Elucidating structure and function in vivo with hybrid fluorescence and magnetic resonance imaging

Proceedings of the IEEE

Volumn 96, Issue 3, 2008, Pages 382-396

  Niedre, Mark ^a   Ntziachristos, Vasilis ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Dual modality; Fluorescence; Imaging; Magnetic resonance imaging (MRI); Optical

Indexed keywords

FLUORESCENCE; IMAGING TECHNIQUES; MAGNETIC RESONANCE IMAGING; MAGNETISM; RESONANCE;

CLINICAL APPLICATION; COMPLEMENTARY FEATURES; COREGISTRATION; DIFFERENT GEOMETRY; DUAL MODALITY; HYBRID IMAGING; MULTI-MODALITY; OPTICAL;

FLUORESCENCE IMAGING;

EID: 64549091353     PISSN: 00189219     EISSN: None     Source Type: Journal    
DOI: 10.1109/JPROC.2007.913498     Document Type: Article

References (88)

1. R. Weissleder, "Molecular imaging in cancer," Science, vol. 312, pp. 1168-1171, May 2006.
2. B. N. Giepmans, S. R. Adams, M. H. Ellisman, and R. Y. Tsien, "The fluorescent toolbox for assessing protein location and function," Science, vol. 312, pp. 217-224, 2006.
3. H. R. Herschman, "Molecular imaging: Looking at problems, seeing solutions," Science, vol. 302, pp. 605-608, 2003.
4. T. Jiang et al., "Tumor imaging by means of proteolytic activation of cell-penetrating peptides," Proc. Nat. Acad. Sci. USA, vol. 101, pp. 17867-17872, 2004.
5. T. F. Massoud and S. S. Gambhir, "Molecular imaging in living subjects: Seeing fundamental biological processes in a new light," Genes Dev., vol. 7, pp. 545-580, 2003.
6. V. Ntziachristos, J. Ripoll, L. V. Wang, and R. Weissleder, "Looking and listening to light: The evolution of whole-body photonic imaging," Nature Biotechnol., vol. 23, pp. 313-320, Mar. 2005.
7. V. Ntziachristos et al., "Visualization of antitumor treatment by means of fluorescence molecular tomography with an annexin V-Cy5.5 conjugate," Proc. Nat. Acad. Sci. USA, vol. 17, pp. 12294-12299, Aug. 2004.
8. J. Grimm et al., "Use of gene expression profiling to direct in vivo molecular imaging of lung cancer," Proc. Nat. Acad. Sci. USA, vol. 102, pp. 14404-14409, Oct. 2005.
9. D. E. Sosnovik et al., "Fluorescence tomography and magnetic resonance imaging of myocardial macrophage infiltration in infarcted myocardium in vivo," Circulation, vol. 115, pp. 1384-1391, Mar. 2007.
10. G. Zacharakis et al., "Volumetric tomography of fluorescent proteins through small animals in vivo," Proc. Nat. Acad. Sci. USA, vol. 102, pp. 18252-18257, Dec. 2005.
11. S. Patwardhan, S. Bloch, S. Achilefu, and J. Culver, "Time-dependent whole-body fluorescence tomography of probe bio-distributions in mice," Opt. Expr., vol. 13, pp. 2564-2577, 2005.
12. S. Ke, X. Wen, M. Gurfinkel, C. Charnsangavej, S. Wallace, E. M. Sevick-Muraca, and C. Li, "Near-infrared optical imaging of epidermal growth factor receptor in breast cancer xenografts," Cancer Res., vol. 63, pp. 7870-7875, Nov. 15, 2003.
13. E. M. Haacke, R. W. Brown, M. R. Thompson, and R. Venkatesan, Magnetic Resonance Imaging: Physical Principles and Sequence Design. New York: Wiley, 1999.
14. Z. Liang and P. C. Lauterbur, Principles of Magnetic Resonance Imaging: A Signal Processing Perspective. New York: IEEE Press, 2000.
