Higher underestimation of tumour size post-neoadjuvant chemotherapy with breast magnetic resonance imaging (MRI)—A concordance comparison cohort analysis

English version

Autoři: Wen-Pei Wu ^aff001; Hwa-Koon Wu ^aff001; Chih-Jung Chen ^aff003; Chih-Wie Lee ^aff001; Shou-Tung Chen ^aff006; Dar-Ren Chen ^aff006; Chen-Te Chou ^aff001; Chi Wei Mok ^aff008; Hung-Wen Lai ^aff006
Působiště autorů: Department of Diagnostic Radiology, Changhua Christian Hospital, Changhua, Taiwan ^aff001; School of Medicine, Kaohusiung Medical University, Kaohsiung, Taiwan ^aff002; Department of Pathology, Taichung Veterans General Hospital, Taichung, Taiwan ^aff003; School of Medicine, Chung Shan Medical University, Taichung, Taiwan ^aff004; Department of Medical Technology, Jen-Teh Junior College of Medicine, Nursing and Management, Miaoli, Taiwan ^aff005; Division of General Surgery, Department of Surgery, Changhua Christian Hospital, Changhua, Taiwan ^aff006; Comprehensive Breast Cancer Center, Department of Surgery, Changhua Christian Hospital, Changhua, Taiwan ^aff007; Division of Breast Surgery, Department of Surgery, Changi General Hospital, Singapore ^aff008; Endoscopic & Oncoplastic Breast Surgery Center, Department of Surgery, Changhua Christian Hospital, Changhua, Taiwan ^aff009; School of Medicine, National Yang Ming University, Taipei, Taiwan ^aff010
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222917

Souhrn

Objectives

The aim of this study was to evaluate the diagnostic accuracy of breast MRI for detecting residual tumor and the tumor size whether it would be affected after neoadjuvant chemotherapy.

Methods

Total 109 patients with NAC and 682 patients without NAC were included in this retrospective study. Measurement of the largest diameter of tumors at pathology was chosen as gold standard and compared with preoperative breast MRI. A concordance threshold of ±25% of maximal tumor size was used. The accuracy of MRI was graded as concordant, underestimation, or overestimation rate. Further subgroup analysis with tumor stages, histologic subgroups and intrinsic subtypes was performed.

Results

The post-NAC MRI was associated with 92.5% sensitivity, 55.2% specificity, 85.1% positive predictive value, 72.7% negative predictive value, and overall 82.6% accuracy for detecting residual tumor. In determining tumor size, the overall concordance rates of the non-NAC group and the NAC group were 43.5% and 41.3%, respectively (p = 0.678). But the overestimation rate and underestimation rate were 26.6% and 32.1% for NAC group, and 52.9% and 3.5% for the non-NAC group (p<0.001). While in the subgroups analysis, the concordance rate of the NAC group (26.7%) was lower than that of the non-NAC group (82.1%) at T3 stage (p<0.001). There were no statistically significant differences between different tumor histologic subgroups and intrinsic subtypes.

Conclusions

The overall accuracy of MRI in predicting tumor size was not affected by NAC; however, it tends to underestimate tumor size after NAC, especially in patients with T3 lesions and above.

Klíčová slova:

Cancer detection and diagnosis – Magnetic resonance imaging – Surgical and invasive medical procedures – Cancer chemotherapy – Carcinomas – Histology – Breast tumors – Breast cancer

Zdroje

1. Sledge GW, Mamounas EP, Hortobagyi GN, Burstein HJ, Goodwin PJ, Wolff AC. Past, present, and future challenges in breast cancer treatment. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2014;32(19):1979–86. Epub 2014/06/04. doi: 10.1200/JCO.2014.55.4139 24888802.

2. Fisher B, Brown A, Mamounas E, Wieand S, Robidoux A, Margolese RG, et al. Effect of preoperative chemotherapy on local-regional disease in women with operable breast cancer: findings from National Surgical Adjuvant Breast and Bowel Project B-18. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 1997;15(7):2483–93. Epub 1997/07/01. doi: 10.1200/JCO.1997.15.7.2483 9215816.

