0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Original Article |

Risk Factors for Invasive Breast Cancer When Core Needle Biopsy Shows Ductal Carcinoma In Situ FREE

Emil D. Kurniawan, BMedSc; Allison Rose, MBBS, FRANZCR, MMed; Arlene Mou, MBBS, FRANZCR; Malcolm Buchanan, MBBS, FRCPA; John P. Collins, MBBS, FRACS; Matthew H. Wong, MBBS, BMedSc; Julie A. Miller, MD, FRACS; G. Bruce Mann, MBBS, PhD, FRACS
[+] Author Affiliations

Author Affiliations: Departments of Surgery (Drs Kurniawan, Collins, Wong, Miller, and Mann), Radiology (Drs Rose and Mou), and Pathology (Dr Buchanan), The Royal Melbourne Hospital, University of Melbourne, Melbourne, Victoria, Australia; and Breast Unit, Royal Women's Hospital, Parkville, Victoria, Australia (Dr Mann).


Arch Surg. 2010;145(11):1098-1104. doi:10.1001/archsurg.2010.243.
Text Size: A A A
Published online

Hypothesis  A core needle biopsy (CNB) diagnosis of ductal carcinoma in situ (DCIS) may be associated with a final diagnosis of invasive cancer. Preoperative radiologic, clinical, and pathological features may identify patients at high risk of diagnostic upstaging, who may be appropriate candidates for sentinel node biopsy at initial surgery.

Design  Review of prospectively collected database.

Setting  Tertiary teaching referral hospital and a population-based breast screening center.

Patients  Consecutive patients from January 1, 1994, to December 31, 2006, whose CNB findings showed DCIS or DCIS with microinvasion.

Main Outcome Measures  Upstaging to invasive cancer.

Results  Eleven of 15 cases of DCIS with microinvasion (73.3%) and 65 of 375 cases of DCIS (17.3%) were upstaged to invasive cancer. Ten of 21 palpable lesions (47.6%) were found to have microinvasion. For impalpable DCIS, multivariate analysis showed that noncalcific mammographic features (mass, architectural distortion, or nonspecific density) (odds ratio [95% confidence interval], 2.00 [1.02-3.94]), mammographic size of 20 mm or greater (2.80 [1.46-5.38]), and prolonged screening interval of 3 years or longer (4.41 [1.60-12.13]) were associated with upstaging. The DCIS grade on CNB was significant on univariate analysis (P = .04). The rate of upstaging increased with the number of significant factors present in a patient: 8.3% in patients with no risk factors, 20.8% in those with 1 risk factor, 39.6% in those with 2 risk factors, and 57.1% in those with 3 risk factors.

Conclusions  The risk of upstaging can be estimated by using preoperative features in patients with DCIS on CNB. We propose a management algorithm that includes sentinel node biopsy for patients with DCIS who have microinvasion on CNB, palpable DCIS, 2 or more predictive factors, and planned total mastectomy.

Percutaneous core needle biopsy (CNB) of suspicious breast lesions is now standard practice, replacing diagnostic open biopsy in most clinical situations.1 The advantages of this change have been to reduce the number of benign surgical biopsy results and to allow appropriate definitive surgical treatment to occur in a single visit to the operating room in most cases.2,3

A significant proportion of neoplastic breast lesions identified in a mammographic screening program are ductal carcinoma in situ (DCIS). Percutaneous CNB is used to differentiate between DCIS and invasive cancer. This distinction is important because it may determine the extent of surgery. Because DCIS is a preinvasive condition, axillary staging is not part of standard surgical treatment.3,4 There is inherent underestimation of invasive cancer in CNB because of the limited amount of tissue taken.5 Published series report that CNB underestimates the number of invasive cancers by 9% to 44%.614 Patients with DCIS on CNB who are treated with breast surgery alone and found to have invasive cancer generally require additional surgery to evaluate their lymph node status. Some studies suggest that sentinel node biopsy (SNB) after breast surgery has a higher failure rate15,16; therefore, it is preferable to stage the axilla during the first surgical procedure if it is deemed necessary.

An SNB could be routinely performed at the time of the first surgical procedure, but the procedure carries some risk, SNB adds significantly to the cost of the procedure, and the rate of lymph node positivity is low in patients with pure DCIS (0%-7%).14,1722 It is therefore desirable to identify the subgroup of patients in whom the rate of invasive cancer is most likely to be underestimated at CNB, for whom SNB may be indicated at initial surgery.

A number of studies have attempted to define predictors of invasive cancer by looking at mammographic and histologic CNB findings. High cytologic grade,810,13 a mass on the mammogram,1012 and larger lesion size8,9,1214 appear to correlate with accompanying invasive cancer, but there is no consensus.

We investigated preoperative demographic, mammographic, and pathological factors that may predict underestimation of invasive cancer when CNB shows DCIS. We restricted the study to breast cancers and DCIS detected within a population-based mammographic screening program. Screen-detected lesions tend to be smaller and are more likely to be impalpable than symptomatic lesions,23,24 and it is possible that results from a screening program would differ from those of both screen-detected and symptomatic lesions. We then assessed the impact of multiple risk factors to generate a possible management algorithm.

All patients with a CNB diagnosis of DCIS or DCIS with microinvasion (DCISM), from January 1, 1994, through December 31, 2006, were identified from the records of North Western BreastScreen, Melbourne, Australia. This is a population-based mammographic screening program serving the northern and western suburbs of Melbourne. Microinvasion was defined as invasive carcinoma measuring less than 1 mm.

Demographic, radiologic, clinical, and pathological data were collected prospectively on all cases. Most of the information was collected contemporaneously by the screening program, and this data collection was supplemented by information from pathology records. Mammograms were further characterized through a systematic review by 2 consultant breast radiologists (A.R. and A.M.).

