Quantitative ptychographic bio-imaging in the water window

Max Rose; Tobias Senkbeil; Andreas R. von Gundlach; Susan Stuhr; Christoph Rumancev; Dmitry Dzhigaev; Ilya Besedin; Petr Skopintsev; Lars Loetgering; Jens Viefhaus; Axel Rosenhahn; Ivan A. Vartanyants

doi:10.1364/OE.26.001237

Quantitative ptychographic bio-imaging in the water window

Max Rose, Tobias Senkbeil, Andreas R. von Gundlach, Susan Stuhr, Christoph Rumancev, Dmitry Dzhigaev, Ilya Besedin, Petr Skopintsev, Lars Loetgering, Jens Viefhaus, Axel Rosenhahn, and Ivan A. Vartanyants

Optics Express
Vol. 26,
Issue 2,
pp. 1237-1254
(2018)
•https://doi.org/10.1364/OE.26.001237

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Max Rose, Tobias Senkbeil, Andreas R. von Gundlach, Susan Stuhr, Christoph Rumancev, Dmitry Dzhigaev, Ilya Besedin, Petr Skopintsev, Lars Loetgering, Jens Viefhaus, Axel Rosenhahn, and Ivan A. Vartanyants, "Quantitative ptychographic bio-imaging in the water window," Opt. Express 26, 1237-1254 (2018)

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Related Topics
Table of Contents Category
- Imaging Systems and Displays
Optics & Photonics Topics
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The topics in this list come from the OSA Optics and Photonics Topics applied to this article.
Previously assigned OCIS codes
- Coherence imaging (110.1650)
- Partial coherence in imaging (110.4980)
- X-ray imaging (340.7440)
- X-ray microscopy (340.7460)
- X-rays, soft x-rays, extreme ultraviolet (EUV) (340.7480)

About this Article
History
- Original Manuscript: September 5, 2017
- Revised Manuscript: October 28, 2017
- Manuscript Accepted: November 5, 2017
- Published: January 11, 2018
Virtual Issues
Virtual Journal for Biomedical Optics Vol. 13, Iss. 3

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Abstract

Coherent X-ray ptychography is a tool for highly dose efficient lensless nano-imaging of biological samples. We have used partially coherent soft X-ray synchrotron radiation to obtain a quantitative image of a laterally extended, dried, and unstained fibroblast cell by ptychography. We used data with and without a beam stop that allowed us to measure coherent diffraction with a high-dynamic range of 1.7·10⁶. As a quantitative result, we obtained the refractive index values for two regions of the cell with respect to a reference area. Due to the photon energy in the water window we obtained an extremely high contrast of 53% at 71 nm half-period resolution. The dose applied in our experiment was 9.5·10⁴ Gy and is well below the radiation damage threshold. The concept for dynamic range improvement for low dynamic range detectors with a beam stop opens the path for high resolution nano-imaging of a variety of samples including cryo-preserved, hydrated and unstained biological cells.

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2017 (5)

Recently it was claimed that although the ePIE algorithm exhibits improved reconstruction speed, it is easy to come across situations when the difficulties of experimental nature may render certain data more difficult to reconstruct. SeeA. Maiden, D. Johnson, and Peng Li, “Further improvements to the ptychographical iterative engine,” Optica 4, 736 (2017).
[Crossref]

H. K. Reddy, C. H. Yoon, A. Aquila, S. Awel, K. Ayyer, A. Barty, P. Berntsen, J. Bielecki, S. Bobkov, M. Bucher, G. A. Carini, S. Carron, H. Chapman, B. Daurer, H. DeMirci, T. Ekeberg, P. Fromme, J. Hajdu, M. F. Hanke, P. Hart, B. G. Hogue, A. Hosseinizadeh, Y. Kim, R. A. Kirian, R. P. Kurta, D. S. Larsson, N. D. Loh, F. R. Maia, A. P. Mancuso, K. Mühlig, A. Munke, D. Nam, C. Nettelblad, A. Ourmazd, M. Rose, P. Schwander, M. Seibert, J. A. Sellberg, C. Song, J. C. Spence, M. Svenda, G. V. der Schot, I. A. Vartanyants, G. J. Williams, and P. L. Xavier, “Coherent soft x-ray diffraction imaging of coliphage pr772 at the linac coherent light source,” Sci. Data 4, 170079 (2017).
[Crossref] [PubMed]