3. Rajan R, Poniecka A, Smith TL, Yang Y, Frye D, Pusztai L, et al. Change in tumor cellularity of breast carcinoma after neoadjuvant chemotherapy as a variable in the pathologic assessment of response. Cancer. 2004;100(7):1365–73. Epub 2004/03/26. doi: 10.1002/cncr.20134 15042669.

4. Rieber A, Brambs HJ, Gabelmann A, Heilmann V, Kreienberg R, Kuhn T. Breast MRI for monitoring response of primary breast cancer to neo-adjuvant chemotherapy. Eur Radiol. 2002;12(7):1711–9. Epub 2002/07/12. doi: 10.1007/s00330-001-1233-x 12111062.

5. Cortazar P, Zhang L, Untch M, Mehta K, Costantino JP, Wolmark N, et al. Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet. 2014;384(9938):164–72. Epub 2014/02/18. doi: 10.1016/S0140-6736(13)62422-8 24529560.

6. Prowell TM, Pazdur R. Pathological complete response and accelerated drug approval in early breast cancer. The New England journal of medicine. 2012;366(26):2438–41. Epub 2012/06/01. doi: 10.1056/NEJMp1205737 22646508.

7. Honkoop AH, van Diest PJ, de Jong JS, Linn SC, Giaccone G, Hoekman K, et al. Prognostic role of clinical, pathological and biological characteristics in patients with locally advanced breast cancer. British journal of cancer. 1998;77(4):621–6. Epub 1998/03/04. doi: 10.1038/bjc.1998.99 9484820.

8. Wang-Lopez Q, Chalabi N, Abrial C, Radosevic-Robin N, Durando X, Mouret-Reynier MA, et al. Can pathologic complete response (pCR) be used as a surrogate marker of survival after neoadjuvant therapy for breast cancer? Crit Rev Oncol Hematol. 2015;95(1):88–104. Epub 2015/04/23. doi: 10.1016/j.critrevonc.2015.02.011 25900915.

9. Park CK, Jung WH, Koo JS. Pathologic Evaluation of Breast Cancer after Neoadjuvant Therapy. J Pathol Transl Med. 2016;50(3):173–80. Epub 2016/04/14. doi: 10.4132/jptm.2016.02.02 27068026.

10. Marinovich ML, Houssami N, Macaskill P, Sardanelli F, Irwig L, Mamounas EP, et al. Meta-analysis of magnetic resonance imaging in detecting residual breast cancer after neoadjuvant therapy. Journal of the National Cancer Institute. 2013;105(5):321–33. Epub 2013/01/09. doi: 10.1093/jnci/djs528 23297042.

11. Londero V, Bazzocchi M, Del Frate C, Puglisi F, Di Loreto C, Francescutti G, et al. Locally advanced breast cancer: comparison of mammography, sonography and MR imaging in evaluation of residual disease in women receiving neoadjuvant chemotherapy. Eur Radiol. 2004;14(8):1371–9. Epub 2004/02/27. doi: 10.1007/s00330-004-2246-z 14986052.

12. Lai HW, Chen DR, Wu YC, Chen CJ, Lee CW, Kuo SJ, et al. Comparison of the Diagnostic Accuracy of Magnetic Resonance Imaging with Sonography in the Prediction of Breast Cancer Tumor Size: A Concordance Analysis with Histopathologically Determined Tumor Size. Annals of surgical oncology. 2015;22(12):3816–23. Epub 2015/02/25. doi: 10.1245/s10434-015-4424-4 25707494.

13. Gruber IV, Rueckert M, Kagan KO, Staebler A, Siegmann KC, Hartkopf A, et al. Measurement of tumour size with mammography, sonography and magnetic resonance imaging as compared to histological tumour size in primary breast cancer. BMC cancer. 2013;13:328. Epub 2013/07/06. doi: 10.1186/1471-2407-13-328 23826951.

14. Houssami N, Turner R, Morrow M. Preoperative magnetic resonance imaging in breast cancer: meta-analysis of surgical outcomes. Annals of surgery. 2013;257(2):249–55. Epub 2012/11/29. doi: 10.1097/SLA.0b013e31827a8d17 23187751.