Percutaneous biopsies were performed by 1 of 3 specialist breast radiologists (including A.R. and A.M.), and the tissues obtained were assessed at the Pathology Department of The Royal Melbourne Hospital, a tertiary teaching referral hospital. Lesions not seen on ultrasonography were subjected to biopsy by means of a 14-gauge automated needle (ProMag Automatic, MD Technologies, Galena, Illinois) on a prone stereotactic table (Lorad DSM, Hologic, Bedford, Massachusetts). After 2001, an 11-gauge vacuum-assisted biopsy device (Mammotome Biopsy System, Ethicon Endo-Surgery Inc, Cincinnati, Ohio) was used, on the same prone stereotactic table. Biopsy specimens of ultrasound-visible lesions were obtained with a 14-gauge automated needle (ProMag Automatic; Bard Magnum Biopsy, Bard Limited, Crawley, West Sussex, England; or Achieve Automatic Biopsy System, Cardinal Health Dublin, Ohio) with the aid of an ultrasound machine (Antares Sonoline, Siemens, New York, New York; or ATL HDI 3000, Universal Diagnostic Solutions, Oceanside, California). Impalpable lesions were then localized by specialist breast radiologists using a hookwire or a carbon track.25 Surgery was performed at The Royal Melbourne Hospital or 1 of 6 private hospitals in Melbourne.

Statistical analyses were performed with SPSS software (SPSS Inc, Chicago, Illinois). Pearson χ2 and Fisher exact tests were used to determine significant associations between patient characteristics and margin status. Multivariate analysis was performed by logistic regression.

A total of 396 women had a CNB diagnosis of DCIS or DCISM at the North Western BreastScreen from January 1, 1994, through December 31, 2006. Five had missing or incomplete data and 1 declined definitive surgery, leaving 390 cases for analysis. The majority of patients (77.4%) were aged 50 to 69 years, which is the target age group of the mammographic screening program at North Western BreastScreen.

The CNB results showed 375 patients (96.2%) who had pure DCIS and 15 (3.8%) who had DCISM (Table 1). After definitive surgery, the diagnosis of 65 (17.3%) of those with pure DCIS on CNB was upstaged to invasive cancer, 16 (4.3%) showed microinvasion, and the remaining 294 (78.4%) retained the diagnosis of pure DCIS (including 11 cases that showed small DCIS on CNB and yielded no pathological findings after definitive surgery). For those with DCISM on CNB, the diagnosis of 11 (73.3%) was upstaged to invasive cancer, and 4 (26.7%) showed microinvasion. The presence of microinvasion on CNB was strongly associated with upstaging to invasive cancer (P < .001) (Table 2). A palpable lump suggestive of a malignant neoplasm was an uncommon finding, accounting for only 21 of 390 cases. Ten of the 21 palpable lesions (47.6%) were upstaged to invasive cancer (P = .01).

Table Graphic Jump LocationTable 1. CNB and Final Pathology Resultsa
Table Graphic Jump LocationTable 2. Palpability and Final Pathology Resultsa
SURGICAL MANAGEMENT

Of 76 patients whose diagnosis was upstaged to invasive cancer, 71 (93.4%) underwent axillary assessment. Twenty-one (27.6%) had either SNB or axillary dissection together with their initial breast surgery owing to surgeon or patient preference. Fifty (65.8%) received axillary assessment as part of their reoperation after final pathological examination results showed invasive cancer. Five patients had no axillary assessment: 4 had cancers measuring less than 3 mm, and 1 elderly patient with a widely excised 10-mm cancer decided against further surgery.

In patients with a final diagnosis of DCISM, 14 of 20 (70%) had axillary assessment: 6 (30%) during the initial surgical procedure and 8 (40%) during a subsequent procedure, leaving 6 without axillary assessment. Only 19 of 294 patients with pure DCIS (6.5%) received axillary assessment. Seventeen (5.8%) were during the initial surgery: 16 were in association with mastectomy, and 1 underwent axillary dissection after suspicion of invasive cancer owing to the discovery of extensive calcification during the preoperative workup. An additional 2 patients (0.7%) had an SNB in association with completion mastectomy during their subsequent surgical procedure.

Overall, of 390 patients, 109 (27.9%) had axillary assessment, and in 44 of them (40.3%) this was at the initial operation. Thirteen of the 109 patients (11.9%) had at least 1 positive lymph node; among them was 1 patient with 10 positive lymph nodes.

The rate of reoperation was highest in the group whose diagnosis was upstaged to invasive cancer (55 of 76 [72.4%]), followed by the DCISM group (9 of 20 [45.0%]), and lowest in the pure DCIS group (85 of 294 [28.9%]). Axillary assessment was involved in the majority of additional procedures in the first 2 groups, whereas reexcisions for unsatisfactory margins predominated in the last group.

IMPALPABLE DCIS

In the 355 patients with impalpable lesions and no microinvasion on CNB, we examined preoperative factors that may be associated with a change in diagnosis after definitive surgery, to either DCISM or invasive cancer (Table 3).

Table Graphic Jump LocationTable 3. Associations With Final Diagnosis for Impalpable DCIS on CNB
Mammographic Features

The presence or absence of mammographic microcalcifications was not associated with a change in the final diagnosis (P = .47). Of the 91 cases in which the patient had a mass, density, or architectural distortion on mammography, the diagnosis in 28 cases (31%) was upstaged. By contrast, the diagnosis in only 44 of 264 patients (16.7%) without any of these features (ie, microcalcification only) was upstaged (P = .004). Thus, lesions with microcalcification as the sole mammographic abnormality were significantly less likely to have invasive cancer on final pathological examination. As the maximum diameter of the mammographic abnormality increased, the presence of invasion became more likely. Only 20 of 260 lesions (12.5%) smaller than 20 mm were upstaged, compared with 52 of 195 lesions (26.7%) measuring 20 mm or greater (P = .001).

CNB Technique

There was no difference in upstaging rates between different CNB techniques: 37 of 184 (20.1%) for the stereotactic method (14-gauge needle), 27 of 134 (20.1%) for the vacuum-assisted method (11-gauge needle), and 8 of 37 (21.6%) for the ultrasound-assisted method (14-gauge needle) (P = .98).

CNB Histologic Findings

A greater proportion of cancers were upstaged with increasing grade of DCIS (10.6% of low-, 16.2% of intermediate-, and 25.0% of high-grade DCIS), and this trend was significant (P = .04). The presence of comedonecrosis on CNB was more likely to be associated with invasive cancer on final pathological examination, but this was not statistically significant (P = .07).

