Abstract

The amount and organization details of peri-tumoural stroma have been linked to patient outcomes in various cancers. In this study, we propose a novel and relatively simple methodology using polarized light microscopy (PLM) to image fibrillar structures within a tumour microenvironment, using only linear crossed polarizers. We demonstrate the technique’s ability to image and extract measurement-geometry-independent quantitative morphological metrics related to stromal density and alignment in human invasive breast cancer samples. The findings are promising towards quantitative characterization of peri-tumoural stroma, with potential to develop a PLM signature of tumour microenvironment for providing clinically important information such as breast cancer behaviour or treatment outcome prognosis.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2019 (4)

M. Van Bockstal, K. Lambein, A. Smeets, L. Slembrouck, P. Neven, I. Nevelsteen, C. Weltens, E. Van Limbergen, M. R. Christiaens, C. Van Ongeval, H. Wildiers, L. Libbrecht, and G. Floris, “Stromal characteristics are adequate prognosticators for recurrence risk in ductal carcinoma in situ of the breast,” Eur. J. Surg. Oncol. 45(4), 550–559 (2019).
[Crossref]

C. J. H. Kramer, K. M. H. Vangangelt, G. W. van Pelt, T. J. A. Dekker, R. A. E. M. Tollenaar, and W. E. Mesker, “The prognostic value of tumour–stroma ratio in primary breast cancer with special attention to triple-negative tumours: a review,” Breast Cancer Res. Treat. 173(1), 55–64 (2019).
[Crossref]

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
[Crossref]

X. C. Id, P. Simon, M. Jondet, and M. Vanhaeverbeek, “Quantification of stromal reaction in breast carcinoma and its correlation with tumor grade and free progression survival,” PLoS One 14(3), e0210263 (2019).
[Crossref]

2018 (1)

C. Jing, Y. Fu, J. Huang, M. Zhang, Y. Yi, W. Gan, X. Xu, H. Shen, J. Lin, S. Zheng, J. Zhang, J. Zhou, J. Fan, Z. Ren, S. Qiu, and B. Zhang, “Prognostic nomogram based on histological characteristics of fibrotic tumor stroma in patients who underwent curative resection for intrahepatic cholangiocarcinoma,” Oncologist 23(12), 1482–1493 (2018).
[Crossref]

2017 (1)

2016 (2)

L. M. Wang, M. A. Silva, Z. D’Costa, R. Bockelmann, Z. Soonawalla, S. Liu, E. O’Neill, S. Mukherjee, W. G. McKenna, R. Muschel, and E. Fokas, “The prognostic role of desmoplastic stroma in pancreatic ductal adenocarcinoma,” OncoTargets Ther. 7(4), 4183–4194 (2016).
[Crossref]

V. V. Tuchin, “Polarized light interaction with tissues,” J. Biomed. Opt. 21(7), 071114 (2016).
[Crossref]

2015 (1)

C. L. Downey, H. H. Thygesen, N. Sharma, and A. M. Shaaban, “Prognostic significance of tumour stroma ratio in inflammatory breast cancer,” SpringerPlus 4(1), 68 (2015).
[Crossref]

2014 (2)

F. J. A. Gujam, J. Edwards, Z. M. A. Mohammed, J. J. Going, and D. C. McMillan, “The relationship between the tumour stroma percentage, clinicopathological characteristics and outcome in patients with operable ductal breast cancer,” Br. J. Cancer 111(1), 157–165 (2014).
[Crossref]

C. L. Downey, S. A. Simpkins, J. White, D. L. Holliday, J. L. Jones, L. B. Jordan, J. Kulka, S. Pollock, S. S. Rajan, H. H. Thygesen, A. M. Hanby, and V. Speirs, “The prognostic significance of tumour-stroma ratio in oestrogen receptor-positive breast cancer,” Br. J. Cancer 110(7), 1744–1747 (2014).
[Crossref]

2013 (3)

M. R. Junttila and F. J. De Sauvage, “Influence of tumour micro-environment heterogeneity on therapeutic response,” Nature 501(7467), 346–354 (2013).
[Crossref]

