Abstract

Analysis of semi-transparent low scattering biological structures in optical coherence tomography (OCT) has been actively pursued in the context of lymphatic imaging, with most approaches relying on the relative absence of signal as a means of detection. Here we present an alternate methodology based on spatial speckle statistics, utilizing the similarity of a distribution of given voxel intensities to the power distribution function of pure noise, to visualize the low-scattering biological structures of interest. In a human tumor xenograft murine model, we show that these correspond to lymphatic vessels and nerves; extensive histopathologic validation studies are reported to unequivocally establish this correspondence. The emerging possibility of OCT lymphangiography and neurography is novel and potentially impactful (especially the latter), although further methodology refinement is needed to distinguish between the visualized lymphatics and nerves.

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

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    [Crossref]
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2019 (1)

A. L. Matveyev, L. A. Matveev, A. A. Moiseev, A. A. Sovetsky, G. V. Gelikonov, and V. Y. Zaitsev, “Semi-analytical full-wave model for simulations of scans in optical coherence tomography with accounting for beam focusing and the motion of scatterers,” Laser Phys. Lett. 16(8), 085601 (2019).
[Crossref]

2018 (5)

V. Demidov, O. Demidova, A. Shabunin, and A. Vitkin, “Alternative contrast mechanism in optical coherence tomography: temporal speckle synchronization effects,” Modern Tech. Med. 10(1), 39–48 (2018).
[Crossref]

V. Demidov, X. Zhao, O. Demidova, H. Y. M. Pang, C. Flueraru, F. F. Liu, and I. A. Vitkin, “Preclinical quantitative in-vivo assessment of skin tissue vascularity in radiation induced fibrosis with optical coherence tomography,” J. Biomed. Opt. 23(10), 1 (2018).
[Crossref]

V. Demidov, A. Maeda, M. Sugita, V. Madge, S. Sadanand, C. Flueraru, and I. A. Vitkin, “Preclinical longitudinal imaging of tumor microvascular radiobiological response with functional optical coherence tomography,” Sci. Rep. 8(1), 38 (2018).
[Crossref]

P. Gong, D. Y. Yu, Q. Wang, P. K. Yu, K. Karnowski, M. Heisler, A. Francke, D. An, M. V. Sarunic, and D. D. Sampson, “Label-free volumetric imaging of conjunctival collecting lymphatics ex vivo by optical coherence tomography lymphangiography,” J. Biophotonics 11(8), e201800070 (2018).
[Crossref]

J. Hope, B. Braeuer, S. Amirapu, A. McDaid, and F. Vanholsbeeck, “Extracting morphometric information from rat sciatic nerve using optical coherence tomography,” J. Biomed. Opt. 23(11), 1 (2018).
[Crossref]

2017 (1)

M. Almasian, T. G. van Leeuwen, and D. J. Faber, “OCT amplitude and speckle statistics of discrete random media,” Sci. Rep. 7(1), 14873–11 (2017).
[Crossref]

2016 (3)

2015 (3)

L. A. Matveev, V. Y. Zaitsev, G. V. Gelikonov, A. L. Matveyev, A. A. Moiseev, S. Y. Ksenofontov, V. M. Gelikonov, M. A. Sirotkina, N. D. Gladkova, V. Demidov, and A. Vitkin, “Hybrid M-mode-like OCT imaging of three-dimensional microvasculature in vivo using reference-free processing of complex valued B-scans,” Opt. Lett. 40(7), 1472–1475 (2015).
[Crossref]

M. Almasian, N. Bosschaart, T. G. van Leeuwen, and D. J. Faber, “Validation of quantitative attenuation and backscattering coefficient measurements by optical coherence tomography in the concentration- dependent and multiple scattering regime,” J. Biomed. Opt. 20(12), 121314 (2015).
[Crossref]

F. P. Henry, Y. Wang, C. Rodriguez, M. A. Randolph, E. Rust, J. M. Winograd, J. F. de Boer, and B. H. Park, “In vivo optical microscopy of peripheral nerve myelination with polarization sensitive-optical coherence tomography,” J. Biomed. Opt. 20(4), 046002 (2015).
[Crossref]

2014 (2)

S. A. Stacker, S. P. Williams, T. Karnezis, R. Shayan, S. B. Fox, and M. G. Achen, “Lymphangiogenesis and lymphatic vessel remodelling in cancer,” Nat. Rev. Cancer 14(3), 159–172 (2014).
[Crossref]

V. Y. Zaitsev, L. A. Matveev, A. L. Matveyev, G. V. Gelikonov, and V. M. Gelikonov, “A model for simulating speckle-pattern evolution based on close to reality procedures used in spectral-domain OCT,” Laser Phys. Lett. 11(10), 105601 (2014).
[Crossref]

2013 (3)

Q. Lu, J. Hua, M. M. Kassir, Z. Delproposto, Y. Dai, J. Sun, M. Haacke, and J. Hu, “Imaging lymphatic system in breast cancer patients with magnetic resonance lymphangiography,” PLoS One 8(7), e69701 (2013).
[Crossref]

S. Li, Y. Sun, and D. Gao, “Role of the nervous system in cancer metastasis,” Oncol. Lett. 5(4), 1101–1111 (2013).
[Crossref]

S. Yousefi, J. Qin, Z. Zhi, and R. K. Wang, “Label-free optical lymphangiography: development of an automatic segmentation method applied to optical coherence tomography to visualize lymphatic vessels using Hessian filters,” J. Biomed. Opt. 18(8), 086004 (2013).
[Crossref]

2012 (1)

M. E. Miller, B. Palla, Q. Chen, D. A. Elashoff, E. Abemayor, J. M. St. John, and C. K. Lai, “A novel classification system for perineural invasion in noncutaneous head and neck squamous cell carcinoma: histologic subcategories and patient outcomes,” Am. J. Otolaryngol. 33(2), 212–215 (2012).
[Crossref]