Screening Interval

The BreastScreen Victoria mammographic screening program sends invitations to women aged 50 to 69 years to attend screening every 2 years. In our series, if 3 years had passed since a woman's last screening mammogram, that woman was considered a “lapsed attendee.” Of 23 lapsed attendees, 10 (43.5%) had microinvasion or invasive cancer on final pathological examination. Among those whose positive screening mammogram was within 3 years of the previous one, 62 of 332 (18.7%) had an invasive component (P = .004).

Multivariate Analysis

On univariate analysis, 4 factors were found to be significantly associated with upstaging to microinvasive or invasive cancer. After adjustment for other factors, the presence of a mass, density, or architectural distortion on mammography; mammographic size 20 mm or greater; and screening interval 3 years or longer remained significant (Table 4). The DCIS grade on CNB was not significant on multivariate analysis.

Table Graphic Jump LocationTable 4. Multivariate Analysis of Factors With Upstaging to DCISM or Invasive Cancer

We then examined the outcome of patients with variable numbers of the significant preoperative factors. The proportion of patients for whom the diagnosis was upstaged rose with each additional risk factor: 9 of 108 (8.3%) of those with no factors, 40 of 192 (20.8%) of those with 1 factor, 19 of 48 (39.6%) of those with 2 factors, and 4 of 7 (57.1%) of those with 3 factors (Table 5).

Table Graphic Jump LocationTable 5. Correlation Between Number of Significant Factors Present and Percentage of Cases Upstaged in Cases of Impalpable DCISa
MANAGEMENT OF HIGH-RISK CASES

Of 355 women with impalpable DCIS on CNB, 55 had 2 or more significant risk factors for upstaging. Twenty-three of the 55 (41.8%) had invasion on final pathological examination, and if they had not been offered SNB as part of the initial surgical procedure, an additional procedure would have been necessary to assess the axilla. However, 15 of them had positive margins and would have needed another operation regardless. Therefore, if those with 2 or more risk factors were offered SNB as part of the initial surgical procedure, we would theoretically have saved 8 reoperations (14.5%). However, the 32 of 55 patients (58.2%) whose findings were not upstaged would have undergone an unnecessary SNB.

Preoperative identification of invasive cancer or DCIS has improved the management of impalpable breast neoplasia. It has increased the proportion of cases in which definitive surgical therapy can be administered during a single operation. Definitive management of the primary tumor occurs with both invasive cancer and DCIS; however, axillary assessment is required only when invasion is present. The dilemma the surgeon faces is that a diagnosis of DCIS on CNB is prone to underestimation, which is demonstrated after definitive surgery. Patients whose cancer is upstaged to invasive cancer will then need an additional procedure to stage the axilla. In our study, 17.3% of patients with a CNB finding of DCIS were found to have invasive cancer. This rate is comparable to those in previous studies, most of which cite rates around 20%.13 Many authors have used this information to recommend SNB in a substantial proportion of cases of DCIS to reduce the need for subsequent axillary staging in cases of underestimation.26 Our study sought to identify subgroups in which underestimation was more common.

The management of DCISM remains controversial. It is uncommon, it is typically seen in approximately 5% of cases of DCIS,27 and reports suggest that the rate of axillary nodal involvement in DCISM is in the range of 4% to 17%.6,10,11,2832 However, most reports have small sample sizes. In our study, none of the 15 patients with a CNB finding of DCISM had a positive axillary node. We found that the cancers of 73.3% of patients with DCISM were upstaged and that microinvasion was the strongest risk factor for upstaging. Recent reports have shown a similar association between DCISM and upstaging.14,33 This rate of upstaging supports the routine use of SNB in DCISM, even if the rate of nodal involvement in DCISM is low.

In our series, palpability was a strong predictor of invasion, with nearly half of the palpable tumors being upstaged. Previous studies have also reported the link between palpability and invasion11,34; therefore, it is reasonable to suggest routine SNB for palpable cancers.

The majority of screen-detected lesions are impalpable, and predicting upstaging in impalpable lesions showing DCIS on CNB is important. Preoperative factors associated with upstaging in multivariate analysis were the presence of a mass, density, or architectural distortion on mammogram; larger mammographic size (≥20 mm); and a screening interval of 3 years or longer. High cytologic grade on CNB was predictive of upstaging in univariate but not multivariate analysis. Several authors have reported grade as a significant risk factor,8,10,13 and it may remain significant in a larger study. The presence of a mass on a mammogram has been consistently reported as a predictor of invasion.1012,35 Previous studies have shown that mammographic size is significantly associated with upstaging,9,13,35 and our study agrees with this finding. The larger volume to sample by biopsy may increase the chance of a sampling error, or the larger volume of disease may be more likely to have focal progression from DCIS to invasive cancer. Results of previous studies were summarized in a recently published meta-analysis,26 and our findings are consistent with the most commonly reported significant predictors of invasive disease.

A potential novel predictor for invasive cancer in screen-detected DCIS relates to the interval between mammograms. Breast screening has been shown to reduce morbidity and mortality due to breast cancer,36 but the optimal screening interval is debated. In Australia, women between 50 and 69 years of age are invited every 2 years for screening. The National Health Service Breast Screening Program in the United Kingdom has a 3-yearly screening program, whereas the average interval between screenings in the United States is 18 months.37 One UK study suggests that shortening the interval to 2 years is beneficial,38 while another disagrees.39 An interesting aspect of our study was that those lapsed attendees with a screening interval of 3 years or longer showed a significant increase in the rate of upstaging. A recent report of a screened population from the United Kingdom by Goyal et al11 also showed a higher rate of upstaging to invasive cancer (38%) than in other studies. Because invasive carcinoma often results from progression of DCIS, an increased screening interval may allow more time for progression. An argument can be made for more vigilance when a lapsed attendee with a preoperative diagnosis of DCIS is examined.

