Abbreviated Breast MRI as a Supplement to Mammography in Family Risk History of Breast Cancer within the Croatian National Breast Screening Program
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Population
2.2. Imaging Techniques and Findings
2.3. Pathology
2.4. Statistical Methods
3. Results
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Bray, F.; Laversanne, M.; Sung, H.; Ferlay, J.; Siegel, R.L.; Soerjomataram, I.; Jemal, A. Global Cancer Statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2024, 74, 229–263. [Google Scholar] [CrossRef] [PubMed]
- Jemal, A.; Center, M.M.; De Santis, C.; Ward, E.M. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol. Biomark. Prev. 2010, 19, 1893–1907. [Google Scholar] [CrossRef] [PubMed]
- Lynch, H.T.; Silva, E.; Snyder, C.; Lynch, J.F. Hereditary breast cancer: Part I. Diagnosing hereditary breast cancer syndromes. Breast J. 2008, 14, 3–13. [Google Scholar] [CrossRef] [PubMed]
- Brewer, H.R.; Jones, M.E.; Schoemaker, M.J.; Ashworth, A.; Swerdlow, A.J. Family history and risk of breast cancer: An analysis ac-counting for family structure. Breast Cancer Res. Treat. 2017, 165, 193–200. [Google Scholar] [CrossRef]
- Jiang, Y.; Weinberg, C.R.; Sandler, D.P.; Zhao, S. Use of detailed family history data to improve risk prediction, with application to breast cancer screening. PLoS ONE 2019, 14, e0226407. [Google Scholar] [CrossRef]
- Dibden, A.; Offman, J.; Duffy, S.W.; Gabe, R. Worldwide review and meta-analysis of cohort studies measuring the effect of mammography screening programmes on incidence-based breast cancer mortality. Cancers 2020, 12, 976. [Google Scholar] [CrossRef]
- Mann, R.M.; Kuhl, C.K.; Kinkel, K.; Boetes, C. Breast MRI: Guidelines from the European Society of Breast Imaging. Eur. Radiol. 2008, 18, 1307–1318. [Google Scholar] [CrossRef]
- Monticciolo, D.L.; Newell, M.S.; Moy, L.; Lee, C.S.; Destounis, S.V. Breast cancer screening for women at higher-than-average risk: Updated recommendations from the ACR. J. Am. Coll. Radiol. 2023, 20, 902–914. [Google Scholar] [CrossRef]
- Lord, S.J.; Lei, W.; Craft, P.; Cawson, J.N.; Morris, I.; Walleser, S.; Griffiths, A.; Parker, S.; Houssami, N. A systematic review of the effectiveness of magnetic resonance imaging (MRI) as an addition to mammography and ultra-sound in screening young women at high risk of breast cancer. Eur. J. Cancer 2007, 43, 1905–1917. [Google Scholar] [CrossRef]
- Kriege, M.; Brekelmans, C.T.M.; Boetes, C.; Besnard, P.E.; Zonderland, H.M.; Obdeijn, I.M.; Manoliu, R.A.; Kok, T.; Peterse, H.; Tilanus-Linthorst, M.M.A.; et al. Efficacy of MRI and mammography for breast-cancer screening in women with a familial or genetic predisposition. N. Engl. J. Med. 2004, 351, 427–437. [Google Scholar] [CrossRef]
- Kuhl, C.K.; Schrading, S.; Leutner, C.C.; Morakkabati-Spitz, N.; Wardelmann, E.; Fimmers, R.; Huhn, W.; Schild, H.H. Mammography, breast ultrasound, and magnetic resonance imaging for surveillance of women at high familial risk for breast cancer. J. Clin. Oncol. 2005, 23, 8469–8476. [Google Scholar] [CrossRef] [PubMed]
- Leach, M.O.; Boggis, C.R.; Dixon, A.K.; Easton, D.F.; Eeles, R.A.; Evans, D.G.; Gilbert, F.J.; Griebsch, I.; Hoff, R.J.C.; Kessar, P. Screening with magnetic resonance imaging and mammography of a UK population at high familial risk of breast cancer: A prospective multicentre cohort study (MARIBS). Lancet 2005, 365, 1769–1778. [Google Scholar] [CrossRef] [PubMed]
- Lehman, C.D. Role of MRI in screening women at high risk for breast cancer. J. Magn. Reason. Imaging 2006, 24, 964–970. [Google Scholar] [CrossRef] [PubMed]
