A Novel Algorithm for Evaluating Bone Metastatic Potential of Breast Cancer through Morphometry and Computational Mathematics

Bone metastases represent about 70% of breast cancer metastases and are associated with worse prognosis as the tumor cells acquire more aggressive features. The selection and investigation of patients with a high risk of developing bone metastasis would have a significant impact on patients’ managem...

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Published inDiagnostics (Basel) Vol. 13; no. 21; p. 3338
Main Authors Duca-Barbu, Simona-Alina, Bratei, Alexandru Adrian, Lisievici, Antonia-Carmen, Georgescu, Tiberiu Augustin, Nemes, Bianca Mihaela, Sajin, Maria, Pop, Florinel
Format Journal Article
LanguageEnglish
Published Basel MDPI AG 01.10.2023
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ISSN2075-4418
2075-4418
DOI10.3390/diagnostics13213338

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Abstract Bone metastases represent about 70% of breast cancer metastases and are associated with worse prognosis as the tumor cells acquire more aggressive features. The selection and investigation of patients with a high risk of developing bone metastasis would have a significant impact on patients’ management and survival. The patients were selected from the database of Carol Davila Clinical Nephrology Hospital of Bucharest. Their tumor specimens were pathologically processed, and a representative area was selected. This area was scanned using an Olympus VS200 slide scanner and further analyzed using QuPath software v0.4.4. A representative group of approximately 60–100 tumor cells was selected from each section, for which the following parameters were analyzed: nuclear area, nuclear perimeter, long axis and cell surface. Starting from these measurements, the following were calculated: the mean nuclear area and mean nuclear volume, the nucleus to cytoplasm ratio, the length of the two axes, the long axis to short axis ratio, the acyclicity and anellipticity grade and the mean internuclear distance. The tumor cells belonging to patients known to have bone metastasis seemed to have a lower nuclear area (<55 µm2, p = 0.0035), smaller long axis (<9 µm, p = 0.0015), smaller values for the small axis (<7 µm, p = 0.0008), smaller mean nuclear volume (<200 µm3, p = 0.0146) and lower mean internuclear distance (<10.5 µm, p = 0.0007) but a higher nucleus to cytoplasm ratio (>1.1, p = 0.0418), higher axis ratio (>1.2, p = 0.088), higher acyclicity grade (>1.145, p = 0.0857) and higher anellipticity grade (>1.14, p = 0.1362). These parameters can be used for the evaluation of risk category of developing bone metastases. These results can be useful for the evaluation of bone metastatic potential of breast cancer and for the selection of high-risk patients whose molecular profiles would require further investigations and evaluation.
AbstractList Bone metastases represent about 70% of breast cancer metastases and are associated with worse prognosis as the tumor cells acquire more aggressive features. The selection and investigation of patients with a high risk of developing bone metastasis would have a significant impact on patients’ management and survival. The patients were selected from the database of Carol Davila Clinical Nephrology Hospital of Bucharest. Their tumor specimens were pathologically processed, and a representative area was selected. This area was scanned using an Olympus VS200 slide scanner and further analyzed using QuPath software v0.4.4. A representative group of approximately 60–100 tumor cells was selected from each section, for which the following parameters were analyzed: nuclear area, nuclear perimeter, long axis and cell surface. Starting from these measurements, the following were calculated: the mean nuclear area and mean nuclear volume, the nucleus to cytoplasm ratio, the length of the two axes, the long axis to short axis ratio, the acyclicity and anellipticity grade and the mean internuclear distance. The tumor cells belonging to patients known to have bone metastasis seemed to have a lower nuclear area (<55 µm[sup.2], p = 0.0035), smaller long axis (<9 µm, p = 0.0015), smaller values for the small axis (<7 µm, p = 0.0008), smaller mean nuclear volume (<200 µm[sup.3], p = 0.0146) and lower mean internuclear distance (<10.5 µm, p = 0.0007) but a higher nucleus to cytoplasm ratio (>1.1, p = 0.0418), higher axis ratio (>1.2, p = 0.088), higher acyclicity grade (>1.145, p = 0.0857) and higher anellipticity grade (>1.14, p = 0.1362). These parameters can be used for the evaluation of risk category of developing bone metastases. These results can be useful for the evaluation of bone metastatic potential of breast cancer and for the selection of high-risk patients whose molecular profiles would require further investigations and evaluation.
