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Published in: Breast Cancer Research 1/2016

Open Access 01-12-2016 | Research article

Mammographic texture and risk of breast cancer by tumor type and estrogen receptor status

Authors: Serghei Malkov, John A. Shepherd, Christopher G. Scott, Rulla M. Tamimi, Lin Ma, Kimberly A. Bertrand, Fergus Couch, Matthew R. Jensen, Amir P. Mahmoudzadeh, Bo Fan, Aaron Norman, Kathleen R. Brandt, V. Shane Pankratz, Celine M. Vachon, Karla Kerlikowske

Published in: Breast Cancer Research | Issue 1/2016

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Abstract

Background

Several studies have shown that mammographic texture features are associated with breast cancer risk independent of the contribution of breast density. Thus, texture features may provide novel information for risk stratification. We examined the association of a set of established texture features with breast cancer risk by tumor type and estrogen receptor (ER) status, accounting for breast density.

Methods

This study combines five case–control studies including 1171 breast cancer cases and 1659 controls matched for age, date of mammogram, and study. Mammographic breast density and 46 breast texture features, including first- and second-order features, Fourier transform, and fractal dimension analysis, were evaluated from digitized film-screen mammograms. Logistic regression models evaluated each normalized feature with breast cancer after adjustment for age, body mass index, first-degree family history, percent density, and study.

Results

Of the mammographic features analyzed, fractal dimension and second-order statistics features were significantly associated (p < 0.05) with breast cancer. Fractal dimensions for the thresholds equal to 10% and 15% (FD_TH_10 and FD_TH_15) were associated with an increased risk of breast cancer while thresholds from 60% to 85% (FD_TH_60 to FD_TH_85) were associated with a decreased risk. Increasing the FD_TH_75 and Energy feature values were associated with a decreased risk of breast cancer while increasing Entropy was associated with a increased risk of breast cancer. For example, 1 standard deviation increase of FD_TH_75 was associated with a 13% reduced risk of breast cancer (odds ratio = 0.87, 95% confidence interval 0.79–0.95). Overall, the direction of associations between features and ductal carcinoma in situ (DCIS) and invasive cancer, and estrogen receptor positive and negative cancer were similar.