Recent trends in radiology to use vacuum-assisted biopsy with a larger needle may mean that invasive cancer is more often identified and that upstaging will be less of an issue.40 However, these new techniques have shown no significant advantage in recent reports.41,42 Our study found that vacuum-assisted 11-gauge needles have underestimation rates similar to those of 14-gauge needles.

The results of our analysis according to the number of risk factors suggest a possible management algorithm. If these findings are confirmed when applied to independent data sets, then in those with no risk factors, the chance of invasive cancer is less than 10%, and therefore SNB could be avoided. Patients with 2 or 3 of the risk factors have an incidence of underestimation of around 40%, and therefore SNB would be appropriate. Management of cases in which the patient has a single risk factor would require individual judgment, and SNB may be appropriate in selected cases. Previous studies have also highlighted the role of SNB in patients undergoing total mastectomy21,43,44 or a wide excision close to the axilla19,45 because axillary assessment may not be possible after this procedure,14,46,47 although recent evidence suggests that SNB can be successfully and reliably performed after previous breast procedures.16,4850

As expected, the rate of additional procedures was higher in patients found to have invasive cancer than in those who were not. This finding underlines the need to increase the preoperative detection of invasion, so that there is less need for reoperation to assess nodal status. However, it is not appropriate to recommend SNB to all patients with DCIS, especially those at very low risk of having invasive cancer. While SNB is undoubtedly a great advance over routine axillary dissection in clinically node-negative patients, it is not a trivial or harmless procedure. Sentinel node biopsy adds significantly to the cost and inconvenience of surgery, and there is definite morbidity, with a 5% incidence of lymphedema recently reported at 5 years of follow-up.51 Recommending SNB to those with 2 or more risk factors means that, in our series, 15.5% of cases (55 of 355) would have received this recommendation and 23 of them (41.8%) would have had invasive cancer at final pathological examination. Although 32 patients (58.2%) would have undergone an unnecessary axillary procedure, it is reassuring to know that there is no disease in the sentinel node of such high-risk cases of DCIS because there is likely to be an incidence of pathological sampling error in the assessment of extensive DCIS.

In our analysis, although 23 of 55 high-risk patients would have avoided reoperation for axillary assessment if they had been offered SNB as part of the initial surgical procedure, 15 would still have had to return because of positive margins, reducing the number in whom a second procedure would have been avoided to 8. Positive margins after the first procedure are a common indication for reoperation,52 especially in patients with pure DCIS. Therefore, attempts to reduce the number of additional procedures performed must take into consideration both the predictors of upstaging and predictors of unsatisfactory margins.

In summary, the finding of invasive cancer in the surgical specimen after a preoperative CNB shows DCIS is common. Microinvasion on CNB and palpability strongly predict upstaging. In patients with impalpable screen-detected cancers with DCIS on CNB, factors significantly associated with upstaging are the presence of a mass, density, or architectural distortion on mammogram; larger mammographic size (≥20 mm); and screening interval of 3 years or longer. This information may allow a more informed discussion of the role of SNB at the initial surgical procedure. We propose an algorithm whereby patients with 2 or more risk factors would be considered high risk and whereby routine SNB would be offered to this group as well.

Correspondence: G. Bruce Mann, MBBS, PhD, FRACS, Breast Unit, Ste 12, Royal Women's Hospital, Parkville 3052, Victoria, Australia (bruce.mann@mh.org.au).

Accepted for Publication: September 14, 2009.

Author Contributions:Study concept and design: Kurniawan, Rose, Mou, Collins, and Mann. Acquisition of data: Kurniawan, Rose, Mou, Buchanan, and Wong. Analysis and interpretation of data: Kurniawan, Rose, Mou, Collins, Wong, Miller, and Mann. Drafting of the manuscript: Kurniawan and Mann. Critical revision of the manuscript for important intellectual content: Kurniawan, Rose, Mou, Buchanan, Collins, Wong, Miller, and Mann. Statistical analysis: Kurniawan. Administrative, technical, and material support: Collins, Wong, and Mann. Study supervision: Rose, Mou, Buchanan, Collins, Miller, and Mann.

Financial Disclosure: None reported.

Previous Presentation: This study was presented in part as a poster at the San Antonio Breast Cancer Symposium; December 11, 2009; San Antonio, Texas.