- Sardanelli, F.; Podo, F.; D’Agnolo, G.; Verdecchia, A.; Santaquilani, M.; Musumci, R.; Trecate, G.; Manoukian, S.; Morassut, S.; de Giacomi, C.; et al. Multicenter comparative multimodality surveillance of women at genetic-familial high risk for breast cancer (HIBCRIT study): Interim results. Radiology 2007, 242, 698–715. [Google Scholar] [CrossRef] [PubMed]
- Lo, G.; Scaranelo, A.M.; Aboras, H.; Ghai, S.; Kulkarni, S.; Fleming, R.; Bukhanov, K.; Crysta, P. Evaluation of the utility of screening mammography for high-risk women undergoing screening breast MR imaging. Radiology 2017, 285, 36–43. [Google Scholar] [CrossRef] [PubMed]
- Chiarelli, A.M.; Blackmore, K.M.; Muradali, D.; Done, S.J.; Majpruz, V.; Weerasinghe, A.; Mirea, L.; Eisen, A.; Rabeneck, L.; Warner, E. Performance measures of magnetic resonance imaging plus mammography in the high risk Ontario breast screening program. J. Natl. Cancer Inst. 2020, 112, 136–144. [Google Scholar] [CrossRef]
- Warner, E.; Messersmith, H.; Causer, P.; Eisen, A.; Shumak, R.; Plewes, D. Systematic review: Using magnetic resonance imaging to screen women at high risk for breast cancer. Ann. Intern. Med. 2008, 148, 671–679. [Google Scholar] [CrossRef] [PubMed]
- Bick, U.; Engel, C.; Krug, B.; Heindel, W.; Fallenberg, E.M.; Rhiem, K.; Maintz, D.; Golatta, M.; Speiser, D.; Rjosk-Dendorfer, D. High-risk breast cancer surveillance with MRI: 10-year experience from the German consortium for hereditary breast and ovarian cancer. Breast Cancer Res. Treat. 2019, 175, 217–228. [Google Scholar] [CrossRef]
- Sippo, D.A.; Burk, K.S.; Mercaldo, S.F.; Rutledge, G.M.; Edmonds, C.; Guan, Z.; Hughes, K.S.; Lehman, C.D. Performance of screening breast MRI across women with different elevated breast cancer risk indications. Radiology 2019, 292, 51–59. [Google Scholar] [CrossRef]
- Phi, X.A.; Houssami, N.; Hooning, M.J.; Riedl, C.C.; Leach, M.O.; Sardanelli, F.; Warner, E.; Trop, I.; Saadatmand, S.; Tilanus-Linthorst, M.M.A. Accuracy of screening women at familial risk of breast cancer without a known gene mutation: Individual patient data meta-analysis. Eur. J. Cancer 2017, 85, 31–38. [Google Scholar] [CrossRef]
- National Institute for Health and Care Excellence. Familial Breast Cancer: Classification, Care and Managing Breast Cancer and Related Risks in People with a Family History of Breast Cancer. In Clinical Guideline (CG164) [Internet]; National Institute for Health and Care Excellence: London, UK, 2013; Available online: https://www.nice.org.uk/guidance/cg164 (accessed on 20 December 2023).
- D’Orsi, C.J.; Mendelson, E.B.; Ikeda, D.M. Breast Imaging Reporting and Data System: ACR BI-RADS-Breast Imaging Atlas; American College of Radiology: Reston, VA, USA, 2003. [Google Scholar]
- Saslow, D.; Boetes, C.; Burke, W.; Harms, S.; Leach, M.O.; Lehman, C.D.; Morris, E.; Pisano, E.; Schnall, M.; Sener, S.; et al. American Cancer Society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J. Clin. 2007, 57, 75–89. [Google Scholar] [CrossRef] [PubMed]
- Kuhl, C.K.; Schrading, S.; Strobel, K.; Schild, H.H.; Hilgers, R.D.; Bieling, H.B. Abbreviated breast magnetic resonance imaging (MRI): First postcontrast subtracted images and maximum-intensity projection—A novel approach to breast cancer screening with MRI. J. Clin. Oncol. 2014, 32, 2304–2310. [Google Scholar] [CrossRef] [PubMed]
- Grimm, L.J.; Conant, E.F.; Dialani, V.M.; Dontchos, B.N.; Harvey, J.A.; Kacharia, V.S.; Plecha, D.M.; Mango, V.L. Abbreviated breast MRI utilization: A Survey of the Society of Breast Imaging. J. Breast Imaging 2022, 4, 506–512. [Google Scholar] [CrossRef] [PubMed]