Conclusion

Mammographic features derived from film-screen mammograms are associated with breast cancer risk independent of percent mammographic density. Some texture features also demonstrated associations for specific tumor types. For future work, we plan to assess risk prediction combining mammographic density and features assessed on digital images.
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Literature
1.
go back to reference Tice JA, Cummings SR, Smith-Bindman R, Ichikawa L, Barlow WE, Kerlikowske K. Using clinical factors and mammographic breast density to estimate breast cancer risk: development and validation of a new predictive model. Ann Intern Med. 2008;148(5):337–47.CrossRefPubMedPubMedCentral Tice JA, Cummings SR, Smith-Bindman R, Ichikawa L, Barlow WE, Kerlikowske K. Using clinical factors and mammographic breast density to estimate breast cancer risk: development and validation of a new predictive model. Ann Intern Med. 2008;148(5):337–47.CrossRefPubMedPubMedCentral
2.
go back to reference Boyd NF, Guo H, Martin LJ, Sun L, Stone J, Fishell E, Jong RA, Hislop G, Chiarelli A, Minkin S, et al. Mammographic density and the risk and detection of breast cancer. N Engl J Med. 2007;356(3):227–36.CrossRefPubMed Boyd NF, Guo H, Martin LJ, Sun L, Stone J, Fishell E, Jong RA, Hislop G, Chiarelli A, Minkin S, et al. Mammographic density and the risk and detection of breast cancer. N Engl J Med. 2007;356(3):227–36.CrossRefPubMed
3.
go back to reference Wolfe JN. Risk for breast cancer development determined by mammographic parenchymal pattern. Cancer. 1976;37:2486–92.CrossRefPubMed Wolfe JN. Risk for breast cancer development determined by mammographic parenchymal pattern. Cancer. 1976;37:2486–92.CrossRefPubMed
4.
go back to reference ACR. Illustrated breast imaging reporting and data system (BI-RADS). 5th ed. Reston, VA: American College of Radiology; 2003. ACR. Illustrated breast imaging reporting and data system (BI-RADS). 5th ed. Reston, VA: American College of Radiology; 2003.
5.
go back to reference Wang J, Azziz A, Fan B, Malkov S, Klifa C, Newitt D, Yitta S, Hylton N, Kerlikowske K, Shepherd JA. Agreement of mammographic measures of volumetric breast density to MRI. PLoS One. 2013;8(12), e81653.CrossRefPubMedPubMedCentral Wang J, Azziz A, Fan B, Malkov S, Klifa C, Newitt D, Yitta S, Hylton N, Kerlikowske K, Shepherd JA. Agreement of mammographic measures of volumetric breast density to MRI. PLoS One. 2013;8(12), e81653.CrossRefPubMedPubMedCentral
6.
go back to reference Torres-Mejia G, De Stavola B, Allen DS, Perez-Gavilan JJ, Ferreira JM, Fentiman IS, Dos Santos SI. Mammographic features and subsequent risk of breast cancer: a comparison of qualitative and quantitative evaluations in the Guernsey prospective studies. Cancer Epidemiol Biomarkers Prev. 2005;14(5):1052–9.CrossRefPubMed Torres-Mejia G, De Stavola B, Allen DS, Perez-Gavilan JJ, Ferreira JM, Fentiman IS, Dos Santos SI. Mammographic features and subsequent risk of breast cancer: a comparison of qualitative and quantitative evaluations in the Guernsey prospective studies. Cancer Epidemiol Biomarkers Prev. 2005;14(5):1052–9.CrossRefPubMed
7.
go back to reference Byng JW, Yaffe M, Lockwood GA, Little LE, Tritchler DL, Boyd NF. Automated analysis of mammographic densities and breast carcinoma risk. Cancer. 1997;80(1):66–74.CrossRefPubMed Byng JW, Yaffe M, Lockwood GA, Little LE, Tritchler DL, Boyd NF. Automated analysis of mammographic densities and breast carcinoma risk. Cancer. 1997;80(1):66–74.CrossRefPubMed
8.
go back to reference Manduca A, Carston MJ, Heine JJ, Scott CG, Pankratz VS, Brandt KR, Sellers TA, Vachon CM, Cerhan JR. Texture features from mammographic images and risk of breast cancer. Cancer Epidemiol Biomark Prev. 2009;18(3):837–45.CrossRef Manduca A, Carston MJ, Heine JJ, Scott CG, Pankratz VS, Brandt KR, Sellers TA, Vachon CM, Cerhan JR. Texture features from mammographic images and risk of breast cancer. Cancer Epidemiol Biomark Prev. 2009;18(3):837–45.CrossRef
9.
go back to reference Häberle L, Wagner F, Fasching PA, Jud SM, Heusinger K, Loehberg CR, Hein A, Bayer CM, Hack CC, Lux MP. Characterizing mammographic images by using generic texture features. Breast Cancer Res. 2012;14(2):R59.CrossRefPubMedPubMedCentral Häberle L, Wagner F, Fasching PA, Jud SM, Heusinger K, Loehberg CR, Hein A, Bayer CM, Hack CC, Lux MP. Characterizing mammographic images by using generic texture features. Breast Cancer Res. 2012;14(2):R59.CrossRefPubMedPubMedCentral
