Predictive factors for the presence of invasive components in patients diagnosed with ductal carcinoma in situ based on preoperative biopsy

Kwan Ho Lee, Jeong Woo Han, Eun Young Kim, Ji Sup Yun, Yong Lai Park, Chan Heun Park, Kwan Ho Lee, Jeong Woo Han, Eun Young Kim, Ji Sup Yun, Yong Lai Park, Chan Heun Park

Abstract

Background: In patients diagnosed with ductal carcinoma in situ (DCIS) with needle biopsy before surgery, invasive component (IC) is often found in the postoperative tissue, which results in altered post-surgical care. However, there are no clinically available factors to predict IC, and few MRI studies are available for the detection of IC in DCIS patients. The purpose of this study was to evaluate which risk factors can predict IC preoperatively.

Methods: Patients with a DCIS diagnosis based on preoperative biopsy, who underwent breast surgery Kangbuk Samsung Hospital between Jan 2005 and June 2018, were retrospectively evaluated. Clinico-pathological and breast MRI factors were compared between DCIS and DCIS with IC in postsurgical specimens.

Results: Of the 431 patients with a preoperative diagnosis of DCIS, 34 (7.9%) showed IC during the postoperative pathological investigations, and 217 (50.3%) underwent breast MRI. Among MRI-related factors, Mass-like enhancement on MRI was the sole but significant predictor of IC (HR = 0.26, C.I. = 0.07-0.93, p = 0.038), while nipple-areolar complex invasion, enhancement peak and pattern were not statistically significant. Nuclear grade was the only significant predictor of IC in the analysis of other clinico-pathological factors (HR = 2.39, C.I. = 1.05-5.42, p = 0.038 in univariate analysis, HR = 2.86, C.I. = 1.14-7.14, p = 0.025 in multivariate analysis).

Conclusions: Mass-like enhancement on MRI and high nuclear grade were associated with IC in patients with preoperative diagnosis of DCIS. Considering the high sensitivity of breast MRI for IC, further evaluation of the predictive value of MRI in preoperative DCIS patients is desirable.

Keywords: Biomarkers; Breast; Ductal carcinoma in situ; Magnetic resonance imaging.

Conflict of interest statement

The authors declare that they have no competing interests.