15. Mennella S, Garlaschi A, Paparo F, Perillo M, Celenza M, Massa T, et al. Magnetic resonance imaging of breast cancer: factors affecting the accuracy of preoperative lesion sizing. Acta radiologica (Stockholm, Sweden: 1987). 2015;56(3):260–8. Epub 2014/02/15. doi: 10.1177/0284185114524089 24526754.

16. Chan SE, Liao CY, Wang TY, Chen ST, Chen DR, Lin YJ, et al. The diagnostic utility of preoperative breast magnetic resonance imaging (MRI) and/or intraoperative sub-nipple biopsy in nipple-sparing mastectomy. Eur J Surg Oncol. 2017;43(1):76–84. Epub 2016/09/07. doi: 10.1016/j.ejso.2016.08.005 27591937.

17. 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. European journal of radiology. 2016;85(4):780–9. Epub 2016/03/15. doi: 10.1016/j.ejrad.2015.12.027 26971424.

18. Lai HW, Chen CJ, Lin YJ, Chen SL, Wu HK, Wu YT, et al. Does Breast Magnetic Resonance Imaging Combined With Conventional Imaging Modalities Decrease the Rates of Surgical Margin Involvement and Reoperation?: A Case-Control Comparative Analysis. Medicine (Baltimore). 2016;95(22):e3810. Epub 2016/06/04. doi: 10.1097/MD.0000000000003810 27258520.

19. Bouzon A, Acea B, Soler R, Iglesias A, Santiago P, Mosquera J, et al. Diagnostic accuracy of MRI to evaluate tumour response and residual tumour size after neoadjuvant chemotherapy in breast cancer patients. Radiol Oncol. 2016;50(1):73–9. Epub 2016/04/14. doi: 10.1515/raon-2016-0007 27069452.

20. Rosen EL, Blackwell KL, Baker JA, Soo MS, Bentley RC, Yu D, et al. Accuracy of MRI in the detection of residual breast cancer after neoadjuvant chemotherapy. AJR American journal of roentgenology. 2003;181(5):1275–82. Epub 2003/10/24. doi: 10.2214/ajr.181.5.1811275 14573420.

21. Moon HG, Han W, Lee JW, Ko E, Kim EK, Yu JH, et al. Age and HER2 expression status affect MRI accuracy in predicting residual tumor extent after neo-adjuvant systemic treatment. Ann Oncol. 2009;20(4):636–41. Epub 2009/01/31. doi: 10.1093/annonc/mdn683 19179551.

22. Straver ME, Loo CE, Rutgers EJ, Oldenburg HS, Wesseling J, Vrancken Peeters MJ, et al. MRI-model to guide the surgical treatment in breast cancer patients after neoadjuvant chemotherapy. Annals of surgery. 2010;251(4):701–7. Epub 2010/03/13. doi: 10.1097/SLA.0b013e3181c5dda3 20224378.

23. Williams M, Eatrides J, Kim J, Talwar H, Esposito N, Szabunio M, et al. Comparison of breast magnetic resonance imaging clinical tumor size with pathologic tumor size in patients status post-neoadjuvant chemotherapy. American journal of surgery. 2013;206(4):567–73. Epub 2013/07/03. doi: 10.1016/j.amjsurg.2013.02.006 23809673.

24. Zhang Z, Zhang W, Jin Y, Wang H, Gu F, Zhou J, et al. Evaluating the response of neoadjuvant chemotherapy for treatment of breast cancer: are tumor biomarkers and dynamic contrast enhanced MR images useful predictive tools? Journal of thoracic disease. 2014;6(6):785–94. Epub 2014/07/01. doi: 10.3978/j.issn.2072-1439.2014.04.28 24977004.

25. Ko ES, Han H, Han BK, Kim SM, Kim RB, Lee GW, et al. Prognostic Significance of a Complete Response on Breast MRI in Patients Who Received Neoadjuvant Chemotherapy According to the Molecular Subtype. Korean journal of radiology. 2015;16(5):986–95. Epub 2015/09/12. doi: 10.3348/kjr.2015.16.5.986 26357493.

