Prognostic value of histopathological DCIS features in a large-scale international interrater reliability study

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Abstract

Purpose

For optimal management of ductal carcinoma in situ (DCIS), reproducible histopathological assessment is essential to distinguish low-risk from high-risk DCIS. Therefore, we analyzed interrater reliability of histopathological DCIS features and assessed their associations with subsequent ipsilateral invasive breast cancer (iIBC) risk.

Methods

Using a case-cohort design, reliability was assessed in a population-based, nationwide cohort of 2767 women with screen-detected DCIS diagnosed between 1993 and 2004, treated by breast-conserving surgery with/without radiotherapy (BCS ± RT) using Krippendorff’s alpha (KA) and Gwet’s AC2 (GAC2). Thirty-eight raters scored histopathological DCIS features including grade (2-tiered and 3-tiered), growth pattern, mitotic activity, periductal fibrosis, and lymphocytic infiltrate in 342 women. Using majority opinion-based scores for each feature, their association with subsequent iIBC risk was assessed using Cox regression.

Results

Interrater reliability of grade using various classifications was fair to moderate, and only substantial for grade 1 versus 2 + 3 when using GAC2 (0.78). Reliability for growth pattern (KA 0.44, GAC2 0.78), calcifications (KA 0.49, GAC2 0.70) and necrosis (KA 0.47, GAC2 0.70) was moderate using KA and substantial using GAC2; for (type of) periductal fibrosis and lymphocytic infiltrate fair to moderate estimates were found and for mitotic activity reliability was substantial using GAC2 (0.70). Only in patients treated with BCS-RT, high mitotic activity was associated with a higher iIBC risk in univariable analysis (Hazard Ratio (HR) 2.53, 95% Confidence Interval (95% CI) 1.05–6.11); grade 3 versus 1 + 2 (HR 2.64, 95% CI 1.35–5.14) and a cribriform/solid versus flat epithelial atypia/clinging/(micro)papillary growth pattern (HR 3.70, 95% CI 1.34–10.23) were independently associated with a higher iIBC risk.

Conclusions

Using majority opinion-based scores, DCIS grade, growth pattern, and mitotic activity are associated with iIBC risk in patients treated with BCS-RT, but interrater variability is substantial. Semi-quantitative grading, incorporating and separately evaluating nuclear pleomorphism, growth pattern, and mitotic activity, may improve the reliability and prognostic value of these features.

Electronic supplementary material

The online version of this article (10.1007/s10549-020-05816-x) contains supplementary material, which is available to authorized users.

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Most cited references 42

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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.

Ian Ellis, Robert Elston (1991)

Morphological assessment of the degree of differentiation has been shown in numerous studies to provide useful prognostic information in breast cancer, but until recently histological grading has not been accepted as a routine procedure, mainly because of perceived problems with reproducibility and consistency. In the Nottingham/Tenovus Primary Breast Cancer Study the most commonly used method, described by Bloom & Richardson, has been modified in order to make the criteria more objective. The revised technique involves semiquantitative evaluation of three morphological features--the percentage of tubule formation, the degree of nuclear pleomorphism and an accurate mitotic count using a defined field area. A numerical scoring system is used and the overall grade is derived from a summation of individual scores for the three variables: three grades of differentiation are used. Since 1973, over 2200 patients with primary operable breast cancer have been entered into a study of multiple prognostic factors. Histological grade, assessed in 1831 patients, shows a very strong correlation with prognosis; patients with grade I tumours have a significantly better survival than those with grade II and III tumours (P less than 0.0001). These results demonstrate that this method for histological grading provides important prognostic information and, if the grading protocol is followed consistently, reproducible results can be obtained. Histological grade forms part of the multifactorial Nottingham prognostic index, together with tumour size and lymph node stage, which is used to stratify individual patients for appropriate therapy.

