Abstract

Ciliary activity, characterized by the coordinated beating of ciliary cells, generates the primary driving force for oviduct tubal transport, which is an essential physiological process for successful pregnancies. Malfunction of the cilium in the fallopian tube, or oviduct, may increase the risk of infertility and tubal pregnancy that can result in maternal death. While many ex-vivo studies have been carried out using bright field microscopy, this technique is not feasible for the in-vivo investigation of oviduct ciliary beating frequency (CBF). Optical coherence tomography (OCT) has been able to provide in-vivo CBF imaging in a mouse model, but its resolution may be insufficient to resolve the spatial and temporal features of the cilium. Our group has recently developed the phase resolved Doppler (PRD) OCT method to visualize ciliary strokes at ultra-high displacement sensitivity. However, the cross-sectional field of view (FOV) may not be ideal for visualizing the surface dynamics of ciliated tissue. In this study, we report on the development of phase resolved Doppler spectrally encoded interferometric microscopy (PRD-SEIM) to visualize the oviduct ciliary activity within an en face FOV. This novel real time imaging system offers micrometer spatial resolution, sub-nanometer displacement sensitivity, and the potential for in-vivo endoscopic adaptation. The feasibility of the approach has been validated through ex-vivo experiments where the porcine oviduct CBF has been measured across different temperature conditions and the application of a drug. CBF ranging from 8 to 12 Hz have been observed at different temperatures, while administration of lidocaine decreased the CBF and deactivated the motile cilia. This study will serve as a stepping stone to in-vivo oviduct ciliary endoscopy and future clinical translations.

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

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References

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2019 (1)

Y. He, Y. Qu, J. Zhu, Y. Zhang, A. Saidi, T. Ma, Q. Zhou, and Z. Chen, “Confocal Shear Wave Acoustic Radiation Force Optical Coherence Elastography for Imaging and Quantification of theIn VivoPosterior Eye,” IEEE J. Sel. Top. Quantum Electron. 25(1), 1–7 (2019).
[Crossref]

2018 (5)

Y. Qu, Y. He, A. Saidi, Y. Xin, Y. Zhou, J. Zhu, T. Ma, R. H. Silverman, D. S. Minckler, and Q. Zhou, “In vivo elasticity mapping of posterior ocular layers using acoustic radiation force optical coherence elastography,” Invest. Ophthalmol. Visual Sci. 59(1), 455–461 (2018).
[Crossref]

S. Wang, R. Syed, O. A. Grishina, and I. V. Larina, “Prolonged in vivo functional assessment of the mouse oviduct using optical coherence tomography through a dorsal imaging window,” J. Biophotonics 11(5), e201700316 (2018).
[Crossref]

S. Grechin and D. Yelin, “Imaging acoustic vibrations in an ear model using spectrally encoded interferometry,” Opt. Commun. 407, 175–180 (2018).
[Crossref]

J. Zhu, J. Yu, Y. Qu, Y. He, Y. Li, Q. Yang, T. Huo, X. He, and Z. Chen, “Coaxial excitation longitudinal shear wave measurement for quantitative elasticity assessment using phase-resolved optical coherence elastography,” Opt. Lett. 43(10), 2388–2391 (2018).
[Crossref]

Y. Qu, Y. He, Y. Zhang, T. Ma, J. Zhu, Y. Miao, C. Dai, M. Humayun, Q. Zhou, and Z. Chen, “Quantified elasticity mapping of retinal layers using synchronized acoustic radiation force optical coherence elastography,” Biomed. Opt. Express 9(9), 4054–4063 (2018).
[Crossref]

2017 (7)

M. Keenan, T. H. Tate, K. Kieu, J. F. Black, U. Utzinger, and J. K. Barton, “Design and characterization of a combined OCT and wide field imaging falloposcope for ovarian cancer detection,” Biomed. Opt. Express 8(1), 124–136 (2017).
[Crossref]

D. Cui, K. K. Chu, B. Yin, T. N. Ford, C. Hyun, H. M. Leung, J. A. Gardecki, G. M. Solomon, S. E. Birket, and L. Liu, “Flexible, high-resolution micro-optical coherence tomography endobronchial probe toward in vivo imaging of cilia,” Opt. Lett. 42(4), 867–870 (2017).
[Crossref]