15. R. G. Pautler and S. E. Fraser, "The year(s) of the contrast agent-Micro-MRI in the new millennium," Curr. Opinion Immunol., vol. 15, pp. 385-392, 2003.
16. D. E. Sosnovik and R. Weissleder, "Emerging concepts in molecular MRI," Curr. Opinion Biotechnol., vol. 18, pp. 4-10, 2007.
17. R. Weissleder et al., "In vivo magnetic resonance imaging of transgene expression," Nature Med., vol. 6, pp. 351-354, 2000.
18. E. A. Schellenberger et al., "Annexin V-CLIO: A nanoparticle for detecting apoptosis by MRI," Mol. Imag., vol. 1, pp. 102-107, Apr. 2002.
19. M. A. Funovics et al., "MR imaging of the her2/neu and 9.2.27 tumor antigens using immunospecific contrast agents," Magn. Res. Imag., vol. 22, pp. 843-850, 2004.
20. J. C. Frias, K. J. Williams, E. A. Fisher, and Z. A. Fayad, "Recombinant HDL-like nanopartides: A specific contrast agent for MRI of atherosclerotic plaques," J. Amer. Chem. Soc., vol. 126, pp. 16316-16317, 2004.
21. V. Amirbekian et al., "Detecting and assessing macrophages in vivo to evaluate atherosclerosis noninvasively using molecular MRI," Proc. Nat. Acad. Sci. USA, vol. 104, pp. 961-966, 2007.
22. B. A. Moffat et al., "A novel Polyacrylamide magnetic nanoparticle contrast agent for molecular imaging using MRI," Mol. Imag., vol. 2, pp. 324-332, 2005.
23. A. Y. Louie et al., "In vivo visualization of gene expression using magnetic resonance imaging," Nature Biotechnol., vol. 18, pp. 321-325, 2000.
24. B. W. Pogue and K. D. Paulsen, "High-resolution near-infrared tomographic imaging simulations of the rat cranium by use of a priori magnetic resonance imaging structural information," Opt. Lett., vol. 23, pp. 1716-1718, Nov. 1998.
25. S. Merritt, F. Bevilacqua, A. J. Durkin, D. J. Cuccia, R. Lanning, B. J. Tromberg, G. Guisen, H. Yu, J. Wang, and O. Nalcioglu, "Coregistration of diffuse optical spectroscopy and magnetic resonance imaging in a rat tumor model," Appl. Opt., vol. 42, pp. 2951-2959, Jun. 2003.
26. V. Ntziachristos, A. G. Yodh, M. Schnall, and B. Chance, "Concurrent MRI and diffuse optical tomography of breast after indocyanine green enhancement," Proc. Nat. Acad. Sci. USA, vol. 97, pp. 2767-2772, Mar. 14, 2000.
27. V. Ntziachristos, A. G. Yodh, M. D. Schnall, and B. Chance, "MRI-guided diffuse optical spectroscopy of malignant and benign breast lesions," Neoplasia, vol. 4, pp. 347-354, 2002.
28. B. Brooksby et al., "Imaging breast adipose and fibroglandular tissue molecular signatures by using hybrid MRI-guided near-infrared spectral tomography," Proc. Nat. Acad. Sci. USA, vol. 103, pp. 8828-8833, 2006.
29. T. Durduran, G. Yu, M. G. Burnett, J. A. Detre, J. H. Greenberg, J. Wang, C. Zhou, and A. G. Yodh, "Diffuse optical measurement of blood flow, blood oxygenation, and metabolism in a human brain during sensorimotor cortex activation," Opt. Lett., vol. 29, pp. 1766-1768, Aug. 2004.
30. T. J. Huppert, R. D. Hoge, A. M. Dale, M. A. Franceschini, and D. A. Boas, "Quantitative spatial comparison of diffuse optical imaging with blood oxygen level-dependent and arterial spin labeling-based functional magnetic resonance imaging," J. Biomed. Opt., vol. 11, p. 064018, Nov. 2006.
