Abstract

Digital Holography (DH) in microscopic configuration is a powerful tool for the imaging of micro-objects contained into a three dimensional (3D) volume, by a single-shot image acquisition. Many studies report on the ability of DH to track particle, microorganism and cells in 3D. However, very few investigations are performed with objects that change severely their morphology during the observation period. Here we study DH as a tool for 3D tracking an osteosarcoma cell line for which extensive changes in cell morphology are associated to cell motion. Due to the great unpredictable morphological change, retrieving cell’s position in 3D can become a complicated issue. We investigate and discuss in this paper how the tridimensional position can be affected by the continuous change of the cells. Moreover we propose and test some strategies to afford the problems and compare it with others approaches. Finally, results on the 3D tracking and comments are reported and illustrated.

© 2012 OSA

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2012

2011

2010

D. Guarnieri, A. De Capua, M. Ventre, A. Borzacchiello, C. Pedone, D. Marasco, M. Ruvo, and P. A. Netti, “Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters,” Acta Biomater.6(7), 2532–2539 (2010).
[CrossRef] [PubMed]

J. Persson, A. Mölder, S. G. Pettersson, and K. Alm, “Cell motility studies using digital holographic microscopy,” in Microscopy: Science, Technology, Applications and Education. Microscopy Series4, 1063–1072 (2010).

A. Aman and T. Piotrowski, “Cell migration during morphogenesis,” Dev. Biol.341(1), 20–33 (2010).
[CrossRef] [PubMed]

E. Van Goethem, R. Poincloux, F. Gauffre, I. Maridonneau-Parini, and V. Le Cabec, “Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures,” J. Immunol.184(2), 1049–1061 (2010).
[CrossRef] [PubMed]

2009

P. P. Provenzano, K. W. Eliceiri, and P. J. Keely, “Shining new light on 3D cell motility and the metastatic process,” Trends Cell Biol.19(11), 638–648 (2009).
[CrossRef] [PubMed]

M. Paturzo and P. Ferraro, “Creating an extended focus image of a tilted object in Fourier digital holography,” Opt. Express17(22), 20546–20552 (2009).
[CrossRef] [PubMed]

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

S. Lee, J. Y. Lee, W. Yang, and D. Y. Kim, “Autofocusing and edge detection schemes in cell volume measurements with quantitative phase microscopy,” Opt. Express17(8), 6476–6486 (2009).
[CrossRef] [PubMed]

2008

2006

2002

K. Schumacher, R. Strehl, U. de Vries, and W. W. Minuth, “Advanced technique for long term culture of epithelia in a continuous luminal-basal medium gradient,” Biomaterials23(3), 805–815 (2002).
[CrossRef] [PubMed]

Z. N. Demou and L. V. McIntire, “Fully automated three-dimensional tracking of cancer cells in collagen gels: determination of motility phenotypes at the cellular level,” Cancer Res.62(18), 5301–5307 (2002).
[PubMed]

1985

R. T. Franceschi, W. M. James, and G. Zerlauth, “1 alpha, 25-dihydroxyvitamin D3 specific regulation of growth, morphology, and fibronectin in a human osteosarcoma cell line,” J. Cell. Physiol.123(3), 401–409 (1985).
[CrossRef] [PubMed]

Alm, K.

J. Persson, A. Mölder, S. G. Pettersson, and K. Alm, “Cell motility studies using digital holographic microscopy,” in Microscopy: Science, Technology, Applications and Education. Microscopy Series4, 1063–1072 (2010).

Aman, A.

A. Aman and T. Piotrowski, “Cell migration during morphogenesis,” Dev. Biol.341(1), 20–33 (2010).
[CrossRef] [PubMed]

Bernhardt, I.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

Bianchi, M.

M. Ventre, F. Valle, M. Bianchi, F. Biscarini, and P. A. Netti, “Cell fluidics: producing cellular streams on micropatterned synthetic surfaces,” Langmuir28(1), 714–721 (2012).
[CrossRef] [PubMed]

Biscarini, F.

