Edibaldo Silva, MD, PhD

 affirmed the long-term validity of breast-conserving surgery (BCS) for the management of early-stage breast cancer (ESBC). BCS is defined as lumpectomy with postoperative whole breast irradiation. Years earlier, in 1991, a National Cancer Institute Consensus Conference endorsed BCS over mastectomy as the preferred treatment of ESBC. Over the years, this led to a decrease in mastectomy rates. By 2003, BCS rates in the United States were approaching 69%.

 Surprisingly, this upward trend reversed after 2003, with the rate of women treated with BCS declining to 58%.

 The decrease in BCS has undermined the progress made over the last three decades in the management of ESBC, which has been firmly based on an accumulation of biological and clinical evidence of the natural history of this disease. 

It is difficult to fathom why rates of BCS are declining at a time when the average size of breast tumors in the United States is <2 cm at diagnosis. With increasingly smaller tumors, one might wonder why rates of margin positivity following BCS are as high as 31% to 50%.

 Nearly 50% of women who elect BCS must undergo subsequent mastectomy to clear these positive margins.

 Once informed consent has been obtained, the success of BCS is completely in the hands of the surgeon at the time of lumpectomy. This problem is not new, of course, and there are other factors that have contributed to the recidivism to mastectomy.

The recent discovery of the potential for magnetic resonance imaging (MRI) to reveal second cancers in a breast affected by ESBC has led many clinicians to recommend and patients to choose mastectomy for this ipsilateral breast. MRI of the ipsilateral breast reveals potential second tumors in as many as 13% to 30% of patients.

 The fact that second lesions are often found in a breast with ESBC is actually a “rediscovery,” because Holland described this likelihood more than 20 years ago, after performing detailed serial section histologic examinations of mastectomy specimens. Holland’s data suggested that as many as two-thirds of these patients had a second lesion within the same breast, most of which were located within 4 cm of the known primary.

 Holland’s data remains timely because, at the time, it was used as an admonition about the validity of BCS. The rediscovery with MRI that many patients have second lesions in the ipsilateral breast is being revisited as a reason for the increasing conversion from BCS to mastectomy in patients with ESBC.

Paradoxically, Japanese investigators recently offered an analysis similar to Holland’s to support the use of accelerated partial breast irradiation (APBI), which spares breast tissue outside of this 4-cm radius from radiation in women who undergo BCS.

 Favorable 4-year recurrence rates of 1% have been published for APBI; patients continue to be followed, and longer outcomes associated with APBI are expected in the future.

 Not surprisingly, a recent report shows that patients selected for BCS on the basis of unifocal disease identified by MRI and similarly treated patients who undergo BCS based on unifocal disease established by routine mammography have identical local recurrence rates (3%-4%) at 8 years’ follow-up.

This compares favorably to the recent update by the Early Breast Cancer Trialists’ report, which shows 10-year local failure rates of 8% for node-negative women undergoing mastectomy and 27% for node-positive women similarly treated. The addition of radiotherapy even in mastectomy patients led to a salutary decrease in local failure rates.

 In women undergoing systemic hormonal ablation or chemotherapy, local failure rates of 7% were noted by the National Surgical Adjuvant Breast and Bowel Project in a review of several of their trials involving BCS.

With increasingly smaller cancers disclosed by effective mammographic screening, the weight of 25 years of clinical experience, and the improvement in systemic therapies to date, it is difficult to see how the rediscovery of the long-recognized existence of subclinical tumors, which are mostly noninvasive and well controlled by contemporary radiotherapy, should discourage physicians and patients alike from BCS. As shown by the Mayo Clinic report, preoperative MRI raised a woman’s odds of undergoing mastectomy by 60% in 2006. Just having surgery in 2006 vs having surgery in 2003 raised her odds of having a mastectomy by 70%.

 This decrease in BCS is attributed to the use of MRI in 2006. Bleicher just reported similar increases in mastectomy rates in patients undergoing preoperative MRI (19% vs 27%).

