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10.1245/ASO.2006.03.098
Annals of Surgical Oncology 13:333-339 (2006)
© 2006 Society of Surgical Oncology
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Original Article

A Pathologic Assessment of Adequate Margin Status in Breast-Conserving Therapy

Mary F. Dillon, MB, MRCSI1,2, Arnold D. K. Hill, MCh, FRCSI1,2,3, Cecily M. Quinn, MD, FRCPI, FRCPath3,4, Enda W. McDermott, MCh, FRCSI1,3 and Niall O’Higgins, MCh, FRCSI1,3

1 Department of Surgery, St. Vincent’s University Hospital, Elm Park, Dublin 4, Ireland
2 Conway Institute of Biomolecular & Biomedical Research, University College Dublin, Dublin 4, Ireland
3 BreastCheck, Merrion Unit, National Breast Screening Programme, Merrion Road, Dublin 4, Ireland
4 Department of Pathology, St. Vincent’s University Hospital, Elm Park, Dublin 4, Ireland

Correspondence: Address correspondence and reprint requests to: Arnold D. K. Hill, MCh, FRCSI; E-mail: adkhill{at}rcsi.ie.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: The definition of a clear margin in breast-conserving therapy is uncertain. The purpose of this study was to correlate the tumor-margin distance of the excision specimen with the presence of residual tumor at reoperation. We also analyzed predictors of compromised margins and of residual disease.

Methods: All patients who underwent breast-conserving therapy for invasive disease from 1999 to 2003 were reviewed. Pathologic characteristics and the precise tumor distance from the radial margin were recorded. A radial margin was compromised if invasive or (ductal) in situ carcinoma was <5 mm from the margin.

Results: Of the 612 patients who underwent breast conservation, 211 (34%) had compromised margins, and 39 had undetermined margins. Of the 161 patients who had a reoperation for compromised margins, 87 (54%) had residual disease. Residual disease after reoperation was present in 58% (56 of 96),56 % (9 of 16), and 45% (22 of 49) of those with tumor-margin distances <1 mm, ≥1 and <2 mm, and ≥2 and <5 mm, respectively. There was a progressive decline in residual disease for each millimeter until a rate of 22% for tumor-margin distances of ≥4 mm and <5 mm was reached. Pathologic size (P = .004), an extensive intraductal component (P = .002), referral from a symptomatic rather than a population-based screening program (P = .02), and the absence of a preoperative diagnosis by core biopsy (P < .0001) were predictive of compromised margins. Only young age (<45 years) was predictive of finding residual disease on reoperation (P = .02).

Conclusions: A total of 45% of patients who had tumor 2 to 5 mm from the radial margin had residual disease on reoperation. Our results support a policy of requiring a 5-mm margin in patients undergoing breast-conserving therapy for invasive disease.

Key Words: Breast-conserving therapy • Residual tumor • Histopathology • Breast neoplasm


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
There is no clear consensus in the surgical community over the definition of an acceptable margin width in breast-conserving therapy (BCT).1 Most studies relating to margin status consider a tumor margin distance of <1 mm2–7 or <2 mm8,9 to represent a compromised margin. Occasionally centers report the use of a 5-mm criterion.1 This variation in practice has been highlighted in a recent report calling for the emergence of consistent guidelines.1 The importance of tumor margin distance is underscored by substantial evidence that positively involved margins constitute a highly significant predictor of local recurrence2,3,10–15 as a result of the increased probability of residual disease. Whether close margins have the same relationship to recurrence is still controversial. 2,6,7,10,16,17 However, the finding of residual tumor in up to 63%18–20 of re-excision specimens implies the need for wider margins. This study focuses on the relationship between precise tumor-margin widths and the presence of residual disease.

This study also seeks to identify risk factors for compromised margins and the presence of residual disease in patients undergoing BCT. Previous studies have documented tumor size,8,20,21 nodal positivity, 8,22 grade,20 method of detection,8 and an extensive intraductal component (EIC)10,22,23 as factors correlated with residual tumor. The identification of significant factors before surgery may help to select patients for a more extensive excision or mastectomy and assist in counseling patients that they may require a second procedure after BCT.

