Advances in Quantitative and Qualitative Assessment of Collagen in Cutaneous Wound Healing
Keywords:
skin, wound, collagen, assessment
Abstract
Wound healing treatment is a challenging strategy in skin drug delivery due to its complexities. During wound healing stages, fibroblast deposit extracellular matrix components, which majority is collagen. Fibrillar collagen, particularly collagen I, is the predominant skin collagen during the healing process. Collagen analysis is a crucial process in wound healing study since it indicates impairment process of collagen production such as scar formation which is aesthetically unwanted. Therefore, recent studies developed quantitative and qualitative evaluation of collagen fiber based on histological staining. Thus, a comprehensive discussion of those studies to provide an insight for pharmacists, dermatologists, and skin researchers to designate a precise assessment in wound healing process.
Keywords: skin, wound, collagen, assessment
References
Babalola, O., Mamalis, A., Lev-Tov, H., & Jagdeo, J. (2014). Optical Coherence Tomography (OCT) of Collagen in Normal Skin and Skin Fibrosis. Archives of Dermatological Research, 306(1), 1–9. https://doi.org/10.1007/s00403-013-1417-7
Benito-Martínez, S., Pérez-Köhler, B., Rodríguez, M., Izco, J. M., Recalde, J.I., & Pascual, G. (2022). Wound Healing Modulation through the Local Application of Powder Collagen-Derived Treatments in an Excisional Cutaneous Murine Model. Biomedicines, 10(5), 960. https://doi.org/10.3390/biomedicines10050960
Boniakowski, A. E., Kimball, A. S., Jacobs, B. N. , Kunkel, S. L., & Gallagher, K. A. (2017). Macrophage-Mediated Inflammation in Normal and Diabetic Wound Healing. The Journal of Immunology : Official Journal of The American Association of Immunologists, 199(1), 17–24. https://doi.org/10.4049/jimmunol.1700223.
Brauer, E., Lippens, E., Klein, O., Nebrich, G., Schreivogel, S., Korus, G., Duda, G. N., & Petersen, A. (2019). Collagen Fibrils Mechanically Contribute to Tissue Contraction in an In Vitro Wound Healing Scenario. Advanced Science, 6(9), 1801780. https://doi.org/10.1002/advs.201801780.
Brianezi, G., Grandi, F., Bagatin, E., Enokihara, M. M. S. S., & Miot, H. A. (2015). Dermal type I collagen assessment by digital image analysis. Anais Brasileiros De Dermatologia, 90(5), 723–727. https://doi.org/10.1590/abd1806-4841.20153331.
Brien, P., De Anda C., Prokocimer, P. (2014) Comparison of Digital Planimetry and Ruler Technique to Measure ABSSSI Lesion Sizes in the ESTABLISH-1 Study.Surgical Infection. 15, 2. https://doi.org/10.1089/sur.2013.070.
Brook, I. (1995). Microbiology of Gastrostomy Site Wound Infections in Children. Journal of Medical Microbiology, 43(3), 221–223. https://doi.org/10.1099/00222615-43-3-221.
Caetano, G. F., Fronza, M., Leite, M. N., Gomes, A., & Frade, M. A. C. (2016). Comparison of collagen content in skin wounds evaluated by biochemical assay and by computer-aided histomorphometric analysis. Pharmaceutical Biology, 54 (11), 2555–2559. https://doi.org/0.3109/13880209.2016.1170861.
Caley, M.P., Martins, V. L. C., O’Toole, E.A. (2015). Metalloproteinases and Wound Healing. Advances in Wound Care, 4(4), 225–234. https://doi.org/10.1089/wound.2014.0581.
Chen, W.T. (1992). Membrane Proteases: Roles In Tissue Remodeling And Tumour Invasion. Current Opinion In Cell Biology, 4(5), 802–809. https://doi.org/10.1016/0955-0674(92)90103-j.
Chen, Y., Yu, Q., & Xu, C. B. (2017). A Convenient Method For Quantifying Collagen Fibers in Atherosclerotic Lesions by Image J Software. International Journal of Clinical and Experimental Medicine, 10(10), 14904–14910.
