Reducing false positives of microcalcification detection systems by removal of breast arterial calcifications

Medical Physics

Volumn 43, Issue 4, 2016, Pages 1676-1687

  Mordang, Jan Jurre ^a   Gubern Mérida, Albert ^a   Den Heeten, Gerard ^b,c   Karssemeijer, Nico ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b National Expert and Training Centre for Breast Cancer Screening   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

breast arterial calcifications; breast cancer screening; computer aided detection; mammography; microcalcifications

Indexed keywords

BIOMINERALIZATION; BONE; CALCIFICATION (BIOCHEMISTRY); COMPUTER AIDED DIAGNOSIS; DISEASES;

BREAST ARTERIAL CALCIFICATION; BREAST CANCER SCREENING; COMPUTER AIDED DETECTION; COMPUTER AIDED DETECTION SYSTEMS; DETECTION RATES; DETECTION SYSTEM; FALSE POSITIVE; MICRO-CALCIFICATION[MC]; MICROCALCIFICATION DETECTION; PERFORMANCE;

MAMMOGRAPHY;

ALGORITHM; ARTERY CALCIFICATION; ARTICLE; BOOTSTRAPPING; BREAST ARTERIAL CALCIFICATION; BREAST CALCIFICATION; BREAST CANCER; COMPUTER ASSISTED DIAGNOSIS; DIAGNOSTIC TEST; FALSE POSITIVE RESULT; HUMAN; MAJOR CLINICAL STUDY; MALIGNANT BREAST MICROCALCIFICATION; MICROCALCIFICATION DETECTION SYSTEM; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; ARTERY; BREAST; CALCINOSIS; DIAGNOSTIC IMAGING; MAMMOGRAPHY; METABOLISM; PROCEDURES; VASCULARIZATION;

ARTERIES; BREAST; CALCINOSIS; FALSE POSITIVE REACTIONS; HUMANS; MAMMOGRAPHY; RADIOGRAPHIC IMAGE INTERPRETATION, COMPUTER-ASSISTED; ROC CURVE;

EID: 84961653081     PISSN: 00942405     EISSN: 24734209     Source Type: Journal    
DOI: 10.1118/1.4943376     Document Type: Article

References (73)

