X-ray Phase Contrast Allows Three Dimensional, Quantitative Imaging of Hydrogel Implants
Abstract
Three dimensional imaging techniques are needed for the evaluation and assessment of biomaterials used for tissue engineering and drug delivery applications. Hydrogels are a particularly popular class of materials for medical applications but are difficult to image in tissue using most available imaging modalities. Imaging techniques based on X-ray Phase Contrast (XPC) have shown promise for tissue engineering applications due to their ability to provide image contrast based on multiple X-ray properties. In this manuscript we describe results using XPC to image a model hydrogel and soft tissue structure. Porous fibrin loaded poly(ethylene glycol) hydrogels were synthesized and implanted in a rodent subcutaneous model. Samples were explanted and imaged with an analyzer-based XPC technique and processed and stained for histology for comparison. Both hydrogel and soft tissues structures could be identified in XPC images. Structure in skeletal muscle adjacent could be visualized and invading fibrovascular tissue could be quantified. In quantitative results, there were no differences between XPC and the gold-standard histological measurements. These results provide evidence of the significant potential of techniques based on XPC for 3D imaging of hydrogel structure and local tissue response.
- Authors:
-
- Illinois Inst. of Technology, Chicago, IL (United States); Edward Hines Jr. VA Hospital, Hines, IL (United States)
- Brookhaven National Lab. (BNL), Upton, NY (United States). National Synchrotron Light Source
- Washington Univ., St. Louis, MO (United States)
- Illinois Inst. of Technology, Chicago, IL (United States)
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1341637
- Report Number(s):
- BNL-113346-2016-JA
Journal ID: ISSN 0090-6964
- Grant/Contract Number:
- SC00112704
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Annals of Biomedical Engineering
- Additional Journal Information:
- Journal Volume: 44; Journal Issue: 3; Journal ID: ISSN 0090-6964
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; X-ray phase contrast; imaging; hydrogels; tissue engineering; micro-computed tomography
Citation Formats
Appel, Alyssa A., Larson, Jeffrey C., Jiang, Bin, Zhong, Zhong, Anastasio, Mark A., and Brey, Eric M. X-ray Phase Contrast Allows Three Dimensional, Quantitative Imaging of Hydrogel Implants. United States: N. p., 2015.
Web. doi:10.1007/s10439-015-1482-5.
Appel, Alyssa A., Larson, Jeffrey C., Jiang, Bin, Zhong, Zhong, Anastasio, Mark A., & Brey, Eric M. X-ray Phase Contrast Allows Three Dimensional, Quantitative Imaging of Hydrogel Implants. United States. https://doi.org/10.1007/s10439-015-1482-5
Appel, Alyssa A., Larson, Jeffrey C., Jiang, Bin, Zhong, Zhong, Anastasio, Mark A., and Brey, Eric M. Tue .
"X-ray Phase Contrast Allows Three Dimensional, Quantitative Imaging of Hydrogel Implants". United States. https://doi.org/10.1007/s10439-015-1482-5. https://www.osti.gov/servlets/purl/1341637.
@article{osti_1341637,
title = {X-ray Phase Contrast Allows Three Dimensional, Quantitative Imaging of Hydrogel Implants},
author = {Appel, Alyssa A. and Larson, Jeffrey C. and Jiang, Bin and Zhong, Zhong and Anastasio, Mark A. and Brey, Eric M.},
abstractNote = {Three dimensional imaging techniques are needed for the evaluation and assessment of biomaterials used for tissue engineering and drug delivery applications. Hydrogels are a particularly popular class of materials for medical applications but are difficult to image in tissue using most available imaging modalities. Imaging techniques based on X-ray Phase Contrast (XPC) have shown promise for tissue engineering applications due to their ability to provide image contrast based on multiple X-ray properties. In this manuscript we describe results using XPC to image a model hydrogel and soft tissue structure. Porous fibrin loaded poly(ethylene glycol) hydrogels were synthesized and implanted in a rodent subcutaneous model. Samples were explanted and imaged with an analyzer-based XPC technique and processed and stained for histology for comparison. Both hydrogel and soft tissues structures could be identified in XPC images. Structure in skeletal muscle adjacent could be visualized and invading fibrovascular tissue could be quantified. In quantitative results, there were no differences between XPC and the gold-standard histological measurements. These results provide evidence of the significant potential of techniques based on XPC for 3D imaging of hydrogel structure and local tissue response.},
doi = {10.1007/s10439-015-1482-5},
journal = {Annals of Biomedical Engineering},
number = 3,
volume = 44,
place = {United States},
year = {Tue Oct 20 00:00:00 EDT 2015},
month = {Tue Oct 20 00:00:00 EDT 2015}
}
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Works referenced in this record:
Experimental setup and the system performance for single-grid-based phase-contrast x-ray imaging (PCXI) with a microfocus x-ray tube
journal, August 2015
- Lim, Hyunwoo; Park, Yeonok; Cho, Hyosung
- Optics Communications, Vol. 348
In-vivo dark-field and phase-contrast x-ray imaging
journal, November 2013
- Bech, M.; Tapfer, A.; Velroyen, A.
