurrence in the first instance due to suboptimal image quality. It was interesting to note that Smallenberg et al.,26 found interval cancers demonstrated more noticeable surgical disfigurement in the breast segment where the cancer was detected, compared to cancers detected through screening. Conversely, one study reported higher screening sensitivity for those with PHBC compared to those without in detecting early stage breast cancers,15 perhaps owing to more frequent screening. Similarly screening sensitivity was higher in women who did not receive systemic therapy, for whom underlying cancer rates were also higher.15 Cil et al.17 reported that those who did not receive radiotherapy had higher mammographic screening sensitivity, yet a doubled risk of recurrence. Radiotherapy treatment was thought to reduce mammographic sensitivity as it leads to increased MD, and therefore higher risk of masking recurrences. There is a clear compromise between providing adequate risk reduction treatment and limiting alterations to the breast which can conceal recurrences. Four studies in this review described the need for a more tailored screening strategy, based on individual risk of recurrence.15,21,27,28 Perhaps due to the lack of evidence-based national guidance there is discordance in the follow-up protocols used across the country, varying in duration and frequency of mammographic surveillance provided.21 Current guidelines for surveillance recommendations which are thought to be employed by the majority of screening centres in the UK, may be considered too broad and do not factor for heterogeneity of the population. It has been suggested that age, stage of initial diagnosis, treatment type, and MD should be considered important factors in developing a strategy based on risk stratification for more individualised care. This method could help target appropriate mammographic surveillance
Please cite this article in press as: Curran J, How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.001
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to those who would benefit, and exploit the survival advantage of early detection. Many of the papers reviewed did not specify if they had used SFM or FFDM which may have had an impact on the sensitivity and specificity values recorded. A recent study however reported similar sensitivities and interval cancer rates for SFM and FFDM.7 Advancements in FFDM technology may further improve sensitivity of mammography to breast cancer recurrence after BCT, an example of such technology is DBT which demonstrated a significant increase in sensitivity and specificity of the screening mammogram and allowed surgical scarring to be effectively differentiated from cancer recurrence in a study by Mansour et al.30 Due to the restrictions of this study, other digital advancements could not be investigated in detail. Future studies may focus on comparisons between FFDM and other modalities/technologies in the detection of breast cancer recurrence. Most of the primary research obtained in this review was retrospective in design, therefore perhaps holds less weight than findings from that of clinical trials. There seemed to be a lack of empirical research which was acknowledged by some of the authors of the literature obtained, however some suggested that clinical trials were infeasible in this subject area due to ethical implications. Despite this, a large randomised controlled trial (MAMMO-50) is currently under way at Warwick Medical School which will generate information from a large number of UK based breast departments over a 30 year period. This trial will compare annual to biennial mammography for ladies treated with BCT or every three years for patients treated with mastectomy. The results will provide a solid evidence base to determine optimal screening frequency and duration for ladies fifty years or over following BCT.31 It should be noted that due to the lack of literature available surrounding this subject area it was difficult to refine my study to focus on either long term or short term surveillance, instead a more generalised overview is given. Although an extensive range of databases, and library catalogues were searched, all relevant information may not have been located. Furthermore, as a single reviewer my research may be assumed to be of less strength than that of a Cochrane-style systematic review. The evidence gathered in this review may help to give health professionals a better appreciation of some challenges of mammographic surveillance after BCT, and the sensitivity and test performance of the modality in detecting breast cancer recurrences in this patient group. Due to the insufficiency