Abstract

Optical coherence tomography (OCT) images largely lack molecular information or molecular contrast. We address that issue here, reporting on the development of biodegradable micro and nano-spheres loaded with methylene blue (MB) as molecular contrast agents for OCT. MB is a constituent of FDA approved therapies and widely used as a dye in off-label clinical applications. The sequestration of MB within the polymer reduced toxicity and improved signal strength by drastically reducing the production of singlet oxygen and leuco-MB. The former leads to tissue damage and the latter to reduced image contrast. The spheres are also strongly scattering which improves molecular contrast signal localization and enhances signal strength. We demonstrate that these contrast agents may be imaged using both pump-probe OCT and photothermal OCT, using a 830 nm frequency domain OCT system and a 1.3 µm swept source OCT system. We also show that these contrast agents may be functionalized and targeted to specific receptors, e.g. the VCAM receptor known to be overexpressed in inflammation.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2020 (2)

C. W. Merkle, M. Augustin, D. J. Harper, and B. Baumann, “Indocyanine green provides absorption and spectral contrast for optical coherence tomography at 840 nm in vivo,” Opt. Lett. 45(8), 2359–2362 (2020).
[Crossref]

P. Si, S. Shevidi, E. Yuan, K. Yuan, Z. Lautman, S. S. Jeffrey, G. W. Sledge, and A. de la Zerda, “Gold Nanobipyramids as Second Near Infrared Optical Coherence Tomography Contrast Agents for in Vivo Multiplexing Studies,” Nano Lett. 20(1), 101–108 (2020).
[Crossref]

2019 (2)

W. Kim, S. Kim, S. N. Huang, J. S. Oghalai, and B. E. Applegate, “Picometer scale vibrometry in the human middle ear using a surgical microscope based optical coherence tomography and vibrometry system,” Biomed. Opt. Express 10(9), 4395–4410 (2019).
[Crossref]

J. B. Dewey, B. E. Applegate, and J. S. Oghalai, “Amplification and Suppression of Traveling Waves along the Mouse Organ of Corti: Evidence for Spatial Variation in the Longitudinal Coupling of Outer Hair Cell-Generated Forces,” J. Neurosci. 39(10), 1805–1816 (2019).
[Crossref]

2017 (1)

J. Zhang, J. Liu, L. M. Wang, Z. Y. Li, and Z. Yuan, “Retroreflective-type Janus microspheres as a novel contrast agent for enhanced optical coherence tomography,” J. Biophotonics 10(6-7), 878–886 (2017).
[Crossref]

2016 (3)

N. Sharma, P. Madan, and S. S. Lin, “Effect of process and formulation variables on the preparation of parenteral paclitaxel-loaded biodegradable polymeric nanoparticles: A co-surfactant study,” Asian J. Pharm. Sci. 11(3), 404–416 (2016).
[Crossref]

C. W. Merkle and V. J. Srinivasan, “Laminar microvascular transit time distribution in the mouse somatosensory cortex revealed by Dynamic Contrast Optical Coherence Tomography,” NeuroImage 125, 350–362 (2016).
[Crossref]

C. Cannava, R. Stancanelli, M. R. Marabeti, V. Venuti, C. Cascio, P. Guarneri, C. Bongiorno, G. Sortino, D. Majolino, A. Mazzaglia, S. Tommasini, and C. A. Ventura, “Nanospheres based on PLGA/amphiphilic cyclodextrin assemblies as potential enhancers of Methylene Blue neuroprotective effect,” RSC Adv. 6(20), 16720–16729 (2016).
[Crossref]

2015 (4)

O. Carrasco-Zevallos, R. L. Shelton, W. Kim, J. Pearson, and B. E. Applegate, “In vivo pump-probe optical coherence tomography imaging in Xenopus laevis,” J. Biophotonics 8(1-2), 25–35 (2015).
[Crossref]

J. Kim, W. Brown, J. R. Maher, H. Levinson, and A. Wax, “Functional optical coherence tomography: principles and progress,” Phys. Med. Biol. 60(10), R211–R237 (2015).
[Crossref]

W. Kim and B. E. Applegate, “In vivo molecular contrast OCT imaging of methylene blue,” Opt. Lett. 40(7), 1426–1429 (2015).
[Crossref]

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U. S. A. 112(10), 3128–3133 (2015).
[Crossref]

2014 (5)

J. Park, E. F. Carbajal, X. Chen, J. S. Oghalai, and B. E. Applegate, “Phase-sensitive optical coherence tomography using an Vernier-tuned distributed Bragg reflector swept laser in the mouse middle ear,” Opt. Lett. 39(21), 6233–6236 (2014).
[Crossref]

Y. Kim, M. E. Lobatto, T. Kawahara, B. Lee Chung, A. J. Mieszawska, B. L. Sanchez-Gaytan, F. Fay, M. L. Senders, C. Calcagno, J. Becraft, M. Tun Saung, R. E. Gordon, E. S. Stroes, M. Ma, O. C. Farokhzad, Z. A. Fayad, W. J. Mulder, and R. Langer, “Probing nanoparticle translocation across the permeable endothelium in experimental atherosclerosis,” Proc. Natl. Acad. Sci. U. S. A. 111(3), 1078–1083 (2014).
[Crossref]

