Abstract

High-contrast, high-resolution imaging of biomedical specimens is indispensable for studying organ function and pathologies. Conventional histology, the gold standard for soft-tissue visualization, is limited by its anisotropic spatial resolution, elaborate sample preparation, and lack of quantitative image information. X-ray absorption or phase tomography have been identified as promising alternatives enabling non-destructive, distortion-free three-dimensional (3D) imaging. However, reaching sufficient contrast and resolution with a simple experimental procedure remains a major challenge. Here, we present a solution based on x-ray phase tomography through speckle-based imaging (SBI). We demonstrate on a mouse kidney that SBI delivers comprehensive 3D maps of hydrated, unstained soft tissue, revealing its microstructure and delivering quantitative tissue-density values at a density resolution of better than $2\,\,{\rm mg}/{{\rm cm}^{3}}$ and spatial resolution of better than 8 µm. We expect that SBI virtual histology will find widespread application in biomedicine and will open up new possibilities for research and histopathology.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2020 (4)

M.-C. Zdora, I. Zanette, T. Walker, N. W. Phillips, R. Smith, H. Deyhle, S. Ahmed, and P. Thibault, “X-ray phase imaging with the unified modulated pattern analysis of near-field speckles at a laboratory source,” Appl. Opt. 59, 2270–2275 (2020).
[Crossref]

K. M. Pavlov, H. T. Li, D. M. Paganin, S. Berujon, H. Rougé-Labriet, and E. Brun, “Single-shot x-ray speckle-based imaging of a single-material object,” Phys. Rev. Appl. 13, 054023 (2020).
[Crossref]

M. Reichardt, M. Töpperwien, A. Khan, F. Alves, and T. Salditt, “Fiber orientation in a whole mouse heart reconstructed by laboratory phase-contrast micro-CT,” J. Med. Imaging 7, 1–16 (2020).
[Crossref]

M. Eckermann, M. Töpperwien, A.-L. Robisch, F. van der Meer, C. Stadelmann, and T. Salditt, “Phase-contrast x-ray tomography of neuronal tissue at laboratory sources with submicron resolution,” J. Med. Imaging 7, 1–15 (2020).
[Crossref]

2019 (1)

R. Hlushchuk, D. Haberthür, and V. Djonov, “Ex vivo microangioCT: advances in microvascular imaging,” Vasc. Pharmacol. 112, 2–7 (2019).
[Crossref]

2018 (8)

M.-C. Zdora, P. Thibault, H. Deyhle, J. Vila-Comamala, C. Rau, and I. Zanette, “Tunable x-ray speckle-based phase-contrast and dark-field imaging using the unified modulated pattern analysis approach,” J. Instrum. 13, C05005 (2018).
[Crossref]

M.-C. Zdora, “State of the art of x-ray speckle-based phase-contrast and dark-field imaging,” J. Imaging 4, 60 (2018).
[Crossref]

J. Pichat, J. E. Iglesias, T. Yousry, S. Ourselin, and M. Modat, “A survey of methods for 3D histology reconstruction,” Med. Image Anal. 46,73–105 (2018).
[Crossref]

J. Missbach-Guentner, D. Pinkert-Leetsch, C. Dullin, R. Ufartes, D. Hornung, B. Tampe, M. Zeisberg, and F. Alves, “3D virtual histology of murine kidneys—high resolution visualization of pathological alterations by micro computed tomography,” Sci. Rep. 8, 1407 (2018).
[Crossref]

M. Busse, M. Müller, M. A. Kimm, S. Ferstl, S. Allner, K. Achterhold, J. Herzen, and F. Pfeiffer, “Three-dimensional virtual histology enabled through cytoplasm-specific x-ray stain for microscopic and nanoscopic computed tomography,” Proc. Natl. Acad. Sci. USA 115, 2293–2298 (2018).
[Crossref]

