Abstract

Ischemic stroke is a leading cause of death and permanent disability worldwide. Middle cerebral artery occlusion (MCAO) of variable duration times could be anticipated to result in varying degrees of injury that evolve spatially over time. Therefore, investigations following strokes require information concerning the spatiotemporal dimensions of the ischemic core as well as of perilesional areas. In the present study, multiphoton microscopy (MPM) based on two-photon excited fluorescence (TPEF) and second harmonic generation (SHG) was applied to image such pathophysiological events. The ischemic time-points for evaluation were set at 6, 24, 48, and 72 hours after MCAO. Our results demonstrated that MPM has the ability to not only identify the normal and ischemic brain regions, but also reveal morphological changes of the cortex and striatum at various times following permanent MCAO. These findings corresponded well with the hematoxylin and eosin (H&E) stained tissue images. With the technologic progression of miniaturized imaging devices, MPM can be developed into an effective diagnostic and monitoring tool for ischemic stroke.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref]

2017 (3)

J. Xu, D. Kang, Y. Zeng, S. Zhuo, X. Zhu, L. Jiang, J. Chen, and J. Lin, “Multiphoton microscopy for label-free identification of intramural metastasis in human esophageal squamous cell carcinoma,” Biomed. Opt. Express 8(7), 3360–3368 (2017).
[Crossref] [PubMed]

S. Wang, X. Chen, W. Wu, Z. Chen, H. Du, X. Wang, Y. V. Fu, L. Hu, and J. Chen, “Rapid, label-free identification of cerebellar structures using multiphoton microscopy,” J. Biophotonics 10(12), 1617–1626 (2017).
[Crossref] [PubMed]

O. Uckermann, R. Galli, S. Leupold, R. Coras, M. Meinhardt, S. Hallmeyer-Elgner, T. Mayer, A. Storch, G. Schackert, E. Koch, I. Blümcke, G. Steiner, and M. Kirsch, “Label-free multiphoton microscopy reveals altered tissue architecture in hippocampal sclerosis,” Epilepsia 58(1), e1–e5 (2017).
[Crossref] [PubMed]

2016 (3)

M. Cai, Z. Yu, L. Wang, X. Song, J. Zhang, Z. Zhang, W. Zhang, W. Li, J. Xiang, and D. Cai, “Tongxinluo reduces brain edema and inhibits post-ischemic inflammation after middle cerebral artery occlusion in rats,” J. Ethnopharmacol. 181, 136–145 (2016).
[Crossref] [PubMed]

H. Du, L. Jiang, X. Wang, G. Liu, S. Wang, L. Zheng, L. Li, S. Zhuo, X. Zhu, and J. Chen, “Label-free distinguishing between neurons and glial cells based on two-photon excited fluorescence signal of neuron perinuclear granules,” Laser Phys. Lett. 13(8), 085603 (2016).
[Crossref]

Z. B. Zhou, L. Meng, A. W. Gelb, R. Lee, and W. Q. Huang, “Cerebral ischemia during surgery: an overview,” J. Biomed. Res. 30(2), 83–87 (2016).
[PubMed]

2015 (3)

V. Jolivel, F. Bicker, F. Binamé, R. Ploen, S. Keller, R. Gollan, B. Jurek, J. Birkenstock, L. Poisa-Beiro, J. Bruttger, V. Opitz, S. C. Thal, A. Waisman, T. Bäuerle, M. K. Schäfer, F. Zipp, and M. H. H. Schmidt, “Perivascular microglia promote blood vessel disintegration in the ischemic penumbra,” Acta Neuropathol. 129(2), 279–295 (2015).
[Crossref] [PubMed]

S. Bok, T. Wang, C. J. Lee, S. U. Jeon, Y. E. Kim, J. Kim, B. J. Hong, C. J. Yoon, S. Kim, S. H. Lee, H. J. Kim, I. H. Kim, K. H. Kim, and G. O. Ahn, “In vivo imaging of activated microglia in a mouse model of focal cerebral ischemia by two-photon microscopy,” Biomed. Opt. Express 6(9), 3303–3312 (2015).
[Crossref] [PubMed]