N. M. Kalwani, C. A. Ong, A. C. Lysaght, S. J. Haward, G. H. McKinley, and K. M. Stankovic, “Quantitative polarized light microscopy of unstained mammalian cochlear sections,” J. Biomed. Opt. 18(2), 026021 (2013).
[Crossref]

S. B. Mehta, “Polarized light imaging of birefringence and diattenuation at high resolution and high sensitivity,” J. Opt. 15(9), 094007 (2013).
[Crossref]

2012 (3)

T. Morikawa, “Prognostic significance and molecular associations of tumor growth pattern in colorectal cancer,” Ann Surg Oncol 19(6), 1944–1953 (2012).
[Crossref]

M. W. Conklin and P. J. Keely, “Why the stroma matters in breast cancer: insights into breast cancer patient outcomes,” Cell Adhes. Migr. 6(3), 249–260 (2012).
[Crossref]

D. Hanahan and L. M. Coussens, “Accessories to the crime: functions of cells recruited to the tumor microenvironment,” Cancer Cell 21(3), 309–322 (2012).
[Crossref]

2011 (3)

E. M. De Kruijf, J. G. H. Van Nes, C. J. H. Van De Velde, H. Putter, V. T. H. B. M. Smit, G. J. Liefers, P. J. K. Kuppen, R. A. E. M. Tollenaar, and W. E. Mesker, “Tumor-stroma ratio in the primary tumor is a prognostic factor in early breast cancer patients, especially in triple-negative carcinoma patients,” Breast Cancer Res. Treat. 125(3), 687–696 (2011).
[Crossref]

N. Ghosh and A. Vitkin, “Tissue polarimetry: concepts, challenges, applications, and outlook,” J. Biomed. Opt. 16(11), 110801 (2011).
[Crossref]

M. F. G. Wood, N. Vurgun, M. A. Wallenburg, and I. A. Vitkin, “Effects of formalin fixation on tissue optical polarization properties,” Phys. Med. Biol. 56(8), N115–N122 (2011).
[Crossref]

2009 (2)

K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
[Crossref]

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

2007 (1)

W. E. Mesker, J. M. C. Junggeburt, K. Szuhai, P. de Heer, H. Morreau, H. J. Tanke, and R. A. E. M. Tollenaar, “The carcinoma-stromal ratio of colon carcinoma is an independent factor for survival compared to lymph node status and tumor stage,” Cell. Oncol. 29(5), 387–398 (2007).
[Crossref]

2004 (2)

H. Ueno, A. M. Jones, K. H. Wilkinson, J. R. Jass, and I. C. Talbot, “Histological categorisation of fibrotic cancer stroma in advanced rectal cancer,” Gut 53(4), 581–586 (2004).
[Crossref]

M. M. Mueller and N. E. Fusenig, “Friends or foes - Bipolar effects of the tumour stroma in cancer,” Nat. Rev. Cancer 4(11), 839–849 (2004).
[Crossref]

2002 (1)

U. Tatsuo, “Collagen fibers, reticular fibers and elastic fibers. A comprehensive understanding from a morphological viewpoint,” Arch. Histol. Cytol. 65(2), 109–126 (2002).
[Crossref]

1989 (1)

T. B. Halvorsen and E. Seimt, “Association between invasiveness, inflammatory reaction, desmoplasia and survival in colorectal cancer,” J. Clin. Pathol. 42(2), 162–166 (1989).
[Crossref]

1975 (1)

M. Wolman, “Polarized light microscopy as a tool of of diagnostic pathology,” J. Histochem. Cytochem. 23(1), 21–50 (1975).
[Crossref]

Aguet, M.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Anderle, P.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

André, S.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Becette, V.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Bergh, J.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Bibeau, F.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Blot, E.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Bockelmann, R.