J. Albers, S. Pacilé, M. A. Markus, M. Wiart, G. Vande Velde, G. Tromba, and C. Dullin, “X-ray-based 3D virtual histology-adding the next dimension to histological analysis,” Mol. Imaging Biol. 20, 732–741 (2018).
[Crossref]

M. Töpperwien, F. van der Meer, C. Stadelmann, and T. Salditt, “Three-dimensional virtual histology of human cerebellum by x-ray phase-contrast tomography,” Proc. Natl. Acad. Sci. USA 115, 6940–6945 (2018).
[Crossref]

A. Khimchenko, C. Bikis, A. Pacureanu, S. E. Hieber, P. Thalmann, H. Deyhle, G. Schweighauser, J. Hench, S. Frank, M. Müller-Gerbl, G. Schulz, P. Cloetens, and B. Müller, “Hard x-ray nanoholotomography: large-scale, label-free, 3D neuroimaging beyond optical limit,” Adv. Sci. 5, 1700694 (2018).
[Crossref]

2017 (1)

M.-C. Zdora, P. Thibault, T. Zhou, F. J. Koch, J. Romell, S. Sala, A. Last, C. Rau, and I. Zanette, “X-ray phase-contrast imaging and metrology through unified modulated pattern analysis,” Phys. Rev. Lett. 118, 203903 (2017).
[Crossref]

2016 (3)

D. A. Ferenbach and J. V. Bonventre, “Kidney tubules: intertubular, vascular, and glomerular cross-talk,” Curr. Opin. Nephrol. Hypertens. 25, 194–202 (2016).
[Crossref]

Y. Kashyap, H. Wang, and K. Sawhney, “Experimental comparison between speckle and grating-based imaging technique using synchrotron radiation x-rays,” Opt. Express 24, 18664–18673 (2016).
[Crossref]

H. Wang, Y. Kashyap, and K. Sawhney, “From synchrotron radiation to lab source: advanced speckle-based x-ray imaging using abrasive paper,” Sci. Rep. 6, 20476 (2016).
[Crossref]

2015 (3)

H. Wang, S. Berujon, J. Herzen, R. Atwood, D. Laundy, A. Hipp, and K. Sawhney, “X-ray phase contrast tomography by tracking near field speckle,” Sci. Rep. 5, 8762 (2015).
[Crossref]

J. M. de Souza e Silva, I. Zanette, P. B. Noël, M. B. Cardoso, M. A. Kimm, and F. Pfeiffer, “Three-dimensional non-destructive soft-tissue visualization with x-ray staining micro-tomography,” Sci. Rep. 5, 14088 (2015).
[Crossref]

I. Zanette, M.-C. Zdora, T. Zhou, A. Burvall, D. H. Larsson, P. Thibault, H. M. Hertz, and F. Pfeiffer, “X-ray microtomography using correlation of near-field speckles for material characterization,” Proc. Natl. Acad. Sci. USA 112, 12569–12573 (2015).
[Crossref]

2014 (3)

R. Shirai, T. Kunii, A. Yoneyama, T. Ooizumi, H. Maruyama, T.-T. Lwin, K. Hyodo, and T. Takeda, “Enhanced renal image contrast by ethanol fixation in phase-contrast x-ray computed tomography,” J. Synchrotron Radiat. 21, 795–800 (2014).
[Crossref]

S. W. Wilkins, Y. I. Nesterets, T. E. Gureyev, S. C. Mayo, A. Pogany, and A. W. Stevenson, “On the evolution and relative merits of hard x-ray phase-contrast imaging methods,” Philos. Trans. R. Soc. A 372, 20130021 (2014).
[Crossref]

I. Zanette, T. Zhou, A. Burvall, U. Lundström, D. H. Larsson, M. Zdora, P. Thibault, F. Pfeiffer, and H. M. Hertz, “Speckle-based x-ray phase-contrast and dark-field imaging with a laboratory source,” Phys. Rev. Lett. 112, 253903 (2014).
[Crossref]

2013 (2)

