Abstract

The measurement of soft tissue fiber orientation is fundamental to pathophysiology and biomechanical function in a multitude of biomedical applications. However, many existing techniques for quantifying fiber structure rely on transmitted light, limiting general applicability and often requiring tissue processing. Herein, we present a novel wide-field reflectance-based imaging modality, which combines polarized light imaging (PLI) and spatial frequency domain imaging (SFDI) to rapidly quantify preferred fiber orientation on soft collagenous tissues. PLI utilizes the polarization dependent scattering property of fibers to determine preferred fiber orientation; SFDI imaging at high spatial frequency is introduced to reject the highly diffuse photons and to control imaging depth. As a result, photons scattered from the superficial layer of a multi-layered sample are highlighted. Thus, fiber orientation quantification can be achieved for the superficial layer with optical sectioning. We demonstrated on aortic heart valve leaflet that, at spatial frequency of f = 1mm−1, the diffuse background can be effectively rejected and the imaging depth can be limited, thus improving quantification accuracy.

© 2015 Optical Society of America

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References

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2012 (1)

S. Alali, M. Ahmad, A. Kim, N. Vurgun, M. F. G. Wood, and I. A. Vitkin, “Quantitative correlation between light depolarization and transport albedo of various porcine tissues,” J. Biomed. Opt. 17(4), 045004 (2012).
[Crossref] [PubMed]

2011 (1)

S. D. Konecky, T. Rice, A. J. Durkin, and B. J. Tromberg, “Imaging scattering orientation with spatial frequency domain imaging,” J. Biomed. Opt. 16(12), 126001 (2011).
[Crossref] [PubMed]

2010 (1)

R. Liao, N. Zeng, X. Jiang, D. Li, T. Yun, Y. He, and H. Ma, “Rotating linear polarization imaging technique for anisotropic tissues,” J. Biomed. Opt. 15(3), 036014 (2010).
[Crossref] [PubMed]

2009 (3)

E. M. Joyce, J. Liao, F. J. Schoen, J. E. Mayer, and M. S. Sacks, “Functional collagen fiber architecture of the pulmonary heart valve cusp,” Ann. Thorac. Surg. 87(4), 1240–1249 (2009).
[Crossref] [PubMed]

Z. Nan, J. Xiaoyu, G. Qiang, H. Yonghong, and M. Hui, “Linear polarization difference imaging and its potential applications,” Appl. Opt. 48(35), 6734–6739 (2009).
[Crossref] [PubMed]

D. J. Cuccia, F. Bevilacqua, A. J. Durkin, F. R. Ayers, and B. J. Tromberg, “Quantitation and mapping of tissue optical properties using modulated imaging,” J. Biomed. Opt. 14(2), 024012 (2009).
[Crossref] [PubMed]

2008 (1)

2007 (2)

L. Bozec, G. van der Heijden, and M. Horton, “Collagen fibrils: nanoscale ropes,” Biophys. J. 92(1), 70–75 (2007).
[Crossref] [PubMed]

D. Arifler, I. Pavlova, A. Gillenwater, and R. Richards-Kortum, “Light scattering from collagen fiber networks: micro-optical properties of normal and neoplastic stroma,” Biophys. J. 92(9), 3260–3274 (2007).
[Crossref] [PubMed]

2005 (1)

2004 (1)

2003 (2)

T. G. Bromage, H. M. Goldman, S. C. McFarlin, J. Warshaw, A. Boyde, and C. M. Riggs, “Circularly polarized light standards for investigations of collagen fiber orientation in bone,” Anat. Rec. B New Anat. 274(1), 157–168 (2003).
[Crossref] [PubMed]

M. S. Sacks, “Incorporation of experimentally-derived fiber orientation into a structural constitutive model for planar collagenous tissues,” J. Biomech. Eng. 125(2), 280–287 (2003).
[Crossref] [PubMed]

2002 (3)

S. Jiao and L. V. Wang, “Two-dimensional depth-resolved Mueller matrix of biological tissue measured with double-beam polarization-sensitive optical coherence tomography,” Opt. Lett. 27(2), 101–103 (2002).
[Crossref] [PubMed]