Chlipala, E., Bendzinski, C. M., Chu, K., Johnson, J. I., Brous, M., Copeland, K., & Bolon, B. (2020). Optical density-based image analysis method for the evaluation of hematoxylin and eosin staining precision. Journal of Histotechnology., 43(1), 29–37. https://doi.org/10.1080/01478885.2019.1708611.
Clark, R. A. F. (2003). Fibrin Is a Many Splendored Thing. Journal of Investigative Dermatology, 121(5), 21-22. https://doi.org/10.1046/j.1523-1747.2003.12575.x.
Clemons, T. D., Bradshaw, M., Toshniwal, P., Chaudari, N., Stevenson, A., Lynch, J., Fear, M. W., Wood, F. M., & Iyer, K. S. (2018). Coherency Image Analysis To Quantify Collagen Architecture: Implications in Scar Assessment. RSC Advances, 8(18), 9661-9669. https://doi.org/10.1039/C7RA12693J.
Cognasse, F., Hamzeh, H., Chavarin, P., Acquart, S., Genin, C., & Garraud, O. (2005). Evidence Of Toll-Like Receptor Molecules On Human Platelets. Immunology and Cell Biology, 83(2), 196–198. https://doi.org/10.1111/j.1440-1711.2005.01314.x.
Desmouliere, A., Redard, M., Darby, I., & Gabbiani, G. (1995). Apoptosis Mediates The Decrease In Cellularity During The Transition Between Granulation Tissue And Scar. The American Journal Of Pathology, 146(1), 56–66.
Dhane, D. M., Maiti, M., Mungle, T., Bar, C., Achar, A., Kolekar, M., Chakraborty, C., (2017). Fuzzy Spectral Clustering For Automated Delineation Of Chronic Wound Region Using Digital Images. Computer in Biology and Medicine, 2017; 89, 551-560. http://dx.doi.org/10.1016/j.compbiomed.2017.04.004
Dhane, D. M., Khrisna, V., Achar A., Bar, C., Sanyal, K., Chakraborty, C. (2016). Spectral Clustering for Unsupervised Segmentation of Lower Extremity Wound Beds Using Optical Images. Journal of Medical System, 2016;40(9), 207. https://doi.org/10.1007/s10916-016-0554-x
Djatumurti, D. R., Rafida, A., Manalu, A. Y. P., & Pangestiningsih, T. W. (2021). Re-epithelization and Density of Collagen Fibers on Wound Healing of Mice’s Skin (Mus musculus) That Treated with Combination of Chitosan Membrane and Eel (Monopterus albus) Mucous. BIO Web of Conferences, 33, 06005. https://doi.org/10.1051/bioconf/20213306005.
Dong, Y., Weidong, Z., Lei, X., Luo, X., Xiang, Q., Zhu, X., Pan, Q., Jin, P., & Cheng, B. (2022). Treatment of Acute Wounds With Recombinant Human-Like Collagen and Recombinant Human-Like Fibronectin in C57BL/6 Mice Individually or in Combination. Frontiers in Bioengineering and Biotechnology, 10, 908585. https://doi.org/10.3389/fbioe.2022.908585.
Duong, T. E., & Hagood, J. S. (2018). Epigenetic Regulation of Myofibroblast Phenotypes in Fibrosis. Current Pathobiology Reports, 6(1), 79–96. https://doi.org/10.1007/s40139-018-0155-0.