The Problem With the Contralateral Breast

The introduction of MRI in breast diagnostics, coupled with inadequate risk assessment by clinicians and understandably fearful patients, has led to unnecessary preventive contralateral prophylactic mastectomy (CPM) in patients with ESBC. Many breast cancer specialists see second opinion requests for patients, young and old, who have opted for contralateral prophylactic mastectomy based on an MRI finding, without any histologic proof of cancer. Invariably, many clinicians making this recommendation do not have the ability to perform MRI-guided core biopsy of lesions not visible with mammography or ultrasonography. The distressing report by Tuttle has shown an increase in contralateral mastectomy from 4.2% in 1998 to 11% in 2003.

 In this report of 152,755 patients included in the Surveillance, Epidemiology and End Results cancer registry, 8.3% were aged ≥60 years at the time of contralateral mastectomy. Understandably, this figure increased to 25% among women aged 18 to 49 undergoing unilateral mastectomy for the treatment of their breast cancer. There can be no question that the greater use of MRI has accelerated this trend, as Tuttle’s report also shows that the contralateral mastectomy rate increased between 2000 and 2003.

It is concerning that the most common reason for CPM was physician’s advice regarding the risk of contralateral breast cancer. This negligible risk has been documented since the days of radical mastectomy and demonstrates how inadequate informed consent can be. The risk of contralateral disease is well established as 3% at 5 years.

 Furthermore, any risk of contralateral disease declines by 50% for patients using tamoxifen and 20% for those treated with chemotherapy.

 Clearly, prophylactic removal of the unaffected breast can have no impact on the survival of a patient in whom the stage of her index cancer is the primary determinant of survival. 

Remarkably, even in high-risk breast cancer patients undergoing prophylactic mastectomy, MRI missed 3 of 4 lesions noted at final pathology (of these, three-quarters were ductal carcinoma in situ), yet added great expense.

 At present, there is no question that the growing use of MRI by physicians unfamiliar with all its limitations, coupled with patients’ fear and an inadequate risk assessment, lead to the difficult conversations surgical oncologists have with patients at the time of informed consent. Many surgical oncologists find all the information hard to convey in a single visit. A thorough discussion may need to encompass information on pursuing reliable alternative surveillance and prevention strategies, along with accurate genetic risk assessment and its limitations, before resorting to alternatives that pre-date the Fisher-Veronese era of progress in breast cancer management.

 It is this wonderful explosion in our knowledge about breast cancer more than anything that affirms the need to use evidence-based algorithms within specialized multidisciplinary breast centers to care for the complicated problem of breast cancer. 

Fisher B, Anderson S, Bryant J, et al. Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. 

Veronesi U, Cascinelli N, Mariani L, et al. Twenty-year follow-up of a randomized study comparing breast-conserving surgery with radical mastectomy for early breast cancer. 

Katipamula R, Degnim AC, Hoskin T, et al. Trends in mastectomy rates at the Mayo Clinic Rochester: effect of surgical year and preoperative magnetic resonance imaging. 

Tuttle TM, Habermann EB, Grund EH, Morris TJ, Virnig BA. Increasing use of contralateral prophylactic mastectomy for breast cancer patients: a trend toward more aggressive surgical treatment. 

Singletary SE. Surgical margins in patients with early-stage breast cancer treated with breast conservation therapy. 

Huston TL, Pigalarga R, Osborne MP, Tousimis E. The influence of additional surgical margins on the total specimen volume excised and the reoperative rate after breast-conserving surgery. 

Cellini C, Huston TL, Martins D, et al. Multiple re-excisions versus mastectomy in patients with persistent residual disease following breast conservation surgery. 

Bluemke DA, Gatsonis CA, Chen MH, et al. Magnetic resonance imaging of the breast prior to biopsy. 