T. T. Tower, M. R. Neidert, and R. T. Tranquillo, “Fiber alignment imaging during mechanical testing of soft tissues,” Ann. Biomed. Eng. 30(10), 1221–1233 (2002).
[Crossref] [PubMed]

S. L. Jacques, J. C. Ramella-Roman, and K. Lee, “Imaging skin pathology with polarized light,” J. Biomed. Opt. 7(3), 329–340 (2002).
[Crossref] [PubMed]

2001 (1)

T. T. Tower and R. T. Tranquillo, “Alignment maps of tissues: I. Microscopic elliptical polarimetry,” Biophys. J. 81(5), 2954–2963 (2001).
[Crossref] [PubMed]

2000 (2)

H. Axer and D. G. Keyserlingk, “Mapping of fiber orientation in human internal capsule by means of polarized light and confocal scanning laser microscopy,” J. Neurosci. Methods 94(2), 165–175 (2000).
[Crossref] [PubMed]

M. S. Sacks, “Biaxial mechanical evaluation of planar biological materials,” Journal of Elasticity and the Physical Science of Solids. 61(1/3), 199–246 (2000).
[Crossref]

1999 (1)

1998 (1)

M. S. Sacks, D. B. Smith, and E. D. Hiester, “The aortic valve microstructure: effects of transvalvular pressure,” J. Biomed. Mater. Res. 41(1), 131–141 (1998).
[Crossref] [PubMed]

1997 (1)

M. S. Sacks, D. B. Smith, and E. D. Hiester, “A small angle light scattering device for planar connective tissue microstructural analysis,” Ann. Biomed. Eng. 25(4), 678–689 (1997).
[Crossref] [PubMed]

1995 (1)

1992 (1)

M. S. Sacks and C. J. Chuong, “Characterization of collagen fiber architecture in the canine diaphragmatic central tendon,” J. Biomech. Eng. 114(2), 183–190 (1992).
[Crossref] [PubMed]

Ahmad, M.

S. Alali, M. Ahmad, A. Kim, N. Vurgun, M. F. G. Wood, and I. A. Vitkin, “Quantitative correlation between light depolarization and transport albedo of various porcine tissues,” J. Biomed. Opt. 17(4), 045004 (2012).
[Crossref] [PubMed]

Alali, S.

S. Alali, M. Ahmad, A. Kim, N. Vurgun, M. F. G. Wood, and I. A. Vitkin, “Quantitative correlation between light depolarization and transport albedo of various porcine tissues,” J. Biomed. Opt. 17(4), 045004 (2012).
[Crossref] [PubMed]

Araki, T.

Arifler, D.

D. Arifler, I. Pavlova, A. Gillenwater, and R. Richards-Kortum, “Light scattering from collagen fiber networks: micro-optical properties of normal and neoplastic stroma,” Biophys. J. 92(9), 3260–3274 (2007).
[Crossref] [PubMed]

Axer, H.

H. Axer and D. G. Keyserlingk, “Mapping of fiber orientation in human internal capsule by means of polarized light and confocal scanning laser microscopy,” J. Neurosci. Methods 94(2), 165–175 (2000).
[Crossref] [PubMed]

Ayers, F. R.

D. J. Cuccia, F. Bevilacqua, A. J. Durkin, F. R. Ayers, and B. J. Tromberg, “Quantitation and mapping of tissue optical properties using modulated imaging,” J. Biomed. Opt. 14(2), 024012 (2009).
[Crossref] [PubMed]

Bevilacqua, F.

D. J. Cuccia, F. Bevilacqua, A. J. Durkin, F. R. Ayers, and B. J. Tromberg, “Quantitation and mapping of tissue optical properties using modulated imaging,” J. Biomed. Opt. 14(2), 024012 (2009).
[Crossref] [PubMed]

D. J. Cuccia, F. Bevilacqua, A. J. Durkin, and B. J. Tromberg, “Modulated imaging: quantitative analysis and tomography of turbid media in the spatial-frequency domain,” Opt. Lett. 30(11), 1354–1356 (2005).
[Crossref] [PubMed]

Boyde, A.

T. G. Bromage, H. M. Goldman, S. C. McFarlin, J. Warshaw, A. Boyde, and C. M. Riggs, “Circularly polarized light standards for investigations of collagen fiber orientation in bone,” Anat. Rec. B New Anat. 274(1), 157–168 (2003).
[Crossref] [PubMed]

Bozec, L.

