Ductal Carcinoma in Situ at Core-Needle Biopsy: Meta-Analysis of Underestimation and Predictors of Invasive Breast Cancer

Published Online:https://doi.org/10.1148/radiol.11102368

This meta-analysis comprehensively addresses the issue of underestimation of invasive breast cancer and its predictors in the setting of diagnoses of ductal carcinoma in situ at core-needle biopsy, providing a pooled random effects estimate of underestimation (25.9%; 95% confidence interval: 22.5%, 29.5%).

Purpose

To perform a meta-analysis to report pooled estimates for underestimation of invasive breast cancer (where core-needle biopsy [CNB] shows ductal carcinoma in situ [DCIS] and excision histologic examination shows invasive breast cancer) and to identify preoperative variables that predict invasive breast cancer.

Materials and Methods

Studies were identified by searching MEDLINE and were included if they provided data on DCIS underestimates (overall and according to preoperative variables). Study-specific and pooled percentages for DCIS underestimates were calculated. By using meta-regression (random effects logistic modeling) the association between each study-level preoperative variable and understaged invasive breast cancer was investigated.

Results

Fifty-two studies that included 7350 cases of DCIS with findings at excision histologic examination as the reference standard met the eligibility criteria and were included. There were 1736 underestimates (invasive breast cancer at excision); the random-effects pooled estimate was 25.9% (95% confidence interval: 22.5%, 29.5%). Preoperative variables that showed significant univariate association with higher underestimation included the use of a 14-gauge automated device (vs 11-gauge vacuum-assisted biopsy, P = .006), high-grade lesion at CNB (vs non–high grade lesion, P < .001), lesion size larger than 20 mm at imaging (vs lesions ≤ 20 mm, P < .001), Breast Imaging Reporting and Data System (BI-RADS) score of 4 or 5 (vs BI-RADS score of 3, P for trend = .005), mammographic mass (vs calcification only, P < .001), and palpability (P < .001).

Conclusion

About one in four DCIS diagnoses at CNB represent understaged invasive breast cancer. Preoperative variables significantly associated with understaging include biopsy device and guidance method, size, grade, mammographic features, and palpability.

© RSNA, 2011

Supplemental material: http://radiology.rsna.org/lookup/suppl/doi:10.1148/radiol.11102368/-/DC1