C. J. Schrandt, S. M. S. Kazmi, T. A. Jones, and A. K. Dunn, “Chronic monitoring of vascular progression after ischemic stroke using multiexposure speckle imaging and two-photon fluorescence microscopy,” J. Cereb. Blood Flow Metab. 35(6), 933–942 (2015).
[Crossref] [PubMed]

2014 (4)

Y. Liu, G. Tang, Y. Li, Y. Wang, X. Chen, X. Gu, Z. Zhang, Y. Wang, and G. Y. Yang, “Metformin attenuates blood-brain barrier disruption in mice following middle cerebral artery occlusion,” J. Neuroinflammation 11(1), 177 (2014).
[Crossref] [PubMed]

Q. Hu, X. Liang, D. Chen, Y. Chen, D. Doycheva, J. Tang, J. Tang, and J. H. Zhang, “Delayed hyperbaric oxygen therapy promotes neurogenesis through reactive oxygen species/hypoxia-inducible factor-1α/β-catenin pathway in middle cerebral artery occlusion rats,” Stroke 45(6), 1807–1814 (2014).
[Crossref] [PubMed]

T. Hirano, “Searching for salvageable brain: the detection of ischemic penumbra using various imaging modalities?” J. Stroke Cerebrovasc. Dis. 23(5), 795–798 (2014).
[Crossref] [PubMed]

K. Deguchi, N. Liu, W. Liu, Y. Omote, S. Kono, T. Yunoki, S. Deguchi, T. Yamashita, Y. Ikeda, and K. Abe, “Pericyte protection by edaravone after tissue plasminogen activator treatment in rat cerebral ischemia,” J. Neurosci. Res. 92(11), 1509–1519 (2014).
[Crossref] [PubMed]

2013 (5)

J. Chen, J. Xu, D. Kang, M. Xu, S. Zhuo, X. Zhu, and X. Jiang, “Multiphoton microscopic imaging of histological sections without hematoxylin and eosin staining differentiates carcinoma in situ lesion from normal oesophagus,” Appl. Phys. Lett. 103(18), 183701 (2013).
[Crossref]

X. Zhu, Y. Tang, J. Chen, S. Xiong, S. Zhuo, and J. Chen, “Monitoring wound healing of elastic cartilage using multiphoton microscopy,” Osteoarthritis Cartilage 21(11), 1799–1806 (2013).
[Crossref] [PubMed]

M. A. Yaseen, S. Sakadžić, W. Wu, W. Becker, K. A. Kasischke, and D. A. Boas, “In vivo imaging of cerebral energy metabolism with two-photon fluorescence lifetime microscopy of NADH,” Biomed. Opt. Express 4(2), 307–321 (2013).
[Crossref] [PubMed]

F. Helmchen, W. Denk, and J. N. D. Kerr,“Miniaturization of two-photon microscopy for imaging in freely moving animals,” Cold Spring Harb Protoc. 2013(10), pdb. top078147 (2013).
[Crossref]

S. Psilodimitrakopoulos, V. Petegnief, N. de Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, “Quantitative imaging of microtubule alteration as an early marker of axonal degeneration after ischemia in neurons,” Biophys. J. 104(5), 968–975 (2013).
[Crossref] [PubMed]

2012 (1)

J. Ramos-Cejudo, M. Gutiérrez-Fernández, B. Rodríguez-Frutos, M. Expósito Alcaide, F. Sánchez-Cabo, A. Dopazo, and E. Díez-Tejedor, “Spatial and temporal gene expression differences in core and periinfarct areas in experimental stroke: a microarray analysis,” PLoS One 7(12), e52121 (2012).
[Crossref] [PubMed]

2011 (1)

S. Fumagalli, J. A. Coles, P. Ejlerskov, F. Ortolano, T. J. Bushell, J. M. Brewer, M. G. De Simoni, G. Dever, P. Garside, P. Maffia, and H. V. Carswell, “In vivo real-time multiphoton imaging of T lymphocytes in the mouse brain after experimental stroke,” Stroke 42(5), 1429–1436 (2011).
[Crossref] [PubMed]

2010 (1)

J. G. Merino and S. Warach, “Imaging of acute stroke,” Nat. Rev. Neurol. 6(10), 560–571 (2010).
[Crossref] [PubMed]

2009 (4)