M. Rose, D. Dzhigaev, T. Senkbeil, A. R. von Gundlach, S. Stuhr, C. Rumancev, I. Besedin, P. Skopintsev, J. Viefhaus, A. Rosenhahn, and I. A. Vartanyants, “High-dynamic-range water window ptychography,” J. Phys: Conf. Ser. 849, 012027 (2017).

J. Reinhardt, R. Hoppe, G. Hofmann, C. D. Damsgaard, J. Patommel, C. Baumbach, S. Baier, A. Rochet, J.-D. Grunwaldt, G. Falkenberg, and C. Schroer, “Beamstop-based low-background ptychography to image weakly scattering objects,” Ultramicroscopy 173, 52–57 (2017).
[Crossref]

S. H. Shahmoradian, E. H. R. Tsai, A. Diaz, M. Guizar-Sicairos, J. Raabe, L. Spycher, M. Britschgi, A. Ruf, H. Stahlberg, and M. Holler, “Three-dimensional imaging of biological tissue by cryo x-ray ptychography,” Sci. Rep. 7, 6291 (2017).
[Crossref] [PubMed]

2016 (3)

A. Khromova, G. Cautero, D. Giuressi, R. Menk, G. Pinaroli, L. Stebel, J. Correa, A. Marras, C. Wunderer, S. Lange, M. Tennert, M. Niemann, H. Hirsemann, S. Smoljanin, S. Reza, H. Graafsma, P. Göttlicher, I. Shevyakov, J. Supra, Q. Xia, M. Zimmer, N. Guerrini, B. Marsh, I. Sedgwick, T. Nicholls, R. Turchetta, U. Pedersen, N. Tartoni, H. Hyun, K. Kim, S. Rah, M. Hoenk, A. Jewell, T. Jones, and S. Nikzad, “Report on recent results of the PERCIVAL soft x-ray imager,” J. Instrum. 11, C11020 (2016).
[Crossref]

C. Y. J. Hémonnot, J. Reinhardt, O. Saldanha, J. Patommel, R. Graceffa, B. Weinhausen, M. Burghammer, C. G. Schroer, and S. Köster, “X-rays reveal the internal structure of keratin bundles in whole cells,” ACS Nano 10, 3553–3561 (2016).
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2015 (8)

K. Giewekemeyer, C. Hackenberg, A. Aquila, R. Wilke, M. Groves, R. Jordanova, V. Lamzin, G. Borchers, K. Saksl, A. Zozulya, M. Sprung, and A. Mancuso, “Tomography of a cryo-immobilized yeast cell using ptychographic coherent x-ray diffractive imaging,” Biophys. J. 109, 1986–1995 (2015).
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M. Rose, P. Skopintsev, D. Dzhigaev, O. Gorobtsov, T. Senkbeil, A. von Gundlach, T. Gorniak, A. Shabalin, J. Viefhaus, A. Rosenhahn, and I. Vartanyants, “Water window ptychographic imaging with characterized coherent x-rays,” J. Synchrotron Radiat. 22, 819–827 (2015).
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J. A. Rodriguez, R. Xu, C.-C. Chen, Z. Huang, H. Jiang, A. L. Chen, K. S. Raines, A. Pryor, D. Nam, L. Wiegart, C. Song, A. Madsen, Y. Chushkin, F. Zontone, P. J. Bradley, and J. Miao, “Three-dimensional coherent x-ray diffractive imaging of whole frozen-hydrated cells,” IUCrJ 2, 575–583 (2015).
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A. Aquila, A. Barty, C. Bostedt, S. Boutet, G. Carini, D. dePonte, P. Drell, S. Doniach, K. H. Downing, T. Earnest, H. Elmlund, V. Elser, M. Gühr, J. Hajdu, J. Hastings, S. P. Hau-Riege, Z. Huang, E. E. Lattman, F. R. N. C. Maia, S. Marchesini, A. Ourmazd, C. Pellegrini, R. Santra, I. Schlichting, C. Schroer, J. C. H. Spence, I. A. Vartanyants, S. Wakatsuki, W. I. Weis, and G. J. Williams, “The linac coherent light source single particle imaging road map,” Struct. Dyn. 2, 041701 (2015).
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J. Deng, D. J. Vine, S. Chen, Y. S. G. Nashed, Q. Jin, N. W. Phillips, T. Peterka, R. Ross, S. Vogt, and C. J. Jacobsen, “Simultaneous cryo x-ray ptychographic and fluorescence microscopy of green algae,” Proc. Natl. Acad. Sci. U.S.A. 112, 2314–2319 (2015).
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2014 (3)