M. Ventre, F. Valle, M. Bianchi, F. Biscarini, and P. A. Netti, “Cell fluidics: producing cellular streams on micropatterned synthetic surfaces,” Langmuir28(1), 714–721 (2012).
[CrossRef] [PubMed]

Borzacchiello, A.

D. Guarnieri, A. De Capua, M. Ventre, A. Borzacchiello, C. Pedone, D. Marasco, M. Ruvo, and P. A. Netti, “Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters,” Acta Biomater.6(7), 2532–2539 (2010).
[CrossRef] [PubMed]

Callens, N.

De Capua, A.

D. Guarnieri, A. De Capua, M. Ventre, A. Borzacchiello, C. Pedone, D. Marasco, M. Ruvo, and P. A. Netti, “Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters,” Acta Biomater.6(7), 2532–2539 (2010).
[CrossRef] [PubMed]

de Vries, U.

K. Schumacher, R. Strehl, U. de Vries, and W. W. Minuth, “Advanced technique for long term culture of epithelia in a continuous luminal-basal medium gradient,” Biomaterials23(3), 805–815 (2002).
[CrossRef] [PubMed]

Demou, Z. N.

Z. N. Demou and L. V. McIntire, “Fully automated three-dimensional tracking of cancer cells in collagen gels: determination of motility phenotypes at the cellular level,” Cancer Res.62(18), 5301–5307 (2002).
[PubMed]

Dirksen, D.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

P. Langehanenberg, B. Kemper, D. Dirksen, and G. von Bally, “Autofocusing in digital holographic phase contrast microscopy on pure phase objects for live cell imaging,” Appl. Opt.47(19), D176–D182 (2008).
[CrossRef] [PubMed]

Distante, C.

Dubois, F.

El Mallahi, A.

Eliceiri, K. W.

P. P. Provenzano, K. W. Eliceiri, and P. J. Keely, “Shining new light on 3D cell motility and the metastatic process,” Trends Cell Biol.19(11), 638–648 (2009).
[CrossRef] [PubMed]

Esnaola, I.

Ferraro, P.

Finizio, A.

Franceschi, R. T.

R. T. Franceschi, W. M. James, and G. Zerlauth, “1 alpha, 25-dihydroxyvitamin D3 specific regulation of growth, morphology, and fibronectin in a human osteosarcoma cell line,” J. Cell. Physiol.123(3), 401–409 (1985).
[CrossRef] [PubMed]

Garcia-Sucerquia, J.

Gauffre, F.

E. Van Goethem, R. Poincloux, F. Gauffre, I. Maridonneau-Parini, and V. Le Cabec, “Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures,” J. Immunol.184(2), 1049–1061 (2010).
[CrossRef] [PubMed]

Georgiev, G.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

Guarnieri, D.

D. Guarnieri, A. De Capua, M. Ventre, A. Borzacchiello, C. Pedone, D. Marasco, M. Ruvo, and P. A. Netti, “Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters,” Acta Biomater.6(7), 2532–2539 (2010).
[CrossRef] [PubMed]

Hennelly, B. M.

Ivanova, L.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

James, W. M.

R. T. Franceschi, W. M. James, and G. Zerlauth, “1 alpha, 25-dihydroxyvitamin D3 specific regulation of growth, morphology, and fibronectin in a human osteosarcoma cell line,” J. Cell. Physiol.123(3), 401–409 (1985).
[CrossRef] [PubMed]

Javidi, B.

Keely, P. J.

P. P. Provenzano, K. W. Eliceiri, and P. J. Keely, “Shining new light on 3D cell motility and the metastatic process,” Trends Cell Biol.19(11), 638–648 (2009).
[CrossRef] [PubMed]

Kemper, B.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

P. Langehanenberg, B. Kemper, D. Dirksen, and G. von Bally, “Autofocusing in digital holographic phase contrast microscopy on pure phase objects for live cell imaging,” Appl. Opt.47(19), D176–D182 (2008).
[CrossRef] [PubMed]

Ketelhut, S.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

Kim, D. Y.

Kolega, J.

