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Published in: Journal of Digital Imaging 5/2019

01-10-2019 | Breast Cancer

Computer-Assisted Nuclear Atypia Scoring of Breast Cancer: a Preliminary Study

Authors: Ziba Gandomkar, Patrick C. Brennan, Claudia Mello-Thoms

Published in: Journal of Imaging Informatics in Medicine | Issue 5/2019

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Abstract

Inter-pathologist agreement for nuclear atypia scoring of breast cancer is poor. To address this problem, previous studies suggested some criteria for describing the variations appearance of tumor cells relative to normal cells. However, these criteria were still assessed subjectively by pathologists. Previous studies used quantitative computer-extracted features for scoring. However, application of these tools is limited as further improvement in their accuracy is required. This study proposes COMPASS (COMputer-assisted analysis combined with Pathologist’s ASSessment) for reproducible nuclear atypia scoring. COMPASS relies on both cytological criteria assessed subjectively by pathologists as well as computer-extracted textural features. Using machine learning, COMPASS combines these two sets of features and output nuclear atypia score. COMPASS’s performance was evaluated using 300 images for which expert-consensus derived reference nuclear pleomorphism scores were available, and they were scanned by two scanners from different vendors. A personalized model was built for three pathologists who gave scores to six atypia-related criteria for each image. Leave-one-out cross validation (LOOCV) was used. COMPASS was trained and tested for each pathologist separately. Percentage agreement between COMPASS and the reference nuclear scores was 93.8%, 92.9%, and 93.1% for three pathologists. COMPASS’s performance in nuclear grading was almost identical for both scanners, with Cohen’s kappa ranging from 0.80 to 0.86 for different pathologists and different scanners. Independently, the images were also assessed by two experienced senior pathologists. Cohen’s kappa of COMPASS was comparable to the Cohen’s kappa for two senior pathologists (0.79 and 0.68).
Literature
1.
go back to reference Mook S, Schmidt MK, Rutgers EJ, van de Velde AO, Visser O, Rutgers SM, Armstrong N, van’t Veer LJ, Ravdin PM: Calibration and discriminatory accuracy of prognosis calculation for breast cancer with the online adjuvant! Program: A hospital-based retrospective cohort study. Lancet Oncol 10(11):1070–1076, 2009CrossRefPubMed Mook S, Schmidt MK, Rutgers EJ, van de Velde AO, Visser O, Rutgers SM, Armstrong N, van’t Veer LJ, Ravdin PM: Calibration and discriminatory accuracy of prognosis calculation for breast cancer with the online adjuvant! Program: A hospital-based retrospective cohort study. Lancet Oncol 10(11):1070–1076, 2009CrossRefPubMed
2.
go back to reference Elston CW, Ellis IO: Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: Experience from a large study with long-term follow-up. Histopathology 19(5):403–410, 1991CrossRef Elston CW, Ellis IO: Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: Experience from a large study with long-term follow-up. Histopathology 19(5):403–410, 1991CrossRef
3.
go back to reference Bueno-de-Mesquita JM, Nuyten D, Wesseling J, van Tinteren H, Linn S, van De Vijver M: The impact of inter-observer variation in pathological assessment of node-negative breast cancer on clinical risk assessment and patient selection for adjuvant systemic treatment. Ann Oncol 21(1):40–47, 2009CrossRefPubMed Bueno-de-Mesquita JM, Nuyten D, Wesseling J, van Tinteren H, Linn S, van De Vijver M: The impact of inter-observer variation in pathological assessment of node-negative breast cancer on clinical risk assessment and patient selection for adjuvant systemic treatment. Ann Oncol 21(1):40–47, 2009CrossRefPubMed
4.
go back to reference Frierson, Jr HF, Wolber RA, Berean KW, Franquemont DW, Gaffey MJ, Boyd JC, Wilbur DC: Interobserver reproducibility of the Nottingham modification of the bloom and Richardson histologic grading scheme for infiltrating ductal carcinoma. Am J Clin Pathol 103(2):195–198, 1995CrossRefPubMed Frierson, Jr HF, Wolber RA, Berean KW, Franquemont DW, Gaffey MJ, Boyd JC, Wilbur DC: Interobserver reproducibility of the Nottingham modification of the bloom and Richardson histologic grading scheme for infiltrating ductal carcinoma. Am J Clin Pathol 103(2):195–198, 1995CrossRefPubMed