Enoch, S., & Leaper, D. J. (2008). Basic Science Of Wound Healing. Surgery, 23(2), 37–42. https://doi.org/10.1383/surg.23.2.37.60352
Filko, D., Nyarko, E. K. (2023). 2D/3D Wound Segmentation and Measurement Based on a Robot-Driven Reconstruction System. Sensors, 23(6), 1-23. https://doi.org/10.3390/s23063298
Folkman, J., & D’Amore, P. A. (1996). Blood vessel formation: What is its molecular basis? Cell, 87(7), 1153–1155. https://doi.org/10.1016/s0092-8674(00)81810-3
Foltynski, P., Ladyzynski P., Ciechanowska, A., Migalska-Musial, K., Judzewicz, G., Sabalinska, S. (2015). Wound Area Measurement with Digital Planimetry: Improved Accuracy and Precision with Calibration Based on 2 Rulers. PLoS ONE, 10(8), 1-13. https://doi.org/10.1371/journal.pone.0134622
Gnyawali, S., C., Sinha, M., El Masry, M., S., Wulff, B., Ghatak, S., Soto-Gonzalez, F., Wilgus, T., A., Roy, S., Sen, C., K. (2020). High Resolution Ultrasound Imaging For Repeated Measure Of Wound Tissue Morphometry, Biomechanics And Hemodynamics Under Fetal, Adult And Diabetic Conditions. PLoS ONE, 15(11), 1-23. https://doi.org/10.1371/journal.pone.0241831
Golebiewska, E. M., & Poole, A. W. (2015). Platelet Secretion: From Haemostasis To Wound Healing And Beyond. Blood Reviews, 2015;29(3), 153- 162. https://doi.org/10.1016/j.blre.2014.10.003
Golebiewska, E. M., & Poole, A.W. (2015). Platelet Secretion: From Haemostasis to Wound Healing and Beyond. Blood Reviews, 29(3), 153–162. https://doi.org/10.1016/j.blre.2014.10.003.
Guo, S., & DiPietro, L. A. (2010). Critical review in oral biology & medicine: Factors affecting wound healing. Journal of Dental Research, 89(3), 219–229. https://doi.org/10.1177/0022034509359125.
Gurtner, G. C., Werner, S., Barrandon,Y., & Longaker, M. T. (2008). Wound repair and regeneration. Nature, 453(7193), 314–321. https://doi.org/10.1038/nature07039.
Ho, J.K., & Hantash, B.M. (2013). The principles of wound healing. Expert Review of Dermatology, 8(6), 639–658. https://doi.org/10.1586/17469872.2013.857161.
Huang, C., Wu, Z., Du, Y., & Ogawa, R. (2020). The Epidemiology of Keloids. In Textbook on Scar Management (pp. 20). Springer, Cham.
Huang, S.P. Wu, M., Shun, C., Wang, H., Hsieh, C., Kuo, M, & Lin, J. (2005). Cyclooxygenase-2 Increases Hypoxia-Inducible Factor-1 And Vascular Endothelial Growth Factor To Promote Angiogenesis In Gastric Carcinoma. Journal of Biomedical Science, 12(1), 229–241. https://doi.org/10.1007/s11373-004-8177-5
Jin, J., Li, H., Chen, Z., Sheng, J., Liu, T., Ma, B., Zhu, S., Xia, Z. (2018). 3-D Wound Scanner: A Novel, Effective, Reliable, And Convenient Tool For Measuring Scar Area. Burns. 44(8), 1930-1939. https://doi.org/10.1016/j.burns.2018.05.009
Jørgensen, L. B., Halekoh, U., Jemec G. B. E., Sørensen, J. A., Yderstræde, K. B. (2020) Monitoring Wound Healing of Diabetic Foot Ulcers Using Two-Dimensional and Three-Dimensional Wound Measurement Techniques: A Prospective Cohort Study. Adv Wound Care (New Rochelle), 9(10), 554–555. https://doi.org/10.1089/wound.2019.1000
Kanitakis, J. (2002). Anatomy, histology and immunohistochemistry of normal human skin. European Journal Of Dermatology, 12(4), 390–401.
Kanitakis, J. (2013). Keloidal Dermatofibroma: Report of A Rare Dermatofibroma Variant in a Young White Woman. The American Journal of Dermatopathology, 35(3), 400-401. https://doi.org/10.1097/DAD.0b013e31825d9d30.