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Histological Grading and Prognosis in Breast Cancer

H. J. G. Bloom, W W Richardson (1957)

Images Figs. 19-24 Figs. 7-12 Figs. 1-6 Figs. 13-18 Figs. 33-36 Figs. 25-29

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Pathology Databanking and Biobanking in The Netherlands, a Central Role for PALGA, the Nationwide Histopathology and Cytopathology Data Network and Archive

M. Casparie, A Tiebosch, A Burger … (2007)

Since 1991, a nationwide histopathology and cytopathology network and archive is in operation in The Netherlands under the name PALGA, encompassing all sixty-four pathology laboratories in The Netherlands. The overall system comprises decentralized systems at the participating laboratories, a central databank, and a dedicated communication and information exchange tool. Excerpts of all histopathology and cytopathology reports are generated automatically at the participating laboratories and transferred to the central databank. Both the decentralized systems and the central system perform checks on the quality and completeness of excerpts. Currently, about 42 million records on almost 10 million patients are stored in the central databank. Each excerpt contains patient identifiers, including demographic data and the so-called PALGA diagnosis. The latter is structured along five classification axes: topography, morphology, function, procedure, and diseases. All data transfer and communication occurs electronically with encryption of patient and laboratory identifiers. All excerpts are continuously available to all participating pathology laboratories, thus contributing to the quality of daily patient care. In addition, external parties may obtain permission to use data from the PALGA system, either on an ongoing basis or on the basis of a specific permission. Annually, 40 to 60 applications for permission to use PALGA data are submitted. Among external users are the Dutch cancer registry, population-based screening programs for cancer of the uterine cervix and breast cancer in The Netherlands, and individual investigators addressing a range of research questions. Many scientific papers and theses incorporating PALGA data have been published already. In conclusion, the PALGA system is a unique system that requires a minimal effort on the part of the participating laboratories, while providing them a powerful tool in their daily practices.

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Author and article information

Contributors

Jelle Wesseling:

ORCID: http://orcid.org/0000-0002-8940-2676

j.wesseling@nki.nl

: precision@nki.nl

Journal

Journal ID (nlm-ta): Breast Cancer Res Treat

Journal ID (iso-abbrev): Breast Cancer Res. Treat

Title: Breast Cancer Research and Treatment

Publisher: Springer US (New York )

ISSN (Print): 0167-6806

ISSN (Electronic): 1573-7217

Publication date (Electronic): 30 July 2020

Publication date PMC-release: 30 July 2020

Publication date (Print): 2020

Volume: 183

Issue: 3

Pages: 759-770

Affiliations

[1 ]GRID grid.430814.a, Department of Pathology, , Netherlands Cancer Institute – Antoni van Leeuwenhoek, ; Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands

[2 ]GRID grid.430814.a, Department of Research IT, , Netherlands Cancer Institute – Antoni van Leeuwenhoek, ; Amsterdam, The Netherlands

[3 ]GRID grid.430814.a, Department of Molecular Pathology, , Netherlands Cancer Institute – Antoni van Leeuwenhoek, ; Amsterdam, The Netherlands

[4 ]Department of Pathology, Oncology Hospital, Sofia, Bulgaria

[5 ]GRID grid.1649.a, ISNI 000000009445082X, Department of Clinical Pathology, , Sahlgrenska University Hospital, ; Gothenburg, Sweden

[6 ]GRID grid.412539.8, ISNI 0000 0004 0609 2284, The Fingerland Department of Pathology, , Charles University Medical Faculty and University Hospital Hradec Kralove, ; Hradec Kralove, Czech Republic

[7 ]GRID grid.412004.3, ISNI 0000 0004 0478 9977, Institute of Pathology and Molecular Pathology, , University Hospital Zurich, ; Zurich, Switzerland

[8 ]Atryshealth Co, S.L., Barcelona, Spain

[9 ]GRID grid.8404.8, ISNI 0000 0004 1757 2304, Division of Pathological Anatomy, Department of Health Sciences, , University of Florence, ; Florence, Italy

[10 ]GRID grid.413327.0, ISNI 0000 0004 0444 9008, Department of Pathology, , Canisius Wilhelmina Hospital, ; Nijmegen, The Netherlands

[11 ]GRID grid.411900.d, ISNI 0000 0004 0646 8325, Department of Pathology, , Herlev University Hospital, ; Herlev, Denmark