L. M. Wang, M. A. Silva, Z. D’Costa, R. Bockelmann, Z. Soonawalla, S. Liu, E. O’Neill, S. Mukherjee, W. G. McKenna, R. Muschel, and E. Fokas, “The prognostic role of desmoplastic stroma in pancreatic ductal adenocarcinoma,” OncoTargets Ther. 7(4), 4183–4194 (2016).
[Crossref]

Bogaerts, J.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Bonnefoi, H.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Brain, E.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Cameron, D.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Campone, M.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
[Crossref]

Chen, D.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
[Crossref]

Chen, G.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
[Crossref]

Chen, J.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
[Crossref]

Chen, W.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
[Crossref]

Chi, L.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
[Crossref]

Christiaens, M. R.

M. Van Bockstal, K. Lambein, A. Smeets, L. Slembrouck, P. Neven, I. Nevelsteen, C. Weltens, E. Van Limbergen, M. R. Christiaens, C. Van Ongeval, H. Wildiers, L. Libbrecht, and G. Floris, “Stromal characteristics are adequate prognosticators for recurrence risk in ductal carcinoma in situ of the breast,” Eur. J. Surg. Oncol. 45(4), 550–559 (2019).
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K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
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L. M. Wang, M. A. Silva, Z. D’Costa, R. Bockelmann, Z. Soonawalla, S. Liu, E. O’Neill, S. Mukherjee, W. G. McKenna, R. Muschel, and E. Fokas, “The prognostic role of desmoplastic stroma in pancreatic ductal adenocarcinoma,” OncoTargets Ther. 7(4), 4183–4194 (2016).
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W. E. Mesker, J. M. C. Junggeburt, K. Szuhai, P. de Heer, H. Morreau, H. J. Tanke, and R. A. E. M. Tollenaar, “The carcinoma-stromal ratio of colon carcinoma is an independent factor for survival compared to lymph node status and tumor stage,” Cell. Oncol. 29(5), 387–398 (2007).
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E. M. De Kruijf, J. G. H. Van Nes, C. J. H. Van De Velde, H. Putter, V. T. H. B. M. Smit, G. J. Liefers, P. J. K. Kuppen, R. A. E. M. Tollenaar, and W. E. Mesker, “Tumor-stroma ratio in the primary tumor is a prognostic factor in early breast cancer patients, especially in triple-negative carcinoma patients,” Breast Cancer Res. Treat. 125(3), 687–696 (2011).
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M. R. Junttila and F. J. De Sauvage, “Influence of tumour micro-environment heterogeneity on therapeutic response,” Nature 501(7467), 346–354 (2013).
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C. J. H. Kramer, K. M. H. Vangangelt, G. W. van Pelt, T. J. A. Dekker, R. A. E. M. Tollenaar, and W. E. Mesker, “The prognostic value of tumour–stroma ratio in primary breast cancer with special attention to triple-negative tumours: a review,” Breast Cancer Res. Treat. 173(1), 55–64 (2019).
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P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
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F. J. A. Gujam, J. Edwards, Z. M. A. Mohammed, J. J. Going, and D. C. McMillan, “The relationship between the tumour stroma percentage, clinicopathological characteristics and outcome in patients with operable ductal breast cancer,” Br. J. Cancer 111(1), 157–165 (2014).
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K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
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Erler, J. T.

K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
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P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
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M. Van Bockstal, K. Lambein, A. Smeets, L. Slembrouck, P. Neven, I. Nevelsteen, C. Weltens, E. Van Limbergen, M. R. Christiaens, C. Van Ongeval, H. Wildiers, L. Libbrecht, and G. Floris, “Stromal characteristics are adequate prognosticators for recurrence risk in ductal carcinoma in situ of the breast,” Eur. J. Surg. Oncol. 45(4), 550–559 (2019).
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L. M. Wang, M. A. Silva, Z. D’Costa, R. Bockelmann, Z. Soonawalla, S. Liu, E. O’Neill, S. Mukherjee, W. G. McKenna, R. Muschel, and E. Fokas, “The prognostic role of desmoplastic stroma in pancreatic ductal adenocarcinoma,” OncoTargets Ther. 7(4), 4183–4194 (2016).
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K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
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W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
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C. Jing, Y. Fu, J. Huang, M. Zhang, Y. Yi, W. Gan, X. Xu, H. Shen, J. Lin, S. Zheng, J. Zhang, J. Zhou, J. Fan, Z. Ren, S. Qiu, and B. Zhang, “Prognostic nomogram based on histological characteristics of fibrotic tumor stroma in patients who underwent curative resection for intrahepatic cholangiocarcinoma,” Oncologist 23(12), 1482–1493 (2018).
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C. Jing, Y. Fu, J. Huang, M. Zhang, Y. Yi, W. Gan, X. Xu, H. Shen, J. Lin, S. Zheng, J. Zhang, J. Zhou, J. Fan, Z. Ren, S. Qiu, and B. Zhang, “Prognostic nomogram based on histological characteristics of fibrotic tumor stroma in patients who underwent curative resection for intrahepatic cholangiocarcinoma,” Oncologist 23(12), 1482–1493 (2018).
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K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
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K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
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Going, J. J.