Q. R. J. G. Tummers, F. P. R. Verbeek, B. E. Schaafsma, M. C. Boonstra, J. R. van der Vorst, G. J. Liefers, C. J. H. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Real-time intraoperative detection of breast cancer using near-infrared fluorescence imaging and Methylene Blue,” Eur J. Surg. Onc. (EJSO) 40(7), 850–858 (2014).
[Crossref]

Y. Pan, J. You, N. D. Volkow, K. Park, and C. Du, “Ultrasensitive detection of 3D cerebral microvascular network dynamics in vivo,” NeuroImage 103, 492–501 (2014).
[Crossref]

H. Sakai, B. Li, W. L. Lim, and Y. Iga, “Red blood cells donate electrons to methylene blue mediated chemical reduction of methemoglobin compartmentalized in liposomes in blood,” Bioconjugate Chem. 25(7), 1301–1310 (2014).
[Crossref]

2013 (2)

M. Adhi and J. S. Duker, “Optical coherence tomography–current and future applications,” Curr. Opin. Ophthalmol. 24(3), 213–221 (2013).
[Crossref]

E. Morgounova, Q. Shao, B. J. Hackel, D. D. Thomas, and S. Ashkenazi, “Photoacoustic lifetime contrast between methylene blue monomers and self-quenched dimers as a model for dual-labeled activatable probes,” J. Biomed. Opt. 18(5), 056004 (2013).
[Crossref]

2012 (1)

A. Phinikaridou, M. E. Andia, A. Protti, A. Indermuehle, A. Shah, A. Smith, A. Warley, and R. M. Botnar, “Noninvasive magnetic resonance imaging evaluation of endothelial permeability in murine atherosclerosis using an albumin-binding contrast agent,” Circulation 126(6), 707–719 (2012).
[Crossref]

2011 (6)

M. Qin, H. J. Hah, G. Kim, G. Nie, Y. E. Lee, and R. Kopelman, “Methylene blue covalently loaded polyacrylamide nanoparticles for enhanced tumor-targeted photodynamic therapy,” Photochem. Photobiol. Sci. 10(5), 832–841 (2011).
[Crossref]

H. J. Hah, G. Kim, Y. E. Lee, D. A. Orringer, O. Sagher, M. A. Philbert, and R. Kopelman, “Methylene blue-conjugated hydrogel nanoparticles and tumor-cell targeted photodynamic therapy,” Macromol. Biosci. 11(1), 90–99 (2011).
[Crossref]

P. Charoenphol, S. Mocherla, D. Bouis, K. Namdee, D. J. Pinsky, and O. Eniola-Adefeso, “Targeting therapeutics to the vascular wall in atherosclerosis–carrier size matters,” Atherosclerosis 217(2), 364–370 (2011).
[Crossref]

H. K. Makadia and S. J. Siegel, “Poly Lactic-co-Glycolic Acid (PLGA) as Biodegradable Controlled Drug Delivery Carrier,” Polymers 3(3), 1377–1397 (2011).
[Crossref]

M. Oz, D. E. Lorke, M. Hasan, and G. A. Petroianu, “Cellular and molecular actions of Methylene Blue in the nervous system,” Med. Res. Rev. 31(1), 93–117 (2011).
[Crossref]

V. Klepac-Ceraj, N. Patel, X. Song, C. Holewa, C. Patel, R. Kent, M. M. Amiji, and N. S. Soukos, “Photodynamic effects of methylene blue-loaded polymeric nanoparticles on dental plaque bacteria,” Lasers Surg. Med. 43(7), 600–606 (2011).
[Crossref]

2010 (5)

D. Jacob, R. L. Shelton, and B. E. Applegate, “Fourier domain pump-probe optical coherence tomography imaging of Melanin,” Opt. Express 18(12), 12399–12410 (2010).
[Crossref]

J. M. Tarbell, “Shear stress and the endothelial transport barrier,” Cardiovasc. Res. 87(2), 320–330 (2010).
[Crossref]

N. V. Jyothi, P. M. Prasanna, S. N. Sakarkar, K. S. Prabha, P. S. Ramaiah, and G. Y. Srawan, “Microencapsulation techniques, factors influencing encapsulation efficiency,” J. Microencapsulation 27(3), 187–197 (2010).
[Crossref]

F. Prati, E. Regar, G. S. Mintz, E. Arbustini, C. Di Mario, I. K. Jang, T. Akasaka, M. Costa, G. Guagliumi, E. Grube, Y. Ozaki, F. Pinto, and P. W. Serruys, O. C. T. R. D. Expert’s, “Expert review document on methodology, terminology, and clinical applications of optical coherence tomography: physical principles, methodology of image acquisition, and clinical application for assessment of coronary arteries and atherosclerosis,” Eur. Heart J. 31(4), 401–415 (2010).
[Crossref]

P. Charoenphol, R. B. Huang, and O. Eniola-Adefeso, “Potential role of size and hemodynamics in the efficacy of vascular-targeted spherical drug carriers,” Biomaterials 31(6), 1392–1402 (2010).
[Crossref]

2009 (4)

S. Ngamruengphong, V. K. Sharma, and A. Das, “Diagnostic yield of methylene blue chromoendoscopy for detecting specialized intestinal metaplasia and dysplasia in Barrett's esophagus: a meta-analysis,” Gastrointest. Endosc. 69(6), 1021–1028 (2009).
[Crossref]