- Lawson, M.B.; Partridge, S.C.; Hippe, D.S.; Rahbar, H.; Lam, D.L.; Lee, C.I.; Lowry, K.P.; Scheel, J.R.; Parsian, S.; Li, I. Comparative performance of contrast-enhanced mammography, abbreviated breast MRI, and standard breast MRI for breast cancer screening. Radiology 2023, 308, e230576. [Google Scholar] [CrossRef] [PubMed]
- Baxter, G.C.; Selamoglu, A.; Mackay, J.W.; Bond, S.; Gray, E.; Gilbert, F.J. A meta-analysis comparing the diagnostic performance of abbreviated MRI and a full diagnostic protocol in breast cancer. Clin. Radiol. 2021, 76, 154.e23–154.e32. [Google Scholar] [CrossRef]
- Vassiou, K.; Kanavou, T.; Vlychou, M.; Poultsidi, A.; Athanasiou, E.; Arvanitis, D.L.; Fezoulidis, I.V. Characterization of breast lesions with CE-MR multimodal morphological and kinetic analysis: Comparison with conventional mammography and high-resolution ultrasound. Eur. J. Radiol. 2009, 70, 69–76. [Google Scholar] [CrossRef]
- Orel, S.G.; Schnall, M.D. MR imaging of the breast for the detection, diagnosis, and staging of breast cancer. Radiology 2001, 220, 13–30. [Google Scholar] [CrossRef]
- Tozaki, M.; Igarashi, T.; Fukuda, K. Positive and negative predictive values of BI-RADS-MRI descriptors for focal breast masses. Magn. Reason. Med. Sci. 2006, 5, 7–15. [Google Scholar] [CrossRef]
- Peters, N.H.G.M.; Rinkes, I.H.M.B.; Zuithoff, N.P.A.; Mali, W.P.T.M.; Moons, K.G.M.; Peeters, P.H.M. Meta-analysis of MR imaging in the diagnosis of breast lesions. Radiology 2008, 246, 116–124. [Google Scholar] [CrossRef]
- Benndorf, M.; Baltzer, P.A.; Vag, T.; Gajda, M.; Runnebaum, I.B.; Kaiser, W.A. Breast MRI as an adjunct to mammography: Does it really suffer from low specificity? A retrospective analysis stratified by mammographic BI-RADS classes. Acta Radiol. 2010, 51, 715–721. [Google Scholar] [CrossRef]
- Nunes, L.W.; Schnall, M.D.; Orel, S.G. Update of breast MR imaging architectural interpretation model. Radiology 2001, 219, 484–494. [Google Scholar] [CrossRef] [PubMed]
- Sardanelli, F.; Magni, V.; Rossini, G.; Kilburn-Toppin, F.; Healy, N.; Gilbert, F.J. The paradox of MRI for breast cancer screening: High-risk and dense breasts-available evidence and current practice. Insights Imaging 2024, 15, 96. [Google Scholar] [CrossRef] [PubMed]
- Warner, E.; Hill, K.; Causer, P.; Plewes, D.; Jong, R.; Yaffe, M.; Foulkes, W.D.; Ghadirian, P.; Lynch, H.; Couch, F. Prospective study of breast cancer incidence in women with a BRCA1 or BRCA2 mutation under surveillance with and without magnetic resonance imaging. J. Clin. Oncol. 2011, 29, 1664–1669. [Google Scholar] [CrossRef] [PubMed]
- Sung, J.S.; Stamler, S.; Brooks, J.; Kaplan, J.; Huang, T.; Dershaw, D.D.; Lee, C.H.; Morris, E.A.; Comstock, C.E. Breast Cancers Detected at Screening MR Imaging and Mammography in Patients at High Risk: Method of Detection Reflects Tumor Histopathologic Results. Radiology 2016, 280, 716–722. [Google Scholar] [CrossRef] [PubMed]
- Jacobi, C.E.; de Bock, G.H.; Siegerink, B.; van Asperen, C.J. Differences and similarities in breast cancer risk assessment models in clinical practice: Which model to choose? Breast Cancer Res. Treat. 2009, 115, 381–390. [Google Scholar] [CrossRef]
- Tollens, F.; Baltzer, P.A.T.; Froelich, M.F.; Kaiser, C.G. Economic evaluation of breast MRI in screening—A systematic review and basic approach to cost-effectiveness analyses. Front. Oncol. 2023, 13, 1292268. [Google Scholar] [CrossRef]
- Tollens, F.; Baltzer, P.A.T.; Dietzel, M.; Rübenthaler, J.; Froelich, M.F.; Kaiser, C.G. Cost-effectiveness of digital breast tomosynthesis vs. abbreviated breast MRI for screening women with intermediate risk of breast cancer-how low-cost must MRI be? Cancers 2021, 13, 1241. [Google Scholar] [CrossRef]
