Abstract

Crohn’s disease (CD) is one type of inflammatory bowel disease where both inflammation and fibrosis cause the thickening of the bowel wall and development of the strictures. Accurate assessment of the strictures is critical for the management of CD because the fibrotic strictures must be removed surgically. In this study, a prototype capsule-shaped acoustic resolution photoacoustic (PA) endoscope, which can perform mulitwavelength side-view scanning, was developed to characterize the intestinal strictures of CD. The imaging performance of the probe was tested in phantom experiments and a rabbit trinitrobenzene sulfonic acid (TNBS) model with acute (inflammatory only) or chronic (mixed fibrotic and inflammatory) colitis in vivo. The motion artifacts due to intestinal peristalsis and the respiratory motion of the animals were compensated to improve image qualities. Quantitative molecular component images derived from multi-wavelength PA measurements of normal, acute and chronic intestinal strictures demonstrated statistically significant differences among the three groups that were confirmed by histopathology. A longitudinal study demonstrated the capability of the system in monitoring the development of fibrosis. The results suggest that the proposed novel, capsule-shaped acoustic resolution PA endoscope can be used to characterize fibrostenotic disease in vivo.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2019 (1)

Y. Li, Z. Zhu, J. C. Jing, J. J. Chen, A. E. Heidari, Y. He, J. Zhu, T. Ma, M. Yu, Q. Zhou, and Z. Chen, “High-Speed Integrated Endoscopic Photoacoustic and Ultrasound Imaging System,” IEEE J. Sel. Top. Quantum Electron. 25(1), 1–5 (2019).
[Crossref]

2018 (1)

2016 (2)

2014 (3)

C. Li, J.-M. Yang, R. Chen, C.-H. Yeh, L. Zhu, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Urogenital photoacoustic endoscope,” Opt. Lett. 39(6), 1473–1476 (2014).
[Crossref] [PubMed]

J.-M. Yang, C. Li, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Catheter-based photoacoustic endoscope,” J. Biomed. Opt. 19(6), 066001 (2014).
[Crossref] [PubMed]

J. R. Dillman, S. D. Swanson, L. A. Johnson, D. S. Moons, J. Adler, R. W. Stidham, and P. D. Higgins, “Comparison of noncontrast MRI magnetization transfer and T -Weighted signal intensity ratios for detection of bowel wall fibrosis in a Crohn’s disease animal model,” J. Magn. Reson. Imaging 42, 801–810 (2014).

2013 (2)

J. R. Dillman, R. W. Stidham, P. D. Higgins, D. S. Moons, L. A. Johnson, and J. M. Rubin, “US elastography-derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model,” Radiology 267(3), 757–766 (2013).
[Crossref] [PubMed]

J. Yuan, G. Xu, Y. Yu, Y. Zhou, P. L. Carson, X. Wang, and X. Liu, “Real-time photoacoustic and ultrasound dual-modality imaging system facilitated with graphics processing unit and code parallel optimization,” J. Biomed. Opt. 18(8), 086001 (2013).
[Crossref] [PubMed]

2012 (3)

J.-M. Yang, R. Chen, C. Favazza, J. Yao, C. Li, Z. Hu, Q. Zhou, K. K. Shung, and L. V. Wang, “A 2.5-mm diameter probe for photoacoustic and ultrasonic endoscopy,” Opt. Express 20(21), 23944–23953 (2012).
[Crossref] [PubMed]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

L. V. Wang and S. Hu, “Photoacoustic Tomography: In Vivo Imaging from Organelles To Organs,” Science 335(6075), 1458–1462 (2012).
[Crossref] [PubMed]

2011 (3)

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-Free Bond-Selective Imaging by Listening to Vibrationally Excited Molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

R. W. Stidham, J. Xu, L. A. Johnson, K. Kim, D. S. Moons, B. J. McKenna, J. M. Rubin, and P. D. Higgins, “Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease,” Gastroenterology 141(3), 819–826 (2011).
[Crossref] [PubMed]

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1(4), 602–631 (2011).
[Crossref] [PubMed]

2010 (2)

G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
[Crossref] [PubMed]

D. W. Jones and S. R. G. Finlayson, “Trends in Surgery for Crohn’s Disease in the Era of Infliximab,” Ann. Surg. 252(2), 307–312 (2010).
[Crossref] [PubMed]

2009 (3)

J. Cosnes, “Can we modulate the clinical course of inflammatory bowel diseases by our current treatment strategies?” Dig. Dis. 27(4), 516–521 (2009).
[Crossref] [PubMed]

I. C. Lawrance, C. J. Welman, P. Shipman, and K. Murray, “Correlation of MRI-determined small bowel Crohn’s disease categories with medical response and surgical pathology,” World J. Gastroenterol. 15(27), 3367–3375 (2009).
[Crossref] [PubMed]

P. Paolantonio, R. Ferrari, F. Vecchietti, S. Cucchiara, and A. Laghi, “Current status of MR imaging in the evaluation of IBD in a pediatric population of patients,” Eur. J. Radiol. 69(3), 418–424 (2009).
[Crossref] [PubMed]

2008 (1)

K. Kim, L. A. Johnson, C. Jia, J. C. Joyce, S. Rangwalla, P. D. R. Higgins, and J. M. Rubin, “Noninvasive Ultrasound Elasticity Imaging (UEI) of Crohn’s Disease: Animal Model,” Ultrasound Med. Biol. 34(6), 902–912 (2008).
[Crossref] [PubMed]

2006 (3)

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
[Crossref] [PubMed]

M.-L. Li, H. E. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in vivo photoacoustic microscopy based on a virtual-detector concept,” Opt. Lett. 31(4), 474–476 (2006).
[Crossref] [PubMed]

2003 (1)

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
[Crossref] [PubMed]

2002 (1)

E. V. Loftus, P. Schoenfeld, and W. J. Sandborn, “The epidemiology and natural history of Crohn’s disease in population-based patient cohorts from North America: a systematic review,” Aliment. Pharmacol. Ther. 16(1), 51–60 (2002).
[Crossref] [PubMed]

2001 (2)

W. A. Faubion, E. V. Loftus, W. S. Harmsen, A. R. Zinsmeister, and W. J. Sandborn, “The natural history of corticosteroid therapy for inflammatory bowel disease: A population-based study,” Gastroenterology 121(2), 255–260 (2001).
[Crossref] [PubMed]