2011 (6)

S. K. Thawait, V. Chaudhry, G. K. Thawait, K. C. Wang, A. Belzberg, J. A. Carrino, and A. Chhabra, “High-resolution MR neurography of diffuse peripheral nerve lesions,” Am. J. Neuroradiol. 32(8), 1365–1372 (2011).
[Crossref]

D. Albo, C. L. Akay, C. L. Marshall, J. A. Wilks, G. Verstovsek, H. Liu, N. Agarwal, D. H. Berger, and G. E. Ayala, “Neurogenesis in colorectal cancer is a marker of aggressive tumor behavior and poor outcomes,” Cancer 117(21), 4834–4845 (2011).
[Crossref]

F. Y. Feng, Y. Qian, M. H. Stenmark, S. Halverson, K. Blas, S. Vance, H. M. Sandler, and D. A. Hamstra, “Perineural invasion predicts increased recurrence, metastasis, and death from prostate cancer following treatment with dose-escalated radiation therapy,” Int. J. Radiat. Oncol., Biol., Phys. 81(4), e361–e367 (2011).
[Crossref]

D. P. Popescu, L. P. Choo-Smith, C. Flueraru, Y. Mao, S. Chang, J. Disano, S. Sherif, and M. G. Sowa, “Optical coherence tomography: fundamental principles, instrumental designs and biomedical applications,” Biophys. Rev. 3(3), 155–169 (2011).
[Crossref]

K. Alitalo, “The lymphatic vasculature in disease,” Nat. Med. 17(11), 1371–1380 (2011).
[Crossref]

Y. Mao, C. Flueraru, S. Chang, D. Popescu, and M. Sowa, “High-quality tissue imaging using a catheter-based swept-source optical coherence tomography systems with an integrated semiconductor optical amplifier,” IEEE Trans. Instrum. Meas. 60(10), 3376–3383 (2011).
[Crossref]

2010 (3)

M. Khasraw and J. B. Posner, “Neurological complications of systemic cancer,” Lancet Neurol. 9(12), 1214–1227 (2010).
[Crossref]

C. A. Chlebicki, A. D. Lee, W. Jung, H. Li, L. H. Liaw, Z. Chen, and B. J. Wong, “Preliminary investigation on use of high-resolution optical coherence tomography to monitor injury and repair in the rat sciatic nerve,” Lasers Surg. Med. 42(4), 306–312 (2010).
[Crossref]

C. Lamirel, N. J. Newman, and V. Biousse, “Optical coherence tomography (OCT) in optic neuritis and multiple sclerosis,” Rev. Neurol. 166(12), 978–986 (2010).
[Crossref]

2009 (5)

M. Jhawer, D. Coit, M. Brennan, L. X. Qin, M. Gonen, D. Klimstra, L. Tang, D. P. Kelsen, and M. A. Shah, “Perineural invasion after preoperative chemotherapy predicts poor survival in patients with locally advanced gastric cancer: gene expression analysis with pathologic validation,” Am. J. Clin. Oncol. 32(4), 356–362 (2009).
[Crossref]

L. M. Sakata, J. Deleon-Ortega, V. Sakata, and C. A. Girkin, “Optical coherence tomography of the retina and optic nerve - a review,” Clin. Experiment. Ophthalmol. 37(1), 90–99 (2009).
[Crossref]

A. Filler, “MR neurography and diffusion tensor imaging: origins, history & clinical impact,” Neurosurgery 65(suppl_4), A29–A43 (2009).
[Crossref]

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med. 15(10), 1219–1223 (2009).
[Crossref]

G. N. Armaiz-Pena, S. K. Lutgendorf, S. W. Cole, and A. K. Sood, “Neuroendocrine modulation of cancer progression,” Brain, Behav., Immun. 23(1), 10–15 (2009).
[Crossref]

2008 (6)

E. Sevick, R. Sharma, J. Rasmussen, M. Marshall, J. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. Blanchard, R. Fisher, S. B. Chiang, R. Elledge, and M. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study1,” Radiology 246(3), 734–741 (2008).
[Crossref]

J. H. Li, Q. Y. Ma, S. G. Shen, and H. T. Hu, “Stimulation of dorsal root ganglion neurons activity by pancreatic cancer cell lines,” Cell Biol. Int. 32(12), 1530–1535 (2008).
[Crossref]

F. Entschladen, D. Palm, B. Niggemann, and K. S. Zaenker, “The cancer's nervous tooth: considering the neuronal crosstalk within tumors,” Semin. Cancer Biol. 18(3), 171–175 (2008).
[Crossref]

Y. Mao, S. Sherif, C. Flueraru, and S. Chang, “3×3 Mach-Zehnder interferometer with unbalanced differential detection for full-range swept-source optical coherence tomography,” Appl. Opt. 47(12), 2004–2010 (2008).
[Crossref]

R. K. Wang, “Directional blood flow imaging in volumetric optical microangiography achieved by digital frequency modulation,” Opt. Lett. 33(16), 1878–1880 (2008).
[Crossref]

A. Mariampillai, B. A. Standish, E. H. Moriyama, M. Khurana, N. R. Munce, M. K. Leung, J. Jiang, A. Cable, B. C. Wilson, I. A. Vitkin, and V. X. Yang, “Speckle variance detection of microvasculature using swept-source optical coherence tomography,” Opt. Lett. 33(13), 1530–1532 (2008).
[Crossref]

2007 (2)

D. T. Raphael, C. Yang, N. Tresser, J. Wu, Y. Zhang, and L. Rever, “Images of spinal nerves and adjacent structures with optical coherence tomography: preliminary animal studies,” J. Pain 8(10), 767–773 (2007).
[Crossref]