T. Gorniak and A. Rosenhahn, “Ptychographic x-ray microscopy with the vacuum imaging apparatus HORST,” Z. Phys. Chem. 228, 1089(2014).
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2013 (5)

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2012 (1)

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2011 (2)

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2010 (3)

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2008 (2)

P. Thibault, M. Dierolf, A. Menzel, O. Bunk, C. David, and F. Pfeiffer, “High-resolution scanning x-ray diffraction microscopy,” Science 321, 379–382 (2008).
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2007 (3)

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2006 (2)

H. N. Chapman, A. Barty, S. Marchesini, A. Noy, S. P. Hau-Riege, C. Cui, M. R. Howells, R. Rosen, H. He, J. C. H. Spence, U. Weierstall, T. Beetz, C. Jacobsen, and D. Shapiro, “High-resolution ab initio three-dimensional x-ray diffraction microscopy,” J. Opt. Soc. Am. A 23, 1179–1200 (2006).
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2005 (1)

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2003 (2)

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2002 (2)

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2000 (1)

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1999 (1)

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J. Als-Nielsen and D. McMorrow, Elements of Modern X-ray Physics (Wiley, 2001).

S. Marchesini, H. N. Chapman, A. Barty, C. Cui, M. R. Howells, J. C. H. Spence, U. Weierstall, and A. M. Minor, “Phase Aberrations in Diffraction Microscopy,” ArXiv Physics e-prints (2005).

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Fig. 1 Experimental geometry inside the HORST chamber for the ptychographic imaging experiment. A beam stop is located on a Si₃N₄ membrane (transparent layer) in front of the detector for dynamic range improvement.

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Fig. 2 Diffraction pattern of a single position of the fibroblast cell without beam stop a) and with semitransparent beam stop b). The white circles mark the effective signal cut-off with the corresponding spatial frequency. The diffraction patterns are shown on the same logarithmic scale.

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Fig. 3 Fibroblast cell images. a) Visible light image with the ptychography scan area marked by the white rectangle. b) Reconstructed fibroblast cell phase of the double exposure HDR data. Regions N (nucleus) and Nu (nucleolus) are quantitatively analyzed with respect to a reference area outside the cell marked by R. c) An enlarged view of the region shown by the black square in b) shows the cells fibrous cytoskeleton and dot structures. The red line denotes a profile used for contrast evaluation.

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Fig. 4 Contrast profile line perpendicular to several aligned filament bundles along the red line in Fig. 3(c). Red and blue markers denote the maximum and minimum phase shift between the filament bundles.

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Fig. 5 Histograms of quantitatively measured transmission a) and phase values b) from two regions. The ratio of the refraction and absorption coefficient is given in c). Mean values of the measurements are indicated by black dashed and solid lines and the literature value for a typical protein compound is indicated by the red line.

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Fig. 6 wPRTF for the ptychographic fibroblast cell reconstructions. The reconstruction yielded 250 nm half-period resolution from single exposure data and 54 nm from HDR data.

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Fig. 7 Power spectral density for both measured data sets and the HDR data set. The dynamic range was improved by roughly two orders of magnitude as indicated by the inset number to the right.

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Fig. 8 Probe modes and corresponding energies ε_l. Hue encodes the phase and brightness the modulus as indicated by the color wheel in the lower right corner.