N | % | 95% CI | |||
---|---|---|---|---|---|
Mammography BI-RADS | 0 | 19 | 10.7% | 6.8% | 15.8% |
1 | 2 | 1.1% | 0.2% | 3.6% | |
2 | 140 | 78.7% | 72.2% | 84.2% | |
3 | 6 | 3.4% | 1.4% | 6.8% | |
4 | 9 | 5.1% | 2.5% | 9.0% | |
5 | 2 | 1.1% | 0.2% | 3.6% | |
ABMRI BI-RADS | 0 | 3 | 1.7% | 0.5% | 4.4% |
1 | 2 | 1.1% | 0.2% | 3.6% | |
2 | 124 | 69.7% | 62.6% | 76.1% | |
3 | 29 | 16.3% | 11.4% | 22.2% | |
4 | 14 | 7.9% | 4.6% | 12.5% | |
5 | 6 | 3.4% | 1.4% | 6.8% | |
Biopsy | Without biopsy | 161 | 90.4% | 85.5% | 94.1% |
B2 | 5 | 2.8% | 1.1% | 6.0% | |
B5a | 3 | 1.7% | 0.5% | 4.4% | |
B5b | 9 | 5.1% | 2.5% | 9.0% | |
Biopsy * | Invasive cancer | 9 | 52.9% | 30.3% | 74.6% |
DCIS | 3 | 17.6% | 5.2% | 40.0% | |
Negative | 5 | 29.4% | 12.2% | 53.0% | |
Mammography BI-RADS | Others | 167 | 93.8% | 89.6% | 96.7% |
Suspicious (BI-RADS 4/5) | 11 | 6.2% | 3.3% | 10.4% | |
ABMRI BI-RADS | Others | 158 | 88.8% | 83.5% | 92.8% |
Suspicious (BI-RADS 4/5) | 20 | 11.2% | 7.2% | 16.5% |
Breast Cancer | p | |||||
---|---|---|---|---|---|---|
No | Yes | |||||
N | % | N | % | |||
Mammography + ABMRI | Non-suspicious mammography and non-suspicious ABMRI | 153 | 92.2% | 0 | 0.0% | <0.001 |
Suspicious mammography and non-suspicious ABMRI | 4 | 2.4% | 1 | 8.3% | ||
Non-suspicious mammography and suspicious ABMRI | 7 | 4.2% | 7 | 58.3% | ||
Suspicious mammography and suspicious ABMRI | 2 | 1.2% | 4 | 33.3% |
Value | 95% CI | |
---|---|---|
Sensitivity | 41.67% | 15.165–72.333% |
Specificity | 96.39% | 92.299–98.662% |
AUC | 0.69 | 0.617–0.757 |
Positive odds ratio | 11.528 | 4.107–32.359 |
Negative odds ratio | 0.605 | 0.375–0.977 |
PPV | 45.46% | 22.891–70.053% |
NPV | 95.81% | 93.402–97.362% |
Accuracy | 92.70% | 87.835–96.054% |
Value | 95% CI | |
---|---|---|
Sensitivity | 91.67% | 61.520–99.789% |
Specificity | 94.58% | 89.958–97.491% |
AUC | 0.931 | 0.884–0.964 |
Positive odds ratio | 16.907 | 8.757–32.643 |
Negative odds ratio | 0.088 | 0.013–0.576 |
PPV | 55.00% | 38.765–70.236% |
NPV | 99.37% | 96.005–99.903% |
Accuracy | 94.38% | 89.911–97.273% |
Value | 95% CI | |
---|---|---|
Sensitivity | 100.00% | 73.535–100.000% |
Specificity | 92.17% | 86.981–95.764% |
AUC | 0.961 | 0.921–0.984 |
Positive odds ratio | 12.769 | 7.577–21.519 |
Negative odds ratio | 0 | |
PPV | 48.00% | 35.390–60.870% |
NPV | 100.00% | 97.618–100.000% |
Accuracy | 92.70% | 87.835–96.054% |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Šupe Parun, A.; Brkljačić, B.; Ivanac, G.; Tešić, V. Abbreviated Breast MRI as a Supplement to Mammography in Family Risk History of Breast Cancer within the Croatian National Breast Screening Program. Biomedicines 2024, 12, 2357. https://doi.org/10.3390/biomedicines12102357
Šupe Parun A, Brkljačić B, Ivanac G, Tešić V. Abbreviated Breast MRI as a Supplement to Mammography in Family Risk History of Breast Cancer within the Croatian National Breast Screening Program. Biomedicines. 2024; 12(10):2357. https://doi.org/10.3390/biomedicines12102357
Chicago/Turabian StyleŠupe Parun, Andrea, Boris Brkljačić, Gordana Ivanac, and Vanja Tešić. 2024. "Abbreviated Breast MRI as a Supplement to Mammography in Family Risk History of Breast Cancer within the Croatian National Breast Screening Program" Biomedicines 12, no. 10: 2357. https://doi.org/10.3390/biomedicines12102357
APA StyleŠupe Parun, A., Brkljačić, B., Ivanac, G., & Tešić, V. (2024). Abbreviated Breast MRI as a Supplement to Mammography in Family Risk History of Breast Cancer within the Croatian National Breast Screening Program. Biomedicines, 12(10), 2357. https://doi.org/10.3390/biomedicines12102357