M. Boudiaf, P. Soyer, C. Terem, J. P. Pelage, E. Maissiat, and R. Rymer, “CT Evaluation of Small Bowel Obstruction,” Radiographics 21(3), 613–624 (2001).
[Crossref] [PubMed]

2000 (4)

Z. Tarján, G. Tóth, T. Györke, A. Mester, K. Karlinger, and E. K. Makó, “Ultrasound in Crohn’s disease of the small bowel,” Eur. J. Radiol. 35(3), 176–182 (2000).
[Crossref] [PubMed]

R. D. Cohen, L. R. Larson, J. M. Roth, R. V. Becker, and L. L. Mummert, “The cost of hospitalization in Crohn’s disease,” Am. J. Gastroenterol. 95(2), 524–530 (2000).
[Crossref] [PubMed]

G. Oberhuber, P. C. Stangl, H. Vogelsang, E. Schober, F. Herbst, and C. Gasche, “Significant association of strictures and internal fistula formation in Crohn’s disease,” Virchows Arch. 437(3), 293–297 (2000).
[Crossref] [PubMed]

I. Depoortere, T. Thijs, G. van Assche, J. C. Keith, and T. L. Peeters, “Dose-dependent effects of recombinant human interleukin-11 on contractile properties in rabbit 2,4,6-trinitrobenzene sulfonic acid colitis,” J. Pharmacol. Exp. Ther. 294(3), 983–990 (2000).
[PubMed]

1995 (2)

D. Anthony, F. Savage, V. Sams, and P. Boulos, “The characterization of a rabbit model of inflammatory bowel disease,” Int. J. Exp. Pathol. 76(3), 215–224 (1995).
[PubMed]

L. Wang, S. L. Jacques, and L. Zheng, “MCML-Monte Carlo modeling of light transport in multi-layered tissues,” Comput. Methods Programs Biomed. 47(2), 131–146 (1995).
[Crossref] [PubMed]

1992 (1)

H. Matthes, H. Herbst, D. Schuppan, A. Stallmach, S. Milani, H. Stein, and E.-O. Riecken, “Cellular localization of procollagen gene transcripts in inflammatory bowel diseases,” Gastroenterology 102(2), 431–442 (1992).
[Crossref] [PubMed]

1990 (1)

W. F. Cheong, S. A. Prahl, and A. J. Welch, “A review of the optical properties of biological tissues,” Quantum Electronics, IEEE Journal of 26(12), 2166–2185 (1990).
[Crossref]

1989 (1)

S. M. Dandalides, W. D. Carey, R. Petras, and E. Achkar, “Endoscopic small bowel mucosal biopsy: a controlled trial evaluating forceps size and biopsy location in the diagnosis of normal and abnormal mucosal architecture,” Gastrointest. Endosc. 35(3), 197–200 (1989).
[Crossref] [PubMed]

1986 (1)

J. K. Kelly and T. O. Siu, “The strictures, sinuses, and fissures of Crohn’s disease,” J. Clin. Gastroenterol. 8(5), 594–598 (1986).
[Crossref] [PubMed]

Achkar, E.

S. M. Dandalides, W. D. Carey, R. Petras, and E. Achkar, “Endoscopic small bowel mucosal biopsy: a controlled trial evaluating forceps size and biopsy location in the diagnosis of normal and abnormal mucosal architecture,” Gastrointest. Endosc. 35(3), 197–200 (1989).
[Crossref] [PubMed]

Adler, J.

J. R. Dillman, S. D. Swanson, L. A. Johnson, D. S. Moons, J. Adler, R. W. Stidham, and P. D. Higgins, “Comparison of noncontrast MRI magnetization transfer and T -Weighted signal intensity ratios for detection of bowel wall fibrosis in a Crohn’s disease animal model,” J. Magn. Reson. Imaging 42, 801–810 (2014).

Aggarwal, A.

G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
[Crossref] [PubMed]

Anthony, D.

D. Anthony, F. Savage, V. Sams, and P. Boulos, “The characterization of a rabbit model of inflammatory bowel disease,” Int. J. Exp. Pathol. 76(3), 215–224 (1995).
[PubMed]

Beard, P.

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1(4), 602–631 (2011).
[Crossref] [PubMed]

Becker, R. V.

R. D. Cohen, L. R. Larson, J. M. Roth, R. V. Becker, and L. L. Mummert, “The cost of hospitalization in Crohn’s disease,” Am. J. Gastroenterol. 95(2), 524–530 (2000).
[Crossref] [PubMed]

Boudiaf, M.

M. Boudiaf, P. Soyer, C. Terem, J. P. Pelage, E. Maissiat, and R. Rymer, “CT Evaluation of Small Bowel Obstruction,” Radiographics 21(3), 613–624 (2001).
[Crossref] [PubMed]

Boulos, P.

D. Anthony, F. Savage, V. Sams, and P. Boulos, “The characterization of a rabbit model of inflammatory bowel disease,” Int. J. Exp. Pathol. 76(3), 215–224 (1995).
[PubMed]

Buehler, A.

Cai, X.

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

Carey, W. D.

S. M. Dandalides, W. D. Carey, R. Petras, and E. Achkar, “Endoscopic small bowel mucosal biopsy: a controlled trial evaluating forceps size and biopsy location in the diagnosis of normal and abnormal mucosal architecture,” Gastrointest. Endosc. 35(3), 197–200 (1989).
[Crossref] [PubMed]

Carson, P. L.

J. Yuan, G. Xu, Y. Yu, Y. Zhou, P. L. Carson, X. Wang, and X. Liu, “Real-time photoacoustic and ultrasound dual-modality imaging system facilitated with graphics processing unit and code parallel optimization,” J. Biomed. Opt. 18(8), 086001 (2013).
[Crossref] [PubMed]

Chai, N.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-Free Bond-Selective Imaging by Listening to Vibrationally Excited Molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Chen, D. M.

G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
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Chen, J. J.

Y. Li, Z. Zhu, J. C. Jing, J. J. Chen, A. E. Heidari, Y. He, J. Zhu, T. Ma, M. Yu, Q. Zhou, and Z. Chen, “High-Speed Integrated Endoscopic Photoacoustic and Ultrasound Imaging System,” IEEE J. Sel. Top. Quantum Electron. 25(1), 1–5 (2019).
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Chen, R.