Parker  SHBurbank  FJackman  RJ  et al.  Percutaneous large-core breast biopsy: a multi-institutional study. Radiology 1994;193 (2) 359- 364
PubMed
Smith  DNChristian  RMeyer  JE Large-core needle biopsy of nonpalpable breast cancers: the impact on subsequent surgical excisions. Arch Surg 1997;132 (3) 256- 259
PubMed Link to Article
Sakorafas  GHFarley  DR Optimal management of ductal carcinoma in situ of the breast. Surg Oncol 2003;12 (4) 221- 240
PubMed Link to Article
Silverstein  MJRosser  RJGierson  ED  et al.  Axillary lymph node dissection for intraductal breast carcinoma—is it indicated? Cancer 1987;59 (10) 1819- 1824
PubMed Link to Article
King  TAFarr  GH  JrCederbom  GJ  et al.  A mass on breast imaging predicts coexisting invasive carcinoma in patients with a core biopsy diagnosis of ductal carcinoma in situ. Am Surg 2001;67 (9) 907- 912
PubMed
S akr  RBarranger  EAntoine  MPrugnolle  HDaraï  EUzan  S Ductal carcinoma in situ: value of sentinel lymph node biopsy. J Surg Oncol 2006;94 (5) 426- 430
PubMed Link to Article
Wahedna  YEvans  AJPinder  SEEllis  IOBlamey  RWGeraghty  JG Mammographic size of ductal carcinoma in situ does not predict the presence of an invasive focus. Eur J Cancer 2001;37 (4) 459- 462
PubMed Link to Article
Hoorntje  LESchipper  MEIPeeters  PHABellot  FStorm  RKBorel Rinkes  IH The finding of invasive cancer after a preoperative diagnosis of ductal carcinoma-in-situ: causes of ductal carcinoma-in-situ underestimates with stereotactic 14-gauge needle biopsy. Ann Surg Oncol 2003;10 (7) 748- 753
PubMed Link to Article
Yen  TWFHunt  KKRoss  MI  et al.  Predictors of invasive breast cancer in patients with an initial diagnosis of ductal carcinoma in situ: a guide to selective use of sentinel lymph node biopsy in management of ductal carcinoma in situ. J Am Coll Surg 2005;200 (4) 516- 526
PubMed Link to Article
Wilkie  CWhite  LDupont  ECantor  ACox  CE An update of sentinel lymph node mapping in patients with ductal carcinoma in situ. Am J Surg 2005;190 (4) 563- 566
PubMed Link to Article
Goyal  ADouglas-Jones  AMonypenny  ISweetland  HStevens  GMansel  RE Is there a role of sentinel lymph node biopsy in ductal carcinoma in situ? analysis of 587 cases. Breast Cancer Res Treat 2006;98 (3) 311- 314
PubMed Link to Article
Dillon  MFMcDermott  EWQuinn  CMO’Doherty  AO’Higgins  NHill  ADK Predictors of invasive disease in breast cancer when core biopsy demonstrates DCIS only. J Surg Oncol 2006;93 (7) 559- 563
PubMed Link to Article
Moran  CJKell  MRFlanagan  FLKennedy  MGorey  TFKerin  MJ Role of sentinel lymph node biopsy in high-risk ductal carcinoma in situ patients. Am J Surg 2007;194 (2) 172- 175
PubMed Link to Article
Sakr  RBezu  CRaoust  I  et al.  The sentinel lymph node procedure for patients with preoperative diagnosis of ductal carcinoma in situ: risk factors for unsuspected invasive disease and for metastatic sentinel lymph nodes. Int J Clin Pract 2008;62 (11) 1730- 1735
PubMed Link to Article
Krag  DWeaver  DAshikaga  T  et al.  The sentinel node in breast cancer—a multicenter validation study. N Engl J Med 1998;339 (14) 941- 946
PubMed Link to Article
Wong  SLEdwards  MJChao  C  et al. University of Louisville Breast Cancer Study Group, The effect of prior breast biopsy method and concurrent definitive breast procedure on success and accuracy of sentinel lymph node biopsy. Ann Surg Oncol 2002;9 (3) 272- 277
PubMed Link to Article
Katz  AGage  IEvans  S  et al.  Sentinel lymph node positivity of patients with ductal carcinoma in situ or microinvasive breast cancer. Am J Surg 2006;191 (6) 761- 766
PubMed Link to Article
Leidenius  MSalmenkivi  Kvon Smitten  KHeikkilä  P Tumour-positive sentinel node findings in patients with ductal carcinoma in situ. J Surg Oncol 2006;94 (5) 380- 384
PubMed Link to Article
Mabry  HGiuliano  AESilverstein  MJ What is the value of axillary dissection or sentinel node biopsy in patients with ductal carcinoma in situ? Am J Surg 2006;192 (4) 455- 457
PubMed Link to Article
Veronesi  PIntra  MVento  AR  et al.  Sentinel lymph node biopsy for localised ductal carcinoma in situ? Breast 2005;14 (6) 520- 522
PubMed Link to Article
Intra  MVeronesi  PMazzarol  G  et al.  Axillary sentinel lymph node biopsy in patients with pure ductal carcinoma in situ of the breast. Arch Surg 2003;138 (3) 309- 313
PubMed Link to Article
Farkas  EAStolier  AJTeng  SCBolton  JSFuhrman  GM An argument against routine sentinel node mapping for DCIS. Am Surg 2004;70 (1) 13- 17
PubMed
Cady  BStone  MDSchuler  JGThakur  RWanner  MALavin  PT The new era in breast cancer: invasion, size, and nodal involvement dramatically decreasing as a result of mammographic screening. Arch Surg 1996;131 (3) 301- 308
PubMed Link to Article
Tabár  LDuffy  SWVitak  BChen  HHPrevost  TC The natural history of breast carcinoma: what have we learned from screening? Cancer 1999;86 (3) 449- 462
PubMed Link to Article
Rose  ACollins  JPNeerhut  PBishop  CVMann  GB Carbon localisation of impalpable breast lesions. Breast 2003;12 (4) 264- 269
PubMed Link to Article
Ansari  BOgston  SAPurdie  CAAdamson  DJBrown  DCThompson  AM Meta-analysis of sentinel node biopsy in ductal carcinoma in situ of the breast. Br J Surg 2008;95 (5) 547- 554
PubMed Link to Article