References

    1. 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. doi: 10.1002/jso.20445.
    1. Maffuz A, Barroso-Bravo S, Najera I, Zarco G, Alvarado-Cabrero I, Rodriguez-Cuevas SA. Tumor size as predictor of microinvasion, invasion, and axillary metastasis in ductal carcinoma in situ. J Exp Clin Cancer Res. 2006;25(2):223–227.
    1. 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. doi: 10.1002/bjs.5735.
    1. Guillot E, Vaysse C, Goetgeluck J, Falcou MC, Couturaud B, Fitoussi A, et al. Extensive pure ductal carcinoma in situ of the breast: identification of predictors of associated infiltrating carcinoma and lymph node metastasis before immediate reconstructive surgery. Breast. 2014;23(2):97–103. doi: 10.1016/j.breast.2013.12.002.
    1. Goto M, Yuen S, Akazawa K, Nishida K, Konishi E, Kajihara M, et al. The role of breast MR imaging in pre-operative determination of invasive disease for ductal carcinoma in situ diagnosed by needle biopsy. Eur Radiol. 2012;22(6):1255–1264. doi: 10.1007/s00330-011-2357-2.
    1. Deurloo EE, Sriram JD, Teertstra HJ, Loo CE, Wesseling J, Rutgers EJ, et al. MRI of the breast in patients with DCIS to exclude the presence of invasive disease. Eur Radiol. 2012;22(7):1504–1511. doi: 10.1007/s00330-012-2394-5.
    1. Mori N, Ota H, Mugikura S, Takasawa C, Tominaga J, Ishida T, et al. Detection of invasive components in cases of breast ductal carcinoma in situ on biopsy by using apparent diffusion coefficient MR parameters. Eur Radiol. 2013;23(10):2705–2712. doi: 10.1007/s00330-013-2902-2.
    1. Wisner DJ, Hwang ES, Chang CB, Tso HH, Joe BN, Lessing JN, et al. Features of occult invasion in biopsy-proven DCIS at breast MRI. Breast J. 2013;19(6):650–658. doi: 10.1111/tbj.12201.
    1. Park AY, Gweon HM, Son EJ, Yoo M, Kim JA, Youk JH. Ductal carcinoma in situ diagnosed at US-guided 14-gauge core-needle biopsy for breast mass: preoperative predictors of invasive breast cancer. Eur J Radiol. 2014;83(4):654–659. doi: 10.1016/j.ejrad.2014.01.010.
    1. Nori J, Meattini I, Giannotti E, Abdulcadir D, Mariscotti G, Calabrese M, et al. Role of preoperative breast MRI in ductal carcinoma in situ for prediction of the presence and assessment of the extent of occult invasive component. Breast J. 2014;20(3):243–248. doi: 10.1111/tbj.12250.
    1. Lee CW, Wu HK, Lai HW, Wu WP, Chen ST, Chen DR, et al. Preoperative clinicopathologic factors and breast magnetic resonance imaging features can predict ductal carcinoma in situ with invasive components. Eur J Radiol. 2016;85(4):780–789. doi: 10.1016/j.ejrad.2015.12.027.
    1. American College of Radiology . BI-RADS Committee. ACR BI-RADS Atlas: Breast Imaging Reporting and Data System. 5. Reston: American College of Radiology; 2013.
    1. Therneau TM, Thomas L. Survival: survival analysis. R package version. 2015;2:38.
    1. Core Team R. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2016.
    1. Wilkie C, White L, Dupont E, Cantor A, Cox CE. An update of sentinel lymph node mapping in patients with ductal carcinoma in situ. Am J Surg. 2005;190(4):563–566. doi: 10.1016/j.amjsurg.2005.06.011.
    1. Yen TW, Hunt KK, Ross MI, Mirza NQ, Babiera GV, Meric-Bernstam F, 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. doi: 10.1016/j.jamcollsurg.2004.11.012.
    1. 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. doi: 10.1007/s10549-006-9167-2.
    1. Rutstein LA, Johnson RR, Poller WR, Dabbs D, Groblewski J, Rakitt T, et al. Predictors of residual invasive disease after core needle biopsy diagnosis of ductal carcinoma in situ. Breast J. 2007;13(3):251–257. doi: 10.1111/j.1524-4741.2007.00418.x.
    1. Lee JM, Kaplan JB, Murray MP, Mazur-Grbec M, Tadic T, Stimac D, et al. Underestimation of DCIS at MRI-guided vacuum-assisted breast biopsy. AJR Am J Roentgenol. 2007;189(2):468–474. doi: 10.2214/AJR.07.2172.
    1. Go EM, Chan SK, Vong JS, Lui PC, Chan AW, Ma TK, et al. Predictors of invasion in needle core biopsies of the breast with ductal carcinoma in situ. Mod Pathol. 2010;23(5):737–742. doi: 10.1038/modpathol.2009.187.
    1. 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. doi: 10.1016/S1015-9584(10)60013-9.
    1. Huang YT, Cheung YC, Lo YF, Ueng SH, Kuo WL, Chen SC. MRI findings of cancers preoperatively diagnosed as pure DCIS at core needle biopsy. Acta Radiol. 2011;52(10):1064–1068. doi: 10.1258/ar.2011.110213.
    1. Han JS, Molberg KH, Sarode V. Predictors of invasion and axillary lymph node metastasis in patients with a core biopsy diagnosis of ductal carcinoma in situ: an analysis of 255 cases. Breast J. 2011;17(3):223–229. doi: 10.1111/j.1524-4741.2011.01069.x.
    1. Brennan ME, Turner RM, Ciatto S, Marinovich ML, French JR, Macaskill P, et al. Ductal carcinoma in situ at core-needle biopsy: meta-analysis of underestimation and predictors of invasive breast cancer. Radiology. 2011;260(1):119–128. doi: 10.1148/radiol.11102368.
    1. Kim J, Han W, Lee JW, You JM, Shin HC, Ahn SK, et al. Factors associated with upstaging from ductal carcinoma in situ following core needle biopsy to invasive cancer in subsequent surgical excision. Breast. 2012;21(5):641–645. doi: 10.1016/j.breast.2012.06.012.
    1. Hollingsworth AB, Stough RG. Multicentric and contralateral invasive tumors identified with pre-op MRI in patients newly diagnosed with ductal carcinoma in situ of the breast. Breast J. 2012;18(5):420–427. doi: 10.1111/j.1524-4741.2012.01273.x.
    1. Trentin C, Dominelli V, Maisonneuve P, Menna S, Bazolli B, Luini A, et al. Predictors of invasive breast cancer and lymph node involvement in ductal carcinoma in situ initially diagnosed by vacuum-assisted breast biopsy: experience of 733 cases. Breast. 2012;21(5):635–640. doi: 10.1016/j.breast.2012.06.009.
    1. Nadrljanski M, Maksimovic R, Plesinac-Karapandzic V, Nikitovic M, Markovic-Vasiljkovic B, Milosevic Z. Positive enhancement integral values in dynamic contrast enhanced magnetic resonance imaging of breast carcinoma: ductal carcinoma in situ vs. invasive ductal carcinoma. Eur J Radiol. 2014;83(8):1363–1367. doi: 10.1016/j.ejrad.2014.05.006.
    1. Santamaria G, Velasco M, Farrus B, Zanon G, Fernandez PL. Preoperative MRI of pure intraductal breast carcinoma--a valuable adjunct to mammography in assessing cancer extent. Breast. 2008;17(2):186–194. doi: 10.1016/j.breast.2007.09.005.
    1. Lee JW, Han W, Ko E, Cho J, Kim EK, Jung SY, 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. doi: 10.1002/jso.21077.
    1. Kim SJ, Park YM, Jung HK. Nonmasslike lesions on breast sonography: comparison between benign and malignant lesions. J Ultrasound Med. 2014;33(3):421–430. doi: 10.7863/ultra.33.3.421.
    1. Ko KH, Hsu HH, Yu JC, Peng YJ, Tung HJ, Chu CM, et al. Non-mass-like breast lesions at ultrasonography: feature analysis and BI-RADS assessment. Eur J Radiol. 2015;84(1):77–85. doi: 10.1016/j.ejrad.2014.10.010.
    1. Lee J, Lee JH, Baik S, Cho E, Kim DW, Kwon HJ, et al. Non-mass lesions on screening breast ultrasound. Med Ultrason. 2016;18(4):446–451. doi: 10.11152/mu-871.
    1. Park JW, Ko KH, Kim EK, Kuzmiak CM, Jung HK. Non-mass breast lesions on ultrasound: final outcomes and predictors of malignancy. Acta Radiol. 2017;58(9):1054–1060. doi: 10.1177/0284185116683574.
    1. Kim HR, Jung HK. Histopathology findings of non-mass cancers on breast ultrasound. Acta Radiol Open. 2018;7(6):2058460118774957.

Source: PubMed

3
Tilaa