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Label-Free Characterization of Collagen Crosslinking in Bone-Engineered Materials Using Nonlinear Optical Microscopy

Published online by Cambridge University Press:  08 April 2021

Chao-Wei Hung ,
Nirmal Mazumder ,
Dan-Jae Lin ,
Wei-Liang Chen ,
Shih-Ting Lin ,
Ming-Che Chan  and
Guan-Yu Zhuo Open the ORCID record for Guan-Yu Zhuo [Opens in a new window]
Chao-Wei Hung
Affiliation:
PhD Program for Biomedical Engineering and Rehabilitation Science, China Medical University, No. 91, Hsueh-Shih Road, Taichung40402, Taiwan R.O.C.
Nirmal Mazumder
Affiliation:
Department of Biophysics, Manipal School of Life Sciences, Manipal Academy of Higher Education, Manipal, Karnataka576104, India
Dan-Jae Lin
Affiliation:
School of Dentistry, College of Dentistry, China Medical University, No. 91, Hsueh-Shih Road, Taichung40402, Taiwan R.O.C.
Wei-Liang Chen
Affiliation:
Center for Condensed Matter Sciences, National Taiwan University, Taipei10617, Taiwan R.O.C.
Shih-Ting Lin
Affiliation:
Integrative Stem Cell Center, China Medical University Hospital, No. 2, Yude Road, Taichung40447, Taiwan R.O.C.
Ming-Che Chan
Affiliation:
Institute of Photonic System, College of Photonics, National Chiao-Tung University, Tainan71150, Taiwan R.O.C. Institute of Biophotonics, National Yang-Ming University, No. 155, Sec. 2, Linong Street, Beitou District, Taipei City112, Taiwan R.O.C.
Guan-Yu Zhuo*
Affiliation:
Integrative Stem Cell Center, China Medical University Hospital, No. 2, Yude Road, Taichung40447, Taiwan R.O.C. Institute of New Drug Development, China Medical University, No. 91, Hsueh-Shih Road, Taichung40402, Taiwan R.O.C.
*
*Author for correspondence: Guan-Yu Zhuo, E-mail: [email protected]
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Abstract

Engineered biomaterials provide unique functions to overcome the bottlenecks seen in biomedicine. Hence, a technique for rapid and routine tests of collagen is required, in which the test items commonly include molecular weight, crosslinking degree, purity, and sterilization induced structural change. Among them, the crosslinking degree mainly influences collagen properties. In this study, second harmonic generation (SHG) and coherent anti-Stokes Raman scattering (CARS) microscopy are used in combination to explore the collagen structure at molecular and macromolecular scales. These measured parameters are applied for the classification and quantification among the different collagen scaffolds, which were verified by other conventional methods. It is demonstrated that the crosslinking status can be analyzed from SHG images and presented as the coherency of collagen organization that is correlated with the mechanical properties. Also, the comparative analyses of SHG signal and relative CARS signal of amide III band at 1,240 cm−1 to δCH2 band at 1,450 cm−1 of these samples provide information regarding the variation of the molecular structure during a crosslinking process, thus serving as nonlinear optical signatures to indicate a successful crosslinking.

Keywords

coherent anti-Stokes Raman scatteringcollagen crosslinkingmolecular orientationnonlinear optical microscopysecond harmonic generation
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 27 , Issue 3 , June 2021 , pp. 587 - 597
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

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Footnotes

†

Chao-Wei Hung and Nirmal Mazumder equally contributed to the present study.