Finally, one of the most important changes over the past decade has been the transition from diagnostic excision procedures to preoperative diagnosis by core biopsy. The effect of this change in reducing compromised margins and operative procedures is not clear.

In this study, we considered a tumor-margin width of <5 mm as representing a compromised margin. The primary aim of this study was to correlate the precise tumor-margin width with rates of residual disease on reoperation. This may aid surgeons in the development of their own institutional policies regarding margin protocol. As a secondary aim, we analyzed predictors of compromised margins and of residual disease.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The study population comprised 612 patients who presented to the symptomatic (n = 391) and screening (n = 221) services of St. Vincent’s University Hospital over a 5-year period (January 1999 to September 2003) and underwent BCT for invasive disease. Patients were identified from a database of clinical information relating to these patients. The symptomatic clinic was attended by patients who were referred with breast abnormalities, typically palpable lesions, by their primary care physicians. The screening population was derived from women attending the Irish National Breast Screening Programme (BreastCheck), a population-based screening program that offers mammographic screening to all women aged 50 to 64 years. Patients who were excluded from the analysis included those who received neoadjuvant therapy and those who had re-excision for reasons other than compromised margins.

Wide local excision specimens were examined according to the UK Royal College of Pathologists Cancer Screening Programmes guidelines.24 Each specimen was oriented by the surgeon by using metal clips (one medial, two anterior, and three superior) and sutures (long, lateral, short, superior, and double deep) according to standard protocol. Specimen radiography was performed, without compression, in the operating room, and a copy was sent with the specimen to the pathology laboratory. The specimen was weighed, measured in three dimensions, and inked by using the alcohol, India ink, and Bouin’s fluid marking regimen. Differential inking was performed in nonradioactive specimens. The specimen was incised to assist fixation. After fixation, the specimen was sliced at 3- to 5-mm intervals in the anteroposterior plane perpendicular to the mediolateral axis. Individual slice radiographs were performed in specimens removed for calcification. Detailed macroscopic examination was performed, including documentation of tumor size and location and the tumor-margin distance for all six margins (anterior, posterior, medial, lateral, superior, and inferior). By using the macroscopic and slice radiograph findings for guidance, tissue blocks were selected for microscopic examination from all six margins, in addition to multiple tumor blocks and representative blocks from the remainder of the specimen, including skin. Separate re-excision specimens taken at the time of the initial operation or during a second procedure were sliced at 3- to 5-mm intervals, radiographed as appropriate, and blocked extensively for histological evaluation.

The tumor-margin distance was specified for each margin with respect to the presence of ductal carcinoma in situ, invasive carcinoma, or both. The margins were considered compromised if foci of ductal carcinoma-in-situ or invasive carcinoma were found within 5mm from the radial resection margin. The presence of lobular carcinoma-in-situ or atypical ductal or lobular hyperplasia was not considered to affect margin status. Patients whose radial margins (superior, inferior, medial, or lateral) were compromised were candidates for reoperation. Re-excision was not indicated for tumor-margin distances of ≥5 mm.

A proportion (n = 269) of patients had a wire inserted before surgery by radiologists to guide excision. Intraoperative ultrasonography was not used in our institution. In patients who did not have a preoperative histological diagnosis, the diagnostic excision was considered as the first operation. Re-excisions were directed toward former close or compromised margins.

The total number of procedures needed to obtain clear margins and the overall final mastectomy rate were determined for cases with compromised margins. Statistical analysis was performed with SPSS (version 11; SPSS Inc., Chicago, IL) statistical software. Chi-squared analysis was used for categorical variables, and the Mann-Whitney U-test was used for continuous variables.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Study Population and Margin Status
Six hundred twelve patients underwent BCT. Of these, 211 (34%) had ≥1 radial margins <5 mm. In a further 39 cases, the definitive margin status was not documented. Seventy-six percent of patients (161 of 211) with a tumor-margin distance <5 mm underwent reoperation. Eighty-seven (54%) of those who underwent reoperation had residual disease. Twelve of the 39 patients with inadequately documented margin status had a further operation, 3 of whom had residual disease.