1. J. Ferlay, H. R. Shin, F. Bray, D. Forman, C. Mathers, and D. M. Parkin, "Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008," Int. J. Cancer 127, 2893-2917 (2010). 10.1002/ijc.25516
2. J. Ferlay, E. Steliarova-Foucher, J. Lortet-Tieulent, S. Rosso, J. W. W. Coebergh, H. Comber, D. Forman, and F. Bray, "Cancer incidence and mortality patterns in Europe: Estimates for 40 countries in 2012," Eur. J. Cancer 49, 1374-1403 (2013). 10.1016/j.ejca.2012.12.027
3. L. Tabár, C. J. Fagerberg, A. Gad, L. Baldetorp, L. H. Holmberg, O. Gröntoft, U. Ljungquist, B. Lundström, J. C. Månson, and G. Eklund, "Reduction in mortality from breast cancer after mass screening with mammography. Randomised trial from the breast cancer screening working group of the Swedish national board of health and welfare," Lancet 1, 829-832 (1985). 10.1016/S0140-6736(85)92204-4
4. L. Tabár, B. Vitak, T. H.-H. Chen, A. M.-F. Yen, A. Cohen, T. Tot, S. Y.-H. Chiu, S. L.-S. Chen, J. C.-Y. Fann, J. Rosell, H. Fohlin, R. A. Smith, and S. W. Duffy, "Swedish two-county trial: Impact of mammographic screening on breast cancer mortality during 3 decades," Radiology 260, 658-663 (2011). 10.1148/radiol.11110469
5. S. Hofvind, B. F. Iversen, L. Eriksen, B. M. Styr, K. Kjellevold, and K. D. Kurz, "Mammographic morphology and distribution of calcifications in ductal carcinoma in situ diagnosed in organized screening," Anticancer Res. 52, 481-487 (2011). 10.1258/ar.2011.100357
6. R. F. Cox, A. Hernandez-Santana, S. Ramdass, G. McMahon, J. H. Harmey, and M. P. Morgan, "Microcalcifications in breast cancer: Novel insights into the molecular mechanism and functional consequence of mammary mineralisation," Br. J. Cancer 106, 525-537 (2012). 10.1038/bjc.2011.583
7. E. A. Sickles, "Mammographic features of 300 consecutive nonpalpable breast cancers," Am. J. Roentgenol. 146, 661-663 (1986). 10.2214/ajr.146.4.661
8. C. J. D'Orsi, L. W. Bassett, W. A. Berg, S. A. Feig, V. P. Jackson, and D. B. Kopans, Breast Imaging Reporting and Data System (BI-RADS) Atlas, 4th ed. (American College of Radiology, Reston, VA, 2003).
9. R. L. Birdwell, "The preponderance of evidence supports computer-aided detection for screening mammography," Radiology 253, 9-16 (2009). 10.1148/radiol.2531090611
10. M. Elter and A. Horsch, "CADx of mammographic masses and clustered microcalcifications: A review," Med. Phys. 36, 2052-2068 (2009). 10.1118/1.3121511
11. J. Tang, R. M. Rangayyan, J. Xu, I. E. Naqa, and Y. Yang, "Computer-aided detection and diagnosis of breast cancer with mammography: Recent advances," IEEE Trans. Inf. Technol. Biomed. 13, 236-251 (2009). 10.1109/TITB.2008.2009441
12. I. Domingues and J. Cardoso, "Using Bayesian surprise to detect calcifications in mammogram images," in Conference Proceedings of the IEEE Engineering in Medicine and Biology Society (IEEE, Piscataway, NJ, 2014), pp. 1091-1094. 10.1109/EMBC.2014.6943784
13. G. H. B. Miranda and J. C. Felipe, "Computer-aided diagnosis system based on fuzzy logic for breast cancer categorization," Comput. Biol. Med. 64, 334-346 (2015). 10.1016/j.compbiomed.2014.10.006
14. H. Mohamed, M. S. Mabrouk, and A. Sharawy, "Computer aided detection system for micro-calcifications in digital mammograms," Comput. Methods Programs Biomed. 116, 226-235 (2014). 10.1016/j.cmpb.2014.04.010
15. G. Apostolopoulos, A. Koutras, I. Christoyianni, and E. Dermatas, "Computer aided classification of mammographic tissue using shapelets and support vector machines," in Artificial Intelligence: Methods and Applications, Lecture Notes in Computer Science (Springer-Verlag, Berlin, Germany, 2014), pp. 510-520.
