Noninvasive in vivo structural and vascular imaging of human oral tissues with spectral domain optical coherence tomography

Bahar Davoudi, Andras Lindenmaier, Beau A Standish, Ghassan Allo, Kostadinka Bizheva, Alex Vitkin, Bahar Davoudi, Andras Lindenmaier, Beau A Standish, Ghassan Allo, Kostadinka Bizheva, Alex Vitkin

Abstract

A spectral domain optical coherence tomography (SD-OCT) system and an oral imaging probe have been developed to visualize the microstructural morphology and microvasculature in the human oral cavity. Structural OCT images of ex vivo pig oral tissues with the histology of the same sites were acquired and compared for correlations. Structural in vivo OCT images of healthy human tissue as well as a pathologic site (ulcer) were obtained and analyzed based on the results of the ex vivo pig study, drawing on the similarity between human and swine oral tissues. In vivo Doppler and speckle variance OCT images of the oral cavity in human volunteers were also acquired, to demonstrate the feasibility of microvascular imaging of healthy and pathologic (scar) oral tissue.

Keywords: (110.4500) Optical coherence tomography; (170.1610) Clinical applications; (170.2655) Functional monitoring and imaging; (170.3880) Medical and biological imaging; (170.4500) Optical coherence tomography; (170.4580) Optical diagnostics for medicine.

Figures

Fig. 1
Fig. 1
(a) Schematic of the SD-OCT system. M: mirror, L: lens, DC: dispersion compensation unit, PC: polarization controllers, DG: diffraction grating, C: circulators (b) Stage for human oral imaging, comprised of the custom-made probe and a head frame. For clarity, the fibers attached to the input (80/20) and output (50/50) couplers are shown in two different colors.
Fig. 2
Fig. 2
(a) Comparison of the light source spectrum at the input to the OCT system (solid line) and at the output of the sample arm (dashed line). The very similar shape and bandwidth signifies that the optics in the OCT system have not caused a spectral distortion (narrowing) and thus a potential reduction of the axial resolution of the system. (b) Decrease in system SNR (proportional to power at the sample arm) as a function of depth, implying a ~13 dB reduction in SNR when going from a depth of ~200 μm to ~1200 μm. The graph is a continuous representation of 22 point measurements.
Fig. 3
Fig. 3
Ex vivo images of pig oral tissue, (a) OCT image and (b) H&E histology of labial tissue; (c) OCT image and (d) H&E histology of buccal tissue; (e) OCT image and (f) H&E histology of dorsal tongue; (g) OCT image and (h) H&E histology of ventral tongue. SL: superficial layer, IL: intermediate layer, BL: basal layer, LP: lamina proria, SM: submucosa, F: fat, M: muscle, BV: blood vessel, *: taste bud. Scale bar = 500 μm.
Fig. 4
Fig. 4
In vivo OCT images of human oral tissue, (a) labial; (b) dorsal surface of the tongue; (c) lateral surface of the tongue; (d) ventral surface of the tongue; (e) buccal; (f) soft palate. SL: superficial layer, IL: intermediate layer, EL: epithelial layer, BL: basal layer, LP: lamina proria, BV: blood vessel, FP: filiform lingual papillae, FoP: foliate lingual papillae, CF: circular furrow, SM: submucosa. Scale bar = 500 μm
Fig. 5
Fig. 5
In vivo OCT images of human labial tissue in (a) absence and (b) presence of ulcer. SL: superficial layer, IL: intermediate layer, BL: basal layer, LP: lamina proria, U: ulcer. Scale bar = 500 μm
Fig. 6
Fig. 6
Consecutive Doppler images and Doppler OCT multimedia of the microvessels in the human labial tissue. The color bar represents the velocity of scatterers in the axial direction. Blue and red hues correspond to two opposite blood flow directions. Microvasculature as small as 16 μm is detectable using the SD-OCT system. Scale bar = 500 μm. Lateral field of view in the multimedia: 1 mm by 1 mm (Media 1)
Fig. 7
Fig. 7
Speckle variance OCT images of the vasculature map in three different regions of the labial tissue of a healthy human volunteer. The images are en face intensity displays formed by projecting three-dimensional tomograms along the depth. The arrows in (a) and (c) show the smallest capillaries detected by the system (~30 μm). Scale bar = 200μm.
Fig. 8
Fig. 8
Speckle variance OCT images in (a) healthy region of the labial tissue, and (b) scar in the labial tissue of the same volunteer. Note the increase in the number of microvasculature in (b); for quantification, see text. Scale bar = 200μm.

