Journal Article
. 2009 Nov; 57(4):841-52.
doi: 10.1109/TBME.2009.2035102.

Improved automatic detection and segmentation of cell nuclei in histopathology images

Yousef Al-Kofahi 1 Wiem Lassoued  William Lee  Badrinath Roysam  
Affiliations
  • PMID: 19884070
  •     153 citations

Abstract

Automatic segmentation of cell nuclei is an essential step in image cytometry and histometry. Despite substantial progress, there is a need to improve accuracy, speed, level of automation, and adaptability to new applications. This paper presents a robust and accurate novel method for segmenting cell nuclei using a combination of ideas. The image foreground is extracted automatically using a graph-cuts-based binarization. Next, nuclear seed points are detected by a novel method combining multiscale Laplacian-of-Gaussian filtering constrained by distance-map-based adaptive scale selection. These points are used to perform an initial segmentation that is refined using a second graph-cuts-based algorithm incorporating the method of alpha expansions and graph coloring to reduce computational complexity. Nuclear segmentation results were manually validated over 25 representative images (15 in vitro images and 10 in vivo images, containing more than 7400 nuclei) drawn from diverse cancer histopathology studies, and four types of segmentation errors were investigated. The overall accuracy of the proposed segmentation algorithm exceeded 86%. The accuracy was found to exceed 94% when only over- and undersegmentation errors were considered. The confounding image characteristics that led to most detection/segmentation errors were high cell density, high degree of clustering, poor image contrast and noisy background, damaged/irregular nuclei, and poor edge information. We present an efficient semiautomated approach to editing automated segmentation results that requires two mouse clicks per operation.