G. G. Martins and J. Kolega, “Endothelial cell protrusion and migration in three-dimensional collagen matrices,” Cell Motil. Cytoskeleton63(2), 101–115 (2006).
[CrossRef] [PubMed]

Langehanenberg, P.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

P. Langehanenberg, B. Kemper, D. Dirksen, and G. von Bally, “Autofocusing in digital holographic phase contrast microscopy on pure phase objects for live cell imaging,” Appl. Opt.47(19), D176–D182 (2008).
[CrossRef] [PubMed]

Le Cabec, V.

E. Van Goethem, R. Poincloux, F. Gauffre, I. Maridonneau-Parini, and V. Le Cabec, “Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures,” J. Immunol.184(2), 1049–1061 (2010).
[CrossRef] [PubMed]

Lee, J. Y.

Lee, S.

Marasco, D.

D. Guarnieri, A. De Capua, M. Ventre, A. Borzacchiello, C. Pedone, D. Marasco, M. Ruvo, and P. A. Netti, “Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters,” Acta Biomater.6(7), 2532–2539 (2010).
[CrossRef] [PubMed]

Maridonneau-Parini, I.

E. Van Goethem, R. Poincloux, F. Gauffre, I. Maridonneau-Parini, and V. Le Cabec, “Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures,” J. Immunol.184(2), 1049–1061 (2010).
[CrossRef] [PubMed]

Martins, G. G.

G. G. Martins and J. Kolega, “Endothelial cell protrusion and migration in three-dimensional collagen matrices,” Cell Motil. Cytoskeleton63(2), 101–115 (2006).
[CrossRef] [PubMed]

McElhinney, C. P.

McIntire, L. V.

Z. N. Demou and L. V. McIntire, “Fully automated three-dimensional tracking of cancer cells in collagen gels: determination of motility phenotypes at the cellular level,” Cancer Res.62(18), 5301–5307 (2002).
[PubMed]

Memmolo, P.

Menq, C.-H.

Miccio, L.

Minuth, W. W.

K. Schumacher, R. Strehl, U. de Vries, and W. W. Minuth, “Advanced technique for long term culture of epithelia in a continuous luminal-basal medium gradient,” Biomaterials23(3), 805–815 (2002).
[CrossRef] [PubMed]

Mölder, A.

J. Persson, A. Mölder, S. G. Pettersson, and K. Alm, “Cell motility studies using digital holographic microscopy,” in Microscopy: Science, Technology, Applications and Education. Microscopy Series4, 1063–1072 (2010).

Naughton, T. J.

Netti, P. A.

M. Ventre, F. Valle, M. Bianchi, F. Biscarini, and P. A. Netti, “Cell fluidics: producing cellular streams on micropatterned synthetic surfaces,” Langmuir28(1), 714–721 (2012).
[CrossRef] [PubMed]

D. Guarnieri, A. De Capua, M. Ventre, A. Borzacchiello, C. Pedone, D. Marasco, M. Ruvo, and P. A. Netti, “Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters,” Acta Biomater.6(7), 2532–2539 (2010).
[CrossRef] [PubMed]

Paturzo, M.

Pedone, C.

D. Guarnieri, A. De Capua, M. Ventre, A. Borzacchiello, C. Pedone, D. Marasco, M. Ruvo, and P. A. Netti, “Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters,” Acta Biomater.6(7), 2532–2539 (2010).
[CrossRef] [PubMed]

Persson, J.

J. Persson, A. Mölder, S. G. Pettersson, and K. Alm, “Cell motility studies using digital holographic microscopy,” in Microscopy: Science, Technology, Applications and Education. Microscopy Series4, 1063–1072 (2010).

Pettersson, S. G.

J. Persson, A. Mölder, S. G. Pettersson, and K. Alm, “Cell motility studies using digital holographic microscopy,” in Microscopy: Science, Technology, Applications and Education. Microscopy Series4, 1063–1072 (2010).

Piotrowski, T.

A. Aman and T. Piotrowski, “Cell migration during morphogenesis,” Dev. Biol.341(1), 20–33 (2010).
[CrossRef] [PubMed]

Poincloux, R.

