Discrimination analysis of breast calcifications using x-ray dark-field radiography.
dark field
discriminant analysis
mammography
microcalcifications
phase-contrast x-ray imaging
Journal
Medical physics
ISSN: 2473-4209
Titre abrégé: Med Phys
Pays: United States
ID NLM: 0425746
Informations de publication
Date de publication:
Apr 2020
Apr 2020
Historique:
received:
29
07
2019
revised:
27
11
2019
accepted:
24
12
2019
pubmed:
25
1
2020
medline:
27
1
2021
entrez:
25
1
2020
Statut:
ppublish
Résumé
X-ray dark-field radiography could enhance mammography by providing more information on imaged tissue and microcalcifications. The dark field signal is a measure of small angle scattering and can thus provide additional information on the imaged materials. This information can be useful for material distinction of calcifications and the diagnosis of breast cancer by classifying benign and malign association of these calcifications. For this study, institutional review board approval was obtained. We present the evaluation of images acquired with interferometric grating-based x-ray imaging of 323 microcalcifications (166 malign and 157 benign associated) in freshly dissected breast tissue and compare the results to the information extracted in follow-up pathological evaluation. The number of imaged calcifications is sufficiently higher than in similar previous studies. Fourteen calcification properties were extracted from the digital images and used as predictors in three different models common in discrimination analysis namely a simple threshold model, a naive Bayes model and a linear regression model, which classify the calcifications as associated with a benign or suspicious finding. Three of these fourteen predictors have been newly defined in this work and are independent from the tissue background surrounding the microcalcifications. Using these predictors no background correction is needed, as in previous works in this field. The new predictors are the length of the first and second principle component of the absorption and dark-field data, as well as the angle between the first principle component and the dark-field axis. We called these predictors data length, data width, and data orientation. In fourfold cross-validation malignancy of the imaged tissue was predicted. Models that take only classical absorption predictors into account reached a sensitivity of 53.3% at a specificity of 81.1%. For a combination of predictors that also include dark field information, a sensitivity of 63.2% and specificity of 80.8% were obtained. The included dark field information consisted of the newly introduced parameters, data orientation and data width. While remaining at a similar specificity, the sensitivity, with which a trained model was able to distinguish malign from benign associated calcifications, was increased by 10% on including dark-field information. This suggests grating-based x-ray imaging as a promising clinical imaging method in the field of mammography.
Sections du résumé
BACKGROUND
BACKGROUND
X-ray dark-field radiography could enhance mammography by providing more information on imaged tissue and microcalcifications. The dark field signal is a measure of small angle scattering and can thus provide additional information on the imaged materials. This information can be useful for material distinction of calcifications and the diagnosis of breast cancer by classifying benign and malign association of these calcifications.
METHODS
METHODS
For this study, institutional review board approval was obtained. We present the evaluation of images acquired with interferometric grating-based x-ray imaging of 323 microcalcifications (166 malign and 157 benign associated) in freshly dissected breast tissue and compare the results to the information extracted in follow-up pathological evaluation. The number of imaged calcifications is sufficiently higher than in similar previous studies. Fourteen calcification properties were extracted from the digital images and used as predictors in three different models common in discrimination analysis namely a simple threshold model, a naive Bayes model and a linear regression model, which classify the calcifications as associated with a benign or suspicious finding. Three of these fourteen predictors have been newly defined in this work and are independent from the tissue background surrounding the microcalcifications. Using these predictors no background correction is needed, as in previous works in this field. The new predictors are the length of the first and second principle component of the absorption and dark-field data, as well as the angle between the first principle component and the dark-field axis. We called these predictors data length, data width, and data orientation.
RESULTS
RESULTS
In fourfold cross-validation malignancy of the imaged tissue was predicted. Models that take only classical absorption predictors into account reached a sensitivity of 53.3% at a specificity of 81.1%. For a combination of predictors that also include dark field information, a sensitivity of 63.2% and specificity of 80.8% were obtained. The included dark field information consisted of the newly introduced parameters, data orientation and data width.
CONCLUSIONS
CONCLUSIONS
While remaining at a similar specificity, the sensitivity, with which a trained model was able to distinguish malign from benign associated calcifications, was increased by 10% on including dark-field information. This suggests grating-based x-ray imaging as a promising clinical imaging method in the field of mammography.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1813-1826Subventions
Organisme : Siemens Healthineers
Organisme : Wilhelm Sander-Foundation
Informations de copyright
© 2020 The Authors. Medical Physics published by Wiley Periodicals, Inc. on behalf of American Association of Physicists in Medicine.
Références
Ward EM, DeSantis CE, Lin CC, et al. Cancer statistics: breast cancer in situ. CA Cancer J Clin. 2015;65:481-495.