Effect of Margin Width on Residual Disease
The relationship between the tumor-margin distance and the presence of residual disease on re-excision is shown in Table 1Go and Fig. 1Go. Twenty-two (45%) of 49 patients with tumors ≥2 and <5 mm from the radial resection margin had residual disease on reoperation. The probability of residual cancer being discovered on reoperation declined for every increasing millimeter of distance between the tumor and margin until a rate of 22% was found for tumor-margin distances of ≥4 and <5 mm.


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  		TABLE 1. Margin distance related to the presence of residual disease found at reoperation
 

Figure 1
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  		FIG. 1. Tumor-margin distance related to the presence of residual disease found at reoperation. P = .03; {chi}2 test for trend.

 
Predictors of Compromised Margins
The characteristics of tumors with negative margins are compared with those of tumors with compromised margins in Table 2Go. Size (P = .04), the presence of EIC, referral from a symptomatic service rather than a population-based screening program (P = .018), and not having a preoperative diagnosis of malignancy on core biopsy (P < .001) increased the risk of compromised margins. Invasive lobular carcinoma also had an increased risk of compromised margins (P = .024).


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  		TABLE 2. Comparison of characteristics of patients who had negative margins on first excision versus those who had compromised margins
 
Predictors of Residual Disease
Fifty-four percent of patients (n = 87) who underwent reoperation had residual disease. No pathologic characteristic of the tumor was found to increase the risk of having residual disease (Table 3Go). However, 17 % (15 of 87) with residual disease, compared with 4% (3 of 74) with no residual disease, were <45 years old (P = .017).


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  		TABLE 3. Comparison of patients who had residual disease on re-excision versus those who did not
 
Further Operations
One hundred sixty-one patients had a second operation for compromised margins, and 24 patients (15%) had more than 2 operations. Eighty-eight (55%) of the 161 who did not have a successful initial breast-conservation procedure underwent an eventual mastectomy. Ninety-two patients had re-excision of margins as their second operation, and in 54 (59%) of these patients, clear margins were obtained.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Our approach to margin status in invasive disease has permitted us to examine the relationship of residual disease in the re-excision specimen with respect to exact tumor-margin distances of up to 5 mm. It should be the aim of every surgeon to reduce tumor burden to a minimum in breast conservation. Our results demonstrate that a tumor-margin distance of <1 to 2 mm is not enough to safeguard against the eventuality of leaving behind a high incidence of residual disease. Tumors as far as 2 to 5 mm from the resection margin had a 45% chance of cancer being identified on reoperation.

The risk of residual tumor being found at re-excision in various studies has been quoted at up to 63%,18 particularly in studies with a high proportion of diagnostic excisions. In this study, despite a high preoperative diagnostic rate and the use of a 5-mm criterion for "clear" margins, we found that residual tumor rates on reoperation were high. We analyzed, for every millimeter distant from the margin, the corresponding rate of residual cancer found at re-excision. There was a consistently high rate of residual carcinoma as the tumor-margin width increased which gradually declined until a rate of 22% was reached for margins just smaller than 5 mm. The level of residual disease found beyond 5 mm was not examined in this study. The results of this study emphasize that the risk of residual disease is high even with a clear margin of 2 mm. Our study has some support from Pittinger et al.16 who defined close margins as ≤3 mm and found that of those who had positive margins that were re-excised, residual carcinoma was found in 44%, compared with 25% (6 of 24) in those who had close margins. In a pathologic study of potentially conservable breast tumors by Holland et al.25 cancerous foci were found within 2 cm of the reference tumor in 20% of patients. In a further 43% of patients, cancerous foci were found at more than this distance.