L. Bozec, G. van der Heijden, and M. Horton, “Collagen fibrils: nanoscale ropes,” Biophys. J. 92(1), 70–75 (2007).
[Crossref] [PubMed]

Bromage, T. G.

T. G. Bromage, H. M. Goldman, S. C. McFarlin, J. Warshaw, A. Boyde, and C. M. Riggs, “Circularly polarized light standards for investigations of collagen fiber orientation in bone,” Anat. Rec. B New Anat. 274(1), 157–168 (2003).
[Crossref] [PubMed]

Chuong, C. J.

M. S. Sacks and C. J. Chuong, “Characterization of collagen fiber architecture in the canine diaphragmatic central tendon,” J. Biomech. Eng. 114(2), 183–190 (1992).
[Crossref] [PubMed]

Crowe, J. A.

Cuccia, D. J.

D. J. Cuccia, F. Bevilacqua, A. J. Durkin, F. R. Ayers, and B. J. Tromberg, “Quantitation and mapping of tissue optical properties using modulated imaging,” J. Biomed. Opt. 14(2), 024012 (2009).
[Crossref] [PubMed]

D. J. Cuccia, F. Bevilacqua, A. J. Durkin, and B. J. Tromberg, “Modulated imaging: quantitative analysis and tomography of turbid media in the spatial-frequency domain,” Opt. Lett. 30(11), 1354–1356 (2005).
[Crossref] [PubMed]

Drezek, R.

Dunn, A.

Durkin, A. J.

S. D. Konecky, T. Rice, A. J. Durkin, and B. J. Tromberg, “Imaging scattering orientation with spatial frequency domain imaging,” J. Biomed. Opt. 16(12), 126001 (2011).
[Crossref] [PubMed]

D. J. Cuccia, F. Bevilacqua, A. J. Durkin, F. R. Ayers, and B. J. Tromberg, “Quantitation and mapping of tissue optical properties using modulated imaging,” J. Biomed. Opt. 14(2), 024012 (2009).
[Crossref] [PubMed]

D. J. Cuccia, F. Bevilacqua, A. J. Durkin, and B. J. Tromberg, “Modulated imaging: quantitative analysis and tomography of turbid media in the spatial-frequency domain,” Opt. Lett. 30(11), 1354–1356 (2005).
[Crossref] [PubMed]

Gillenwater, A.

D. Arifler, I. Pavlova, A. Gillenwater, and R. Richards-Kortum, “Light scattering from collagen fiber networks: micro-optical properties of normal and neoplastic stroma,” Biophys. J. 92(9), 3260–3274 (2007).
[Crossref] [PubMed]

Goldman, H. M.

T. G. Bromage, H. M. Goldman, S. C. McFarlin, J. Warshaw, A. Boyde, and C. M. Riggs, “Circularly polarized light standards for investigations of collagen fiber orientation in bone,” Anat. Rec. B New Anat. 274(1), 157–168 (2003).
[Crossref] [PubMed]

He, Y.

R. Liao, N. Zeng, X. Jiang, D. Li, T. Yun, Y. He, and H. Ma, “Rotating linear polarization imaging technique for anisotropic tissues,” J. Biomed. Opt. 15(3), 036014 (2010).
[Crossref] [PubMed]

Hiester, E. D.

M. S. Sacks, D. B. Smith, and E. D. Hiester, “The aortic valve microstructure: effects of transvalvular pressure,” J. Biomed. Mater. Res. 41(1), 131–141 (1998).
[Crossref] [PubMed]

M. S. Sacks, D. B. Smith, and E. D. Hiester, “A small angle light scattering device for planar connective tissue microstructural analysis,” Ann. Biomed. Eng. 25(4), 678–689 (1997).
[Crossref] [PubMed]

Horton, M.

L. Bozec, G. van der Heijden, and M. Horton, “Collagen fibrils: nanoscale ropes,” Biophys. J. 92(1), 70–75 (2007).
[Crossref] [PubMed]

Hui, M.

Jacques, S. L.