16. D. C. Pereira, R. P. Ramos, and M. Z. do Nascimento, "Segmentation and detection of breast cancer in mammograms combining wavelet analysis and genetic algorithm," Comput. Methods Programs Biomed. 114, 88-101 (2014). 10.1016/j.cmpb.2014.01.014
17. N. Karssemeijer, A. M. Bluekens, D. Beijerinck, J. J. Deurenberg, M. Beekman, R. Visser, R. van Engen, A. Bartels-Kortland, and M. J. Broeders, "Breast cancer screening results 5 years after introduction of digital mammography in a population-based screening program," Radiology 253, 353-358 (2009). 10.1148/radiol.2532090225
18. E. B. Cole, Z. Zhang, H. S. Marques, R. M. Nishikawa, R. E. Hendrick, M. J. Yaffe, W. Padungchaichote, C. Kuzmiak, J. Chayakulkheeree, E. F. Conant, L. L. Fajardo, J. Baum, C. Gatsonis, and E. Pisano, "Assessing the stand-alone sensitivity of computer-aided detection with cancer cases from the digital mammographic imaging screening trial," Am. J. Roentgenol. 199, W392-W401 (2012). 10.2214/AJR.11.7255
19. R. M. Nishikawa, "Current status and future directions of computer-aided diagnosis in mammography," Comput. Med. Imaging Graphics 31, 224-235 (2007). 10.1016/j.compmedimag.2007.02.009
20. L. H. Eadie, P. Taylor, and A. P. Gibson, "A systematic review of computer-assisted diagnosis in diagnostic cancer imaging," Eur. J. Radiol. 81, e70-e76 (2012). 10.1016/j.ejrad.2011.01.098
21. T. E. Cupples, J. E. Cunningham, and J. C. Reynolds, "Impact of computer-aided detection in a regional screening mammography program," Am. J. Roentgenol. 185, 944-950 (2005). 10.2214/AJR.04.1300
22. J. J. Fenton, S. H. Taplin, P. A. Carney, L. Abraham, E. A. Sickles, C. D'Orsi, E. A. Berns, G. Cutter, R. E. Hendrick, W. E. Barlow, and J. G. Elmore, "Influence of computer-aided detection on performance of screening mammography," N. Engl. J. Med. 356, 1399-1409 (2007). 10.1056/NEJMoa066099
23. P. Taylor and H. W. W. Potts, "Computer aids and human second reading as interventions in screening mammography: Two systematic reviews to compare effects on cancer detection and recall rate," Eur. J. Cancer 44, 798-807 (2008). 10.1016/j.ejca.2008.02.016
24. X. Bargalló, G. Santamaría, M. Del Amo, P. Arguis, J. Ríos, J. Grau, M. Burrel, E. Cores, and M. Velasco, "Single reading with computer-aided detection performed by selected radiologists in a breast cancer screening program," Eur. J. Radiol. 83, 2019-2023 (2014). 10.1016/j.ejrad.2014.08.010
25. R. M. Nishikawa and D. Gur, "Cade for early detection of breast cancer-current status and why we need to continue to explore new approaches," Acad. Radiol. 21, 1320-1321 (2014). 10.1016/j.acra.2014.05.018
26. P. A. van Luijt, J. Fracheboud, E. A. M. Heijnsdijk, G. J. den Heeten, H. J. de Koning, and National Evaluation Team for Breast Cancer Screening in the Netherlands Study Group (NETB), "Nation-wide data on screening performance during the transition to digital mammography: Observations in 6 million screens," Eur. J. Cancer 49, 3517-3525 (2013). 10.1016/j.ejca.2013.06.020
27. R. Smith-Bindman, P. W. Chu, D. L. Miglioretti, E. A. Sickles, R. Blanks, R. Ballard-Barbash, J. K. Bobo, N. C. Lee, M. G. Wallis, J. Patnick, and K. Kerlikowske, "Comparison of screening mammography in the United States and the United Kingdom," J. Am. Med. Assoc. 290, 2129-2137 (2003). 10.1001/jama.290.16.2129