Adamovich  TLSimmons  RM Ductal carcinoma in situ with microinvasion. Am J Surg 2003;186 (2) 112- 116
PubMed Link to Article
Zavagno  GBelardinelli  VMarconato  R  et al.  Sentinel lymph node metastasis from mammary ductal carcinoma in situ with microinvasion. Breast 2007;16 (2) 146- 151
PubMed Link to Article
Intra  MZurrida  SMaffini  F  et al.  Sentinel lymph node metastasis in microinvasive breast cancer. Ann Surg Oncol 2003;10 (10) 1160- 1165
PubMed Link to Article
Klauber-DeMore  NTan  LKLiberman  L  et al.  Sentinel lymph node biopsy: is it indicated in patients with high-risk ductal carcinoma-in-situ and ductal carcinoma-in-situ with microinvasion? Ann Surg Oncol 2000;7 (9) 636- 642
PubMed Link to Article
Guth  AAMercado  CRoses  DFDarvishian  FSingh  BCangiarella  JF Microinvasive breast cancer and the role of sentinel node biopsy: an institutional experience and review of the literature. Breast J 2008;14 (4) 335- 339
PubMed Link to Article
Wasserberg  NMorgenstern  SSchachter  JFenig  ELelcuk  SGutman  H Risk factors for lymph node metastases in breast ductal carcinoma in situ with minimal invasive component. Arch Surg 2002;137 (11) 1249- 1252
PubMed Link to Article
Le Bouëdec  Gde Lapasse  CMishellany  F  et al.  Ductal carcinoma in situ of the breast with microinvasion: role of sentinel lymph node biopsy [in French]. Gynecol Obstet Fertil 2007;35 (4) 317- 322
PubMed Link to Article
Meijnen  POldenburg  HSALoo  CENieweg  OEPeterse  JLRutgers  EJT Risk of invasion and axillary lymph node metastasis in ductal carcinoma in situ diagnosed by core-needle biopsy. Br J Surg 2007;94 (8) 952- 956
PubMed Link to Article
Jackman  RJBurbank  FParker  SH  et al.  Stereotactic breast biopsy of nonpalpable lesions: determinants of ductal carcinoma in situ underestimation rates. Radiology 2001;218 (2) 497- 502
PubMed Link to Article
Tabár  LVitak  BChen  HH  et al.  The Swedish Two-County Trial twenty years later: updated mortality results and new insights from long-term follow-up. Radiol Clin North Am 2000;38 (4) 625- 651
PubMed Link to Article
Smith-Bindman  RBallard-Barbash  RMiglioretti  DLPatnick  JKerlikowske  K Comparing the performance of mammography screening in the USA and the UK. J Med Screen 2005;12 (1) 50- 54
PubMed Link to Article
Boer  Rde Koning  HThrelfall  A  et al.  Cost effectiveness of shortening screening interval or extending age range of NHS breast screening programme: computer simulation study. BMJ 1998;317 (7155) 376- 379
PubMed Link to Article
Blamey  RWDay  NEYoung  JR  et al. Breast Screening Frequency Trial Group; United Kingdom Co-ordinating Committee on Cancer Research, The frequency of breast cancer screening: results from the UKCCCR Randomised Trial. Eur J Cancer 2002;38 (11) 1458- 1464
PubMed Link to Article
Sohn  VArthurs  ZHerbert  G  et al.  Atypical ductal hyperplasia: improved accuracy with the 11-gauge vacuum-assisted versus the 14-gauge core biopsy needle. Ann Surg Oncol 2007;14 (9) 2497- 2501
PubMed Link to Article
Lourenco  APMainiero  MBLazarus  EGiri  DSchepps  B Stereotactic breast biopsy: comparison of histologic underestimation rates with 11- and 9-gauge vacuum-assisted breast biopsy. AJR Am J Roentgenol 2007;189 (5) W275- W279
PubMed Link to Article
Philpotts  LEHooley  RJLee  CH Comparison of automated versus vacuum-assisted biopsy methods for sonographically guided core biopsy of the breast. AJR Am J Roentgenol 2003;180 (2) 347- 351
PubMed Link to Article
Dominguez  FJGolshan  MBlack  DM  et al.  Sentinel node biopsy is important in mastectomy for ductal carcinoma in situ. Ann Surg Oncol 2008;15 (1) 268- 273
PubMed Link to Article
Tan  JCCMcCready  DREasson  AMLeong  WL Role of sentinel lymph node biopsy in ductal carcinoma-in-situ treated by mastectomy. Ann Surg Oncol 2007;14 (2) 638- 645
PubMed Link to Article
Zavagno  GCarcoforo  PMarconato  R  et al.  Role of axillary sentinel lymph node biopsy in patients with pure ductal carcinoma in situ of the breast. BMC Cancer 2005;528
PubMed Link to Article
Mittendorf  EAArciero  CAGutchell  VHooke  JShriver  CD Core biopsy diagnosis of ductal carcinoma in situ: an indication for sentinel lymph node biopsy. Curr Surg 2005;62 (2) 253- 257
PubMed Link to Article
Julian  TBLand  SRFourchotte  V  et al.  Is sentinel node biopsy necessary in conservatively treated DCIS? Ann Surg Oncol 2007;14 (8) 2202- 2208
PubMed Link to Article
Heuts  EMvan der Ent  FWCKengen  RAMvan der Pol  HAGHulsewé  KWEHoofwijk  AGM Results of sentinel node biopsy not affected by previous excisional biopsy. Eur J Surg Oncol 2006;32 (3) 278- 281
PubMed Link to Article
Kaminski  AAmr  DKimbrell  MLDifronzo  LA Lymphatic mapping in patients with breast cancer and previous augmentation mammoplasty. Am Surg 2007;73 (10) 981- 983
PubMed
Rodriguez Fernandez  JMartella  STrifirò  G  et al.  Sentinel node biopsy in patients with previous breast aesthetic surgery. Ann Surg Oncol 2009;16 (4) 989- 992
PubMed Link to Article
McLaughlin  SAWright  MJMorris  KT  et al.  Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: objective measurements. J Clin Oncol 2008;26 (32) 5213- 5219
PubMed Link to Article
Kurniawan  EDWong  MHWindle  I  et al.  Predictors of surgical margin status in breast-conserving surgery within a breast screening program. Ann Surg Oncol 2008;15 (9) 2542- 2549
PubMed Link to Article