References

    1. W. Drexler and J. G. Fujimoto, Optical Coherence Tomography: Technology and Applications (Springer, 2008).
    1. Bizheva K., Hutchings N., Sorbara L., Moayed A. A., Simpson T., “In vivo volumetric imaging of the human corneo-scleral limbus with spectral domain OCT,” Biomed. Opt. Express 2(7), 1794–02 (2011).10.1364/BOE.2.001794
    1. Yang V. X. D., Tang S.-j., Gordon M. L., Qi B., Gardiner G., Cirocco M., Kortan P., Haber G. B., Kandel G., Vitkin I. A., Wilson B. C., Marcon N. E., “Endoscopic Doppler optical coherence tomography in the human GI tract: initial experience,” Gastrointest. Endosc. 61(7), 879–890 (2005).10.1016/S0016-5107(05)00323-8
    1. Atif M., Ullah H., Hamza M. Y., Ikram M., “Catheters for optical coherence tomography,” Laser Phys. Lett. 8, 629–646 (2011).
    1. Yoo H., Kim J. W., Shishkov M., Namati E., Morse T., Shubochkin R., McCarthy J. R., Ntziachristos V., Bouma B. E., Jaffer F. A., Tearney G. J., “Intra-arterial catheter for simultaneous microstructural and molecular imaging in vivo,” Nat. Med. 17(12), 1680–1684 (2011).10.1038/nm.2555
    1. Lee C.-K., Tsai M.-T., Lee H.-C., Chen H.-M., Chiang C.-P., Wang Y.-M., Yang C. C., “Diagnosis of oral submucous fibrosis with optical coherence tomography,” J. Biomed. Opt. 14(5), 054008 (2009).10.1117/1.3233653
    1. Wilder-Smith P., Hammer-Wilson M. J., Zhang J., Wang Q., Osann K., Chen Z., Wigdor H., Schwartz J., Epstein J., “In vivo imaging of oral mucositis in an animal model using optical coherence tomography and optical Doppler tomography,” Clin. Cancer Res. 13(8), 2449–2454 (2007).10.1158/1078-0432.CCR-06-2234
    1. Gladkova N., Maslennikova A., Balalaeva I., Feldchtein F., Kiseleva E., Karabut M., Iksanov R., “Application of optical coherence tomography in the diagnosis of mucositis in patients with head and neck cancer during a course of radio(chemo)therapy,” Med. Laser Appl. 23(4), 186–195 (2008).10.1016/j.mla.2008.07.008
    1. Muanza T. M., Cotrim A. P., McAuliffe M., Sowers A. L., Baum B. J., Cook J. A., Feldchtein F., Amazeen P., Coleman C. N., Mitchell J. B., “Evaluation of radiation-induced oral mucositis by optical coherence tomography,” Clin. Cancer Res. 11(14), 5121–5127 (2005).10.1158/1078-0432.CCR-05-0403
    1. Wilder-Smith P., Jung W. G., Brenner M., Osann K., Beydoun H., Messadi D., Chen Z., “In vivo optical coherence tomography for the diagnosis of oral malignancy,” Lasers Surg. Med. 35(4), 269–275 (2004).10.1002/lsm.20098
    1. Ridgway J. M., Armstrong W. B., Guo S., Mahmood U., Su J., Jackson R. P., Shibuya T., Crumley R. L., Gu M., Chen Z., Wong B. J., “In vivo optical coherence tomography of the human oral cavity and oropharynx,” Arch. Otolaryngol. Head Neck Surg. 132(10), 1074–1081 (2006).10.1001/archotol.132.10.1074
    1. Matheny E. S., Hanna N. M., Jung W. G., Chen Z., Wilder-Smith P., Mina-Araghi R., Brenner M., “Optical coherence tomography of malignancy in hamster cheek pouches,” J. Biomed. Opt. 9(5), 978–981 (2004).10.1117/1.1783897
    1. Jerjes W., Upile T., Conn B., Hamdoon Z., Betz C. S., McKenzie G., Radhi H., Vourvachis M., El Maaytah M., Sandison A., Jay A., Hopper C., “In vitro examination of suspicious oral lesions using optical coherence tomography,” Br. J. Oral Maxillofac. Surg. 48(1), 18–25 (2010).10.1016/j.bjoms.2009.04.019
    1. Tsai M. T., Lee H.-C., Lee C.-K., Yu C. H., Chen H. M., Chiang C.-P., Chang C.-C., Wang Y.-M., Yang C. C., “Effective indicators for diagnosis of oral cancer using optical coherence tomography,” Opt. Express 16(20), 15847–15862 (2008).10.1364/OE.16.015847
    1. Tsai M.-T., Lee C.-K., Lee H.-C., Chen H.-M., Chiang C.-P., Wang Y.-M., Yang C.-C., “Differentiating oral lesions in different carcinogenesis stages with optical coherence tomography,” J. Biomed. Opt. 14(4), 044028 (2009).10.1117/1.3200936