J. F. De Boer, R. Leitgeb, and M. Wojtkowski, “Twenty-five years of optical coherence tomography: the paradigm shift in sensitivity and speed provided by Fourier domain OCT,” Biomed. Opt. Express 8(7), 3248–3280 (2017).
[Crossref]

J. Zhu, Y. Miao, L. Qi, Y. Qu, Y. He, Q. Yang, and Z. Chen, “Longitudinal shear wave imaging for elasticity mapping using optical coherence elastography,” Appl. Phys. Lett. 110(20), 201101 (2017).
[Crossref]

G. M. Solomon, R. Francis, K. K. Chu, S. E. Birket, G. Gabriel, J. E. Trombley, K. L. Lemke, N. Klena, B. Turner, and G. J. Tearney, “Assessment of ciliary phenotype in primary ciliary dyskinesia by micro-optical coherence tomography,” JCI insight 2(5), e91702 (2017).
[Crossref]

J. C. Jing, J. J. Chen, L. Chou, B. J. Wong, and Z. Chen, “Visualization and detection of ciliary beating pattern and frequency in the upper airway using phase resolved Doppler optical coherence tomography,” Sci. Rep. 7(1), 8522 (2017).
[Crossref]

S. Li and W. Winuthayanon, “Oviduct: roles in fertilization and early embryo development,” J. Endocrinol. 232(1), R1–R26 (2017).
[Crossref]

2016 (2)

J. Zhu, L. Qi, Y. Miao, T. Ma, C. Dai, Y. Qu, Y. He, Y. Gao, Q. Zhou, and Z. Chen, “3D mapping of elastic modulus using shear wave optical micro-elastography,” Sci. Rep. 6(1), 35499 (2016).
[Crossref]

Y. Qu, T. Ma, Y. He, J. Zhu, C. Dai, M. Yu, S. Huang, F. Lu, K. K. Shung, and Q. Zhou, “Acoustic radiation force optical coherence elastography of corneal tissue,” IEEE J. Sel. Top. Quantum Electron. 22(3), 288–294 (2016).
[Crossref]

2015 (3)

S. Wang, J. C. Burton, R. R. Behringer, and I. V. Larina, “In vivo micro-scale tomography of ciliary behavior in the mammalian oviduct,” Sci. Rep. 5(1), 13216 (2015).
[Crossref]

D. M. Panelli, C. H. Phillips, and P. C. Brady, “Incidence, diagnosis and management of tubal and nontubal ectopic pregnancies: a review,” Fertility Research and Practice 1(1), 15 (2015).
[Crossref]

W. Zhao, Q. Zhu, M. Yan, C. Li, J. Yuan, G. Qin, and J. J. C. Zhang, “Levonorgestrel decreases cilia beat frequency of human fallopian tubes and rat oviducts without changing morphological structure,” Clin. Exp. Pharmacol. Physiol. 42(2), 171–178 (2015).
[Crossref]

2014 (1)

M. Ezzati, O. Djahanbakhch, S. Arian, and B. R. Carr, “Tubal transport of gametes and embryos: a review of physiology and pathophysiology,” J. Assist. Reprod. Genet. 31(10), 1337–1347 (2014).
[Crossref]

2013 (1)

2011 (3)

D. Shi, K. Komatsu, T. Uemura, and T. Fujimori, “Analysis of ciliary beat frequency and ovum transport ability in the mouse oviduct,” Genes Cells 16(3), 282–290 (2011).
[Crossref]

S. B. Liao, J. Ho, and F. J. R. Tang, “Adrenomedullin increases ciliary beat frequency and decreases muscular contraction in the rat oviduct,” Reproduction (Bristol, U. K.) 141(3), 367–372 (2011).
[Crossref]

T. Nakahari, A. Nishimura, C. Shimamoto, A. Sakai, H. Kuwabara, T. Nakano, S. Tanaka, Y. Kohda, H. Matsumura, and H. Mori, “The regulation of ciliary beat frequency by ovarian steroids in the guinea pig Fallopian tube: interactions between oestradiol and progesterone,” Biomed. Res. 32(5), 321–328 (2011).
[Crossref]

2010 (2)

A. Bylander, M. Nutu, R. Wellander, M. Goksör, H. Billig, and D. J. J. Larsson, “Rapid effects of progesterone on ciliary beat frequency in the mouse fallopian tube,” Reprod. Biol. Endocrinol. 8(1), 48 (2010).
[Crossref]