5.
go back to reference Harvey JM, de Klerk NH, Sterrett GF: Histological grading in breast cancer: Interobserver agreement, and relation to other prognostic factors including ploidy. Pathology 24(2):63–68, 1992CrossRefPubMed Harvey JM, de Klerk NH, Sterrett GF: Histological grading in breast cancer: Interobserver agreement, and relation to other prognostic factors including ploidy. Pathology 24(2):63–68, 1992CrossRefPubMed
6.
go back to reference Longacre TA, Ennis M, Quenneville LA, Bane AL, Bleiweiss IJ, Carter BA, Catelano E, Hendrickson MR, Hibshoosh H, Layfield LJ: Interobserver agreement and reproducibility in classification of invasive breast carcinoma: An NCI breast cancer family registry study. Mod Pathol 19(2):195–207, 2006CrossRefPubMed Longacre TA, Ennis M, Quenneville LA, Bane AL, Bleiweiss IJ, Carter BA, Catelano E, Hendrickson MR, Hibshoosh H, Layfield LJ: Interobserver agreement and reproducibility in classification of invasive breast carcinoma: An NCI breast cancer family registry study. Mod Pathol 19(2):195–207, 2006CrossRefPubMed
7.
go back to reference Meyer JS, Alvarez C, Milikowski C, Olson N, Russo I, Russo J, Glass A, Zehnbauer BA, Lister K, Parwaresch R: Breast carcinoma malignancy grading by Bloom–Richardson system vs proliferation index: Reproducibility of grade and advantages of proliferation index. Mod Pathol 18(8):1067–1078, 2005CrossRefPubMed Meyer JS, Alvarez C, Milikowski C, Olson N, Russo I, Russo J, Glass A, Zehnbauer BA, Lister K, Parwaresch R: Breast carcinoma malignancy grading by Bloom–Richardson system vs proliferation index: Reproducibility of grade and advantages of proliferation index. Mod Pathol 18(8):1067–1078, 2005CrossRefPubMed
8.
go back to reference Paradiso A, Ellis I, Zito F, Marubini E, Pizzamiglio S, Verderio P: Short-and long-term effects of a training session on pathologists’ performance: The INQAT experience for histological grading in breast cancer. J Clin Pathol 62(3):279–281, 2009CrossRefPubMed Paradiso A, Ellis I, Zito F, Marubini E, Pizzamiglio S, Verderio P: Short-and long-term effects of a training session on pathologists’ performance: The INQAT experience for histological grading in breast cancer. J Clin Pathol 62(3):279–281, 2009CrossRefPubMed
9.
go back to reference Adams AL, Chhieng DC, Bell WC, Winokur T, Hameed O: Histologic grading of invasive lobular carcinoma: Does use of a 2-tiered nuclear grading system improve interobserver variability? Ann Diagn Pathol 13(4):223–225, 2009CrossRefPubMed Adams AL, Chhieng DC, Bell WC, Winokur T, Hameed O: Histologic grading of invasive lobular carcinoma: Does use of a 2-tiered nuclear grading system improve interobserver variability? Ann Diagn Pathol 13(4):223–225, 2009CrossRefPubMed
11.
go back to reference Cosatto E, Miller M, Graf HP, Meyer JS. Grading nuclear pleomorphism on histological micrographs. InPattern Recognition, 2008. ICPR 2008. 19th International Conference on 2008 Dec 8 (pp. 1-4). IEEE. Cosatto E, Miller M, Graf HP, Meyer JS. Grading nuclear pleomorphism on histological micrographs. InPattern Recognition, 2008. ICPR 2008. 19th International Conference on 2008 Dec 8 (pp. 1-4). IEEE.
12.
go back to reference Khan AM, Sirinukunwattana K, Rajpoot N: A global covariance descriptor for nuclear atypia scoring in breast histopathology images. IEEE J Biomed Health Inform 19(5):1637–1647, 2015CrossRefPubMed Khan AM, Sirinukunwattana K, Rajpoot N: A global covariance descriptor for nuclear atypia scoring in breast histopathology images. IEEE J Biomed Health Inform 19(5):1637–1647, 2015CrossRefPubMed
13.
go back to reference Dunne B, Going J: Scoring nuclear pleomorphism in breast cancer. Histopathology 39(3):259–265, 2001CrossRefPubMed Dunne B, Going J: Scoring nuclear pleomorphism in breast cancer. Histopathology 39(3):259–265, 2001CrossRefPubMed
14.