- Scientific Reports, Vol. 3, Issue 1
A computed tomography implementation of multiple-image radiography: A computed tomography implementation of multiple-image radiography
journal, January 2006
- Brankov, Jovan G.; Wernick, Miles N.; Yang, Yongyi
- Medical Physics, Vol. 33, Issue 2
Characterization of type I collagen gels modified by glycation
journal, March 2009
- Francis-Sedlak, Megan E.; Uriel, Shiri; Larson, Jeffery C.
- Biomaterials, Vol. 30, Issue 9
Boundary-enhancement in propagation-based x-ray phase-contrast tomosynthesis improves depth position characterization
journal, April 2015
- Guan, Huifeng; Xu, Qiaofeng; Garson, Alfred B.
- Physics in Medicine and Biology, Vol. 60, Issue 8
Three dimensional visualization of engineered bone and soft tissue by combined x-ray micro-diffraction and phase contrast tomography
journal, December 2013
- Cedola, Alessia; Campi, Gaetano; Pelliccia, Daniele
- Physics in Medicine and Biology, Vol. 59, Issue 1
Evaluation of Submucosally Injected Polyethylene Glycol-Based Hydrogel and Bovine Cross-Linked Collagen in the Canine Urethra using Cystoscopy, Magnetic Resonance Imaging and Histopathology: Evaluation of Urethral Bulking Agents for Canine Incontinence
journal, July 2012
- Sumner, Julia P.; Hardie, Robert J.; Henningson, Jamie N.
- Veterinary Surgery, Vol. 41, Issue 6
Assessment of Dermal Wound Repair after Collagen Implantation with Optical Coherence Tomography
journal, March 2008
- Wang, Zhenguo; Pan, Hui; Yuan, Zhijia
- Tissue Engineering Part C: Methods, Vol. 14, Issue 1
Noninvasive and High-Resolution Optical Monitoring of Healing of Diabetic Dermal Excisional Wounds Implanted with Biodegradable In Situ Gelable Hydrogels
journal, April 2010
- Yuan, Zhijia; Zakhaleva, Julia; Ren, Hugang
- Tissue Engineering Part C: Methods, Vol. 16, Issue 2
X-Ray Imaging of Poly(Ethylene Glycol) Hydrogels Without Contrast Agents
journal, December 2010
- Brey, Eric M.; Appel, Alyssa; Chiu, Yu-Chieh
- Tissue Engineering Part C: Methods, Vol. 16, Issue 6, p. 1597-1600
A Study of the Intrinsic Autofluorescence of Poly (ethylene glycol)-co-( L -Lactic acid) Diacrylate
journal, January 2012
- Chiu, Yu-Chieh; Brey, Eric M.; Pérez-Luna, Víctor H.
- Journal of Fluorescence, Vol. 22, Issue 3
Fibrin-Loaded Porous Poly(Ethylene Glycol) Hydrogels as Scaffold Materials for Vascularized Tissue Formation
journal, January 2013
- Jiang, Bin; Waller, Thomas M.; Larson, Jeffery C.
- Tissue Engineering Part A, Vol. 19, Issue 1-2
Imaging Strategies for Tissue Engineering Applications
journal, February 2015
- Nam, Seung Yun; Ricles, Laura M.; Suggs, Laura J.
- Tissue Engineering Part B: Reviews, Vol. 21, Issue 1
Imaging of Poly(α-hydroxy-ester) Scaffolds with X-ray Phase-Contrast Microcomputed Tomography
journal, November 2012
- Appel, Alyssa A.; Larson, Jeffery C.; Somo, Sami
- Tissue Engineering Part C: Methods, Vol. 18, Issue 11
Computed Tomography Diffraction-Enhanced Imaging for In Situ Visualization of Tissue Scaffolds Implanted in Cartilage
journal, February 2014
- Izadifar, Zohreh; Chapman, Leroy Dean; Chen, Xiongbiao
- Tissue Engineering Part C: Methods, Vol. 20, Issue 2
Diffraction-enhanced X-ray imaging of articular cartilage
journal, March 2002
- Mollenhauer, J.; Aurich, M. E.; Zhong, Z.