F. J. A. Gujam, J. Edwards, Z. M. A. Mohammed, J. J. Going, and D. C. McMillan, “The relationship between the tumour stroma percentage, clinicopathological characteristics and outcome in patients with operable ductal breast cancer,” Br. J. Cancer 111(1), 157–165 (2014).
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Dennis H. Goldstein, Polarized Light (Marcel Dekker Inc, 2010).

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F. J. A. Gujam, J. Edwards, Z. M. A. Mohammed, J. J. Going, and D. C. McMillan, “The relationship between the tumour stroma percentage, clinicopathological characteristics and outcome in patients with operable ductal breast cancer,” Br. J. Cancer 111(1), 157–165 (2014).
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T. B. Halvorsen and E. Seimt, “Association between invasiveness, inflammatory reaction, desmoplasia and survival in colorectal cancer,” J. Clin. Pathol. 42(2), 162–166 (1989).
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D. Hanahan and L. M. Coussens, “Accessories to the crime: functions of cells recruited to the tumor microenvironment,” Cancer Cell 21(3), 309–322 (2012).
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Hanby, A. M.

C. L. Downey, S. A. Simpkins, J. White, D. L. Holliday, J. L. Jones, L. B. Jordan, J. Kulka, S. Pollock, S. S. Rajan, H. H. Thygesen, A. M. Hanby, and V. Speirs, “The prognostic significance of tumour-stroma ratio in oestrogen receptor-positive breast cancer,” Br. J. Cancer 110(7), 1744–1747 (2014).
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N. M. Kalwani, C. A. Ong, A. C. Lysaght, S. J. Haward, G. H. McKinley, and K. M. Stankovic, “Quantitative polarized light microscopy of unstained mammalian cochlear sections,” J. Biomed. Opt. 18(2), 026021 (2013).
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Holliday, D. L.

C. L. Downey, S. A. Simpkins, J. White, D. L. Holliday, J. L. Jones, L. B. Jordan, J. Kulka, S. Pollock, S. S. Rajan, H. H. Thygesen, A. M. Hanby, and V. Speirs, “The prognostic significance of tumour-stroma ratio in oestrogen receptor-positive breast cancer,” Br. J. Cancer 110(7), 1744–1747 (2014).
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C. Jing, Y. Fu, J. Huang, M. Zhang, Y. Yi, W. Gan, X. Xu, H. Shen, J. Lin, S. Zheng, J. Zhang, J. Zhou, J. Fan, Z. Ren, S. Qiu, and B. Zhang, “Prognostic nomogram based on histological characteristics of fibrotic tumor stroma in patients who underwent curative resection for intrahepatic cholangiocarcinoma,” Oncologist 23(12), 1482–1493 (2018).
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X. C. Id, P. Simon, M. Jondet, and M. Vanhaeverbeek, “Quantification of stromal reaction in breast carcinoma and its correlation with tumor grade and free progression survival,” PLoS One 14(3), e0210263 (2019).
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P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
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H. Ueno, A. M. Jones, K. H. Wilkinson, J. R. Jass, and I. C. Talbot, “Histological categorisation of fibrotic cancer stroma in advanced rectal cancer,” Gut 53(4), 581–586 (2004).
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P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
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W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
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C. Jing, Y. Fu, J. Huang, M. Zhang, Y. Yi, W. Gan, X. Xu, H. Shen, J. Lin, S. Zheng, J. Zhang, J. Zhou, J. Fan, Z. Ren, S. Qiu, and B. Zhang, “Prognostic nomogram based on histological characteristics of fibrotic tumor stroma in patients who underwent curative resection for intrahepatic cholangiocarcinoma,” Oncologist 23(12), 1482–1493 (2018).
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Jondet, M.

