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Performance characteristics of specimen radiography for margin assessment for ductal carcinoma in situ: a systematic review

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Abstract

Background

Reducing positive margin rate (PMR) and reoperation rate in breast-conserving operations remains a challenge, mainly regarding ductal carcinoma in situ (DCIS). Intra-operative margin assessment tools have emerged to reduce PMR over the last decades, including specimen radiography (SR). No consensus has been reached on the reliability and efficacy of SR in DCIS.

Objective

We performed a systematic literature review to assess the performance characteristics of SR for margin assessment of breast lesions with pure DCIS and invasive cancers with DCIS components.

Methods

A literature search was conducted for diagnostic studies up to April 2017 concerning SR for intra-operative margin assessment of breast lesions with pure DCIS or with DCIS components. Studies reporting sensitivity and specificity calculated using final pathology report as reference test were included. Due to improved imaging technology, studies published more than 15 years ago were excluded. Methodological quality was assessed using quality assessment of diagnostic accuracy studies-2 checklist. Due to clinical and methodological diversity, meta-analysis was considered not useful.

Results

Of 235 citations identified, 9 met predefined inclusion criteria and documented diagnostic efficacy data. Sensitivity ranged from 22 to 77% and specificity ranged from 51 to 100%. Positive predictive value and negative predictive value ranged from 53 to 100% and 32 to 95%, respectively. High or unclear risk of bias was found in reference standard in 5 of 9 studies. High concerns regarding applicability of index test were found in 6 of 9 studies.

Conclusions

The present results do not support the routine use of intra-operative specimen radiography to reduce the rate of positive margins in patients undergoing breast-conserving surgery for pure DCIS or the DCIS component in invasive cancer. Future studies need to differentiate between initial and final specimen margin involvement. This could provide surgeons with a number needed to treat for a more applicable outcome.

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References

  1. Fisher B, Anderson S, Bryant J, Margolese RG, Deutsch M, Fisher ER, Jeong JH, Wolmark N (2002) Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med 347(16):1233–1241

    Article  PubMed  Google Scholar 

  2. Arriagada R, Le MG, Rochard F, Contesso G (1996) Conservative treatment versus mastectomy in early breast cancer: patterns of failure with 15 years of follow-up data. Institut Gustave-Roussy Breast Cancer Group. J Clin Oncol 14(5):1558–1564

    Article  CAS  PubMed  Google Scholar 

  3. Jacobson JA, Danforth DN, Cowan KH, d’Angelo T, Steinberg SM, Pierce L, Lippman ME, Lichter AS, Glatstein E, Okunieff P (1995) Ten-year results of a comparison of conservation with mastectomy in the treatment of stage I and II breast cancer. N Engl J Med 332(14):907–911

    Article  CAS  PubMed  Google Scholar 

  4. Veronesi U, Cascinelli N, Mariani L, Greco M, Saccozzi R, Luini A, Aguilar M, Marubini E (2002) Twenty-year follow-up of a randomized study comparing breast-conserving surgery with radical mastectomy for early breast cancer. N Engl J Med 347(16):1227–1232

    Article  PubMed  Google Scholar 

  5. van Maaren MC, de Munck L, Jobsen JJ, Poortmans P, de Bock GH, Siesling S, Strobbe LJ (2016) Breast-conserving therapy versus mastectomy in T1-2N2 stage breast cancer: a population-based study on 10-year overall, relative, and distant metastasis-free survival in 3071 patients. Breast Cancer Res Treat 160(3):511–521

    Article  PubMed  Google Scholar 

  6. Houssami N, Macaskill P, Marinovich ML, Morrow M (2014) The association of surgical margins and local recurrence in women with early-stage invasive breast cancer treated with breast-conserving therapy: a meta-analysis. Ann Surg Oncol 21(3):717–730

    Article  PubMed  Google Scholar 

  7. Clarke M, Collins R, Darby S, Davies C, Elphinstone P, Evans V, Godwin J, Gray R, Hicks C, James S, MacKinnon E, McGale P, McHugh T, Peto R, Taylor C, Wang Y (2005) Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials. Lancet 366(9503):2087–2106

