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Published in: Medical & Biological Engineering & Computing 7-8/2021

10-07-2021 | Original Article

A whole-slide image grading benchmark and tissue classification for cervical cancer precursor lesions with inter-observer variability

Authors: Abdulkadir Albayrak, Asli Unlu Akhan, Nurullah Calik, Abdulkerim Capar, Gokhan Bilgin, Behcet Ugur Toreyin, Bahar Muezzinoglu, Ilknur Turkmen, Lutfiye Durak-Ata

Published in: Medical & Biological Engineering & Computing | Issue 7-8/2021

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Abstract

The cervical cancer developing from the precancerous lesions caused by the human papillomavirus (HPV) has been one of the preventable cancers with the help of periodic screening. Cervical intraepithelial neoplasia (CIN) and squamous intraepithelial lesion (SIL) are two types of grading conventions widely accepted by pathologists. On the other hand, inter-observer variability is an important issue for final diagnosis. In this paper, a whole-slide image grading benchmark for cervical cancer precursor lesions is created and the “Uterine Cervical Cancer Database” introduced in this article is the first publicly available cervical tissue microscopy image dataset. In addition, a morphological feature representing the angle between the basal membrane (BM) and the major axis of each nucleus in the tissue is proposed. The presence of papillae of the cervical epithelium and overlapping cell problems are also discussed. Besides that, the inter-observer variability is also evaluated by thorough comparisons among decisions of pathologists, as well as the final diagnosis.

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Literature
1.
go back to reference Achanta R, Shaji A, Smith K, Lucchi A, Fua P, Süsstrunk S (2012) Slic superpixels compared to state-of-the-art superpixel methods. IEEE Trans Pattern Anal Mach Intell 34(11):2274–2282CrossRef Achanta R, Shaji A, Smith K, Lucchi A, Fua P, Süsstrunk S (2012) Slic superpixels compared to state-of-the-art superpixel methods. IEEE Trans Pattern Anal Mach Intell 34(11):2274–2282CrossRef
2.
go back to reference Al-Janabi S, Huisman A, VDP J (2012) Digital pathology: current status and future perspectives. Histopathology 61(1):1–9CrossRef Al-Janabi S, Huisman A, VDP J (2012) Digital pathology: current status and future perspectives. Histopathology 61(1):1–9CrossRef
3.
go back to reference Arteta C, Lempitsky V, Noble JA, Zisserman A (2012) Learning to detect cells using non-overlapping extremal regions. In: International conference on medical image computing and computer-assisted intervention, Springer, pp 348–356 Arteta C, Lempitsky V, Noble JA, Zisserman A (2012) Learning to detect cells using non-overlapping extremal regions. In: International conference on medical image computing and computer-assisted intervention, Springer, pp 348–356
4.
go back to reference Cox JT, Wilkinson EJ, O’connor DM (2013) Historical perspective: terminology for lower anogenital tract pathology. AJSP: Rev Reports 18(4):158–167 Cox JT, Wilkinson EJ, O’connor DM (2013) Historical perspective: terminology for lower anogenital tract pathology. AJSP: Rev Reports 18(4):158–167
5.
go back to reference Darragh TM, Colgan TJ, Cox JT, Heller DS, Henry MR, Luff RD, McCalmont T, Nayar R, Palefsky JM, Stoler MH et al (2013) The lower anogenital squamous terminology standardization project for hpv-associated lesions: background and consensus recommendations from the college of american pathologists and the american society for colposcopy and cervical pathology. Int J Gynecol Pathol 32(1):76–115CrossRef Darragh TM, Colgan TJ, Cox JT, Heller DS, Henry MR, Luff RD, McCalmont T, Nayar R, Palefsky JM, Stoler MH et al (2013) The lower anogenital squamous terminology standardization project for hpv-associated lesions: background and consensus recommendations from the college of american pathologists and the american society for colposcopy and cervical pathology. Int J Gynecol Pathol 32(1):76–115CrossRef
6.