Khorasani, H., Zheng, Z., Nguyen, C., Zara, J., Zhang, X., Wang, J., Ting, K. & Soo, C. (2011). A Quantitative Approach to Scar Analysis. American Journal of Pathology, 178(2), 621–628. https://doi.org/10.1016/j.ajpath.2010.10.019.
Limandjaja, G. C., Van den Broek, L. J., Waaijman, T., Van Veen, H. A., Everts, V., Monstrey, S., Scheper, R. J., Niessen, F. B., & Gibbs, S., (2017). Increased epidermal thickness and abnormal epidermal differentiation in keloid scars. The British Journal Of Dermatology, 176(1), 116–126. https://doi.org/10.1111/bjd.14844
Mahbod, A., Ecker, R., Schaefer, G., Ellinger, I., 2021. Automatic Foot Ulcer Segmentation Using an Ensemble of Convolutional Neural Networks. https://doi.org/10.48550/arXiv.2109.01408
Mathew-Steiner, S. S., Roy, S., & Sen, C. K. (2021). Collagen in Wound Healing. Bioengineering, 8(5), 63. https://doi.org/10.3390/bioengineering8050063
Matsumoto, M., Nakagami, G., Kitamura, A., Kurita M., Suga, H., Miyake, T., Kawamoto, A., Sanada, H. (2021). Ultrasound Assessment of Deep Tissue On The Wound Bed And Periwound Skin: A Classification System Using Ultrasound Images. Journal of Tissue Viability, 30(1), 28-35. https://doi.org/10.1016/j.jtv.2020.08.002.
McGibbon, D. (2005). Rook’s Textbook of Dermatology, 7th editionClinical and Experimental Dermatology, 31(1), 178–179. https://doi.org/10.1111/j.1365-2230.2005.02034.x.
McGrath, J. A. (2020). The structure and function of skin. In McKee’s Pathology of The Skin With Clinical Correlations, 5th edition, volume 1 (pp. 26). Elsevier, Edinburgh
Moulin, V., Larochelle, S., Langlois, C., Thibault, I., Lopez-Vallé, C. A., & Roy, M. (2004). Normal Skin Wound and Hypertrophic Scar Myofibroblasts Have Differential Responses to Apoptotic Inductors. Journal of Cellular Physiology, 198(3), 350–358. https://doi.org/10.1002/jcp.10415.
Murphy, P. S., & Evans, G. R. D. (2012). Advances in Wound Healing: A Review of Current Wound Healing Products. Plastic Surgery International, 2012, 190436. https://doi.org/10.1155/2012/190436.
Naik, S., Bouladoux, N., Linehan, J. L., Han, S., Harrison, O. J., Wilhelm, C., Conlan, S., Himmelfarb, S., Byrd, A. L., Deming, C., Quinones, M., Brenchley, J. M., Kong, H. H., Tussiwand, R., Murphy, K. M., Merad. M., Segre, J. A., & Belkaid, Y. (2015). Commensal-Dendritic-Cell Interaction Specifies A Unique Protective Skin Immune Signature. Nature, 520(7545), 104-108. https://doi.org/10.1038/nature14052.
Osman, O. S., Selway, J. L., Harikumar, P.E., Jassim, S., & Langlands, K. (2014). Automated Analysis of Collagen Histology in Ageing Skin. Proceedings of The International Conference on Bioimaging (Bioimaging 2014), 41-48 https://doi.org/10.5220/0004786600410048.
Owczarzy, A., Kurasiński, R., Kulig, K., Rogóż, W., Szkudlarek, A., & Maciążek-Jurczyk, M. (2020). Collagen-structure properties and application. Engineering of Biomaterials, 2020(156), 17-23. https://doi.org/10.34821/eng.biomat.156.2020.17-23.
Petrov, V. V., Fagard, R. H., & Lijnen, P. J. (2002). Stimulation of Collagen Production by Transforming Growth Factor-Β1 During Differentiation of Cardiac Fibroblasts to Myofibroblasts. Hypertension,39(2), 258–263. https://doi.org/10.1161/hy0202.103268.
