In Vivo Assessment of Deep Vascular Patterns in Murine Colitis Using Optoacoustic Mesoscopic Imaging.

dextran sodium sulfate induced colitis inflammatory bowel disease murine acute colitis optoacoustic imaging photoacoustic imaging raster‐scanning optoacoustic mesoscopy vessel morphology analysis

Journal

Advanced science (Weinheim, Baden-Wurttemberg, Germany)
ISSN: 2198-3844
Titre abrégé: Adv Sci (Weinh)
Pays: Germany
ID NLM: 101664569

Informations de publication

Date de publication:
22 Oct 2024
Historique:
revised: 15 08 2024
received: 29 04 2024
medline: 23 10 2024
pubmed: 23 10 2024
entrez: 23 10 2024
Statut: aheadofprint

Résumé

The analysis of vascular morphology and functionality enables the assessment of disease activity and therapeutic effects in various pathologies. Raster-scanning optoacoustic mesoscopy (RSOM) is an imaging modality that enables the visualization of superficial vascular networks in vivo. In murine models of colitis, deep vascular networks in the colon wall can be visualized by transrectal absorber guide raster-scanning optoacoustic mesoscopy (TAG-RSOM). In order to accelerate the implementation of this technology in translational studies of inflammatory bowel disease, an image-processing pipeline for TAG-RSOM data has been developed. Using optoacoustic data from a murine model of chemically-induced colitis, different image segmentation methods are compared for visualization and quantification of deep vascular patterns in terms of vascular network length and complexity, blood volume, and vessel diameter. The presented image-processing pipeline for TAG-RSOM enables label-free in vivo assessment of changes in the vascular network in murine colitis with broad applications for inflammatory bowel disease research.

Identifiants

pubmed: 39439243
doi: 10.1002/advs.202404618
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2404618

Subventions

Organisme : Else Kröner-Fresenius-Stiftung
Organisme : Cancer Research UK
ID : C9545/A29580
Pays : United Kingdom

Informations de copyright

© 2024 The Author(s). Advanced Science published by Wiley‐VCH GmbH.