Figures

Tables

Table Graphic Jump LocationTable 1. CNB and Final Pathology Resultsa
Table Graphic Jump LocationTable 2. Palpability and Final Pathology Resultsa
Table Graphic Jump LocationTable 3. Associations With Final Diagnosis for Impalpable DCIS on CNB
Table Graphic Jump LocationTable 4. Multivariate Analysis of Factors With Upstaging to DCISM or Invasive Cancer
Table Graphic Jump LocationTable 5. Correlation Between Number of Significant Factors Present and Percentage of Cases Upstaged in Cases of Impalpable DCISa

References

Parker  SHBurbank  FJackman  RJ  et al.  Percutaneous large-core breast biopsy: a multi-institutional study. Radiology 1994;193 (2) 359- 364
PubMed
Smith  DNChristian  RMeyer  JE Large-core needle biopsy of nonpalpable breast cancers: the impact on subsequent surgical excisions. Arch Surg 1997;132 (3) 256- 259
PubMed Link to Article
Sakorafas  GHFarley  DR Optimal management of ductal carcinoma in situ of the breast. Surg Oncol 2003;12 (4) 221- 240
PubMed Link to Article
Silverstein  MJRosser  RJGierson  ED  et al.  Axillary lymph node dissection for intraductal breast carcinoma—is it indicated? Cancer 1987;59 (10) 1819- 1824
PubMed Link to Article
King  TAFarr  GH  JrCederbom  GJ  et al.  A mass on breast imaging predicts coexisting invasive carcinoma in patients with a core biopsy diagnosis of ductal carcinoma in situ. Am Surg 2001;67 (9) 907- 912
PubMed
S akr  RBarranger  EAntoine  MPrugnolle  HDaraï  EUzan  S Ductal carcinoma in situ: value of sentinel lymph node biopsy. J Surg Oncol 2006;94 (5) 426- 430
PubMed Link to Article
Wahedna  YEvans  AJPinder  SEEllis  IOBlamey  RWGeraghty  JG Mammographic size of ductal carcinoma in situ does not predict the presence of an invasive focus. Eur J Cancer 2001;37 (4) 459- 462
PubMed Link to Article
Hoorntje  LESchipper  MEIPeeters  PHABellot  FStorm  RKBorel Rinkes  IH The finding of invasive cancer after a preoperative diagnosis of ductal carcinoma-in-situ: causes of ductal carcinoma-in-situ underestimates with stereotactic 14-gauge needle biopsy. Ann Surg Oncol 2003;10 (7) 748- 753
PubMed Link to Article
Yen  TWFHunt  KKRoss  MI  et al.  Predictors of invasive breast cancer in patients with an initial diagnosis of ductal carcinoma in situ: a guide to selective use of sentinel lymph node biopsy in management of ductal carcinoma in situ. J Am Coll Surg 2005;200 (4) 516- 526
PubMed Link to Article
Wilkie  CWhite  LDupont  ECantor  ACox  CE An update of sentinel lymph node mapping in patients with ductal carcinoma in situ. Am J Surg 2005;190 (4) 563- 566
PubMed Link to Article
Goyal  ADouglas-Jones  AMonypenny  ISweetland  HStevens  GMansel  RE Is there a role of sentinel lymph node biopsy in ductal carcinoma in situ? analysis of 587 cases. Breast Cancer Res Treat 2006;98 (3) 311- 314
PubMed Link to Article
Dillon  MFMcDermott  EWQuinn  CMO’Doherty  AO’Higgins  NHill  ADK Predictors of invasive disease in breast cancer when core biopsy demonstrates DCIS only. J Surg Oncol 2006;93 (7) 559- 563
PubMed Link to Article
Moran  CJKell  MRFlanagan  FLKennedy  MGorey  TFKerin  MJ Role of sentinel lymph node biopsy in high-risk ductal carcinoma in situ patients. Am J Surg 2007;194 (2) 172- 175
PubMed Link to Article
Sakr  RBezu  CRaoust  I  et al.  The sentinel lymph node procedure for patients with preoperative diagnosis of ductal carcinoma in situ: risk factors for unsuspected invasive disease and for metastatic sentinel lymph nodes. Int J Clin Pract 2008;62 (11) 1730- 1735
PubMed Link to Article
Krag  DWeaver  DAshikaga  T  et al.  The sentinel node in breast cancer—a multicenter validation study. N Engl J Med 1998;339 (14) 941- 946
PubMed Link to Article
Wong  SLEdwards  MJChao  C  et al. University of Louisville Breast Cancer Study Group, The effect of prior breast biopsy method and concurrent definitive breast procedure on success and accuracy of sentinel lymph node biopsy. Ann Surg Oncol 2002;9 (3) 272- 277
PubMed Link to Article
Katz  AGage  IEvans  S  et al.  Sentinel lymph node positivity of patients with ductal carcinoma in situ or microinvasive breast cancer. Am J Surg 2006;191 (6) 761- 766
PubMed Link to Article
Leidenius  MSalmenkivi  Kvon Smitten  KHeikkilä  P Tumour-positive sentinel node findings in patients with ductal carcinoma in situ. J Surg Oncol 2006;94 (5) 380- 384
PubMed Link to Article
Mabry  HGiuliano  AESilverstein  MJ What is the value of axillary dissection or sentinel node biopsy in patients with ductal carcinoma in situ? Am J Surg 2006;192 (4) 455- 457
PubMed Link to Article
Veronesi  PIntra  MVento  AR  et al.  Sentinel lymph node biopsy for localised ductal carcinoma in situ? Breast 2005;14 (6) 520- 522
PubMed Link to Article
Intra  MVeronesi  PMazzarol  G  et al.  Axillary sentinel lymph node biopsy in patients with pure ductal carcinoma in situ of the breast. Arch Surg 2003;138 (3) 309- 313
PubMed Link to Article
Farkas  EAStolier  AJTeng  SCBolton  JSFuhrman  GM An argument against routine sentinel node mapping for DCIS. Am Surg 2004;70 (1) 13- 17
PubMed
Cady  BStone  MDSchuler  JGThakur  RWanner  MALavin  PT The new era in breast cancer: invasion, size, and nodal involvement dramatically decreasing as a result of mammographic screening. Arch Surg 1996;131 (3) 301- 308
PubMed Link to Article
Tabár  LDuffy  SWVitak  BChen  HHPrevost  TC The natural history of breast carcinoma: what have we learned from screening? Cancer 1999;86 (3) 449- 462
PubMed Link to Article
Rose  ACollins  JPNeerhut  PBishop  CVMann  GB Carbon localisation of impalpable breast lesions. Breast 2003;12 (4) 264- 269
PubMed Link to Article
Ansari  BOgston  SAPurdie  CAAdamson  DJBrown  DCThompson  AM Meta-analysis of sentinel node biopsy in ductal carcinoma in situ of the breast. Br J Surg 2008;95 (5) 547- 554
PubMed Link to Article