J. M. Lu, X. Wang, C. Marin-Muller, H. Wang, P. H. Lin, Q. Yao, and C. Chen, “Current advances in research and clinical applications of PLGA-based nanotechnology,” Expert Rev. Mol. Diagn. 9(4), 325–341 (2009).
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X. He, X. Wu, K. Wang, B. Shi, and L. Hai, “Methylene blue-encapsulated phosphonate-terminated silica nanoparticles for simultaneous in vivo imaging and photodynamic therapy,” Biomaterials 30(29), 5601–5609 (2009).
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M. J. Heslinga, E. M. Mastria, and O. Eniola-Adefeso, “Fabrication of biodegradable spheroidal microparticles for drug delivery applications,” J. Controlled Release 138(3), 235–242 (2009).
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2008 (5)

W. Tang, H. Xu, E. J. Park, M. A. Philbert, and R. Kopelman, “Encapsulation of methylene blue in polyacrylamide nanoparticle platforms protects its photodynamic effectiveness,” Biochem. Biophys. Res. Commun. 369(2), 579–583 (2008).
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X. Song, Y. Zhao, W. Wu, Y. Bi, Z. Cai, Q. Chen, Y. Li, and S. Hou, “PLGA nanoparticles simultaneously loaded with vincristine sulfate and verapamil hydrochloride: systematic study of particle size and drug entrapment efficiency,” Int. J. Pharm. 350(1-2), 320–329 (2008).
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S. Mao, Y. Shi, L. Li, J. Xu, A. Schaper, and T. Kissel, “Effects of process and formulation parameters on characteristics and internal morphology of poly(d,l-lactide-co-glycolide) microspheres formed by the solvent evaporation method,” Eur. J. Pharm. Biopharm. 68(2), 214–223 (2008).
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K. H. Song, E. W. Stein, J. A. Margenthaler, and L. V. Wang, “Noninvasive photoacoustic identification of sentinel lymph nodes containing methylene blue in vivo in a rat model,” J. Biomed. Opt. 13(5), 054033 (2008).
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2007 (2)

A. Budhian, S. J. Siegel, and K. I. Winey, “Haloperidol-loaded PLGA nanoparticles: systematic study of particle size and drug content,” Int. J. Pharm. 336(2), 367–375 (2007).
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J. Davies, D. Burke, J. R. Olliver, L. J. Hardie, C. P. Wild, and M. N. Routledge, “Methylene blue but not indigo carmine causes DNA damage to colonocytes in vitro and in vivo at concentrations used in clinical chromoendoscopy,” Gut 56(1), 155–156 (2007).
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2006 (1)

2005 (5)

W. Tang, H. Xu, R. Kopelman, and M. A. Philbert, “Photodynamic characterization and in vitro application of methylene blue-containing nanoparticle platforms,” Photochem. Photobiol. 81(2), 242–249 (2005).
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G. Isenberg, M. V. Sivak, A. Chak, R. C. Wong, J. E. Willis, B. Wolf, D. Y. Rowland, A. Das, and A. Rollins, “Accuracy of endoscopic optical coherence tomography in the detection of dysplasia in Barrett’s esophagus: a prospective, double-blinded study,” Gastrointest. Endosc. 62(6), 825–831 (2005).
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J. P. Tardivo, A. Del Giglio, C. S. de Oliveira, D. S. Gabrielli, H. C. Junqueira, D. B. Tada, D. Severino, R. de Fatima Turchiello, and M. S. Baptista, “Methylene blue in photodynamic therapy: From basic mechanisms to clinical applications,” Photodiagn. Photodyn. Ther. 2(3), 175–191 (2005).
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T. Gambichler, G. Moussa, M. Sand, D. Sand, P. Altmeyer, and K. Hoffmann, “Applications of optical coherence tomography in dermatology,” J. Dermatol. Sci. 40(2), 85–94 (2005).
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B. E. Applegate, C. H. Yang, and J. A. Izatt, “Theoretical comparison of the sensitivity of molecular contrast optical coherence tomography techniques,” Opt. Express 13(20), 8146–8163 (2005).
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2004 (5)

M. E. Keegan, J. L. Falcone, T. C. Leung, and W. M. Saltzman, “Biodegradable microspheres with enhanced capacity for covalently bound surface ligands,” Macromolecules 37(26), 9779–9784 (2004).
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J. M. May, Z. C. Qu, and C. E. Cobb, “Reduction and uptake of methylene blue by human erythrocytes,” Am. J. Physiol. Cell Physiol. 286(6), C1390–C1398 (2004).
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D. Gabrielli, E. Belisle, D. Severino, A. J. Kowaltowski, and M. S. Baptista, “Binding, aggregation and photochemical properties of methylene blue in mitochondrial suspensions,” Photochem. Photobiol. 79(3), 227–232 (2004).
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2003 (3)

N. C. Chesler and O. C. Enyinna, “Particle deposition in arteries ex vivo: effects of pressure, flow, and waveform,” J. Biomech. Eng. 125(3), 389–394 (2003).
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K. D. Rao, M. A. Choma, S. Yazdanfar, A. M. Rollins, and J. A. Izatt, “Molecular contrast in optical coherence tomography by use of a pump-probe technique,” Opt. Lett. 28(5), 340–342 (2003).
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D. Severino, H. C. Junqueira, M. Gugliotti, D. S. Gabrielli, and M. S. Baptista, “Influence of negatively charged interfaces on the ground and excited state properties of methylene blue,” Photochem. Photobiol. 77(5), 459–468 (2003).
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2002 (1)