    1. Ozawa N., Sumi Y., Chong C., Kurabayashi T., “Evaluation of oral vascular anomalies using optical coherence tomography,” Br. J. Oral Maxillofac. Surg. 47(8), 622–626 (2009).10.1016/j.bjoms.2009.03.012
    1. Yang V., Gordon M., Qi B., Pekar J., Lo S., Seng-Yue E., Mok A., Wilson B., Vitkin I., “High speed, wide velocity dynamic range Doppler optical coherence tomography (Part I): System design, signal processing, and performance,” Opt. Express 11(7), 794–809 (2003).10.1364/OE.11.000794
    1. Mariampillai A., Leung M. K. K., Jarvi M., Standish B. A., Lee K., Wilson B. C., Vitkin A., Yang V. X. D., “Optimized speckle variance OCT imaging of microvasculature,” Opt. Lett. 35(8), 1257–1259 (2010).10.1364/OL.35.001257
    1. Hanna N. M., Waite W., Taylor K., Jung W.-G., Mukai D., Matheny E., Kreuter K., Wilder-Smith P., Brenner M., Chen Z., “Feasibility of three-dimensional optical coherence tomography and optical Doppler tomography of malignancy in hamster cheek pouches,” Photomed. Laser Surg. 24(3), 402–409 (2006).10.1089/pho.2006.24.402
    1. Sudheendran N., Syed S. H., Dickinson M. E., Larina I. V., Larin K. V., “Speckle variance OCT imaging of the vasculature in live mammalian embryos,” Laser Phys. Lett. 8(3), 247–252 (2011).10.1002/lapl.201010120
    1. Wong J. W., Gallant-Behm C., Wiebe C., Mak K., Hart D. A., Larjava H., Häkkinen L., “Wound healing in oral mucosa results in reduced scar formation as compared with skin: evidence from the red Duroc pig model and humans,” Wound Repair Regen. 17(5), 717–729 (2009).10.1111/j.1524-475X.2009.00531.x
    1. Wojtkowski M., Srinivasan V., Ko T., Fujimoto J., Kowalczyk A., Duker J., “Ultrahigh-resolution, high-speed, Fourier domain optical coherence tomography and methods for dispersion compensation,” Opt. Express 12(11), 2404–2422 (2004).10.1364/OPEX.12.002404
    1. Mariampillai A., Standish B. A., Moriyama E. H., Khurana M., Munce N. R., Leung M. K. K., Jiang J., Cable A., Wilson B. C., Vitkin I. A., Yang V. X. D., “Speckle variance detection of microvasculature using swept-source optical coherence tomography,” Opt. Lett. 33(13), 1530–1532 (2008).10.1364/OL.33.001530
    1. Hsiung P.-L., Nambiar P. R., Fujimoto J. G., “Effect of tissue preservation on imaging using ultrahigh resolution optical coherence tomography,” J. Biomed. Opt. 10(6), 064033 (2005).10.1117/1.2147155
    1. M. Bath-Balogh and M. J. Fehrenbach, Illustrated Dental Embryology, Histology, and Anatomy (Elsevier Saunders, 2011).
    1. J. W. Eveson and C. Scully, Color Atlas of Oral Pathology (Mosby-Wolfe, 1995).
    1. Standish B. A., Jin X., Smolen J., Mariampillai A., Munce N. R., Wilson B. C., Vitkin I. A., Yang V. X. D., “Interstitial Doppler optical coherence tomography monitors microvascular changes during photodynamic therapy in a Dunning prostate model under varying treatment conditions,” J. Biomed. Opt. 12(3), 034022 (2007).10.1117/1.2744068
    1. Spence R. A. J., “The venous anatomy of the lower oesophagus in normal subjects and in patients with varices: an image analysis study,” Br. J. Surg. 71(10), 739–744 (1984).10.1002/bjs.1800711002
    1. Sciubba J. J., Goldenberg D., “Oral complications of radiotherapy,” Lancet Oncol. 7(2), 175–183 (2006).10.1016/S1470-2045(06)70580-0
    1. Ozawa N., Sumi Y., Shimozato K., Chong C., Kurabayashi T., “In vivo imaging of human labial glands using advanced optical coherence tomography,” Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 108(3), 425–429 (2009).10.1016/j.tripleo.2009.05.035

Source: PubMed

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