X. C. Id, P. Simon, M. Jondet, and M. Vanhaeverbeek, “Quantification of stromal reaction in breast carcinoma and its correlation with tumor grade and free progression survival,” PLoS One 14(3), e0210263 (2019).
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Jones, A. M.

H. Ueno, A. M. Jones, K. H. Wilkinson, J. R. Jass, and I. C. Talbot, “Histological categorisation of fibrotic cancer stroma in advanced rectal cancer,” Gut 53(4), 581–586 (2004).
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Jones, J. L.

C. L. Downey, S. A. Simpkins, J. White, D. L. Holliday, J. L. Jones, L. B. Jordan, J. Kulka, S. Pollock, S. S. Rajan, H. H. Thygesen, A. M. Hanby, and V. Speirs, “The prognostic significance of tumour-stroma ratio in oestrogen receptor-positive breast cancer,” Br. J. Cancer 110(7), 1744–1747 (2014).
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Jordan, L. B.

C. L. Downey, S. A. Simpkins, J. White, D. L. Holliday, J. L. Jones, L. B. Jordan, J. Kulka, S. Pollock, S. S. Rajan, H. H. Thygesen, A. M. Hanby, and V. Speirs, “The prognostic significance of tumour-stroma ratio in oestrogen receptor-positive breast cancer,” Br. J. Cancer 110(7), 1744–1747 (2014).
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Junggeburt, J. M. C.

W. E. Mesker, J. M. C. Junggeburt, K. Szuhai, P. de Heer, H. Morreau, H. J. Tanke, and R. A. E. M. Tollenaar, “The carcinoma-stromal ratio of colon carcinoma is an independent factor for survival compared to lymph node status and tumor stage,” Cell. Oncol. 29(5), 387–398 (2007).
[Crossref]

Junttila, M. R.

M. R. Junttila and F. J. De Sauvage, “Influence of tumour micro-environment heterogeneity on therapeutic response,” Nature 501(7467), 346–354 (2013).
[Crossref]

Kalwani, N. M.

N. M. Kalwani, C. A. Ong, A. C. Lysaght, S. J. Haward, G. H. McKinley, and K. M. Stankovic, “Quantitative polarized light microscopy of unstained mammalian cochlear sections,” J. Biomed. Opt. 18(2), 026021 (2013).
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Kass, L.

K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
[Crossref]

Keely, P. J.

M. W. Conklin and P. J. Keely, “Why the stroma matters in breast cancer: insights into breast cancer patient outcomes,” Cell Adhes. Migr. 6(3), 249–260 (2012).
[Crossref]

Keikhosravi, A.

Kramer, C. J. H.

C. J. H. Kramer, K. M. H. Vangangelt, G. W. van Pelt, T. J. A. Dekker, R. A. E. M. Tollenaar, and W. E. Mesker, “The prognostic value of tumour–stroma ratio in primary breast cancer with special attention to triple-negative tumours: a review,” Breast Cancer Res. Treat. 173(1), 55–64 (2019).
[Crossref]

Kulka, J.

C. L. Downey, S. A. Simpkins, J. White, D. L. Holliday, J. L. Jones, L. B. Jordan, J. Kulka, S. Pollock, S. S. Rajan, H. H. Thygesen, A. M. Hanby, and V. Speirs, “The prognostic significance of tumour-stroma ratio in oestrogen receptor-positive breast cancer,” Br. J. Cancer 110(7), 1744–1747 (2014).
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Kuppen, P. J. K.