A. Popp, N. Jaenisch, O. W. Witte, and C. Frahm, “Identification of ischemic regions in a rat model of stroke,” PLoS One 4(3), e4764 (2009).
[Crossref] [PubMed]

Q. Liu, J. Chen, S. Zhuo, X. Jiang, and K. Lu, “Nonlinear spectral imaging microscopy of rabbit aortic wall,” Chin. Opt. Lett. 7(3), 240–243 (2009).
[Crossref]

E. Candelario-Jalil, “Injury and repair mechanisms in ischemic stroke: considerations for the development of novel neurotherapeutics,” Curr. Opin. Investig. Drugs 10(7), 644–654 (2009).
[PubMed]

W. Piyawattanametha, E. D. Cocker, L. D. Burns, R. P. Barretto, J. C. Jung, H. Ra, O. Solgaard, and M. J. Schnitzer, “In vivo brain imaging using a portable 2.9 g two-photon microscope based on a microelectromechanical systems scanning mirror,” Opt. Lett. 34(15), 2309–2311 (2009).
[Crossref] [PubMed]

2008 (2)

S. W. Hou, Y. Q. Wang, M. Xu, D. H. Shen, J. J. Wang, F. Huang, Z. Yu, and F. Y. Sun, “Functional integration of newly generated neurons into striatum after cerebral ischemia in the adult rat brain,” Stroke 39(10), 2837–2844 (2008).
[Crossref] [PubMed]

T. H. Chia, A. Williamson, D. D. Spencer, and M. J. Levene, “Multiphoton fluorescence lifetime imaging of intrinsic fluorescence in human and rat brain tissue reveals spatially distinct NADH binding,” Opt. Express 16(6), 4237–4249 (2008).
[Crossref] [PubMed]

2006 (1)

M. Wintermark, A. E. Flanders, B. Velthuis, R. Meuli, M. van Leeuwen, D. Goldsher, C. Pineda, J. Serena, I. van der Schaaf, A. Waaijer, J. Anderson, G. Nesbit, I. Gabriely, V. Medina, A. Quiles, S. Pohlman, M. Quist, P. Schnyder, J. Bogousslavsky, W. P. Dillon, and S. Pedraza, “Perfusion-CT assessment of infarct core and penumbra: receiver operating characteristic curve analysis in 130 patients suspected of acute hemispheric stroke,” Stroke 37(4), 979–985 (2006).
[Crossref] [PubMed]

2003 (3)

D. A. Dombeck, K. A. Kasischke, H. D. Vishwasrao, M. Ingelsson, B. T. Hyman, and W. W. Webb, “Uniform polarity microtubule assemblies imaged in native brain tissue by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7081–7086 (2003).
[Crossref] [PubMed]

W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, “Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075–7080 (2003).
[Crossref] [PubMed]

C. S. Kidwell, J. R. Alger, and J. L. Saver, “Beyond mismatch: evolving paradigms in imaging the ischemic penumbra with multimodal magnetic resonance imaging,” Stroke 34(11), 2729–2735 (2003).
[Crossref] [PubMed]

2002 (2)

T. L. Butler, C. A. Kassed, P. R. Sanberg, A. E. Willing, and K. R. Pennypacker, “Neurodegeneration in the rat hippocampus and striatum after middle cerebral artery occlusion,” Brain Res. 929(2), 252–260 (2002).
[Crossref] [PubMed]

A. Arvidsson, T. Collin, D. Kirik, Z. Kokaia, and O. Lindvall, “Neuronal replacement from endogenous precursors in the adult brain after stroke,” Nat. Med. 8(9), 963–970 (2002).
[Crossref] [PubMed]

1999 (2)

P. Lipton, “Ischemic cell death in brain neurons,” Physiol. Rev. 79(4), 1431–1568 (1999).
[Crossref] [PubMed]

U. Dirnagl, C. Iadecola, and M. A. Moskowitz, “Pathobiology of ischaemic stroke: an integrated view,” Trends Neurosci. 22(9), 391–397 (1999).
[Crossref] [PubMed]

1998 (2)

D. Aggoun-Zouaoui, I. Margalli, F. Borrega, A. Represa, M. Plotkine, Y. Ben-Ari, and C. Charriaut-Marlangue, “Ultrastructural morphology of neuronal death following reversible focal ischemia in the rat,” Apoptosis 3(2), 133–141 (1998).
[Crossref] [PubMed]

