Multimodal Optical Imaging of Ex Vivo Fallopian Tubes to Distinguish Early and Occult Tubo-Ovarian Cancers
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Design
- Is there a statistical difference in these measurements between disease states, within an individual image, or between images of patients with a lesion/without a lesion? Can these biomarkers be used to visualize areas of lesion?
- In non-lesion cases, are there statistical differences in these measurements in different regions of the fallopian tube?
- How repeatable are these measurements? Are there differences between the left and right fallopian tubes in patients when paired imaging is acquired?
- Are there statistical correlations with age/other patient demographics that might be confounders?
2.1.1. Inclusion Criteria
2.1.2. Exclusion Criteria
2.2. Imaging System
2.3. Image Collection
2.4. Image Preparation
2.4.1. Cross-Sectional Lumen Segmentation
2.4.2. Cross-Sectional Depth Segmentation
2.4.3. A-Line Truncation
2.4.4. En Face Segmentations
2.4.5. Diagnostic and Regional Labels
2.5. Biomarkers
2.5.1. Functional Features
2.5.2. Attenuation Features
2.5.3. Speckle Features
2.5.4. Gray Level Co-Occurrence Matrix (GLCM) Features
2.6. Statistical Analysis
3. Results
3.1. Dataset
3.2. Sample Imaging
3.2.1. Non-Lesion Specimen
3.2.2. Low-Grade Serous Ovarian Carcinoma
3.2.3. High-Grade Serous Ovarian Carcinoma
3.2.4. Endometriosis Specimen
3.3. Quantitative Comparison of Biomarkers and Disease State
3.4. Regional Assessment, Demographic Relations, and Other Potential Confounders
4. Discussion
4.1. Functional Biomarkers
4.2. Attenuation Biomarkers
4.3. Texture Biomarkers
4.4. Study Limitations
4.5. Translation and Future Directions
5. Conclusions
- Key findings include the following:
- Autofluorescence intensity is reduced in regions of HGSOC, LGSOC, or carcinoid cancers, which can be visualized as a region of low-intensity autofluorescence co-registered with homogenous tissue in OCT.
- The median autofluorescence is increased in specimens containing cancer compared to those with no lesions.
- The optical attenuation coefficient is reduced in areas of lesion but increased in the fimbriae compared to the isthmus or the ampulla in non-cancerous fallopian tubes.
- The GLCM Shannon entropy is reduced in specimens containing a cancerous lesion.
- Hemosiderin deposits associated with endometriosis appear as intensely bright focal structures in OCT and AFI, with high optical attenuation and stratification, with reduced mean speckle distribution, and with sharp changes in GLCM features.
- We also demonstrated visualization of structures in the fallopian tubes:
- Folded and overlapping plicae resulting in subsurface gaps in OCT, including the appearance of plicae in hydrosalpinx.
- Vessel-like structures as regions of decreased or increased autofluorescence compared to surrounding tissue, increased optical attenuation, stratification, and speckle distribution.
- Regions of potential fibrotic changes as areas of high intensity OCT and autofluorescence.
- Tissue layering suggestive of differentiable regions of endosalpinx, myosalpinx, and potentially serosa in some specimens.
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Peres, L.C.; Cushing-Haugen, K.L.; Köbel, M.; Harris, H.R.; Berchuck, A.; Rossing, M.A.; Schildkraut, J.M.; Doherty, J.A. Invasive Epithelial Ovarian Cancer Survival by Histotype and Disease Stage. J. Natl. Cancer Inst. 2019, 111, 60–68. [Google Scholar] [CrossRef] [PubMed]
- Gohagan, J.K.; Prorok, P.C.; Hayes, R.B.; Kramer, B.-S. The Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial of the National Cancer Institute: History, Organization, and Status. Control. Clin. Trials 2000, 21, 251S–272S. [Google Scholar] [CrossRef] [PubMed]
