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Automated Detection of Collagen Bundles in Second Harmonic Generation Microscopy Images

Year 2023, Volume: 11 Issue: 4, 352 - 363, 22.12.2023
https://doi.org/10.17694/bajece.1269884

Abstract

Collagen is one of the most abundant proteins in the body. It is essential for the structure, functionality, and strength of the connective tissue such as skin, bone, tendon, and cornea. It is known that a change in the arrangement or morphology of these fibrillar structures relates to multiple dysfunctions including corneal diseases and various cancer types. Due to their critical roles in wide-range abnormalities, there is an increasing interest in the pattern analysis of collagen arrangements. In recent years, Second Harmonic Generation (SHG) microscopy is proven to be an efficient imaging modality for visualizing unstained collagen fibrils. There are plenty of studies in the literature on the analysis of collagen distribution in SHG images. However, the majority of these methods are limited to detecting simple, statistical and non-local properties such as pixel intensity and orientation variance. There is a need for a method to detect the local structural properties of collagen bundles. This paper is to introduce an automated method to detect collagen bundles in 3-dimensional SHG microscopy images. The origin of the proposed method is based on multiscale directional representation systems. The proposed method detects the collagen bundles by measuring the dominant orientation of local regions and an orientation-based connected component analysis. Through more local analysis and the detection of collagen bundles separately, the proposed method would lead to the extraction of more detailed structural information on collagen bundle distribution.

References

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  • [38] C. Kayasandik, P. Negi, F. Laezza, M. Papadakis, and D. Labate, “Automated sorting of neuronal trees in fluorescent images of neuronal networks using neurotreetracer,” Scientific reports, vol. 8, no. 1, p. 6450, 2018.
  • [39] D. Labate, F. Laezza, P. Negi, B. Ozcan, and M. Papadakis, “Efficient processing of fluorescence images using directional multiscale representations,” Mathematical modelling of natural phenomena, vol. 9, no. 5, pp. 177–193, 2014.
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  • [41] B. Ozcan, P. Negi, F. Laezza, M. Papadakis, and D. Labate, “Automated detection of soma location and morphology in neuronal network cultures,” PloS one, vol. 10, no. 4, p. e0121886, 2015.
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Year 2023, Volume: 11 Issue: 4, 352 - 363, 22.12.2023
https://doi.org/10.17694/bajece.1269884