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J Pathol Inform, 2018 Apr 06; 9. PMID: 29619277    Free PMC article.
Robust Cell Detection for Large-Scale 3D Microscopy Using GPU-Accelerated Iterative Voting.
Leila Saadatifard, Louise C Abbott, +2 authors, David Mayerich.
Front Neuroanat, 2018 May 15; 12. PMID: 29755325    Free PMC article.
Multi-tissue and multi-scale approach for nuclei segmentation in H&E stained images.
Massimo Salvi, Filippo Molinari.
Biomed Eng Online, 2018 Jun 22; 17(1). PMID: 29925379    Free PMC article.
Fusion of encoder-decoder deep networks improves delineation of multiple nuclear phenotypes.
Mina Khoshdeli, Garrett Winkelmaier, Bahram Parvin.
BMC Bioinformatics, 2018 Aug 09; 19(1). PMID: 30086715    Free PMC article.
Identifying the morphologic basis for radiomic features in distinguishing different Gleason grades of prostate cancer on MRI: Preliminary findings.
Gregory Penzias, Asha Singanamalli, +13 authors, Anant Madabhushi.
PLoS One, 2018 Sep 01; 13(8). PMID: 30169514    Free PMC article.
A deep learning-based algorithm for 2-D cell segmentation in microscopy images.
Yousef Al-Kofahi, Alla Zaltsman, +2 authors, Mirabela Rusu.
BMC Bioinformatics, 2018 Oct 05; 19(1). PMID: 30285608    Free PMC article.
Investigating the Relevance of Graph Cut Parameter on Interactive and Automatic Cell Segmentation.
Kazeem Oyeyemi Oyebode, Shengzhi Du, Barend Jacobus van Wyk, Karim Djouani.
Comput Math Methods Med, 2018 Oct 23; 2018. PMID: 30344617    Free PMC article.
Comparative Study on Automated Cell Nuclei Segmentation Methods for Cytology Pleural Effusion Images.
Khin Yadanar Win, Somsak Choomchuay, Kazuhiko Hamamoto, Manasanan Raveesunthornkiat.
J Healthc Eng, 2018 Oct 23; 2018. PMID: 30344991    Free PMC article.
Artificial intelligence in digital pathology - new tools for diagnosis and precision oncology.
Kaustav Bera, Kurt A Schalper, +2 authors, Anant Madabhushi.
Nat Rev Clin Oncol, 2019 Aug 11; 16(11). PMID: 31399699    Free PMC article.
Highly Cited. Review.
TDP-43 cytoplasmic inclusion formation is disrupted in C9orf72-associated amyotrophic lateral sclerosis/frontotemporal lobar degeneration.
Samuel M Lee, Seneshaw Asress, +7 authors, Jonathan D Glass.
Brain Commun, 2019 Oct 22; 1(1). PMID: 31633109    Free PMC article.
Automated Individualization of Size-Varying and Touching Neurons in Macaque Cerebral Microscopic Images.
Zhenzhen You, Yaël Balbastre, +6 authors, Thierry Delzescaux.
Front Neuroanat, 2020 Jan 11; 13. PMID: 31920567    Free PMC article.
Effective nuclei segmentation with sparse shape prior and dynamic occlusion constraint for glioblastoma pathology images.
Pengyue Zhang, Fusheng Wang, +4 authors, Jun Kong.
J Med Imaging (Bellingham), 2019 Mar 21; 6(1). PMID: 30891467    Free PMC article.
Segmentation of Heavily Clustered Nuclei from Histopathological Images.
Mahmoud Abdolhoseini, Murielle G Kluge, Frederick R Walker, Sarah J Johnson.
Sci Rep, 2019 Mar 16; 9(1). PMID: 30872619    Free PMC article.
Multiplexed (18-Plex) Measurement of Signaling Targets and Cytotoxic T Cells in Trastuzumab-Treated Patients using Imaging Mass Cytometry.
Daniel E Carvajal-Hausdorf, Jonathan Patsenker, +10 authors, David L Rimm.
Clin Cancer Res, 2019 Feb 24; 25(10). PMID: 30796036    Free PMC article.
Three-dimensional GPU-accelerated active contours for automated localization of cells in large images.
Mahsa Lotfollahi, Sebastian Berisha, +3 authors, David Mayerich.
PLoS One, 2019 Jun 08; 14(6). PMID: 31173591    Free PMC article.
Nessys: A new set of tools for the automated detection of nuclei within intact tissues and dense 3D cultures.
Guillaume Blin, Daina Sadurska, +3 authors, Sally Lowell.
PLoS Biol, 2019 Aug 10; 17(8). PMID: 31398189    Free PMC article.
DeepSynth: Three-dimensional nuclear segmentation of biological images using neural networks trained with synthetic data.
Kenneth W Dunn, Chichen Fu, +4 authors, Edward J Delp.
Sci Rep, 2019 Dec 05; 9(1). PMID: 31797882    Free PMC article.
Deep learning pathological microscopic features in endemic nasopharyngeal cancer: Prognostic value and protentional role for individual induction chemotherapy.
Kuiyuan Liu, Weixiong Xia, +4 authors, Xing Lv.
Cancer Med, 2019 Dec 21; 9(4). PMID: 31860791    Free PMC article.
Introduction to digital pathology and computer-aided pathology.
Soojeong Nam, Yosep Chong, +5 authors, Heounjeong Go.
J Pathol Transl Med, 2020 Feb 13; 54(2). PMID: 32045965    Free PMC article.
Review.
Nucleus segmentation of cervical cytology images based on multi-scale fuzzy clustering algorithm.
Jinjie Huang, Tao Wang, Dequan Zheng, Yongjun He.
Bioengineered, 2020 Apr 14; 11(1). PMID: 32279589    Free PMC article.
Spatial models of cell distribution in human lumbar dorsal root ganglia.
Zachariah J Sperry, Robert D Graham, +2 authors, Tim M Bruns.
J Comp Neurol, 2019 Dec 25; 528(10). PMID: 31872433    Free PMC article.