K. Hayashi, P. Jiang, K. Yamauchi, N. Yamamoto, H. Tsuchiya, K. Tomita, A. R. Moossa, M. Bouvet, and R. M. Hoffman, “Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels,” Cancer Res. 67(17), 8223–8228 (2007).
[Crossref]

2006 (1)

K. Yasufuku, T. Nakajima, K. Motoori, Y. Sekine, K. Shibuya, K. Hiroshima, and T. Fujisawa, “Comparison of endobronchial ultrasound, positron emission tomography, and CT for lymph node staging of lung cancer,” Chest 130(3), 710–718 (2006).
[Crossref]

2005 (2)

O. Birim, A. P. Kappetein, T. Stijnen, and A. J. Bogers, “Meta-analysis of positron emission tomographic and computed tomographic imaging in detecting mediastinal lymph node metastases in nonsmall cell lung cancer,” Ann. Thorac. Surg. 79(1), 375–382 (2005).
[Crossref]

B. Karamata, K. Hassler, M. Laubscher, and T. Lasser, “Speckle statistics in optical coherence tomography,” J. Opt. Soc. Am. A 22(4), 593–596 (2005).
[Crossref]

2004 (1)

N. Isaka, T. P. Padera, J. Hagendoorn, D. Fukumura, and R. K. Jain, “Peritumor lymphatics induced by Vascular Endothelial Growth Factor-C exhibit abnormal function,” Cancer Res. 64(13), 4400–4404 (2004).
[Crossref]

2001 (1)

P. Seifert and M. Spitznas, “Tumours may be innervated,” Virchows Arch. 438(3), 228–231 (2001).
[Crossref]

1999 (2)

G. A. Dumanian, M. A. McClinton, and T. M. Brushart, “The effects of free fat grafts on the stiffness of the rat sciatic nerve and perineural scar,” J. Hand Surg. 24(1), 30–36 (1999).
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J. M. Schmitt, S. H. Xiang, and K. M. Yung, “Speckle in optical coherence tomography,” J. Biomed. Opt. 4(1), 95 (1999).
[Crossref]

1990 (1)

R. K. Jain, “Delivery of novel therapeutic agents in tumors: physiological barriers and strategies,” J. Natl. Cancer Inst. 81(8), 570–576 (1990).
[Crossref]

Abemayor, E.

M. E. Miller, B. Palla, Q. Chen, D. A. Elashoff, E. Abemayor, J. M. St. John, and C. K. Lai, “A novel classification system for perineural invasion in noncutaneous head and neck squamous cell carcinoma: histologic subcategories and patient outcomes,” Am. J. Otolaryngol. 33(2), 212–215 (2012).
[Crossref]

Achen, M. G.

S. A. Stacker, S. P. Williams, T. Karnezis, R. Shayan, S. B. Fox, and M. G. Achen, “Lymphangiogenesis and lymphatic vessel remodelling in cancer,” Nat. Rev. Cancer 14(3), 159–172 (2014).
[Crossref]

Adams, K. E.

E. Sevick, R. Sharma, J. Rasmussen, M. Marshall, J. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. Blanchard, R. Fisher, S. B. Chiang, R. Elledge, and M. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study1,” Radiology 246(3), 734–741 (2008).
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Agarwal, N.

D. Albo, C. L. Akay, C. L. Marshall, J. A. Wilks, G. Verstovsek, H. Liu, N. Agarwal, D. H. Berger, and G. E. Ayala, “Neurogenesis in colorectal cancer is a marker of aggressive tumor behavior and poor outcomes,” Cancer 117(21), 4834–4845 (2011).
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Akay, C. L.

D. Albo, C. L. Akay, C. L. Marshall, J. A. Wilks, G. Verstovsek, H. Liu, N. Agarwal, D. H. Berger, and G. E. Ayala, “Neurogenesis in colorectal cancer is a marker of aggressive tumor behavior and poor outcomes,” Cancer 117(21), 4834–4845 (2011).
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Albo, D.

D. Albo, C. L. Akay, C. L. Marshall, J. A. Wilks, G. Verstovsek, H. Liu, N. Agarwal, D. H. Berger, and G. E. Ayala, “Neurogenesis in colorectal cancer is a marker of aggressive tumor behavior and poor outcomes,” Cancer 117(21), 4834–4845 (2011).
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Alitalo, K.

K. Alitalo, “The lymphatic vasculature in disease,” Nat. Med. 17(11), 1371–1380 (2011).
[Crossref]

Almasian, M.

M. Almasian, T. G. van Leeuwen, and D. J. Faber, “OCT amplitude and speckle statistics of discrete random media,” Sci. Rep. 7(1), 14873–11 (2017).
[Crossref]

M. Almasian, N. Bosschaart, T. G. van Leeuwen, and D. J. Faber, “Validation of quantitative attenuation and backscattering coefficient measurements by optical coherence tomography in the concentration- dependent and multiple scattering regime,” J. Biomed. Opt. 20(12), 121314 (2015).
[Crossref]

Amirapu, S.

J. Hope, B. Braeuer, S. Amirapu, A. McDaid, and F. Vanholsbeeck, “Extracting morphometric information from rat sciatic nerve using optical coherence tomography,” J. Biomed. Opt. 23(11), 1 (2018).
[Crossref]

An, D.

P. Gong, D. Y. Yu, Q. Wang, P. K. Yu, K. Karnowski, M. Heisler, A. Francke, D. An, M. V. Sarunic, and D. D. Sampson, “Label-free volumetric imaging of conjunctival collecting lymphatics ex vivo by optical coherence tomography lymphangiography,” J. Biophotonics 11(8), e201800070 (2018).
[Crossref]

Armaiz-Pena, G. N.