M. C. DeRosa and R. J. Crutchley, “Photosensitized singlet oxygen and its applications,” Coord. Chem. Rev. 233-234, 351–371 (2002).
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2000 (2)

K. Orth, G. Beck, F. Genze, and A. Ruck, “Methylene blue mediated photodynamic therapy in experimental colorectal tumors in mice,” J. Photochem. Photobiol., B 57(2-3), 186–192 (2000).
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J. G. Fujimoto, C. Pitris, S. A. Boppart, and M. E. Brezinski, “Optical coherence tomography: An emerging technology for biomedical imaging and optical biopsy,” Neoplasia 2(1-2), 9–25 (2000).
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1999 (1)

R. W. Redmond and J. N. Gamlin, “A compilation of singlet oxygen yields from biologically relevant molecules,” Photochem. Photobiol. 70(4), 391–475 (1999).
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1995 (1)

R. Bonnett, “Photosensitizers of the Porphyrin and Phthalocyanine Series for Photodynamic Therapy,” Chem. Soc. Rev. 24(1), 19–33 (1995).
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1990 (1)

R. Alex and R. Bodmeier, “Encapsulation of water-soluble drugs by a modified solvent evaporation method. I. Effect of process and formulation variables on drug entrapment,” J. Microencapsulation 7(3), 347–355 (1990).
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1972 (1)

A. R. DiSanto and J. G. Wagner, “Pharmacokinetics of highly ionized drugs. II. Methylene blue–absorption, metabolism, and excretion in man and dog after oral administration,” J. Pharm. Sci. 61(4), 598–602 (1972).
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1967 (1)

G. S. Singhal and E. Rabinowi, “Changes in Absorption Spectrum of Methylene Blue with Ph,” J. Phys. Chem. 71(10), 3347–3349 (1967).
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M. Adhi and J. S. Duker, “Optical coherence tomography–current and future applications,” Curr. Opin. Ophthalmol. 24(3), 213–221 (2013).
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F. Prati, E. Regar, G. S. Mintz, E. Arbustini, C. Di Mario, I. K. Jang, T. Akasaka, M. Costa, G. Guagliumi, E. Grube, Y. Ozaki, F. Pinto, and P. W. Serruys, O. C. T. R. D. Expert’s, “Expert review document on methodology, terminology, and clinical applications of optical coherence tomography: physical principles, methodology of image acquisition, and clinical application for assessment of coronary arteries and atherosclerosis,” Eur. Heart J. 31(4), 401–415 (2010).
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Alex, R.

R. Alex and R. Bodmeier, “Encapsulation of water-soluble drugs by a modified solvent evaporation method. I. Effect of process and formulation variables on drug entrapment,” J. Microencapsulation 7(3), 347–355 (1990).
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Altmeyer, P.

T. Gambichler, G. Moussa, M. Sand, D. Sand, P. Altmeyer, and K. Hoffmann, “Applications of optical coherence tomography in dermatology,” J. Dermatol. Sci. 40(2), 85–94 (2005).
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Amiji, M. M.

V. Klepac-Ceraj, N. Patel, X. Song, C. Holewa, C. Patel, R. Kent, M. M. Amiji, and N. S. Soukos, “Photodynamic effects of methylene blue-loaded polymeric nanoparticles on dental plaque bacteria,” Lasers Surg. Med. 43(7), 600–606 (2011).
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Andia, M. E.

A. Phinikaridou, M. E. Andia, A. Protti, A. Indermuehle, A. Shah, A. Smith, A. Warley, and R. M. Botnar, “Noninvasive magnetic resonance imaging evaluation of endothelial permeability in murine atherosclerosis using an albumin-binding contrast agent,” Circulation 126(6), 707–719 (2012).
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Applegate, B. E.

J. B. Dewey, B. E. Applegate, and J. S. Oghalai, “Amplification and Suppression of Traveling Waves along the Mouse Organ of Corti: Evidence for Spatial Variation in the Longitudinal Coupling of Outer Hair Cell-Generated Forces,” J. Neurosci. 39(10), 1805–1816 (2019).
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W. Kim, S. Kim, S. N. Huang, J. S. Oghalai, and B. E. Applegate, “Picometer scale vibrometry in the human middle ear using a surgical microscope based optical coherence tomography and vibrometry system,” Biomed. Opt. Express 10(9), 4395–4410 (2019).
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H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U. S. A. 112(10), 3128–3133 (2015).
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W. Kim and B. E. Applegate, “In vivo molecular contrast OCT imaging of methylene blue,” Opt. Lett. 40(7), 1426–1429 (2015).
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O. Carrasco-Zevallos, R. L. Shelton, W. Kim, J. Pearson, and B. E. Applegate, “In vivo pump-probe optical coherence tomography imaging in Xenopus laevis,” J. Biophotonics 8(1-2), 25–35 (2015).
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J. Park, E. F. Carbajal, X. Chen, J. S. Oghalai, and B. E. Applegate, “Phase-sensitive optical coherence tomography using an Vernier-tuned distributed Bragg reflector swept laser in the mouse middle ear,” Opt. Lett. 39(21), 6233–6236 (2014).
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D. Jacob, R. L. Shelton, and B. E. Applegate, “Fourier domain pump-probe optical coherence tomography imaging of Melanin,” Opt. Express 18(12), 12399–12410 (2010).
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B. E. Applegate and J. A. Izatt, “Molecular imaging of endogenous and exogenous chromophores using ground state recovery pump-probe optical coherence tomography,” Opt. Express 14(20), 9142–9155 (2006).
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B. E. Applegate, C. H. Yang, and J. A. Izatt, “Theoretical comparison of the sensitivity of molecular contrast optical coherence tomography techniques,” Opt. Express 13(20), 8146–8163 (2005).
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Arbustini, E.