E. Van Goethem, R. Poincloux, F. Gauffre, I. Maridonneau-Parini, and V. Le Cabec, “Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures,” J. Immunol.184(2), 1049–1061 (2010).
[CrossRef] [PubMed]

Provenzano, P. P.

P. P. Provenzano, K. W. Eliceiri, and P. J. Keely, “Shining new light on 3D cell motility and the metastatic process,” Trends Cell Biol.19(11), 638–648 (2009).
[CrossRef] [PubMed]

Restrepo, J. F.

Ruvo, M.

D. Guarnieri, A. De Capua, M. Ventre, A. Borzacchiello, C. Pedone, D. Marasco, M. Ruvo, and P. A. Netti, “Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters,” Acta Biomater.6(7), 2532–2539 (2010).
[CrossRef] [PubMed]

Schockaert, C.

Schumacher, K.

K. Schumacher, R. Strehl, U. de Vries, and W. W. Minuth, “Advanced technique for long term culture of epithelia in a continuous luminal-basal medium gradient,” Biomaterials23(3), 805–815 (2002).
[CrossRef] [PubMed]

Strehl, R.

K. Schumacher, R. Strehl, U. de Vries, and W. W. Minuth, “Advanced technique for long term culture of epithelia in a continuous luminal-basal medium gradient,” Biomaterials23(3), 805–815 (2002).
[CrossRef] [PubMed]

Tulino, A. M.

Valle, F.

M. Ventre, F. Valle, M. Bianchi, F. Biscarini, and P. A. Netti, “Cell fluidics: producing cellular streams on micropatterned synthetic surfaces,” Langmuir28(1), 714–721 (2012).
[CrossRef] [PubMed]

Van Goethem, E.

E. Van Goethem, R. Poincloux, F. Gauffre, I. Maridonneau-Parini, and V. Le Cabec, “Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures,” J. Immunol.184(2), 1049–1061 (2010).
[CrossRef] [PubMed]

Ventre, M.

M. Ventre, F. Valle, M. Bianchi, F. Biscarini, and P. A. Netti, “Cell fluidics: producing cellular streams on micropatterned synthetic surfaces,” Langmuir28(1), 714–721 (2012).
[CrossRef] [PubMed]

D. Guarnieri, A. De Capua, M. Ventre, A. Borzacchiello, C. Pedone, D. Marasco, M. Ruvo, and P. A. Netti, “Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters,” Acta Biomater.6(7), 2532–2539 (2010).
[CrossRef] [PubMed]

Vollmer, A.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

von Bally, G.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

P. Langehanenberg, B. Kemper, D. Dirksen, and G. von Bally, “Autofocusing in digital holographic phase contrast microscopy on pure phase objects for live cell imaging,” Appl. Opt.47(19), D176–D182 (2008).
[CrossRef] [PubMed]

Yang, W.

Yourassowsky, C.

Zerlauth, G.

R. T. Franceschi, W. M. James, and G. Zerlauth, “1 alpha, 25-dihydroxyvitamin D3 specific regulation of growth, morphology, and fibronectin in a human osteosarcoma cell line,” J. Cell. Physiol.123(3), 401–409 (1985).
[CrossRef] [PubMed]

Zhang, Z.

Acta Biomater.

D. Guarnieri, A. De Capua, M. Ventre, A. Borzacchiello, C. Pedone, D. Marasco, M. Ruvo, and P. A. Netti, “Covalently immobilized RGD gradient on PEG hydrogel scaffold influences cell migration parameters,” Acta Biomater.6(7), 2532–2539 (2010).
[CrossRef] [PubMed]

Appl. Opt.

Biomaterials

K. Schumacher, R. Strehl, U. de Vries, and W. W. Minuth, “Advanced technique for long term culture of epithelia in a continuous luminal-basal medium gradient,” Biomaterials23(3), 805–815 (2002).
[CrossRef] [PubMed]

Cancer Res.

Z. N. Demou and L. V. McIntire, “Fully automated three-dimensional tracking of cancer cells in collagen gels: determination of motility phenotypes at the cellular level,” Cancer Res.62(18), 5301–5307 (2002).
[PubMed]

Cell Motil. Cytoskeleton

G. G. Martins and J. Kolega, “Endothelial cell protrusion and migration in three-dimensional collagen matrices,” Cell Motil. Cytoskeleton63(2), 101–115 (2006).
[CrossRef] [PubMed]

Dev. Biol.