- Jacobs, I.J.; Menon, U.; Ryan, A.; Gentry-Maharaj, A.; Burnell, M.; Kalsi, J.K.; Amso, N.N.; Apostolidou, S.; Benjamin, E.; Cruickshank, D.; et al. Ovarian Cancer Screening and Mortality in the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS): A Randomised Controlled Trial. Lancet 2016, 387, 945–956. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, H.; Yamada, Y.; Sado, T.; Sakata, M.; Yoshida, S.; Kawaguchi, R.; Kanayama, S.; Shigetomi, H.; Haruta, S.; Tsuji, Y.; et al. A Randomized Study of Screening for Ovarian Cancer: A Multicenter Study in Japan. Int. J. Gynecol. Cancer 2008, 18, 414–420. [Google Scholar] [CrossRef]
- Menon, U.; Gentry-Maharaj, A.; Burnell, M.; Singh, N.; Ryan, A.; Karpinskyj, C.; Carlino, G.; Taylor, J.; Massingham, S.K.; Raikou, M.; et al. Ovarian Cancer Population Screening and Mortality after Long-Term Follow-up in the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS): A Randomised Controlled Trial. Lancet 2021, 397, 2182–2193. [Google Scholar] [CrossRef]
- Bachert, S.E.; McDowell, A.; Piecoro, D.; Branch, L.B. Serous Tubal Intraepithelial Carcinoma: A Concise Review for the Practicing Pathologist and Clinician. Diagnostics 2020, 10, 102. [Google Scholar] [CrossRef]
- Lengyel, E. Ovarian Cancer Development and Metastasis. Am. J. Pathol. 2010, 177, 1053–1064. [Google Scholar] [CrossRef]
- Corzo, C.; Iniesta, M.D.; Patrono, M.G.; Lu, K.H.; Ramirez, P.T. Role of Fallopian Tubes in the Development of Ovarian Cancer. J. Minim. Invasive Gynecol. 2017, 24, 230–234. [Google Scholar] [CrossRef]
- Gilks, C.B.; Miller, D. Opportunistic Salpingectomy for Women at Low Risk for Development of Ovarian Carcinoma: The Time Has Come. Gynecol. Oncol. 2013, 129, 443–444. [Google Scholar] [CrossRef]
- Hanley, G.E.; McAlpine, J.N.; Kwon, J.S.; Mitchell, G. Opportunistic Salpingectomy for Ovarian Cancer Prevention. Gynaecol. Oncol. Res. Pract. 2015, 2, 5. [Google Scholar] [CrossRef]
- Gaba, F.; Manchanda, R. Systematic Review of Acceptability, Cardiovascular, Neurological, Bone Health and HRT Outcomes Following Risk Reducing Surgery in BRCA Carriers. Best Pract. Res. Clin. Obstet. Gynaecol. 2020, 65, 46–65. [Google Scholar] [CrossRef] [PubMed]
- Castro, P.T.; Aranda, O.L.; Alves, H.D.L.; Lopes, R.T.; Werner, H.; Araujo Júnior, E. Fallopian Tube Vascularization Observed by Microfocus Computed Tomography. Radiol. Bras. 2020, 53, 36–37. [Google Scholar] [CrossRef]
- Sokol, E.R. Clinical Anatomy of the Uterus, Fallopian Tubes, and Ovaries. Glob. Libr. Women’s Med. 2011, 1, 1–14. [Google Scholar] [CrossRef]
- Standring, S. The Female Reproductive System. In Gray’s Anatomy: The anatomical Basis of Clinical Practice; Elsevier: Amsterdam, The Netherlands, 2021; Volume 42, pp. 1307–1330. ISBN 978-0-7020-7705-0. [Google Scholar]
- Verco, C.J. Fallopian Tube Anatomy, Microanatomy, Microcirculation and Counter-current Exchange. In The Fallopian Tube: Clinical and Surgical Aspects; Springer: Berlin/Heidelberg, Germany, 1994; pp. 3–16. ISBN 978-1-4471-1989-0. [Google Scholar]
- Castro, P.T.; Aranda, O.L.; Matos, A.P.P.; Marchiori, E.; Araújo, L.F.B.D.; Alves, H.D.L.; Machado, A.S.; Lopes, R.T.; Werner, H.; Júnior, E.A. The Human Endosalpinx: Anatomical Three-Dimensional Study and Reconstruction Using Confocal Microtomography. Pol. J. Radiol. 2019, 84, 281–288. [Google Scholar] [CrossRef] [PubMed]
- Castro, P.T.; Aranda, O.L.; Marchiori, E.; Araújo, L.F.B.D.; Alves, H.D.L.; Lopes, R.T.; Werner, H.; Araujo Júnior, E. Proportional Vascularization along the Fallopian Tubes and Ovarian Fimbria: Assessment by Confocal Microtomography. Radiol. Bras. 2020, 53, 161–166. [Google Scholar] [CrossRef]