G. N. Armaiz-Pena, S. K. Lutgendorf, S. W. Cole, and A. K. Sood, “Neuroendocrine modulation of cancer progression,” Brain, Behav., Immun. 23(1), 10–15 (2009).
[Crossref]

Assadi, H.

H. Assadi, V. Demidov, R. Karshafian, A. Douplik, and A. Vitkin, “Microvascular contrast enhancement in optical coherence tomography using microbubbles,” J. Biomed. Opt. 21(7), 076014 (2016).
[Crossref]

Ayala, G. E.

D. Albo, C. L. Akay, C. L. Marshall, J. A. Wilks, G. Verstovsek, H. Liu, N. Agarwal, D. H. Berger, and G. E. Ayala, “Neurogenesis in colorectal cancer is a marker of aggressive tumor behavior and poor outcomes,” Cancer 117(21), 4834–4845 (2011).
[Crossref]

Bartlett, L. A.

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med. 15(10), 1219–1223 (2009).
[Crossref]

Belzberg, A.

S. K. Thawait, V. Chaudhry, G. K. Thawait, K. C. Wang, A. Belzberg, J. A. Carrino, and A. Chhabra, “High-resolution MR neurography of diffuse peripheral nerve lesions,” Am. J. Neuroradiol. 32(8), 1365–1372 (2011).
[Crossref]

Berger, D. H.

D. Albo, C. L. Akay, C. L. Marshall, J. A. Wilks, G. Verstovsek, H. Liu, N. Agarwal, D. H. Berger, and G. E. Ayala, “Neurogenesis in colorectal cancer is a marker of aggressive tumor behavior and poor outcomes,” Cancer 117(21), 4834–4845 (2011).
[Crossref]

Biousse, V.

C. Lamirel, N. J. Newman, and V. Biousse, “Optical coherence tomography (OCT) in optic neuritis and multiple sclerosis,” Rev. Neurol. 166(12), 978–986 (2010).
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Birim, O.

O. Birim, A. P. Kappetein, T. Stijnen, and A. J. Bogers, “Meta-analysis of positron emission tomographic and computed tomographic imaging in detecting mediastinal lymph node metastases in nonsmall cell lung cancer,” Ann. Thorac. Surg. 79(1), 375–382 (2005).
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Bizheva, K.

Blanchard, D.

E. Sevick, R. Sharma, J. Rasmussen, M. Marshall, J. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. Blanchard, R. Fisher, S. B. Chiang, R. Elledge, and M. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study1,” Radiology 246(3), 734–741 (2008).
[Crossref]

Blas, K.

F. Y. Feng, Y. Qian, M. H. Stenmark, S. Halverson, K. Blas, S. Vance, H. M. Sandler, and D. A. Hamstra, “Perineural invasion predicts increased recurrence, metastasis, and death from prostate cancer following treatment with dose-escalated radiation therapy,” Int. J. Radiat. Oncol., Biol., Phys. 81(4), e361–e367 (2011).
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Bogers, A. J.

O. Birim, A. P. Kappetein, T. Stijnen, and A. J. Bogers, “Meta-analysis of positron emission tomographic and computed tomographic imaging in detecting mediastinal lymph node metastases in nonsmall cell lung cancer,” Ann. Thorac. Surg. 79(1), 375–382 (2005).
[Crossref]

Bonefas, E.

E. Sevick, R. Sharma, J. Rasmussen, M. Marshall, J. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. Blanchard, R. Fisher, S. B. Chiang, R. Elledge, and M. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study1,” Radiology 246(3), 734–741 (2008).
[Crossref]

Bosschaart, N.

M. Almasian, N. Bosschaart, T. G. van Leeuwen, and D. J. Faber, “Validation of quantitative attenuation and backscattering coefficient measurements by optical coherence tomography in the concentration- dependent and multiple scattering regime,” J. Biomed. Opt. 20(12), 121314 (2015).
[Crossref]

Bouma, B. E.

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med. 15(10), 1219–1223 (2009).
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Bouvet, M.

K. Hayashi, P. Jiang, K. Yamauchi, N. Yamamoto, H. Tsuchiya, K. Tomita, A. R. Moossa, M. Bouvet, and R. M. Hoffman, “Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels,” Cancer Res. 67(17), 8223–8228 (2007).
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Braeuer, B.

J. Hope, B. Braeuer, S. Amirapu, A. McDaid, and F. Vanholsbeeck, “Extracting morphometric information from rat sciatic nerve using optical coherence tomography,” J. Biomed. Opt. 23(11), 1 (2018).
[Crossref]

Brennan, M.

M. Jhawer, D. Coit, M. Brennan, L. X. Qin, M. Gonen, D. Klimstra, L. Tang, D. P. Kelsen, and M. A. Shah, “Perineural invasion after preoperative chemotherapy predicts poor survival in patients with locally advanced gastric cancer: gene expression analysis with pathologic validation,” Am. J. Clin. Oncol. 32(4), 356–362 (2009).
[Crossref]

Brushart, T. M.

G. A. Dumanian, M. A. McClinton, and T. M. Brushart, “The effects of free fat grafts on the stiffness of the rat sciatic nerve and perineural scar,” J. Hand Surg. 24(1), 30–36 (1999).
[Crossref]

Cable, A.

Carrino, J. A.

S. K. Thawait, V. Chaudhry, G. K. Thawait, K. C. Wang, A. Belzberg, J. A. Carrino, and A. Chhabra, “High-resolution MR neurography of diffuse peripheral nerve lesions,” Am. J. Neuroradiol. 32(8), 1365–1372 (2011).
[Crossref]

Chang, S.