28. J.-J. Mordang, J. Hauth, G. den Heeten, and N. Karssemeijer, "Automated labeling of screening mammograms with arterial calcifications," in Breast Imaging, edited by H. Fujita, T. Hara, and C. Muramatsu, Lecture Notes in Computer Science Vol. 8539 (Springer-Verlag, Berlin, Germany, 2014). 10.1007/978-3-319-07887-8˙82
29. J.-J. Mordang and N. Karssemeijer, "Vessel segmentation in screening mammograms," Proc. SPIE 9414, 94140J (2015). 10.1117/12.2081804
30. J. Shi, B. Sahiner, H.-P. Chan, J. Ge, L. Hadjiiski, M. A. Helvie, A. Nees, Y.-T. Wu, J. Wei, C. Zhou, Y. Zhang, and J. Cui, "Characterization of mammographic masses based on level set segmentation with new image features and patient information," Med. Phys. 35, 280-290 (2008). 10.1118/1.2820630
31. I. El-Naqa, Y. Yang, M. N. Wernick, N. P. Galatsanos, and R. M. Nishikawa, "A support vector machine approach for detection of microcalcifications," IEEE Trans. Med. Imaging 21, 1552-1563 (2002). 10.1109/TMI.2002.806569
32. H. Jing, Y. Yang, and R. Nishikawa, "Detection of clustered microcalcifications using spatial point process modeling," Phys. Med. Biol. 56, 1-17 (2011). 10.1088/0031-9155/56/1/001
33. Y. Jiang, R. M. Nishikawa, D. E. Wolverton, C. E. Metz, M. L. Giger, R. A. Schmidt, C. J. Vyborny, and K. Doi, "Malignant and benign clustered microcalcifications: Automated feature analysis and classification," Radiology 198, 671-678 (1996). 10.1148/radiology.198.3.8628853
34. J. Wei, B. Sahiner, L. M. Hadjiiski, H.-P. Chan, N. Petrick, M. A. Helvie, M. A. Roubidoux, J. Ge, and C. Zhou, "Computer-aided detection of breast masses on full field digital mammograms," Med. Phys. 32, 2827-2838 (2005). 10.1118/1.1997327
35. A. Bria, N. Karssemeijer, and F. Tortorella, "Learning from unbalanced data: A cascade-based approach for detecting clustered microcalcifications," Med. Image Anal. 18, 241-252 (2013). 10.1016/j.media.2013.10.014
36. K. J. McLoughlin, P. J. Bones, and N. Karssemeijer, "Noise equalization for detection of microcalcification clusters in direct digital mammogram images," IEEE Trans. Med. Imaging 23, 313-320 (2004). 10.1109/TMI.2004.824240
37. G. van Schie and N. Karssemeijer, "Detection of microcalcifications using a nonuniform noise model," in IWDM '08: Proceedings of the 9th International Workshop on Digital Mammography (Springer-Verlag, Berlin, Germany, 2008), pp. 378-384.
38. P. Viola and M. Jones, "Rapid object detection using a boosted cascade of simple features," in Proceedings of IEEE Conference on Computer Vision and Pattern Recognition (IEEE, Piscataway, NJ, 2001), Vol. 1, pp. I-511-I-518. 10.1109/CVPR.2001.990517
39. A. Torralba, K. Murphy, and W. Freeman, "Sharing visual features for multiclass and multiview object detection," IEEE Trans. Pattern Anal. Mach. Intell. 29, 854-869 (2007). 10.1109/TPAMI.2007.1055
40. C. Papageorgiou, M. Oren, and T. Poggio, "A general framework for object detection," in Sixth International Conference on Computer Vision (IEEE, Piscataway, NJ, 1998), pp. 555-562. 10.1109/ICCV.1998.710772
41. R. Lienhart and J. Maydt, "An extended set of Haar-like features for rapid object detection," in Proceedings of International Conference on Image Processing (IEEE, Piscataway, NJ, 2002), Vol. 1, pp. I-900-I-903. 10.1109/ICIP.2002.1038171
42. W. J. H. Veldkamp and N. Karssemeijer, "Improved method for detection of microcalcification clusters in digital mammograms," Proc. SPIE 3661, 512-522 (1999). 10.1117/12.348607
43. P. A. van Noord, D. Beijerinck, J. M. Kemmeren, and Y. van der Graaf, "Mammograms may convey more than breast cancer risk: Breast arterial calcification and arterio-sclerotic related diseases in women of the DOM cohort," Eur. J. Cancer Prev. 5, 483-487 (1996).