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J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
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Y. Li, Z. Zhu, J. C. Jing, J. J. Chen, A. E. Heidari, Y. He, J. Zhu, T. Ma, M. Yu, Q. Zhou, and Z. Chen, “High-Speed Integrated Endoscopic Photoacoustic and Ultrasound Imaging System,” IEEE J. Sel. Top. Quantum Electron. 25(1), 1–5 (2019).
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G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
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R. D. Cohen, L. R. Larson, J. M. Roth, R. V. Becker, and L. L. Mummert, “The cost of hospitalization in Crohn’s disease,” Am. J. Gastroenterol. 95(2), 524–530 (2000).
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P. Paolantonio, R. Ferrari, F. Vecchietti, S. Cucchiara, and A. Laghi, “Current status of MR imaging in the evaluation of IBD in a pediatric population of patients,” Eur. J. Radiol. 69(3), 418–424 (2009).
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G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
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G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
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I. Depoortere, T. Thijs, G. van Assche, J. C. Keith, and T. L. Peeters, “Dose-dependent effects of recombinant human interleukin-11 on contractile properties in rabbit 2,4,6-trinitrobenzene sulfonic acid colitis,” J. Pharmacol. Exp. Ther. 294(3), 983–990 (2000).
[PubMed]

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G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
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J. R. Dillman, S. D. Swanson, L. A. Johnson, D. S. Moons, J. Adler, R. W. Stidham, and P. D. Higgins, “Comparison of noncontrast MRI magnetization transfer and T -Weighted signal intensity ratios for detection of bowel wall fibrosis in a Crohn’s disease animal model,” J. Magn. Reson. Imaging 42, 801–810 (2014).

J. R. Dillman, R. W. Stidham, P. D. Higgins, D. S. Moons, L. A. Johnson, and J. M. Rubin, “US elastography-derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model,” Radiology 267(3), 757–766 (2013).
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H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-Free Bond-Selective Imaging by Listening to Vibrationally Excited Molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
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W. A. Faubion, E. V. Loftus, W. S. Harmsen, A. R. Zinsmeister, and W. J. Sandborn, “The natural history of corticosteroid therapy for inflammatory bowel disease: A population-based study,” Gastroenterology 121(2), 255–260 (2001).
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Favazza, C.

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

J.-M. Yang, R. Chen, C. Favazza, J. Yao, C. Li, Z. Hu, Q. Zhou, K. K. Shung, and L. V. Wang, “A 2.5-mm diameter probe for photoacoustic and ultrasonic endoscopy,” Opt. Express 20(21), 23944–23953 (2012).
[Crossref] [PubMed]

Feagan, B. G.

G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
[Crossref] [PubMed]

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P. Paolantonio, R. Ferrari, F. Vecchietti, S. Cucchiara, and A. Laghi, “Current status of MR imaging in the evaluation of IBD in a pediatric population of patients,” Eur. J. Radiol. 69(3), 418–424 (2009).
[Crossref] [PubMed]

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D. W. Jones and S. R. G. Finlayson, “Trends in Surgery for Crohn’s Disease in the Era of Infliximab,” Ann. Surg. 252(2), 307–312 (2010).
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G. Oberhuber, P. C. Stangl, H. Vogelsang, E. Schober, F. Herbst, and C. Gasche, “Significant association of strictures and internal fistula formation in Crohn’s disease,” Virchows Arch. 437(3), 293–297 (2000).
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G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
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Gupta, S. D.

G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
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Z. Tarján, G. Tóth, T. Györke, A. Mester, K. Karlinger, and E. K. Makó, “Ultrasound in Crohn’s disease of the small bowel,” Eur. J. Radiol. 35(3), 176–182 (2000).
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G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
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W. A. Faubion, E. V. Loftus, W. S. Harmsen, A. R. Zinsmeister, and W. J. Sandborn, “The natural history of corticosteroid therapy for inflammatory bowel disease: A population-based study,” Gastroenterology 121(2), 255–260 (2001).
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He, H.

He, Y.

Y. Li, Z. Zhu, J. C. Jing, J. J. Chen, A. E. Heidari, Y. He, J. Zhu, T. Ma, M. Yu, Q. Zhou, and Z. Chen, “High-Speed Integrated Endoscopic Photoacoustic and Ultrasound Imaging System,” IEEE J. Sel. Top. Quantum Electron. 25(1), 1–5 (2019).
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Heidari, A. E.

Y. Li, Z. Zhu, J. C. Jing, J. J. Chen, A. E. Heidari, Y. He, J. Zhu, T. Ma, M. Yu, Q. Zhou, and Z. Chen, “High-Speed Integrated Endoscopic Photoacoustic and Ultrasound Imaging System,” IEEE J. Sel. Top. Quantum Electron. 25(1), 1–5 (2019).
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G. Oberhuber, P. C. Stangl, H. Vogelsang, E. Schober, F. Herbst, and C. Gasche, “Significant association of strictures and internal fistula formation in Crohn’s disease,” Virchows Arch. 437(3), 293–297 (2000).
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Herbst, H.

H. Matthes, H. Herbst, D. Schuppan, A. Stallmach, S. Milani, H. Stein, and E.-O. Riecken, “Cellular localization of procollagen gene transcripts in inflammatory bowel diseases,” Gastroenterology 102(2), 431–442 (1992).
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H. Lei, L. A. Johnson, S. Liu, D. S. Moons, T. Ma, Q. Zhou, M. D. Rice, J. Ni, X. Wang, P. D. Higgins, and G. Xu, “Characterizing intestinal inflammation and fibrosis in Crohn’s disease by photoacoustic imaging: feasibility study,” Biomed. Opt. Express 7(7), 2837–2848 (2016).
[Crossref] [PubMed]

J. R. Dillman, S. D. Swanson, L. A. Johnson, D. S. Moons, J. Adler, R. W. Stidham, and P. D. Higgins, “Comparison of noncontrast MRI magnetization transfer and T -Weighted signal intensity ratios for detection of bowel wall fibrosis in a Crohn’s disease animal model,” J. Magn. Reson. Imaging 42, 801–810 (2014).