D. P. Popescu, L. P. Choo-Smith, C. Flueraru, Y. Mao, S. Chang, J. Disano, S. Sherif, and M. G. Sowa, “Optical coherence tomography: fundamental principles, instrumental designs and biomedical applications,” Biophys. Rev. 3(3), 155–169 (2011).
[Crossref]

Y. Mao, C. Flueraru, S. Chang, D. Popescu, and M. Sowa, “High-quality tissue imaging using a catheter-based swept-source optical coherence tomography systems with an integrated semiconductor optical amplifier,” IEEE Trans. Instrum. Meas. 60(10), 3376–3383 (2011).
[Crossref]

Y. Mao, S. Sherif, C. Flueraru, and S. Chang, “3×3 Mach-Zehnder interferometer with unbalanced differential detection for full-range swept-source optical coherence tomography,” Appl. Opt. 47(12), 2004–2010 (2008).
[Crossref]

Chaudhry, V.

S. K. Thawait, V. Chaudhry, G. K. Thawait, K. C. Wang, A. Belzberg, J. A. Carrino, and A. Chhabra, “High-resolution MR neurography of diffuse peripheral nerve lesions,” Am. J. Neuroradiol. 32(8), 1365–1372 (2011).
[Crossref]

Chen, Q.

M. E. Miller, B. Palla, Q. Chen, D. A. Elashoff, E. Abemayor, J. M. St. John, and C. K. Lai, “A novel classification system for perineural invasion in noncutaneous head and neck squamous cell carcinoma: histologic subcategories and patient outcomes,” Am. J. Otolaryngol. 33(2), 212–215 (2012).
[Crossref]

Chen, Z.

C. A. Chlebicki, A. D. Lee, W. Jung, H. Li, L. H. Liaw, Z. Chen, and B. J. Wong, “Preliminary investigation on use of high-resolution optical coherence tomography to monitor injury and repair in the rat sciatic nerve,” Lasers Surg. Med. 42(4), 306–312 (2010).
[Crossref]

Chhabra, A.

S. K. Thawait, V. Chaudhry, G. K. Thawait, K. C. Wang, A. Belzberg, J. A. Carrino, and A. Chhabra, “High-resolution MR neurography of diffuse peripheral nerve lesions,” Am. J. Neuroradiol. 32(8), 1365–1372 (2011).
[Crossref]

Chiang, S. B.

E. Sevick, R. Sharma, J. Rasmussen, M. Marshall, J. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. Blanchard, R. Fisher, S. B. Chiang, R. Elledge, and M. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study1,” Radiology 246(3), 734–741 (2008).
[Crossref]

Chlebicki, C. A.

C. A. Chlebicki, A. D. Lee, W. Jung, H. Li, L. H. Liaw, Z. Chen, and B. J. Wong, “Preliminary investigation on use of high-resolution optical coherence tomography to monitor injury and repair in the rat sciatic nerve,” Lasers Surg. Med. 42(4), 306–312 (2010).
[Crossref]

Choo-Smith, L. P.

D. P. Popescu, L. P. Choo-Smith, C. Flueraru, Y. Mao, S. Chang, J. Disano, S. Sherif, and M. G. Sowa, “Optical coherence tomography: fundamental principles, instrumental designs and biomedical applications,” Biophys. Rev. 3(3), 155–169 (2011).
[Crossref]

Coit, D.

M. Jhawer, D. Coit, M. Brennan, L. X. Qin, M. Gonen, D. Klimstra, L. Tang, D. P. Kelsen, and M. A. Shah, “Perineural invasion after preoperative chemotherapy predicts poor survival in patients with locally advanced gastric cancer: gene expression analysis with pathologic validation,” Am. J. Clin. Oncol. 32(4), 356–362 (2009).
[Crossref]

Cole, S. W.

G. N. Armaiz-Pena, S. K. Lutgendorf, S. W. Cole, and A. K. Sood, “Neuroendocrine modulation of cancer progression,” Brain, Behav., Immun. 23(1), 10–15 (2009).
[Crossref]

Dai, Y.

Q. Lu, J. Hua, M. M. Kassir, Z. Delproposto, Y. Dai, J. Sun, M. Haacke, and J. Hu, “Imaging lymphatic system in breast cancer patients with magnetic resonance lymphangiography,” PLoS One 8(7), e69701 (2013).
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de Boer, J. F.

F. P. Henry, Y. Wang, C. Rodriguez, M. A. Randolph, E. Rust, J. M. Winograd, J. F. de Boer, and B. H. Park, “In vivo optical microscopy of peripheral nerve myelination with polarization sensitive-optical coherence tomography,” J. Biomed. Opt. 20(4), 046002 (2015).
[Crossref]

Deleon-Ortega, J.

L. M. Sakata, J. Deleon-Ortega, V. Sakata, and C. A. Girkin, “Optical coherence tomography of the retina and optic nerve - a review,” Clin. Experiment. Ophthalmol. 37(1), 90–99 (2009).
[Crossref]

Delproposto, Z.

Q. Lu, J. Hua, M. M. Kassir, Z. Delproposto, Y. Dai, J. Sun, M. Haacke, and J. Hu, “Imaging lymphatic system in breast cancer patients with magnetic resonance lymphangiography,” PLoS One 8(7), e69701 (2013).
[Crossref]

Demidov, V.