Bone metastases represent about 70% of breast cancer metastases and are associated with worse prognosis as the tumor cells acquire more aggressive features. The selection and investigation of patients with a high risk of developing bone metastasis would have a significant impact on patients' management and survival. The patients were selected from the database of Carol Davila Clinical Nephrology Hospital of Bucharest. Their tumor specimens were pathologically processed, and a representative area was selected. This area was scanned using an Olympus VS200 slide scanner and further analyzed using QuPath software v0.4.4. A representative group of approximately 60-100 tumor cells was selected from each section, for which the following parameters were analyzed: nuclear area, nuclear perimeter, long axis and cell surface. Starting from these measurements, the following were calculated: the mean nuclear area and mean nuclear volume, the nucleus to cytoplasm ratio, the length of the two axes, the long axis to short axis ratio, the acyclicity and anellipticity grade and the mean internuclear distance. The tumor cells belonging to patients known to have bone metastasis seemed to have a lower nuclear area (<55 µm2, p = 0.0035), smaller long axis (<9 µm, p = 0.0015), smaller values for the small axis (<7 µm, p = 0.0008), smaller mean nuclear volume (<200 µm3, p = 0.0146) and lower mean internuclear distance (<10.5 µm, p = 0.0007) but a higher nucleus to cytoplasm ratio (>1.1, p = 0.0418), higher axis ratio (>1.2, p = 0.088), higher acyclicity grade (>1.145, p = 0.0857) and higher anellipticity grade (>1.14, p = 0.1362). These parameters can be used for the evaluation of risk category of developing bone metastases. These results can be useful for the evaluation of bone metastatic potential of breast cancer and for the selection of high-risk patients whose molecular profiles would require further investigations and evaluation.Bone metastases represent about 70% of breast cancer metastases and are associated with worse prognosis as the tumor cells acquire more aggressive features. The selection and investigation of patients with a high risk of developing bone metastasis would have a significant impact on patients' management and survival. The patients were selected from the database of Carol Davila Clinical Nephrology Hospital of Bucharest. Their tumor specimens were pathologically processed, and a representative area was selected. This area was scanned using an Olympus VS200 slide scanner and further analyzed using QuPath software v0.4.4. A representative group of approximately 60-100 tumor cells was selected from each section, for which the following parameters were analyzed: nuclear area, nuclear perimeter, long axis and cell surface. Starting from these measurements, the following were calculated: the mean nuclear area and mean nuclear volume, the nucleus to cytoplasm ratio, the length of the two axes, the long axis to short axis ratio, the acyclicity and anellipticity grade and the mean internuclear distance. The tumor cells belonging to patients known to have bone metastasis seemed to have a lower nuclear area (<55 µm2, p = 0.0035), smaller long axis (<9 µm, p = 0.0015), smaller values for the small axis (<7 µm, p = 0.0008), smaller mean nuclear volume (<200 µm3, p = 0.0146) and lower mean internuclear distance (<10.5 µm, p = 0.0007) but a higher nucleus to cytoplasm ratio (>1.1, p = 0.0418), higher axis ratio (>1.2, p = 0.088), higher acyclicity grade (>1.145, p = 0.0857) and higher anellipticity grade (>1.14, p = 0.1362). These parameters can be used for the evaluation of risk category of developing bone metastases. These results can be useful for the evaluation of bone metastatic potential of breast cancer and for the selection of high-risk patients whose molecular profiles would require further investigations and evaluation.