Pfisterer, K., Shaw, L. E., Symmank, D., & Weninger, W. (2021). The Extracellular Matrix in Skin Inflammation and Infection. Frontiers In Cell and Developmental Biology, 9, 682414. https://doi.org/10.3389/fcell.2021.682414.
Potekaev, N. N., Borzkyh, O. B., Medvedev, G. V., Pushkin, D. V., Petrova, M. M., Gavrilyuk, O. A., Karpova, E. I., Trefilova, V. V., Deminas, O. M., Popova, T. E. & Shanayder, N. A. (2021). Genetic and Epigenetic Aspects of Skin Collagen Fiber Turnover and Functioning. Cosmetics, 8(4), 92. https://doi.org/10.3390/cosmetics8040092.
Quan, T., & Fisher, G. J. (2015). Role of Age-Associated Alterations of The Dermal Extracellular Matrix Microenvironment in Human Skin Aging: A Mini-Review. Gerontology. 2015;61(5), 427–434. https://doi.org/10.1159/000371708.
Rangaraj, A., Harding, K., & Leaper, D. (2011). Role of Collagen in Wound Management. Wounds UK, 7(2), 54–63.
Rezakhaniha, R., Agianniotis, A., Schrauwen, J. T. C., Griffa, A., Sage, D., Bouten, C. V. C., Van de Vosse, F. N., Unser, M., & Stergiopulos, N. (2012). Experimental Investigation of Collagen Waviness and Orientation in The Arterial Adventitia Using Confocal Laser Scanning Microscopy. Biomechanics and Modeling in Mechanobiology, 11(3-4):461–473. https://doi.org/10.1007/s10237-011-0325-z.
Rodrigues, M., Kosaric, N., Bonham, C. A., & Gurtner, G.C. (2019). Wound healing: A cellular perspective. Physiological Reviews, 99(1), 665–706. https://doi.org/10.1152/physrev.00067.2017.
Sabol, F., Dancakova, L, Gál, P. Vasilenko, T., Novotny, M., Smetana, K., & Lenhards, L. (2012) Immunohistological Changes in Skin Wounds During The Early Periods of Healing in a Rat Model. Veterinarni Medicina, 57, 77–82. https://doi.org/10.17221/5253-VETMED
Senejko, M., Pasek, J., Szajkowski, S., Cieślar, G., Sieroń, A. (2021). Evaluation Of The Therapeutic Efficacy Of Active Specialistic Medical Dressings In The Treatment Of Decubitus. Postepy Dermatologii i Alergologii, 38(1), 75-79. https://doi.org/10.5114/ada.2021.104282
Setiawati, A., Jang, D., Cho, D., Cho, S., Jeong, H., Park, S., Gwak, J., Ryu, S. R., Jung, W. H., Ju, B., Jung, K., Kwon, O., & Shin, K. (2021). An Accelerated Wound-Healing Surgical Suture Engineered with an Extracellular Matrix. Advanced Healthcare Materials, 10(6), 1–10. https://doi.org/10.1002/adhm.202001686.
Singer, A. J., & Clark, R. A. (1999). Cutaneous Wound Healing. The New England Journal of Medicine, 341(10), 738-746. https://doi.org/10.1056/NEJM199909023411006.
Somaiah, C., Kumar, A., Mawrie, D., Sharma, A., Patil, S. D., Bhattacharyya, J., Swaminathan, R., & Jaganathan, B. G. (2015). Collagen Promotes Higher Adhesion, Survival And Proliferation Of Mesenchymal Stem Cells. PLoS One, 10(120), 1–15. https://doi.org/10.1371/journal.pone.0145068.
Takeo, M., Lee, W., & Ito, M. (2015). Wound healing and skin regeneration. Cold Spring Habour Perspective in Medicine, ;5:a023267. https://doi.org/10.1101/cshperspect.a023267.
Tang, Y. Q., Yeaman, M. R., & Selsted, M.E. (2002). Antimicrobial Peptides from Human Platelets. Infection and Immunity, 70(12), 6524–6533. https://doi.org/10.1128/IAI.70.12.6524-6533.2002.