V. Demidov, X. Zhao, O. Demidova, H. Y. M. Pang, C. Flueraru, F. F. Liu, and I. A. Vitkin, “Preclinical quantitative in-vivo assessment of skin tissue vascularity in radiation induced fibrosis with optical coherence tomography,” J. Biomed. Opt. 23(10), 1 (2018).
[Crossref]

V. Demidov, O. Demidova, A. Shabunin, and A. Vitkin, “Alternative contrast mechanism in optical coherence tomography: temporal speckle synchronization effects,” Modern Tech. Med. 10(1), 39–48 (2018).
[Crossref]

V. Demidov, A. Maeda, M. Sugita, V. Madge, S. Sadanand, C. Flueraru, and I. A. Vitkin, “Preclinical longitudinal imaging of tumor microvascular radiobiological response with functional optical coherence tomography,” Sci. Rep. 8(1), 38 (2018).
[Crossref]

H. Assadi, V. Demidov, R. Karshafian, A. Douplik, and A. Vitkin, “Microvascular contrast enhancement in optical coherence tomography using microbubbles,” J. Biomed. Opt. 21(7), 076014 (2016).
[Crossref]

L. A. Matveev, V. Y. Zaitsev, G. V. Gelikonov, A. L. Matveyev, A. A. Moiseev, S. Y. Ksenofontov, V. M. Gelikonov, M. A. Sirotkina, N. D. Gladkova, V. Demidov, and A. Vitkin, “Hybrid M-mode-like OCT imaging of three-dimensional microvasculature in vivo using reference-free processing of complex valued B-scans,” Opt. Lett. 40(7), 1472–1475 (2015).
[Crossref]

Demidova, O.

V. Demidov, O. Demidova, A. Shabunin, and A. Vitkin, “Alternative contrast mechanism in optical coherence tomography: temporal speckle synchronization effects,” Modern Tech. Med. 10(1), 39–48 (2018).
[Crossref]

V. Demidov, X. Zhao, O. Demidova, H. Y. M. Pang, C. Flueraru, F. F. Liu, and I. A. Vitkin, “Preclinical quantitative in-vivo assessment of skin tissue vascularity in radiation induced fibrosis with optical coherence tomography,” J. Biomed. Opt. 23(10), 1 (2018).
[Crossref]

Disano, J.

D. P. Popescu, L. P. Choo-Smith, C. Flueraru, Y. Mao, S. Chang, J. Disano, S. Sherif, and M. G. Sowa, “Optical coherence tomography: fundamental principles, instrumental designs and biomedical applications,” Biophys. Rev. 3(3), 155–169 (2011).
[Crossref]

Douplik, A.

H. Assadi, V. Demidov, R. Karshafian, A. Douplik, and A. Vitkin, “Microvascular contrast enhancement in optical coherence tomography using microbubbles,” J. Biomed. Opt. 21(7), 076014 (2016).
[Crossref]

Dumanian, G. A.

G. A. Dumanian, M. A. McClinton, and T. M. Brushart, “The effects of free fat grafts on the stiffness of the rat sciatic nerve and perineural scar,” J. Hand Surg. 24(1), 30–36 (1999).
[Crossref]

Elashoff, D. A.

M. E. Miller, B. Palla, Q. Chen, D. A. Elashoff, E. Abemayor, J. M. St. John, and C. K. Lai, “A novel classification system for perineural invasion in noncutaneous head and neck squamous cell carcinoma: histologic subcategories and patient outcomes,” Am. J. Otolaryngol. 33(2), 212–215 (2012).
[Crossref]

Elledge, R.

E. Sevick, R. Sharma, J. Rasmussen, M. Marshall, J. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. Blanchard, R. Fisher, S. B. Chiang, R. Elledge, and M. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study1,” Radiology 246(3), 734–741 (2008).
[Crossref]

Entschladen, F.

F. Entschladen, D. Palm, B. Niggemann, and K. S. Zaenker, “The cancer's nervous tooth: considering the neuronal crosstalk within tumors,” Semin. Cancer Biol. 18(3), 171–175 (2008).
[Crossref]

Es’haghian, S.

Faber, D. J.

M. Almasian, T. G. van Leeuwen, and D. J. Faber, “OCT amplitude and speckle statistics of discrete random media,” Sci. Rep. 7(1), 14873–11 (2017).
[Crossref]

M. Almasian, N. Bosschaart, T. G. van Leeuwen, and D. J. Faber, “Validation of quantitative attenuation and backscattering coefficient measurements by optical coherence tomography in the concentration- dependent and multiple scattering regime,” J. Biomed. Opt. 20(12), 121314 (2015).
[Crossref]

Feng, F. Y.

F. Y. Feng, Y. Qian, M. H. Stenmark, S. Halverson, K. Blas, S. Vance, H. M. Sandler, and D. A. Hamstra, “Perineural invasion predicts increased recurrence, metastasis, and death from prostate cancer following treatment with dose-escalated radiation therapy,” Int. J. Radiat. Oncol., Biol., Phys. 81(4), e361–e367 (2011).
[Crossref]

Filler, A.

A. Filler, “MR neurography and diffusion tensor imaging: origins, history & clinical impact,” Neurosurgery 65(suppl_4), A29–A43 (2009).
[Crossref]

Fisher, R.

E. Sevick, R. Sharma, J. Rasmussen, M. Marshall, J. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. Blanchard, R. Fisher, S. B. Chiang, R. Elledge, and M. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study1,” Radiology 246(3), 734–741 (2008).
[Crossref]

Flueraru, C.