Berg WA, Gutierrez L, NessAiver MS, et al. Diagnostic accuracy of mammography, clinical examination, US, and MR imaging in preoperative assessment of breast cancer. 

Holland R, Veling SH, Mravunac M, Hendriks JH. Histologic multifocality of Tis, T1-2 breast carcinomas. Implications for clinical trials of breast-conserving surgery. 

Bedrosian I, Mick R, Orel SG, et al. Changes in the surgical management of patients with breast carcinoma based on preoperative magnetic resonance imaging. 

Sardanelli F, Giuseppetti GM, Panizza P, et al. Sensitivity of MRI versus mammography for detecting foci of multifocal, multicentric breast cancer in fatty and dense breasts using the whole-breast pathologic examination as a gold standard. 

Imamura H, Haga S, Shimizu T, et al. Relationship between the morphological and biological characteristics of intraductal components accompanying invasive ductal breast carcinoma and patient age. 

Beitsch PD, Vicini F, Zannis V, et al. Recurrence and survival in the American Society of Breast Surgeons MammoSite RTS Registry Trial [ASTRO abstract 5]. 

Solin LJ, Orel SG, Hwang WT, Harris EE, Schnall MD. Relationship of breast magnetic resonance imaging to outcome after breast-conservation treatment with radiation for women with early-stage invasive breast carcinoma or ductal carcinoma in situ.

Clarke M, Collins R, Darby S, et al. Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials. 

Wapnir I, Anderson S, Mamounas E, et al. Survival after IBTR in NSABP node negative protocols B-13, B-14, B-19, B-20 and B-23 [ASCO abstract 517]. 

Bleicher RJ, Ciocca RM, Egleston BL, et al. The influence of routine pretreatment MRI on time to treatment, mastectomy rate, and positive margins. In: Proceedings from the American Society of Clinical Oncology Breast Cancer Symposium; 2008; Washington, DC. Abstract 227.

Gao X, Fisher SG, Emami B. Risk of second primary cancer in the contralateral breast in women treated for early-stage breast cancer: a population-based study. 

Black D, Specht M, Lee JM, et al. Detecting occult malignancy in prophylactic mastectomy: preoperative MRI versus sentinel lymph node biopsy. 

Schwartz MD. Contralateral prophylactic mastectomy: efficacy, satisfaction, and regret. 

Edibaldo Silva, MD, PhD, is an associate professor of surgical oncology, Division of Surgical Oncology, at the University of Nebraska Medical Center in Omaha and a member of the editorial advisory board for 

Articles

Since 2003, the rate of women choosing breast-conserving surgery for the
management of early-stage breast cancer has declined, with an accompanying
recidivism to mastectomy. Edibaldo Silva, MD, PhD, examines the reasons for
the treatment regression.

Back to the Future:  Why Are More Women Having Bilateral Mastectomy for Unilateral Breast Cancer?

Advances in diagnostic imaging have led to general improvement in treating patients for various maladies. Recently, advances in breast diagnostic imaging with magnetic resonance imaging (MRI) in unselected patient populations have exposed a number of pitfalls that threaten well-established, data-proven medical practice. Recognition of these pitfalls should lead to clinical trials to resolve the more controversial issues and result in practice algorithms to support the use of breast MRI in targeted patient populations.

Diagnostic imaging with mammography has identified many more women with cancerous tumors smaller than 2 cm. Decrease in stage at presentation of these smaller tumors has led to a survival benefit beyond that expected by simple stage migration alone for patients with screen-detected cancer versus those whose cancers are detected by clinical examination.

 Decreases in mortality resulting from mammographic screening are estimated to be 46% and vary by the age of the cohort examined.

 Still, mammography misses about 20% of all breast cancer, particularly in young women with dense breast parenchyma.

Advances in breast imaging with MRI have heightened sensitivity in breast cancer detection, though at increased cost: the sensitivity gained is plagued by significant variation in specificity, with most studies showing it to be inferior to that of screening mammography.