31. R. L. Barbour, H. L. Graber, and J. Chang, "MRI-guided optical tomography: Prospects and computation for a new imaging method," IEEE Numer. Algorithms Comput. Electromagn., vol. 2, pp. 63-77, 1995.
32. S. R. Arridge and M. Schweiger, "Sensitivity to prior knowledge in optical tomographic reconstruction," in Proc. SPIE, 1995, vol. 2389, pp. 378-388.
33. A. Li et al., "Tomographic optical breast imaging guided by three-dimensional mammography," Appl. Opt., vol. 42, pp. 5181-5190, Sep. 2003.
34. Q. Zhu, T. Durduran, V. Ntziachristos, M. Holboke, and A. G. Yodh, "Imager that combines near-infrared diffusive light and ultrasound," Opt. Lett., vol. 24, pp. 1050-1052, Aug. 1999.
35. Q. Zhu, N. G. Chen, and S. H. Kurtzman, "Imaging tumor angiogenesis by use of combined near-infrared diffusive light and ultrasound," Opt. Lett, vol. 23, pp. 337-339, 2003.
36. E. E. Graves, R. Weissleder, and V. Ntziachristos, "Fluorescence molecular imaging of small animal tumor models," Curr. Mol. Med., vol. 4, pp. 419-430, 2004.
37. A. P. Gibson, J. C. Hebden, and S. R. Arridge, "Recent advances in diffuse optical imaging," Phys. Med. Biol., vol. 50, pp. R1-R43, 2005.
38. M. A. O'Leary, D. A. Boas, B. Chance, and A. G. Yodh, "Experimental images of heterogeneous turbid media by frequency-domain diffusing-photon tomography," Opt. Expr., vol. 20, pp. 426-428, 1995.
39. V. Ntziachristos, C. H. Tung, C. Bremer, and R. Weissleder, "Fluorescence molecular tomography resolves protease activity in vivo," Nat. Med., vol. 8, pp. 757-760, 2002.
40. A. Yodh and B. Chance, "Spectroscopy and imaging with diffusing light," Phys. Today, vol. 48, pp. 34-40, Mar. 1995.
41. M. Gurfinkel, S. Ke, X. Wen, C. Li, and E. M. Sevick-Muraca, "Near-infrared fluorescence optical imaging and tomography," Dis. Markers, vol. 9, pp. 107-121, 2004.
42. W. Cai et al., "Time-resolved optical diffusion tomographic image reconstruction in highly scattering turbid media," Proc. Nat. Acad. Sci. USA, vol. 93, pp. 13561-13564, 1996.
43. G. M. Turner, G. Zacharakis, A. Soubret, J. Ripoll, and V. Ntziachristos, "Complete-angle projection diffuse optical tomography by use of early photons," Opt. Lett., vol. 30, pp. 409-411, 2005.
44. M. S. Patterson, B. Chance, and B. C. Wilson, "Time resolved reflectance and transmittance for the non-invasive measurement of tissue optical properties," Appl. Opt., vol. 28, pp. 2331-2336, 1989.
45. W. Cai, M. Lax, and R. R. Alfano, "Cumulant solution of the elastic Boltzmann transport equation in an infinite uniform medium," Phys. Rev. E., vol. 61, pp. 3871-3876, 2000.
46. M. Xu, W. Cai, M. Lax, and R. R. Alfano, "Photon migration in turbid media using a cumulant approximation to radiative transfer," Phys. Rev. E., vol. 65, p. 066609, 2002.
47. A. Bluestone, G. Abdoulaev, C. Schmitz, R. Barbour, and A. Hielscher, "Three-dimensional optical tomography of hemodynamics in the human head," Opt. Expr., vol. 9, pp. 272-286, Sep. 2001.