References

  • 1 Houssami N, Ciatto S, Ellis I, Ambrogetti D. Underestimation of malignancy of breast core-needle biopsy: concepts and precise overall and category-specific estimates. Cancer 2007;109(3):487–495.
  • 2 Jackman RJ, Burbank F, Parker SH, et al.. Stereotactic breast biopsy of nonpalpable lesions: determinants of ductal carcinoma in situ underestimation rates. Radiology 2001;218(2):497–502.
  • 3 O’Flynn EA, Morel JC, Gonzalez J, et al.. Prediction of the presence of invasive disease from the measurement of extent of malignant microcalcification on mammography and ductal carcinoma in situ grade at core biopsy. Clin Radiol 2009;64(2):178–183.
  • 4 Sauer G, Deissler H, Strunz K, et al.. Ultrasound-guided large-core needle biopsies of breast lesions: analysis of 962 cases to determine the number of samples for reliable tumour classification. Br J Cancer 2005;92(2):231–235.
  • 5 Senn Bahls E, Dupont Lampert V, Oelschlegel C, Senn HJ. Multitarget stereotactic core-needle breast biopsy (MSBB): an effective and safe diagnostic intervention for non-palpable breast lesions—a large prospective single institution study. Breast 2006;15(3):339–346.
  • 6 Bagnall MJ, Evans AJ, Wilson AR, et al.. Predicting invasion in mammographically detected microcalcification. Clin Radiol 2001;56(10):828–832.
  • 7 Leikola J, Heikkilä P, Pamilo M, Salmenkivi K, Von Smitten K, Leidenius M. Predicting invasion in patients with DCIS in the preoperative percutaneous biopsy. Acta Oncol 2007;46(6):798–802.
  • 8 Lee CH, Carter D, Philpotts LE, et al.. Ductal carcinoma in situ diagnosed with stereotactic core needle biopsy: can invasion be predicted? Radiology 2000;217(2):466–470.
  • 9 National Health and Medical Research Council. How to review the evidence: systematic identification and review of the scientific literature. Canberra, Australia: National Health and Medical Research Council, 2000; 62–63.
  • 10 Acheson MB, Patton RG, Howisey RL, Lane RF, Morgan A. Histologic correlation of image-guided core biopsy with excisional biopsy of nonpalpable breast lesions. Arch Surg 1997;132(8):815–818.
  • 11 Bauer RL, Sung J, Eckhert KHJ, Koul A, Castillo NB, Nemoto T. Comparison of histologic diagnosis between stereotactic core needle biopsy and open surgical biopsy. Ann Surg Oncol 1997;4(4):316–320.
  • 12 Bonnett M, Wallis T, Rossmann M, et al.. Histologic and radiographic analysis of ductal carcinoma in situ diagnosed using stereotactic incisional core breast biopsy. Mod Pathol 2002;15(2):95–101.
  • 13 Burak WEJ, Owens KE, Tighe MB, et al.. Vacuum-assisted stereotactic breast biopsy: histologic underestimation of malignant lesions. Arch Surg 2000;135(6):700–703.
  • 14 Cangiarella J, Waisman J, Symmans WF, et al.. Mammotome core biopsy for mammary microcalcification: analysis of 160 biopsies from 142 women with surgical and radiologic followup. Cancer 2001;91(1):173–177.
  • 15 Chan MY, Lim S. Predictors of invasive breast cancer in ductal carcinoma in situ initially diagnosed by core biopsy. Asian J Surg 2010;33(2):76–82.
  • 16 Cho N, Moon WK, Cha JH, et al.. Sonographically guided core biopsy of the breast: comparison of 14-gauge automated gun and 11-gauge directional vacuum-assisted biopsy methods. Korean J Radiol 2005;6(2):102–109.
  • 17 Cipolla C, Fricano S, Vieni S, et al.. Validity of needle core biopsy in the histological characterisation of mammary lesions. Breast 2006;15(1):76–80.
  • 18 Cox D, Bradley S, England D. The significance of mammotome core biopsy specimens without radiographically identifiable microcalcification and their influence on surgical management: a retrospective review with histological correlation. Breast 2006;15(2):210–218.
  • 19 Crowe JPJ, Patrick RJ, Rybicki LA, et al.. Does ultrasound core breast biopsy predict histologic finding on excisional biopsy? Am J Surg 2003;186(4):397–399.
  • 20 Dillon MF, McDermott EW, Quinn CM, O’Doherty A, O’Higgins N, Hill AD. Predictors of invasive disease in breast cancer when core biopsy demonstrates DCIS only. J Surg Oncol 2006;93(7):559–563.
  • 21 El-Tamer M, Axiotis C, Kim E, et al.. Accurate prediction of the amount of in situ tumor in palpable breast cancers by core needle biopsy: implications for neoadjuvant therapy. Ann Surg Oncol 1999;6(5):461–466.
  • 22 Frayne J, Sterrett GF, Harvey J, et al.. Stereotactic 14 gauge core-biopsy of the breast: results from 101 patients. Aust N Z J Surg 1996;66(9):585–591.
  • 23 Go EM, Chan SK, Vong JS, et al.. Predictors of invasion in needle core biopsies of the breast with ductal carcinoma in situ. Mod Pathol 2010;23(5):737–742.
  • 24 Goyal A, Douglas-Jones A, Monypenny I, Sweetland H, Stevens G, Mansel 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.
  • 25 Hoorntje LE, Schipper ME, Peeters PH, Bellot F, Storm RK, Borel 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.
  • 26 Houssami N, Ambrogetti D, Marinovich ML, et al.. Accuracy of a preoperative model for predicting invasive breast cancer in women with ductal carcinoma-in-situ on vacuum-assisted core needle biopsy. Ann Surg Oncol 2010 Nov 24. [Epub ahead of print].
  • 27 Huo L, Sneige N, Hunt KK, Albarracin CT, Lopez A, Resetkova E. Predictors of invasion in patients with core-needle biopsy-diagnosed ductal carcinoma in situ and recommendations for a selective approach to sentinel lymph node biopsy in ductal carcinoma in situ. Cancer 2006;107(8):1760–1768.
  • 28 Killebrew LK, Oneson RH. Comparison of the diagnostic accuracy of a vacuum-assisted percutaneous intact specimen sampling device to a vacuum-assisted core needle sampling device for breast biopsy: initial experience. Breast J 2006;12(4):302–308.