Computer-Assisted Nuclear Atypia Scoring of Breast Cancer: a Preliminary Study.
Ziba Gandomkar, Patrick C Brennan, Claudia Mello-Thoms.
J Digit Imaging, 2019 Feb 06; 32(5). PMID: 30719586    Free PMC article.
Identification of topological features in renal tumor microenvironment associated with patient survival.
Jun Cheng, Xiaokui Mo, +3 authors, Kun Huang.
Bioinformatics, 2017 Nov 15; 34(6). PMID: 29136101    Free PMC article.
Artificial intelligence in digital breast pathology: Techniques and applications.
Asmaa Ibrahim, Paul Gamble, +4 authors, Emad A Rakha.
Breast, 2020 Jan 15; 49. PMID: 31935669    Free PMC article.
Review.
An automatic nuclei segmentation method based on deep convolutional neural networks for histopathology images.
Hwejin Jung, Bilal Lodhi, Jaewoo Kang.
BMC Biomed Eng, 2020 Sep 10; 1. PMID: 32903361    Free PMC article.
Deep-learning-based accurate hepatic steatosis quantification for histological assessment of liver biopsies.
Mousumi Roy, Fusheng Wang, +6 authors, Jun Kong.
Lab Invest, 2020 Jul 15; 100(10). PMID: 32661341    Free PMC article.
Machine Learning Models for Multiparametric Glioma Grading With Quantitative Result Interpretations.
Xiuying Wang, Dingqian Wang, +7 authors, Yingchao Liu.
Front Neurosci, 2019 Jan 29; 12. PMID: 30686996    Free PMC article.
Convolutional neural network initialized active contour model with adaptive ellipse fitting for nuclear segmentation on breast histopathological images.
Jun Xu, Lei Gong, +4 authors, Anant Madabhushi.
J Med Imaging (Bellingham), 2019 Mar 07; 6(1). PMID: 30840729    Free PMC article.
Introduction to Digital Image Analysis in Whole-slide Imaging: A White Paper from the Digital Pathology Association.
Famke Aeffner, Mark D Zarella, +11 authors, Douglas Bowman.
J Pathol Inform, 2019 Apr 16; 10. PMID: 30984469    Free PMC article.
Highly Cited. Review.
Deep Learning for Semantic Segmentation vs. Classification in Computational Pathology: Application to Mitosis Analysis in Breast Cancer Grading.
Gabriel Jiménez, Daniel Racoceanu.
Front Bioeng Biotechnol, 2019 Jul 10; 7. PMID: 31281813    Free PMC article.
Multi-Organ Gland Segmentation Using Deep Learning.
Thomas Binder, El Mehdi Tantaoui, +3 authors, Maria Gabrani.
Front Med (Lausanne), 2019 Aug 21; 6. PMID: 31428614    Free PMC article.
Three-Dimensional Segmentation and Reconstruction of Neuronal Nuclei in Confocal Microscopic Images.
Błażej Ruszczycki, Katarzyna Karolina Pels, +12 authors, Grzegorz Marek Wilczyński.
Front Neuroanat, 2019 Sep 05; 13. PMID: 31481881    Free PMC article.
Detection and segmentation of morphologically complex eukaryotic cells in fluorescence microscopy images via feature pyramid fusion.
Nikolaus Korfhage, Markus Mühling, +3 authors, Bernd Freisleben.
PLoS Comput Biol, 2020 Sep 09; 16(9). PMID: 32898132    Free PMC article.
Multi-aspect testing and ranking inference to quantify dimorphism in the cytoarchitecture of cerebellum of male, female and intersex individuals: a model applied to bovine brains.
L Corain, E Grisan, +3 authors, A Peruffo.
Brain Struct Funct, 2020 Sep 30; 225(9). PMID: 32989472    Free PMC article.
Automatic segmentation and supervised learning-based selection of nuclei in cancer tissue images.
Kaustav Nandy, Prabhakar R Gudla, +3 authors, Stephen J Lockett.
Cytometry A, 2012 Aug 18; 81(9). PMID: 22899462    Free PMC article.
A novel computational method for automatic segmentation, quantification and comparative analysis of immunohistochemically labeled tissue sections.
Elena Casiraghi, Veronica Huber, +6 authors, Barbara Vergani.
BMC Bioinformatics, 2018 Oct 28; 19(Suppl 10). PMID: 30367588    Free PMC article.
Cell segmentation methods for label-free contrast microscopy: review and comprehensive comparison.
Tomas Vicar, Jan Balvan, +4 authors, Jaromir Gumulec.
BMC Bioinformatics, 2019 Jun 30; 20(1). PMID: 31253078    Free PMC article.
Review.
A deep learning algorithm for one-step contour aware nuclei segmentation of histopathology images.
Yuxin Cui, Guiying Zhang, +2 authors, Jianjun Hu.
Med Biol Eng Comput, 2019 Jul 28; 57(9). PMID: 31346949
Accurate Neuronal Soma Segmentation Using 3D Multi-Task Learning U-Shaped Fully Convolutional Neural Networks.
Tianyu Hu, Xiaofeng Xu, Shangbin Chen, Qian Liu.
Front Neuroanat, 2021 Feb 09; 14. PMID: 33551758    Free PMC article.
Whole-brain tissue mapping toolkit using large-scale highly multiplexed immunofluorescence imaging and deep neural networks.
Dragan Maric, Jahandar Jahanipour, +6 authors, Badrinath Roysam.
Nat Commun, 2021 Mar 12; 12(1). PMID: 33692351    Free PMC article.
Applications of Topological Data Analysis in Oncology.
Anuraag Bukkuri, Noemi Andor, Isabel K Darcy.
Front Artif Intell, 2021 May 01; 4. PMID: 33928240    Free PMC article.
Review.
Automatic wavelet-based 3D nuclei segmentation and analysis for multicellular embryo quantification.
Tzu-Ching Wu, Xu Wang, +2 authors, David M Umulis.
Sci Rep, 2021 May 12; 11(1). PMID: 33972575    Free PMC article.