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Fig. 9 Reconstructed and propagated illumination intensity as the sum over all modes a). Intensity distribution in the pinhole b) and the sample plane c).

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Fig. 10 Reconstructed fibroblast cell phase of the single exposure data without beam stop a). Unwrapping artifacts arise due to the low SNR. The magnified view without unwrapping artifacts show only low resolution without the cell details b).

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Tables (1)

Table 1 Quantitative transmission and phase values for cell regions.

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Equations (21)

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W (r_{1}, r_{2}) = \sum_{l} β_{l} P_{l}^{*} (r_{1}) P_{l} (r_{2}),

ψ_{i, l} = β_{l} P_{l} \cdot O_{i} .

\begin{array}{l} I_{i} = \sum_{l} {| F {ψ_{i, l}} |}^{2} \end{array}

\begin{array}{l} = \sum_{l} β_{l}^{2} {| F {P_{l} \cdot O_{i}} |}^{2}, \end{array}

O (r) = e^{- \frac{1}{2} μ Δ z (r)} \cdot e^{- i Δ φ (r)},

C = \frac{φ_{m a x} - φ_{m i n}}{φ_{m a x} + φ_{m i n}} .

ψ_{j} (r) = P (r - r_{j}) \cdot O_{j} (r), \forall j

I_{j} = {| F {ψ_{j}} |}^{2}, \forall j

O^{n + 1} (r) = \frac{\sum_{j} \bar{P^{n}} (r - r_{j}) ψ_{j}^{n + 1} (r)}{\sum_{j} {| P^{n} (r - r_{j}) |}^{2}}

P^{n + 1} (r) = \frac{\sum_{j} \bar{O^{n}} (r + r_{j}) ψ_{j}^{n + 1} (r + r_{j})}{\sum_{j} {| O^{n} (r - r_{j}) |}^{2}},

ψ_{j}^{n + 1} (r) = ψ_{j}^{n} + π_{F} [2 π_{O} (ψ_{j}^{n}) - ψ_{j}^{n}] - π_{O} [ψ_{j}^{n}]

π_{O} [ψ_{j}^{n} (r)] = P^{n} (r - r_{j}) \cdot O_{j}^{n} (r)

π_{F} [ψ_{j}^{n}] = F^{- 1} (\sqrt{I_{j}} \frac{F ψ_{j}}{| F ψ_{j} |}) .

O^{n + 1} (r) = O^{n} (r) + β_{O} \frac{\bar{P^{n}}}{\max {| \bar{P^{n}} |}^{2}} (ψ_{j}^{n + 1} - ψ_{j}^{n})

P^{n + 1} = P^{n} + β_{P} \frac{\bar{O^{n}}}{\max {| \bar{O^{n}} |}^{2}} (ψ_{j}^{n + 1} - ψ_{j}^{n}),

ψ_{j}^{n + 1} = π_{F} [P^{n} (r - r_{j}) \cdot O (r)]

ψ_{j}^{n} = P^{n} (r - r_{j}) \cdot O (r) .

O^{n + 1} (r) = O^{n} (r) + β_{O} \frac{\bar{P^{n}}}{\max {| \bar{P^{n}} |}^{2}} (ψ_{j}^{n + 1} - ψ_{j}^{n})

P^{n + 1} = P^{n} + β_{P} \frac{\bar{O^{n}}}{\max {| \bar{O^{n}} |}^{2}} (ψ_{j}^{n + 1} - ψ_{j}^{n}) .

ψ_{j}^{n + 1} = π_{M} [P^{n} O_{j}^{n}] + π_{M} [2 P^{n} O_{j}^{n} - π_{M} (P^{n} O_{j}^{n})] - P^{n} O_{j}^{n},

e ~ \sum_{j} {(| ψ_{j}^{n + 1} | - | π_{M} [P^{n} O_{j}^{n}] |)}^{2} .

	region	T_mean	Δφ_mean [rad]	(δ/β)_mean
nucleus	N	0.36	−4.01	3.95
nucleolus	Nu	0.26	−5.21	3.91