- Rao, B.; Leng, X.; Zeng, Y.; Lin, Y.; Chen, R.; Zhou, Q.; Hagemann, A.R.; Kuroki, L.M.; McCourt, C.K.; Mutch, D.G.; et al. Optical Resolution Photoacoustic Microscopy of Ovary and Fallopian Tube. Sci. Rep. 2019, 9, 14306. [Google Scholar] [CrossRef]
- Leng, X.; Kou, S.; Lin, Y.; Hagemann, A.R.; Hagemann, I.S.; Thaker, P.H.; Kuroki, L.M.; McCourt, C.K.; Mutch, D.G.; Siegel, C.; et al. Quantification of Ovarian Lesion and Fallopian Tube Vasculature Using Optical-Resolution Photoacoustic Microscopy. Sci. Rep. 2022, 12, 15850. [Google Scholar] [CrossRef]
- Reade, C.J.; McVey, R.M.; Tone, A.A.; Finlayson, S.J.; McAlpine, J.N.; Fung-Kee-Fung, M.; Ferguson, S.E. The Fallopian Tube as the Origin of High Grade Serous Ovarian Cancer: Review of a Paradigm Shift. J. Obstet. Gynaecol. Can. 2014, 36, 133–140. [Google Scholar] [CrossRef]
- Bergsten, T.M.; Burdette, J.E.; Dean, M. Fallopian Tube Initiation of High Grade Serous Ovarian Cancer and Ovarian Metastasis: Mechanisms and Therapeutic Implications. Cancer Lett. 2020, 476, 152–160. [Google Scholar] [CrossRef]
- Laokulrath, N.; Warnnissorn, M.; Chuangsuwanich, T.; Hanamornroongruang, S. Sectioning and Extensively Examining the Fimbriated End (SEE-FIM) of the Fallopian Tube in Routine Practices, Is It Worth the Effort? J. Obstet. Gynaecol. Res. 2019, 45, 665–670. [Google Scholar] [CrossRef]
- Mingels, M.J.; van Ham, M.A.; de Kievit, I.M.; Snijders, M.P.; van Tilborg, A.A.; Bulten, J.; Massuger, L.F. Müllerian Precursor Lesions in Serous Ovarian Cancer Patients: Using the SEE-Fim and SEE-End Protocol. Mod. Pathol. 2014, 27, 1002–1013. [Google Scholar] [CrossRef] [PubMed]
- Surrey, E.S. Falloposcopy. Obstet. Gynecol. Clin. N. Am. 1999, 26, 53–62. [Google Scholar] [CrossRef] [PubMed]
- Keenan, M.; Tate, T.H.; Kieu, K.; Black, J.F.; Utzinger, U.; Barton, J.K. Design and Characterization of a Combined OCT and Wide Field Imaging Falloposcope for Ovarian Cancer Detection. Biomed. Opt. Express 2017, 8, 124–136. [Google Scholar] [CrossRef] [PubMed]
- Madore, W.-J.; De Montigny, E.; Deschênes, A.; Benboujja, F.; Leduc, M.; Mes-Masson, A.-M.; Provencher, D.M.; Rahimi, K.; Boudoux, C.; Godbout, N. Morphologic Three-Dimensional Scanning of Fallopian Tubes to Assist Ovarian Cancer Diagnosis. J. Biomed. Opt. 2017, 22, 076012. [Google Scholar] [CrossRef]
- Rocha, A.D.; Drake, W.K.; Rice, P.F.; Long, D.J.; Shir, H.; Walton, R.H.M.; Reed, M.N.; Galvez, D.; Gorman, T.; Heusinkveld, J.M.; et al. Iterative Prototyping Based on Lessons Learned from the Falloposcope In Vivo Pilot Study Experience. J. Biomed. Opt. 2023, 28, 121206. [Google Scholar] [CrossRef]
- Cordova, R.; Kiekens, K.; Burrell, S.; Drake, W.; Kmeid, Z.; Rice, P.; Rocha, A.; Diaz, S.; Yamada, S.; Yozwiak, M.; et al. Sub-Millimeter Endoscope Demonstrates Feasibility of in Vivo Reflectance Imaging, Fluorescence Imaging, and Cell Collection in the Fallopian Tubes. J. Biomed. Opt. 2021, 26, 076001. [Google Scholar] [CrossRef]
- Tate, T.H.; Keenan, M.; Black, J.; Utzinger, U.; Barton, J.K. Ultraminiature Optical Design for Multispectral Fluorescence Imaging Endoscopes. J. Biomed. Opt. 2017, 22, 036013. [Google Scholar] [CrossRef]
- Pahlevaninezhad, H.; Lee, A.M.D.; Hohert, G.; Lam, S.; Shaipanich, T.; Beaudoin, E.-L.; MacAulay, C.; Boudoux, C.; Pierre, M. Lane Endoscopic High-Resolution Autofluorescence Imaging and OCT of Pulmonary Vascular Networks. Opt. Lett. 2016, 41, 3209. [Google Scholar] [CrossRef]
- Pahlevaninezhad, H.; Lee, A.M.D.; Shaipanich, T.; Raizada, R.; Cahill, L.; Hohert, G.; Yang, V.X.D.; Lam, S.; MacAulay, C.; Pierre, M. Lane A high-Efficiency Fiber-Based Imaging System for Co-Registered Autofluorescence and Optical Coherence Tomography. Biomed. Opt. Express 2014, 5, 2978. [Google Scholar] [CrossRef]