E. Pauwels, D. van Loo, P. Cornillie, L. Brabant, and L. van Hoorebeke, “An exploratory study of contrast agents for soft tissue visualization by means of high resolution x-ray computed tomography imaging,” J. Microsc. 250, 21–31 (2013).
[Crossref]

I. Zanette, T. Weitkamp, G. Le Duc, and F. Pfeiffer, “X-ray grating-based phase tomography for 3D histology,” RSC Adv. 3, 19816–19819 (2013).
[Crossref]

2012 (5)

S. Berujon, E. Ziegler, R. Cerbino, and L. Peverini, “Two-dimensional x-ray beam phase sensing,” Phys. Rev. Lett. 108, 158102 (2012).
[Crossref]

K. S. Morgan, D. M. Paganin, and K. K. W. Siu, “X-ray phase imaging with a paper analyzer,” Appl. Phys. Lett. 100, 124102 (2012).
[Crossref]

S. Berujon, H. Wang, and K. Sawhney, “X-ray multimodal imaging using a random-phase object,” Phys. Rev. A 86, 063813 (2012).
[Crossref]

U. Lundström, D. H. Larsson, A. Burvall, P. A. C. Takman, L. Scott, H. Brismar, and H. M. Hertz, “X-ray phase contrast for CO2 microangiography,” Phys. Med. Biol. 57, 2603 (2012).
[Crossref]

A. T. Layton, “Modeling transport and flow regulatory mechanisms of the kidney,” ISRN Biomath. 2012, 170594 (2012).
[Crossref]

2011 (2)

P. Modregger, B. R. Pinzer, T. Thüring, S. Rutishauser, C. David, and M. Stampanoni, “Sensitivity of x-ray grating interferometry,” Opt. Express 19, 18324–18338 (2011).
[Crossref]

R. Wagner, D. Van Loo, F. Hossler, K. Czymmek, E. Pauwels, and L. Van Hoorebeke, “High-resolution imaging of kidney vascular corrosion casts with nano-CT,” Microsc. Microanal. 17, 215–219 (2011).
[Crossref]

2010 (2)

G. Schulz, T. Weitkamp, I. Zanette, F. Pfeiffer, F. Beckmann, C. David, S. Rutishauser, E. Reznikova, and B. Müller, “High-resolution tomographic imaging of a human cerebellum: comparison of absorption and grating-based phase contrast,” J. R. Soc. Interface 7, 1665–1676 (2010).
[Crossref]

L. Zagorchev, P. Oses, Z. W. Zhuang, K. Moodie, M. J. Mulligan-Kehoe, M. Simons, and T. Couffinhal, “Micro computed tomography for vascular exploration,” J. Angiogenes. Res. 2, 7 (2010).
[Crossref]

2009 (1)

B. D. Metscher, “MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions,” Dev. Dyn. 238, 632–640 (2009).
[Crossref]

2008 (1)

R. Cerbino, L. Peverini, M. A. C. Potenza, A. Robert, P. Bösecke, and M. Giglio, “X-ray-scattering information obtained from near-field speckle,” Nat. Phys. 4, 238–243 (2008).
[Crossref]

2007 (1)

2006 (1)

F. Pfeiffer, T. Weitkamp, O. Bunk, and C. David, “Phase retrieval and differential phase-contrast imaging with low-brilliance x-ray sources,” Nat. Phys. 2, 258–261 (2006).
[Crossref]

2005 (2)

2003 (3)

O. Smithies, “Why the kidney glomerulus does not clog: a gel permeation/diffusion hypothesis of renal function,” Proc. Natl. Acad. Sci. USA 100, 4108–4113 (2003).
[Crossref]

X. Y. Zhai, H. Birn, K. B. Jensen, J. S. Thomsen, A. Andreasen, and E. I. Christensen, “Digital three-dimensional reconstruction and ultrastructure of the mouse proximal tubule,” J. Am. Soc. Nephrol. 14, 611–619 (2003).
[Crossref]