 Comparison of the specificity and sensitivity of MRI versus mammography in breast cancer screening has been studied primarily in women at high risk for developing breast cancer, such as BRCA gene carriers. Even in the groups where young age compromises the reliability of mammography, MRI has resulted in additional recall examinations in 10.7% of women, compared with 3.9% for mammography.

 In turn, these additional exams have led to a 3-fold increase in recommendations for biopsy (3.1% vs 1.3%). The increased cost of MRI, with its attendant increase in repeat exams and biopsies in high-risk populations, is likely to forestall its application to the routine screening of all women, where the putative marginal advantage of the sensitivity of MRI over that of digital mammography in the 50-year-or-older group may be slim.

The role of MRI in the management of patients newly diagnosed with breast cancer represents the area of controversy where the accumulated evidence of the past 30 years provides significant insight into the pitfalls associated with routine MRI use. It is here where MRI interpretation has the most significant impact, and a possibly deleterious effect on the care of the patient. To become fully aware of these pitfalls, we must review some of the remarkable progress made over the past 40 years in our understanding of the history of breast cancer and its treatment.

 affirmed the long-term validity of breast-conserving surgery (BCS) for the management of early-stage breast cancer (ESBC). More than a decade earlier (in 1991), a National Cancer Institute Consensus Conference had endorsed BCS—margin-clear lumpectomy with postoperative whole-breast irradiation&mdash;over mastectomy as the preferred treatment of ESBC. This recommendation has been strengthened by the accumulating biological and clinical evidence of the natural history of this disease in patients with a single breast cancer documented by mammographic evaluation. When patients with ESBC are treated with BCS or mastectomy, local recurrence rates are the same at 5% to 10%.

 As discussed previously, the success of BCS has come from the increased use of screening mammography and the concomitant early diagnosis of smaller tumors.

Traditionally, BCS has been contraindicated in patients with multicentric disease (tumors in other quadrants of the breast) as documented by mammography at the time of diagnosis. The increasing use of MRI in patients with a known breast cancer has led to the detection of multiple lesions in patients who heretofore had only a single primary tumor identified by physical examination or mammography. The increased sensitivity of MRI in this setting leads to the identification of potential second cancers in the same breast in 13% to 30% of patients.

 Curiously, the presence of multifocal tumors in patients with even the smallest of breast cancers was noted by Holland more than 20 years ago in detailed serial section histologic examination of mastectomy specimens.

 In fact, Holland’s data suggested that as many as two-thirds of these patients had a second lesion within the same breast, with most of them mapping within 4 cm of the known primary. Holland‘s data remain timely because they were used then as an admonition about the validity of BCS. The rediscovery of these lesions by MRI is now revisited as a reason for the conversion from BCS to mastectomy in patients with ESBC.

 Paradoxically, an analysis similar to Holland’s recently reported by Japanese investigators supports the use of accelerated partial-breast irradiation (APBI), which spares the breast tissue outside this 4-cm radius from any radiation in BCS. In this setting, none of the multifocal lesions outside the quadrant in question would have been subjected to radiation therapy, and thus a higher local failure rate would have been expected.

 Favorable 4-year recurrence rates of 1% have been published for APBI, with longer follow-up continuing.

In a more remarkable study, conducted by Sardanelli, MRI was performed in women who had elected to undergo mastectomy for a single known cancer.

 Subsequent pathologic step section of the entire breast specimen using 5-mm sections in the manner of Holland then attempted to localize the patient’s primary cancer as well as any other suspected cancers detected by the preoperative MRI. In 99 breast specimens, mammography and MRI missed 64 and 36 malignant tumors, 8 mm and 5 mm in median size, respectively. In fact, MRI failed to detect 19% of the malignant foci discovered by the pathologic evaluation of the breast. Although MRI was more sensitive than mammography, its predictive positive value was low (only 70%) for both modalities. Therefore, even if patients were to be selected for BCS by MRI, 19% would have a second unknown primary cancer in the breast. This figure is clearly much higher than any reported local recurrence rate in patients treated with BCS and appropriate systemic therapy. Not surprisingly, a recent report shows that BCS patients selected on the basis of unifocal disease by MRI have identical local recurrence rates (3%-4%) at 8-year follow-up when compared with a similarly treated cohort undergoing BCS based on unifocal disease established by routine mammography only.