The clinical relevance of residual disease remains controversial. The weight of evidence supports the view that positive margins increase local recurrence rates (LRRs),2,3,10–15 and in addition margins are often found as the only or most potent predictor of local regional recurrence.3,10 The most plausible explanation for this is that positive margins are associated with high rates of residual disease and that radiotherapy alone is not sufficient to eliminate residual tumor burden in these cases. The question of whether close margin status affects local regional recurrence is unresolved.2,6,7,10,16,17 Lack of consistency in the definition of close margin, variations in radiotherapy, and the decision by some authors to increase their radiation dose according to the proximity of the cancer to the margins contribute to the lack of clear consensus and results. The evidence conflicts over whether close margins have a risk similar to negative margins or, alternatively, have an intermediate risk between positive and negative margins. In a study by Smitt et al.12 it was found that re-excision conveyed a local control benefit for patients with close, indeterminate, or positive initial margins, and Ryoo et al.26 found that failure to deliver a boost radiation dose when the tumor was present at or close to the margin of the specimen was associated with an increased LRR. Singletary,17 in an analysis of 34 studies, found an overall significant correlation with positive margin status and LRR. She concluded that because of the heterogeneity of trials, there was conflicting evidence over whether close margins—as opposed to positively involved margins—affected LRR. One of the few studies using a 5-mm criterion for margin width demonstrated a significantly increased rate of local recurrence in compromised versus negative margins. 27

Although further consensus from trials on the effect of close, as opposed to positive, margins on LRR is needed, our study illustrates the spectrum of residual disease that may be expected with given margins. It is most probable that the rate of LRR is increased in patients with positive margins because of an associated high rate of residual disease. In this study we have shown this residual disease to gradually decrease with distance from the margin. It is still unclear what the acceptable threshold is for residual disease that can be safely dealt with by radiotherapy. There are also concerns that radiotherapy may not always cover the entire tumor bed in all cases.28 This study demonstrates that there is a 58% risk of residual disease if a 1-mm clear margin is accepted, compared with a risk of 22% if a clear margin of 5 mm is used. If the surgeon is concerned about residual disease and if cosmesis is unlikely to be affected, a 5-mm margin may be a more acceptable standard of care.

A secondary aim of this study was to determine whether there were any preoperative or primary tumor characteristics that may predict the likelihood of either compromised margins or residual disease. Tumor size, the presence of EIC, referral from a symptomatic rather than a breast-screening service, and not having a preoperative histological diagnosis of cancer significantly affected compromised margin rates. The finding that T2 tumors (>2 cm) were more likely to have positive margins is supported by the findings of Wazer et al.9 Similarly, it is likely that patients with screen-detected breast tumors have an increased rate of negative margins as a result of their smaller tumor size at detection, and we have previously shown that this group of patients are more likely to undergo BCT than symptomatic patients.29 Most (90%) of our patients had a preoperative diagnosis. Our results confirm that a preoperative diagnosis by core biopsy statistically reduces the risk of compromised margins. A preoperative diagnosis allows surgeons to excise therapeutically and gives them a rationale for achieving wider margins. The trend over the past decade to move away from diagnostic excision biopsies toward preoperative diagnosis in breast cancer patients has proven to be an important development in achieving an overall better margin status and improving patient care.

Clinically, predictors of residual disease may be more important than predictors of compromised margins. The studies that have tried to correlate primary tumor characteristics with the risk of residual disease have identified tumor size,8,20,21 nodal positivity,8,22 grade,20 method of detection,8 and EIC10,22,23 as factors associated with residual carcinoma. The only factor we found that increased the probability of finding residual disease was being of an age <45 years. Young age was also noted as a risk factor for residual disease in studies by Smitt et al.10 and Wazer et al.9 It has been suggested that this may be a result of an attempt by surgeons to conserve more of the breast in younger women. With the 5-mm protocol that we use, this may not be an adequate explanation for this finding. We did not find that any primary tumor characteristic, including size, predicted residual disease.

In addition, this study found that EIC was not a predictor of residual disease. EIC has previously been thought of as a relative contraindication for BCT. The presence of EIC has been associated with an increased risk of local failure in some studies,30–32 even in the presence of negative margins.30 However, other studies have not supported these findings.2,33 The higher local failure rate was attributed to higher rates of residual disease associated with EIC.4,5,9,12,23 Vicini et al.31 found that in EIC-positive patients, the largest resections were associated with a significantly lower risk of recurrence when compared to the lowest volume resections. The current study found, as others have,7,13 that EIC is a predictor of compromised margins. However, EIC was not found to be associated with residual disease, and this may be due to the wider margins used in our study.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
This study has demonstrated that accepting a microscopic tumor-margin width criterion of <2 mm is associated with a high risk of residual disease, and this risk decreases progressively for each additional millimeter of margin obtained. Obtaining a preoperative diagnosis of breast cancer and then attempting to achieve wider therapeutic margins at the time of operation can considerably reduce the risk of residual disease.