F. Prati, E. Regar, G. S. Mintz, E. Arbustini, C. Di Mario, I. K. Jang, T. Akasaka, M. Costa, G. Guagliumi, E. Grube, Y. Ozaki, F. Pinto, and P. W. Serruys, O. C. T. R. D. Expert’s, “Expert review document on methodology, terminology, and clinical applications of optical coherence tomography: physical principles, methodology of image acquisition, and clinical application for assessment of coronary arteries and atherosclerosis,” Eur. Heart J. 31(4), 401–415 (2010).
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E. Morgounova, Q. Shao, B. J. Hackel, D. D. Thomas, and S. Ashkenazi, “Photoacoustic lifetime contrast between methylene blue monomers and self-quenched dimers as a model for dual-labeled activatable probes,” J. Biomed. Opt. 18(5), 056004 (2013).
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Augustin, M.

Baptista, M. S.

J. P. Tardivo, A. Del Giglio, C. S. de Oliveira, D. S. Gabrielli, H. C. Junqueira, D. B. Tada, D. Severino, R. de Fatima Turchiello, and M. S. Baptista, “Methylene blue in photodynamic therapy: From basic mechanisms to clinical applications,” Photodiagn. Photodyn. Ther. 2(3), 175–191 (2005).
[Crossref]

D. Gabrielli, E. Belisle, D. Severino, A. J. Kowaltowski, and M. S. Baptista, “Binding, aggregation and photochemical properties of methylene blue in mitochondrial suspensions,” Photochem. Photobiol. 79(3), 227–232 (2004).
[Crossref]

D. Severino, H. C. Junqueira, M. Gugliotti, D. S. Gabrielli, and M. S. Baptista, “Influence of negatively charged interfaces on the ground and excited state properties of methylene blue,” Photochem. Photobiol. 77(5), 459–468 (2003).
[Crossref]

Baumann, B.

Beck, G.

K. Orth, G. Beck, F. Genze, and A. Ruck, “Methylene blue mediated photodynamic therapy in experimental colorectal tumors in mice,” J. Photochem. Photobiol., B 57(2-3), 186–192 (2000).
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Becraft, J.

Y. Kim, M. E. Lobatto, T. Kawahara, B. Lee Chung, A. J. Mieszawska, B. L. Sanchez-Gaytan, F. Fay, M. L. Senders, C. Calcagno, J. Becraft, M. Tun Saung, R. E. Gordon, E. S. Stroes, M. Ma, O. C. Farokhzad, Z. A. Fayad, W. J. Mulder, and R. Langer, “Probing nanoparticle translocation across the permeable endothelium in experimental atherosclerosis,” Proc. Natl. Acad. Sci. U. S. A. 111(3), 1078–1083 (2014).
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Belisle, E.

D. Gabrielli, E. Belisle, D. Severino, A. J. Kowaltowski, and M. S. Baptista, “Binding, aggregation and photochemical properties of methylene blue in mitochondrial suspensions,” Photochem. Photobiol. 79(3), 227–232 (2004).
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Bi, Y.

X. Song, Y. Zhao, W. Wu, Y. Bi, Z. Cai, Q. Chen, Y. Li, and S. Hou, “PLGA nanoparticles simultaneously loaded with vincristine sulfate and verapamil hydrochloride: systematic study of particle size and drug entrapment efficiency,” Int. J. Pharm. 350(1-2), 320–329 (2008).
[Crossref]

Bodmeier, R.

R. Alex and R. Bodmeier, “Encapsulation of water-soluble drugs by a modified solvent evaporation method. I. Effect of process and formulation variables on drug entrapment,” J. Microencapsulation 7(3), 347–355 (1990).
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Bongiorno, C.

C. Cannava, R. Stancanelli, M. R. Marabeti, V. Venuti, C. Cascio, P. Guarneri, C. Bongiorno, G. Sortino, D. Majolino, A. Mazzaglia, S. Tommasini, and C. A. Ventura, “Nanospheres based on PLGA/amphiphilic cyclodextrin assemblies as potential enhancers of Methylene Blue neuroprotective effect,” RSC Adv. 6(20), 16720–16729 (2016).
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R. Bonnett, “Photosensitizers of the Porphyrin and Phthalocyanine Series for Photodynamic Therapy,” Chem. Soc. Rev. 24(1), 19–33 (1995).
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Q. R. J. G. Tummers, F. P. R. Verbeek, B. E. Schaafsma, M. C. Boonstra, J. R. van der Vorst, G. J. Liefers, C. J. H. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Real-time intraoperative detection of breast cancer using near-infrared fluorescence imaging and Methylene Blue,” Eur J. Surg. Onc. (EJSO) 40(7), 850–858 (2014).
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J. G. Fujimoto, C. Pitris, S. A. Boppart, and M. E. Brezinski, “Optical coherence tomography: An emerging technology for biomedical imaging and optical biopsy,” Neoplasia 2(1-2), 9–25 (2000).
[Crossref]

Botnar, R. M.