    Article  CAS  PubMed  Google Scholar 

  8. Jeevan R, Cromwell DA, Trivella M, Lawrence G, Kearins O, Pereira J, Sheppard C, Caddy CM, van der Meulen JH (2012) Reoperation rates after breast conserving surgery for breast cancer among women in England: retrospective study of hospital episode statistics. BMJ 345:e4505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Landercasper J, Whitacre E, Degnim AC, Al-Hamadani M (2014) Reasons for re-excision after lumpectomy for breast cancer: insight from the American Society of Breast Surgeons Mastery(SM) database. Ann Surg Oncol 21(10):3185–3191

    Article  PubMed  Google Scholar 

  10. Kurniawan ED, Wong MH, Windle I, Rose A, Mou A, Buchanan M, Collins JP, Miller JA, Gruen RL, Mann GB (2008) Predictors of surgical margin status in breast-conserving surgery within a breast screening program. Ann Surg Oncol 15(9):2542–2549

    Article  PubMed  Google Scholar 

  11. Bani MR, Lux MP, Heusinger K, Wenkel E, Magener A, Schulz-Wendtland R, Beckmann MW, Fasching PA (2009) Factors correlating with reexcision after breast-conserving therapy. Eur J Surg Oncol 35(1):32–37

    Article  CAS  PubMed  Google Scholar 

  12. Bathla L, Harris A, Davey M, Sharma P, Silva E (2011) High resolution intra-operative two-dimensional specimen mammography and its impact on second operation for re-excision of positive margins at final pathology after breast conservation surgery. Am J Surg 202(4):387–394

    Article  PubMed  Google Scholar 

  13. McCormick JT, Keleher AJ, Tikhomirov VB, Budway RJ, Caushaj PF (2004) Analysis of the use of specimen mammography in breast conservation therapy. Am J Surg 188(4):433–436

    Article  PubMed  Google Scholar 

  14. St John ER, Al-Khudairi R, Ashrafian H, Athanasiou T, Takats Z, Hadjiminas DJ, Darzi A, Leff DR (2017) Diagnostic accuracy of intraoperative techniques for margin assessment in breast cancer surgery: a meta-analysis. Ann Surg 265(2):300–310

    Article  PubMed  Google Scholar 

  15. Holland R, Hendriks JH, Vebeek AL, Mravunac M, Schuurmans Stekhoven JH (1990) Extent, distribution, and mammographic/histological correlations of breast ductal carcinoma in situ. Lancet 335(8688):519–522

    Article  CAS  PubMed  Google Scholar 

  16. Schmachtenberg C, Engelken F, Fischer T, Bick U, Poellinger A, Fallenberg EM (2012) Intraoperative specimen radiography in patients with nonpalpable malignant breast lesions. Rofo 184(7):635–642

    Article  CAS  PubMed  Google Scholar 

  17. Thomas J, Evans A, Macartney J, Pinder SE, Hanby A, Ellis I, Kearins O, Roberts T, Clements K, Lawrence G, Bishop H (2010) Radiological and pathological size estimations of pure ductal carcinoma in situ of the breast, specimen handling and the influence on the success of breast conservation surgery: a review of 2564 cases from the Sloane Project. Br J Cancer 102(2):285–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lange M, Reimer T, Hartmann S, Glass A, Stachs A (2016) The role of specimen radiography in breast-conserving therapy of ductal carcinoma in situ. Breast 26:73–79

    Article  CAS  PubMed  Google Scholar 

  19. Dillon MF, Mc Dermott EW, O’Doherty A, Quinn CM, Hill AD, O’Higgins N (2007) Factors affecting successful breast conservation for ductal carcinoma in situ. Ann Surg Oncol 14(5):1618–1628

    Article  PubMed  Google Scholar 

  20. Hisada T, Sawaki M, Ishiguro J, Adachi Y, Kotani H, Yoshimura A, Hattori M, Yatabe Y, Iwata H (2016) Impact of intraoperative specimen mammography on margins in breast-conserving surgery. Mol Clin Oncol 5(3):269–272

    Article  PubMed  PubMed Central  Google Scholar 

  21. Leung BST, Wan AYH, Au AKY, Lo SSW, Wong WWC, Khoo JLS (2015) Can intraoperative specimen radiograph predict resection margin status for radioguided occult lesion localisation lumpectomy for ductal carcinoma in situ presenting with microcalcifications? Hong Kong J. Radiol. 18(1):11–21