This compares favorably to the recent update by the Early Breast Cancer Trialists, which shows 10-year local failure rates of 8% for node-negative women undergoing a more deforming mastectomy and 27% for node-positive women similarly treated.

 Thus, with increasingly smaller cancers disclosed by effective mammographic screening, the added weight of 25 years of clinical experience, and the improvement in systemic therapies to date, it is difficult to see how the rediscovery of well-known subclinical tumors, which are well controlled by contemporary radiotherapy, should discourage physicians and patients alike from BCS. The resulting pitfalls in treatment recommendations resulting from indiscriminate use of breast MRI are shown by the Mayo Clinic report, in which preoperative MRI raised the odds of undergoing mastectomy by 60%, and in which having surgery in 2006 versus 2003 raised the odds by 70%.

 Bleicher just reported similar increases in mastectomy rates (19%-27%) in patients undergoing preoperative MRI.

 In Berg’s 2004 report, 12% of women chose an unneeded mastectomy without any biopsy to exclude malignancy of the questionable second ipsilateral lesion detected by MRI and which were determined at mastectomy not to be alignant.10 Thus, the adoption of MRI without any prospective data on its benefit in the management of ESBC undermines the long prospective and data-driven efficacy record of BCS compared with mastectomy. Indiscriminate use of breast MRI threatens to reverse breast conservation trends, to the detriment of women in the United States.

Examining contralateral prophylactic mastectomy 

More alarming is the parallel increasing trend of contralateral prophylactic mastectomy (CPM)— removal of the opposite, unaffected breast. The introduction of MRI in breast diagnostics, coupled with inadequate risk assessment by clinicians and understandable apprehension on the part of patients, has led to unnecessary preventive CPM in patients with ESBC. Many breast cancer patients opt for CPM based on an MRI finding without histologic proof of cancer. Invariably, many who make this recommendation do not have the ability to perform MRI-guided core biopsy of lesions not detected by mammography or ultrasonography. The distressing report by Tuttle has shown an increase in CPM from 4.2% in 1998 to 11% in 2003.

 In this report of 152,755 patients from the Surveillance, Epidemiology and End Results cancer registry, 8.3% were 60 or older at the time of CPM. Understandably, the figure was only 25% among women aged 18-49 years undergoing a unilateral mastectomy for the treatment of their breast cancer. There can be no question that this trend has been accelerated with the recent increased use of MRI, as Tuttle’s report also shows that the rate of CPM increased between 2000 and 2003.

 It is of concern that the most common reason for CPM was a physician’s characterization of the risk of contralateral breast cancer, known since the days of the radical mastectomy to be negligible. This exemplifies how damaging informed consent can be if it is inadequate.

The risk of contralateral disease is well established as 3% at 5 years.

 Furthermore, any risk of contralateral disease is decreased by 50% in patients using tomoxifen and by 20% in those treated with chemotherapy.

 Clearly, prophylactic removal of the unaffected breast can have no impact on the survival of a patient in whom the stage of the index cancer is the primary determinant of survival. Remarkably, even in high-risk breast cancer patients undergoing CPM, MRI missed 3 of 4 lesions (of these, 3/4 were ductal carcinoma in situ) noted at final pathology and treated at great additional cost.