S. L. Jacques, J. C. Ramella-Roman, and K. Lee, “Imaging skin pathology with polarized light,” J. Biomed. Opt. 7(3), 329–340 (2002).
[Crossref] [PubMed]

I. S. Saidi, S. L. Jacques, and F. K. Tittel, “Mie and Rayleigh modeling of visible-light scattering in neonatal skin,” Appl. Opt. 34(31), 7410–7418 (1995).
[Crossref] [PubMed]

Jiang, X.

R. Liao, N. Zeng, X. Jiang, D. Li, T. Yun, Y. He, and H. Ma, “Rotating linear polarization imaging technique for anisotropic tissues,” J. Biomed. Opt. 15(3), 036014 (2010).
[Crossref] [PubMed]

Jiao, S.

Joyce, E. M.

E. M. Joyce, J. Liao, F. J. Schoen, J. E. Mayer, and M. S. Sacks, “Functional collagen fiber architecture of the pulmonary heart valve cusp,” Ann. Thorac. Surg. 87(4), 1240–1249 (2009).
[Crossref] [PubMed]

Keyserlingk, D. G.

H. Axer and D. G. Keyserlingk, “Mapping of fiber orientation in human internal capsule by means of polarized light and confocal scanning laser microscopy,” J. Neurosci. Methods 94(2), 165–175 (2000).
[Crossref] [PubMed]

Kim, A.

S. Alali, M. Ahmad, A. Kim, N. Vurgun, M. F. G. Wood, and I. A. Vitkin, “Quantitative correlation between light depolarization and transport albedo of various porcine tissues,” J. Biomed. Opt. 17(4), 045004 (2012).
[Crossref] [PubMed]

Konecky, S. D.

S. D. Konecky, T. Rice, A. J. Durkin, and B. J. Tromberg, “Imaging scattering orientation with spatial frequency domain imaging,” J. Biomed. Opt. 16(12), 126001 (2011).
[Crossref] [PubMed]

Lee, K.

S. L. Jacques, J. C. Ramella-Roman, and K. Lee, “Imaging skin pathology with polarized light,” J. Biomed. Opt. 7(3), 329–340 (2002).
[Crossref] [PubMed]

Li, D.

R. Liao, N. Zeng, X. Jiang, D. Li, T. Yun, Y. He, and H. Ma, “Rotating linear polarization imaging technique for anisotropic tissues,” J. Biomed. Opt. 15(3), 036014 (2010).
[Crossref] [PubMed]

Liao, J.

E. M. Joyce, J. Liao, F. J. Schoen, J. E. Mayer, and M. S. Sacks, “Functional collagen fiber architecture of the pulmonary heart valve cusp,” Ann. Thorac. Surg. 87(4), 1240–1249 (2009).
[Crossref] [PubMed]

Liao, R.

R. Liao, N. Zeng, X. Jiang, D. Li, T. Yun, Y. He, and H. Ma, “Rotating linear polarization imaging technique for anisotropic tissues,” J. Biomed. Opt. 15(3), 036014 (2010).
[Crossref] [PubMed]

Ma, H.

R. Liao, N. Zeng, X. Jiang, D. Li, T. Yun, Y. He, and H. Ma, “Rotating linear polarization imaging technique for anisotropic tissues,” J. Biomed. Opt. 15(3), 036014 (2010).
[Crossref] [PubMed]

Mayer, J. E.

E. M. Joyce, J. Liao, F. J. Schoen, J. E. Mayer, and M. S. Sacks, “Functional collagen fiber architecture of the pulmonary heart valve cusp,” Ann. Thorac. Surg. 87(4), 1240–1249 (2009).
[Crossref] [PubMed]

McFarlin, S. C.

T. G. Bromage, H. M. Goldman, S. C. McFarlin, J. Warshaw, A. Boyde, and C. M. Riggs, “Circularly polarized light standards for investigations of collagen fiber orientation in bone,” Anat. Rec. B New Anat. 274(1), 157–168 (2003).
[Crossref] [PubMed]

Morgan, S. P.

Nan, Z.

Neidert, M. R.

T. T. Tower, M. R. Neidert, and R. T. Tranquillo, “Fiber alignment imaging during mechanical testing of soft tissues,” Ann. Biomed. Eng. 30(10), 1221–1233 (2002).
[Crossref] [PubMed]

Pavlova, I.