10.
go back to reference Wei J, Chan H-P, Wu Y-T, Zhou C, Helvie MA, Tsodikov A, Hadjiiski LM, Sahiner B. Association of computerized mammographic parenchymal pattern measure with breast cancer risk: a pilot case-control study. Radiology. 2011;260(1):42–9.CrossRefPubMedPubMedCentral Wei J, Chan H-P, Wu Y-T, Zhou C, Helvie MA, Tsodikov A, Hadjiiski LM, Sahiner B. Association of computerized mammographic parenchymal pattern measure with breast cancer risk: a pilot case-control study. Radiology. 2011;260(1):42–9.CrossRefPubMedPubMedCentral
11.
go back to reference Zheng Y, Keller BM, Ray S, Wang Y, Conant EF, Gee JC, Kontos D. Parenchymal texture analysis in digital mammography: a fully automated pipeline for breast cancer risk assessment. Med Phys. 2015;42(7):4149–60.CrossRefPubMedPubMedCentral Zheng Y, Keller BM, Ray S, Wang Y, Conant EF, Gee JC, Kontos D. Parenchymal texture analysis in digital mammography: a fully automated pipeline for breast cancer risk assessment. Med Phys. 2015;42(7):4149–60.CrossRefPubMedPubMedCentral
12.
go back to reference Huo Z, Giger ML, Olopade OI, Wolverton DE, Weber BL, Metz CE, Zhong W, Cummings SA. Computerized analysis of digitized mammograms of BRCA1 and BRCA2 gene mutation carriers 1. Radiology. 2002;225(2):519–26.CrossRefPubMed Huo Z, Giger ML, Olopade OI, Wolverton DE, Weber BL, Metz CE, Zhong W, Cummings SA. Computerized analysis of digitized mammograms of BRCA1 and BRCA2 gene mutation carriers 1. Radiology. 2002;225(2):519–26.CrossRefPubMed
13.
go back to reference Gierach GL, Li H, Loud JT, Greene MH, Chow CK, Lan L, Prindiville SA, Eng-Wong J, Soballe PW, Giambartolomei C. Relationships between computer-extracted mammographic texture pattern features and BRCA1/2 mutation status: a cross-sectional study. Breast Cancer Res. 2014;16(4):424.PubMedPubMedCentral Gierach GL, Li H, Loud JT, Greene MH, Chow CK, Lan L, Prindiville SA, Eng-Wong J, Soballe PW, Giambartolomei C. Relationships between computer-extracted mammographic texture pattern features and BRCA1/2 mutation status: a cross-sectional study. Breast Cancer Res. 2014;16(4):424.PubMedPubMedCentral
14.
go back to reference Li H, Giger ML, Sun C, Ponsukcharoen U, Huo D, Lan L, Olopade OI, Jamieson AR, Brown JB, Di Rienzo A. Pilot study demonstrating potential association between breast cancer image-based risk phenotypes and genomic biomarkers. Med Phys. 2014;41(3):031917.CrossRefPubMedPubMedCentral Li H, Giger ML, Sun C, Ponsukcharoen U, Huo D, Lan L, Olopade OI, Jamieson AR, Brown JB, Di Rienzo A. Pilot study demonstrating potential association between breast cancer image-based risk phenotypes and genomic biomarkers. Med Phys. 2014;41(3):031917.CrossRefPubMedPubMedCentral
15.
go back to reference Keller BM, Chen J, Conant EF, Kontos D. Breast density and parenchymal texture measures as potential risk factors for estrogen-receptor positive breast cancer. In SPIE Medical Imaging. Bellingham: International Society for Optics and Photonics; 2014. pp. 90351D–90351D. Keller BM, Chen J, Conant EF, Kontos D. Breast density and parenchymal texture measures as potential risk factors for estrogen-receptor positive breast cancer. In SPIE Medical Imaging. Bellingham: International Society for Optics and Photonics; 2014. pp. 90351D–90351D.
16.
go back to reference Bertrand KA, Tamimi RM, Scott CG, Jensen MR, Pankratz VS, Visscher D, Norman A, Couch F, Shepherd J, Fan B. Mammographic density and risk of breast cancer by age and tumor characteristics. Breast Cancer Res. 2013;15(6):1.CrossRef Bertrand KA, Tamimi RM, Scott CG, Jensen MR, Pankratz VS, Visscher D, Norman A, Couch F, Shepherd J, Fan B. Mammographic density and risk of breast cancer by age and tumor characteristics. Breast Cancer Res. 2013;15(6):1.CrossRef
17.
go back to reference Bertrand KA, Scott CG, Tamimi RM, Jensen MR, Pankratz VS, Norman AD, Visscher DW, Couch FJ, Shepherd J, Chen Y-Y. Dense and nondense mammographic area and risk of breast cancer by age and tumor characteristics. Cancer Epidemiol Biomarkers Prev. 2015;24(5):798–809. Bertrand KA, Scott CG, Tamimi RM, Jensen MR, Pankratz VS, Norman AD, Visscher DW, Couch FJ, Shepherd J, Chen Y-Y. Dense and nondense mammographic area and risk of breast cancer by age and tumor characteristics. Cancer Epidemiol Biomarkers Prev. 2015;24(5):798–809.