of empirical research available there are still many areas surrounding the subject that remain uncertain. This emphasises the need for future studies to provide a solid evidence base for practice in areas such as; the use of FFDM in detecting breast cancer recurrences, comparative studies to determine the optimal modality for breast cancer recurrence, and investigating alternative surveillance follow-up strategies based on risk of recurrence in individual patients. Implications for practice e conclusion Regular mammographic surveillance following BCT has been shown to facilitate early detection of asymptomatic breast cancer recurrences, which can provide a significant survival advantage to the patient. This is despite the fact that image quality is thought to be compromised to varying degrees due to surgical disfigurement, scar tissue overlay, increased breast density and limited compressibility of the breast. Although overall mammographic sensitivity is reduced after BCT, it is still proven to be effective in detecting recurrences in the ipsilateral and contralateral breast, and therefore remains an important surveillance tool. It is important to consider also that although ladies with a history of BCT will
generally feel more pain from follow-up mammograms, surveillance screening is still welcomed by these women due to the reassurance it provides. Technological developments in FFDM including DBT may further improve sensitivity in imaging the postsurgical breast, however more research is needed in this area. There is evidence to suggest that a more individualistic structure to mammographic surveillance would be beneficial, regarding frequency and duration of follow-up procedures. Anticipated future findings from the ongoing Mammo-50 trial will be hugely influential in providing a solid evidence-base from which decisions can be made to optimise screening strategy for ladies with a history of BCT. This could potentially maximise the survival advantage of early detection and minimise the adverse effects of unnecessary mammography and false positive results. With the rising demand for post-operative surveillance after treatment for early breast cancer, this strategy could elicit better use of breast screening services, improving efficiencies with a more patient centred approach and ultimately further improve long-term survival after BCT. Conflict of interest statement None declared. Acknowledgements
Joshua Rogers-Evans Zebby Rees Noel Curran Jayne Skillen Gillian Rogers Danielle Moakes Melanie Button Isobelle Puscus Katie Pyne
Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.radi.2016.02.001. References 1. Autier P, Boniol M, LaVecchia C, Vatten L, Gavin A, Hery C, et al. Disparities in breast cancer mortality rates between 30 European countries: retrospective trend analysis of WHO mortality database. Br Med J 2010;341(c3620):1e7. Available from: http://www.bmj.com/content/341/bmj.c3620.full.pdfþhtml [accessed 10.01.15]. 2. Northern Ireland Statistics and Research Agency. Publications and statistics. 2013. Available from: http://www.nisra.gov.uk/publications/default.asp.htm [accessed 10.01.15]. 3. National Records of Scotland. Statistics and data. 2014. Available from: http:// www.gro-scotland.gov.uk/statistics-and-data [accessed 10.01.15]. 4. Office of National Statistics. All releases of mortality statistics: deaths registered in England and Wales. 2014. Available from: http://www.ons.gov.uk/ons/ publications/all-releases.html?definition¼tcm:77-27475 [accessed 10.01.15]. 5. Neal CH, Yilmaz ZN, Noroozian M, Klein KA, Sundaram B, Kazerooni EA, et al. Imaging of breast cancer-related changes after surgical therapy. Am J Roentgenol 2014;202(2):262e72. Available from: http://www.ajronline.org/doi/pdf/ 10.2214/AJR.13.11517 [accessed 10.01.15]. 6. Lu WL, Jansen L, Post WJ, Bonnema J, Van de Velde JC, De Bock GH. Impact on survival of early detection of isolated breast recurrences after the primary treatment for breast cancer: a meta-analysis. Breast Cancer Res Treat 2009;114(3):403e12. Available from: http://link.springer.com/article/10.1007/ s10549-008-0023-4#page-1 [accessed 10.01.15]. 7. Nederend J, Duijm LEM, Louwman MWJ, Coebergh JW, Roumen RMH, Lohle PL, et al. Impact of the transition from screen-film to digital screening mammography on the interval cancer characteristics and treatment e a population based study from the Netherlands. Eur J Cancer 2014;50(1):31e9. Available from: http://www.ejcancer.com/article/S0959-8049(13)00893-9/pdf [accessed 15.02.15]. 8. Association of Breast Surgery at BASO. Surgical guidelines for the management of breast cancer. London: Elsevier Ltd.; 2009. Available from: http://www.