    Article  Google Scholar 

  22. Moher D, Liberati A, Tetzlaff J, Altman DG (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8(5):336–341

    Article  PubMed  Google Scholar 

  23. Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155(8):529–536

    Article  PubMed  Google Scholar 

  24. Weber WP, Engelberger S, Viehl CT, Zanetti-Dallenbach R, Kuster S, Dirnhofer S, Wruk D, Oertli D, Marti WR (2008) Accuracy of frozen section analysis versus specimen radiography during breast-conserving surgery for nonpalpable lesions. World J Surg 32(12):2599–2606

    Article  PubMed  Google Scholar 

  25. Rua C, Lebas P, Michenet P, Ouldamer L (2012) Evaluation of lumpectomy surgical specimen radiographs in subclinical, in situ and invasive breast cancer, and factors predicting positive margins. Diagn Interv Imaging 93(11):871–877

    Article  CAS  PubMed  Google Scholar 

  26. Jaafar H (2006) Intra-operative frozen section consultation: concepts, applications and limitations. Malays J Med Sci 13(1):4–12

    PubMed  PubMed Central  Google Scholar 

  27. Keating JJ, Fisher C, Batiste R, Singhal S (2016) Advances in intraoperative margin assessment for breast cancer. Curr Surg Rep 4:15

    Article  Google Scholar 

  28. Butler-Henderson K, Lee AH, Price RI, Waring K (2014) Intraoperative assessment of margins in breast conserving therapy: a systematic review. Breast 23(2):112–119

    Article  PubMed  Google Scholar 

  29. Britton PD, Sonoda LI, Yamamoto AK, Koo B, Soh E, Goud A (2011) Breast surgical specimen radiographs: how reliable are they? Eur J Radiol 79(2):245–249

    Article  CAS  PubMed  Google Scholar 

  30. Goldfeder S, Davis D, Cullinan J (2006) Breast specimen radiography: can it predict margin status of excised breast carcinoma? Acad Radiol 13(12):1453–1459

    Article  PubMed  Google Scholar 

  31. Aziz D, Rawlinson E, Narod SA, Sun P, Lickley HL, McCready DR, Holloway CM (2006) The role of reexcision for positive margins in optimizing local disease control after breast-conserving surgery for cancer. Breast J 12(4):331–337

    Article  PubMed  Google Scholar 

  32. Miller AR, Brandao G, Prihoda TJ, Hill C, Cruz AB Jr, Yeh IT (2004) Positive margins following surgical resection of breast carcinoma: analysis of pathologic correlates. J Surg Oncol 86(3):134–140

    Article  PubMed  Google Scholar 

  33. Mai KT, Chaudhuri M, Perkins DG, Mirsky D (2001) Resection margin status in lumpectomy specimens for duct carcinoma of the breast: correlation with core biopsy and mammographic findings. J Surg Oncol 78(3):189–193

    Article  CAS  PubMed  Google Scholar 

  34. Laws A, Brar MS, Bouchard-Fortier A, Leong B, Quan ML (2016) Intraoperative margin assessment in wire-localized breast-conserving surgery for invasive cancer: a population-level comparison of techniques. Ann Surg Oncol 23(10):3290–3296

    Article  PubMed  Google Scholar 

  35. van der Velden APS, Boetes C, Bult P, Wobbes T (2006) The value of magnetic resonance imaging in diagnosis and size assessment of in situ and small invasive breast carcinoma. Am J Surg 192(2):172–178

    Article  Google Scholar 

  36. Santamaria G, Velasco M, Farrus B, Zanon G, Fernandez PL (2008) Preoperative MRI of pure intraductal breast carcinoma–a valuable adjunct to mammography in assessing cancer extent. Breast 17(2):186–194

    Article  PubMed  Google Scholar 

  37. Kuhl CK, Schrading S, Bieling HB, Wardelmann E, Leutner CC, Koenig R, Kuhn W, Schild HH (2007) MRI for diagnosis of pure ductal carcinoma in situ: a prospective observational study. Lancet 370(9586):485–492

    Article  PubMed  Google Scholar 

  38. Daniel OK, Lim S, Kim J, Park HS, Park S, Kim SI (2017) Preoperative prediction of the size of pure ductal carcinoma in situ using three imaging modalities as compared to histopathological size: does magnetic resonance imaging add value? Breast Cancer Res Treat 164(2):437–444