- Fujimoto, J.G.; Drexler, W. Introduction to Optical Coherence Tomography. In Optical Coherence Tomography: Technology and Applications; Springer: Berlin/Heidelberg, Germany, 2008. [Google Scholar]
- Hariri, L.P.; Applegate, M.B.; Mino-Kenudson, M.; Mark, E.J.; Medoff, B.D.; Luster, A.D.; Bouma, B.E.; Tearney, G.J.; Suter, M.J. Volumetric Optical Frequency Domain Imaging of Pulmonary Pathology with Precise Correlation to Histopathology. Chest 2013, 143, 64–74. [Google Scholar] [CrossRef]
- van Manen, L.; Dijkstra, J.; Boccara, C.; Benoit, E.; Vahrmeijer, A.L.; Gora, M.J.; Mieog, J.S.D. The Clinical Usefulness of Optical Coherence Tomography during Cancer Interventions. J. Cancer Res. Clin. Oncol. 2018, 144, 1967–1990. [Google Scholar] [CrossRef] [PubMed]
- Gora, M.J.; Suter, M.J.; Tearney, G.J.; Li, X. Endoscopic Optical Coherence Tomography: Technologies and Clinical Applications. Biomed. Opt. Express 2017, 8, 2405. [Google Scholar] [CrossRef] [PubMed]
- Zhou, C.; Fujimoto, J.G.; Tsai, T.-H.; Mashimo, H. Endoscopic OCT. In Optical Coherence Tomography: Technology and Applications, 2nd, ed.; Springer International Publishing: Cham, Switzerland, 2015; pp. 2077–2108. ISBN 978-3-319-06419-2. [Google Scholar]
- Drexler, W.; Chen, Y.; Aguirre, A.D.; Považay, B.; Unterhuber, A.; Fujimoto, J.G. Ultrahigh Resolution Optical Coherence Tomography. In Optical Coherence Tomography; Drexler, W., Fujimoto, J.G., Eds.; Springer International Publishing: Cham, Switzerland, 2015; pp. 277–318. ISBN 978-3-319-06418-5. [Google Scholar]
- Kirillin, M.; Motovilova, T.; Shakhova, N. Optical Coherence Tomography in Gynecology: A Narrative Review. J. Biomed. Opt. 2017, 22, 121709. [Google Scholar] [CrossRef] [PubMed]
- Kirillin, M.; Panteleeva, O.; Yunusova, E.; Donchenko, E.; Shakhova, N. Criteria for Pathology Recognition in Optical Coherence Tomography of Fallopian Tubes. J. Biomed. Opt. 2012, 17, 081413. [Google Scholar] [CrossRef] [PubMed]
- Luo, H.; Li, S.; Kou, S.; Lin, Y.; Hagemann, I.S.; Zhu, Q. Enhanced 3D Visualization of Human Fallopian Tube Morphology Using a Miniature Optical Coherence Tomography Catheter. Biomed. Opt. Express 2023, 14, 3225. [Google Scholar] [CrossRef]
- Li, S.; Luo, H.; Kou, S.; Hagemann, I.S.; Zhu, Q. Depth-resolved Attenuation Mapping of the Human Ovary and Fallopian Tube Using Optical Coherence Tomography. J. Biophotonics 2023, 16, e202300002. [Google Scholar] [CrossRef]
- Hariri, L.P.; Bonnema, G.T.; Schmidt, K.; Winkler, A.M.; Korde, V.; Hatch, K.D.; Davis, J.R.; Brewer, M.A.; Barton, J.K. Laparoscopic Optical Coherence Tomography Imaging of Human Ovarian Cancer. Gynecol. Oncol. 2009, 114, 188–194. [Google Scholar] [CrossRef]
- Wang, J.; Xu, Y.; Boppart, S.A. Review of Optical Coherence Tomography in Oncology. J. Biomed. Opt. 2017, 22, 121711. [Google Scholar] [CrossRef]
- Chang, S.; Bowden, A.K. Review of Methods and Applications of Attenuation Coefficient Measurements with Optical Coherence Tomography. J. Biomed. Opt. 2019, 24, 090901. [Google Scholar] [CrossRef]
- Jacques, S.L. Optical Properties of Biological Tissues: A Review. Phys. Med. Biol. 2013, 58, R37–R61. [Google Scholar] [CrossRef]
- Haralick, R.M.; Shanmugam, K.; Dinstein, I. Textural Features for Image Classification. IEEE Trans. Syst. Man. Cybern. 1973, SMC-3, 610–621. [Google Scholar] [CrossRef]
- Sawyer, T.W.; Chandra, S.; Rice, P.F.S.; Koevary, J.W.; Barton, J.K. Three-Dimensional Texture Analysis of Optical Coherence Tomography Images of Ovarian Tissue. Phys. Med. Biol. 2018, 63, 235020. [Google Scholar] [CrossRef] [PubMed]
- St-Pierre, C.; Madore, W.-J.; De Montigny, E.; Trudel, D. Dimension Reduction Technique Using a Multilayered Descriptor for High-Precision Classification of Ovarian Cancer Tissue Using Optical Coherence Tomography: A Feasibility Study. J. Med. Imaging 2017, 4, 041306. [Google Scholar] [CrossRef] [PubMed]