Abstract

References

  • [1] K. M. Meek and C. Knupp, “Corneal structure and transparency,” Progress in retinal and eye research, vol. 49, pp. 1–16, 2015.
  • [2] C. Raoux, M. Schmeltz, M. Bied, M. Alnawaiseh, U. Hansen, G. Latour, and M.-C. Schanne-Klein, “Quantitative structural imaging of keratoconic corneas using polarization-resolved shg microscopy,” Biomedical optics express, vol. 12, no. 7, pp. 4163–4178, 2021.
  • [3] M. S. Sridhar, “Anatomy of cornea and ocular surface,” Indian journal of ophthalmology, vol. 66, no. 2, p. 190, 2018.
  • [4] H.-Y. Zhou, Y. Cao, J. Wu, and W.-S. Zhang, “Role of corneal collagen fibrils in corneal disorders and related pathological conditions,” International journal of ophthalmology, vol. 10, no. 5, p. 803, 2017.
  • [5] G. A. Di Lullo, S. M. Sweeney, J. Korkko, L. Ala-Kokko, and J. D. San Antonio, “Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, type i collagen,” Journal of Biological Chemistry, vol. 277, no. 6, pp. 4223–4231, 2002.
  • [6] S. Xu, H. Xu, W. Wang, S. Li, H. Li, T. Li, W. Zhang, X. Yu, and L. Liu, “The role of collagen in cancer: from bench to bedside,” Journal of translational medicine, vol. 17, pp. 1–22, 2019.
  • [7] R. M. Mart´ınez-Ojeda, M. D. P´erez-C´arceles, L. C. Ardelean, S. G. Stanciu, and J. M. Bueno, “Multiphoton microscopy of oral tissues,” Frontiers in Physics, vol. 8, p. 128, 2020.
  • [8] E. A. Gibson, O. Masihzadeh, T. C. Lei, D. A. Ammar, and M. Y. Kahook, “Multiphoton microscopy for ophthalmic imaging,” Journal of ophthalmology, vol. 2011, 2011.
  • [9] R. LaComb, O. Nadiarnykh, and P. J. Campagnola, “Quantitative second harmonic generation imaging of the diseased state osteogenesis imperfecta: experiment and simulation,” Biophysical journal, vol. 94, no. 11, pp. 4504–4514, 2008.
  • [10] S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophysical journal, vol. 90, no. 2, pp. 693–703, 2006.
  • [11] S.-W. Chu, S.-Y. Chen, G.-W. Chern, T.-H. Tsai, Y.-C. Chen, B.-L. Lin, and C.-K. Sun, “Studies of χ (2)/χ (3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophysical journal, vol. 86, no. 6, pp. 3914–3922, 2004.
  • [12] Z. Liu, K. P. Quinn, L. Speroni, L. Arendt, C. Kuperwasser, C. Sonnenschein, A. M. Soto, and I. Georgakoudi, “Rapid three-dimensional quantification of voxel-wise collagen fiber orientation,” Biomedical optics express, vol. 6, no. 7, pp. 2294–2310, 2015.
  • [13] Z. Liu, D. Pouli, D. Sood, A. Sundarakrishnan, C. K. H. Mingalone, L. M. Arendt, C. Alonzo, K. P. Quinn, C. Kuperwasser, L. Zeng et al., “Automated quantification of three-dimensional organization of fiberlike structures in biological tissues,” Biomaterials, vol. 116, pp. 34–47, 2017.
  • [14] E. C. Rentchler, K. L. Gant, R. Drapkin, M. Patankar, and P. J. Campagnola, “Imaging collagen alterations in stics and high grade ovarian cancers in the fallopian tubes by second harmonic generation microscopy,” Cancers, vol. 11, no. 11, p. 1805, 2019.
  • [15] J. M. Watson, P. F. Rice, S. L. Marion, M. A. Brewer, J. R. Davis, J. J. Rodriguez, U. Utzinger, P. B. Hoyer, and J. K. Barton, “Analysis of second-harmonic-generation microscopy in a mouse model of ovarian carcinoma,” Journal of Biomedical Optics, vol. 17, no. 7, pp. 076 002– 076 002, 2012.
  • [16] D. S. James and P. J. Campagnola, “Recent advancements in optical harmonic generation microscopy: Applications and perspectives,” BME Frontiers, vol. 2021, 2021.
  • [17] Y. Ogura, Y. Tanaka, E. Hase, T. Yamashita, and T. Yasui, “Texture analysis of second-harmonic-generation images for quantitative analysis of reticular dermal collagen fibre in vivo in human facial cheek skin,” Experimental Dermatology, vol. 28, no. 8, pp. 899–905, 2019.