[12 ]GRID grid.7177.6, ISNI 0000000084992262, Department of Pathology, , Amsterdam University Medical Center, Location VUmc, ; Amsterdam, The Netherlands

[13 ]GRID grid.11804.3c, ISNI 0000 0001 0942 9821, 2nd Department of Pathology, , Semmelweis University, ; Budapest, Hungary

[14 ]GRID grid.418165.f, ISNI 0000 0004 0540 2543, Tumor Pathology Department, , Maria Sklodowska-Curie National Research Institute of Oncology, ; Gliwice Branch, Gliwice, Poland

[15 ]GRID grid.417773.1, ISNI 0000 0004 0501 2983, Symbiant Pathology Expert Centre, Location ZMC, ; Zaandam, The Netherlands

[16 ]Department of Pathology, Zuyderland Medical Center, Location Sittard-Geleen, Sittard-Geleen, The Netherlands

[17 ]GRID grid.413607.7, ISNI 0000 0004 0624 062X, Department of Pathology, , Gävle Hospital, ; Gävle, Sweden

[18 ]GRID grid.413649.d, ISNI 0000 0004 0396 5908, Department of Pathology, , Deventer Hospital, ; Deventer, The Netherlands

[19 ]GRID grid.11598.34, ISNI 0000 0000 8988 2476, Diagnostic and Research Institute of Pathology, , Medical University of Graz, ; Graz, Austria

[20 ]Laboratory for Pathology Dordrecht, Dordrecht, The Netherlands

[21 ]GRID grid.412966.e, ISNI 0000 0004 0480 1382, Department of Pathology and GROW School for Oncology and Developmental Biology, , Maastricht University Medical Centre, ; Maastricht, The Netherlands

[22 ]GRID grid.412751.4, ISNI 0000 0001 0315 8143, Department of Pathology and Laboratory Medicine, , St. Vincent’s University Hospital, ; Dublin, Ireland

[23 ]GRID grid.5596.f, ISNI 0000 0001 0668 7884, Laboratory of Translational Cell & Tissue Research, Department of Imaging and Pathology, , KU Leuven - University of Leuven, ; Leuven, Belgium

[24 ]GRID grid.410569.f, ISNI 0000 0004 0626 3338, Department of Pathology, , University Hospitals Leuven, ; Leuven, Belgium

[25 ]GRID grid.413169.8, ISNI 0000 0000 9715 0291, Department of Pathology, , Bács-Kiskun County Teaching Hospital, ; Kecskemét, Hungary

[26 ]GRID grid.9008.1, ISNI 0000 0001 1016 9625, Department of Pathology, , University of Szeged, ; Szeged, Hungary

[27 ]GRID grid.7692.a, ISNI 0000000090126352, Department of Pathology, , University Medical Center Utrecht, ; Utrecht, The Netherlands

[28 ]GRID grid.430814.a, Division of Psychosocial Research and Epidemiology, , Netherlands Cancer Institute – Antoni van Leeuwenhoek, ; Amsterdam, The Netherlands

Author information

Jelle Wesseling http://orcid.org/0000-0002-8940-2676

Article

Publisher ID: 5816

DOI: 10.1007/s10549-020-05816-x

PMC ID: 7497690

PubMed ID: 32734520

SO-VID: adb9633b-4b32-4ebd-a3e9-5280508fa983

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 25 April 2020

Date accepted : 17 July 2020

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100004622, KWF Kankerbestrijding;

Award ID: NKI2014-7167

Award Recipient : Jelle Wesseling

Funded by: Cancer Research UK and KWF Kankerbestrijding in a joint grant

Award ID: C38317/A24043

Award Recipient : Jelle Wesseling

Custom metadata

ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: ductal carcinoma in situ,invasive breast cancer,interrater reliability,risk stratification

Data availability:

ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: ductal carcinoma in situ, invasive breast cancer, interrater reliability, risk stratification

Prognostic value of histopathological DCIS features in a large-scale international interrater reliability study

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Most cited references 42

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.

Histological Grading and Prognosis in Breast Cancer

Pathology Databanking and Biobanking in The Netherlands, a Central Role for PALGA, the Nationwide Histopathology and Cytopathology Data Network and Archive

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