References

Adany, P, Arnett, DC, Johnson, CK & Hui, R (2011). Tunable excitation source for coherent Raman spectroscopy based on a single fiber laser. Appl Phys Lett 99(18), 181112.CrossRefGoogle ScholarPubMed
Aït-Belkacem, D, Gasecka, A, Munhoz, F, Brustlein, S & Brasselet, S (2010). Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging. Opt Express 18(14), 14859–14870.Google Scholar
Andrews, ME, Murali, J, Muralidharan, C, Madhulata, W & Jayakumar, R (2003). Interaction of collagen with corilagin. Colloid Polym Sci 281(8), 766–770.CrossRefGoogle Scholar
Angele, P, Abke, J, Kujat, R, Faltermeier, H, Schumann, D, Nerlich, M, Kinner, B, Englert, C, Ruszczak, Z, Mehrl, R & Mueller, R (2004). Influence of different collagen species on physico-chemical properties of crosslinked collagen matrices. Biomaterials 25(14), 2831–2841.CrossRefGoogle ScholarPubMed
Bandekar, J (1992). Amide modes and protein conformation. Biochim Biophys Acta 1120(2), 123–143.CrossRefGoogle ScholarPubMed
Barnes, CP, Pemble, CW, Brand, DD, Simpson, DG & Bowlin, GL (2007). Cross-linking electrospun type II collagen tissue engineering scaffolds with carbodiimide in ethanol. Tissue Eng 13(7), 1593–1605.CrossRefGoogle Scholar
Bastiaansen-Jenniskens, Y, Koevoet, W, de Bart, A, van der Linden, J, Zuurmond, A-M, Weinans, H, Verhaar, J, van Osch, G & DeGroot, JJO (2008). Contribution of collagen network features to functional properties of engineered cartilage. Osteoarthr Cartil 16(3), 359–366.CrossRefGoogle ScholarPubMed
Bax, DV, Davidenko, N, Gullberg, D, Hamaia, SW, Farndale, RW, Best, SM & Cameron, RE (2017). Fundamental insight into the effect of carbodiimide crosslinking on cellular recognition of collagen-based scaffolds. Acta Biomater 49, 218–234.CrossRefGoogle ScholarPubMed
Beenakker, J-WM, Ashcroft, BA, Lindeman, JHN & Oosterkamp, TH (2012). Mechanical properties of the extracellular matrix of the aorta studied by enzymatic treatments. Biophys J 102(8), 1731–1737.CrossRefGoogle ScholarPubMed
Bergholt, MS, St-Pierre, J-P, Offeddu, GS, Parmar, PA, Albro, MB, Puetzer, JL, Oyen, ML & Stevens, MM (2016). Raman spectroscopy reveals new insights into the zonal organization of native and tissue-engineered articular cartilage. ACS Cent Sci 2(12), 885–895.CrossRefGoogle ScholarPubMed
Bigi, A, Cojazzi, G, Panzavolta, S, Rubini, K & Roveri, NJB (2001). Mechanical and thermal properties of gelatin films at different degrees of glutaraldehyde crosslinking. Biomaterials 22(8), 763–768.CrossRefGoogle ScholarPubMed
Bonner, MC, Tunney, MM, Jones, DS & Gorman, SP (1997). Factors affecting in vitro adherence of ureteral stent biofilm isolates to polyurethane. Int J Pharm 151(2), 201–207.CrossRefGoogle Scholar
Butler, MF, Ng, YF & Pudney, PDA (2003). Mechanism and kinetics of the crosslinking reaction between biopolymers containing primary amine groups and genipin. J Polym Sci 41(24), 3941–3953.CrossRefGoogle Scholar
Campbell, KR, Chaudhary, R, Handel, JM, Patankar, MS & Campagnola, PJ (2018). Polarization-resolved second harmonic generation imaging of human ovarian cancer. J Biomed Opt 23(6), 1–8.Google ScholarPubMed
Cao, H & Xu, S-Y (2008). EDC/NHS-crosslinked type II collagen-chondroitin sulfate scaffold: Characterization and in vitro evaluation. J Mater Sci: Mater Med 19(2), 567–575.Google ScholarPubMed
Chang, MC, Ikoma, T, Kikuchi, M & Tanaka, J (2002). The cross-linkage effect of hydroxyapatite/collagen nanocomposites on a self-organization phenomenon. J Mater Sci: Mater Med 13(10), 993–997.Google ScholarPubMed