go back to reference Darragh TM, et al. (2012) The lower anogenital squamous terminology standardization project for hpv-associated lesions: background and consensus recommendations from the college of american pathologists and the american society for colposcopy and cervical pathology. Arch Path Lab Med 136(10):1266–1297CrossRef Darragh TM, et al. (2012) The lower anogenital squamous terminology standardization project for hpv-associated lesions: background and consensus recommendations from the college of american pathologists and the american society for colposcopy and cervical pathology. Arch Path Lab Med 136(10):1266–1297CrossRef
7.
go back to reference De S, Stanley RJ, Lu C, Long R, Antani S, Thoma G, Zuna R (2013) A fusion-based approach for uterine cervical cancer histology image classification. Comput Med Imaging Graph 37(7):475–487CrossRef De S, Stanley RJ, Lu C, Long R, Antani S, Thoma G, Zuna R (2013) A fusion-based approach for uterine cervical cancer histology image classification. Comput Med Imaging Graph 37(7):475–487CrossRef
8.
go back to reference Doorbar J (2007) Papillomavirus life cycle organization and biomarker selection. Dis Markers 23 (4):297–313CrossRef Doorbar J (2007) Papillomavirus life cycle organization and biomarker selection. Dis Markers 23 (4):297–313CrossRef
9.
go back to reference Galgano MT, Castle PE, Atkins KA, Brix WK, Nassau SR, Stoler MH (2010) Using biomarkers as objective standards in the diagnosis of cervical biopsies. Am J Surg Path 34(8):1077CrossRef Galgano MT, Castle PE, Atkins KA, Brix WK, Nassau SR, Stoler MH (2010) Using biomarkers as objective standards in the diagnosis of cervical biopsies. Am J Surg Path 34(8):1077CrossRef
10.
go back to reference Guo M, Baruch A, Silva E, Jan Y, Lin E, Sneige N, Deavers MT (2011) Efficacy of p16 and proexc immunostaining in the detection of high-grade cervical intraepithelial neoplasia and cervical carcinoma. Am J Clin Pathol 135(2):212–220CrossRef Guo M, Baruch A, Silva E, Jan Y, Lin E, Sneige N, Deavers MT (2011) Efficacy of p16 and proexc immunostaining in the detection of high-grade cervical intraepithelial neoplasia and cervical carcinoma. Am J Clin Pathol 135(2):212–220CrossRef
11.
go back to reference Guo P, Banerjee K, Stanley RJ, Long R, Antani S, Thoma G, Zuna R, Frazier SR, Moss RH, Stoecker WV (2016) Nuclei-based features for uterine cervical cancer histology image analysis with fusion-based classification. IEEE J Biomed Health Inform 20(6):1595–1607CrossRef Guo P, Banerjee K, Stanley RJ, Long R, Antani S, Thoma G, Zuna R, Frazier SR, Moss RH, Stoecker WV (2016) Nuclei-based features for uterine cervical cancer histology image analysis with fusion-based classification. IEEE J Biomed Health Inform 20(6):1595–1607CrossRef
12.
go back to reference He L, Long LR, Antani S, Thoma GR (2012) Histology image analysis for carcinoma detection and grading. Comput Methods Programs Biomed 107(3):538–556CrossRef He L, Long LR, Antani S, Thoma GR (2012) Histology image analysis for carcinoma detection and grading. Comput Methods Programs Biomed 107(3):538–556CrossRef
13.
go back to reference Hong X, Chen S, Harris CJ (2007) A kernel-based two-class classifier for imbalanced data sets. IEEE Trans Neur Netw 18(1):28–41CrossRef Hong X, Chen S, Harris CJ (2007) A kernel-based two-class classifier for imbalanced data sets. IEEE Trans Neur Netw 18(1):28–41CrossRef
14.
go back to reference Jordan J, Arbyn M, Martin-Hirsch P, Schenck U, Baldauf JJ, Da Silva D, Anttila A, Nieminen P, Prendiville W (2008) European guidelines for quality assurance in cervical cancer screening: recommendations for clinical management of abnormal cervical cytology, part 1. Cytopathology 19(6):342–354CrossRef Jordan J, Arbyn M, Martin-Hirsch P, Schenck U, Baldauf JJ, Da Silva D, Anttila A, Nieminen P, Prendiville W (2008) European guidelines for quality assurance in cervical cancer screening: recommendations for clinical management of abnormal cervical cytology, part 1. Cytopathology 19(6):342–354CrossRef
15.