D. Arifler, I. Pavlova, A. Gillenwater, and R. Richards-Kortum, “Light scattering from collagen fiber networks: micro-optical properties of normal and neoplastic stroma,” Biophys. J. 92(9), 3260–3274 (2007).
[Crossref] [PubMed]

Qiang, G.

Ramella-Roman, J. C.

S. L. Jacques, J. C. Ramella-Roman, and K. Lee, “Imaging skin pathology with polarized light,” J. Biomed. Opt. 7(3), 329–340 (2002).
[Crossref] [PubMed]

Rice, T.

S. D. Konecky, T. Rice, A. J. Durkin, and B. J. Tromberg, “Imaging scattering orientation with spatial frequency domain imaging,” J. Biomed. Opt. 16(12), 126001 (2011).
[Crossref] [PubMed]

Richards-Kortum, R.

D. Arifler, I. Pavlova, A. Gillenwater, and R. Richards-Kortum, “Light scattering from collagen fiber networks: micro-optical properties of normal and neoplastic stroma,” Biophys. J. 92(9), 3260–3274 (2007).
[Crossref] [PubMed]

R. Drezek, A. Dunn, and R. Richards-Kortum, “Light scattering from cells: finite-difference time-domain simulations and goniometric measurements,” Appl. Opt. 38(16), 3651–3661 (1999).
[Crossref] [PubMed]

Riggs, C. M.

T. G. Bromage, H. M. Goldman, S. C. McFarlin, J. Warshaw, A. Boyde, and C. M. Riggs, “Circularly polarized light standards for investigations of collagen fiber orientation in bone,” Anat. Rec. B New Anat. 274(1), 157–168 (2003).
[Crossref] [PubMed]

Sacks, M. S.

E. M. Joyce, J. Liao, F. J. Schoen, J. E. Mayer, and M. S. Sacks, “Functional collagen fiber architecture of the pulmonary heart valve cusp,” Ann. Thorac. Surg. 87(4), 1240–1249 (2009).
[Crossref] [PubMed]

M. S. Sacks, “Incorporation of experimentally-derived fiber orientation into a structural constitutive model for planar collagenous tissues,” J. Biomech. Eng. 125(2), 280–287 (2003).
[Crossref] [PubMed]

M. S. Sacks, “Biaxial mechanical evaluation of planar biological materials,” Journal of Elasticity and the Physical Science of Solids. 61(1/3), 199–246 (2000).
[Crossref]

M. S. Sacks, D. B. Smith, and E. D. Hiester, “The aortic valve microstructure: effects of transvalvular pressure,” J. Biomed. Mater. Res. 41(1), 131–141 (1998).
[Crossref] [PubMed]

M. S. Sacks, D. B. Smith, and E. D. Hiester, “A small angle light scattering device for planar connective tissue microstructural analysis,” Ann. Biomed. Eng. 25(4), 678–689 (1997).
[Crossref] [PubMed]

M. S. Sacks and C. J. Chuong, “Characterization of collagen fiber architecture in the canine diaphragmatic central tendon,” J. Biomech. Eng. 114(2), 183–190 (1992).
[Crossref] [PubMed]

Saidi, I. S.

Schoen, F. J.

E. M. Joyce, J. Liao, F. J. Schoen, J. E. Mayer, and M. S. Sacks, “Functional collagen fiber architecture of the pulmonary heart valve cusp,” Ann. Thorac. Surg. 87(4), 1240–1249 (2009).
[Crossref] [PubMed]

Smith, D. B.

M. S. Sacks, D. B. Smith, and E. D. Hiester, “The aortic valve microstructure: effects of transvalvular pressure,” J. Biomed. Mater. Res. 41(1), 131–141 (1998).
[Crossref] [PubMed]

M. S. Sacks, D. B. Smith, and E. D. Hiester, “A small angle light scattering device for planar connective tissue microstructural analysis,” Ann. Biomed. Eng. 25(4), 678–689 (1997).
[Crossref] [PubMed]

Stockford, I. M.

Tittel, F. K.

Tohno, Y.

Tower, T. T.

T. T. Tower, M. R. Neidert, and R. T. Tranquillo, “Fiber alignment imaging during mechanical testing of soft tissues,” Ann. Biomed. Eng. 30(10), 1221–1233 (2002).
[Crossref] [PubMed]

T. T. Tower and R. T. Tranquillo, “Alignment maps of tissues: I. Microscopic elliptical polarimetry,” Biophys. J. 81(5), 2954–2963 (2001).
[Crossref] [PubMed]

Tranquillo, R. T.