Chen, W-C, Chen, Y-J, Lin, S-T, Hung, W-H, Chan, M-C, Wu, IC, Wu, M-T, Kuo, C-T, Das, S, Kao, F-J & Zhuo, G-Y (2020). Label-free characterization of collagen fibers in cancerous esophagus tissues using ratiometric nonlinear optical microscopy. Exp Biol Med 245(14), 1213–1221.CrossRefGoogle ScholarPubMed
Chen, W-L, Li, T-H, Su, P-J, Chou, C-K, Fwu, PT, Lin, S-J, Kim, D, So, PTC & Dong, C-Y (2009). Second harmonic generation χ tensor microscopy for tissue imaging. Appl Phys Lett 94(18), 183902.Google Scholar
Clemons, TD, Bradshaw, M, Toshniwal, P, Chaudhari, N, Stevenson, AW, Lynch, J, Fear, MW, Wood, FM & Iyer, KS (2018). Coherency image analysis to quantify collagen architecture: Implications in scar assessment. RSC Adv 8(18), 9661–9669.CrossRefGoogle Scholar
Cooper, DR & Davidson, RJ (1965). The effect of ultraviolet irradiation on soluble collagen. Biochem J 97(1), 139–147.CrossRefGoogle ScholarPubMed
Cooper, DR & Davidson, RJ (1966). The effect of ultraviolet irradiation on collagen-fold formation. Biochem J 98(3), 655–661.CrossRefGoogle ScholarPubMed
Cui, F-Z, Li, Y, Ge, JJMS & Reports, ER (2007). Self-assembly of mineralized collagen composites. Mater Sci Eng R 57(1–6), 1–27.CrossRefGoogle Scholar
Cunniffe, GM, Dickson, GR, Partap, S, Stanton, KT & O'Brien, FJ (2010). Development and characterisation of a collagen nano-hydroxyapatite composite scaffold for bone tissue engineering. J Mater Sci: Mater Med 21(8), 2293–2298.Google ScholarPubMed
Deshmukh, K, Sankaran, S, Ahamed, B, Sadasivuni, KK, Pasha, KSK, Ponnamma, D, Rama Sreekanth, PS & Chidambaram, K (2017). Chapter 10—Dielectric spectroscopy. In Spectroscopic Methods for Nanomaterials Characterization, Thomas, S, Thomas, R, Zachariah, AK & Mishra, RK (Eds.), pp. 237–299. Amsterdam: Elsevier.CrossRefGoogle Scholar
Du, C, Cui, FZ, Feng, QL, Zhu, XD & de Groot, K (1998). Tissue response to nano-hydroxyapatite/collagen composite implants in marrow cavity. J Biomed Mater Res 42(4), 540–548.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Duan, X & Sheardown, H (2005). Crosslinking of collagen with dendrimers. J Biomed Mater Res A 75(3), 510–518.CrossRefGoogle ScholarPubMed
Ducourthial, G, Affagard, J-S, Schmeltz, M, Solinas, X, Lopez-Poncelas, M, Bonod-Bidaud, C, Rubio-Amador, R, Ruggiero, F, Allain, J-M, Beaurepaire, E & Schanne-Klein, M-C (2019). Monitoring dynamic collagen reorganization during skin stretching with fast polarization-resolved second harmonic generation imaging. J Biophotonics 12(5), e201800336.CrossRefGoogle ScholarPubMed
Durowoju, IB, Bhandal, KS, Hu, J, Carpick, B & Kirkitadze, M (2017). Differential scanning calorimetry—A method for assessing the thermal stability and conformation of protein antigen. J Vis Exp (121), 55262.Google Scholar
Ellis, R, Green, E & Winlove, CP (2009). Structural analysis of glycosaminoglycans and proteoglycans by means of Raman microspectrometry. Connect Tissue Res 50(1), 29–36.CrossRefGoogle ScholarPubMed
Farrell, HM, Wickham, ED, Unruh, JJ, Qi, PX & Hoagland, PD (2001). Secondary structural studies of bovine caseins: Temperature dependence of β-casein structure as analyzed by circular dichroism and FTIR spectroscopy and correlation with micellization. Food Hydrocoll 15(4), 341–354.CrossRefGoogle Scholar
Fathima, NN, Baias, M, Blumich, B & Ramasami, T (2010). Structure and dynamics of water in native and tanned collagen fibers: Effect of crosslinking. Int J Biol Macromol 47(5), 590–596.CrossRefGoogle ScholarPubMed