go back to reference Keenan S, Diamond J, McCluggage G, Bharucha H, Thompson D, Bartels PH, Hamilton PW (2000) An automated machine vision system for the histological grading of cervical intraepithelial neoplasia (cin). J Pathol 192(3):351–362CrossRef Keenan S, Diamond J, McCluggage G, Bharucha H, Thompson D, Bartels PH, Hamilton PW (2000) An automated machine vision system for the histological grading of cervical intraepithelial neoplasia (cin). J Pathol 192(3):351–362CrossRef
16.
go back to reference Kurman RJ (2013) Blaustein’s pathology of the female genital tract. Springer Science & Business Media, Berlin Kurman RJ (2013) Blaustein’s pathology of the female genital tract. Springer Science & Business Media, Berlin
17.
go back to reference Lim S, Lee M, Cho I, Hong R, Lim S (2016) Efficacy of p16 and ki-67 immunostaining in the detection of squamous intraepithelial lesions in a high-risk hpv group. Oncol Lett 11(2):1447–1452CrossRef Lim S, Lee M, Cho I, Hong R, Lim S (2016) Efficacy of p16 and ki-67 immunostaining in the detection of squamous intraepithelial lesions in a high-risk hpv group. Oncol Lett 11(2):1447–1452CrossRef
18.
go back to reference Liu W, Chawla S (2011) Class confidence weighted knn algorithms for imbalanced data sets. In: Pacific-asia conference on knowledge discovery and data mining, Springer, pp 345–356 Liu W, Chawla S (2011) Class confidence weighted knn algorithms for imbalanced data sets. In: Pacific-asia conference on knowledge discovery and data mining, Springer, pp 345–356
19.
go back to reference Madabhushi A, Lee G (2016) Image analysis and machine learning in digital pathology: Challenges and opportunities. Med Image Anal 33:170–175CrossRef Madabhushi A, Lee G (2016) Image analysis and machine learning in digital pathology: Challenges and opportunities. Med Image Anal 33:170–175CrossRef
20.
go back to reference Mazurowski MA, Habas PA, Zurada JM, Lo JY, Baker JA, Tourassi GD (2008) Training neural network classifiers for medical decision making: The effects of imbalanced datasets on classification performance. Neural Netw 21(2-3):427–436CrossRef Mazurowski MA, Habas PA, Zurada JM, Lo JY, Baker JA, Tourassi GD (2008) Training neural network classifiers for medical decision making: The effects of imbalanced datasets on classification performance. Neural Netw 21(2-3):427–436CrossRef
21.
go back to reference McCluggage W, Bharucha H, Caughley L, Date A, Hamilton P, Thornton C, Walsh M (1996) Interobserver variation in the reporting of cervical colposcopic biopsy specimens: Comparison of grading systems. J Clin Path 49(10):833–835CrossRef McCluggage W, Bharucha H, Caughley L, Date A, Hamilton P, Thornton C, Walsh M (1996) Interobserver variation in the reporting of cervical colposcopic biopsy specimens: Comparison of grading systems. J Clin Path 49(10):833–835CrossRef
22.
go back to reference McCluggage W, Walsh M, Thornton C, Hamilton P, Caughley L, Bharucha H, et al. (1998) Inter-and intra-observer variation in the histopathological reporting of cervical squamous in traepithelial lesion susing a modified bethesda grading system. Br J Obstet Gynaecol 105(2):206–210CrossRef McCluggage W, Walsh M, Thornton C, Hamilton P, Caughley L, Bharucha H, et al. (1998) Inter-and intra-observer variation in the histopathological reporting of cervical squamous in traepithelial lesion susing a modified bethesda grading system. Br J Obstet Gynaecol 105(2):206–210CrossRef
23.