  • [18] T. Hsu, A. Calway, and R. Wilson, “Texture analysis using the multiresolution fourier transform,” Bristol, UK, Tech. Rep, 1993.
  • [19] W. Hu, H. Li, C. Wang, S. Gou, and L. Fu, “Characterization of collagen fibers by means of texture analysis of second harmonic generation images using orientation-dependent gray level co-occurrence matrix method,” Journal of biomedical optics, vol. 17, no. 2, pp. 026 007– 026 007, 2012.
  • [20] C. C. Gotlieb and H. E. Kreyszig, “Texture descriptors based on cooccurrence matrices,” Computer vision, graphics, and image processing, vol. 51, no. 1, pp. 70–86, 1990.
  • [21] C. Y. Park, J. K. Lee, and R. S. Chuck, “Second harmonic generation imaging analysis of collagen arrangement in human cornea,” Investigative ophthalmology & visual science, vol. 56, no. 9, pp. 5622–5629, 2015.
  • [22] M. Send´ın-Mart´ın, J. Posner, U. Harris, M. Moronta, J. Conejo- Mir S´anchez, S. Mukherjee, M. Rajadhyaksha, K. Kose, and M. Jain, “Quantitative collagen analysis using second harmonic generation images for the detection of basal cell carcinoma with ex vivo multiphoton microscopy,” Experimental Dermatology, vol. 32, no. 4, pp. 392–402, 2023.
  • [23] Y. Liu, A. Keikhosravi, G. S. Mehta, C. R. Drifka, and K. W. Eliceiri, “Methods for quantifying fibrillar collagen alignment,” Fibrosis: methods and protocols, pp. 429–451, 2017.
  • [24] J. S. Bredfeldt, Y. Liu, C. A. Pehlke, M. W. Conklin, J. M. Szulczewski, D. R. Inman, P. J. Keely, R. D. Nowak, T. R. Mackie, and K. W. Eliceiri, “Computational segmentation of collagen fibers from secondharmonic generation images of breast cancer,” Journal of biomedical optics, vol. 19, no. 1, pp. 016 007–016 007, 2014.
  • [25] Y. Liu, A. Keikhosravi, C. A. Pehlke, J. S. Bredfeldt, M. Dutson, H. Liu, G. S. Mehta, R. Claus, A. J. Patel, M. W. Conklin et al., “Fibrillar collagen quantification with curvelet transform based computational methods,” Frontiers in bioengineering and biotechnology, vol. 8, p. 198, 2020.
  • [26] J. Liu, M.-y. Xu, J. Wu, H. Zhang, L. Yang, D.-x. Lun, Y.-c. Hu, and B. Liu, “Picrosirius-polarization method for collagen fiber detection in tendons: A mini-review,” Orthopaedic Surgery, vol. 13, no. 3, pp. 701– 707, 2021.
  • [27] Y. Zhang, Y. Chen, B. Zhao, J. Gao, L. Xia, F. Xing, Y. Kong, Y. Li, and G. Zhang, “Detection of type i and iii collagen in porcine acellular matrix using hplc–ms,” Regenerative biomaterials, vol. 7, no. 6, pp. 577–582, 2020.
  • [28] X. Wang, B. Le, N. Zhang, K. H. Bak, Y. Zhang, and Y. Fu, “Off-flavour compounds in collagen peptides from fish: Formation, detection and removal,” International Journal of Food Science & Technology, vol. 58, no. 3, pp. 1543–1563, 2023.
  • [29] J. Zhang, Y. Ning, H. Zhu, N. J. Rotile, H. Wei, H. Diyabalanage, E. C. Hansen, I. Y. Zhou, S. C. Barrett, M. Sojoodi et al., “Fast detection of liver fibrosis with collagen-binding single-nanometer iron oxide nanoparticles via t 1-weighted mri,” Proceedings of the National Academy of Sciences, vol. 120, no. 18, p. e2220036120, 2023.
  • [30] M. Salarian, H. Yang, R. C. Turaga, S. Tan, J. Qiao, S. Xue, Z. Gui, G. Peng, H. Han, P. Mittal et al., “Precision detection of liver metastasis by collagen-targeted protein mri contrast agent,” Biomaterials, vol. 224, p. 119478, 2019.
  • [31] O. Y. Ibhagui, D. Li, H. Han, G. Peng, M. L. Meister, Z. Gui, J. Qiao, M. Salarian, B. Dong, Y. Yuan et al., “Early detection and staging of lung fibrosis enabled by collagen-targeted mri protein contrast agent,” Chemical & Biomedical Imaging, 2023.
  • [32] C. Roa, V. N. Du Le, M. Mahendroo, I. Saytashev, and J. C. Ramella- Roman, “Auto-detection of cervical collagen and elastin in mueller matrix polarimetry microscopic images using k-nn and semantic segmentation classification,” Biomedical Optics Express, vol. 12, no. 4, pp. 2236–2249, 2021.