Adamovich  TLSimmons  RM Ductal carcinoma in situ with microinvasion. Am J Surg 2003;186 (2) 112- 116
PubMed Link to Article
Zavagno  GBelardinelli  VMarconato  R  et al.  Sentinel lymph node metastasis from mammary ductal carcinoma in situ with microinvasion. Breast 2007;16 (2) 146- 151
PubMed Link to Article
Intra  MZurrida  SMaffini  F  et al.  Sentinel lymph node metastasis in microinvasive breast cancer. Ann Surg Oncol 2003;10 (10) 1160- 1165
PubMed Link to Article
Klauber-DeMore  NTan  LKLiberman  L  et al.  Sentinel lymph node biopsy: is it indicated in patients with high-risk ductal carcinoma-in-situ and ductal carcinoma-in-situ with microinvasion? Ann Surg Oncol 2000;7 (9) 636- 642
PubMed Link to Article
Guth  AAMercado  CRoses  DFDarvishian  FSingh  BCangiarella  JF Microinvasive breast cancer and the role of sentinel node biopsy: an institutional experience and review of the literature. Breast J 2008;14 (4) 335- 339
PubMed Link to Article
Wasserberg  NMorgenstern  SSchachter  JFenig  ELelcuk  SGutman  H Risk factors for lymph node metastases in breast ductal carcinoma in situ with minimal invasive component. Arch Surg 2002;137 (11) 1249- 1252
PubMed Link to Article
Le Bouëdec  Gde Lapasse  CMishellany  F  et al.  Ductal carcinoma in situ of the breast with microinvasion: role of sentinel lymph node biopsy [in French]. Gynecol Obstet Fertil 2007;35 (4) 317- 322
PubMed Link to Article
Meijnen  POldenburg  HSALoo  CENieweg  OEPeterse  JLRutgers  EJT Risk of invasion and axillary lymph node metastasis in ductal carcinoma in situ diagnosed by core-needle biopsy. Br J Surg 2007;94 (8) 952- 956
PubMed Link to Article
Jackman  RJBurbank  FParker  SH  et al.  Stereotactic breast biopsy of nonpalpable lesions: determinants of ductal carcinoma in situ underestimation rates. Radiology 2001;218 (2) 497- 502
PubMed Link to Article
Tabár  LVitak  BChen  HH  et al.  The Swedish Two-County Trial twenty years later: updated mortality results and new insights from long-term follow-up. Radiol Clin North Am 2000;38 (4) 625- 651
PubMed Link to Article
Smith-Bindman  RBallard-Barbash  RMiglioretti  DLPatnick  JKerlikowske  K Comparing the performance of mammography screening in the USA and the UK. J Med Screen 2005;12 (1) 50- 54
PubMed Link to Article
Boer  Rde Koning  HThrelfall  A  et al.  Cost effectiveness of shortening screening interval or extending age range of NHS breast screening programme: computer simulation study. BMJ 1998;317 (7155) 376- 379
PubMed Link to Article
Blamey  RWDay  NEYoung  JR  et al. Breast Screening Frequency Trial Group; United Kingdom Co-ordinating Committee on Cancer Research, The frequency of breast cancer screening: results from the UKCCCR Randomised Trial. Eur J Cancer 2002;38 (11) 1458- 1464
PubMed Link to Article
Sohn  VArthurs  ZHerbert  G  et al.  Atypical ductal hyperplasia: improved accuracy with the 11-gauge vacuum-assisted versus the 14-gauge core biopsy needle. Ann Surg Oncol 2007;14 (9) 2497- 2501
PubMed Link to Article
Lourenco  APMainiero  MBLazarus  EGiri  DSchepps  B Stereotactic breast biopsy: comparison of histologic underestimation rates with 11- and 9-gauge vacuum-assisted breast biopsy. AJR Am J Roentgenol 2007;189 (5) W275- W279
PubMed Link to Article
Philpotts  LEHooley  RJLee  CH Comparison of automated versus vacuum-assisted biopsy methods for sonographically guided core biopsy of the breast. AJR Am J Roentgenol 2003;180 (2) 347- 351
PubMed Link to Article
Dominguez  FJGolshan  MBlack  DM  et al.  Sentinel node biopsy is important in mastectomy for ductal carcinoma in situ. Ann Surg Oncol 2008;15 (1) 268- 273
PubMed Link to Article
Tan  JCCMcCready  DREasson  AMLeong  WL Role of sentinel lymph node biopsy in ductal carcinoma-in-situ treated by mastectomy. Ann Surg Oncol 2007;14 (2) 638- 645
PubMed Link to Article
Zavagno  GCarcoforo  PMarconato  R  et al.  Role of axillary sentinel lymph node biopsy in patients with pure ductal carcinoma in situ of the breast. BMC Cancer 2005;528
PubMed Link to Article
Mittendorf  EAArciero  CAGutchell  VHooke  JShriver  CD Core biopsy diagnosis of ductal carcinoma in situ: an indication for sentinel lymph node biopsy. Curr Surg 2005;62 (2) 253- 257
PubMed Link to Article
Julian  TBLand  SRFourchotte  V  et al.  Is sentinel node biopsy necessary in conservatively treated DCIS? Ann Surg Oncol 2007;14 (8) 2202- 2208
PubMed Link to Article
Heuts  EMvan der Ent  FWCKengen  RAMvan der Pol  HAGHulsewé  KWEHoofwijk  AGM Results of sentinel node biopsy not affected by previous excisional biopsy. Eur J Surg Oncol 2006;32 (3) 278- 281
PubMed Link to Article
Kaminski  AAmr  DKimbrell  MLDifronzo  LA Lymphatic mapping in patients with breast cancer and previous augmentation mammoplasty. Am Surg 2007;73 (10) 981- 983
PubMed
Rodriguez Fernandez  JMartella  STrifirò  G  et al.  Sentinel node biopsy in patients with previous breast aesthetic surgery. Ann Surg Oncol 2009;16 (4) 989- 992
PubMed Link to Article
McLaughlin  SAWright  MJMorris  KT  et al.  Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: objective measurements. J Clin Oncol 2008;26 (32) 5213- 5219
PubMed Link to Article
Kurniawan  EDWong  MHWindle  I  et al.  Predictors of surgical margin status in breast-conserving surgery within a breast screening program. Ann Surg Oncol 2008;15 (9) 2542- 2549
PubMed Link to Article

Correspondence

CME
Also Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
Please click the checkbox indicating that you have read the full article in order to submit your answers.
Your answers have been saved for later.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
Submit a Comment

Multimedia

Some tools below are only available to our subscribers or users with an online account.

Web of Science® Times Cited: 16

Related Content

Customize your page view by dragging & repositioning the boxes below.

Articles Related By Topic
Related Collections