- Osteoarthritis and Cartilage, Vol. 10, Issue 3
Implementation of diffraction-enhanced imaging experiments: at the NSLS and APS
journal, August 2000
- Zhong, Z.; Thomlinson, W.; Chapman, D.
- Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 450, Issue 2-3
Low-dose phase contrast x-ray medical imaging
journal, October 1998
- Arfelli, F.; Assante, M.; Bonvicini, V.
- Physics in Medicine and Biology, Vol. 43, Issue 10
In Vivo Magnetic Resonance Imaging and Relaxometry Study of a Porous Hydrogel Implanted in the Trapezius Muscle of Rabbits
journal, June 2000
- Traoré, A. S.; Woerly, S.; Doan, V. D.
- Tissue Engineering, Vol. 6, Issue 3
Medical phase contrast x-ray imaging: current status and future prospects
journal, July 2004
- Lewis, R. A.
- Physics in Medicine and Biology, Vol. 49, Issue 16, p. 3573-3583
Label-free imaging of gelatin-containing hydrogel scaffolds
journal, February 2015
- Liang, Yajie; Bar-Shir, Amnon; Song, Xiaolei
- Biomaterials, Vol. 42
X-ray phase contrast imaging of calcified tissue and biomaterial structure in bioreactor engineered tissues: 3D Imaging of Tissues Engineered in Bioreactor
journal, November 2014
- Appel, Alyssa A.; Larson, Jeffery C.; Garson, Alfred B.
- Biotechnology and Bioengineering, Vol. 112, Issue 3
The role of pore size on vascularization and tissue remodeling in PEG hydrogels
journal, September 2011
- Chiu, Yu-Chieh; Cheng, Ming-Huei; Engel, Holger
- Biomaterials, Vol. 32, Issue 26
MRI-detectable pH nanosensors incorporated into hydrogels for in vivo sensing of transplanted-cell viability
journal, January 2013
- Chan, Kannie W. Y.; Liu, Guanshu; Song, Xiaolei
- Nature Materials, Vol. 12, Issue 3
X-Ray Diffraction Enhanced Imaging as a Novel Method to Visualize Low-Density Scaffolds in Soft Tissue Engineering
journal, November 2011
- Zhu, Ning; Chapman, Dean; Cooper, David
- Tissue Engineering Part C: Methods, Vol. 17, Issue 11
Noninvasive Quantitative Imaging of Collagen Microstructure in Three-Dimensional Hydrogels Using High-Frequency Ultrasound
journal, July 2015
- Mercado, Karla P.; Helguera, María; Hocking, Denise C.
- Tissue Engineering Part C: Methods, Vol. 21, Issue 7
Intravital Confocal and Two-Photon Imaging of Dual-Color Cells and Extracellular Matrix Mimics
journal, February 2013
- Bal, Ufuk; Andresen, Volker; Baggett, Brenda
- Microscopy and Microanalysis, Vol. 19, Issue 1
Chemical exchange saturation transfer (CEST): What is in a name and what isn't?
journal, February 2011
- van Zijl, Peter C. M.; Yadav, Nirbhay N.
- Magnetic Resonance in Medicine, Vol. 65, Issue 4
Protein polymer MRI contrast agents: Longitudinal analysis of biomaterials in vivo: PPCAs for in Vivo MRI of Biomaterials
journal, August 2010
- Karfeld-Sulzer, Lindsay S.; Waters, Emily A.; Kohlmeir, Ellen K.
- Magnetic Resonance in Medicine, Vol. 65, Issue 1
Using swept-source optical coherence tomography to monitor the formation of neo-epidermis in tissue-engineered skin
journal, November 2010
- Smith, Louise E.; Bonesi, Marco; Smallwood, Rod
- Journal of Tissue Engineering and Regenerative Medicine, Vol. 4, Issue 8
Magnetization transfer contrast MRI for non-invasive assessment of innate and adaptive immune responses against alginate-encapsulated cells
journal, September 2014
- Chan, Kannie W. Y.; Liu, Guanshu; van Zijl, Peter C. M.
- Biomaterials, Vol. 35, Issue 27
An analysis of the integration between articular cartilage and nondegradable hydrogel using magnetic resonance imaging
journal, January 2006
- Ramaswamy, Sharan; Wang, Dong-An; Fishbein, Kenneth W.
- Journal of Biomedical Materials Research Part B: Applied Biomaterials, Vol. 77B, Issue 1
Imaging challenges in biomaterials and tissue engineering
journal, September 2013
- Appel, Alyssa A.; Anastasio, Mark A.; Larson, Jeffery C.