48. T. O. McBride et al., "Multispectral near-infrared tomography: A case study in compensating for water and lipid content in hemoglobin imaging of the breast," J. Biomed. Opt., vol. 7, pp. 72-79, Jan. 2002.
49. S. R. Arridge, "Photon-measurement density functions. Part I: Analytical forms," Appl. Opt., vol. 34, pp. 7395-7409, 1995.
50. V. Ntziachristos, B. Chance, and A. G. Yodh, "Differential diffuse optical tomography," Opt. Expr., vol. 5, pp. 230-242, 1999.
51. N. Shah, J. Gibbs, D. Wolverton, A. Cerussi, N. Hylton, and B. J. Tromberg, "Combined diffuse optical spectroscopy and contrast-enhanced magnetic resonance imaging for monitoring breast cancer neoadjuvant chemotherapy: A case study," J. Biomed. Opt., vol. 10, p. 051503, Sep.-Oct. 2005.
52. D. Hsiang, N. Shaw, H. Yu, M. Y. Su, A. Cerussi, J. Butler, C. Baick, R. Mehta, O. Nalcioglu, and B. Tromberg, "Coregistration of dynamic contrast enhance MRI and broadband diffuse optical spectroscopy for characterizing breast cancer," Technol. Cancer Res. Treat., vol. 4, pp. 549-558, Oct. 2005.
53. M. Paley, J. E. Mayhew, A. J. Martindale, J. McGinley, J. Berwick, P. Coffey, P. Redgrave, P. Furness, M. Port, A. Ham, Y. Zheng, M. Jones, E. Whitby, E. J. van Beek, I. D. Wilkinson, G. Darwent, and P. D. Griffiths, "Design and initial evaluation of a low-cost 3-Tesla research system for combined optical and functional MR imaging with interventional capability," J. Magn. Res. Imag., vol. 13, pp. 87-92, Jan. 2001.
54. T. Lasser and V. Ntziachristos, "Optimization of 360 degrees projection fluorescence molecular tomography," Med. Image Anal., vol. 11, pp. 389-399, Aug. 2007.
55. E. E. Graves, J. P. Culver, J. Ripoll, R. Weissleder, and V. Ntziachristos, "Singular-value analysis and optimization of experimental parameters in fluorescence molecular tomography," J. Opt. Soc. Amer. A: Opt. Image Sci. Vis., vol. 21, pp. 231-241, Feb. 2004.
56. J. P. Culver, V. Ntziachristos, M. J. Holboke, and A. G. Yodh, "Optimization of optode arrangements for diffuse optical tomography: A singular-value analysis," Opt. Lett., vol. 26, pp. 701-703, May 2001.
57. X. Ouyang, W. H. Wong, V. E. Johnson, X. Hu, and C. Chen, "Incorporation of correlated structural images in PET image reconstruction," IEEE Trans. Med. Imag., vol. 13, pp. 627-640, 1994.
58. C. T. Chen, X. Ouyang, W. H. Wong, X. Hu, V. E. Johnson, C. Ordonez, and C. E. Metz, "Sensor fusion in image reconstruction," IEEE Trans. Nucl. Sci., vol. 48, pp. 687-692, 1991.
59. J. Chang, H. L. Graber, P. C. Koo, R. Aronson, S. S. Barbour, and R. L. Barbour, "Optical imaging of anatomical maps derived from magnetic resonance images using time-independent optical sources," IEEE Trans. Med. Imag., vol. 16, pp. 68-77, Feb. 1997.
60. B. A. Brooksby, H. Dehghani, B. W. Pogue, and K. D. Paulsen, "Near-infrared (NIR) tomography breast image reconstruction with a priori structural information from MRI: Algorithm development for reconstructing heterogeneities," IEEE J. Sel. Topics Quantum Electron., vol. 9, pp. 199-209, Mar./Apr. 2003.
61. M. A. O'Leary, "Imaging with diffuse photon density waves," Ph.D. dissertation, Univ. of Pennsylvania, Philadelphia, 1996.