go back to reference de Melo F, Lancellotti C, da Silva M (2016) 16 and ki-67 and their usefulness in the diagnosis of cervicalexpression of the immunohistochemical markers p intraepithelial neoplasms. Rev Bras Ginicol Obstet 38(2):82–87CrossRef de Melo F, Lancellotti C, da Silva M (2016) 16 and ki-67 and their usefulness in the diagnosis of cervicalexpression of the immunohistochemical markers p intraepithelial neoplasms. Rev Bras Ginicol Obstet 38(2):82–87CrossRef
24.
go back to reference Miranda G H B, Soares E G, Barrera J, Felipe JC (2012) Method to support diagnosis of cervical intraepithelial neoplasia (cin) based on structural analysis of histological images. In: 2012 25th IEEE International symposium on computer-based medical systems (CBMS) IEEE, pp 1–6 Miranda G H B, Soares E G, Barrera J, Felipe JC (2012) Method to support diagnosis of cervical intraepithelial neoplasia (cin) based on structural analysis of histological images. In: 2012 25th IEEE International symposium on computer-based medical systems (CBMS) IEEE, pp 1–6
25.
go back to reference Mitra A, MacIntyre D, Lee Y, Smith A, Marchesi JR, Lehne B, Bhatia R, Lyons D, Paraskevaidis E, Li J et al (2015) Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity. Sci Rep 5:16,865CrossRef Mitra A, MacIntyre D, Lee Y, Smith A, Marchesi JR, Lehne B, Bhatia R, Lyons D, Paraskevaidis E, Li J et al (2015) Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity. Sci Rep 5:16,865CrossRef
26.
go back to reference Naghdy G, Ros MB, Todd C et al (2012) Computer aided decision support system for cervical cancer classification. In: Applications of Digital Image Processing XXXV, SPIE, vol 8499, p 849919 Naghdy G, Ros MB, Todd C et al (2012) Computer aided decision support system for cervical cancer classification. In: Applications of Digital Image Processing XXXV, SPIE, vol 8499, p 849919
27.
go back to reference Najar F, Bourouis S, Bouguila N, Belghith S (2017) A comparison between different gaussian-based mixture models. In: 2017 IEEE/ACS 14th International conference on computer systems and applications, AICCSA’17, IEEE, pp 704–708 Najar F, Bourouis S, Bouguila N, Belghith S (2017) A comparison between different gaussian-based mixture models. In: 2017 IEEE/ACS 14th International conference on computer systems and applications, AICCSA’17, IEEE, pp 704–708
28.
go back to reference Nayar R, Wilbur DC (2015) The Bethesda system for reporting cervical cytology: definitions, criteria, and explanatory notes. Springer, BerlinCrossRef Nayar R, Wilbur DC (2015) The Bethesda system for reporting cervical cytology: definitions, criteria, and explanatory notes. Springer, BerlinCrossRef
29.
go back to reference Ozaki S, Zen Y, Inoue M (2011) Biomarker expression in cervical intraepithelial neoplasia: potential progression predictive factors for low-grade lesions. Hum Pathol 42(7):1007–1012CrossRef Ozaki S, Zen Y, Inoue M (2011) Biomarker expression in cervical intraepithelial neoplasia: potential progression predictive factors for low-grade lesions. Hum Pathol 42(7):1007–1012CrossRef
30.
go back to reference Park KJ, Soslow RA (2009) Current concepts in cervical pathology. Arch Pathol Lab Med 133(5):729–738CrossRef Park KJ, Soslow RA (2009) Current concepts in cervical pathology. Arch Pathol Lab Med 133(5):729–738CrossRef
31.
go back to reference Qi X, Xing F, Foran D J, Yang L (2011) Robust segmentation of overlapping cells in histopathology specimens using parallel seed detection and repulsive level set. IEEE Trans Biomed Eng 59(3):754–765PubMed Qi X, Xing F, Foran D J, Yang L (2011) Robust segmentation of overlapping cells in histopathology specimens using parallel seed detection and repulsive level set. IEEE Trans Biomed Eng 59(3):754–765PubMed
32.
