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01-07-2017 | Review

Multivariate model to identify women at low risk of cancer upgrade after a core needle biopsy diagnosis of atypical ductal hyperplasia

Authors: Alvaro Peña, Sejal S. Shah, Robert T. Fazzio, Tanya L. Hoskin, Rushin D. Brahmbhatt, Tina J. Hieken, James W. Jakub, Judy C. Boughey, Daniel W. Visscher, Amy C. Degnim

Published in: Breast Cancer Research and Treatment | Issue 2/2017

Abstract

Purpose

Atypical ductal hyperplasia (ADH) identified on percutaneous breast biopsy represents a high-risk lesion, upgrading to cancer with surgical excision in ~7–45.8% of cases. Routine excision is questioned due to potential overtreatment and cost. This study evaluates clinical, imaging, and histologic features to predict the risk of upgrade.

Methods

With IRB approval, a single-institution retrospective review was performed of patients who underwent surgical excision of ADH diagnosed by core biopsy from June 2005 to June 2013. We reviewed electronic medical records, breast imaging, and biopsy slides. Multiple imputation was used for missing data. Association of various features with cancer upgrade was assessed using logistic regression.

Results

Among 399 cases, the upgrade rate to cancer was 16.0%, (95% CI: 12.8–20.0%), with nine invasive cancers and 55 ductal carcinoma in situ (DCIS) only. Via a logistic regression approach, we defined a subgroup with low risk for upgrade: women whose biopsies showed no individual cell necrosis, and either a) 1 focus of ADH with ≥50% removal, or b) 2–3 foci with ≥90% removal. Cases meeting these criteria had an upgrade rate of 4.9% (95% CI: 1.0–8.9%), compared to 21.4% (16.4–26.3%) in cases that did not meet this low-risk definition.

Conclusions

ADH on core biopsy with low risk of upgrade to cancer is defined by lack of individual cell necrosis, number of foci of ADH, and percent of imaging lesion removed. If these findings are validated, women whose biopsies meet low-risk criteria might be considered for prevention therapy and surveillance without surgical excision.

McGhan LJ, Pockaj BA, Wasif N, Giurescu ME, McCullough AE, Gray RJ (2012) Atypical ductal hyperplasia on core biopsy: an automatic trigger for excisional biopsy? Ann Surg Oncol 19(10):3264–3269. doi:10.1245/s10434-012-2575-0 CrossRefPubMed

Wagoner MJ, Laronga C, Acs G (2009) Extent and histologic pattern of atypical ductal hyperplasia present on core needle biopsy specimens of the breast can predict ductal carcinoma in situ in subsequent excision. Am J Clin Pathol 131(1):112–121. doi:10.1309/AJCPGHEJ2R8UYFGP CrossRefPubMed

Bleyer A, Welch HG (2012) Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med 367(21):1998–2005. doi:10.1056/NEJMoa1206809 CrossRefPubMed

Neal CH, Coletti MC, Joe A, Jeffries DO, Helvie MA (2013) Does digital mammography increase detection of high-risk breast lesions presenting as calcifications? AJR Am J Roentgenol 201(5):1148–1154. doi:10.2214/AJR.12.10195 CrossRefPubMed

Pearlman MD, Griffin JL (2010) Benign breast disease. Obstet Gynecol 116(3):747–758. doi:10.1097/AOG.0b013e3181ee9fc7 CrossRefPubMed

Dupont WD, Page DL (1985) Risk factors for breast cancer in women with proliferative breast disease. N Engl J Med 312(3):146–151CrossRefPubMed

Hartmann LC, Sellers TA, Frost MH, Lingle WL, Degnim AC, Ghosh K, Vierkant RA, Maloney SD, Pankratz VS, Hillman DW, Suman VJ, Johnson J, Blake C, Tlsty T, Vachon CM, Melton LJ 3rd, Visscher DW (2005) Benign breast disease and the risk of breast cancer. N Engl J Med 353(3):229–237CrossRefPubMed