- Schmitt, J.M.; Xiang, S.H.; Yung, K.M. Speckle in Optical Coherence Tomography. J. Biomed. Opt. 1999, 4, 95–105. [Google Scholar] [CrossRef]
- Lindenmaier, A.A.; Conroy, L.; Farhat, G.; DaCosta, R.S.; Flueraru, C.; Vitkin, I.A. Texture Analysis of Optical Coherence Tomography Speckle for Characterizing Biological Tissues In Vivo. Opt. Lett. 2013, 38, 1280. [Google Scholar] [CrossRef]
- Benavides, J.M.; Chang, S.; Park, S.Y.; Richards-Kortum, R.; Mackinnon, N.; MacAulay, C.; Milbourne, A.; Malpica, A.; Follen, M. Multispectral Digital Colposcopy for In Vivo Detection of Cervical Cancer. Opt. Express 2003, 11, 1223–1236. [Google Scholar] [CrossRef]
- McWilliams, A.; Shaipanich, T.; Lam, S. Fluorescence and Navigational Bronchoscopy. Thorac. Surg. Clin. 2013, 23, 153–161. [Google Scholar] [CrossRef]
- Kennedy, T.C.; Lam, S.; Hirsch, F.R. Review of Recent Advances in Fluorescence Bronchoscopy in Early Localization of Central Airway Lung Cancer. Oncologist 2001, 6, 257–262. [Google Scholar] [CrossRef]
- Lane, P.M.; Gilhuly, T.; Whitehead, P.; Zeng, H.; Poh, C.F.; Ng, S.; Williams, P.M.; Zhang, L.; Rosin, M.P.; MacAulay, C.E. Simple Device for the Direct Visualization of Oral-Cavity Tissue Fluorescence. J. Biomed. Opt. 2006, 11, 024006. [Google Scholar] [CrossRef]
- Wang, Y.; Wang, Q.; Feng, J.; Wu, Q. Comparison of Autofluorescence Imaging Bronchoscopy and White Light Bronchoscopy for Detection of Lung Cancers and Precancerous Lesions. Patient Prefer. Adherence 2013, 7, 621–631. [Google Scholar] [CrossRef]
- McAlpine, J.N.; El Hallani, S.; Lam, S.F.; Kalloger, S.E.; Luk, M.; Huntsman, D.G.; Macaulay, C.; Gilks, C.B.; Miller, D.M.; Lane, P.M. Autofluorescence Imaging Can Identify Preinvasive or Clinically Occult Lesions in Fallopian Tube Epithelium: A Promising Step towards Screening and Early Detection. Gynecol. Oncol. 2011, 120, 385–392. [Google Scholar] [CrossRef] [PubMed]
- Tate, T.H.; Baggett, B.; Rice, P.F.S.; Koevary, J.W.; Orsinger, G.V.; Nymeyer, A.C.; Welge, W.A.; Saboda, K.; Roe, D.J.; Hatch, K.D.; et al. Multispectral Fluorescence Imaging of Human Ovarian and Fallopian Tube Tissue for Early-Stage Cancer Detection. J. Biomed. Opt. 2016, 21, 056005. [Google Scholar] [CrossRef] [PubMed]
- Sawyer, T.W.; Koevary, J.W.; Rice, F.P.S.; Howard, C.C.; Austin, O.J.; Connolly, D.C.; Cai, K.Q.; Barton, J.K. Quantification of Multiphoton and Fluorescence Images of Reproductive Tissues from a Mouse Ovarian Cancer Model Shows Promise for Early Disease Detection. J. Biomed. Opt. 2019, 24, 096010. [Google Scholar] [CrossRef] [PubMed]
- George, R.; Michaelides, M.; Brewer, M.A.; Utzinger, U. Parallel Factor Analysis of Ovarian Autofluorescence as a Cancer Diagnostic. Lasers Surg. Med. 2012, 44, 282–295. [Google Scholar] [CrossRef]
- Hariri, L.P.; Liebmann, E.R.; Marion, S.L.; Hoyer, P.B.; Davis, J.R.; Brewer, M.A.; Barton, J.K. Simultaneous Optical Coherence Tomography and Laser Induced Fluorescence Imaging in Rat Model of Ovarian Carcinogenesis. Cancer Biol. Ther. 2010, 10, 438–447. [Google Scholar] [CrossRef]
- De Veld, D.C.G.; Witjes, M.J.H.; Sterenborg, H.J.C.M.; Roodenburg, J.L.N. The Status of in Vivo Autofluorescence Spectroscopy and Imaging for Oral Oncology. Oral. Oncol. 2005, 41, 117–131. [Google Scholar] [CrossRef]
- Udovich, J.A.; Kirkpatrick, N.D.; Kano, A.; Tanbakuchi, A.; Utzinger, U.; Gmitro, A.F. Spectral Background and Transmission Characteristics of Fiber Optic Imaging Bundles. Appl. Opt. 2008, 47, 4560–4568. [Google Scholar] [CrossRef]
- Li, J.; Thiele, S.; Kirk, R.W.; Quirk, B.C.; Hoogendoorn, A.; Chen, Y.C.; Peter, K.; Nicholls, S.J.; Verjans, J.W.; Psaltis, P.J.; et al. 3D-Printed Micro Lens-in-Lens for In Vivo Multimodal Microendoscopy. Small 2022, 18, 2107032. [Google Scholar] [CrossRef]