Please cite this article in press as: Curran J, How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.001
J. Curran / Radiography xxx (2016) 1e5
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
associationofbreastsurgery.org.uk/media/4565/surgical_guidelines_for_the_ management_of_breast_cancer.pdf [accessed 10.01.15]. Chansakul T, Lai KC, Slanetz PJ. The postconservation breast: part 2, imaging findings of tumor recurrence and other long-term sequelae. Am J Roentgenol 2012b;198(2):331e43. Available from: http://www.ajronline.org/doi/pdf/10. 2214/AJR.11.6881 [accessed 15.12.14]. Guitierrez R, Horst KC, Dirbas FM, Ikeda DM. Breast imaging following breast conservation therapy. In: Dirbas FM, Scott-Conner CFH, editors. Breast surgical techniques and interdisciplinary management. Washington: Springer; 2011. p. 975e95. Schneble EJ, Graham LJ, Shupe MP, Flynt FI, Banks KP, Kirkpatrick AD, et al. Current approaches and challenges in early detection of breast cancer recurrence. J Cancer 2014;5(4):281e90. Available from: http://www.jcancer.org/ v05p0281.pdf [accessed 10.01.15]. Puglisi F, Fontanella C, Numico G, Sini V, Evangelista L, Monetti F, et al. Followup of patients with early breast cancer: is it time to rewrite the story? Crit Rev Oncol Hematol 2014;91(2):130e41. Available from: http://ac.els-cdn.com/ S104084281400050X/1-s2.0-S104084281400050X-main.pdf?_tid¼0cf33aba0317-11e5-8761-00000aacb35d&acdnat¼1432583504_ 6419301dcb1ee4eaa382ffc72f218317 [accessed 15.12.14]. National Institute for Health and Care Excellence. Early and locally advanced breast cancer: diagnosis and treatment. London: National Institute for Health and Care Excellence; 2014. Available from: http://www.nice.org.uk/guidance/ cg80/resources/guidance-early-and-locally-advanced-breast-cancer-pdf [accessed 10.11.14]. Royal College of Radiologists. Guidance on screening and symptomatic breast imaging. London: Royal College of Radiologists; 2010. Available from: https:// www.rcr.ac.uk/sites/default/files/publication/BFCR%2813%295_breast.pdf [accessed 10.12.14]. Houssami N, Abraham LA, Miglioretti DL, Sickles EA, Kerlikowske K, Buist DSM, et al. Accuracy and outcomes of screening mammography in women with a personal history of early-stage breast cancer. J Am Med Assoc 2011;305(8): 790e9. Available from: http://jama.jamanetwork.com/article.aspx? articleid¼645792 [accessed 15.12.14]. Chansakul T, Lai KC, Slanetz PJ. The postconservation breast: part 1, expected imaging findings. Am J Roentgenol 2012a;198(2):321e30. Available from: http://www.ajronline.org/doi/pdf/10.2214/AJR.10.7298 [accessed 15.12.14]. Cil T, Fishell E, Hanna W, Sun P, Rawlinson E, Narod SA, et al. Mammographic density and the risk of breast cancer recurrence after breast conserving surgery. Cancer 2009;115(24):5781e7. Available from: http://onlinelibrary.wiley. com/doi/10.1002/cncr.24638/epdf [accessed 10.01.15]. Eriksson L, Czene K, Rosenberg L, Humphreys K, Hall P. Possible influence of mammographic density on local and locoregional recurrence of breast cancer. Breast Cancer Res 2013;15(4):1e9. Available from: http://breast-cancerresearch.com/content/pdf/bcr3450.pdf [accessed 10.01.15]. Groot JE, Broeders MJM, Branderhorst W, Den Heeten GJ, Grimbergen CA. Mammographic compression after breast conserving therapy: controlling pressure instead of force. Med Phys 2014;41(2). pp. 023501e1-023501023501-8. Available from: http://scitation.aip.org/docserver/fulltext/aapm/ journal/medphys/41/2/1.4862512.pdf?expires¼1432312517&id¼id&accname ¼guest&checksum¼BDA6BB2B6ECB2B53A3FA48BB5FA95013 [accessed 26.10.14].