A. Phinikaridou, M. E. Andia, A. Protti, A. Indermuehle, A. Shah, A. Smith, A. Warley, and R. M. Botnar, “Noninvasive magnetic resonance imaging evaluation of endothelial permeability in murine atherosclerosis using an albumin-binding contrast agent,” Circulation 126(6), 707–719 (2012).
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Bouis, D.

P. Charoenphol, S. Mocherla, D. Bouis, K. Namdee, D. J. Pinsky, and O. Eniola-Adefeso, “Targeting therapeutics to the vascular wall in atherosclerosis–carrier size matters,” Atherosclerosis 217(2), 364–370 (2011).
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Brezinski, M. E.

J. G. Fujimoto, C. Pitris, S. A. Boppart, and M. E. Brezinski, “Optical coherence tomography: An emerging technology for biomedical imaging and optical biopsy,” Neoplasia 2(1-2), 9–25 (2000).
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J. Kim, W. Brown, J. R. Maher, H. Levinson, and A. Wax, “Functional optical coherence tomography: principles and progress,” Phys. Med. Biol. 60(10), R211–R237 (2015).
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Budhian, A.

A. Budhian, S. J. Siegel, and K. I. Winey, “Haloperidol-loaded PLGA nanoparticles: systematic study of particle size and drug content,” Int. J. Pharm. 336(2), 367–375 (2007).
[Crossref]

Burke, D.

J. Davies, D. Burke, J. R. Olliver, L. J. Hardie, C. P. Wild, and M. N. Routledge, “Methylene blue but not indigo carmine causes DNA damage to colonocytes in vitro and in vivo at concentrations used in clinical chromoendoscopy,” Gut 56(1), 155–156 (2007).
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Cai, Z.

X. Song, Y. Zhao, W. Wu, Y. Bi, Z. Cai, Q. Chen, Y. Li, and S. Hou, “PLGA nanoparticles simultaneously loaded with vincristine sulfate and verapamil hydrochloride: systematic study of particle size and drug entrapment efficiency,” Int. J. Pharm. 350(1-2), 320–329 (2008).
[Crossref]

Calcagno, C.

Y. Kim, M. E. Lobatto, T. Kawahara, B. Lee Chung, A. J. Mieszawska, B. L. Sanchez-Gaytan, F. Fay, M. L. Senders, C. Calcagno, J. Becraft, M. Tun Saung, R. E. Gordon, E. S. Stroes, M. Ma, O. C. Farokhzad, Z. A. Fayad, W. J. Mulder, and R. Langer, “Probing nanoparticle translocation across the permeable endothelium in experimental atherosclerosis,” Proc. Natl. Acad. Sci. U. S. A. 111(3), 1078–1083 (2014).
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Cannava, C.

C. Cannava, R. Stancanelli, M. R. Marabeti, V. Venuti, C. Cascio, P. Guarneri, C. Bongiorno, G. Sortino, D. Majolino, A. Mazzaglia, S. Tommasini, and C. A. Ventura, “Nanospheres based on PLGA/amphiphilic cyclodextrin assemblies as potential enhancers of Methylene Blue neuroprotective effect,” RSC Adv. 6(20), 16720–16729 (2016).
[Crossref]

Carbajal, E. F.

Carrasco-Zevallos, O.

O. Carrasco-Zevallos, R. L. Shelton, W. Kim, J. Pearson, and B. E. Applegate, “In vivo pump-probe optical coherence tomography imaging in Xenopus laevis,” J. Biophotonics 8(1-2), 25–35 (2015).
[Crossref]

Cascio, C.

C. Cannava, R. Stancanelli, M. R. Marabeti, V. Venuti, C. Cascio, P. Guarneri, C. Bongiorno, G. Sortino, D. Majolino, A. Mazzaglia, S. Tommasini, and C. A. Ventura, “Nanospheres based on PLGA/amphiphilic cyclodextrin assemblies as potential enhancers of Methylene Blue neuroprotective effect,” RSC Adv. 6(20), 16720–16729 (2016).
[Crossref]

Chak, A.

G. Isenberg, M. V. Sivak, A. Chak, R. C. Wong, J. E. Willis, B. Wolf, D. Y. Rowland, A. Das, and A. Rollins, “Accuracy of endoscopic optical coherence tomography in the detection of dysplasia in Barrett’s esophagus: a prospective, double-blinded study,” Gastrointest. Endosc. 62(6), 825–831 (2005).
[Crossref]

Charoenphol, P.

P. Charoenphol, S. Mocherla, D. Bouis, K. Namdee, D. J. Pinsky, and O. Eniola-Adefeso, “Targeting therapeutics to the vascular wall in atherosclerosis–carrier size matters,” Atherosclerosis 217(2), 364–370 (2011).
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P. Charoenphol, R. B. Huang, and O. Eniola-Adefeso, “Potential role of size and hemodynamics in the efficacy of vascular-targeted spherical drug carriers,” Biomaterials 31(6), 1392–1402 (2010).
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Chen, C.

J. M. Lu, X. Wang, C. Marin-Muller, H. Wang, P. H. Lin, Q. Yao, and C. Chen, “Current advances in research and clinical applications of PLGA-based nanotechnology,” Expert Rev. Mol. Diagn. 9(4), 325–341 (2009).
[Crossref]

Chen, Q.