Bone metastases represent about 70% of breast cancer metastases and are associated with worse prognosis as the tumor cells acquire more aggressive features. The selection and investigation of patients with a high risk of developing bone metastasis would have a significant impact on patients’ management and survival. The patients were selected from the database of Carol Davila Clinical Nephrology Hospital of Bucharest. Their tumor specimens were pathologically processed, and a representative area was selected. This area was scanned using an Olympus VS200 slide scanner and further analyzed using QuPath software v0.4.4. A representative group of approximately 60–100 tumor cells was selected from each section, for which the following parameters were analyzed: nuclear area, nuclear perimeter, long axis and cell surface. Starting from these measurements, the following were calculated: the mean nuclear area and mean nuclear volume, the nucleus to cytoplasm ratio, the length of the two axes, the long axis to short axis ratio, the acyclicity and anellipticity grade and the mean internuclear distance. The tumor cells belonging to patients known to have bone metastasis seemed to have a lower nuclear area (<55 µm2, p = 0.0035), smaller long axis (<9 µm, p = 0.0015), smaller values for the small axis (<7 µm, p = 0.0008), smaller mean nuclear volume (<200 µm3, p = 0.0146) and lower mean internuclear distance (<10.5 µm, p = 0.0007) but a higher nucleus to cytoplasm ratio (>1.1, p = 0.0418), higher axis ratio (>1.2, p = 0.088), higher acyclicity grade (>1.145, p = 0.0857) and higher anellipticity grade (>1.14, p = 0.1362). These parameters can be used for the evaluation of risk category of developing bone metastases. These results can be useful for the evaluation of bone metastatic potential of breast cancer and for the selection of high-risk patients whose molecular profiles would require further investigations and evaluation.
Audience Academic
Author Pop, Florinel
Georgescu, Tiberiu Augustin
Nemes, Bianca Mihaela
Sajin, Maria
Lisievici, Antonia-Carmen
Duca-Barbu, Simona-Alina
Bratei, Alexandru Adrian
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Cites_doi 10.1177/1178223419830978
10.1007/s10585-017-9871-9
10.1038/s41598-017-17204-5
10.21037/apm-21-438
10.1200/JCO.2005.03.111
10.1038/s41568-019-0213-x
10.1158/1055-9965.EPI-08-1082
10.1007/978-3-030-20301-6_7
10.1016/j.molonc.2010.04.004
10.1038/srep45411
10.1634/theoncologist.2018-0085
10.1038/s41416-020-01161-4
10.1158/1078-0432.CCR-06-0931
10.18632/oncotarget.15856
10.18632/oncotarget.14300
10.1007/s10555-006-9032-0
10.3332/ecancer.2017.715
10.3322/caac.21660
10.3390/ijms23126806
10.1016/j.jbo.2013.09.001
10.1111/j.1365-2559.1982.tb02727.x
10.4137/CPath.S31563
10.1038/35021093
10.1038/s41523-018-0054-x
10.4103/0970-9371.197591
10.3390/cancers13174310
10.3390/cells10061377
10.32074/1591-951X-1-20
10.2147/CMAR.S155524
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References Parkes (ref_27) 2018; 4
Wu (ref_30) 2017; 8
ref_14
Xiong (ref_24) 2018; 10
Baak (ref_34) 1981; 2
ref_12
ref_10
Jin (ref_19) 2015; 9
Kashyap (ref_36) 2017; 34
Weigelt (ref_8) 2010; 4
Gong (ref_29) 2017; 7
Makki (ref_1) 2015; 8
ref_18
Huanmei (ref_37) 2021; 10
ref_15
Eheman (ref_11) 2009; 18
Tahara (ref_7) 2019; 1152
Parkes (ref_28) 2018; 23
Pratap (ref_22) 2006; 25
Kuchuk (ref_25) 2013; 2
Pulido (ref_39) 2017; 11
Press (ref_32) 2017; 34
Riggio (ref_23) 2021; 124
Cristofanilli (ref_16) 2005; 23
ref_21
Yazdani (ref_38) 2019; 13
Perou (ref_17) 2000; 406
Baak (ref_35) 1982; 6
ref_3
Sung (ref_6) 2021; 71
ref_2
Cserni (ref_13) 2020; 112
ref_9
Coleman (ref_26) 2006; 12
Bankhead (ref_33) 2017; 7
ref_5
Wang (ref_31) 2016; 8
ref_4
Williams (ref_20) 2019; 19
References_xml – ident: ref_9
– volume: 13
  start-page: 1178223419830978
  year: 2019
  ident: ref_38
  article-title: Bone Metastasis Prognostic Factors in Breast Cancer
  publication-title: Breast Cancer
  doi: 10.1177/1178223419830978
– ident: ref_3
– volume: 34
  start-page: 457
  year: 2017
  ident: ref_32
  article-title: De novo metastasis in breast cancer: Occurrence and overall survival stratified by molecular subtype
  publication-title: Clin. Exp. Metastasis.