Received for publication March 28, 2005. Accepted for publication September 8, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

  1. Taghian A, Mohiuddin M, Jagsi R, Golberg S, Ceilley E, Powell S. Current perceptions regarding surgical margin status after breast-conserving therapy: results of a survey. Ann Surg 2005; 241:629–39.[CrossRef][Medline]
  2. Park CC, Mitsumori M, Nixon A, et al. Outcome at 8 years after breast-conserving surgery and radiation therapy for invasive breast cancer: influence of margin status and systemic therapy on local recurrence. J Clin Oncol 2000; 18:1668–75.[Abstract/Free Full Text]
  3. Spivack B, Khanna MM, Tafra L, Juillard G, Giuliano AE. Margin status, local recurrence after breast conserving therapy. Arch Surg 1994; 129:952–7.[Abstract]
  4. Schnitt SJ, Connolly JL, Khettry U, et al. Pathological findings on re-excision of the primary site in breast cancer patients considered for treatment by primary radiation therapy. Cancer 1987; 59:675–81.[CrossRef][Medline]
  5. Beron PJ, Horwitz EM, Martinez AA, et al. Pathologic and mammographic findings predicting the adequacy of tumour excision before breast-conserving therapy. AJR Am J Roentgenol 1996; 167:1409–14.[Abstract/Free Full Text]
  6. Tartter PI, Kaplan J, Bleiweiss I, et al. Lumpectomy margins, reexcision, and local recurrence of breast cancer. Am J Surg 2000; 179:81–85.[CrossRef][Medline]
  7. Gage I, Schnitt SJ, Nixon AJ, et al. Pathological margin involvement and the risk of recurrence in patients treated with breast-conserving therapy. Cancer 1996; 78:1921–28.[CrossRef][Medline]
  8. Jardines L, Fowble B, Schultz D, et al. Factors associated with a positive reexcision after excisional biopsy for invasive breast cancer. Surgery 1995; 118:803–9.[CrossRef][Medline]
  9. Wazer DE, Schmidt-Ullrich RK, Ruthazer R, et al. The influence of age and extensive intraductal component histology upon breast lumpectomy margin assessment as a predictor of residual disease. Int J Radiat Oncol Biol Phys 1999; 45:885–91.[CrossRef][Medline]
  10. Smitt MC, Nowels K, Carlson RW, Jeffrey SS. Predictors of re excision findings, recurrence after breast conservation. Int J Radiat Oncol Biol Phys 2003; 57:979–85.[CrossRef][Medline]
  11. Anscher MS, Jones P, Prosnitz LR, et al. Local failure and margin status in early-stage breast carcinoma treated with conservation surgery and radiation therapy. Ann Surg 1993; 218:22–8.[Medline]
  12. Smitt MC, Nowels KW, Zdeblick MJ, et al. The importance of the lumpectomy surgical margin status in long term results of breast conservation. Cancer 1995; 77:259–67.
  13. Schnitt SJ, Abner A, Gelman R, et al. The relationship between microscopic margins of resection and the risk of local recurrence in patients with breast cancer treated with breast-conserving surgery and radiation therapy. Cancer 1994; 74:1746–51.[CrossRef][Medline]
  14. Meric F, Mirza NQ, Vlastos G, et al. Positive surgical margins and ipsilateral breast tumour recurrence predict disease-specific survival after breast conserving therapy. Cancer 2003; 97:926–33.[CrossRef][Medline]
  15. Leong C, Boyages J, Jayasinghe UP, et al. Effects of margins on ipsilateral breast tumour recurrence after breast conservation therapy for lymph node negative breast carcinoma. Cancer 2004; 100:1823–32.[CrossRef][Medline]
  16. Pittinger TP, Maronian NC, Poulter CA, Peacock JL. Importance of margin status in outcome of breast-conserving surgery for carcinoma. Surgery 1994; 116:605–9.[Medline]