A. Momose, “Phase-sensitive imaging and phase tomography using x-ray interferometers,” Opt. Express 11, 2303–2314 (2003).
[Crossref]

2002 (2)

D. Paganin, S. C. Mayo, T. E. Gureyev, P. R. Miller, and S. W. Wilkins, “Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object,” J. Microsc. 206, 33–40 (2002).
[Crossref]

M. D. Bentley, M. C. Ortiz, E. L. Ritman, and J. C. Romero, “The use of microcomputed tomography to study microvasculature in small rodents,” Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R1267–R1279 (2002).
[Crossref]

1999 (1)

P. Cloetens, W. Ludwig, J. Baruchel, D. V. Dyck, J. V. Landuyt, J. P. Guigay, and M. Schlenker, “Holotomography: quantitative phase tomography with micrometer resolution using hard synchrotron radiation x rays,” Appl. Phys. Lett. 75, 2912–2914 (1999).
[Crossref]

1995 (1)

A. Snigirev, I. Snigireva, V. Kohn, S. Kuznetsov, and I. Schelokov, “On the possibilities of x-ray phase contrast microimaging by coherent high-energy synchrotron radiation,” Rev. Sci. Instrum. 66, 5486–5492 (1995).
[Crossref]

Achterhold, K.

M. Busse, M. Müller, M. A. Kimm, S. Ferstl, S. Allner, K. Achterhold, J. Herzen, and F. Pfeiffer, “Three-dimensional virtual histology enabled through cytoplasm-specific x-ray stain for microscopic and nanoscopic computed tomography,” Proc. Natl. Acad. Sci. USA 115, 2293–2298 (2018).
[Crossref]

Ahmed, S.

Albers, J.

J. Albers, S. Pacilé, M. A. Markus, M. Wiart, G. Vande Velde, G. Tromba, and C. Dullin, “X-ray-based 3D virtual histology-adding the next dimension to histological analysis,” Mol. Imaging Biol. 20, 732–741 (2018).
[Crossref]

Allner, S.

M. Busse, M. Müller, M. A. Kimm, S. Ferstl, S. Allner, K. Achterhold, J. Herzen, and F. Pfeiffer, “Three-dimensional virtual histology enabled through cytoplasm-specific x-ray stain for microscopic and nanoscopic computed tomography,” Proc. Natl. Acad. Sci. USA 115, 2293–2298 (2018).
[Crossref]

Als-Nielsen, J.

J. Als-Nielsen and D. McMorrow, Elements of Modern X-ray Physics (Wiley, 2011).

Alves, F.

M. Reichardt, M. Töpperwien, A. Khan, F. Alves, and T. Salditt, “Fiber orientation in a whole mouse heart reconstructed by laboratory phase-contrast micro-CT,” J. Med. Imaging 7, 1–16 (2020).
[Crossref]

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I. Zanette, T. Zhou, A. Burvall, U. Lundström, D. H. Larsson, M. Zdora, P. Thibault, F. Pfeiffer, and H. M. Hertz, “Speckle-based x-ray phase-contrast and dark-field imaging with a laboratory source,” Phys. Rev. Lett. 112, 253903 (2014).
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T. Weitkamp, A. Diaz, C. David, F. Pfeiffer, M. Stampanoni, P. Cloetens, and E. Ziegler, “X-ray phase imaging with a grating interferometer,” Opt. Express 13, 6296–6304 (2005).
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C. Kottler, C. David, F. Pfeiffer, and O. Bunk, “A two-directional approach for grating based differential phase contrast imaging using hard x-rays,” Opt. Express 15, 1175–1181 (2007).
[Crossref]