DeSantis CE, Fedewa SA, Goding Sauer A, et al. Breast cancer statistics, 2015: convergence of incidence rates between black and white women. CA Cancer J Clin. 2016;66:31-42.
Nelson HD, Cantor A, Humphrey L, et al. Screening for Breast Cancer: A Systematic Review to Update the 2009. U.S. Preventive Services Task Force Recommendation, Rockville (MD): Agency for Healthcare Research and Quality (US) (Jan 2016, 2016).
Liberman L, Gougoutas CA, Zakowski MF, et al. Calcifications highly suggestive of malignancy. Am J Roentgenol. 2001;177:165-172.
Bent CK, Bassett LW, D'Orsi CJ, Sayre JW. The positive predictive value of BI-RADS microcalcification descriptors and final assessment categories. AJR Am J Roentgenol. 2010;194:1378-1383.
Atasoy MM, Tasali N, Cubuk R, et al. Vacuum-assisted stereotactic biopsy for isolated BI-RADS 4 microcalcifications: evaluation with histopathology and midterm follow-up results. Diagn Intervent Radiol. 2015;21:22-27.
Gotzsche PC, Jorgensen KJ. Screening for breast cancer with mammography. Cochrane Database Syst Rev. 2013;6:CD001877.
Myers ER, Moorman P, Gierisch JM, et al. Benefits and harms of breast cancer screening: a systematic review. JAMA. 2015;314:1615-1634.
Bluekens AMJ, Holland R, Karssemeijer N, Broeders MJM, den Heeten GJ. Comparison of digital screening mammography and screen-film mammography in the early detection of clinically relevant cancers: a multicenter study. Radiology. 2012;265:707-714.
Luiten JD, Voogd AC, Luiten EJT, Duijm LEM. Trends in incidence and tumor grade in screen-detected ductal carcinoma in situ and invasive breast cancer. Breast Cancer Res Treat. 2017;166:307-314.
Le Gal M, Chavanne G, Pellier D. Valeur diagnostique des microcalcifications groupées découvertes par mammographie. Bull Cancer. 1984;71:57-64.
Willekens I, Van de Casteele E, Buls N, et al. High-resolution 3D micro-CT imaging of breast microcalcifications: a preliminary analysis. BMC Cancer. 2014;14:9
Fitzgerald R.Phase-Sensitive X-Ray Imaging. PHYSICS TODAY, pp. 23-26 July, 2000.
Keyriläinen J. Diffraction-enhanced X-ray imaging of in vitro breast tumours PhD thesis Helsinki: University of Helsinki, Yliopistopaino (2004-10).
Bravin A, Coan P, Suortti P. X-ray phase-contrast imaging: from pre-clinical applications towards clinics. Phys Med Biol. 2013;58:R1-R35.
Wilkins SW, Nesterets YI, Gureyev TE, Mayo SC, Pogany A, Stevenson AW. On the evolution and relative merits of hard X-ray phase-contrast imaging methods. Philos Trans A Math Phys Eng Sci. 2014;372:20130021.
Snigirev A, Snigireva I, Kohn V, Kuznetsov S, Schelokov I. On the possibilities of x-ray phase contrast microimaging by coherent high-energy synchrotron radiation. Rev Sci Instrum. 1995;66:5486-5492.
Förster E, Goetz K, Zaumseil P. Double crystal diffractometry for the characterization of targets for laser fusion experiments. Kristall und Technik. 1980;15:937-945.
Davis TJ, Gureyev TE, Gao D, Stevenson AW, Wilkins SW. X-ray image contrast from a simple phase object. Phys Rev Lett. 1995;74:3173-3176.
Bonse U, Hart M. An x-ray interferometer. Appl Phys Lett. 1965;6:155-156.
Momose A. Demonstration of phase-contrast X-ray computed tomography using an X-ray interferometer. Nucl Instrum Methods Phys Res, Sect A. 1995;352:622-628.
David C, Nöhammer B, Solak HH, Ziegler E. Differential x-ray phase contrast imaging using a shearing interferometer. Appl Phys Lett. 2002;81:3287-3289.
Momose A, Kawamoto S, Koyama I, Hamaishi Y, Takai K, Suzuki Y. Demonstration of x-ray talbot interferometry. Jpn J Appl Phys. 2003;42:L866.
Weitkamp T, Diaz A, David C, et al. X-ray phase imaging with a grating interferometer. Opt Express. 2005;13:6296-6304.
Olivo A, Speller R. A coded-aperture technique allowing x-ray phase contrast imaging with conventional sources. Appl Phys Lett. 2007;91:074106.
Pfeiffer F, Weitkamp T, Bunk O, David C. Phase retrieval and differential phase-contrast imaging with low-brilliance X-ray sources. Nature Phys. 2006;2:258EP.
Keyriläinen J, Fernandez M, Fiedler S, et al. Visualisation of calcifications and thin collagen strands in human breast tumour specimens by the diffraction-enhanced imaging technique: a comparison with conventional mammography and histology. Eur J Radiol. 2008;53:226-237.