Figueiró, SD, Macêdo, AAM, Melo, MRS, Freitas, ALP, Moreira, RA, de Oliveira, RS, Góes, JC & Sombra, ASB (2006). On the dielectric behaviour of collagen–algal sulfated polysaccharide blends: Effect of glutaraldehyde crosslinking. Biophys Chem 120(2), 154–159.CrossRefGoogle ScholarPubMed
Forouhesh Tehrani, K, Pendleton, EG, Southern, WM, Call, JA & Mortensen, LJ (2021). Spatial frequency metrics for analysis of microscopic images of musculoskeletal tissues. Connect Tissue Res 62(1), 4–14.CrossRefGoogle ScholarPubMed
Fratzl, P (2008). Structure and mechanics, an introduction. In Collagen, Fratzl P (Ed.), pp. 1–13. Boston: Springer.Google Scholar
Fuentes-Corona, CG, Licea-Rodriguez, J, Younger, R, Rangel-Rojo, R, Potma, EO & Rocha-Mendoza, I (2019). Second harmonic generation signal from type I collagen fibers grown in vitro. Biomed Opt Express 10(12), 6449–6461.CrossRefGoogle ScholarPubMed
Fujimori, E (1965). Ultraviolet light-induced change in collagen macromolecules. Biopolymers 3(2), 115–119.CrossRefGoogle ScholarPubMed
Gamsjaeger, S, Robins, SP, Tatakis, DN, Klaushofer, K & Paschalis, EP (2017). Identification of pyridinoline trivalent collagen cross-links by Raman microspectroscopy. Calcif Tissue Int 100(6), 565–574.CrossRefGoogle ScholarPubMed
Gao, S, Yuan, Z, Guo, W, Chen, M, Liu, S, Xi, T & Guo, Q (2017). Comparison of glutaraldehyde and carbodiimides to crosslink tissue engineering scaffolds fabricated by decellularized porcine menisci. Mater Sci Eng C Mater Biol Appl 71, 891–900.CrossRefGoogle ScholarPubMed
Gordon, PL, Huang, C, Lord, RC & Yannas, IV (1974). The far-infrared spectrum of collagen. Macromolecules 7(6), 954–956.CrossRefGoogle ScholarPubMed
Gorham, SD, Light, ND, Diamond, AM, Willins, MJ, Bailey, AJ, Wess, TJ & Leslie, NJ (1992). Effect of chemical modifications on the susceptibility of collagen to proteolysis. II. Dehydrothermal crosslinking. Int J Biol Macromol 14(3), 129–138.CrossRefGoogle ScholarPubMed
Gusachenko, I, Latour, G & Schanne-Klein, M-C (2010). Polarization-resolved second harmonic microscopy in anisotropic thick tissues. Opt Express 18(18), 19339–19352.CrossRefGoogle ScholarPubMed
Haugh, MG, Jaasma, MJ & O'Brien, FJ (2009). The effect of dehydrothermal treatment on the mechanical and structural properties of collagen-GAG scaffolds. J Biomed Mater Res A 89(2), 363–369.CrossRefGoogle ScholarPubMed
Hay, ED (1991). Cell Biology of Extracellular Matrix, 2nd ed. New York: Springer US.CrossRefGoogle Scholar
He, L, Mu, C, Shi, J, Zhang, Q, Shi, B & Lin, W (2011). Modification of collagen with a natural cross-linker, procyanidin. Int J Biol Macromol 48(2), 354–359.CrossRefGoogle ScholarPubMed
Kadler, KE, Baldock, C, Bella, J & Boot-Handford, RP (2007). Collagens at a glance. J Cell Sci 120(12), 1955–1958.CrossRefGoogle ScholarPubMed
Kikuchi, M, Itoh, S, Ichinose, S, Shinomiya, K & Tanaka, J (2001). Self-organization mechanism in a bone-like hydroxyapatite/collagen nanocomposite synthesized in vitro and its biological reaction in vivo. Biomaterials 22(13), 1705–1711.CrossRefGoogle Scholar
Kopp, J, Bonnet, M & Renou, JP (1990). Effect of collagen crosslinking on collagen-water interactions (a DSC investigation). Matrix 9(6), 443–450.CrossRefGoogle Scholar
Kozlowska, J, Sionkowska, A, Osyczka, AM & Dubiel, M (2017). Stabilizing effect of carbodiimide and dehydrothermal treatment crosslinking on the properties of collagen/hydroxyapatite scaffolds. Polym Int 66(8), 1164–1172.CrossRefGoogle Scholar
Kumar, R, Grønhaug, KM, Romijn, EI, Finnøy, A, Davies, CL, Drogset, JO & Lilledahl, MB (2015). Polarization second harmonic generation microscopy provides quantitative enhanced molecular specificity for tissue diagnostics. J Biophotonics 8(9), 730–739.CrossRefGoogle ScholarPubMed