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S. Alali, M. Ahmad, A. Kim, N. Vurgun, M. F. G. Wood, and I. A. Vitkin, “Quantitative correlation between light depolarization and transport albedo of various porcine tissues,” J. Biomed. Opt. 17(4), 045004 (2012).
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Figures (8)

Fig. 1
Fig. 1 Cylinder light scattering simulation geometry. The cylinders orient at 30 degree with respect to x axis. The polarized light illuminates a collection of cylinders with multiple diameters at normal incidence. The polarization angle θ of the incident light rotates anti-clockwise from 0 degree to 180 degrees.
Fig. 2
Fig. 2 (a) Color picture of pSFDI imaging system. (b) Schematic of the pSFDI imaging system.
Fig. 3
Fig. 3 SHG image shows the collagen fibers in porcine aortic valve leaflet tissue.
Fig. 4
Fig. 4 Polarization dependent back-scattered light over 180-degree polarization range for (a) collagen fibers and (b) collagen fibrils. Two peaks can be identified. The higher peak indicates that illumination polarization is parallel to the fiber orientation, while lower peak indicates they are perpendicular.
Fig. 5
Fig. 5 Polarization dependent back-scattered light over 180-degree polarization range for 6 fiber distributions. The higher peaks locate at 30 degree for normal distribution. With higher fiber orientation deviation, both higher peak and lower peak intensity decrease. No peak can be found for random distribution.
Fig. 6
Fig. 6 Collagen fiber orientation mapping on bovine tendons. (a) Blue arrows indicate the gross fiber orientation of the bovine tendons. Red rectangle shows the imaged area. (b) Back-scattered intensity plot over a small region indicated by a black square using both DC and AC components. (c) Fiber orientation map extracted using on AC components. (d) Fiber orientation map extracted using DC component.
Fig. 7
Fig. 7 Depth controlled pSFDI imaging of a two-layer bovine tendon sample (a). The collagen fiber orientation map retrieved using polarized light imaging without spatial pattern in map (b). The collagen fiber orientation maps (c) and (d) retrieved at spatial frequencies 0.09 and 0.5 mm-1, respectively. The intensity plot (e-g) for localized regions in (b-d), respectively.
Fig. 8
Fig. 8 pSFDI imaing on PVL (a-1 and 2) and PLV-tendon combination (f-1 and 2). DC component based fiber orientaion maps (b and g) for PLV and PLV-tendon combination, respectively. AC component based fiber orientation maps (c and h) for PLV and PLV-tendon combination, respectively. A SALS based orientation map (d) for PLV was obtained for comparison purpose. Polar plots of both AC and DC components from a small region indicated by black sqares (b and g) for both PLV (e) and PLV-tendon combination (i) respectively. Black arrows in (b) and (d) indicate unreliable fiber orientation. Dashed black rectangle in (g) indicates the overlapping region of PLV-tendon combination.

Equations (10)

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S out (θ)= scat=1 n M pol M rot (θ) M scat M rot (θ) M pol S in ,
M scat = φ= φ col φ= φ col [ M 11 (φ) M 12 (φ) 0 0 M 12 (φ) M 11 (φ) 0 0 0 0 M 33 (φ) M 34 (φ) 0 0 M 34 (φ) M 33 (φ) ] ,
M pol =[ 1 1 0 0 1 1 0 0 0 0 0 0 0 0 0 0 ],
M rot (θ)=[ 1 0 0 0 0 cos(2θ) sin(2θ) 0 0 sin(2θ) cos(2θ) 0 0 0 0 1 ],
S in = [ I in , Q in , U in , V in ] T ,
S out = [ I out , Q out , U out , V out ] T .
δ eff ' = ( 3 μ a ( μ a + μ s ' )+ (2πf) 2 ) 1 ,
δ eff ' (2πf) 1
I ac = 2 3 ( ( I 1 I 2 ) 2 + ( I 2 I 3 ) 2 + ( I 3 I 1 ) 2 )
I dc = 1 3 ( I 1 + I 2 + I 3 )

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