  17. Singletary SE. Surgical margins in patients with early-stage breast cancer treated with breast conservation therapy. Am J Surg 2002; 184:383–93.[CrossRef][Medline]
  18. Solin LJ, Fowble B, Martz K, Goodman RL. Results of reexcisional biopsy of the primary tumor in preparation for definitive irradiation of patients with early stage breast cancer. Int J Radiat Oncol Biol Phys 1986; 12:721–25.[Medline]
  19. Millar AR, Brandao G, Prihoda TJ, Hill C, Cruz AB, Yeh I. Positive margins following surgical resection of breast carcinoma: analyses of pathological correlates. J Surg Oncol 2004; 86:134–40.[CrossRef][Medline]
  20. Cellini C, Hollenbeck ST, Christos P, et al. Factors associated with residual breast cancer after re-excision for close or positive margins. Ann Surg Oncol 2004; 11:915–20.[Abstract/Free Full Text]
  21. Gwin JL, Eisenberg BL, Hoffman JP, Ottery FD, Boraas M, Solin LJ. Incidence of gross, microscopic carcinoma in specimens from patients with breast cancer after re-excision lumpectomy. Ann Surg 1993; 218:729–34.[Medline]
  22. Landheer MLEA, Klinkenberg JHG, Pasker-de Jong PCM, Wobbes T. Residual disease after excision of non-palpable breast tumours: analysis of tumour characteristics. Eur J Surg Oncol 2004; 30:824–8.[Medline]
  23. Holland R, Connolly J, Gelman R, et al. The presence of an extensive intraductal component following a limited resection correlates with prominent residual disease in the remainder of the breast. J Clin Oncol 1990; 8:113–8.[Abstract/Free Full Text]
  24. The Royal College of Pathologists. NHS Cancer Screening Programmes. Pathology Reporting of Breast Disease. NHS BSP Publication No. 58. 2005. Available: http://www.cancerscreening.nhs.uk/breastscreen/publications/nhsbsp58-high-resolution.pdf.
  25. Holland R, Veling SH, Mravunac M, Hendriks JH. Histological multifocality of Tis T1-2 breast carcinomas. Cancer 1985; 56:979–90.[CrossRef][Medline]
  26. Ryoo MC, Kagan AR, Wollin M, et al. Prognostic factors for recurrence and cosmesis in 393 patients after radiation therapy for early mammary carcinoma. Radiology 1989; 172:555–9.[Abstract/Free Full Text]
  27. Horiguchi J, Iino Y, Takei H, et al. Surgical margin and breast recurrence after breast-conserving therapy. Oncol Rep 1999; 6:135–8.[Medline]
  28. Bedwinek J. Breast conserving surgery, irradiation: the importance of demarcating the excision cavity with surgical clips. Int J Radiat Oncol Biol Phys 1993; 26:675–9.[Medline]
  29. Dillon MF, Hill AD, Quinn C, et al. Surgical intervention in screen-detected patients versus symptomatic patients with breast cancer. J Med Screen 2004; 11:130–4.[Medline]
  30. Jacquemier J, Kurtz JM, Amalric R, Brandone H, Ayme Y, Spitalier JM. An assessment of extensive intraductal component as a risk factor for local recurrence after breast conserving therapy. Br J Cancer 1990; 61:873–6.[Medline]
  31. Vicini FA, Eberlein TJ, Connolly JL, et al. The optimal extent of resection for patients with stages I or II breast cancer treated with conservative surgery and radiotherapy. Ann Surg 1991; 214:200–5.[Medline]
  32. Schnitt SJ, Connolly JL. Processing, evaluation of breast excision specimens. A clinically orientated approach. Am J Clin Pathol 1992; 98:125–37.[Medline]
  33. Fisher ER, Sass R, Fisher B, Gregorio R, Brown R, Wickerham L. Pathological findings from the National Surgical Adjuvant Breast Cancer Project (protocol 6) II: relation of local breast recurrence to multicentricity. Cancer 1986; 57:1717–24.[CrossRef][Medline]



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