- Feroldi, F.; Verlaan, M.; Knaus, H.; Davidoiu, V.; Vugts, D.J.; van Dongen, G.A.M.S.; Molthoff, C.F.M.; de Boer, J.F. High Resolution Combined Molecular and Structural Optical Imaging of Colorectal Cancer in a Xenograft Mouse Model. Biomed. Opt. Express 2018, 9, 6186–6204. [Google Scholar] [CrossRef]
- Beaudette, K.; Baac, H.W.; Madore, W.-J.; Villiger, M.; Godbout, N.; Bouma, B.E.; Boudoux, C. Laser Tissue Coagulation and Concurrent Optical Coherence Tomography through a Double-Clad Fiber Coupler. Biomed. Opt. Express 2015, 6, 1293–1303. [Google Scholar] [CrossRef]
- Turashvili, G.; Krishnamurti, U.G.; Crothers, B.A.; Giannico, G.A.; Hanley, K.; Plotkin, A.; Karnezis, A.N. Protocol for the Examination of Specimens from Patients with Primary Tumors of the Ovary, Fallopian Tube, or Peritoneum; College of American Pathologist: Chicago, IL, USA, 2024. [Google Scholar]
- Pahlevaninezhad, H.; Lee, A.M.D.; Cahill, L.; Lam, S.; MacAulay, C.; Pierre, M. Lane Fiber-Based Polarization Diversity Detection for Polarization-Sensitive Optical Coherence Tomography. Opt. Lett. 2014, 1, 283–295. [Google Scholar] [CrossRef]
- Zuckermann Cynamon, A. Lumen Segmentation in Endobronchial Optical Coherence Tomography with Deep Learning. Bachelor’s Thesis, Simon Fraser University, Burnaby, BC, Canada, 2023. [Google Scholar]
- Hill, C.; Malone, J.; Liu, K.; Ng, S.P.-Y.; MacAulay, C.; Poh, C.; Lane, P. 3-Dimension Epithelial Segmentation in Optical Coherence Tomography of the Oral Cavity Using Deep Learning 2024. Cancers 2024, 16, 2144. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Ding, N.; Yu, Y.; Yuan, X.; Luo, S.; Luan, J.; Zhao, Y.; Wang, Y.; Ma, Z. Optimized Depth-Resolved Estimation to Measure Optical Attenuation Coefficients from Optical Coherence Tomography and Its Application in Cerebral Damage Determination. J. Biomed. Opt. 2019, 24, 035002. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez, R.C.; Woods, R.E.; Eddins, S.L. Digital Image Processing Using MATLAB, 3rd ed.; Gatesmark Publishing: Knoxville, TN, USA, 2020; ISBN 978-0-9820854-1-7. [Google Scholar]
- Vermeer, K.A.; Mo, J.; Weda, J.J.A.; Lemij, H.G.; Boer, J.F. de Depth-Resolved Model-Based Reconstruction of Attenuation Coefficients in Optical Coherence Tomography. Biomed. Opt. Express 2013, 5, 322–337. [Google Scholar] [CrossRef]
- Zwanenburg, A.; Leger, S.; Vallières, M.; Löck, S. Image Biomarker Standardisation Initiative. Radiology 2020, 295, 328–338. [Google Scholar] [CrossRef]
- Shapiro, S.S.; Wilk, M.B. An Analysis of Variance Test for Normality (Complete Samples). Biometrika 1965, 52, 591. [Google Scholar] [CrossRef]
- Levene, H. Robust Tests for Equality of Variances. In Contributions to Probability and Statistics: Essays in Honor of Harold Hotelling; Stanford University Press: Palo Alto, CA, USA, 1960; pp. 278–292. [Google Scholar]
- Grubbs, F.E. Procedures for Detecting Outlying Observations in Samples. Technometrics 1969, 11, 1–21. [Google Scholar] [CrossRef]
- Student. The Probable Error of a Mean. Biometrika 1908, 6, 1–25. [Google Scholar] [CrossRef]
- Mann, H.B.; Whitney, D.R. On a Test of Whether One of Two Random Variables is Stochastically Larger than the Other. Ann. Math. Statist. 1947, 18, 50–60. [Google Scholar] [CrossRef]
- Zimmerman, D.W. A Note on Preliminary Tests of Equality of Variances. Br. J. Math. Stat. Psychol. 2004, 57, 173–181. [Google Scholar] [CrossRef]
- Welch, B.L. The Generalization of “Student’s” Problem When Several Different Population Variances Are Involved. Biometrika 1947, 34, 28–35. [Google Scholar] [CrossRef] [PubMed]
- Wilcoxon, F. Individual Comparisons by Ranking Methods. Biom. Bull. 1945, 1, 80–83. [Google Scholar] [CrossRef]