Hartmann LC, Radisky DC, Frost MH, Santen RJ, Vierkant RA, Benetti LL, Tarabishy Y, Ghosh K, Visscher DW, Degnim AC (2014) Understanding the premalignant potential of atypical hyperplasia through its natural history: a longitudinal cohort study. Cancer Prev Res 7(2):211–217. doi:10.1158/1940-6207.CAPR-13-0222 CrossRef

Tice JA, O’Meara ES, Weaver DL, Vachon C, Ballard-Barbash R, Kerlikowske K (2013) Benign breast disease, mammographic breast density, and the risk of breast cancer. J Natl Cancer Inst 105(14):1043–1049. doi:10.1093/jnci/djt124 CrossRefPubMedPubMedCentral

10.

Jacobs TW, Byrne C, Colditz G, Connolly JL, Schnitt SJ (2001) Pathologic features of breast cancers in women with previous benign breast disease. Am J Clin Pathol 115(3):362–369. doi:10.1309/UP07-K3KD-25NL-D3M8 CrossRefPubMed

11.

Degnim AC, King TA (2013) Surgical management of high-risk breast lesions. Surg clin North Am 93(2):329–340. doi:10.1016/j.suc.2012.12.005 CrossRefPubMed

12.

Allison KH, Eby PR, Kohr J, DeMartini WB, Lehman CD (2011) Atypical ductal hyperplasia on vacuum-assisted breast biopsy: suspicion for ductal carcinoma in situ can stratify patients at high risk for upgrade. Hum Pathol 42(1):41–50. doi:10.1016/j.humpath.2010.06.011 CrossRefPubMed

13.

Forgeard C, Benchaib M, Guerin N, Thiesse P, Mignotte H, Faure C, Clement-Chassagne C, Treilleux I (2008) Is surgical biopsy mandatory in case of atypical ductal hyperplasia on 11-gauge core needle biopsy? A retrospective study of 300 patients. Am J Surg 196(3):339–345. doi:10.1016/j.amjsurg.2007.07.038 CrossRefPubMed

14.

Ely KA, Carter BA, Jensen RA, Simpson JF, Page DL (2001) Core biopsy of the breast with atypical ductal hyperplasia: a probabilistic approach to reporting. Am J Surg Pathol 25(8):1017–1021CrossRefPubMed

15.

Sneige N, Lim SC, Whitman GJ, Krishnamurthy S, Sahin AA, Smith TL, Stelling CB (2003) Atypical ductal hyperplasia diagnosis by directional vacuum-assisted stereotactic biopsy of breast microcalcifications. Considerations for surgical excision. Am J Clin Pathol 119(2):248–253. doi:10.1309/0GYV-4F2L-LJAV-4GFN CrossRefPubMed

16.

Kim J, Han W, Go EY, Moon HG, Ahn SK, Shin HC, You JM, Chang JM, Cho N, Moon WK, Park IA, Noh DY (2012) Validation of a scoring system for predicting malignancy in patients diagnosed with atypical ductal hyperplasia using an ultrasound-guided core needle biopsy. J Breast Cancer 15(4):407–411. doi:10.4048/jbc.2012.15.4.407 CrossRefPubMedPubMedCentral

17.

Ko E, Han W, Lee JW, Cho J, Kim EK, Jung SY, Kang MJ, Moon WK, Park IA, Kim SW, Kim KS, Lee ES, Min KH, Kim SW, Noh DY (2008) Scoring system for predicting malignancy in patients diagnosed with atypical ductal hyperplasia at ultrasound-guided core needle biopsy. Breast Cancer Res Treat 112(1):189–195. doi:10.1007/s10549-007-9824-0 CrossRefPubMed

18.

Nguyen CV, Albarracin CT, Whitman GJ, Lopez A, Sneige N (2011) Atypical ductal hyperplasia in directional vacuum-assisted biopsy of breast microcalcifications: considerations for surgical excision. Ann Surg Oncol 18(3):752–761. doi:10.1245/s10434-010-1127-8 CrossRefPubMed

19.

Kunju LP, Kleer CG (2007) Significance of flat epithelial atypia on mammotome core needle biopsy: should it be excised? Hum Pathol 38(1):35–41. doi:10.1016/j.humpath.2006.08.008 CrossRefPubMed

20.