There is no question that increased use of MRI by physicians not familiar with all its limitations, coupled with inordinate fear in patients and inadequate assessment of risk, has led to difficult conversations with patients at the time of informed consent. Many breast cancer specialists find that all this information is hard to convey during a single visit, as it may require discussion about BCS, fear of radiation therapy, surveillance strategies, and prevention strategies, as well as accurate genetic risk assessment. The pitfall here is that it is easier to recommend bilateral mastectomy than to adhere to data-driven practice patterns established over the past 30 years.

 Thus, the current indiscriminate use of MRI in the screening and management of breast cancer is associated with a significant negative impact to the breast cancer patient in the absence of any evidence that it improves surgical care or prognosis.

Edibaldo Silva, MD, is attending surgical oncologist, Division of Surgical 

Oncology, University of Nebraska Medical Center’s Eppley Cancer Center, Omaha, Nebraska. He is also the program leader of the Melanoma & Soft Tissue Sarcoma service and manages breast cancer patients at the Olson Breast Center of the University of Nebraska Medical Center. 

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14. Beitsh P,Vicini F, Zannis V, et al. Recurrence and survival in the American Society of Breast Surgeons (ASBS) MammoSite® RTS Registry Trial. Int J Radiat Oncol Biol Phys. 2008;72(suppl 1):S2-S3. No abstract available online.

15. Sardanelli F, Giuseppetti GM, Panizza P, et al. Sensitivity of MRI versus mammography for detecting foci of multifocal, multicentric breast cancer in fatty and dense breasts using the whole-breast pathologic examination as the gold standard. AJR Am J Roentgenol. 2004;183(4):1149-1157. Abstract available at: 

16. Solin LJ, Orel SG, Hwang WT, et al. Relationship of breast magnetic resonance imaging to outcome after breast-conservation treatment with radiation for women with early-stage invasive breast carcinoma or ductal carcinoma in situ. J Clin Oncol. 2008;26(3):386-391. Abstract available at: 

17. Clarke M, Collins R, Darby S, et al. Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials. Lancet. 2005;366(9503):2087-2106. Abstract available at: 

18. Katipamula R, Degnim AC, Hoskin T, et al. Trends in mastectomy rates at the Mayo Clinic Rochester: effect of surgical year and preoperative magnetic resonance imaging. J Clin Oncol. 9009;27(25):4082-4088. Abstract available at: 

19. Bleicher RJ, Ciocca RM, Egleston BL, et al. Association of routine pretreatment magnetic resonance imaging with time to surgery, mastectomy rate and margin status. J Am Coll Surg. 2009;209(2):180-187. Abstract available at: 

20. Tuttle T, Haberman E, Grund E, et al. Increasing use of contralateral prophylactic mastectomy for breast cancer patients: a trend toward more aggressive surgical treatment. J Clin Oncol. 2007;25(33):5203-5209. Abstract available at: 

21. Gao X, Fisher SG, Emami B. Risk of second primary cancer in the contralateral breast in women treated for early-stage breast cancer: a population-based study. Int J Radiat Oncol Biol Phys. 2003;56(4):1038-1045. Abstract available at: 

22. Black D, Specht M, Lee J, et al. Detecting occult malignancy in prophylactic mastectomy: preoperative MRI versus sentinel lymph node biopsy. Ann Surg Oncol. 2007;14(9):2477- 2484. Abstract available at: 

23. Schwartz M. Contralateral prophylactic mastectomy: efficacy, satisfaction, regrets. 23. J Clin Oncol. 2005;23(31):7777-7779. No abstract available online.

24. Houssami N, Hayes DF. Review of preoperative magnetic resonance imaging (MRI) in breast cancer: should MRI be performed on all women with newly diagnosed, early stage breast cancer? CA Cancer J Clin. 2009;59(5):290-302. Abstract available at: 

Advances in diagnostic imaging have led to general improvement in treating patients for various maladies. Recently, advances in breast diagnostic imaging with magnetic resonance imaging (MRI) in unselected patient populations have exposed a number of pitfalls that threaten well-established, data-proven medical practice. 

Edibaldo Silva, MD, PhD

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