62. M. Schweiger and S. R. Arridge, "Optical tomographic reconstruction in a complex head model using a priori region boundary information," Phys. Med. Biol., vol. 44, pp. 2703-2721, 1999.
63. B. Brooksby et al., "Combining near-infrared tomography and magnetic resonance imaging to study in vivo breast tissue: Implementation of a Laplacian-type regularization to incorporate magnetic resonance structure," J. Biomed. Opt., vol. 10, p. 051504, Sep.-Oct. 2005.
64. H. Dehghani, B. W. Pogue, J. Shudong, B. Brooksby, and K. D. Paulsen, "Three-dimensional optical tomography: Resolution in small-object imaging," Appl. Opt., vol. 42, pp. 3117-3128, Jun. 2003.
65. P. K. Yalavarthy, B. W. Pogue, H. Dehghani, and K. D. Paulsen, "Weight-matrix structured regularization provides optimal generalized least-squares estimate in diffuse optical tomography," Med. Phys., vol. 24, pp. 2085-2098, Jun. 2007.
66. C. M. Carpenter, B. W. Pogue, S. Jiang, H. Dehghani, X. Wang, K. D. Paulsen, W. A. Wells, J. Forero, C. Kogel, J. B. Weaver, S. P. Poplack, and P. A. Kaufman, "Image-guided optical spectroscopy provides molecular-specific information in vivo: MRI-guided spectroscopy of breast cancer hemoglobin, water, and scatterer size," Opt. Lett, vol. 15, pp. 933-935, Apr. 2007.
67. S. C. Davis et al, "Image-guided diffuse optical fluorescence tomography implemented with Laplacian-type regularization," Opt. Expr., vol. 15, pp. 4066-4082, 2007.
68. D. Hyde, R. H. de Kleine, S. A. MacLaurin, E. Miller, D. H. Brooks, T. Krucker, and V. Ntziachristos, "Multi-modal FMT-CT method for in-vivo imaging of amyloid-beta plaques in a murine Alzheimer's model," unpublished.
69. L. Shan, S. Wang, R. Sridhar, Z. M. Bhujwalla, and P. C. Wang, "Dual probe with fluorescent and magnetic properties for imaging solid tumor xenografts," Mol. Imag., vol. 6, pp. 85-95, Apr.-Jun. 2007.
70. H. Li, B. D. Gray, I. Corbin, C. Lebherz, H. Choi, S. Lund-Katz, J. M. Wilson, J. D. Glickson, and R. Zhou, "MR and fluorescent imaging of low-density lipoprotein receptors," Acad. Radiol., vol. 11, pp. 1251-1259, Nov. 2004.
71. N. V. Evgenov, Z. Medarova, G. Dai, S. Bonner-Weir, and A. Moore, "In vivo imaging of islet transplantation," Nature Med., vol. 12, pp. 144-148, Jan. 2006.
72. E. A. Schellenberger, D. Sosnovik, R. Weissleder, and L. Josephson, "Magneto/optical annexin V, a multimodal protein," Bioconj. Chem., vol. 15, pp. 1062-1067, 2004.
73. X. Montet, R. Weissleder, and L. Josephson, "Imaging pancreatic cancer with a peptide-nanoparticle conjugate targeted to normal pancreas," Bioconj. Chem., vol. 17, pp. 905-911, 2006.
74. W. J. Mulder, G. J. Strijkers, J. W. Habets, E. J. Bleeker, D. W. van der Schaft, G. Storm, G. A. Koning, A. W. Griffioen, and K. Nicolay, "MR molecular imaging and fluorescence microscopy for identification of activated tumor endothelium using a bimodal lipidic nanoparticle," FASEB J., vol. 19, pp. 2008-2010, Dec. 2005.