  • [33] M. Zaffar and A. Pradhan, “Assessment of anisotropy of collagen structures through spatial frequencies of mueller matrix images for cervical pre-cancer detection,” Applied Optics, vol. 59, no. 4, pp. 1237– 1248, 2020.
  • [34] J. Li, Y. Chen, W. Zhi, and Q. Cheng, “Photoacoustics spectral analysis for in vivo detection of collagen contents in cancers,” in 2022 IEEE International Ultrasonics Symposium (IUS). IEEE, 2022, pp. 1–4.
  • [35] J.-E. Cota, A. Spadigam, and A. Dhupar, “Detection of type vii collagen in odontogenic keratocyst: An immunohistochemical study,” Journal of clinical and experimental dentistry, vol. 11, no. 4, p. e310, 2019.
  • [36] J. T. Stefano, L. V. Guedes, A. A. A. de Souza, D. S. Vanni, V. A. F. Alves, F. J. Carrilho, A. Largura, M. Arrese, and C. P. Oliveira, “Usefulness of collagen type iv in the detection of significant liver fibrosis in nonalcoholic fatty liver disease,” Annals of hepatology, vol. 20, p. 100253, 2021.
  • [37] R. C. Gonzalez, Digital image processing. Pearson education india, 2009.
  • [38] C. Kayasandik, P. Negi, F. Laezza, M. Papadakis, and D. Labate, “Automated sorting of neuronal trees in fluorescent images of neuronal networks using neurotreetracer,” Scientific reports, vol. 8, no. 1, p. 6450, 2018.
  • [39] D. Labate, F. Laezza, P. Negi, B. Ozcan, and M. Papadakis, “Efficient processing of fluorescence images using directional multiscale representations,” Mathematical modelling of natural phenomena, vol. 9, no. 5, pp. 177–193, 2014.
  • [40] C. B. Kayasandik and D. Labate, “Improved detection of soma location and morphology in fluorescence microscopy images of neurons,” Journal of neuroscience methods, vol. 274, pp. 61–70, 2016.
  • [41] B. Ozcan, P. Negi, F. Laezza, M. Papadakis, and D. Labate, “Automated detection of soma location and morphology in neuronal network cultures,” PloS one, vol. 10, no. 4, p. e0121886, 2015.
  • [42] C. Kayasandik, K. Guo, and D. Labate, “Directional multiscale representations and applications in digital neuron reconstruction,” Journal of computational and applied mathematics, vol. 349, pp. 482–493, 2019.
  • [43] L. Schmarje, C. Zelenka, U. Geisen, C.-C. Gl¨uer, and R. Koch, “2d and 3d segmentation of uncertain local collagen fiber orientations in shg microscopy,” in Pattern Recognition: 41st DAGM German Conference, DAGM GCPR 2019, Dortmund, Germany, September 10–13, 2019, Proceedings 41. Springer, 2019, pp. 374–386.
  • [44] D. M. Powers, “Evaluation: from precision, recall and f-measure to roc, informedness, markedness and correlation,” arXiv preprint arXiv:2010.16061, 2020.
  • [45] J. N. Ouellette, C. R. Drifka, K. B. Pointer, Y. Liu, T. J. Lieberthal, W. J. Kao, J. S. Kuo, A. G. Loeffler, and K. W. Eliceiri, “Navigating the collagen jungle: the biomedical potential of fiber organization in cancer,” Bioengineering, vol. 8, no. 2, p. 17, 2021.
  • [46] E. Brown, T. McKee, E. DiTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nature medicine, vol. 9, no. 6, pp. 796–800, 2003.
There are 46 citations in total.

Details

Primary Language English
Subjects Artificial Intelligence
Journal Section Araştırma Articlessi
Authors

Cihan Bilge Kayasandık 0000-0002-9282-6568

Early Pub Date January 25, 2024
Publication Date December 22, 2023
Published in Issue Year 2023 Volume: 11 Issue: 4

Cite

APA Kayasandık, C. B. (2023). Automated Detection of Collagen Bundles in Second Harmonic Generation Microscopy Images. Balkan Journal of Electrical and Computer Engineering, 11(4), 352-363. https://doi.org/10.17694/bajece.1269884

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