E. M. De Kruijf, J. G. H. Van Nes, C. J. H. Van De Velde, H. Putter, V. T. H. B. M. Smit, G. J. Liefers, P. J. K. Kuppen, R. A. E. M. Tollenaar, and W. E. Mesker, “Tumor-stroma ratio in the primary tumor is a prognostic factor in early breast cancer patients, especially in triple-negative carcinoma patients,” Breast Cancer Res. Treat. 125(3), 687–696 (2011).
[Crossref]

Lakins, J. N.

K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
[Crossref]

Lambein, K.

M. Van Bockstal, K. Lambein, A. Smeets, L. Slembrouck, P. Neven, I. Nevelsteen, C. Weltens, E. Van Limbergen, M. R. Christiaens, C. Van Ongeval, H. Wildiers, L. Libbrecht, and G. Floris, “Stromal characteristics are adequate prognosticators for recurrence risk in ductal carcinoma in situ of the breast,” Eur. J. Surg. Oncol. 45(4), 550–559 (2019).
[Crossref]

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D. Layden, N. Ghosh, and A. Vitkin, “Quantitative polarimetry for tissue characterization and diagnosis,” in Advanced Biophotonics: Tissue Optical Sectioning (CRC Press, 2013), pp. 459–494.

Levental, K. R.

K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. T. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, and V. M. Weaver, “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell 139(5), 891–906 (2009).
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Li, G.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
[Crossref]

Li, K.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
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Libbrecht, L.

M. Van Bockstal, K. Lambein, A. Smeets, L. Slembrouck, P. Neven, I. Nevelsteen, C. Weltens, E. Van Limbergen, M. R. Christiaens, C. Van Ongeval, H. Wildiers, L. Libbrecht, and G. Floris, “Stromal characteristics are adequate prognosticators for recurrence risk in ductal carcinoma in situ of the breast,” Eur. J. Surg. Oncol. 45(4), 550–559 (2019).
[Crossref]

Liefers, G. J.

E. M. De Kruijf, J. G. H. Van Nes, C. J. H. Van De Velde, H. Putter, V. T. H. B. M. Smit, G. J. Liefers, P. J. K. Kuppen, R. A. E. M. Tollenaar, and W. E. Mesker, “Tumor-stroma ratio in the primary tumor is a prognostic factor in early breast cancer patients, especially in triple-negative carcinoma patients,” Breast Cancer Res. Treat. 125(3), 687–696 (2011).
[Crossref]

Lin, D.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
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Lin, J.

C. Jing, Y. Fu, J. Huang, M. Zhang, Y. Yi, W. Gan, X. Xu, H. Shen, J. Lin, S. Zheng, J. Zhang, J. Zhou, J. Fan, Z. Ren, S. Qiu, and B. Zhang, “Prognostic nomogram based on histological characteristics of fibrotic tumor stroma in patients who underwent curative resection for intrahepatic cholangiocarcinoma,” Oncologist 23(12), 1482–1493 (2018).
[Crossref]

Liu, S.

L. M. Wang, M. A. Silva, Z. D’Costa, R. Bockelmann, Z. Soonawalla, S. Liu, E. O’Neill, S. Mukherjee, W. G. McKenna, R. Muschel, and E. Fokas, “The prognostic role of desmoplastic stroma in pancreatic ductal adenocarcinoma,” OncoTargets Ther. 7(4), 4183–4194 (2016).
[Crossref]

Liu, W.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
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Liu, Y.

Liu, Z.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
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Lu, J.

W. Jiang, J. Yan, M. Fu, W. Liu, G. Li, K. Li, X. Zheng, S. Zhuo, J. Lu, D. Chen, N. Zuo, S. Xu, J. Chen, W. Chen, D. Lin, J. Sui, Z. Liu, L. Chi, and G. Chen, “Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer,” JAMA Surg. 154(3), e185249 (2019).
[Crossref]

Lysaght, A. C.