Rubin DB (1987) Multiple imputations for nonresponse in surveys. Wiley, New YorkCrossRef

21.

Sterne JA, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, Wood AM, Carpenter JR (2009) Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ 338:b2393. doi:10.1136/bmj.b2393 CrossRefPubMedPubMedCentral

22.

van Buuren S (2007) Multiple imputation of discrete and continuous data by fully conditional specification. Stat Methods Med Res 16(3):219–242. doi:10.1177/0962280206074463 CrossRefPubMed

23.

van Buuren S, Groothuis-Oudshoorn K (2011) Mice: multivariate imputation by chained equations in R. J Stat Softw 45(3):1–67CrossRef

24.

Peduzzi P, Concato J, Kemper E, Holford TR, Feinstein AR (1996) A simulation study of the number of events per variable in logistic regression analysis. J Clin Epidemiol 49(12):1373–1379CrossRefPubMed

25.

Harrell FE (2001) Regression modeling strategies: with applications to linear models, logistic regression, and survival. Springer, New YorkCrossRef

26.

Jackman RJ, Birdwell RL, Ikeda DM (2002) Atypical ductal hyperplasia: can some lesions be defined as probably benign after stereotactic 11-gauge vacuum-assisted biopsy, eliminating the recommendation for surgical excision? Radiology 224(2):548–554CrossRefPubMed

27.

Kohr JR, Eby PR, Allison KH, DeMartini WB, Gutierrez RL, Peacock S, Lehman CD (2010) Risk of upgrade of atypical ductal hyperplasia after stereotactic breast biopsy: effects of number of foci and complete removal of calcifications. Radiology 255(3):723–730. doi:10.1148/radiol.09091406 CrossRefPubMed

28.

Yeh IT, Dimitrov D, Otto P, Miller AR, Kahlenberg MS, Cruz A (2003) Pathologic review of atypical hyperplasia identified by image-guided breast needle core biopsy. Correlation with excision specimen. Arch Pathol Lab Med 127(1):49–54. doi:10.1043/0003-9985(2003)127<49:PROAHI>2.0.CO;2 PubMed

29.

Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239–257CrossRefPubMedPubMedCentral

30.

NCCN (2016) National Comprehensive Cancer Network Clinical Guidelines, Breast Cancer Risk Reduction, v1,2916. http://www.nccn.org/professionals/physician_gls/pdf/breast_risk.pdf. Accessed 14 Dec 2016

31.

Degnim AC, Visscher DW, Berman HK, Frost MH, Sellers TA, Vierkant RA, Maloney SD, Pankratz VS, de Groen PC, Lingle WL, Ghosh K, Penheiter L, Tlsty T, Melton LJ 3rd, Reynolds CA, Hartmann LC (2007) Stratification of breast cancer risk in women with atypia: a Mayo cohort study. J Clin Oncol 25(19):2671–2677. doi:10.1200/JCO.2006.09.0217 CrossRefPubMed

32.

Coopey SB, Mazzola E, Buckley JM, Sharko J, Belli AK, Kim EM, Polubriaginof F, Parmigiani G, Garber JE, Smith BL, Gadd MA, Specht MC, Guidi AJ, Roche CA, Hughes KS (2012) The role of chemoprevention in modifying the risk of breast cancer in women with atypical breast lesions. Breast Cancer Res Treat 136(3):627–633. doi:10.1007/s10549-012-2318-8 CrossRefPubMed

33.

Degnim AC, Dupont WD, Radisky DC, Vierkant RA, Frank RD, Frost MH, Winham SJ, Sanders ME, Smith JR, Page DL, Hoskin TL, Vachon CM, Ghosh K, Hieken TJ, Denison LA, Carter JM, Hartmann LC, Visscher DW (2016) Extent of atypical hyperplasia stratifies breast cancer risk in 2 independent cohorts of women. Cancer 122(19):2971–2978. doi:10.1002/cncr.30153 CrossRefPubMedPubMedCentral

34.

Fisher B, Costantino JP, Wickerham DL, Cecchini RS, Cronin WM, Robidoux A, Bevers TB, Kavanah MT, Atkins JN, Margolese RG, Runowicz CD, James JM, Ford LG, Wolmark N (2005) Tamoxifen for the prevention of breast cancer: current status of the National Surgical Adjuvant Breast and Bowel Project P-1 study. J Natl Cancer Inst 97(22):1652–1662. doi:10.1093/jnci/dji372 CrossRefPubMed

35.

Vogel VG, Costantino JP, Wickerham DL, Cronin WM, Cecchini RS, Atkins JN, Bevers TB, Fehrenbacher L, Pajon ER, Wade JL 3rd, Robidoux A, Margolese RG, James J, Runowicz CD, Ganz PA, Reis SE, McCaskill-Stevens W, Ford LG, Jordan VC, Wolmark N (2010) Update of the national surgical adjuvant breast and bowel project study of tamoxifen and raloxifene (STAR) P-2 trial: preventing breast cancer. Cancer Prev Res 3(6):696–706. doi:10.1158/1940-6207.CAPR-10-0076 CrossRef

36.

Goss PE, Ingle JN, Ales-Martinez JE, Cheung AM, Chlebowski RT, Wactawski-Wende J, McTiernan A, Robbins J, Johnson KC, Martin LW, Winquist E, Sarto GE, Garber JE, Fabian CJ, Pujol P, Maunsell E, Farmer P, Gelmon KA, Tu D, Richardson H (2011) Exemestane for breast-cancer prevention in postmenopausal women. N Engl J Med 364(25):2381–2391. doi:10.1056/NEJMoa1103507 CrossRefPubMed

37.

Cuzick J, Sestak I, Forbes JF, Dowsett M, Knox J, Cawthorn S, Saunders C, Roche N, Mansel RE, von Minckwitz G, Bonanni B, Palva T, Howell A (2014) Anastrozole for prevention of breast cancer in high-risk postmenopausal women (IBIS-II): an international, double-blind, randomised placebo-controlled trial. Lancet 383(9922):1041–1048. doi:10.1016/S0140-6736(13)62292-8 CrossRefPubMed

38.

Chen YY, DeVries S, Anderson J, Lessing J, Swain R, Chin K, Shim V, Esserman LJ, Waldman FM, Hwang ES (2009) Pathologic and biologic response to preoperative endocrine therapy in patients with ER-positive ductal carcinoma in situ. BMC Cancer 9:285. doi:10.1186/1471-2407-9-285 CrossRefPubMedPubMedCentral

39.

Menen RS, Ganesan N, Bevers T, Ying J, Coyne R, Lane D, Albarracin C, Bedrosian I (2017) Long-term safety of observation in selected women following core biopsy diagnosis of atypical ductal hyperplasia. Ann Surg Oncol. 24(1):70–76. doi: 10.1245/s10434-016-5512-9. Epub 2016 Aug 29. doi:10.1245/s10434-016-5512-9

40.

Deshaies I, Provencher L, Jacob S, Cote G, Robert J, Desbiens C, Poirier B, Hogue JC, Vachon E, Diorio C (2011) Factors associated with upgrading to malignancy at surgery of atypical ductal hyperplasia diagnosed on core biopsy. Breast 20(1):50–55. doi:10.1016/j.breast.2010.06.004 CrossRefPubMed

Title: Multivariate model to identify women at low risk of cancer upgrade after a core needle biopsy diagnosis of atypical ductal hyperplasia
Authors: Alvaro Peña
Sejal S. Shah
Robert T. Fazzio
Tanya L. Hoskin
Rushin D. Brahmbhatt
Tina J. Hieken
James W. Jakub
Judy C. Boughey
Daniel W. Visscher
Amy C. Degnim
Publication date: 01-07-2017
Publisher: Springer US
Published in: Breast Cancer Research and Treatment / Issue 2/2017
Print ISSN: 0167-6806
Electronic ISSN: 1573-7217
DOI: https://doi.org/10.1007/s10549-017-4253-1

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