A. Aman and T. Piotrowski, “Cell migration during morphogenesis,” Dev. Biol.341(1), 20–33 (2010).
[CrossRef] [PubMed]

J. Biomed. Opt.

P. Langehanenberg, L. Ivanova, I. Bernhardt, S. Ketelhut, A. Vollmer, D. Dirksen, G. Georgiev, G. von Bally, and B. Kemper, “Automated three-dimensional tracking of living cells by digital holographic microscopy,” J. Biomed. Opt.14(1), 014018 (2009).
[CrossRef] [PubMed]

J. Cell. Physiol.

R. T. Franceschi, W. M. James, and G. Zerlauth, “1 alpha, 25-dihydroxyvitamin D3 specific regulation of growth, morphology, and fibronectin in a human osteosarcoma cell line,” J. Cell. Physiol.123(3), 401–409 (1985).
[CrossRef] [PubMed]

J. Immunol.

E. Van Goethem, R. Poincloux, F. Gauffre, I. Maridonneau-Parini, and V. Le Cabec, “Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures,” J. Immunol.184(2), 1049–1061 (2010).
[CrossRef] [PubMed]

Langmuir

M. Ventre, F. Valle, M. Bianchi, F. Biscarini, and P. A. Netti, “Cell fluidics: producing cellular streams on micropatterned synthetic surfaces,” Langmuir28(1), 714–721 (2012).
[CrossRef] [PubMed]

Opt. Express

F. Dubois, C. Schockaert, N. Callens, and C. Yourassowsky, “Focus plane detection criteria in digital holography microscopy by amplitude analysis,” Opt. Express14(13), 5895–5908 (2006).
[CrossRef] [PubMed]

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Supplementary Material (3)

» Media 1: AVI (2413 KB)     
» Media 2: AVI (2431 KB)     
» Media 3: AVI (2369 KB)     

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Figures (8)

Fig. 1
Fig. 1

Set-up of the holographic microscope. FS Fiber Splitter; MI Micro-Incubator; MO Microscope Objective; F Filter; BS Beam Splitter; IP Image Plane; HP Hologram Plane

Fig. 2
Fig. 2

(a) initial phase map of the tracking sequence reconstructed at the middle plane of the sample volume; (b) labeled cells extracted from (a) with thresholding filter. The white boxes highlight the cells that we will track, identified by (A,B,C).

Fig. 3
Fig. 3

focus distance for the cell B. (a,c,e) are the amplitude reconstructions computed at distance given by the values indicated by the red arrows. (b,d,f) are the corresponding phase maps. (c,d) represent the best focus image corresponding to the estimated dfoc by Tamura coefficient.

Fig. 4
Fig. 4

(a,b,c) are the initial frames of the sequence under analysis, (d,e,f) are the 11th, 22nd, and 20th frame respectively.

Fig. 5
Fig. 5

(a,b,c) are the results of the superimposition of 21st and 22nd filters, for the three cells considered in Fig. 1(b). Their corresponding MBFs are reported in (d,e,f) respectively.

Fig. 6
Fig. 6

Frame 24 of Media 1. In (a) there is the cell A with the (X,Y) positions estimated using the 4 methods. The in-focus distance is reported on the top of (a). (b) contains the trajectories estimated of the 4 methods up to 24 frames.

Fig. 7
Fig. 7

Frame 25 of Media 2. In (a) there is the cell B with the (X,Y) positions estimated using the 4 methods. The in-focus distance is reported on the top of (a). (b) contains the trajectories estimated of the 4 methods up to 25 frames.

Fig. 8
Fig. 8

Frame 13 of Media 3. In (a) there is the cell C with the (X,Y) positions estimated using the 4 methods. The in-focus distance is reported on the top of (a). (b) contains the trajectories estimated of the 4 methods up to 13 frames.

Equations (2)

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C= σ( I ) μ( I )
d foc =min{ C d }

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