go back to reference Zhang R, Chen H-j, Wei B, Zhang H-y, Pang Z-g, Zhu H, Zhang Z, Fu J, Bu H: Reproducibility of the Nottingham modification of the Scarff-Bloom-Richardson histological grading system and the complementary value of Ki-67 to this system. Chin Med J (Engl Ed) 123(15):1976, 2010 Zhang R, Chen H-j, Wei B, Zhang H-y, Pang Z-g, Zhu H, Zhang Z, Fu J, Bu H: Reproducibility of the Nottingham modification of the Scarff-Bloom-Richardson histological grading system and the complementary value of Ki-67 to this system. Chin Med J (Engl Ed) 123(15):1976, 2010
15.
go back to reference Racoceanu D, Capron F: Semantic integrative digital pathology: Insights into microsemiological semantics and image analysis scalability. Pathobiology 83(2–3):148–155, 2016CrossRefPubMed Racoceanu D, Capron F: Semantic integrative digital pathology: Insights into microsemiological semantics and image analysis scalability. Pathobiology 83(2–3):148–155, 2016CrossRefPubMed
16.
go back to reference Saha K, Raychaudhuri G, Chattopadhyay BK, Das I: Comparative evaluation of six cytological grading systems in breast carcinoma. J Cytol 30(2):87–93, 2013CrossRefPubMedPubMedCentral Saha K, Raychaudhuri G, Chattopadhyay BK, Das I: Comparative evaluation of six cytological grading systems in breast carcinoma. J Cytol 30(2):87–93, 2013CrossRefPubMedPubMedCentral
17.
go back to reference Abati A, McKee G: Grading of breast carcinoma in fine-needle aspiration cytology. Diagn Cytopathol 19(2):153–154, 1998CrossRefPubMed Abati A, McKee G: Grading of breast carcinoma in fine-needle aspiration cytology. Diagn Cytopathol 19(2):153–154, 1998CrossRefPubMed
18.
go back to reference Robinson I, McKee G, Kissin M: Typing and grading breast carcinoma on fine-needle aspiration: Is this clinically useful information? Diagn Cytopathol 13(3):260–265, 1995CrossRefPubMed Robinson I, McKee G, Kissin M: Typing and grading breast carcinoma on fine-needle aspiration: Is this clinically useful information? Diagn Cytopathol 13(3):260–265, 1995CrossRefPubMed
19.
go back to reference Macenko M, Niethammer M, Marron JS, Borland D, Woosley JT, Guan X, Schmitt C, and Thomas NE, A method for normalizing histology slides for quantitative analysis. pp. 1107–1110 Macenko M, Niethammer M, Marron JS, Borland D, Woosley JT, Guan X, Schmitt C, and Thomas NE, A method for normalizing histology slides for quantitative analysis. pp. 1107–1110
20.
go back to reference Al-Kofahi Y, Lassoued W, Lee W, Roysam B: Improved automatic detection and segmentation of cell nuclei in histopathology images. IEEE Trans Biomed Eng 57(4):841–852, 2010CrossRefPubMed Al-Kofahi Y, Lassoued W, Lee W, Roysam B: Improved automatic detection and segmentation of cell nuclei in histopathology images. IEEE Trans Biomed Eng 57(4):841–852, 2010CrossRefPubMed
21.
22.
go back to reference Gandomkar Z, Brennan PC, Mello-Thoms C: Determining image processing features describing the appearance of challenging mitotic figures and miscounted nonmitotic objects. J Pathol Inform 8:34, 2017CrossRefPubMedPubMedCentral Gandomkar Z, Brennan PC, Mello-Thoms C: Determining image processing features describing the appearance of challenging mitotic figures and miscounted nonmitotic objects. J Pathol Inform 8:34, 2017CrossRefPubMedPubMedCentral
23.
go back to reference Shahriari B, Swersky K, Wang Z, Adams RP, De Freitas N: Taking the human out of the loop: A review of Bayesian optimization. Proc IEEE 104(1):148–175, 2016CrossRef Shahriari B, Swersky K, Wang Z, Adams RP, De Freitas N: Taking the human out of the loop: A review of Bayesian optimization. Proc IEEE 104(1):148–175, 2016CrossRef
24.
go back to reference Chawla NV, Bowyer KW, Hall LO, Kegelmeyer WP: SMOTE: Synthetic minority over-sampling technique. J Artif Intell Res 16:321–357, 2002CrossRef Chawla NV, Bowyer KW, Hall LO, Kegelmeyer WP: SMOTE: Synthetic minority over-sampling technique. J Artif Intell Res 16:321–357, 2002CrossRef
25.
go back to reference Viera AJ, Garrett JM: Understanding interobserver agreement: The kappa statistic. Fam Med 37(5):360–363, 2005PubMed Viera AJ, Garrett JM: Understanding interobserver agreement: The kappa statistic. Fam Med 37(5):360–363, 2005PubMed
26.