  • 29 King TA, Farr GHJ, Cederbom 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.
  • 30 Kurniawan ED, Rose A, Mou A, et al.. Risk factors for invasive breast cancer when core needle biopsy shows ductal carcinoma in situ. Arch Surg 2010;145(11):1098–1104.
  • 31 Lee JW, Han W, Ko E, et al.. Sonographic lesion size of ductal carcinoma in situ as a preoperative predictor for the presence of an invasive focus. J Surg Oncol 2008;98(1):15–20.
  • 32 Liberman L, LaTrenta LR, Van Zee KJ, Morris EA, Abramson AF, Dershaw DD. Stereotactic core biopsy of calcifications highly suggestive of malignancy. Radiology 1997;203(3):673–677.
  • 33 Londero V, Zuiani C, Furlan A, Nori J, Bazzocchi M. Role of ultrasound and sonographically guided core biopsy in the diagnostic evaluation of ductal carcinoma in situ (DCIS) of the breast. Radiol Med (Torino) 2007;112(6):863–876.
  • 34 Meijnen P, Oldenburg HS, Loo CE, Nieweg OE, Peterse JL, Rutgers EJ. 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.
  • 35 Méndez I, Andreu FJ, Sáez E, et al.. Ductal carcinoma in situ and atypical ductal hyperplasia of the breast diagnosed at stereotactic core biopsy. Breast J 2001;7(1):14–18.
  • 36 Mittendorf EA, Arciero CA, Gutchell V, Hooke J, Shriver CD. Core biopsy diagnosis of ductal carcinoma in situ: an indication for sentinel lymph node biopsy. Curr Surg 2005;62(2):253–257.
  • 37 Moran CJ, Kell MR, Flanagan FL, Kennedy M, Gorey TF, Kerin MJ. Role of sentinel lymph node biopsy in high-risk ductal carcinoma in situ patients. Am J Surg 2007;194(2):172–175.
  • 38 Nagashima T, Hashimoto H, Oshida K, et al.. Ultrasound demonstration of mammographically detected microcalcifications in patients with ductal carcinoma in situ of the breast. Breast Cancer 2005;12(3):216–220.
  • 39 Orel SG, Rosen M, Mies C, Schnall MDMR. MR imaging-guided 9-gauge vacuum-assisted core-needle breast biopsy: initial experience. Radiology 2006;238(1):54–61.
  • 40 Pandelidis S, Heiland D, Jones D, Stough K, Trapeni J, Suliman Y. Accuracy of 11-gauge vacuum-assisted core biopsy of mammographic breast lesions. Ann Surg Oncol 2003;10(1):43–47.
  • 41 Peters N, Hoorntje LE, Mali WP, Borel Rinkes IH, Peeters PH. Diagnostic performance of stereotactic large core needle biopsy for nonpalpable breast lesions in routine clinical practice. Int J Cancer 2008;122(2):468–471.
  • 42 Pijnappel RM, van den Donk M, Holland R, et al.. Diagnostic accuracy for different strategies of image-guided breast intervention in cases of nonpalpable breast lesions. Br J Cancer 2004;90(3):595–600.
  • 43 Renshaw AA. Predicting invasion in the excision specimen from breast core needle biopsy specimens with only ductal carcinoma in situ. Arch Pathol Lab Med 2002;126(1):39–41.
  • 44 Rutstein LA, Johnson RR, Poller WR, et al.. Predictors of residual invasive disease after core needle biopsy diagnosis of ductal carcinoma in situ. Breast J 2007;13(3):251–257.
  • 45 Tan JC, McCready DR, Easson AM, Leong WL. Role of sentinel lymph node biopsy in ductal carcinoma-in-situ treated by mastectomy. Ann Surg Oncol 2007;14(2):638–645.
  • 46 Tonegutti M, Girardi V. Stereotactic vacuum-assisted breast biopsy in 268 nonpalpable lesions. Radiol Med (Torino) 2008;113(1):65–75.
  • 47 Verkooijen HM; Core Biopsy After Radiological Localisation (COBRA) Study Group. Diagnostic accuracy of stereotactic large-core needle biopsy for nonpalpable breast disease: results of a multicenter prospective study with 95% surgical confirmation. Int J Cancer 2002;99(6):853–859.
  • 48 Wei X, Li Y, Zhang S, Zhu Y, Fan Y. Experience in large-core needle biopsy in the diagnosis of 1431 breast lesions. Med Oncol 2010 Mar 26. [Epub ahead of print].
  • 49 Wu YC, Chen DR, Kuo SJ. Personal experience of ultrasound-guided 14-gauge core biopsy of breast tumor. Eur J Surg Oncol 2006;32(7):715–718.
  • 50 Yamamoto D, Yamada M, Okugawa H, Tanaka K. Predicting invasion in mammographically detected microcalcifcation: a preliminary report. World J Surg Oncol 2004;2:8.
  • 51 Yen TW, Hunt KK, Ross 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.
  • 52 Youk JH, Kim EK, Kim MJ, Oh KK. Sonographically guided 14-gauge core needle biopsy of breast masses: a review of 2,420 cases with long-term follow-up. AJR Am J Roentgenol 2008;190(1):202–207.
  • 53 Zuiani C, Mazzarella F, Londero V, Linda A, Puglisi F, Bazzocchi M. Stereotactic vacuum-assisted breast biopsy: results, follow-up and correlation with radiological suspicion. Radiol Med (Torino) 2007;112(2):304–317.
  • 54 Liberman L, Dershaw DD, Glassman JR, et al.. Analysis of cancers not diagnosed at stereotactic core breast biopsy. Radiology 1997;203(1):151–157.
  • 55 Wallis MG, Cheung S, Kearins O, Lawrence GM. Non-operative diagnosis: effect on repeat-operation rates in the UK breast screening programme. Eur Radiol 2009;19(2):318–323.
  • 56 Mansel RE, Fallowfield L, Kissin M, et al.. Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial. J Natl Cancer Inst 2006;98(9):599–609.
  • 57 Liu CQ, Guo Y, Shi JY, Sheng Y. Late morbidity associated with a tumour-negative sentinel lymph node biopsy in primary breast cancer patients: a systematic review. Eur J Cancer 2009;45(9):1560–1568.
  • 58 McLaughlin SA, Wright MJ, Morris 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.

Article History

Received December 1, 2010; revision requested January 7, 2011; revision received February 14; accepted February 22; final version accepted February 25.
Published online: July 2011
Published in print: July 2011