  doi: 10.1007/s10585-017-9871-9
– volume: 7
  start-page: 16878
  year: 2017
  ident: ref_33
  article-title: QuPath: Open source software for digital pathology image analysis
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-017-17204-5
– volume: 10
  start-page: 4435
  year: 2021
  ident: ref_37
  article-title: Factors associated with bone metastasis in breast cancer: A systematic review and meta-analysis
  publication-title: Ann. Palliat. Med.
  doi: 10.21037/apm-21-438
– volume: 23
  start-page: 41
  year: 2005
  ident: ref_16
  article-title: Invasive lobular carcinoma classic type: Response to primary chemotherapy and survival outcomes
  publication-title: J. Clin. Oncol.
  doi: 10.1200/JCO.2005.03.111
– volume: 19
  start-page: 716
  year: 2019
  ident: ref_20
  article-title: Controversies around epithelial-mesenchymal plasticity in cancer metastasis
  publication-title: Nat. Rev. Cancer
  doi: 10.1038/s41568-019-0213-x
– volume: 18
  start-page: 1763
  year: 2009
  ident: ref_11
  article-title: The changing incidence of in situ and invasive ductal and lobular breast carcinomas
  publication-title: Cancer Epidemiol. Biomarkers Prev.
  doi: 10.1158/1055-9965.EPI-08-1082
– volume: 1152
  start-page: 105
  year: 2019
  ident: ref_7
  article-title: Bone Metastasis of Breast Cancer
  publication-title: Adv. Exp. Med. Biol.
  doi: 10.1007/978-3-030-20301-6_7
– volume: 4
  start-page: 192
  year: 2010
  ident: ref_8
  article-title: Histological types of breast cancer: How special are they?
  publication-title: Mol. Oncol.
  doi: 10.1016/j.molonc.2010.04.004
– ident: ref_14
– volume: 2
  start-page: 351
  year: 1981
  ident: ref_34
  article-title: Morphometry for the prognosis prediction in breast cancer
  publication-title: Lancet
– volume: 7
  start-page: 45411
  year: 2017
  ident: ref_29
  article-title: Impact of molecular subtypes on metastatic breast cancer patients: A SEER population-based study
  publication-title: Sci. Rep.
  doi: 10.1038/srep45411
– volume: 23
  start-page: 1282
  year: 2018
  ident: ref_28
  article-title: Prognostic Factors in Patients with Metastatic Breast Cancer with Bone-Only Metastases
  publication-title: Oncologist
  doi: 10.1634/theoncologist.2018-0085
– volume: 124
  start-page: 13
  year: 2021
  ident: ref_23
  article-title: The lingering mysteries of metastatic recurrence in breast cancer
  publication-title: Br. J. Cancer
  doi: 10.1038/s41416-020-01161-4
– ident: ref_4
– ident: ref_2
– volume: 12
  start-page: 6243
  year: 2006
  ident: ref_26
  article-title: Clinical Features of Metastatic Bone Disease and Risk of Skeletal Morbidity
  publication-title: Clin. Cancer Res.