V. Demidov, X. Zhao, O. Demidova, H. Y. M. Pang, C. Flueraru, F. F. Liu, and I. A. Vitkin, “Preclinical quantitative in-vivo assessment of skin tissue vascularity in radiation induced fibrosis with optical coherence tomography,” J. Biomed. Opt. 23(10), 1 (2018).
[Crossref]

V. Demidov, A. Maeda, M. Sugita, V. Madge, S. Sadanand, C. Flueraru, and I. A. Vitkin, “Preclinical longitudinal imaging of tumor microvascular radiobiological response with functional optical coherence tomography,” Sci. Rep. 8(1), 38 (2018).
[Crossref]

D. P. Popescu, L. P. Choo-Smith, C. Flueraru, Y. Mao, S. Chang, J. Disano, S. Sherif, and M. G. Sowa, “Optical coherence tomography: fundamental principles, instrumental designs and biomedical applications,” Biophys. Rev. 3(3), 155–169 (2011).
[Crossref]

Y. Mao, C. Flueraru, S. Chang, D. Popescu, and M. Sowa, “High-quality tissue imaging using a catheter-based swept-source optical coherence tomography systems with an integrated semiconductor optical amplifier,” IEEE Trans. Instrum. Meas. 60(10), 3376–3383 (2011).
[Crossref]

Y. Mao, S. Sherif, C. Flueraru, and S. Chang, “3×3 Mach-Zehnder interferometer with unbalanced differential detection for full-range swept-source optical coherence tomography,” Appl. Opt. 47(12), 2004–2010 (2008).
[Crossref]

Fox, S. B.

S. A. Stacker, S. P. Williams, T. Karnezis, R. Shayan, S. B. Fox, and M. G. Achen, “Lymphangiogenesis and lymphatic vessel remodelling in cancer,” Nat. Rev. Cancer 14(3), 159–172 (2014).
[Crossref]

Francke, A.

P. Gong, D. Y. Yu, Q. Wang, P. K. Yu, K. Karnowski, M. Heisler, A. Francke, D. An, M. V. Sarunic, and D. D. Sampson, “Label-free volumetric imaging of conjunctival collecting lymphatics ex vivo by optical coherence tomography lymphangiography,” J. Biophotonics 11(8), e201800070 (2018).
[Crossref]

Fujisawa, T.

K. Yasufuku, T. Nakajima, K. Motoori, Y. Sekine, K. Shibuya, K. Hiroshima, and T. Fujisawa, “Comparison of endobronchial ultrasound, positron emission tomography, and CT for lymph node staging of lung cancer,” Chest 130(3), 710–718 (2006).
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Fukumura, D.

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med. 15(10), 1219–1223 (2009).
[Crossref]

N. Isaka, T. P. Padera, J. Hagendoorn, D. Fukumura, and R. K. Jain, “Peritumor lymphatics induced by Vascular Endothelial Growth Factor-C exhibit abnormal function,” Cancer Res. 64(13), 4400–4404 (2004).
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Gao, D.

S. Li, Y. Sun, and D. Gao, “Role of the nervous system in cancer metastasis,” Oncol. Lett. 5(4), 1101–1111 (2013).
[Crossref]

Gelikonov, G. V.

A. L. Matveyev, L. A. Matveev, A. A. Moiseev, A. A. Sovetsky, G. V. Gelikonov, and V. Y. Zaitsev, “Semi-analytical full-wave model for simulations of scans in optical coherence tomography with accounting for beam focusing and the motion of scatterers,” Laser Phys. Lett. 16(8), 085601 (2019).
[Crossref]

L. A. Matveev, V. Y. Zaitsev, G. V. Gelikonov, A. L. Matveyev, A. A. Moiseev, S. Y. Ksenofontov, V. M. Gelikonov, M. A. Sirotkina, N. D. Gladkova, V. Demidov, and A. Vitkin, “Hybrid M-mode-like OCT imaging of three-dimensional microvasculature in vivo using reference-free processing of complex valued B-scans,” Opt. Lett. 40(7), 1472–1475 (2015).
[Crossref]

V. Y. Zaitsev, L. A. Matveev, A. L. Matveyev, G. V. Gelikonov, and V. M. Gelikonov, “A model for simulating speckle-pattern evolution based on close to reality procedures used in spectral-domain OCT,” Laser Phys. Lett. 11(10), 105601 (2014).
[Crossref]

Gelikonov, V. M.

Girkin, C. A.

L. M. Sakata, J. Deleon-Ortega, V. Sakata, and C. A. Girkin, “Optical coherence tomography of the retina and optic nerve - a review,” Clin. Experiment. Ophthalmol. 37(1), 90–99 (2009).
[Crossref]

Gladkova, N. D.

Gonen, M.

M. Jhawer, D. Coit, M. Brennan, L. X. Qin, M. Gonen, D. Klimstra, L. Tang, D. P. Kelsen, and M. A. Shah, “Perineural invasion after preoperative chemotherapy predicts poor survival in patients with locally advanced gastric cancer: gene expression analysis with pathologic validation,” Am. J. Clin. Oncol. 32(4), 356–362 (2009).
[Crossref]

Gong, P.

P. Gong, D. Y. Yu, Q. Wang, P. K. Yu, K. Karnowski, M. Heisler, A. Francke, D. An, M. V. Sarunic, and D. D. Sampson, “Label-free volumetric imaging of conjunctival collecting lymphatics ex vivo by optical coherence tomography lymphangiography,” J. Biophotonics 11(8), e201800070 (2018).
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Y. Mao, C. Flueraru, S. Chang, D. Popescu, and M. Sowa, “High-quality tissue imaging using a catheter-based swept-source optical coherence tomography systems with an integrated semiconductor optical amplifier,” IEEE Trans. Instrum. Meas. 60(10), 3376–3383 (2011).
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P. Gong, S. Es’haghian, K. A. Harms, A. Murray, S. Rea, F. M. Wood, D. D. Sampson, and R. A. McLaughlin, “In vivo label-free lymphangiography of cutaneous lymphatic vessels in human burn scars using optical coherence tomography,” Biomed. Opt. Express 7(12), 4886–4898 (2016).
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F. Y. Feng, Y. Qian, M. H. Stenmark, S. Halverson, K. Blas, S. Vance, H. M. Sandler, and D. A. Hamstra, “Perineural invasion predicts increased recurrence, metastasis, and death from prostate cancer following treatment with dose-escalated radiation therapy,” Int. J. Radiat. Oncol., Biol., Phys. 81(4), e361–e367 (2011).
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Figures (5)