- Spearman, C. The Proof and Measurement of Association between Two Things. Am. J. Psychol. 1904, 15, 72. [Google Scholar] [CrossRef]
- Panzarella, V.; Buttacavoli, F.; Gambino, A.; Capocasale, G.; Di Fede, O.; Mauceri, R.; Rodolico, V.; Campisi, G. Site-Coded Oral Squamous Cell Carcinoma Evaluation by Optical Coherence Tomography (OCT): A Descriptive Pilot Study. Cancers 2022, 14, 5916. [Google Scholar] [CrossRef]
- Cabe, A.G.; Estrada, A.D.; Hoyt, T.; Yang, X.; Jenney, S.; Valente, P.T.; Cox, B.; McLaughlin, J.E.; Robinson, R.D.; Milner, T.E.; et al. Endogenous Fluorescence of Hemosiderin in Endometriosis to Improve Clinical Detection. Transl. Med. Commun. 2019, 4, 9. [Google Scholar] [CrossRef]
- Tanskanen, A.; Malone, J.; Hohert, G.; MacAulay, C.; Lane, P.M. Triple-Clad W-Type Fiber Mitigates Multipath Artifacts in Multimodal Optical Coherence Tomography. Opt. Express 2023, 31, 4465–4481. [Google Scholar] [CrossRef]
- Tanskanen, A.; Malone, J.; MacAulay, C.; Lane, P.M. Multipath Artifacts Enable Angular Contrast in Multimodal Endoscopic Optical Coherence Tomography. Opt. Express 2023, 31, 44224–44245. [Google Scholar] [CrossRef]
- Malone, J.; Hohert, G.; Hoang, L.; Miller, D.M.; McAlpine, J.N.; MacAulay, C.E.; Lane, P.M. Endoscopic Optical Coherence Tomography (OCT) and Autofluorescence Imaging (AFI) of Ex Vivo Fallopian Tubes. In Proceedings of the Multimodal Biomedical Imaging XV, San Francisco, CA, USA, 1 February 2020; SPIE: San Francisco, CA, USA, 2020. [Google Scholar]
- Malone, J.; Hohert, G.; McAlpine, J.N.; Hoang, L.; MacAulay, C.; Lane, P.M. Co-Registered Optical Coherence Tomography (OCT) and Autofluorescence Imaging (AFI) of Ex Vivo Fallopian Tubes for Early Ovarian Cancer Detection. In Proceedings of the Multimodal Biomedical Imaging XVII, San Francisco, CA, USA, 22–27 January 2022; SPIE: San Francisco, CA, USA, 2022. [Google Scholar]
Category | Feature [Units] | Description | Calculation |
---|---|---|---|
Functional | Autofluorescence [µM fluorescein] | Intensity after calibration with respect to distance between optical core and tissue using positive (0.98 µM fluorescein) and negative (water) standards. | |
Attenuation | Overall Attenuation Coefficient [mm−1] | Mean optical attenuation coefficient over entire visualized tissue depth. | Depth-resolved method for estimating optical attenuation coefficient from OCT from Jian Liu et al. [70]: |
Superficial Attenuation Coefficient [mm−1] | Mean optical attenuation coefficient over upper 50% of visualized tissue depth. | ||
Deep Attenuation Coefficient [mm−1] | Mean optical attenuation coefficient over lower 50% of visualized tissue depth. | ||
Stratification [a.u.] | Ratiometric comparison of mean attenuation coefficient of superficial and deep regions. Ranges from −1 (higher deep attenuation) to +1 (higher superficial attenuation). | ||
Texture | Speckle Distribution | Mean of the gamma distribution found by fitting all A-lines in the OCT cross-section. | |
GLCM Contrast | Sum of squares variance or inertia; local variations between a pixel and its adjacent neighbours in the azimuthal direction. Value of 0 represents no variation. | Haralick features calculated from the gray level co-occurrence matrix (GLCM) via MATLAB function graycoprops [46]: | |
GLCM Correlation | Joint probability of occurrence of intensity pairs between a pixel and its neighbor. Measured from −1 (perfect negative correlation) to +1 (perfect positive correlation). | …via graycoprops [46]: | |
GLCM Energy | Angular second moment; uniformity of gray level distribution. Measured from 0 (no uniformity) to 1 (complete uniformity). | …via graycoprops [46]: | |
GLCM Homogeneity | Inverse difference moment; similarity between a pixel and its adjacent neighbours in the azimuthal direction. Value of 0 represents strong similarity. | …via graycoprops [46]: | |