Lin, H, Xin, Z & Shuo, T (2018). Optimization of frequency-doubled Er-doped fiber laser for miniature multiphoton endoscopy. J Biomed Opt 23(12), 1–12.Google Scholar
Liu, C, Han, Z & Czernuszka, JT (2009). Gradient collagen/nanohydroxyapatite composite scaffold: Development and characterization. Acta Biomater 5(2), 661–669.CrossRefGoogle ScholarPubMed
Magnusson, SP, Hansen, M, Langberg, H, Miller, B, Haraldsson, B, Kjoeller Westh, E, Koskinen, S, Aagaard, P & Kjær, M (2007). The adaptability of tendon to loading differs in men and women. Int J Clin Exp Pathol 88(4), 237–240.CrossRefGoogle ScholarPubMed
Markiewicz, M, Asano, Y, Znoyko, S, Gong, Y, Watson, DK & Trojanowska, M (2007). Distinct effects of gonadectomy in male and female mice on collagen fibrillogenesis in the skin. J Dermatol Sci 47(3), 217–226.CrossRefGoogle ScholarPubMed
Martinez, MG, Bullock, AJ, MacNeil, S & Rehman, IU (2019). Characterisation of structural changes in collagen with Raman spectroscopy. Appl Spectrosc Rev 54(6), 509–542.CrossRefGoogle Scholar
Marzec, E & Pietrucha, K (2008). The effect of different methods of cross-linking of collagen on its dielectric properties. Biophys Chem 132(2), 89–96.CrossRefGoogle ScholarPubMed
Mazumder, N, Balla, NK, Zhuo, G-Y, Kistenev, YV, Kumar, R, Kao, F-J, Brasselet, S, Nikolaev, VV & Krivova, NA (2019). Label-free non-linear multimodal optical microscopy—Basics, development, and applications. Front Phys 7, 170.CrossRefGoogle Scholar
McColl, IH, Blanch, EW, Gill, AC, Rhie, AGO, Ritchie, MA, Hecht, L, Nielsen, K & Barron, LD (2003). A new perspective on β-sheet structures using vibrational Raman optical activity: From poly(l-lysine) to the prion protein. J Am Chem Soc 125(33), 10019–10026.CrossRefGoogle ScholarPubMed
Ming-Che, W, Pins, GD & Silver, FH (1994). Collagen fibres with improved strength for the repair of soft tissue injuries. Biomaterials 15(7), 507–512.CrossRefGoogle Scholar
Mostaço-Guidolin, L, Rosin, NL & Hackett, T-L (2017). Imaging collagen in scar tissue: Developments in second harmonic generation microscopy for biomedical applications. Int J Mol Sci 18(8), 1772.CrossRefGoogle ScholarPubMed
Nam, K, Kimura, T & Kishida, A (2008). Controlling coupling reaction of EDC and NHS for preparation of collagen gels using ethanol/water co-solvents. Macromol Biosci 8(1), 32–37.CrossRefGoogle ScholarPubMed
Nimni, ME (2018). Collagen: Volume II: Biochemistry and Biomechanics. Florida: CRC Press.Google Scholar
Pachence, JM (1996). Collagen-based devices for soft tissue repair. J Biomed Mater Res 33(1), 35–40.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Park, S-N, Lee, HJ, Lee, KH & Suh, H (2003). Biological characterization of EDC-crosslinked collagen–hyaluronic acid matrix in dermal tissue restoration. Biomaterials 24(9), 1631–1641.CrossRefGoogle ScholarPubMed
Park, S-N, Park, J-C, Kim, HO, Song, MJ & Suh, H (2002). Characterization of porous collagen/hyaluronic acid scaffold modified by 1-ethyl-3-(3-dimethylaminopropyl)carbodiimide cross-linking. Biomaterials 23(4), 1205–1212.CrossRefGoogle ScholarPubMed
Paschalis, EP, Verdelis, K, Doty, SB, Boskey, AL, Mendelsohn, R & Yamauchi, M (2001). Spectroscopic characterization of collagen cross-links in bone. J Bone Miner Res 16(10), 1821–1828.CrossRefGoogle ScholarPubMed
Pieper, JS, Hafmans, T, Veerkamp, JH & van Kuppevelt, TH (2000). Development of tailor-made collagen–glycosaminoglycan matrices: EDC/NHS crosslinking, and ultrastructural aspects. Biomaterials 21(6), 581–593.CrossRefGoogle ScholarPubMed