J. R. Dillman, R. W. Stidham, P. D. Higgins, D. S. Moons, L. A. Johnson, and J. M. Rubin, “US elastography-derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model,” Radiology 267(3), 757–766 (2013).
[Crossref] [PubMed]

R. W. Stidham, J. Xu, L. A. Johnson, K. Kim, D. S. Moons, B. J. McKenna, J. M. Rubin, and P. D. Higgins, “Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease,” Gastroenterology 141(3), 819–826 (2011).
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Higgins, P. D. R.

Y. Zhu, L. A. Johnson, Z. Huang, J. M. Rubin, J. Yuan, H. Lei, J. Ni, X. Wang, P. D. R. Higgins, and G. Xu, “Identifying intestinal fibrosis and inflammation by spectroscopic photoacoustic imaging: an animal study in vivo,” Biomed. Opt. Express 9(4), 1590–1600 (2018).
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K. Kim, L. A. Johnson, C. Jia, J. C. Joyce, S. Rangwalla, P. D. R. Higgins, and J. M. Rubin, “Noninvasive Ultrasound Elasticity Imaging (UEI) of Crohn’s Disease: Animal Model,” Ultrasound Med. Biol. 34(6), 902–912 (2008).
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Huang, Z.

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Jing, J. C.

Y. Li, Z. Zhu, J. C. Jing, J. J. Chen, A. E. Heidari, Y. He, J. Zhu, T. Ma, M. Yu, Q. Zhou, and Z. Chen, “High-Speed Integrated Endoscopic Photoacoustic and Ultrasound Imaging System,” IEEE J. Sel. Top. Quantum Electron. 25(1), 1–5 (2019).
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Y. Zhu, L. A. Johnson, Z. Huang, J. M. Rubin, J. Yuan, H. Lei, J. Ni, X. Wang, P. D. R. Higgins, and G. Xu, “Identifying intestinal fibrosis and inflammation by spectroscopic photoacoustic imaging: an animal study in vivo,” Biomed. Opt. Express 9(4), 1590–1600 (2018).
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H. Lei, L. A. Johnson, S. Liu, D. S. Moons, T. Ma, Q. Zhou, M. D. Rice, J. Ni, X. Wang, P. D. Higgins, and G. Xu, “Characterizing intestinal inflammation and fibrosis in Crohn’s disease by photoacoustic imaging: feasibility study,” Biomed. Opt. Express 7(7), 2837–2848 (2016).
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J. R. Dillman, S. D. Swanson, L. A. Johnson, D. S. Moons, J. Adler, R. W. Stidham, and P. D. Higgins, “Comparison of noncontrast MRI magnetization transfer and T -Weighted signal intensity ratios for detection of bowel wall fibrosis in a Crohn’s disease animal model,” J. Magn. Reson. Imaging 42, 801–810 (2014).

J. R. Dillman, R. W. Stidham, P. D. Higgins, D. S. Moons, L. A. Johnson, and J. M. Rubin, “US elastography-derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model,” Radiology 267(3), 757–766 (2013).
[Crossref] [PubMed]

R. W. Stidham, J. Xu, L. A. Johnson, K. Kim, D. S. Moons, B. J. McKenna, J. M. Rubin, and P. D. Higgins, “Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease,” Gastroenterology 141(3), 819–826 (2011).
[Crossref] [PubMed]

K. Kim, L. A. Johnson, C. Jia, J. C. Joyce, S. Rangwalla, P. D. R. Higgins, and J. M. Rubin, “Noninvasive Ultrasound Elasticity Imaging (UEI) of Crohn’s Disease: Animal Model,” Ultrasound Med. Biol. 34(6), 902–912 (2008).
[Crossref] [PubMed]

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D. W. Jones and S. R. G. Finlayson, “Trends in Surgery for Crohn’s Disease in the Era of Infliximab,” Ann. Surg. 252(2), 307–312 (2010).
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Joyce, J. C.

K. Kim, L. A. Johnson, C. Jia, J. C. Joyce, S. Rangwalla, P. D. R. Higgins, and J. M. Rubin, “Noninvasive Ultrasound Elasticity Imaging (UEI) of Crohn’s Disease: Animal Model,” Ultrasound Med. Biol. 34(6), 902–912 (2008).
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Z. Tarján, G. Tóth, T. Györke, A. Mester, K. Karlinger, and E. K. Makó, “Ultrasound in Crohn’s disease of the small bowel,” Eur. J. Radiol. 35(3), 176–182 (2000).
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Keith, J. C.

I. Depoortere, T. Thijs, G. van Assche, J. C. Keith, and T. L. Peeters, “Dose-dependent effects of recombinant human interleukin-11 on contractile properties in rabbit 2,4,6-trinitrobenzene sulfonic acid colitis,” J. Pharmacol. Exp. Ther. 294(3), 983–990 (2000).
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R. W. Stidham, J. Xu, L. A. Johnson, K. Kim, D. S. Moons, B. J. McKenna, J. M. Rubin, and P. D. Higgins, “Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease,” Gastroenterology 141(3), 819–826 (2011).
[Crossref] [PubMed]

K. Kim, L. A. Johnson, C. Jia, J. C. Joyce, S. Rangwalla, P. D. R. Higgins, and J. M. Rubin, “Noninvasive Ultrasound Elasticity Imaging (UEI) of Crohn’s Disease: Animal Model,” Ultrasound Med. Biol. 34(6), 902–912 (2008).
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X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
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P. Paolantonio, R. Ferrari, F. Vecchietti, S. Cucchiara, and A. Laghi, “Current status of MR imaging in the evaluation of IBD in a pediatric population of patients,” Eur. J. Radiol. 69(3), 418–424 (2009).
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Larson, L. R.

R. D. Cohen, L. R. Larson, J. M. Roth, R. V. Becker, and L. L. Mummert, “The cost of hospitalization in Crohn’s disease,” Am. J. Gastroenterol. 95(2), 524–530 (2000).
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I. C. Lawrance, C. J. Welman, P. Shipman, and K. Murray, “Correlation of MRI-determined small bowel Crohn’s disease categories with medical response and surgical pathology,” World J. Gastroenterol. 15(27), 3367–3375 (2009).
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Li, C.

Li, M.-L.

Li, Y.