44. J. M. Kemmeren, P. A. van Noord, D. Beijerinck, J. Fracheboud, J. D. Banga, and Y. van der Graaf, "Arterial calcification found on breast cancer screening mammograms and cardiovascular mortality in women: The DOM project. doorlopend onderzoek morbiditeit en mortaliteit," Am. J. Epidemiol. 147, 333-341 (1998). 10.1093/oxfordjournals.aje.a009455
45. J. Reddy, H. Son, S. J. Smith, F. Paultre, and L. Mosca, "Prevalence of breast arterial calcifications in an ethnically diverse population of women," Ann. Epidemiol. 15, 344-350 (2005). 10.1016/j.annepidem.2004.11.006
46. J. Sklansky, "Finding the convex hull of a simple polygon," Pattern Recognit. Lett. 1, 79-83 (1982). 10.1016/0167-8655(82)90016-2
47. R. Diestel, Graph Theory, 4th ed., Graduate Texts in Mathematics Vol. 173 (Springer-Verlag, Heidelberg, 2007).
48. T. Koller, G. Gerig, G. Szekely, and D. Dettwiler, "Multiscale detection of curvilinear structures in 2-D and 3-D image data," in Proceedings of the IEEE Fifth International Conference on Computer Vision-ICCV 1995 (IEEE, Piscataway, NJ, 1995), pp. 864-869.
49. Q. Li, S. Sone, and K. Doi, "Selective enhancement filters for nodules, vessels, and airway walls in two- and three-dimensional CT scans," Med. Phys. 30, 2040-2051 (2003). 10.1118/1.1581411
50. B. Efron and R. J. Tibshirani, An Introduction to the Bootstrap (CRC, Boca Raton, FL, 1994), Vol. 57.
51. H. Bornefalk and A. B. Hermansson, "On the comparison of FROC curves in mammography CAD systems," Med. Phys. 32, 412-417 (2005). 10.1118/1.1844433
52. F. Samuelson and N. Petrick, "Comparing image detection algorithms using resampling," in IEEE International Symposium on Biomedical Imaging (IEEE, Piscataway, NJ, 2006), pp. 1312-1315. 10.1109/ISBI.2006.1625167
53. J. Ge, H.-P. Chan, B. Sahiner, C. Zhou, M. A. Helvie, J. Wei, L. M. Hadjiiski, Y. Zhang, Y.-T. Wu, and J. Shi, "Automated detection of breast vascular calcification on full-field digital mammograms," Proc. SPIE 6915, 691517 (2008). 10.1117/12.773096
54. J.-Z. Cheng, E. B. Cole, E. D. Pisano, and D. Shen, "Detection of arterial calcification in mammograms by random walks," in Information Processing in Medical Imaging (Springer-Verlag, Berlin, Germany, 2009), Vol. 21, pp. 713-724.
55. J.-Z. Cheng, C.-M. Chen, E. Cole, E. Pisano, and D. Shen, "Automated delineation of calcified vessels in mammography by tracking with uncertainty and graphical linking techniques," IEEE Trans. Med. Imaging 31, 2143-2155 (2012). 10.1109/TMI.2012.2215880
56. A. H. E. M. Maas, Y. T. van der Schouw, D. Beijerinck, J. J. M. Deurenberg, W. P. T. M. Mali, and Y. van der Graaf, "Arterial calcifications seen on mammograms: Cardiovascular risk factors, pregnancy, and lactation," Radiology 240, 33-38 (2006). 10.1148/radiol.2401050170
57. A. H. E. M. Maas, Y. T. van der Schouw, F. Atsma, D. Beijerinck, J. J. M. Deurenberg, W. P. T. M. Mali, and Y. van der Graaf, "Breast arterial calcifications are correlated with subsequent development of coronary artery calcifications, but their aetiology is predominantly different," Eur. J. Radiol. 63, 396-400 (2007). 10.1016/j.ejrad.2007.02.009
58. A. H. E. M. Maas, Y. T. van der Schouw, W. P. T. M. Mali, and Y. van der Graaf, "Prevalence and determinants of breast arterial calcium in women at high risk of cardiovascular disease," Am. J. Cardiol. 94, 655-659 (2004). 10.1016/j.amjcard.2004.05.036