Theocharis, A. D., Skandalis, S. S., Gialeli, C., & Karamanos, N. K. (2016). Extracellular Matrix Structure. Advanced Drug Delivery Reviews, 1(97), 4–27. htps://doi.org/10.1016/j.addr.2015.11.001.
Velez, A. M. A, & Howard, M. S. (2012). Collagen IV in Normal and in Disease Process. North American Journal of Medical Sciences, 4(1), 1–8. https://doi.org/10.4103/1947-2714.92892.
Velnar, T., Bailey, T., & Smrkolj, V. (2009). The wound healing process: An overview of the cellular and molecular mechanisms. The Journal of International Medical Research, 37(5), 1528–1542. https://doi.org/10.1177/147323000903700531.
Verhaegen, P. D. H. M, Van Zujilen, P. P. M., Pennings, N. M., Van Marle, J., Niessen, F. B., Van der Horst, C. M. A. M., & Middelkoop, E. (2009). Differences in Collagen Architecture Between Keloid, Hypertrophic Scar, Normotrophic Scar, and Normal Skin: An Objective Histopathological Analysis. Wound Repair And Regeneration: Official Publication of The Wound Healing Society [and] The European Tissue Repair Society, 17(5), 649–656. https://doi.org/10.1111/j.1524-475X.2009.00533.x.
Wang, H. (2021). A Review of The Effects of Collagen Treatment in Clinical Studies. Polymers, 13(22), 3868. https://doi.org/10.3390/polym13223868
Wang, C., Anisuzzaman, D., M., Williamson, V., Dhar, M., K., Rostami, B., Niezgoda, J., Gopalakrishnan, S., Zeyun, Y. (2020). Fully Automatic Wound Segmentation With Deep Convolutional Neural Networks. Scientific Reports, 10(1), 1-9. https://doi.org/10.1038/s41598-020-78799-w
Wershof, E., Park, D., Barry, D. J., Jenkins, R. P., Rulan, A., Wilkins, A., Schlegelmilch, K, Roxanis, I, Anderson, K. I., Bates, P. A., & Sahai, E. (2021). A FIJI Macro for Quantifying Pattern in Extracellular Matrix. Life Science Alliance, 4(3), 1–11. https://doi.org/10.26508/lsa.202000880.
Whittaker, P., Kloner, R. A., Boughner, D. R., & Pickering, J. G. (1994). Quantitative Assessment of Myocardial Collagen with Picrosirius Red Staining and Circularly Polarized Light. Basic Res Cardiol. 89(5), 397–410. https://doi.org/10.1007/BF00788278
Wilkinson, H. N., & Hardman, M. J. (2020). Wound Healing: Cellular Mechanisms And Pathological Outcomes. Open Biology, 10. 200223. https://doi.org/10.1098/rsob.200223.
Wolfram, D., Tzankov, A., Pülzl, P., & Piza-Katzer, H. (2009). Hypertrophic Scars and Keloids - A Review of Their pathophysiology, Risk Factors, and Therapeutic Management. Dermatologic Surgery: Official Publication For American Society For Dermatologic Surgery, 35(2), 171-181. https://doi.org/171–181. 10.1111/j.1524-4725.2008.34406.x.
Xue, M., & Jackson, C. J. (2015). Extracellular Matrix Reorganization During Wound Healing and Its Impact on Abnormal Scarring. Advances in Wound Care, 4(3), 119–136. https://doi.org/10.1089/wound.2013.0485.
Yang, H. J., & Kang, S.Y. (2019). The Clinical Uses of Collagen-Based Matrices in the Treatment of Chronic Wounds. Journal of Wound Management and Research, 15(2), 103-108. https://doi.org/10.22467/jwmr.2019.00640.
Zaidi, A., & Green, L. (2019). Physiology of Haemostasis. Anaesthesia and Intensive Care Medicine, 20(3), 152–158. https://doi.org/10.1016/j.mpaic.2019.01.005.
Zhou, S., Wang, W., Zhou, S., Zhang, G., He, J., & Li, