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Radiology for Ductal Carcinoma In Situ of the Breast: Updates on Invasive Cancer Progression and Active Monitoring

  • Lars J Grimm (Department of Radiology, Duke University, Duke University Medical Center)
  • Received : 2024.01.31
  • Accepted : 2024.04.30
  • Published : 2024.08.01

Abstract

Ductal carcinoma in situ (DCIS) accounts for approximately 30% of new breast cancer diagnoses. However, our understanding of how normal breast tissue evolves into DCIS and invasive cancers remains insufficient. Further, conclusions regarding the mechanisms of disease progression in terms of histopathology, genetics, and radiology are often conflicting and have implications for treatment planning. Moreover, the increase in DCIS diagnoses since the adoption of organized breast cancer screening programs has raised concerns about overdiagnosis and subsequent overtreatment. Active monitoring, a nonsurgical management strategy for DCIS, avoids surgery in favor of close imaging follow-up to de-escalate therapy and provides more treatment options. However, the two major challenges in active monitoring are identifying occult invasive cancer and patients at risk of invasive cancer progression. Subsequently, four prospective active monitoring trials are ongoing to determine the feasibility of active monitoring and refine the patient eligibility criteria and follow-up intervals. Radiologists play a major role in determining eligibility for active monitoring and reviewing surveillance images for disease progression. Trial results published over the next few years would support a new era of multidisciplinary DCIS care.