J. Walther, G. Mueller, H. Morawietz, and E. Koch, “Signal power decrease due to fringe washout as an extension of the limited Doppler flow measurement range in spectral domain optical coherence tomography,” J. Biomed. Opt. 15(4), 041511 (2010).
[Crossref]

2009 (1)

2008 (1)

2006 (2)

R. Lyons, E. Saridogan, and O. Djahanbakhch, “The effect of ovarian follicular fluid and peritoneal fluid on Fallopian tube ciliary beat frequency,” Hum. Reprod. 21(1), 52–56 (2006).
[Crossref]

R. Lyons, E. Saridogan, and O. Djahanbakhch, “The reproductive significance of human Fallopian tube cilia,” Hum. Reprod. Update 12(4), 363–372 (2006).
[Crossref]

2004 (1)

2003 (2)

2002 (3)

G. Tearney, M. Shishkov, and B. E. Bouma, “Spectrally encoded miniature endoscopy,” Opt. Lett. 27(6), 412–414 (2002).
[Crossref]

H. B. Croxatto, “Physiology of gamete and embryo transport through the fallopian tube,” Reprod. BioMed. Online 4(2), 160–169 (2002).
[Crossref]

R. Lyons, O. Djahanbakhch, T. Mahmood, E. Saridogan, S. Sattar, M. Sheaff, A. Naftalin, and R. J. Chenoy, “Fallopian tube ciliary beat frequency in relation to the stage of menstrual cycle and anatomical site,” Hum. Reprod. 17(3), 584–588 (2002).
[Crossref]

2000 (1)

1998 (2)

G. J. Tearney, R. Webb, and B. E. Bouma, “Spectrally encoded confocal microscopy,” Opt. Lett. 23(15), 1152–1154 (1998).
[Crossref]

P. Talbot, G. DiCarlantonio, M. Knoll, and C. Gomez, “Identification of cigarette smoke components that alter functioning of hamster (Mesocricetus auratus) oviducts in vitro,” Biol. Reprod. 58(4), 1047–1053 (1998).
[Crossref]

1997 (2)

1995 (1)

M. Knoll, R. Shaoulian, T. Magers, and P. Talbot, “Ciliary beat frequency of hamster oviducts is decreased in vitro by exposure to solutions of mainstream and sidestream cigarette smoke,” Biol. Reprod. 53(1), 29–37 (1995).
[Crossref]

1994 (1)

K. J. Ingels, M. R. Nijziel, K. Graamans, and E. H. Huizing, “Influence of cocaine and lidocaine on human nasal cilia: beat frequency and harmony in vitro,” Arch. Otolaryngol., Head Neck Surg. 120(2), 197–201 (1994).
[Crossref]

1989 (1)

S. A. Halbert, D. R. Becker, and S. E. Szal, “Ovum transport in the rat oviductal ampulla in the absence of muscle contractility,” Biol. Reprod. 40(6), 1131–1136 (1989).
[Crossref]

1976 (1)

S. Halbert, P. Tam, and R. J. S. Blandau, “Egg transport in the rabbit oviduct: the roles of cilia and muscle,” Science 191(4231), 1052–1053 (1976).
[Crossref]

1968 (1)

C. J. Pauerstein, J. D. Woodruff, and A. S. Zachary, “Factors influencing physiologic activities in the fallopian tube; the anatomy, physiology, and pharmacology of tubal transport,” Obstet. Gynecol. Surv. 23(3), 215–243 (1968).
[Crossref]

Arian, S.

M. Ezzati, O. Djahanbakhch, S. Arian, and B. R. Carr, “Tubal transport of gametes and embryos: a review of physiology and pathophysiology,” J. Assist. Reprod. Genet. 31(10), 1337–1347 (2014).
[Crossref]

Armengot, M.

E. Parrilla, M. Armengot, M. Mata, J. Cortijo, J. Riera, J. L. Hueso, and D. Moratal, “Optical flow method in phase-contrast microscopy images for the diagnosis of primary ciliary dyskinesia through measurement of ciliary beat frequency. Preliminary results,” in 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI). 2012. IEEE.

Barton, J. K.

Becker, D. R.

S. A. Halbert, D. R. Becker, and S. E. Szal, “Ovum transport in the rat oviductal ampulla in the absence of muscle contractility,” Biol. Reprod. 40(6), 1131–1136 (1989).
[Crossref]

Behringer, R. R.