75. W. J. Mulder, R. Koole, R. J. Brandwijk, G. Storm, P. T. Chin, G. J. Strijkers, C. de Mello Donegá, K. Nicolay, and A. W. Griffioen, "Quantum dots with a paramagnetic coating as a bimodal molecular imaging probe," Nano Lett., vol. 6, pp. 1-6, Jan. 2006.
76. S. Wang, B. R. Jarrett, S. M. Kauzlarich, and A. Y. Louie, "Core/shell quantum dots with high relaxivity and photoluminescence for multimodality imaging," J. Amer. Chem. Soc., vol. 129, pp. 3848-3856, Apr. 2007.
77. Y. M. Huh, Y. W. Jun, H. T. Song, K. Sungjin, J. S. Choi, J. H. Lee, S. Yoon, K. S. Kim, J. S. Shin, J. S. Suh, and J. Cheon, "In vivo magnetic resonance detection of cancer using multifunctional magnetic nanocrystals," J. Amer. Chem. Soc., vol. 127, pp. 12387-12391, Sep. 2005.
78. H. Choi, S. R. Choi, R. Zhou, H. F. Kung, and I. W. Chen, "Iron oxide nanoparticles as magnetic resonance contrast agent for tumor imaging via folate receptor-targeted delivery," Acad. Radiol., vol. 11, pp. 996-1004, Sep. 2004.
79. P. Varallyay, G. Nesbit, L. L. Muldoon, R. R. Nixon, J. Delashaw, J. I. Cohen, A. Petrillo, D. Rink, and E. A. Neuwelt, "Comparison of two superparamagnetic viral-sized iron oxide particles ferumoxides and ferumoxtran-10 with a gadolinium chelate in imaging intracranial tumors," AJNR Amer. I. Neuroradiol., vol. 23, pp. 510-519, 2002.
80. W. S. Enochs, G. Harsh, F. Hochberg, and R. Weissleder, "Improved delineation of human brain tumors on MR images using a long-circulating, superparamagnetic iron oxide agent," J. Magn. Res. Imag., vol. 9, pp. 228-232, 1999.
81. M. G. Harisinghani, J. Barentsz, P. F. Hahn, W. M. Deserno, S. Tabatabaei, C. H. van de Kaa, J. de la Rosette, and R. Weissleder, "Noninvasive detection of clinically occult lymph-node metastases in prostate cancer," New Eng. J. Med., vol. 348, pp. 2491-2499, 2003.
82. A. Bogaards, A. Varma, S. P. Collens, A. Lin, A. Giles, V. X. Yang, J. M. Bilbao, L. D. Lilge, P. J. Muller, and B. C. Wilson, "Increased brain tumor resection using fluorescence image guidance in a preclinical model," Lasers Surg. Med., vol. 35, pp. 181-190, 2004.
83. M. F. Kircher, U. Mahmood, R. S. King, R. Weissleder, and L. Josephson, "A multimodal nanoparticle for preoperative magnetic resonance imaging and intraoperative optical brain tumor delineation," Cancer Res., vol. 63, pp. 8122-8125, 2003.
84. F. Amersi and N. M. Hansen, "The benefits and limitations of sentinel lymph node biopsy," Curr. Treatment Options Oncol., vol. 7, pp. 141-151, Mar. 2006.
85. V. S. Talanov et al., "Dendrimer-based nanoprobe for dual modality magnetic resonance and fluorescence imaging," Nano Lett., vol. 6, pp. 1459-1463, 2006.
86. Y. Koyama et al., "A dendrimer-based nanosized contrast agent dual-labeled for magnetic resonance and optical fluorescence imaging to localize the sentinel lymph node in mice, " J. Magn. Res. Imag., vol. 25, pp. 866-871, 2007.
87. R. H. de Kleine and N. Deliolanis, personal communication.
88. X. Montet, V. Ntziachristos, J. Grimm, and R. Weissleder, "Tomographic fluorescence mapping of tumor targets," Cancer Res., vol. 65, pp. 6330-6336, Jul. 15, 2005.