18.
go back to reference Olson JE, Sellers TA, Scott CG, Schueler BA, Brandt KR, Serie DJ, Jensen MR, Wu F-F, Morton MJ, Heine JJ. The influence of mammogram acquisition on the mammographic density and breast cancer association in the Mayo mammography health study cohort. Breast Cancer Res. 2012;14(6):1.CrossRef Olson JE, Sellers TA, Scott CG, Schueler BA, Brandt KR, Serie DJ, Jensen MR, Wu F-F, Morton MJ, Heine JJ. The influence of mammogram acquisition on the mammographic density and breast cancer association in the Mayo mammography health study cohort. Breast Cancer Res. 2012;14(6):1.CrossRef
19.
go back to reference Colditz GA. Estrogen, estrogen plus progestin therapy, and risk of breast cancer. Clin Cancer Res. 2005;11(2 Pt 2):909s–17.PubMed Colditz GA. Estrogen, estrogen plus progestin therapy, and risk of breast cancer. Clin Cancer Res. 2005;11(2 Pt 2):909s–17.PubMed
20.
go back to reference Vachon CM, van Gils CH, Sellers TA, Ghosh K, Pruthi S, Brandt KR, Pankratz VS. Mammographic density, breast cancer risk and risk prediction. Breast Cancer Res. 2007;9(6):217.CrossRefPubMedPubMedCentral Vachon CM, van Gils CH, Sellers TA, Ghosh K, Pruthi S, Brandt KR, Pankratz VS. Mammographic density, breast cancer risk and risk prediction. Breast Cancer Res. 2007;9(6):217.CrossRefPubMedPubMedCentral
21.
go back to reference Kerlikowske K, Shepherd J, Creasman J, Tice JA, Ziv E, Cummings SR. Are breast density and bone mineral density independent risk factors for breast cancer? J Natl Cancer Inst. 2005;97(5):368–74.CrossRefPubMed Kerlikowske K, Shepherd J, Creasman J, Tice JA, Ziv E, Cummings SR. Are breast density and bone mineral density independent risk factors for breast cancer? J Natl Cancer Inst. 2005;97(5):368–74.CrossRefPubMed
22.
go back to reference Byng J, Boyd N, Fishell E, Jong R, Yaffe M. Automated analysis of mammographic densities. Phys Med Biol. 1996;41(5):909.CrossRefPubMed Byng J, Boyd N, Fishell E, Jong R, Yaffe M. Automated analysis of mammographic densities. Phys Med Biol. 1996;41(5):909.CrossRefPubMed
23.
go back to reference Shepherd JA, Kerlikowske K, Ma L, Duewer F, Fan B, Wang J, Malkov S, Vittinghoff E, Cummings SR. Volume of mammographic density and risk of breast cancer. Cancer Epidemiol Biomarkers Prev. 2011;20(7):1473–82.CrossRefPubMedPubMedCentral Shepherd JA, Kerlikowske K, Ma L, Duewer F, Fan B, Wang J, Malkov S, Vittinghoff E, Cummings SR. Volume of mammographic density and risk of breast cancer. Cancer Epidemiol Biomarkers Prev. 2011;20(7):1473–82.CrossRefPubMedPubMedCentral
24.
go back to reference Castella C, Kinkel K, Eckstein MP, Sottas P-E, Verdun FR, Bochud FO. Semiautomatic mammographic parenchymal patterns classification using multiple statistical features. Acad Radiol. 2007;14(12):1486–99.CrossRefPubMed Castella C, Kinkel K, Eckstein MP, Sottas P-E, Verdun FR, Bochud FO. Semiautomatic mammographic parenchymal patterns classification using multiple statistical features. Acad Radiol. 2007;14(12):1486–99.CrossRefPubMed
25.
go back to reference Mavroforakis ME, Georgiou HV, Dimitropoulos N, Cavouras D, Theodoridis S. Mammographic masses characterization based on localized texture and dataset fractal analysis using linear, neural and support vector machine classifiers. Artif Intell Med. 2006;37(2):145–62.CrossRefPubMed Mavroforakis ME, Georgiou HV, Dimitropoulos N, Cavouras D, Theodoridis S. Mammographic masses characterization based on localized texture and dataset fractal analysis using linear, neural and support vector machine classifiers. Artif Intell Med. 2006;37(2):145–62.CrossRefPubMed
26.
go back to reference Burgess AE. Mammographic structure: Data preparation and spatial statistics analysis. In Medical Imaging'99. Bellingham: International Society for Optics and Photonics; 1999. pp. 642–653. Burgess AE. Mammographic structure: Data preparation and spatial statistics analysis. In Medical Imaging'99. Bellingham: International Society for Optics and Photonics; 1999. pp. 642–653.
27.
go back to reference Haralick RM, Shanmugam K, Dinstein IH. Textural features for image classification. Syst Man Cybernetics IEEE Trans. 1973;6:610–21.CrossRef Haralick RM, Shanmugam K, Dinstein IH. Textural features for image classification. Syst Man Cybernetics IEEE Trans. 1973;6:610–21.CrossRef