Y. Li, Z. Zhu, J. C. Jing, J. J. Chen, A. E. Heidari, Y. He, J. Zhu, T. Ma, M. Yu, Q. Zhou, and Z. Chen, “High-Speed Integrated Endoscopic Photoacoustic and Ultrasound Imaging System,” IEEE J. Sel. Top. Quantum Electron. 25(1), 1–5 (2019).
[Crossref]

Lichtenstein, G. R.

G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
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Liu, X.

J. Yuan, G. Xu, Y. Yu, Y. Zhou, P. L. Carson, X. Wang, and X. Liu, “Real-time photoacoustic and ultrasound dual-modality imaging system facilitated with graphics processing unit and code parallel optimization,” J. Biomed. Opt. 18(8), 086001 (2013).
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E. V. Loftus, P. Schoenfeld, and W. J. Sandborn, “The epidemiology and natural history of Crohn’s disease in population-based patient cohorts from North America: a systematic review,” Aliment. Pharmacol. Ther. 16(1), 51–60 (2002).
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W. A. Faubion, E. V. Loftus, W. S. Harmsen, A. R. Zinsmeister, and W. J. Sandborn, “The natural history of corticosteroid therapy for inflammatory bowel disease: A population-based study,” Gastroenterology 121(2), 255–260 (2001).
[Crossref] [PubMed]

Lucht, R.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-Free Bond-Selective Imaging by Listening to Vibrationally Excited Molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Ma, T.

Y. Li, Z. Zhu, J. C. Jing, J. J. Chen, A. E. Heidari, Y. He, J. Zhu, T. Ma, M. Yu, Q. Zhou, and Z. Chen, “High-Speed Integrated Endoscopic Photoacoustic and Ultrasound Imaging System,” IEEE J. Sel. Top. Quantum Electron. 25(1), 1–5 (2019).
[Crossref]

H. Lei, L. A. Johnson, S. Liu, D. S. Moons, T. Ma, Q. Zhou, M. D. Rice, J. Ni, X. Wang, P. D. Higgins, and G. Xu, “Characterizing intestinal inflammation and fibrosis in Crohn’s disease by photoacoustic imaging: feasibility study,” Biomed. Opt. Express 7(7), 2837–2848 (2016).
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G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
[Crossref] [PubMed]

Makó, E. K.

Z. Tarján, G. Tóth, T. Györke, A. Mester, K. Karlinger, and E. K. Makó, “Ultrasound in Crohn’s disease of the small bowel,” Eur. J. Radiol. 35(3), 176–182 (2000).
[Crossref] [PubMed]

Maslov, K.

Matthes, H.

H. Matthes, H. Herbst, D. Schuppan, A. Stallmach, S. Milani, H. Stein, and E.-O. Riecken, “Cellular localization of procollagen gene transcripts in inflammatory bowel diseases,” Gastroenterology 102(2), 431–442 (1992).
[Crossref] [PubMed]

McKenna, B. J.

R. W. Stidham, J. Xu, L. A. Johnson, K. Kim, D. S. Moons, B. J. McKenna, J. M. Rubin, and P. D. Higgins, “Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease,” Gastroenterology 141(3), 819–826 (2011).
[Crossref] [PubMed]

Mester, A.

Z. Tarján, G. Tóth, T. Györke, A. Mester, K. Karlinger, and E. K. Makó, “Ultrasound in Crohn’s disease of the small bowel,” Eur. J. Radiol. 35(3), 176–182 (2000).
[Crossref] [PubMed]

Milani, S.

H. Matthes, H. Herbst, D. Schuppan, A. Stallmach, S. Milani, H. Stein, and E.-O. Riecken, “Cellular localization of procollagen gene transcripts in inflammatory bowel diseases,” Gastroenterology 102(2), 431–442 (1992).
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Moons, D. S.

H. Lei, L. A. Johnson, S. Liu, D. S. Moons, T. Ma, Q. Zhou, M. D. Rice, J. Ni, X. Wang, P. D. Higgins, and G. Xu, “Characterizing intestinal inflammation and fibrosis in Crohn’s disease by photoacoustic imaging: feasibility study,” Biomed. Opt. Express 7(7), 2837–2848 (2016).
[Crossref] [PubMed]

J. R. Dillman, S. D. Swanson, L. A. Johnson, D. S. Moons, J. Adler, R. W. Stidham, and P. D. Higgins, “Comparison of noncontrast MRI magnetization transfer and T -Weighted signal intensity ratios for detection of bowel wall fibrosis in a Crohn’s disease animal model,” J. Magn. Reson. Imaging 42, 801–810 (2014).

J. R. Dillman, R. W. Stidham, P. D. Higgins, D. S. Moons, L. A. Johnson, and J. M. Rubin, “US elastography-derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model,” Radiology 267(3), 757–766 (2013).
[Crossref] [PubMed]

R. W. Stidham, J. Xu, L. A. Johnson, K. Kim, D. S. Moons, B. J. McKenna, J. M. Rubin, and P. D. Higgins, “Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease,” Gastroenterology 141(3), 819–826 (2011).
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Mummert, L. L.

R. D. Cohen, L. R. Larson, J. M. Roth, R. V. Becker, and L. L. Mummert, “The cost of hospitalization in Crohn’s disease,” Am. J. Gastroenterol. 95(2), 524–530 (2000).
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I. C. Lawrance, C. J. Welman, P. Shipman, and K. Murray, “Correlation of MRI-determined small bowel Crohn’s disease categories with medical response and surgical pathology,” World J. Gastroenterol. 15(27), 3367–3375 (2009).
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Ni, J.

Ntziachristos, V.

Oberhuber, G.

G. Oberhuber, P. C. Stangl, H. Vogelsang, E. Schober, F. Herbst, and C. Gasche, “Significant association of strictures and internal fistula formation in Crohn’s disease,” Virchows Arch. 437(3), 293–297 (2000).
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G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
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Pang, Y.

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
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Paolantonio, P.