26. Knopp MV, Weiss E, Sinn HP, Mattern J, Junkermann H, Radeleff J, et al. Pathophysiologic basis of contrast enhancement in breast tumors. J Magn Reson Imaging. 1999;10(3):260–6. Epub 1999/10/03. doi: 10.1002/(sici)1522-2586(199909)10:3<260::aid-jmri6>3.0.co;2-7 10508285.

27. Pham CD, Roberts TP, van Bruggen N, Melnyk O, Mann J, Ferrara N, et al. Magnetic resonance imaging detects suppression of tumor vascular permeability after administration of antibody to vascular endothelial growth factor. Cancer Invest. 1998;16(4):225–30. Epub 1998/05/20. doi: 10.3109/07357909809039771 9589031.

28. Kuo WH, Chen CN, Hsieh FJ, Shyu MK, Chang LY, Lee PH, et al. Vascularity change and tumor response to neoadjuvant chemotherapy for advanced breast cancer. Ultrasound in medicine & biology. 2008;34(6):857–66. Epub 2008/04/01. doi: 10.1016/j.ultrasmedbio.2007.11.011 18374468.

29. Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thurlimann B, Senn HJ, et al. Strategies for subtypes—dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol. 2011;22(8):1736–47. Epub 2011/06/29. doi: 10.1093/annonc/mdr304 21709140.

30. Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M, Thurlimann B, et al. Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann Oncol. 2013;24(9):2206–23. Epub 2013/08/07. doi: 10.1093/annonc/mdt303 23917950.

31. Provenzano E, Bossuyt V, Viale G, Cameron D, Badve S, Denkert C, et al. Standardization of pathologic evaluation and reporting of postneoadjuvant specimens in clinical trials of breast cancer: recommendations from an international working group. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc. 2015;28(9):1185–201. Epub 2015/07/25. doi: 10.1038/modpathol.2015.74 26205180.

32. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). European journal of cancer (Oxford, England: 1990). 2009;45(2):228–47. Epub 2008/12/23. doi: 10.1016/j.ejca.2008.10.026 19097774.

33. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1986;1(8476):307–10. Epub 1986/02/08. 2868172.

34. Nakamura S, Ishiyama M, Tsunoda-Shimizu H. Magnetic resonance mammography has limited ability to estimate pathological complete remission after primary chemotherapy or radiofrequency ablation therapy. Breast cancer (Tokyo, Japan). 2007;14(2):123–30. Epub 2007/05/09. 17485896.

35. Boileau JF, Poirier B, Basik M, Holloway CM, Gaboury L, Sideris L, et al. Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2015;33(3):258–64. Epub 2014/12/03. doi: 10.1200/JCO.2014.55.7827 25452445.

36. Fu JF, Chen HL, Yang J, Yi CH, Zheng S. Feasibility and accuracy of sentinel lymph node biopsy in clinically node-positive breast cancer after neoadjuvant chemotherapy: a meta-analysis. PloS one. 2014;9(9):e105316. Epub 2014/09/12. doi: 10.1371/journal.pone.0105316 25210779.

37. Warren RM, Bobrow LG, Earl HM, Britton PD, Gopalan D, Purushotham AD, et al. Can breast MRI help in the management of women with breast cancer treated by neoadjuvant chemotherapy? British journal of cancer. 2004;90(7):1349–60. Epub 2004/04/01. doi: 10.1038/sj.bjc.6601710 15054453.

38. Rauch GM, Adrada BE, Kuerer HM, van la Parra RF, Leung JW, Yang WT. Multimodality Imaging for Evaluating Response to Neoadjuvant Chemotherapy in Breast Cancer. AJR American journal of roentgenology. 2017;208(2):290–9. Epub 2016/11/05. doi: 10.2214/AJR.16.17223 27809573.

39. Schrading S, Kuhl CK. Breast Cancer: Influence of Taxanes on Response Assessment with Dynamic Contrast-enhanced MR Imaging. Radiology. 2015;277(3):687–96. Epub 2015/07/16. doi: 10.1148/radiol.2015150006 26176656.