28.
go back to reference Amadasun M, King R. Textural features corresponding to textural properties. IEEE Trans Syst Man Cybern. 1989;19(5):1264–74.CrossRef Amadasun M, King R. Textural features corresponding to textural properties. IEEE Trans Syst Man Cybern. 1989;19(5):1264–74.CrossRef
29.
go back to reference Li H, Giger ML, Olopade OI, Margolis A, Lan L, Chinander MR. computerized texture analysis of mammographic parenchymal patterns of digitized mammograms 1. Acad Radiol. 2005;12(7):863–73.CrossRefPubMed Li H, Giger ML, Olopade OI, Margolis A, Lan L, Chinander MR. computerized texture analysis of mammographic parenchymal patterns of digitized mammograms 1. Acad Radiol. 2005;12(7):863–73.CrossRefPubMed
30.
go back to reference Caldwell CB, Stapleton SJ, Holdsworth DW, Jong RA, Weiser WJ, Cooke G, Yaffe MJ. Characterisation of mammographic parenchymal pattern by fractal dimension. Phys Med Biol. 1990;35(2):235–47.CrossRefPubMed Caldwell CB, Stapleton SJ, Holdsworth DW, Jong RA, Weiser WJ, Cooke G, Yaffe MJ. Characterisation of mammographic parenchymal pattern by fractal dimension. Phys Med Biol. 1990;35(2):235–47.CrossRefPubMed
31.
go back to reference Boone JM, Lindfors KK, Beatty CS, Seibert JA. A breast density index for digital mammograms based on radiologists’ ranking. J Digit Imaging. 1998;11(3):101–15.CrossRefPubMedPubMedCentral Boone JM, Lindfors KK, Beatty CS, Seibert JA. A breast density index for digital mammograms based on radiologists’ ranking. J Digit Imaging. 1998;11(3):101–15.CrossRefPubMedPubMedCentral
32.
go back to reference Malkov S, Mahmoudzadeh AP, Kerlikowske K, Shepherd J. Automated Volumetric Breast Density Derived by Statistical Model Approach. In International Workshop on Digital Mammography. Cham: Springer International Publishing; 2014. pp. 257–264. Malkov S, Mahmoudzadeh AP, Kerlikowske K, Shepherd J. Automated Volumetric Breast Density Derived by Statistical Model Approach. In International Workshop on Digital Mammography. Cham: Springer International Publishing; 2014. pp. 257–264.
33.
go back to reference Li H, Giger ML, Olopade OI, Lan L. Fractal analysis of mammographic parenchymal patterns in breast cancer risk assessment. Acad Radiol. 2007;14(5):513–21.CrossRefPubMed Li H, Giger ML, Olopade OI, Lan L. Fractal analysis of mammographic parenchymal patterns in breast cancer risk assessment. Acad Radiol. 2007;14(5):513–21.CrossRefPubMed
34.
go back to reference Boyd NF, Martin LJ, Bronskill M, Yaffe MJ, Duric N, Minkin S. Breast tissue composition and susceptibility to breast cancer. J Nat Cancer Inst. 2010;102(16):1. Boyd NF, Martin LJ, Bronskill M, Yaffe MJ, Duric N, Minkin S. Breast tissue composition and susceptibility to breast cancer. J Nat Cancer Inst. 2010;102(16):1.
35.
go back to reference Tarabichi M, Antoniou A, Saiselet M, Pita JM, Andry G, Dumont JE, Detours V, Maenhaut C. Systems biology of cancer: entropy, disorder, and selection-driven evolution to independence, invasion and “swarm intelligence”. Cancer Metastasis Rev. 2013;32(3–4):403–21.CrossRefPubMedPubMedCentral Tarabichi M, Antoniou A, Saiselet M, Pita JM, Andry G, Dumont JE, Detours V, Maenhaut C. Systems biology of cancer: entropy, disorder, and selection-driven evolution to independence, invasion and “swarm intelligence”. Cancer Metastasis Rev. 2013;32(3–4):403–21.CrossRefPubMedPubMedCentral
36.
go back to reference Jing H, Yang YY, Wernick MN, Yarusso LM, Nishikawa RM. A comparison study of image features between FFDM and film mammogram images. Med Phys. 2012;39(7):4386–94.CrossRefPubMedPubMedCentral Jing H, Yang YY, Wernick MN, Yarusso LM, Nishikawa RM. A comparison study of image features between FFDM and film mammogram images. Med Phys. 2012;39(7):4386–94.CrossRefPubMedPubMedCentral
Metadata
Title
Mammographic texture and risk of breast cancer by tumor type and estrogen receptor status
Authors
Serghei Malkov
John A. Shepherd
Christopher G. Scott
Rulla M. Tamimi
Lin Ma
Kimberly A. Bertrand
Fergus Couch
Matthew R. Jensen
Amir P. Mahmoudzadeh
Bo Fan
Aaron Norman
Kathleen R. Brandt
V. Shane Pankratz
Celine M. Vachon
Karla Kerlikowske
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 1/2016
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/s13058-016-0778-1

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