Herzen J, Donath T, Pfeiffer F, et al. Quantitative phase-contrast tomography of a liquid phantom using a conventional x-ray tube source. Opt Express. 2009;17:10010-10018.
Donath T, Pfeiffer F, Bunk O, et al. Toward clinical X-ray phase-contrast CT: demonstration of enhanced soft-tissue contrast in human specimen. Invest Radiol. 2010;45:445-452.
Stampanoni M, Wang Z, Thuring T, et al. The first analysis and clinical evaluation of native breast tissue using differential phase-contrast mammography. Invest Radiol. 2011;46:801-806.
Stutman D, Beck TJ, Carrino JA, Bingham CO. Talbot phase-contrast x-ray imaging for the small joints of the hand. Phys Med Biol. 2011;56:5697-5720.
Schleede S, Meinel FG, Bech M, et al. Emphysema diagnosis using X-ray dark-field imaging at a laser-driven compact synchrotron light source. Proc Natl Acad Sci USA. 2012;109:17880-17885.
Weber T, Bayer F, Haas W, et al.Investigation of the signature of lung tissue in X-ray grating-based phase-contrast imaging. ArXiv e-prints (December, 2012).
Tühring T, Guggenberger R, Alkadhi H. Human hand radiography using X-ray differential phase contrast combined with dark-field imaging. Skelet Radiol. 2013;42:827-835.
Yaroshenko A, Meinel FG, Bech M, et al. Pulmonary emphysema diagnosis with a preclinical small-animal X-ray dark-field scatter-contrast scanner. Radiology. 2013;269:427-433.
Nagashima M, Tanaka J, Kiyohara J, et al. Application of X-ray grating interferometry for the imaging of joint structures. Anatom Sci Int. 2014;89:95-100.
Momose A, Yashiro W, Kido K, et al. X-ray phase imaging: from synchrotron to hospital. Phil Trans. 2014;372:20130023.
Horn F, Gelse K, Jabari S, et al. High-energy x-ray Talbot-Lau radiography of a human knee. Phys Med Biol. 2017;62:6729-6745.
Horn F, Leghissa M, Kaeppler S, et al. Implementation of a Talbot-Lau interferometer in a clinical-like c-arm setup: a feasibility study. Sci Rep. 2018;8:2325.
Endrizzi M, Vittoria F, Brombal L, Longo R, Zanconati F, Olivo A. X-ray phase-contrast tomography of breast tissue specimen with a multi-aperture analyser synchrotron set-up. J Instrum. 2018;13:C02004.
Pisano ED, Johnston RE, Chapman D, et al. Human breast cancer specimens: diffraction-enhanced imaging with histologic correlation-improved conspicuity of lesion detail compared with digital radiography. Radiology. 2000;214:895-901.
Arfelli F, Assante M, Bonvicini V, et al. Low-dose phase contrast x-ray medical imaging. Phys Med Biol. 1998;43:2845-2852.
Castelli E, Tonutti M, Arfelli F, et al. Mammography with synchrotron radiation: first clinical experience with phase-detection technique. Radiology. 2011;259:684-694.
Longo R, Tonutti M, Rigon L, et al. Clinical study in phase-contrast mammography: image-quality analysis. Phil Trans R Soc A. 2014;372:20130025.
Munro PR, Ignatyev K, Speller RD, Olivo A. Phase and absorption retrieval using incoherent X-ray sources. Proc Natl Acad Sci USA. 2012;109:13922-13927.
Parham C, Zhong Z, Connor DM, Chapman LD, Pisano ED. Design and implementation of a compact low-dose diffraction enhanced medical imaging system. Acad Radiol. 2009;16:911-917.
Bech M, Jensen TH, Feidenhans'l R, Bunk O, David C, Pfeiffer F. Soft-tissue phase-contrast tomography with an x-ray tube source. Phys Med Biol. 2009;54:2747.
Koehler T, Daerr H, Martens G, et al. Slit-scanning differential x-ray phase-contrast mammography: Proof-of-concept experimental studies. Med Phys. 2015;42:1959-1965.
Gromann LB, De Marco F, Willer K, et al. In-vivo x-ray dark-field chest radiography of a pig. Sci Rep. 2017;7:4807.
Bachche S, Nonoguchi M, Kato K, et al. Laboratory- based X-ray phase-imaging scanner using Talbot-Lau interferometer for non-destructive testing. Sci Rep. 2017;7:6711.
Michel T, Rieger J, Anton G, et al. On a dark-field signal generated by micrometer-sized calcifications in phase-contrast mammography. Phys Med Biol. 2013;58:2713-2732.
Pfeiffer F, Bech M, Bunk O, et al. Hard-X-ray dark-field imaging using a grating interferometer. Nature Mater. 2008;7:134EP.