P. Paolantonio, R. Ferrari, F. Vecchietti, S. Cucchiara, and A. Laghi, “Current status of MR imaging in the evaluation of IBD in a pediatric population of patients,” Eur. J. Radiol. 69(3), 418–424 (2009).
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I. Depoortere, T. Thijs, G. van Assche, J. C. Keith, and T. L. Peeters, “Dose-dependent effects of recombinant human interleukin-11 on contractile properties in rabbit 2,4,6-trinitrobenzene sulfonic acid colitis,” J. Pharmacol. Exp. Ther. 294(3), 983–990 (2000).
[PubMed]

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M. Boudiaf, P. Soyer, C. Terem, J. P. Pelage, E. Maissiat, and R. Rymer, “CT Evaluation of Small Bowel Obstruction,” Radiographics 21(3), 613–624 (2001).
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W. F. Cheong, S. A. Prahl, and A. J. Welch, “A review of the optical properties of biological tissues,” Quantum Electronics, IEEE Journal of 26(12), 2166–2185 (1990).
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G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
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K. Kim, L. A. Johnson, C. Jia, J. C. Joyce, S. Rangwalla, P. D. R. Higgins, and J. M. Rubin, “Noninvasive Ultrasound Elasticity Imaging (UEI) of Crohn’s Disease: Animal Model,” Ultrasound Med. Biol. 34(6), 902–912 (2008).
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Riecken, E.-O.

H. Matthes, H. Herbst, D. Schuppan, A. Stallmach, S. Milani, H. Stein, and E.-O. Riecken, “Cellular localization of procollagen gene transcripts in inflammatory bowel diseases,” Gastroenterology 102(2), 431–442 (1992).
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Roth, J. M.

R. D. Cohen, L. R. Larson, J. M. Roth, R. V. Becker, and L. L. Mummert, “The cost of hospitalization in Crohn’s disease,” Am. J. Gastroenterol. 95(2), 524–530 (2000).
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Rubin, J. M.

Y. Zhu, L. A. Johnson, Z. Huang, J. M. Rubin, J. Yuan, H. Lei, J. Ni, X. Wang, P. D. R. Higgins, and G. Xu, “Identifying intestinal fibrosis and inflammation by spectroscopic photoacoustic imaging: an animal study in vivo,” Biomed. Opt. Express 9(4), 1590–1600 (2018).
[Crossref] [PubMed]

J. R. Dillman, R. W. Stidham, P. D. Higgins, D. S. Moons, L. A. Johnson, and J. M. Rubin, “US elastography-derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model,” Radiology 267(3), 757–766 (2013).
[Crossref] [PubMed]

R. W. Stidham, J. Xu, L. A. Johnson, K. Kim, D. S. Moons, B. J. McKenna, J. M. Rubin, and P. D. Higgins, “Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease,” Gastroenterology 141(3), 819–826 (2011).
[Crossref] [PubMed]

K. Kim, L. A. Johnson, C. Jia, J. C. Joyce, S. Rangwalla, P. D. R. Higgins, and J. M. Rubin, “Noninvasive Ultrasound Elasticity Imaging (UEI) of Crohn’s Disease: Animal Model,” Ultrasound Med. Biol. 34(6), 902–912 (2008).
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Rymer, R.

M. Boudiaf, P. Soyer, C. Terem, J. P. Pelage, E. Maissiat, and R. Rymer, “CT Evaluation of Small Bowel Obstruction,” Radiographics 21(3), 613–624 (2001).
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G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
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G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
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E. V. Loftus, P. Schoenfeld, and W. J. Sandborn, “The epidemiology and natural history of Crohn’s disease in population-based patient cohorts from North America: a systematic review,” Aliment. Pharmacol. Ther. 16(1), 51–60 (2002).
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G. Oberhuber, P. C. Stangl, H. Vogelsang, E. Schober, F. Herbst, and C. Gasche, “Significant association of strictures and internal fistula formation in Crohn’s disease,” Virchows Arch. 437(3), 293–297 (2000).
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E. V. Loftus, P. Schoenfeld, and W. J. Sandborn, “The epidemiology and natural history of Crohn’s disease in population-based patient cohorts from North America: a systematic review,” Aliment. Pharmacol. Ther. 16(1), 51–60 (2002).
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H. Matthes, H. Herbst, D. Schuppan, A. Stallmach, S. Milani, H. Stein, and E.-O. Riecken, “Cellular localization of procollagen gene transcripts in inflammatory bowel diseases,” Gastroenterology 102(2), 431–442 (1992).
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Shipman, P.

I. C. Lawrance, C. J. Welman, P. Shipman, and K. Murray, “Correlation of MRI-determined small bowel Crohn’s disease categories with medical response and surgical pathology,” World J. Gastroenterol. 15(27), 3367–3375 (2009).
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Shung, K. K.

J.-M. Yang, C. Li, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Catheter-based photoacoustic endoscope,” J. Biomed. Opt. 19(6), 066001 (2014).
[Crossref] [PubMed]

C. Li, J.-M. Yang, R. Chen, C.-H. Yeh, L. Zhu, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Urogenital photoacoustic endoscope,” Opt. Lett. 39(6), 1473–1476 (2014).
[Crossref] [PubMed]

J.-M. Yang, R. Chen, C. Favazza, J. Yao, C. Li, Z. Hu, Q. Zhou, K. K. Shung, and L. V. Wang, “A 2.5-mm diameter probe for photoacoustic and ultrasonic endoscopy,” Opt. Express 20(21), 23944–23953 (2012).
[Crossref] [PubMed]

J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
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G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
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M. Boudiaf, P. Soyer, C. Terem, J. P. Pelage, E. Maissiat, and R. Rymer, “CT Evaluation of Small Bowel Obstruction,” Radiographics 21(3), 613–624 (2001).
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G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
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G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
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H. Matthes, H. Herbst, D. Schuppan, A. Stallmach, S. Milani, H. Stein, and E.-O. Riecken, “Cellular localization of procollagen gene transcripts in inflammatory bowel diseases,” Gastroenterology 102(2), 431–442 (1992).
[Crossref] [PubMed]

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G. Oberhuber, P. C. Stangl, H. Vogelsang, E. Schober, F. Herbst, and C. Gasche, “Significant association of strictures and internal fistula formation in Crohn’s disease,” Virchows Arch. 437(3), 293–297 (2000).
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H. Matthes, H. Herbst, D. Schuppan, A. Stallmach, S. Milani, H. Stein, and E.-O. Riecken, “Cellular localization of procollagen gene transcripts in inflammatory bowel diseases,” Gastroenterology 102(2), 431–442 (1992).
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J. R. Dillman, S. D. Swanson, L. A. Johnson, D. S. Moons, J. Adler, R. W. Stidham, and P. D. Higgins, “Comparison of noncontrast MRI magnetization transfer and T -Weighted signal intensity ratios for detection of bowel wall fibrosis in a Crohn’s disease animal model,” J. Magn. Reson. Imaging 42, 801–810 (2014).