F. Pfeiffer, T. Weitkamp, O. Bunk, and C. David, “Phase retrieval and differential phase-contrast imaging with low-brilliance x-ray sources,” Nat. Phys. 2, 258–261 (2006).
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T. Weitkamp, A. Diaz, C. David, F. Pfeiffer, M. Stampanoni, P. Cloetens, and E. Ziegler, “X-ray phase imaging with a grating interferometer,” Opt. Express 13, 6296–6304 (2005).
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J. Missbach-Guentner, D. Pinkert-Leetsch, C. Dullin, R. Ufartes, D. Hornung, B. Tampe, M. Zeisberg, and F. Alves, “3D virtual histology of murine kidneys—high resolution visualization of pathological alterations by micro computed tomography,” Sci. Rep. 8, 1407 (2018).
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M. Busse, M. Müller, M. A. Kimm, S. Ferstl, S. Allner, K. Achterhold, J. Herzen, and F. Pfeiffer, “Three-dimensional virtual histology enabled through cytoplasm-specific x-ray stain for microscopic and nanoscopic computed tomography,” Proc. Natl. Acad. Sci. USA 115, 2293–2298 (2018).
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I. Zanette, T. Zhou, A. Burvall, U. Lundström, D. H. Larsson, M. Zdora, P. Thibault, F. Pfeiffer, and H. M. Hertz, “Speckle-based x-ray phase-contrast and dark-field imaging with a laboratory source,” Phys. Rev. Lett. 112, 253903 (2014).
[Crossref]

Thomsen, J. S.

X. Y. Zhai, H. Birn, K. B. Jensen, J. S. Thomsen, A. Andreasen, and E. I. Christensen, “Digital three-dimensional reconstruction and ultrastructure of the mouse proximal tubule,” J. Am. Soc. Nephrol. 14, 611–619 (2003).
[Crossref]

Thüring, T.

Töpperwien, M.

M. Reichardt, M. Töpperwien, A. Khan, F. Alves, and T. Salditt, “Fiber orientation in a whole mouse heart reconstructed by laboratory phase-contrast micro-CT,” J. Med. Imaging 7, 1–16 (2020).
[Crossref]

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[Crossref]

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J. Albers, S. Pacilé, M. A. Markus, M. Wiart, G. Vande Velde, G. Tromba, and C. Dullin, “X-ray-based 3D virtual histology-adding the next dimension to histological analysis,” Mol. Imaging Biol. 20, 732–741 (2018).
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M.-C. Zdora, P. Thibault, H. Deyhle, J. Vila-Comamala, C. Rau, and I. Zanette, “Tunable x-ray speckle-based phase-contrast and dark-field imaging using the unified modulated pattern analysis approach,” J. Instrum. 13, C05005 (2018).
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R. Wagner, D. Van Loo, F. Hossler, K. Czymmek, E. Pauwels, and L. Van Hoorebeke, “High-resolution imaging of kidney vascular corrosion casts with nano-CT,” Microsc. Microanal. 17, 215–219 (2011).
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F. Pfeiffer, T. Weitkamp, O. Bunk, and C. David, “Phase retrieval and differential phase-contrast imaging with low-brilliance x-ray sources,” Nat. Phys. 2, 258–261 (2006).
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T. Weitkamp, A. Diaz, C. David, F. Pfeiffer, M. Stampanoni, P. Cloetens, and E. Ziegler, “X-ray phase imaging with a grating interferometer,” Opt. Express 13, 6296–6304 (2005).
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I. Zanette, T. Zhou, A. Burvall, U. Lundström, D. H. Larsson, M. Zdora, P. Thibault, F. Pfeiffer, and H. M. Hertz, “Speckle-based x-ray phase-contrast and dark-field imaging with a laboratory source,” Phys. Rev. Lett. 112, 253903 (2014).
[Crossref]