Keywords

References

  1. Menon G, Alkabban FM, Ferguson T. Breast cancer. In: StatPearls [Internet]. Treasure Island: StatPearls Publishing, 2024 [accessed on January 1, 2024]. Available at: https://pubmed.ncbi.nlm.nih.gov/29493913
  2. Grimm LJ, Rahbar H, Abdelmalak M, Hall AH, Ryser MD. Ductal carcinoma in situ: state-of-the-art review. Radiology 2022;302:246-255
  3. National Cancer Institute. Cancer stat facts: female breast cancer [accessed on July 12, 2021]. Available at: https://seer.cancer.gov/statfacts/html/breast.html
  4. Bombonati A, Sgroi DC. The molecular pathology of breast cancer progression. J Pathol 2011;223:307-317
  5. Dyrstad SW, Yan Y, Fowler AM, Colditz GA. Breast cancer risk associated with benign breast disease: systematic review and meta-analysis. Breast Cancer Res Treat 2015;149:569-575
  6. Elston CW, Sloane JP, Amendoeira I, Apostolikas N, Bellocq JP, Bianchi S, et al. Causes of inconsistency in diagnosing and classifying intraductal proliferations of the breast. Eur J Cancer 2000;36:1769-1772
  7. 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;260:119-128
  8. van Seijen M, Joz'wiak K, Pinder SE, Hall A, Krishnamurthy S, Thomas JS, et al. Variability in grading of ductal carcinoma in situ among an international group of pathologists. J Pathol Clin Res 2021;7:233-242
  9. Casasent AK, Edgerton M, Navin NE. Genome evolution in ductal carcinoma in situ: invasion of the clones. J Pathol 2017;241:208-218
  10. Kim SY, Jung SH, Kim MS, Baek IP, Lee SH, Kim TM, et al. Genomic differences between pure ductal carcinoma in situ and synchronous ductal carcinoma in situ with invasive breast cancer. Oncotarget 2015;6:7597-7607
  11. Casasent AK, Schalck A, Gao R, Sei E, Long A, Pangburn W, et al. Multiclonal invasion in breast tumors identified by topographic single cell sequencing. Cell 2018;172:205-217. e12
  12. Turashvili G, Brogi E. Tumor heterogeneity in breast cancer. Front Med (Lausanne) 2017;4:227
  13. Gajdos C, Tartter PI, Bleiweiss IJ, Hermann G, de Csepel J, Estabrook A, et al. Mammographic appearance of nonpalpable breast cancer reflects pathologic characteristics. Ann Surg 2002;235:246-251
  14. Bare M, Tora N, Salas D, Sentis M, Ferrer J, Ibanez J, et al. Mammographic and clinical characteristics of different phenotypes of screen-detected and interval breast cancers in a nationwide screening program. Breast Cancer Res Treat 2015;154:403-415
  15. Berg WA, Zhang Z, Lehrer D, Jong RA, Pisano ED, Barr RG, et al. Detection of breast cancer with addition of annual screening ultrasound or a single screening MRI to mammography in women with elevated breast cancer risk. JAMA 2012;307:1394-1404
  16. Saadatmand S, Geuzinge HA, Rutgers EJT, Mann RM, de Roy van Zuidewijn DBW, Zonderland HM, et al. MRI versus mammography for breast cancer screening in women with familial risk (FaMRIsc): a multicentre, randomised, controlled trial. Lancet Oncol 2019;20:1136-1147
  17. Gradishar WJ, Moran MS, Abraham J, Aft R, Agnese D, Allison KH, et al. Breast cancer, version 3.2022, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 2022;20:691-722
  18. Wheelwright S, Matthews L, Jenkins V, May S, Rea D, Fairbrother P, et al. Recruiting women with ductal carcinoma in situ to a randomised controlled trial: lessons from the LORIS study. Trials 2023;24:670
  19. Nelson HD, Pappas M, Cantor A, Griffin J, Daeges M, Humphrey L. Harms of breast cancer screening: systematic review to update the 2009 U.S. preventive services task force recommendation. Ann Intern Med 2016;164:256-267
  20. Ryser MD, Lange J, Inoue LYT, O'Meara ES, Gard C, Miglioretti DL, et al. Estimation of breast cancer overdiagnosis in a U.S. breast screening cohort. Ann Intern Med 2022;175:471-478
  21. Virnig BA, Tuttle TM, Shamliyan T, Kane RL. Ductal carcinoma in situ of the breast: a systematic review of incidence, treatment, and outcomes. J Natl Cancer Inst 2010;102:170-178
  22. Oseni TO, Zhang B, Coopey SB, Gadd MA, Hughes KS, Chang DC. Twenty-five year trends in the incidence of ductal carcinoma in situ in US women. J Am Coll Surg 2019;228:932-939
  23. Katalinic A, Eisemann N, Kraywinkel K, Noftz MR, Hubner J. Breast cancer incidence and mortality before and after implementation of the German mammography screening program. Int J Cancer 2020;147:709-718
  24. Duffy SW, Dibden A, Michalopoulos D, Offman J, Parmar D, Jenkins J, et al. Screen detection of ductal carcinoma in situ and subsequent incidence of invasive interval breast cancers: a retrospective population-based study. Lancet Oncol 2016;17:109-114
  25. Giannakeas V, Sopik V, Narod SA. Association of a diagnosis of ductal carcinoma in situ with death from breast cancer. JAMA Netw Open 2020;3:e2017124
  26. Worni M, Akushevich I, Greenup R, Sarma D, Ryser MD, Myers ER, et al. Trends in treatment patterns and outcomes for ductal carcinoma in situ. J Natl Cancer Inst 2015;107:djv263
  27. Oseni TO, Smith BL, Lehman CD, Vijapura CA, Pinnamaneni N, Bahl M. Do eligibility criteria for ductal carcinoma in situ (DCIS) active surveillance trials identify patients at low risk for upgrade to invasive carcinoma? Ann Surg Oncol 2020;27:4459-4465
  28. Grimm LJ, Ryser MD, Partridge AH, Thompson AM, Thomas JS, Wesseling J, et al. Surgical upstaging rates for vacuum assisted biopsy proven DCIS: implications for active surveillance trials. Ann Surg Oncol 2017;24:3534-3540
  29. Pilewskie M, Stempel M, Rosenfeld H, Eaton A, Van Zee KJ, Morrow M. Do LORIS trial eligibility criteria identify a ductal carcinoma in situ patient population at low risk of upgrade to invasive carcinoma? Ann Surg Oncol 2016;23:3487-3493
  30. Selvakumaran V, Hou R, Baker JA, Yoon SC, Ghate SV, Walsh R, et al. Predicting upstaging of DCIS to invasive disease: radiologists's predictive performance. Acad Radiol 2020;27:1580-1585
  31. Grimm LJ, Neely B, Hou R, Selvakumaran V, Baker JA, Yoon SC, et al. Mixed-methods study to predict upstaging of DCIS to invasive disease on mammography. AJR Am J Roentgenol 2021;216:903-911
  32. Hashiba KA, Mercaldo S, Venkatesh SL, Bahl M. Prediction of surgical upstaging risk of ductal carcinoma in situ using machine learning models. J Breast Imaging 2023;5:695-702
  33. Shi B, Grimm LJ, Mazurowski MA, Baker JA, Marks JR, King LM, et al. Prediction of occult invasive disease in ductal carcinoma in situ using deep learning features. J Am Coll Radiol 2018;15(3 Pt B):527-534
  34. Hou R, Grimm LJ, Mazurowski MA, Marks JR, King LM, Maley CC, et al. Prediction of upstaging in ductal carcinoma in situ based on mammographic radiomic features. Radiology 2022;303:54-62
  35. Grimm LJ, Miller MM, Thomas SM, Liu Y, Lo JY, Hwang ES, et al. Growth dynamics of mammographic calcifications: differentiating ductal carcinoma in situ from benign breast disease. Radiology 2019;292:77-83
  36. Grimm LJ, Ghate SV, Hwang ES, Soo MS. Imaging features of patients undergoing active surveillance for ductal carcinoma in situ. Acad Radiol 2017;24:1364-1371
  37. Nguyen DL, Shelley Hwang E, Ryser MD, Grimm LJ. Imaging changes and outcomes of patients undergoing active monitoring for ductal carcinoma in situ: seven-year follow-up study. Acad Radiol 2024 Jan 5 [Epub]. https://doi.org/10.1016/j.acra.2023.12.021
  38. Hwang ES, Hyslop T, Lynch T, Frank E, Pinto D, Basila D, et al. The COMET (comparison of operative versus monitoring and endocrine therapy) trial: a phase III randomised controlled clinical trial for low-risk ductal carcinoma in situ (DCIS). BMJ Open 2019;9:e026797
  39. Francis A, Fallowfield L, Rea D. The LORIS trial: addressing overtreatment of ductal carcinoma in situ. Clin Oncol (R Coll Radiol) 2015;27:6-8
  40. Elshof LE, Tryfonidis K, Slaets L, van Leeuwen-Stok AE, Skinner VP, Dif N, et al. Feasibility of a prospective, randomised, open-label, international multicentre, phase III, non-inferiority trial to assess the safety of active surveillance for low risk ductal carcinoma in situ - the LORD study. Eur J Cancer 2015;51:1497-1510
  41. Kanbayashi C, Thompson AM, Hwang ESS, Partridge AH, Rea DW, Wesseling J, et al. The international collaboration of active surveillance trials for low-risk DCIS (LORIS, LORD, COMET, LORETTA). J Clin Oncol 2019;37:TPS603
  42. Iwata H. Single-arm confirmatory trial of endocrine therapy alone for estrogen receptor-positive, low-risk ductal carcinoma in situ of the breast (JCOG1505, LORETTA trial) [accessed on July 14, 2021]. Available at: https://upload.umin.ac.jp/cgi-open-bin/ctr_e/ctr_view.cgi?recptno=R000032260