J. R. Dillman, R. W. Stidham, P. D. Higgins, D. S. Moons, L. A. Johnson, and J. M. Rubin, “US elastography-derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model,” Radiology 267(3), 757–766 (2013).
[Crossref] [PubMed]

R. W. Stidham, J. Xu, L. A. Johnson, K. Kim, D. S. Moons, B. J. McKenna, J. M. Rubin, and P. D. Higgins, “Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease,” Gastroenterology 141(3), 819–826 (2011).
[Crossref] [PubMed]

Stoica, G.

M.-L. Li, H. E. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in vivo photoacoustic microscopy based on a virtual-detector concept,” Opt. Lett. 31(4), 474–476 (2006).
[Crossref] [PubMed]

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
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H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-Free Bond-Selective Imaging by Listening to Vibrationally Excited Molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
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J. R. Dillman, S. D. Swanson, L. A. Johnson, D. S. Moons, J. Adler, R. W. Stidham, and P. D. Higgins, “Comparison of noncontrast MRI magnetization transfer and T -Weighted signal intensity ratios for detection of bowel wall fibrosis in a Crohn’s disease animal model,” J. Magn. Reson. Imaging 42, 801–810 (2014).

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Z. Tarján, G. Tóth, T. Györke, A. Mester, K. Karlinger, and E. K. Makó, “Ultrasound in Crohn’s disease of the small bowel,” Eur. J. Radiol. 35(3), 176–182 (2000).
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M. Boudiaf, P. Soyer, C. Terem, J. P. Pelage, E. Maissiat, and R. Rymer, “CT Evaluation of Small Bowel Obstruction,” Radiographics 21(3), 613–624 (2001).
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I. Depoortere, T. Thijs, G. van Assche, J. C. Keith, and T. L. Peeters, “Dose-dependent effects of recombinant human interleukin-11 on contractile properties in rabbit 2,4,6-trinitrobenzene sulfonic acid colitis,” J. Pharmacol. Exp. Ther. 294(3), 983–990 (2000).
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G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
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Z. Tarján, G. Tóth, T. Györke, A. Mester, K. Karlinger, and E. K. Makó, “Ultrasound in Crohn’s disease of the small bowel,” Eur. J. Radiol. 35(3), 176–182 (2000).
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G. R. Lichtenstein, A. Olson, S. Travers, R. H. Diamond, D. M. Chen, M. L. Pritchard, B. G. Feagan, R. D. Cohen, B. A. Salzberg, S. B. Hanauer, and W. J. Sandborn, “Factors Associated with the Development of Intestinal Strictures or Obstructions in Patients with Crohn’s Disease,” Am. J. Gastroenterol. 101(5), 1030–1038 (2006).
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G. K. Makharia, S. Srivastava, P. Das, P. Goswami, U. Singh, M. Tripathi, V. Deo, A. Aggarwal, R. P. Tiwari, V. Sreenivas, and S. D. Gupta, “Clinical, Endoscopic, and Histological Differentiations Between Crohn’s Disease and Intestinal Tuberculosis,” Am. J. Gastroenterol. 105(3), 642–651 (2010).
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H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-Free Bond-Selective Imaging by Listening to Vibrationally Excited Molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
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I. Depoortere, T. Thijs, G. van Assche, J. C. Keith, and T. L. Peeters, “Dose-dependent effects of recombinant human interleukin-11 on contractile properties in rabbit 2,4,6-trinitrobenzene sulfonic acid colitis,” J. Pharmacol. Exp. Ther. 294(3), 983–990 (2000).
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P. Paolantonio, R. Ferrari, F. Vecchietti, S. Cucchiara, and A. Laghi, “Current status of MR imaging in the evaluation of IBD in a pediatric population of patients,” Eur. J. Radiol. 69(3), 418–424 (2009).
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G. Oberhuber, P. C. Stangl, H. Vogelsang, E. Schober, F. Herbst, and C. Gasche, “Significant association of strictures and internal fistula formation in Crohn’s disease,” Virchows Arch. 437(3), 293–297 (2000).
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H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-Free Bond-Selective Imaging by Listening to Vibrationally Excited Molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
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J.-M. Yang, C. Li, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Catheter-based photoacoustic endoscope,” J. Biomed. Opt. 19(6), 066001 (2014).
[Crossref] [PubMed]

C. Li, J.-M. Yang, R. Chen, C.-H. Yeh, L. Zhu, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Urogenital photoacoustic endoscope,” Opt. Lett. 39(6), 1473–1476 (2014).
[Crossref] [PubMed]

J.-M. Yang, R. Chen, C. Favazza, J. Yao, C. Li, Z. Hu, Q. Zhou, K. K. Shung, and L. V. Wang, “A 2.5-mm diameter probe for photoacoustic and ultrasonic endoscopy,” Opt. Express 20(21), 23944–23953 (2012).
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L. V. Wang and S. Hu, “Photoacoustic Tomography: In Vivo Imaging from Organelles To Organs,” Science 335(6075), 1458–1462 (2012).
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J.-M. Yang, C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, “Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo,” Nat. Med. 18(8), 1297–1302 (2012).
[Crossref] [PubMed]

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-Free Bond-Selective Imaging by Listening to Vibrationally Excited Molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
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M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
[Crossref]

M.-L. Li, H. E. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in vivo photoacoustic microscopy based on a virtual-detector concept,” Opt. Lett. 31(4), 474–476 (2006).
[Crossref] [PubMed]

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
[Crossref] [PubMed]

Wang, P.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-Free Bond-Selective Imaging by Listening to Vibrationally Excited Molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
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Y. Zhu, L. A. Johnson, Z. Huang, J. M. Rubin, J. Yuan, H. Lei, J. Ni, X. Wang, P. D. R. Higgins, and G. Xu, “Identifying intestinal fibrosis and inflammation by spectroscopic photoacoustic imaging: an animal study in vivo,” Biomed. Opt. Express 9(4), 1590–1600 (2018).
[Crossref] [PubMed]

H. Lei, L. A. Johnson, S. Liu, D. S. Moons, T. Ma, Q. Zhou, M. D. Rice, J. Ni, X. Wang, P. D. Higgins, and G. Xu, “Characterizing intestinal inflammation and fibrosis in Crohn’s disease by photoacoustic imaging: feasibility study,” Biomed. Opt. Express 7(7), 2837–2848 (2016).
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J. Yuan, G. Xu, Y. Yu, Y. Zhou, P. L. Carson, X. Wang, and X. Liu, “Real-time photoacoustic and ultrasound dual-modality imaging system facilitated with graphics processing unit and code parallel optimization,” J. Biomed. Opt. 18(8), 086001 (2013).
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X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
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Welch, A. J.