GLCM Shannon Entropy | Randomness of the image. Value of 0 represents a completely uniform image. | MATLAB function entropy [71]: |
Statistical Question | Parametric Test | Non-Parametric Test |
---|---|---|
Is there a difference in measurements of biomarkers in volumes of different disease states? | Unpaired t-test [77] | Mann–Whitney U test [78] |
In volumes containing a lesion, is there a difference in measurements of biomarkers within the area of lesion compared to the area of non-lesion? | Welch’s paired t-test [79,80] | Wilcoxon rank sum [81] |
In volumes without a lesion, is there a difference in measurements of biomarkers in different regions (isthmus, ampulla, fimbriae)? | Welch’s paired t-test [79,80] | Wilcoxon rank sum [81] |
Are there differences between the left and right fallopian tubes in patients when paired imaging is acquired? | Welch’s paired t-test [79,80] | Wilcoxon rank sum [81] |
In volumes without a lesion, are there statistical correlations between measurements and patient age? | Spearman’s rank order [82] | |
In volumes without a lesion, are there statistical correlations between measurements and time difference between arrival and imaging of the specimen? | Spearman’s rank order [82] |
Diagnosis | Sample Size | Age | Time to Imaging | |||
---|---|---|---|---|---|---|
Left | Right | Total | ||||
[#] | [#] | [#] | [Years] | [Minutes] | ||
No lesion | 10 | 9 | 19 | 61 | 69 | |
3 | 5.4 | |||||
(42–81) | (23–128) | |||||
Cancerous lesions | 3 | 4 | 7 | 65 | 75 | |
3 | 14.7 | |||||
(51–77) | (30–127) | |||||
LGSOC | 0 | 2 | 2 | 65 | 69 | |
4 | 6.0 | |||||
(61–69) | (63–75) | |||||
HGSOC | 3 | 1 | 4 | 69 | 80 | |
3 | 27 | |||||
(60–77) | (30–127) | |||||
Carcinoid | 0 | 1 | 1 | 66 | 66 | |
- | - | |||||
- | - | |||||
Endometriosis | 1 | 1 | 2 | 62 | 88 | |
18 | 2.5 | |||||
(44–80) | (85–90) | |||||
Total | 14 | 14 | 28 | 62 | 72 |
Sample Size | Age | Time to Imaging | |
---|---|---|---|
Diagnosis | [#] | [Years] | [Minutes] |
Paired non-lesion | 5 | 57 | 73 |
6 | 7.3 | ||
(44–80) | (49–90) |
Functional | Attenuation | Texture | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Site | Sample Size | Autofluorescence | Overall Attenuation | Superficial Attenuation | Deep Attenuation | Stratification | Speckle Distribution | GLCM Contrast | GLCM Correlation | GLCM Energy | GLCM Homogeneity | GLCM Shannon Entropy |
Overall | 5 | 39.6 | 1.3 | 3.0 | 2.3 | 9.7 | 4.5 | 11.3 | 1.8 | 26.7 | 5.7 | 10.0 |
Fimbriae | 5 | 51.4 | 6.4 | 7.7 | 5.8 | 7.3 | 11.8 | 13.8 | 5.2 | 28.8 | 6.2 | 18.9 |
Ampulla | 5 | 37.3 | 1.7 | 3.5 | 2.6 | 12.7 | 7.8 | 8.4 | 1.2 | 23.1 | 4.7 | 8.4 |
Isthmus | 4 | 29.8 | 2.1 | 2.9 | 5.3 | 21.0 | 3.4 | 9.1 | 2.2 | 27.9 | 5.6 | 7.4 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Malone, J.; Tanskanen, A.S.; Hill, C.; Zuckermann Cynamon, A.; Hoang, L.; MacAulay, C.; McAlpine, J.N.; Lane, P.M. Multimodal Optical Imaging of Ex Vivo Fallopian Tubes to Distinguish Early and Occult Tubo-Ovarian Cancers. Cancers 2024, 16, 3618. https://doi.org/10.3390/cancers16213618
Malone J, Tanskanen AS, Hill C, Zuckermann Cynamon A, Hoang L, MacAulay C, McAlpine JN, Lane PM. Multimodal Optical Imaging of Ex Vivo Fallopian Tubes to Distinguish Early and Occult Tubo-Ovarian Cancers. Cancers. 2024; 16(21):3618. https://doi.org/10.3390/cancers16213618
Chicago/Turabian StyleMalone, Jeanie, Adrian S. Tanskanen, Chloe Hill, Allan Zuckermann Cynamon, Lien Hoang, Calum MacAulay, Jessica N. McAlpine, and Pierre M. Lane. 2024. "Multimodal Optical Imaging of Ex Vivo Fallopian Tubes to Distinguish Early and Occult Tubo-Ovarian Cancers" Cancers 16, no. 21: 3618. https://doi.org/10.3390/cancers16213618