Y. Li, C. Powers, N. Jiang, and M. Chopp, “Intact, injured, necrotic and apoptotic cells after focal cerebral ischemia in the rat,” J. Neurol. Sci. 156(2), 119–132 (1998).
[Crossref] [PubMed]

1996 (1)

M. Tsacopoulos and P. J. Magistretti, “Metabolic coupling between glia and neurons,” J. Neurosci. 16(3), 877–885 (1996).
[Crossref] [PubMed]

1989 (1)

E. Z. Longa, P. R. Weinstein, S. Carlson, and R. Cummins, “Reversible middle cerebral artery occlusion without craniectomy in rats,” Stroke 20(1), 84–91 (1989).
[Crossref] [PubMed]

1986 (1)

J. Koizumi, Y. Yoshida, T. Nakazawa, and G. Ooneda, “Experimental studies of ischemic brain edema, I: a new experimental model of cerebral embolism in rats in which recirculation can be introduced in the ischemic area,” Jpn. J. Stroke 8(1), 1–8 (1986).
[Crossref]

1984 (1)

J. C. Baron, D. Rougemont, F. Soussaline, P. Bustany, C. Crouzel, M. G. Bousser, and D. Comar, “Local interrelationships of cerebral oxygen consumption and glucose utilization in normal subjects and in ischemic stroke patients: a positron tomography study,” J. Cereb. Blood Flow Metab. 4(2), 140–149 (1984).
[Crossref] [PubMed]

1965 (1)

B. Chance and B. Schoener, “A correlation of absorption and fluorescence changes in ischemia of rat liver in vivo,” Biochem. Z. 341(4), 340 (1965).

1964 (1)

A. Coimbra, “Nerve cell changes in the experimental occlusion of the middle cerebral artery,” Acta Neuropathol. 3(6), 547–557 (1964).
[Crossref]

Abe, K.

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Figures (6)

Fig. 1
Fig. 1 (A) The diagram of sample preparation. (B) The sequence of the five H&E stained coronal sections (4 × magnification) at 6 hours after permanent MCAO. The boundary between infarction and normal brain was marked with a black solid line. (C) The percentage of infarct area at various times shows significantly increased infarction with increasing occlusion duration.
Fig. 2
Fig. 2 TPEF images of cerebral cortex from (A) a normal brain section, (B) an infarct core, and (C) a partial edge of the infarction. The color bar indicates the minimum and maximum signal intensities. The corresponding H&E stained images of cerebral cortex from (D) a normal brain section, (E) the infarct core, and (F) the partial edge of the infarction. Inset frame in (A): representative neurons and glial cells. Normal neurons: white arrowheads; injured neurons: yellow arrowheads; glial cells: arrows; white dashed lines: the boundary between normal and infarct area. The color bar indicates the range of TPEF intensity.
Fig. 3
Fig. 3 TPEF (A-D) and corresponding H&E stained images (E-H) of neuronal necrosis in the cerebral cortex varied with occlusion duration of 6, 24, 48, and 72 hours after MCAO. (I) Average area of neuronal nuclei. (J) TPEF intensity of neuronal cytoplasm. Inset frames: representative magnified injured neurons; Normal neurons: white arrowheads; injured neurons: yellow arrowheads.
Fig. 4
Fig. 4 The emission spectrum of cortex and striatum at an excitation wavelength of 810 nm.
Fig. 5
Fig. 5 TPEF, SHG, their overlaid images, and corresponding H&E stained images of striatum sectioned in the coronal plane of normal and ischemic rat brain at 6, 24, 48, and 72 hours after MCAO. (A-E): TPEF image (red); (F-J): SHG image (green); (K-L): overlaid images; (P-T): corresponding H&E stained images. Axon bundles: asterisk; neurons: white arrowheads; injured neurons: yellow arrowheads.
Fig. 6
Fig. 6 The nuclear-to-cytoplasmic ratio of neurons in cortex (A) and striatum (B)varied with occlusion duration. The ratio of injured neurons over normal neurons in cortex (C) and striatum (D) varied with occlusion duration.

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