    Article  PubMed  Google Scholar 

  39. Kuhl CK, Strobel K, Bieling H, Wardelmann E, Kuhn W, Maass N, Schrading S (2017) Impact of preoperative breast MR imaging and MR-guided surgery on diagnosis and surgical outcome of women with invasive breast cancer with and without DCIS component. Radiology. doi:10.1148/radiol.2017161449

    Google Scholar 

  40. Proulx F, Correa JA, Ferré R, Omeroglu A, Aldis A, Meterissian S, Mesurolle B (1058) Value of pre-operative breast MRI for the size assessment of ductal carcinoma in situ. Br J Radiol 2016(89):20150543

    Google Scholar 

  41. Fancellu A, Turner RM, Dixon JM, Pinna A, Cottu P, Houssami N (2015) Meta-analysis of the effect of preoperative breast MRI on the surgical management of ductal carcinoma in situ. Br J Surg 102(8):883–893

    Article  CAS  PubMed  Google Scholar 

  42. Turnbull L, Brown S, Harvey I, Olivier C, Drew P, Napp V, Hanby A, Brown J (2010) Comparative effectiveness of MRI in breast cancer (COMICE) trial: a randomised controlled trial. Lancet 375(9714):563–571

    Article  PubMed  Google Scholar 

  43. Peters NH, van Esser S, van den Bosch MA, Storm RK, Plaisier PW, van Dalen T, Diepstraten SC, Weits T, Westenend PJ, Stapper G, Fernandez-Gallardo MA, Borel Rinkes IH, van Hillegersberg R, Mali WP, Peeters PH (2011) Preoperative MRI and surgical management in patients with nonpalpable breast cancer: the MONET—randomised controlled trial. Eur J Cancer 47(6):879–886

    Article  CAS  PubMed  Google Scholar 

  44. Pengel KE, Loo CE, Teertstra HJ, Muller SH, Wesseling J, Peterse JL, Bartelink H, Rutgers EJ, Gilhuijs KG (2009) The impact of preoperative MRI on breast-conserving surgery of invasive cancer: a comparative cohort study. Breast Cancer Res Treat 116(1):161–169

    Article  CAS  PubMed  Google Scholar 

  45. Houssami N, Turner R, Morrow M (2013) Preoperative magnetic resonance imaging in breast cancer: meta-analysis of surgical outcomes. Ann Surg 257(2):249–255

    Article  PubMed  Google Scholar 

  46. Fouche CJ, Tabareau F, Michenet P, Lebas P, Simon EG (2011) Specimen radiography assessment of surgical margins status in subclinical breast carcinoma: a diagnostic study. J Gynecol Obstet Biol Reprod (Paris) 40(4):314–322

    Article  Google Scholar 

  47. Mazouni C, Rouzier R, Balleyguier C, Sideris L, Rochard F, Delaloge S, Marsiglia H, Mathieu MC, Spielman M, Garbay JR (2006) Specimen radiography as predictor of resection margin status in non-palpable breast lesions. Clin Radiol 61(9):789–796

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank the following for their contribution in this paper: Ton de Haan and Joanna in‘t Hout for their help and statistical advice and On Ying Chan for her help in conducting a search term.

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Authors and Affiliations

  1. Department of Surgery, Canisius Wilhelmina Hospital, Weg door Jonkerbos 100, 6532 SB, Nijmegen, The Netherlands

    D. P. A. Versteegden, L. G. G. Keizer, M. S. Schlooz-Vries & L. J. A. Strobbe

  2. Department of Radiology, Canisius Wilhelmina Hospital, Weg Door Jonkerbos 100, 6532 SB, Nijmegen, The Netherlands

    L. E. M. Duijm

  3. Department of Pathology, Canisius Wilhelmina Hospital, Weg door Jonkerbos 100, 6532 SB, Nijmegen, The Netherlands

    C. A. P. Wauters

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  1. D. P. A. Versteegden
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Correspondence to D. P. A. Versteegden.

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Versteegden, D.P.A., Keizer, L.G.G., Schlooz-Vries, M.S. et al. Performance characteristics of specimen radiography for margin assessment for ductal carcinoma in situ: a systematic review. Breast Cancer Res Treat 166, 669–679 (2017). https://doi.org/10.1007/s10549-017-4475-2

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