59. E. J. E. Hendriks, P. A. de Jong, Y. van der Graaf, W. P. T. M. Mali, Y. T. van der Schouw, and J. W. J. Beulens, "Breast arterial calcifications: A systematic review and meta-analysis of their determinants and their association with cardiovascular events," Atherosclerosis 239, 11-20 (2015). 10.1016/j.atherosclerosis.2014.12.035
60. P. F. Schnatz, K. A. Marakovits, and D. M. O'Sullivan, "The association of breast arterial calcification and coronary heart disease," Obstet. Gynecol. 117, 233-241 (2011). 10.1097/AOG.0b013e318206c8cb
61. M. Kataoka, R. Warren, R. Luben, J. Camus, E. Denton, E. Sala, N. Day, and K.-T. Khaw, "How predictive is breast arterial calcification of cardiovascular disease and risk factors when found at screening mammography?," Am. J. Roentgenol. 187, 73-80 (2006). 10.2214/AJR.05.0365
62. U. Topal, A. Kaderli, N. B. Topal, B. Ozdemir, D. Yeilbursa, J. Cordan, B. Ediz, and A. Aydinlar, "Relationship between the arterial calcification detected in mammography and coronary artery disease," Eur. J. Radiol. 63, 391-395 (2007). 10.1016/j.ejrad.2007.01.035
63. P. S. Dale, M. Richards, and G. C. Mackie, "Vascular calcifications on screening mammography identify women with increased risk of coronary artery disease and diabetes," Am. J. Surg. 196, 537-540 (2008). 10.1016/j.amjsurg.2008.06.012
64. M. A. Rotter, P. F. Schnatz, A. A. Currier, Jr., and D. M. O'Sullivan, "Breast arterial calcifications (BACs) found on screening mammography and their association with cardiovascular disease," Menopause 15, 276-281 (2008). 10.1097/gme.0b013e3181405d0a
65. K. J. Ahn, Y. J. Kim, H. J. Cho, H. W. Yim, B. J. Kang, S. H. Kim, H. S. Kim, K. T. Kim, J. H. Lee, and I. Y. Whang, "Correlation between breast arterial calcification detected on mammography and cerebral artery disease," Arch. Gynecol. Obstet. 284, 957-964 (2011). 10.1007/s00404-010-1742-4
66. M. J. Bae, S. Y. Lee, Y. J. Kim, J. G. Lee, D. W. Jeong, Y. H. Yi, Y. H. Cho, E. J. Choi, and K. S. Choo, "Association of breast arterial calcifications, metabolic syndrome, and the 10-year coronary heart disease risk: A cross-sectional case-control study," J. Women's Health 22, 625-630 (2013). 10.1089/jwh.2012.4148
67. N. Shah, V. Chainani, P. Delafontaine, A. Abdo, J. Lafferty, and N. Abi Rafeh, "Mammographically detectable breast arterial calcification and atherosclerosis," Cardiol. Rev. 22, 69-78 (2014). 10.1097/CRD.0b013e318295e029
68. M. Cetin, R. Cetin, N. Tamer, and S. Kelekçi, "Breast arterial calcifications associated with diabetes and hypertension," J. Diabetes Complications 18, 363-366 (2004). 10.1016/j.jdiacomp.2004.04.004
69. M. Cetin, R. Cetin, and N. Tamer, "Prevalence of breast arterial calcification in hypertensive patients," Clin. Radiol. 59, 92-95 (2004). 10.1016/j.crad.2003.09.007
70. J. Reddy, J. P. Bilezikian, S. J. Smith, and L. Mosca, "Reduced bone mineral density is associated with breast arterial calcification," J. Clin. Endocrinol. Metab. 93, 208-211 (2008). 10.1210/jc.2007-0693
71. V. Duhn, E. T. D'Orsi, S. Johnson, C. J. D'Orsi, A. L. Adams, and W. C. O'Neill, "Breast arterial calcification: A marker of medial vascular calcification in chronic kidney disease," Clin. J. Am. Soc. Nephrol. 6, 377-382 (2011). 10.2215/CJN.07190810
72. A. N. Zafar, S. Khan, and S. N. Zafar, "Factors associated with breast arterial calcification on mammography," J. Coll. Phys. Surg. Pak. 23, 178-181 (2013). 03.2013/JCPSP.178181
73. H. Wada, M. Kitada, K. Sato, T. Sasajima, N. Miyokawa, and T. Kuroda, "Prevalence of breast arterial calcification by mammography contributes to breast cancer," Breast Cancer 19, 266-269 (2012). 10.1007/s12282-011-0281-6