S. Wang, J. C. Burton, R. R. Behringer, and I. V. Larina, “In vivo micro-scale tomography of ciliary behavior in the mammalian oviduct,” Sci. Rep. 5(1), 13216 (2015).
[Crossref]

Billig, H.

A. Bylander, M. Nutu, R. Wellander, M. Goksör, H. Billig, and D. J. J. Larsson, “Rapid effects of progesterone on ciliary beat frequency in the mouse fallopian tube,” Reprod. Biol. Endocrinol. 8(1), 48 (2010).
[Crossref]

Birket, S. E.

G. M. Solomon, R. Francis, K. K. Chu, S. E. Birket, G. Gabriel, J. E. Trombley, K. L. Lemke, N. Klena, B. Turner, and G. J. Tearney, “Assessment of ciliary phenotype in primary ciliary dyskinesia by micro-optical coherence tomography,” JCI insight 2(5), e91702 (2017).
[Crossref]

D. Cui, K. K. Chu, B. Yin, T. N. Ford, C. Hyun, H. M. Leung, J. A. Gardecki, G. M. Solomon, S. E. Birket, and L. Liu, “Flexible, high-resolution micro-optical coherence tomography endobronchial probe toward in vivo imaging of cilia,” Opt. Lett. 42(4), 867–870 (2017).
[Crossref]

Black, J. F.

Blandau, R. J. S.

S. Halbert, P. Tam, and R. J. S. Blandau, “Egg transport in the rabbit oviduct: the roles of cilia and muscle,” Science 191(4231), 1052–1053 (1976).
[Crossref]

Bouma, B.

Bouma, B. E.

Brady, P. C.

D. M. Panelli, C. H. Phillips, and P. C. Brady, “Incidence, diagnosis and management of tubal and nontubal ectopic pregnancies: a review,” Fertility Research and Practice 1(1), 15 (2015).
[Crossref]

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Supplementary Material (1)

NameDescription
» Visualization 1       Video showing synchronized cilia beats

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Figures (7)

Fig. 1.
Fig. 1. System setup for spectrally encoded interferometric microscopy. OC1-OC2: optical coupler, C1-C2: circulator, CO1-CO2: collimator, OA: optical attenuator, M1-M2: mirror, BD: balanced detector, GR: diffraction grating (1145 lines per mm), L1-L4: achromatic lens, L5: 0.4 NA objective lens, G1: galvanometer, FP: focal plane
Fig. 2.
Fig. 2. Processing algorithm for PRD-SS-SEIM system. a) Conversion of the raw signal to its analytical form using the Hilbert Transform. b) Extraction of the phase term and calculation of the displacement using the phase resolved Doppler algorithm. c) En face displacement images of a ciliated area over time.
Fig. 3.
Fig. 3. Analysis method for spatial ciliary activity. a) Temporal displacement images showing periodical ciliary activity. b) M-mode displacement of a single fast scan. c) Quantitative displacement at a single location. d) Spectrum of the displacement showing the ciliary beat frequency (CBF) at its peak. e) Spatial mapping of CBF. f) Histogram of the CBF.
Fig. 4.
Fig. 4. Periodical Ciliary activity at different temperature. a-d) Coordinated ciliary beating cycle from 0 to 0.17 s at 23 °C, 26 °C, 29 °C, and 33 °C respectively (Visualization 1).
Fig. 5.
Fig. 5. Fourier domain analysis on the temporal ciliary movement at a single location. a-d) Temporal displacement for an A-line within the ciliated area, d-i) Temporal displacement at the corresponding site, j-m) Spectrum after FFT, where the peak frequency corresponds to the CBF.
Fig. 6.
Fig. 6. Analysis of the spatial characteristics of the CBF at various temperatures. a-d) Spatial distribution of the CBF at 23 °C, 26 °C, 29 °C, and 33 °C respectively. e) Histogram of the CBF at different temperatures.
Fig. 7.
Fig. 7. Effect of 2% lidocaine administration on the CBF and the region of active cilia. a-b) Spatial CBF maps before and after lidocaine administration. c) Histogram showing the mean and standard deviation of the CBF for the control and experimental conditions.

Equations (2)

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Δd(x,t)=λ4πnΔφ(x,t)
Δφ(x,t)=φ(x,t+Δt)Δφ(x,t)

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