go back to reference Hanley JA, McNeil BJ: The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143(1):29–36, 1982CrossRefPubMed Hanley JA, McNeil BJ: The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143(1):29–36, 1982CrossRefPubMed
27.
go back to reference Mirza AN, Mirza NQ, Vlastos G, Singletary SE: Prognostic factors in node-negative breast cancer: A review of studies with sample size more than 200 and follow-up more than 5 years. Ann Surg 235(1):10–26, 2002CrossRefPubMedPubMedCentral Mirza AN, Mirza NQ, Vlastos G, Singletary SE: Prognostic factors in node-negative breast cancer: A review of studies with sample size more than 200 and follow-up more than 5 years. Ann Surg 235(1):10–26, 2002CrossRefPubMedPubMedCentral
28.
go back to reference Gandomkar Z, Brennan PC, Mello-Thoms C. A framework for distinguishing benign from malignant breast histopathological images using deep residual networks. In14th International Workshop on Breast Imaging (IWBI 2018), International Society for Optics and Photonics, Vol. 10718, p. 107180U, 2018. Gandomkar Z, Brennan PC, Mello-Thoms C. A framework for distinguishing benign from malignant breast histopathological images using deep residual networks. In14th International Workshop on Breast Imaging (IWBI 2018), International Society for Optics and Photonics, Vol. 10718, p. 107180U, 2018.
29.
go back to reference Cireşan DC, Giusti A, Gambardella LM, and Schmidhuber J, Mitosis detection in breast cancer histology images with deep neural networks. pp. 411–418 Cireşan DC, Giusti A, Gambardella LM, and Schmidhuber J, Mitosis detection in breast cancer histology images with deep neural networks. pp. 411–418
30.
go back to reference Gandomkar Z, Brennan PC, Mello-Thoms C: MuDeRN: Multi-category classification of breast histopathological image using deep residual networks. Artif Intell Med 88:14–24, 2018CrossRefPubMed Gandomkar Z, Brennan PC, Mello-Thoms C: MuDeRN: Multi-category classification of breast histopathological image using deep residual networks. Artif Intell Med 88:14–24, 2018CrossRefPubMed
31.
go back to reference Gandomkar Z, Tay K, Brennan PC, and Mello-Thoms C, A model based on temporal dynamics of fixations for distinguishing expert radiologists’ scanpaths. p. 1013606 Gandomkar Z, Tay K, Brennan PC, and Mello-Thoms C, A model based on temporal dynamics of fixations for distinguishing expert radiologists’ scanpaths. p. 1013606
32.
go back to reference Gandomkar Z, Tay K, Brennan PC, Mello-Thoms C: Recurrence quantification analysis of radiologists’ scanpaths when interpreting mammograms. Med Phys 45:3052–3062, 2018CrossRefPubMed Gandomkar Z, Tay K, Brennan PC, Mello-Thoms C: Recurrence quantification analysis of radiologists’ scanpaths when interpreting mammograms. Med Phys 45:3052–3062, 2018CrossRefPubMed
33.
go back to reference Gandomkar Z, Tay K, Ryder W, Brennan PC, and Mello-Thoms C, Predicting radiologists’ true and false positive decisions in reading mammograms by using gaze parameters and image-based features. p. 978715 Gandomkar Z, Tay K, Ryder W, Brennan PC, and Mello-Thoms C, Predicting radiologists’ true and false positive decisions in reading mammograms by using gaze parameters and image-based features. p. 978715
34.
go back to reference Gandomkar Z, Tay K, Ryder W, Brennan PC, Mello-Thoms C: iCAP: An individualized model combining gaze parameters and image-based features to predict radiologists’ decisions while Reading mammograms. IEEE Trans Med Imaging 36(5):1066–1075, 2017CrossRefPubMed Gandomkar Z, Tay K, Ryder W, Brennan PC, Mello-Thoms C: iCAP: An individualized model combining gaze parameters and image-based features to predict radiologists’ decisions while Reading mammograms. IEEE Trans Med Imaging 36(5):1066–1075, 2017CrossRefPubMed
Metadata
Title
Computer-Assisted Nuclear Atypia Scoring of Breast Cancer: a Preliminary Study
Authors
Ziba Gandomkar
Patrick C. Brennan
Claudia Mello-Thoms
Publication date
01-10-2019
Publisher
Springer International Publishing
Published in
Journal of Imaging Informatics in Medicine / Issue 5/2019
Print ISSN: 2948-2925
Electronic ISSN: 2948-2933
DOI
https://doi.org/10.1007/s10278-019-00181-8

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