NuCLS: A scalable crowdsourcing approach and dataset for nucleus classification and segmentation in breast cancer

Author:

Amgad Mohamed1ORCID,Atteya Lamees A2,Hussein Hagar3,Mohammed Kareem Hosny4,Hafiz Ehab5ORCID,Elsebaie Maha A T6ORCID,Alhusseiny Ahmed M7ORCID,AlMoslemany Mohamed Atef8,Elmatboly Abdelmagid M9ORCID,Pappalardo Philip A10,Sakr Rokia Adel11ORCID,Mobadersany Pooya1ORCID,Rachid Ahmad12,Saad Anas M13ORCID,Alkashash Ahmad M14ORCID,Ruhban Inas A15,Alrefai Anas12,Elgazar Nada M16,Abdulkarim Ali17,Farag Abo-Alela12ORCID,Etman Amira8ORCID,Elsaeed Ahmed G16,Alagha Yahya17,Amer Yomna A8,Raslan Ahmed M18,Nadim Menatalla K19ORCID,Elsebaie Mai A T12,Ayad Ahmed20,Hanna Liza E3,Gadallah Ahmed12ORCID,Elkady Mohamed21ORCID,Drumheller Bradley22,Jaye David22ORCID,Manthey David23ORCID,Gutman David A24ORCID,Elfandy Habiba2526ORCID,Cooper Lee A D12728ORCID

Affiliation:

1. Department of Pathology, Northwestern University, 750 N Lake Shore Dr., Chicago, IL 60611, USA

2. Cairo Health Care Administration, Egyptian Ministry of Health, 3 Magles El Shaab Street, Cairo, Postal code 222, Egypt

3. Department of Pathology, Nasser institute for research and treatment, 3 Magles El Shaab Street, Cairo, Postal code 222, Egypt

4. Department of Pathology and Laboratory Medicine, University of Pennsylvania, 3620 Hamilton Walk M163, Philadelphia, PA 19104, USA

5. Department of Clinical Laboratory Research, Theodor Bilharz Research Institute, 1 El-Nile Street, Imbaba Warrak El-Hadar, Giza, Postal code 12411, Egypt

6. Department of Medicine, Cook County Hospital, 1969 W Ogden Ave, Chicago, IL 60612, USA

7. Department of Pathology, Baystate Medical Center, University of Massachusetts, 759 Chestnut St, Springfield, MA 01199, USA

8. Faculty of Medicine, Menoufia University, Gamal Abd El-Nasir, Qism Shebeen El-Kom, Shibin el Kom, Menofia Governorate, Postal code: 32511, Egypt

9. Faculty of Medicine, Al-Azhar University, 15 Mohammed Abdou, El-Darb El-Ahmar, Cairo Governorate, Postal code 11651, Egypt

10. Consultant for The Center for Applied Proteomics and Molecular Medicine (CAPMM), George Mason University, 10920 George Mason Circle Institute for Advanced Biomedical Research Room 2008, MS1A9 Manassas, Virginia 20110, USA

11. Department of Pathology, National Liver Institute, Gamal Abd El-Nasir, Qism Shebeen El-Kom, Shibin el Kom, Menofia Governorate, Postal code: 32511, Egypt

12. Faculty of Medicine, Ain Shams University, 38 Abbassia, Next to the Al-Nour Mosque, Cairo, Postal code: 1181, Egypt

13. Cleveland Clinic Foundation, 9500 Euclid Ave. Cleveland, Ohio 44195, USA

14. Department of Pathology, Indiana University, 635 Barnhill Drive Medical Science Building A-128 Indianapolis, IN 46202, USA

15. Faculty of Medicine, Damascus University, Damascus, Damaskus, PO Box 30621, Syria

16. Faculty of Medicine, Mansoura University, 1 El Gomhouria St, Dakahlia Governorate 35516, Egypt

17. Faculty of Medicine, Cairo University, Kasr Al Ainy Hospitals, Kasr Al Ainy St., Cairo, Postal code: 11562, Egypt

18. Department of Anaesthesia and Critical Care, Menoufia University Hospital, Gamal Abd El-Nasir, Qism Shebeen El-Kom, Shibin el Kom, Menofia Governorate, Postal code: 32511, Egypt

19. Department of Clinical Pathology, Ain Shams University, 38 Abbassia, Next to the Al-Nour Mosque, Cairo, Postal code: 1181, Egypt

20. Research Department, Oncology Consultants, 2130 W. Holcombe Blvd, 10th Floor, Houston, Texas 77030, USA

21. Siparadigm Diagnostic Informatics, 25 Riverside Dr no. 2, Pine Brook, NJ 07058, USA

22. Department of Pathology and Laboratory Medicine, Emory University School of Medicine, 201 Dowman Dr, Atlanta, GA 30322, USA

23. Kitware Inc., 1712 Route 9. Suite 300. Clifton Park, New York 12065, USA

24. Department of Neurology, Emory University School of Medicine, 201 Dowman Dr, Atlanta, GA 30322, USA

25. Department of Pathology, National Cancer Institute, Kasr Al Eini Street, Fom El Khalig, Cairo, Postal code: 11562, Egypt

26. Department of Pathology, Children’s Cancer Hospital Egypt (CCHE 57357), 1 Seket Al-Emam Street, El-Madbah El-Kadeem Yard, El-Saida Zenab, Cairo, Postal code: 11562, Egypt

27. Lurie Cancer Center, Northwestern University, 675 N St Clair St Fl 21 Ste 100, Chicago, IL 60611, USA

28. Center for Computational Imaging and Signal Analytics, Northwestern University Feinberg School of Medicine, 750 N Lake Shore Dr., Chicago, IL 60611, USA

Abstract

Abstract Background Deep learning enables accurate high-resolution mapping of cells and tissue structures that can serve as the foundation of interpretable machine-learning models for computational pathology. However, generating adequate labels for these structures is a critical barrier, given the time and effort required from pathologists. Results This article describes a novel collaborative framework for engaging crowds of medical students and pathologists to produce quality labels for cell nuclei. We used this approach to produce the NuCLS dataset, containing >220,000 annotations of cell nuclei in breast cancers. This builds on prior work labeling tissue regions to produce an integrated tissue region- and cell-level annotation dataset for training that is the largest such resource for multi-scale analysis of breast cancer histology. This article presents data and analysis results for single and multi-rater annotations from both non-experts and pathologists. We present a novel workflow that uses algorithmic suggestions to collect accurate segmentation data without the need for laborious manual tracing of nuclei. Our results indicate that even noisy algorithmic suggestions do not adversely affect pathologist accuracy and can help non-experts improve annotation quality. We also present a new approach for inferring truth from multiple raters and show that non-experts can produce accurate annotations for visually distinctive classes. Conclusions This study is the most extensive systematic exploration of the large-scale use of wisdom-of-the-crowd approaches to generate data for computational pathology applications.

Funder

National Institutes of Health

Publisher

Oxford University Press (OUP)

Subject

Computer Science Applications,Health Informatics

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