W. F. Cheong, S. A. Prahl, and A. J. Welch, “A review of the optical properties of biological tissues,” Quantum Electronics, IEEE Journal of 26(12), 2166–2185 (1990).
[Crossref]

Welman, C. J.

I. C. Lawrance, C. J. Welman, P. Shipman, and K. Murray, “Correlation of MRI-determined small bowel Crohn’s disease categories with medical response and surgical pathology,” World J. Gastroenterol. 15(27), 3367–3375 (2009).
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Wissmeyer, G.

Xie, X.

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 21(7), 803–806 (2003).
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Xu, G.

Xu, J.

R. W. Stidham, J. Xu, L. A. Johnson, K. Kim, D. S. Moons, B. J. McKenna, J. M. Rubin, and P. D. Higgins, “Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease,” Gastroenterology 141(3), 819–826 (2011).
[Crossref] [PubMed]

Xu, M.

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77(4), 041101 (2006).
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J. Yuan, G. Xu, Y. Yu, Y. Zhou, P. L. Carson, X. Wang, and X. Liu, “Real-time photoacoustic and ultrasound dual-modality imaging system facilitated with graphics processing unit and code parallel optimization,” J. Biomed. Opt. 18(8), 086001 (2013).
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Y. Li, Z. Zhu, J. C. Jing, J. J. Chen, A. E. Heidari, Y. He, J. Zhu, T. Ma, M. Yu, Q. Zhou, and Z. Chen, “High-Speed Integrated Endoscopic Photoacoustic and Ultrasound Imaging System,” IEEE J. Sel. Top. Quantum Electron. 25(1), 1–5 (2019).
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J. Yuan, G. Xu, Y. Yu, Y. Zhou, P. L. Carson, X. Wang, and X. Liu, “Real-time photoacoustic and ultrasound dual-modality imaging system facilitated with graphics processing unit and code parallel optimization,” J. Biomed. Opt. 18(8), 086001 (2013).
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Figures (8)

Fig. 1
Fig. 1 (a) Schematics of the prototype capsule-shaped acoustic resolution PA microscopy probe including the acquisition system. (b) Cross-section of the capsule-shaped probe. (c) Bottom view of the translation stage without capsule shell. (d) Illustration of the light path through the optical prism. (e) Calculated beam pattern projected onto bowel wall. (f) Photograph of the capsule-shaped probe.
Fig. 2
Fig. 2 (a) Relative optical absorption spectra of blood and collagen [34,35]. The vertical dashed lines mark the selected wavelengths at 720 and 1310 nm, respectively. a.u. = arbitrary units. Hb. = Hemoglobin. (b) and (c) are Monte Carlo simulated 2D light fluence distribution in the scanning plane at 720 and 1310 nm, respectively. (d) Light fluence distribution along the transducer focusing axis (red dashed lines in b and c).
Fig. 3
Fig. 3 (a) Acquired raw signals at signal step before taking average. (b) A-scan signal averaged from (a). (c) Delay compensated signals after data in (a) applied phase correlation, (d) A-scan signal averaged from (c). (e) Signals at 80 acquisition locations without compensation. (f) Signals at 80 acquisition locations after compensation. More consistent phase is shown among the measurements.
Fig. 4
Fig. 4 (a) Simulated US beam pattern for the focused transducer. (b) and (c) PA images show cross-sections of 40 μm nichrome wires at different depths before and after applying SAFT-CF, respectively. (d) Axial profiles for 3 targets labeled in (b) and (c) with an averaged FWHM of 65 μm (e) Lateral profiles with an averaged FWHM of 90 μm.
Fig. 5
Fig. 5 Experiment setup for rabbit intestine imaging in vivo.
Fig. 6
Fig. 6 (a) Histologic appearance of tissue from normal (untreated), acute, and chronic TNBS treated rabbit colons. Scalebars are 150 microns. (b) Gross appearance of unaffected, acute, and chronic colitis. (c) Fibrosis scores as determined by quantification in trichrome-stained sections (see 2.3.5 in methods section).
Fig. 7
Fig. 7 (a) Representative PA molecular component images of normal, acute and chronic conditions. Hemoglobin distribution was rendered in red and collagen distribution was rendered in green. Both color scales were normalized to the maximum relative concentration of hemoglobin. (b) The boxplots of averaged intensities of hemoglobin distribution for normal, acute, and chronic images. An approximately two-fold increase in hemoglobin signal intensity was observed in the acute condition compared to the normal condition (p = 0.0189). (c) The boxplots of averaged intensities of collagen distributions for normal, acute, and chronic condition. An approximately three-fold collagen signal intensity was observed in the chronic condition compared to the acute condition (p = 0.0002).
Fig. 8
Fig. 8 (a) Timeline of TNBS treatments (red arrows) and PA scans (blue arrows) in the longitudinal rabbit TNBS experiment. For each rabbit, the 1st in vivo imaging was acquired prior to the first TNBS treatment (T1) as the baseline. Considering the health/disease conditions of the rabbits, the 2nd imaging was acquired 2 or 3 weeks after T1 and right before T2. The 3rd imaging was acquired 3 or 4 weeks after T2 and right before T3. Rabbits were euthanized after the 4th imaging at week 8 (red dashed arrow). (b) PA molecular component images for longitudinal rabbit #4 at different time points. Both color scales were normalized to the maximum relative concentration of hemoglobin. (c) Averaged intensities of collagen distributions resolved from the four scans applied during the whole longitudinal study. The collagen development can be detected in all rabbits. A correlation of 0.798 can be found between the resolved collagen content and the number of TNBS treatments (p = 0.0002).

Equations (1)

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[ c Hb c cg ]= [ μ Hb720 μ cg720 μ Hb1310 μ cg1310 ] 1 ×[ A 720 A 1310 ]