Références

a) A. E. Larsson, S. Melgar, E. Rehnstrom, E. Michaelsson, L. Svensson, P. Hockings, L. E. Olsson, Inflamm Bowel Dis 2006, 12, 478;
b) D. Jung, R. Heiss, V. Kramer, O. M. Thoma, A. P. Regensburger, W. Rascher, M. Uder, M. F. Neurath, F. Knieling, M. J. Waldner, Theranostics 2018, 8, 6357.
A. Hoerning, J. Jungert, G. Siebenlist, F. Knieling, A. P. Regensburger, Children (Basel) 2024, 11, 156.
D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, V. Ntziachristos, Nat. Photonics 2009, 3, 412.
A. A. Oraevsky, S. L. Jacques R. O. Esenaliev, F. K. Tittel, Laser‐Tissue Interaction V; and Ultraviolet Radiation Hazards, Vol. 2134, SPIE, 1994, pp. 122–128.
L. V. Wang, J. Yao, Nat. Methods 2016, 13, 627.
S. Tzoumas, N. Deliolanis, S. Morscher, V. Ntziachristos, IEEE Trans Med Imaging 2014, 33, 48.
A. Karlas, N. A. Fasoula, K. Paul‐Yuan, J. Reber, M. Kallmayer, D. Bozhko, M. Seeger, H. H. Eckstein, M. Wildgruber, V. Ntziachristos, Photoacoustics 2019, 14, 19.
A. P. Regensburger, E. Brown, G. Kronke, M. J. Waldner, F. Knieling, Biomedicines 2021, 9, 483.
A. B. E. Attia, G. Balasundaram, M. Moothanchery, U. S. Dinish, R. Bi, V. Ntziachristos, M. Olivo, Photoacoustics 2019, 16, 100144.
a) F. Knieling, C. Neufert, A. Hartmann, J. Claussen, A. Urich, C. Egger, M. Vetter, S. Fischer, L. Pfeifer, A. Hagel, C. Kielisch, R. S. Gortz, D. Wildner, M. Engel, J. Rother, W. Uter, J. Siebler, R. Atreya, W. Rascher, D. Strobel, M. F. Neurath, M. J. Waldner, N. Engl. J. Med. 2017, 376, 1292;
b) A. P. Regensburger, M. Eckstein, M. Wetzl, R. Raming, L.‐P. Paulus, A. Buehler, E. Nedoschill, V. Danko, J. Jüngert, A. L. Wagner, A. Schnell, A. Rückel, U. Rother, O. Rompel, M. Uder, A. Hartmann, M. F. Neurath, J. Woelfle, M. J. Waldner, A. Hoerning, F. Knieling, Photoacoustics 2024, 35, 100578.
N. Britzen‐Laurent, C. Weidinger, M. Sturzl, Int. J. Mol. Sci. 2023, 24, 5517.
A. Buehler, E. Brown, L. P. Paulus, M. Eckstein, O. M. Thoma, M. E. Oraiopoulou, U. Rother, A. Hoerning, A. Hartmann, M. F. Neurath, J. Woelfle, O. Friedrich, M. J. Waldner, F. Knieling, S. E. Bohndiek, A. P. Regensburger, Adv. Sci. 2023, 10, e2300564.
E. L. Brown, T. L. Lefebvre, P. W. Sweeney, B. J. Stolz, J. Gröhl, L. Hacker, Z. Huang, D. L. Couturier, H. A. Harrington, H. M. Byrne, S. E. Bohndiek, Photoacoustics 2022, 26, 100357.
M. Schwarz, D. Soliman, M. Omar, A. Buehler, S. V. Ovsepian, J. Aguirre, V. Ntziachristos, IEEE Trans Med Imaging 2017, 36, 1287.
A. F. Frangi, W. J. Niessen, K. L. Vincken, M. A. Viergever, in Medical Image Computing and Computer‐Assisted Intervention—MICCAI’98: First International Conference Cambridge, MA, USA, October, 1998.
K. Haedicke, L. Agemy, M. Omar, A. Berezhnoi, S. Roberts, C. Longo‐Machado, M. Skubal, K. Nagar, H. T. Hsu, K. Kim, T. Reiner, J. Coleman, V. Ntziachristos, A. Scherz, J. Grimm, Nat. Biomed. Eng. 2020, 4, 286.
W. Liu, K. M. Schultz, K. Zhang, A. Sasman, F. Gao, T. Kume, H. F. Zhang, Photoacoustics 2014, 2, 81.
a) D. Razansky, J. Klohs, R. Ni, Eur. J. Nucl. Med. Mol. Imaging 2021, 48, 4152;
b) J. Yao, L. V. Wang, Neurophotonics 2014, 1, 011003.
T. Oruganti, A. A., J. G. Laufer, L. V., B. E. Treeby, Photons Plus Ultrasound: Imaging and Sensing 2013, Vol. 8581, SPIE 2013, pp. 319–328.
H. Saijo, N. Tatsumi, S. Arihiro, T. Kato, M. Okabe, H. Tajiri, H. Hashimoto, Lab Invest 2015, 95, 728.
S. Danese, M. Sans, D. M. Spencer, I. Beck, F. Donate, M. L. Plunkett, C. de la Motte, R. Redline, D. E. Shaw, A. D. Levine, A. P. Mazar, C. Fiocchi, Gut 2007, 56, 855.
O. A. Hatoum, D. G. Binion, M. F. Otterson, D. D. Gutterman, Gastroenterology 2003, 125, 58.
S. Danese, M. Sans, C. de la Motte, C. Graziani, G. West, M. H. Phillips, R. Pola, S. Rutella, J. Willis, A. Gasbarrini, C. Fiocchi, Gastroenterology 2006, 130, 2060.
a) M. Mori, K. Y. Stokes, T. Vowinkel, N. Watanabe, J. W. Elrod, N. R. Harris, D. J. Lefer, T. Hibi, D. N. Granger, Am J Physiol Gastrointest Liver Physiol 2005, 289, G1024;
b) T. Foitzik, M. Kruschewski, A. Kroesen, H. J. Buhr, Int. J. Colorectal Dis. 1999, 14, 29.
L. Kreiss, O. M. Thoma, A. Dilipkumar, B. Carle, P. Longequeue, T. Kunert, T. Rath, K. Hildner, C. Neufert, M. Vieth, M. F. Neurath, O. Friedrich, S. Schurmann, M. J. Waldner, Gastroenterology 2020, 159, 832.
Y. Li, S. Lu, Y. Zhang, J. Li, L. Xiong, Adv. Healthcare Mater. 2022, 11, 2200978.
M. Hirata, S. Tanaka, S. Oka, I. Kaneko, S. Yoshida, M. Yoshihara, K. Chayama, Gastrointest. Endosc. 2007, 66, 945.
C.‐L. Tsai, J.‐C. Chen, W.‐J. Wang, J. Biol. Eng. 2001, 21, 7.
B. Cox, J. G. Laufer, S. R. Arridge, P. C. Beard, J. Biomed. Opt. 2012, 17, 061202.
L. P. Paulus, A. Buehler, A. L. Wagner, R. Raming, J. Jüngert, D. Simon, K. Tascilar, A. Schnell, U. Rother, M. Eckstein, Adv. Sci. 2023, 10, 2302562.
a) J. M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, L. V. Wang, Nat. Med. 2012, 18, 1297;
b) H. He, A. Stylogiannis, P. Afshari, T. Wiedemann, K. Steiger, A. Buehler, C. Zakian, V. Ntziachristos, J Biophotonics 2019, 12, e201800439;
c) D. J. Waterhouse, S. Bano, W. Januszewicz, D. Stoyanov, R. C. Fitzgerald, M. di Pietro, S. E. Bohndiek, J. Biomed. Opt. 2021, 26, 106002.
P. Bankhead, M. B. Loughrey, J. A. Fernandez, Y. Dombrowski, D. G. McArt, P. D. Dunne, S. McQuaid, R. T. Gray, L. J. Murray, H. G. Coleman, J. A. James, M. Salto‐Tellez, P. W. Hamilton, Sci. Rep. 2017, 7, 16878.
S. R. Sternberg, Computer 1983, 16, 22.
M. Rashed, E. A. Rashed, Comput. Geosci. 2017, 102, 12.
S. Berg, D. Kutra, T. Kroeger, C. N. Straehle, B. X. Kausler, C. Haubold, M. Schiegg, J. Ales, T. Beier, M. Rudy, K. Eren, J. I. Cervantes, B. Xu, F. Beuttenmueller, A. Wolny, C. Zhang, U. Koethe, F. A. Hamprecht, A. Kreshuk, Nat. Methods 2019, 16, 1226.