X. Song, Y. Zhao, W. Wu, Y. Bi, Z. Cai, Q. Chen, Y. Li, and S. Hou, “PLGA nanoparticles simultaneously loaded with vincristine sulfate and verapamil hydrochloride: systematic study of particle size and drug entrapment efficiency,” Int. J. Pharm. 350(1-2), 320–329 (2008).
[Crossref]

Chen, X.

Chesler, N. C.

N. C. Chesler and O. C. Enyinna, “Particle deposition in arteries ex vivo: effects of pressure, flow, and waveform,” J. Biomech. Eng. 125(3), 389–394 (2003).
[Crossref]

Choma, M. A.

Cobb, C. E.

J. M. May, Z. C. Qu, and C. E. Cobb, “Reduction and uptake of methylene blue by human erythrocytes,” Am. J. Physiol. Cell Physiol. 286(6), C1390–C1398 (2004).
[Crossref]

Costa, M.

F. Prati, E. Regar, G. S. Mintz, E. Arbustini, C. Di Mario, I. K. Jang, T. Akasaka, M. Costa, G. Guagliumi, E. Grube, Y. Ozaki, F. Pinto, and P. W. Serruys, O. C. T. R. D. Expert’s, “Expert review document on methodology, terminology, and clinical applications of optical coherence tomography: physical principles, methodology of image acquisition, and clinical application for assessment of coronary arteries and atherosclerosis,” Eur. Heart J. 31(4), 401–415 (2010).
[Crossref]

Crutchley, R. J.

M. C. DeRosa and R. J. Crutchley, “Photosensitized singlet oxygen and its applications,” Coord. Chem. Rev. 233-234, 351–371 (2002).
[Crossref]

Das, A.

S. Ngamruengphong, V. K. Sharma, and A. Das, “Diagnostic yield of methylene blue chromoendoscopy for detecting specialized intestinal metaplasia and dysplasia in Barrett's esophagus: a meta-analysis,” Gastrointest. Endosc. 69(6), 1021–1028 (2009).
[Crossref]

G. Isenberg, M. V. Sivak, A. Chak, R. C. Wong, J. E. Willis, B. Wolf, D. Y. Rowland, A. Das, and A. Rollins, “Accuracy of endoscopic optical coherence tomography in the detection of dysplasia in Barrett’s esophagus: a prospective, double-blinded study,” Gastrointest. Endosc. 62(6), 825–831 (2005).
[Crossref]

Davies, J.

J. Davies, D. Burke, J. R. Olliver, L. J. Hardie, C. P. Wild, and M. N. Routledge, “Methylene blue but not indigo carmine causes DNA damage to colonocytes in vitro and in vivo at concentrations used in clinical chromoendoscopy,” Gut 56(1), 155–156 (2007).
[Crossref]

de Fatima Turchiello, R.

J. P. Tardivo, A. Del Giglio, C. S. de Oliveira, D. S. Gabrielli, H. C. Junqueira, D. B. Tada, D. Severino, R. de Fatima Turchiello, and M. S. Baptista, “Methylene blue in photodynamic therapy: From basic mechanisms to clinical applications,” Photodiagn. Photodyn. Ther. 2(3), 175–191 (2005).
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P. Si, S. Shevidi, E. Yuan, K. Yuan, Z. Lautman, S. S. Jeffrey, G. W. Sledge, and A. de la Zerda, “Gold Nanobipyramids as Second Near Infrared Optical Coherence Tomography Contrast Agents for in Vivo Multiplexing Studies,” Nano Lett. 20(1), 101–108 (2020).
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J. P. Tardivo, A. Del Giglio, C. S. de Oliveira, D. S. Gabrielli, H. C. Junqueira, D. B. Tada, D. Severino, R. de Fatima Turchiello, and M. S. Baptista, “Methylene blue in photodynamic therapy: From basic mechanisms to clinical applications,” Photodiagn. Photodyn. Ther. 2(3), 175–191 (2005).
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Del Giglio, A.

J. P. Tardivo, A. Del Giglio, C. S. de Oliveira, D. S. Gabrielli, H. C. Junqueira, D. B. Tada, D. Severino, R. de Fatima Turchiello, and M. S. Baptista, “Methylene blue in photodynamic therapy: From basic mechanisms to clinical applications,” Photodiagn. Photodyn. Ther. 2(3), 175–191 (2005).
[Crossref]

DeRosa, M. C.

M. C. DeRosa and R. J. Crutchley, “Photosensitized singlet oxygen and its applications,” Coord. Chem. Rev. 233-234, 351–371 (2002).
[Crossref]

Dewey, J. B.

J. B. Dewey, B. E. Applegate, and J. S. Oghalai, “Amplification and Suppression of Traveling Waves along the Mouse Organ of Corti: Evidence for Spatial Variation in the Longitudinal Coupling of Outer Hair Cell-Generated Forces,” J. Neurosci. 39(10), 1805–1816 (2019).
[Crossref]

Di Mario, C.

F. Prati, E. Regar, G. S. Mintz, E. Arbustini, C. Di Mario, I. K. Jang, T. Akasaka, M. Costa, G. Guagliumi, E. Grube, Y. Ozaki, F. Pinto, and P. W. Serruys, O. C. T. R. D. Expert’s, “Expert review document on methodology, terminology, and clinical applications of optical coherence tomography: physical principles, methodology of image acquisition, and clinical application for assessment of coronary arteries and atherosclerosis,” Eur. Heart J. 31(4), 401–415 (2010).
[Crossref]

DiSanto, A. R.