Reháková, M, Bakoš, D, Vizárová, K, Soldán, M & Juríc̆ková, M (1996). Properties of collagen and hyaluronic acid composite materials and their modification by chemical crosslinking. J Biomed Mater Res 30(3), 369–372.3.0.CO;2-F>CrossRefGoogle ScholarPubMed
Rezakhaniha, R, Agianniotis, A, Schrauwen, JTC, Griffa, A, Sage, D, Bouten, CVC, van de Vosse, FN, Unser, M & Stergiopulos, N (2012). Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy. Biomech Model Mechanobiol 11(3–4), 461–473.CrossRefGoogle ScholarPubMed
Riaz, T, Zeeshan, R, Zarif, F, Ilyas, K, Muhammad, N, Safi, SZ, Rahim, A, Rizvi, SAA & Rehman, IU (2018). FTIR analysis of natural and synthetic collagen. Appl Spectrosc Rev 53(9), 703–746.CrossRefGoogle Scholar
Rocha-Mendoza, I, Langbein, W & Borri, P (2008). Coherent anti-Stokes Raman microspectroscopy using spectral focusing with glass dispersion. Appl Phys Lett 93(20), 201103.CrossRefGoogle Scholar
Rodrigues, APH, Pereira, IM, de Souza, SD, Gil, CSB, Machado, G, Carvalho, SM, Pereira, FV, Paiva, PRP, de Oliveira, LCA & Patricio, SdO (2017). Control of properties of nanocomposites bio-based collagen and cellulose nanocrystals. Cellulose 24(4), 1731–1744.CrossRefGoogle Scholar
Schroepfer, M & Meyer, M (2017). DSC investigation of bovine hide collagen at varying degrees of crosslinking and humidities. Int J Biol Macromol 103, 120–128.CrossRefGoogle ScholarPubMed
Sionkowska, A & Kozłowska, J (2013). Properties and modification of porous 3-D collagen/hydroxyapatite composites. Int J Biol Macromol 52, 250–259.CrossRefGoogle ScholarPubMed
Stoller, P, Reiser, KM, Celliers, PM & Rubenchik, AM (2002). Polarization-modulated second harmonic generation in collagen. Biophys J 82(6), 3330–3342.CrossRefGoogle ScholarPubMed
Tokarz, D, Cisek, R, Golaraei, A, Asa, SL, Barzda, V & Wilson, BC (2015). Ultrastructural features of collagen in thyroid carcinoma tissue observed by polarization second harmonic generation microscopy. Biomed Opt Express 6(9), 3475–3481.CrossRefGoogle ScholarPubMed
Tronci, G, Doyle, A, Russell, SJ & Wood, DJ (2013). Triple-helical collagen hydrogels via covalent aromatic functionalisation with 1,3-phenylenediacetic acid. J Mater Chem B 1(40), 5478–5488.CrossRefGoogle Scholar
Vickers, SM, Squitieri, LS & Spector, M (2006). Effects of cross-linking type II collagen-GAG scaffolds on chondrogenesis in vitro: Dynamic pore reduction promotes cartilage formation. Tissue Eng 12(5), 1345–1355.CrossRefGoogle ScholarPubMed
Wang, L, An, X, Xin, Z, Zhao, L & Hu, Q (2007). Isolation and characterization of collagen from the skin of deep-sea redfish (Sebastes mentella). J Food Sci 72(8), E450–E455.CrossRefGoogle Scholar
Wu, S, Li, H, Yang, H, Zhang, X, Li, Z & Xu, S (2011). Quantitative analysis on collagen morphology in aging skin based on multiphoton microscopy. J Biomed Opt 16(4), 040502.CrossRefGoogle ScholarPubMed
Yannas, IV (1972). Collagen and gelatin in the solid state. J Macromol Sci C 7(1), 49–106.CrossRefGoogle Scholar
Yue, S, Slipchenko, MN & Cheng, J-X (2011). Multimodal nonlinear optical microscopy. Laser Photon Rev 5(4), 496–512.CrossRefGoogle ScholarPubMed
Zhang, Y, Snow, T, Smith, AJ, Holmes, G & Prabakar, S (2019). A guide to high-efficiency chromium (III)-collagen cross-linking: Synchrotron SAXS and DSC study. Int J Biol Macromol 126, 123–129.CrossRefGoogle ScholarPubMed
Zhuo, G-Y, Tsai, P-L, Wang, H-Y & Chan, M-C (2020). Wave-vector-encoded nonlinear endomicroscopy. Opt Lett 45(13), 3713–3716.CrossRefGoogle ScholarPubMed