  doi: 10.1158/1078-0432.CCR-06-0931
– ident: ref_12
– volume: 8
  start-page: 27990
  year: 2017
  ident: ref_30
  article-title: Breast cancer subtypes predict the preferential site of distant metastases: A SEER based study
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.15856
– volume: 8
  start-page: 26368
  year: 2016
  ident: ref_31
  article-title: The prognosis analysis of different metastasis pattern in patients with different breast cancer subtypes: A SEER based study
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.14300
– ident: ref_10
– volume: 25
  start-page: 589
  year: 2006
  ident: ref_22
  article-title: Regulatory roles of Runx2 in metastatic tumor and cancer cell interactions with bone
  publication-title: Cancer Metastasis Rev.
  doi: 10.1007/s10555-006-9032-0
– volume: 11
  start-page: 715
  year: 2017
  ident: ref_39
  article-title: Bone metastasis risk factors in breast cancer
  publication-title: Ecancermedicalscience
  doi: 10.3332/ecancer.2017.715
– volume: 71
  start-page: 209
  year: 2021
  ident: ref_6
  article-title: Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries
  publication-title: CA Cancer J. Clin.
  doi: 10.3322/caac.21660
– ident: ref_18
  doi: 10.3390/ijms23126806
– volume: 9
  start-page: 23
  year: 2015
  ident: ref_19
  article-title: Targeting Breast Cancer Metastasis
  publication-title: Breast Cancer
– volume: 2
  start-page: 137
  year: 2013
  ident: ref_25
  article-title: Incidence, consequences and treatment of bone metastases in breast cancer patients—Experience from a single cancer centre
  publication-title: J. Bone Oncol.
  doi: 10.1016/j.jbo.2013.09.001
– ident: ref_15
– volume: 6
  start-page: 327
  year: 1982
  ident: ref_35
  article-title: Prognostic indicators in breast cancer—Morphometric methods
  publication-title: Histopathology
  doi: 10.1111/j.1365-2559.1982.tb02727.x
– volume: 8
  start-page: 23
  year: 2015
  ident: ref_1
  article-title: Diversity of Breast Carcinoma: Histological Subtypes and Clinical Relevance
  publication-title: Clin. Med. Insights Pathol.
  doi: 10.4137/CPath.S31563
– volume: 406
  start-page: 747
  year: 2000
  ident: ref_17
  article-title: Molecular portraits of human breast tumours
  publication-title: Nature
  doi: 10.1038/35021093
– volume: 4
  start-page: 1
  year: 2018
  ident: ref_27
  article-title: Characterization of bone only metastasis patients with respect to tumor subtypes
  publication-title: NPJ Breast Cancer
  doi: 10.1038/s41523-018-0054-x
– volume: 34
  start-page: 10
  year: 2017
  ident: ref_36
  article-title: Study of nuclear morphometry on cytology specimens of benign and malignant breast lesions: A study of 122 cases
  publication-title: J. Cytol.
  doi: 10.4103/0970-9371.197591
– ident: ref_21
  doi: 10.3390/cancers13174310
– ident: ref_5
  doi: 10.3390/cells10061377
– volume: 112
  start-page: 25
  year: 2020
  ident: ref_13
  article-title: Histological type and typing of breast carcinomas and the WHO classification changes over time
  publication-title: Pathologica
  doi: 10.32074/1591-951X-1-20
– volume: 10
  start-page: 287
  year: 2018
  ident: ref_24
  article-title: Bone metastasis pattern in initial metastatic breast cancer: A population-based study
  publication-title: Cancer Manag. Res.
  doi: 10.2147/CMAR.S155524
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Snippet Bone metastases represent about 70% of breast cancer metastases and are associated with worse prognosis as the tumor cells acquire more aggressive features....
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SubjectTerms Algorithms
bone metastasis
Breast cancer
Cancer therapies
Computational mathematics
Cytoplasm
Denosumab
digital pathology
Endocrine therapy
Fractures
Medical prognosis
Metastasis
Quality of life
tumor morphometry
Tumors
Womens health
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