A. R. DiSanto and J. G. Wagner, “Pharmacokinetics of highly ionized drugs. II. Methylene blue–absorption, metabolism, and excretion in man and dog after oral administration,” J. Pharm. Sci. 61(4), 598–602 (1972).
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Kim, W.

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M. Oz, D. E. Lorke, M. Hasan, and G. A. Petroianu, “Cellular and molecular actions of Methylene Blue in the nervous system,” Med. Res. Rev. 31(1), 93–117 (2011).
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Figures (9)

Fig. 1.
Fig. 1. SEM images of (A) MB-PLGA microparticles (50:50 PLGA) and (C) MB-PLGA nanoparticles (75:25 PLGA). Effect of mechanical stir speed on MB-PLGA particle size: (B) Magnetic stirrer speed on 50:50 PLGA microparticles (3% surfactant, pH 8.4), (D) Sonicator tip resonance amplitude on 75:25 PLGA nanoparticles (3% surfactant, pH 8.4). Value = mean ± SD (n = 3, number of particle batches analyzed).
Fig. 2.
Fig. 2. (A) Optical density of methylene blue solutions at different concentrations suspended in DI water. (B) Effect of continuous phase pH on MB encapsulation efficiency and particle size of PLGA microparticles (50:50 PLGA, 3% surfactant). (C) Optical density spectrum of PLGA microparticles loaded with different concentrations of methylene blue. (D) Methylene blue release from 50:50 PLGA microparticles and 50:50 and 75:25 PLGA nanoparticles in DPBS at pH 7.4, 37°C. Value = mean ± SD (n = 3).
Fig. 3.
Fig. 3. (A) Normalized absorption spectrum of MB solution, MB-PLGA microparticles (MB µp), and nanoparticles (MB np). (B) Diagram of molecular energy transitions for the methylene blue transient absorption and photothermal effect. Driven energy transitions are indicated by straight arrows and spontaneous transitions as wavy arrows. (C) Normalized MB fluorescence emission at 680 nm over time after addition of NADH enzyme to free MB, MB-PLGA microparticles and MB-PLGA nanoparticles in DI water. (D) Percentage of ADPA bleaching for free MB, MB-PLGA microparticles and MB-PLGA-nanoparticles with our pump 660 nm light source for 30 min. Value = mean ± SD (n = 3).
Fig. 4.
Fig. 4. (A) Schematic of PLGA particle surface functionalization with biotinylated antibodies. (B) Flow cytometry histogram of aVCAM-1 MB-PLGA microparticles labeled with a FITC-secondary antibody (blue) and uncoated MB-PLGA microparticles (gray). (C) ELISA assay results of functionalized MB-PLGA micro (MP) and nanoparticles (NP) (HRP-secondary antibody). Statistical significance is indicated as * for p < 0.05.
Fig. 5.
Fig. 5. Fourier domain analysis along time of (A) magnitude and (B) phase components from FD-OCT M-scans containing signal MB microparticles. Doted lines indicate range of frequencies considered as noise floor.
Fig. 6.
Fig. 6. Transient absorption decays of (A) MB-PLGA micro and nanoparticles, and (B) MB solution and MB nanoparticles suspended in DI water with atmospheric oxygen saturation (assumed a SO2 of 20.95%). (C) Transient absorption decays of MB-PLGA nanoparticles at different relative SO2%. (B) Avg lifetime of MB nanoparticles as function of relative SO2%. NEOFOX oxygen sensor probe (Ocean Optics, Inc.) was used to estimate the relative SO2%.
Fig. 7.
Fig. 7. (A) PLGA microparticles with average diameter of 2.7 µm loaded with 8.9, 22.9 and 42.9 mM of MB. (B) Magnitude and (C) phase and (D) complex B-scans of MB-PLGA particles suspended in 200 µm capillary tubes. (E) CNR values at the magnitude, phase and complex images for each batch of PLGA-MB microparticles. (F) Number of pixels with CNR greater than the established threshold (CNR≥4).
Fig. 8.
Fig. 8. PDMS microchannels (500 µm inner diameter) loaded with MB solution, MB-PLGA microparticles and MB-PLGA nanoparticles. The OCT B-scan is shown in gray scale with the molecular contrast signal overlain in blue. Images were recorded with the FD-OCT system (830 nm probe) for the top 3 rows and the SS-OCT system (1310 nm) in the bottom row. Note: The nanospheres had not entirely settled to the bottom of the microchannel in the SS-OCT images, hence the weak signal above a stronger signal at the bottom of the microchannel. Pump-off images show no molecular contrast signal because the threshold, CNR≥4, was sufficient to remove all background, hence there was no molecular contrast signal when the pump was off.
Fig. 9.
Fig. 9. Images of human artery sections treated with (A-B) aVCAM-1 MB-PLGA microparticles and (C-D) aVCAM-1 MB-PLGA nanoparticles. OCT B-scans (gray scale) with overlain molecular contrast (complex) signal (blue) (A,C) and their respective histology sections (B,D). Calcified regions are indicated with reds arrows.

Tables (1)

Tables Icon

Table 1. Fabrication parameters optimized to form MB loaded PLGA particles of the intended average diameters.