- Biomaterials, Vol. 34, Issue 28
An extended diffraction-enhanced imaging method for implementing multiple-image radiography
journal, March 2007
- Chou, Cheng-Ying; Anastasio, Mark A.; Brankov, Jovan G.
- Physics in Medicine and Biology, Vol. 52, Issue 7
Multiple-image radiography
journal, November 2003
- Wernick, Miles N.; Wirjadi, Oliver; Chapman, Dean
- Physics in Medicine and Biology, Vol. 48, Issue 23
Imaging approaches in functional assessment of implantable myogenic biomaterials and engineered muscle tissue
journal, March 2015
- Edmunds, Kyle J.; Gargiulo, Paolo
- European Journal of Translational Myology, Vol. 25, Issue 2
An Overview of Methods for the In Vivo Evaluation of Tissue-Engineered Skin Constructs
journal, February 2011
- Lammers, Gerwen; Verhaegen, Pauline D. H. M.; Ulrich, Magda M. W.
- Tissue Engineering Part B: Reviews, Vol. 17, Issue 1
Injectable In Situ Forming Hybrid Iron Oxide-Hyaluronic Acid Hydrogel for Magnetic Resonance Imaging and Drug Delivery: Injectable In Situ Forming Hybrid Iron Oxide-Hyaluronic Acid Hydrogel …
journal, May 2014
- Zhang, Yu; Sun, Yi; Yang, Xia
- Macromolecular Bioscience, Vol. 14, Issue 9
Noninvasive Quantification of In Vitro Osteoblastic Differentiation in 3D Engineered Tissue Constructs Using Spectral Ultrasound Imaging
journal, January 2014
- Gudur, Madhu Sudhan Reddy; Rao, Rameshwar R.; Peterson, Alexis W.
- PLoS ONE, Vol. 9, Issue 1
Evaluation of gold nanotracers to track adipose-derived stem cells in a PEGylated fibrin gel for dermal tissue engineering applications
journal, January 2013
- Chung, Eunna; Nam, Seung Yun; Ricles, Laura M.
- International Journal of Nanomedicine
Differential X-ray phase-contrast imaging with a grating interferometer using a laboratory X-ray micro-focus tube
journal, December 2014
- Yoon, Kwon-Ha; Ryu, Jong Hyun; Jung, Chang Won
- Journal of the Korean Physical Society, Vol. 65, Issue 12
A tunable silk–alginate hydrogel scaffold for stem cell culture and transplantation
journal, April 2014
- Ziv, Keren; Nuhn, Harald; Ben-Haim, Yael
- Biomaterials, Vol. 35, Issue 12
In vivo and in vitro tracking of erosion in biodegradable materials using non-invasive fluorescence imaging
journal, August 2011
- Artzi, Natalie; Oliva, Nuria; Puron, Cristina
- Nature Materials, Vol. 10, Issue 9
Non-invasive monitoring of tissue scaffold degradation using ultrasound elasticity imaging
journal, July 2008
- Kim, Kang; Jeong, Claire G.; Hollister, Scott J.
- Acta Biomaterialia, Vol. 4, Issue 4
Interest of multimodal imaging in tissue engineering
journal, January 2008
- Werkmeister, Elisabeth; Dumas, Dominique; de Isla, Natalia
- Bio-Medical Materials and Engineering, Vol. 18, Issue 4-5
Phase contrast imaging using a micro focus x-ray source
conference, September 2014
- Zhou, Wei; Majidi, Keivan; Brankov, Jovan G.
- SPIE Optical Engineering + Applications, SPIE Proceedings
Works referencing / citing this record:
Hydrogel-based scaffolds to support intrathecal stem cell transplantation as a gateway to the spinal cord: clinical needs, biomaterials, and imaging technologies
journal, April 2018
- Oliveira, J. Miguel; Carvalho, Luisa; Silva-Correia, Joana
- npj Regenerative Medicine, Vol. 3, Issue 1
In Vivo Tracking of Tissue Engineered Constructs
journal, July 2019
- Gil, Carmen J.; Tomov, Martin L.; Theus, Andrea S.
- Micromachines, Vol. 10, Issue 7
Hydrogel-based scaffolds to support intrathecal stem cell transplantation as a gateway to the spinal cord: clinical needs, biomaterials, and imaging technologies
journal, April 2018
- Oliveira, J. Miguel; Carvalho, Luisa; Silva-Correia, Joana
- npj Regenerative Medicine, Vol. 3, Issue 1