N. M. Kalwani, C. A. Ong, A. C. Lysaght, S. J. Haward, G. H. McKinley, and K. M. Stankovic, “Quantitative polarized light microscopy of unstained mammalian cochlear sections,” J. Biomed. Opt. 18(2), 026021 (2013).
[Crossref]

MacGrogan, G.

P. Farmer, H. Bonnefoi, P. Anderle, D. Cameron, P. Wirapati, V. Becette, S. André, M. Piccart, M. Campone, E. Brain, G. MacGrogan, T. Petit, J. Jassem, F. Bibeau, E. Blot, J. Bogaerts, M. Aguet, J. Bergh, R. Iggo, and M. Delorenzi, “A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer,” Nat. Med. 15(1), 68–74 (2009).
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Figures (3)

Fig. 1.
Fig. 1. Signal processing workflow showing various types of PLM images with improved contrast between tumour and intratumoural stroma, using an invasive human ductal carcinoma as an illustrative example. A) A single cross polarization image at 20x magnification. Only stroma aligned at certain orientations can be seen; other structures, possibly in the tumour cellular compartment, are also visible. The contrast between the two tissue types is modest. B) The relative intensity as a function of measurement angle for a representative pixel of stromal and tumour tissues (blue and red arrows in A), respectively) Stroma contains fibrous structures that are birefringent, so the intensity of pixels corresponding to these areas is higher and varies significantly; conversely, tumour regions are less birefringent and more random / heterogenous, with resultant intensities and its variation significantly lower. C) A standard deviation (SD) image of the angular oscillations in B), now yielding a higher-contrast, measurement-angle-independent image compared to A). Certain stromal regions become more visible while the brightness of others (tumour cellular compartment) is diminished. D) A direction image where the colour at each pixel (derived from the polarizer measurement angle that yielded the highest intensity) displays the relative fibre orientation at that pixel. E) An alignment image derived from D), based on the amount of directional variation in nearest-neighbour pixels (for details, see text). F) Corresponding H&E histology, with stromal regions in pink reddish hues, and tumoural masses in darker purple. Good qualitative agreement is seen with the derived parametric PLM images of stromal density in C) and stromal alignment in E). The 2 mm scale bar in F) applies to all images in this figure.
Fig. 2.
Fig. 2. PLM can differentiate regions of low and high stromal density in human breast cancer samples. Following Fig. 1(c)., an illustrative example of breast stroma from a case of human invasive ductal carcinoma slide is shown, designated as Slide 5 in Table 1. A) PLM density image containing regions of low-density stroma. B) H&E histology image from an adjacent section. The red square ROI is chosen by a pathologist, blinded to the polarization images, to indicate an area of low stromal density. This is projected to the PLM density image as the dotted green square in A) for quantification, with results summarized in Table 1. C) PLM density image of an area containing high density stroma. D) Corresponding H&E histology image with a pathologist-marked ROI to indicate a region of high-density stroma, projected as the dotted green square in C).
Fig. 3.
Fig. 3. PLM can differentiate regions of low and high stromal alignment in human breast cancer samples. Following Fig. 1(e)., an illustrative example of breast stroma from a case of human invasive ductal carcinoma slide is shown, designated as Slide 1 in Table 1. A) PLM alignment image containing regions of low-alignment stroma. B) H&E histology image from an adjacent section. The red square ROI is chosen by a pathologist, blinded to the polarization images, to indicate an area of low stromal alignment. This is projected to the PLM alignment image as the dotted green square in A) for quantification, with results summarized in Table 1. C) PLM alignment image of an area containing high-alignment stroma. D) Corresponding H&E histology image with a pathologist-marked ROI to indicate a region of high-alignment stroma, projected as the dotted green square in C).

Tables (1)

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Table 1. Pathologist categories versus PLM scores for density and alignment.

Equations (5)

Equations on this page are rendered with MathJax. Learn more.

L=100%×{sin2(2τ)×sin2[(Δn×tλ)×π]}
Lsin2(2τ)
angulardifference=min{mod[(θ1θ2),180],mod[(θ1θ2),180]}
meananglulardifference=i=1n1j=i+1nangulardifferenceijn(n1)2
Δn=sin1(L100%)×λt×π

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