Auteurs

Adrian Buehler (A)

Department of Pediatrics and Adolescent Medicine, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Emma L Brown (EL)

Cancer Research UK Cambridge Institute, University of Cambridge, CB2 0RE, Cambridge, United Kingdom.

Emmanuel Nedoschill (E)

Department of Pediatrics and Adolescent Medicine, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Markus Eckstein (M)

Institute of Pathology, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Petra Ludwig (P)

Department of Pediatrics and Adolescent Medicine, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Felix Wachter (F)

Department of Pediatrics and Adolescent Medicine, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Henriette Mandelbaum (H)

Department of Pediatrics and Adolescent Medicine, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Roman Raming (R)

Department of Pediatrics and Adolescent Medicine, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Mariam-Eleni Oraiopoulou (ME)

Cancer Research UK Cambridge Institute, University of Cambridge, CB2 0RE, Cambridge, United Kingdom.

Lars-Philip Paulus (LP)

Department of Pediatrics and Adolescent Medicine, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Ulrich Rother (U)

Department of Vascular Surgery, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Oliver Friedrich (O)

Institute of Medical Biotechnology, Department of Chemical and Biological Engineering, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91052, Erlangen, Germany.

Markus F Neurath (MF)

Department of Medicine 1, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91052, Erlangen, Germany.

Joachim Woelfle (J)

Department of Pediatrics and Adolescent Medicine, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Maximilian J Waldner (MJ)

Department of Medicine 1, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91052, Erlangen, Germany.

Ferdinand Knieling (F)

Department of Pediatrics and Adolescent Medicine, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Sarah E Bohndiek (SE)

Cancer Research UK Cambridge Institute, University of Cambridge, CB2 0RE, Cambridge, United Kingdom.

Adrian P Regensburger (AP)

Department of Pediatrics and Adolescent Medicine, University Hospital Erlangen, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, 91054, Erlangen, Germany.

Classifications MeSH