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20. Mathers SA, Graham AM, Robertson EM. ‘It was daunting’ experience of women with a diagnosis of breast cancer attending for breast imaging. Radiography 2013;19(2):156e63. 21. Greenwood-Haigh L. Mammographic surveillance in the follow-up of early breast cancer in england: a cross-sectional survey. Radiography 2009;15(3): 220e7. Available from: http://www.radiographyonline.com/article/S10788174(08)00093-X/pdf [accessed 10.01.15]. 22. Arasu VA, Joe BN, Lvoff NM, Leung JWT, Brenner RJ, Flowers CI, et al. Benefit of semiannual ipsilateral mammographic surveillance following breast conservation therapy. Radiology 2012;264(2):371e7. Available from: http://www.ncbi. nlm.nih.gov/pmc/articles/PMC3401347/pdf/111458.pdf [accessed 10.01.15]. 23. Dershaw DD, Lee CH, Morris EA. Letters to the editor. Radiology 2013;266(2): 685. Available from: http://pubs.rsna.org/doi/pdf/10.1148/radiol.12121630 [accessed 10.01.15]. 24. Arasu VA, Joe BN, Lvoff NM, Leung JWT, Brenner RJ, Flowers CI, et al. Letter to the editor. Radiology 2013;266(2):685e6. Available from: http://pubs.rsna.org/ doi/pdf/10.1148/radiol.12121630 [accessed 10.01.15]. 25. Houssami N, Ciatto S, Martinello F, Bonardi R, Duffy SW. Early detection of second breast cancers improves prognosis in breast cancer survivors. Ann Oncol 2009;20(9):1505e10. Available from: http://annonc.oxfordjournals.org/ content/20/9/1505.full.pdfþhtml [accessed 15.12.14]. 26. Smallenburg VVB, Duijm LEM, Voogd AC, Jansen FH, Louwman WJ. Mammographic changes from benign breast surgery impair breast cancer detection at screening mammography. Eur J Cancer 2012;48(14):2097e103. Available from: http://0-ac.els-cdn.com.lispac.lsbu.ac.uk/S0959804912002663/1-s2.0-S09598 04912002663-main.pdf?_tid¼ab15b020-0573-11e5-bf93-00000aab0f26&ac dnat¼1432843185_839ab1e97a4e7c0539d021a1f3666707 [accessed 10.01.15]. 27. Buist DSM, Abraham LA, Barlow WE, Krishnaraj A, Holdridge RC, Sickles EA, et al. Diagnosis of second breast cancer events after initial diagnosis of early stage breast cancer. Breast Cancer Res Treat 2010;124(3):863e73. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2976764/pdf/nihms233 153.pdf [accessed 15.12.14]. 28. Drukteinis JS, Mooney BP, Flowers CI, Gatenby RA. Beyond mammography: new frontiers in breast cancer screening. Am J Med 2013;126(6):472e9. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4010151/pdf/ nihms571320.pdf [accessed 10.01.15]. 29. Robertson C, Ragupathy SKA, Boachie C, Fraser C, Heys SD, MacLennan G, et al. Surveillance mammography for detecting ipsilateral breast tumour recurrence and metachronous contralateral breast cancer: a systematic review. Eur Radiol 2011;21(12):2484e91. Available from: http://www.ncbi.nlm.nih.gov/pmc/ articles/PMC3217137/pdf/330_2011_Article_2226.pdf [accessed 10.01.15]. 30. Mansour S, Adel L, Mokhtar O, Sherif Omar O. Comparative study between breast tomosynthesis and classic digital mammography in the evaluation of different breast lesions. Egypt J Radiol Nucl Med 2014;45(3):1053e61. Available from: http://ac.els-cdn.com/S0378603X14000539/1-s2.0-S0378603X14000 539-main.pdf?_tid¼5810f9d4-0569-11e5-b8e000000aab0f6c&acdnat¼1432838751_21659c39dd6f49117b4b305d7579aeaa [accessed 10.02.15]. 31. Warwick Medical School. Mammo- 50 mammographic surveillance in breast cancer patients aged 50 years or older. 2015. Available from: http://www2. warwick.ac.uk/fac/med/research/hscience/ctu/trials/cancer/mammo50/ [accessed 16.01.16].
Please cite this article in press as: Curran J, How effective is mammography in detecting breast cancer recurrence in women after Breast Conservation Therapy (BCT) e A systematic literature review, Radiography (2016), http://dx.doi.org/10.1016/j.radi.2016.02.001