Yashiro W, Terui Y, Kawabata K, Momose A. On the origin of visibility contrast in x-ray Talbot interferometry. Opt Express. 2010;18:16890-16901.
Lynch SK, Pai V, Auxier J, et al. Interpretation of dark-field contrast and particle-size selectivity in grating interferometers. Appl Opt. 2011;50:4310-4319.
Strobl M. General solution for quantitative dark-field contrast imaging with grating interferometers. Sci Rep. 2014;4:7243.
Wang Z, Hauser N, Singer G, et al. Non-invasive classification of microcalcifications with phase-contrast X-ray mammography. Nature Commun. 2014;5:3797EP.
Scherer K, Braig E, Ehn S, et al. Improved diagnostics by assessing the micromorphology of breast calcifications via x-ray dark-field radiography. Sci Rep. 2016;6:36991EP.
Hellbach K, Baehr A, De Marco F, et al. Depiction of pneumothoraces in a large animal model using x-ray dark-field radiography. Sci Rep. 2018;8:2602.
Anton G, Bayer F, Beckmann MW, et al. Grating-based darkfield imaging of human breast tissue. Z Med Phys. 2013;23:228-235.
Hauser N, Wang Z, Kubik-Huch RA, et al. A study on mastectomy samples to evaluate breast imaging quality and potential clinical relevance of differential phase contrast mammography. Invest Radiol. 2014;49:131-137.
Morita T, Yamada M, Kano A, Nagatsuka S, Honda C, Endo T.A comparison between film-screen mammography and full-field digital mammography utilizing phase contrast technology in breast cancer screening programs. In Krupinski EA, ed. Digital Mammography. Berlin, Heidelberg: Springer; 2008:48-54.
Williams IM, Siu KKW, Gan R, et al. Towards the clinical application of X-ray phase contrast imaging. Eur J Radiol. 2008;68:S73-S77.
Gonzalez JE, Caldwell RG, Valaitis J. Calcium oxalate crystals in the breast. Pathology and significance. Am J Surg Pathol. 1991;15:586-591.
Winston JS, Yeh IT, Evers K, Friedman AK. Calcium oxalate is associated with benign breast tissue. Can we avoid biopsy? Am J Clin Pathol. 1993;100:488-492.
Frappart L, Boudeulle M, Boumendil J, et al. Structure and composition of microcalcifications in benign and malignant lesions of the breast: study by light microscopy, transmission and scanning electron microscopy, microprobe analysis, and X-ray diffraction. Hum Pathol. 1984;15:880-889.
Scimeca M, Giannini E, Antonacci C, et al. Microcalcifications in breast cancer: an active phenomenon mediated by epithelial cells with mesenchymal characteristics. BMC Cancer. 2014;14:286.
Scherer K, Birnbacher L, Willer K, Chabior M, Herzen J, Pfeiffer F. Correspondence: quantitative evaluation of X-ray dark-field images for microcalcification analysis in mammography. Nat Commun. 2016;7:10863.
Wang Z, Hauser N, Singer G, et al. Correspondence: reply to ‘quantitative evaluation of X-ray dark-field images for microcalcification analysis in mammography’. Nat. Comm. 2016;7:10868.
Roessl E, Daerr H, Koehler T, Martens G, van Stevendaal U. Clinical boundary conditions for grating-based differential phase-contrast mammography. Philos Trans A Math Phys Eng Sci. 2014;372:20130033.
Arboleda C, Wang Z, Koehler T, et al. Sensitivity-based optimization for the design of a grating interferometer for clinical X-ray phase contrast mammography. Opt Express. 2017;25:6349-6364.
Rieger J, Meyer P, Pelzer G, et al. Designing the phase grating for Talbot-Lau phase-contrast imaging systems: a simulation and experiment study. Opt. Express. 2016;24:13357-13364.
Engelhardt M, Kottler C, Bunk O, et al. The fractional Talbot effect in differential x-ray phase-contrast imaging for extended and polychromatic x-ray sources. J Microsc. 2008;232:145-157.
Rieger J, Meyer P, Horn F, et al. Optimization procedure for a Talbot-Lau x-ray phase-contrast imaging system. JINST. 2017;12:P04018.
Schulz-Wendtland R, Fuchsjager M, Wacker T, Hermann KP. Digital mammography: an update. Eur J Radiol. 2009;72:258-265.
McCormick B, Winter K, Hudis C, et al. RTOG 9804: a prospective randomized trial for good-risk ductal carcinoma in situ comparing radiotherapy with observation. J Clin Oncol. 2015;33:709-715.
Goodwin A, Parker S, Ghersi D, Wilcken N. Post-operative radiotherapy for ductal carcinoma in situ of the breast. Cochrane Database Syst Rev. 2013;11:Cd000563.