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I. Zanette, T. Zhou, A. Burvall, U. Lundström, D. H. Larsson, M. Zdora, P. Thibault, F. Pfeiffer, and H. M. Hertz, “Speckle-based x-ray phase-contrast and dark-field imaging with a laboratory source,” Phys. Rev. Lett. 112, 253903 (2014).
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T. Weitkamp, A. Diaz, C. David, F. Pfeiffer, M. Stampanoni, P. Cloetens, and E. Ziegler, “X-ray phase imaging with a grating interferometer,” Opt. Express 13, 6296–6304 (2005).
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J. M. de Souza e Silva, I. Zanette, P. B. Noël, M. B. Cardoso, M. A. Kimm, and F. Pfeiffer, “Three-dimensional non-destructive soft-tissue visualization with x-ray staining micro-tomography,” Sci. Rep. 5, 14088 (2015).
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Supplementary Material (4)

NameDescription
» Supplement 1       Supplementary Information
» Visualization 1       Visualization 1: Tubule network in the different kidney regions
» Visualization 2       Visualization 2: Journey through the blood vessel network of the murine kidney
» Visualization 3       Visualization 3: Summary of the 3D virtual histology of the mouse kidney

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Figures (5)

Fig. 1.
Fig. 1. Experimental setup for x-ray speckle-based phase tomography. (a) Setup for the measurement of the mouse kidney specimen. (b) One of the raw speckle projections acquired with the diffuser and the sample in the beam. (c) Zoomed region of the speckle pattern in panel (b).
Fig. 2.
Fig. 2. Comparison of virtual phase volume slices and H&E-stained histological sections. (a) Long-axis cut through the phase volume (partly in false colors) and (b) corresponding histological slice (H&E staining, $10 \times$ magnification) of the same specimen. (c) and (d) Short-axis cuts through the phase volume [locations indicated in panel (a)] and (f) and (g) corresponding histological slices. The kidney regions, cortex (COR), outer stripe of the outer medulla (OSOM), inner stripe of the outer medulla (ISOM) and inner medulla (IM), can be identified. (e) and (h) Enlarged ROIs from panels (d) and (g) [panel (h) obtained with $20 \times$ magnification] visualizing fine details.
Fig. 3.
Fig. 3. Quantitative density analysis of the phase volume. (a) Slice through the electron density map of the kidney. The small density differences between the regions (COR, OSOM, ISOM, IM) can be resolved (black areas: peri-renal fat). (b) Enlarged ROI (COR/OSOM region) visualizing the network of the renal tubules, blood vessels, and glomeruli (renal corpuscle: glomerulus and surrounding Bowman’s capsule). (c) Histograms of the electron and mass density distributions in the slice. (d) Histograms of the IM, ISOM, OSOM, and COR regions only. Skewed Gaussians were fitted to the histograms (dashed curves). Peak positions (vertical lines) and distribution widths can be found in Table 1.
Fig. 4.
Fig. 4. 3D quantitative density and structural information. (a) Location of a cuboid of interest in the phase volume. (b) 3D rendering of the cuboid. The arrangement of the tubules in the different kidney regions is visualized. Blood vessels (red) and glomeruli (green) can be identified and were segmented from the volume. (c) Line profile along the long axis of the cuboid, showing the mass and electron density values averaged over all slices along the short axes. Glomeruli and vessels were excluded for this analysis.
Fig. 5.
Fig. 5. 3D visualization and segmentation of the phase volume. (a) Renal capsule with ureter (yellow) and surrounding fatty tissue (semi-transparent gray). (b) Vascular network (arteries and veins) of the kidney extracted from the same data set. (c) Combined visualization of vascularization and tissue microstructure. A slice through the phase volume is shown in semi-transparent colors (blue, IM and ISOM; green, OSOM and COR). (d) Location of one renal nephron in the 3D phase volume and (e) segmented nephron consisting of blood vessel supply, glomerulus, and tubule (segmentation was terminated at the onset of the thin limb of the loop of Henle).

Tables (1)

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Table 1. Mass Density Values and Distribution Within the Different Kidney Regionsa,b,c,d

Equations (1)

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Φ x = 2 π λ α x = 2 π λ s x d 2 , Φ y = 2 π λ α y = 2 π λ s y d 2 ,