go back to reference Stoler MH (2000a) Advances in cervical screening technology. Mod Pathol 13(3):275–284CrossRef Stoler MH (2000a) Advances in cervical screening technology. Mod Pathol 13(3):275–284CrossRef
33.
go back to reference Stoler MH (2000b) Human papillomaviruses and cervical neoplasia: a model for carcinogenesis. Int J Gynecol Pathol 19(1):16–28CrossRef Stoler MH (2000b) Human papillomaviruses and cervical neoplasia: a model for carcinogenesis. Int J Gynecol Pathol 19(1):16–28CrossRef
34.
go back to reference Stoler MH, Schiffman M, et al. (2001) Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ascus-lsil triage study. Jama 285(11):1500–1505CrossRef Stoler MH, Schiffman M, et al. (2001) Interobserver reproducibility of cervical cytologic and histologic interpretations: realistic estimates from the ascus-lsil triage study. Jama 285(11):1500–1505CrossRef
35.
go back to reference Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2012) Global cancer statistics. CA Cancer J Clin 65(2):87–108CrossRef Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2012) Global cancer statistics. CA Cancer J Clin 65(2):87–108CrossRef
36.
go back to reference Van Zummeren M, Kremer WW, Leeman A, Bleeker MC, Jenkins D, van de Sandt M, Doorbar J, Heideman DA, Steenbergen RD, Snijders PJ et al (2018) Hpv e4 expression and dna hypermethylation of cadm1, mal, and mir124-2 genes in cervical cancer and precursor lesions. Mod Pathol 1 Van Zummeren M, Kremer WW, Leeman A, Bleeker MC, Jenkins D, van de Sandt M, Doorbar J, Heideman DA, Steenbergen RD, Snijders PJ et al (2018) Hpv e4 expression and dna hypermethylation of cadm1, mal, and mir124-2 genes in cervical cancer and precursor lesions. Mod Pathol 1
37.
go back to reference Crookes D, Wang Y, Eldin OS, Hamilton P, Wang S, Diamond J (2009) Assisted diagnosis of cervical intraepithelial neoplasia (cin). IEEE J Sel Top Signal Process 3(1):112–121CrossRef Crookes D, Wang Y, Eldin OS, Hamilton P, Wang S, Diamond J (2009) Assisted diagnosis of cervical intraepithelial neoplasia (cin). IEEE J Sel Top Signal Process 3(1):112–121CrossRef
38.
go back to reference Zhuang L, Dai H (2006) Parameter optimization of kernel-based one-class classifier on imbalance learning. J Comput 1(7):32–40CrossRef Zhuang L, Dai H (2006) Parameter optimization of kernel-based one-class classifier on imbalance learning. J Comput 1(7):32–40CrossRef
39.
go back to reference Zuo W, Lu W, Wang K, Zhang H (2008) Diagnosis of cardiac arrhythmia using kernel difference weighted knn classifier. In: 2008 Computers in cardiology, IEEE, pp 253–256 Zuo W, Lu W, Wang K, Zhang H (2008) Diagnosis of cardiac arrhythmia using kernel difference weighted knn classifier. In: 2008 Computers in cardiology, IEEE, pp 253–256
40.
go back to reference Zur HH (2009) Papillomaviruses in the causation of human cancers—a brief historical account. Virol J 384(2):260–265CrossRef Zur HH (2009) Papillomaviruses in the causation of human cancers—a brief historical account. Virol J 384(2):260–265CrossRef
Metadata
Title
A whole-slide image grading benchmark and tissue classification for cervical cancer precursor lesions with inter-observer variability
Authors
Abdulkadir Albayrak
Asli Unlu Akhan
Nurullah Calik
Abdulkerim Capar
Gokhan Bilgin
Behcet Ugur Toreyin
Bahar Muezzinoglu
Ilknur Turkmen
Lutfiye Durak-Ata
Publication date
10-07-2021
Publisher
Springer Berlin Heidelberg
Published in
Medical & Biological Engineering & Computing / Issue 7-8/2021
Print ISSN: 0140-0118
Electronic ISSN: 1741-0444
DOI
https://doi.org/10.1007/s11517-021-02388-w

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