Fig. 1.
Fig. 1. Schematic diagram of the swept-source OCT system setup with quadrature Mach-Zehnder fiber-based interferometer and optical amplification: SOA - semiconductor optical amplifier, PC - polarization controller, A - fiber attenuator, DB - dual balanced photo-detector, DAQ - data acquisition card, C - collimator, MZ Interferometer - Mach-Zehnder interferometer, M - mirror. SGx and SGy - scanning mirrors driven by galvanometers in x and y lateral dimensions, CR - circulator, L - lens. Red lines represent optical paths, blue lines are electrical signals.
Fig. 2.
Fig. 2. Speckle statistical data analysis of OCT images. (a) White-light photo of a mouse with installed dorsal skin window chamber; (b) The photo of the chamber with grown pancreatic adenocarcinoma tumor. Blue line indicates the location of (c) the structural OCT image. ROI1 – deep location (noise area), ROI2 - solid tumor tissue, ROI3 - lymphatic vessel lumen; (d) Speckle statistics for OCT signal noise: left and right are statistics for detection channels |Q1| and |Q2| used to form full complex signal S. DB – dual balanced photo-detector (for details see Fig. 1); (e) Speckle statistics of the noise speckle amplitudes A in ROI1, well described by the Rayleigh distribution (R2 = 0.9996); (f) Speckle statistics of the signal-rich tumor tissue in ROI2, displaying a poorer Rayleigh fit (R2 = 0.82); (g) Speckle statistics of the lymphatic vessel lumen in ROI3, showing closer-to-noise goodness of fit (R2 = 0.98). Red curves correspond to Gaussian fit for (d), and Rayleigh fit for (e), (f) and (g).
Fig. 3.
Fig. 3. Simultaneous mapping of low-scattering tissues by spatial speckle filtering and of blood vessels by temporal speckle variance methods. (a) The white light photo of a pancreatic adenocarcinoma tumor grown in a window chamber model; (b) N = 24 OCT B-scans from the same lateral location within the scanned volume. Scale bar is 0.3 mm; (c) Nerves and lymphatic vessels mapping. Step 1: Speckle amplitudes from each voxel are plotted as a histogram and fitted with Rayleigh distribution function to find the R2 value. Step 2: 0.95 < R2<0.99 thresholding is applied to the entire imaged volume to map nerves and lymphatic vessels (shown in the same B-scan as in (b), and in a lateral-view average intensity projection (AIP) below it). Nerves appear as oval ring-shaped structures. LV-lymphatic vessel; (d) Blood vessels mapping using conventional speckle variance algorithm (shown in the same B-scan as in (b) and in average intensity projection (AIP) below it). BV – blood vessel; (e) Combined 3D volumes of lymphatic/blood vessels and nerves, presented in a lateral-view average intensity projection form.
Fig. 4.
Fig. 4. Mouse dorsal skin angiography, lymphangiography/neurography, and histology. (a) White-light photo of dorsal skin in window chamber, field of view = 6 × 6 mm2. (b) Depth-encoded blood microvasculature map of (a). (c) Grey-scale average R2– thresholded projection for low-scattering regions in (a). Dashed-line white (A) and yellow (B) rectangular areas are expanded in (d) for blood microvasculature, and (e) for lymphatic vessels and nerves, some of which are labeled with arrows, the former as cyan and the latter as purple. (f) OCT B-scan with histological stains in (g), (h) and (i) from approximately same location in tissue. (g) Overall tissue architecture and cellular morphology are visualized with Hematoxylin and Eosin (H&E) staining; (h) Nerves are distinguished from surrounding connective tissues with Masson’s Trichrome (MT) staining; (f) Lymphatic vessels are visualized with lymphatic vessel endothelial hyaluronan receptor 1 (LYVE-1). Tissue layers are labelled in the bottom row images as Fs – fascia, M- muscle, F – fat, D – dermis, E – epidermis. Nerves are labeled with purple arrows, lymphatic vessels – with cyan arrows. Scale bars in top row panels are 1 mm; in bottom row are 0.1 mm.
Fig. 5.
Fig. 5. Angiography, lymphangiography/neurography and histology of pancreatic adenocarcinoma grown in a mouse dorsal skin window chamber. (a) White-light photo of dorsal skin in window chamber, field of view – 6 × 6 mm2; (b) Depth-encoded blood microvasculature map of (a); (c) Grey-scale average R2– thresholded projection for low-scattering regions in (a). Dashed-line white (A) and yellow (B) rectangular areas are expanded in (d) for blood microvasculature, and (e) for lymphatic vessels and nerves, some of which are labeled with arrows, the former as cyan and the latter as purple. Scale bars in (a), (b) and (c) are 1 mm; (f) OCT B-scan with corresponding Hematoxylin and Eosin (H&E) staining in (g) from approximately same location in tissue. Black dash-lined rectangular areas are enlarged in (g) and (h); (h) Nerves are distinguished from surrounding connective tissues with Masson’s Trichrome (MT) staining; (i) Peri-tumoral lymphatic vessels are visualized with lymphatic vessel endothelial hyaluronan receptor 1 (LYVE-1). Nerves are labeled with purple arrows, lymphatic vessels – with cyan arrows. (j) LYVE-1 staining of the tumor core tissue (location labeled with green line in (c)), identifying two newly formed lymphatic vessels with thinner walls. Scale bars in (h), (i) and (j) are 0.1 mm.

Equations (3)

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S ( n ) = Q 1 ( n ) + i Q 2 ( n ) ,
A = | F T 1 [ S ] | ,
P ( x ; a , b , c ) = a ( x c ) b 2 e ( x c ) 2 2 b 2 ,

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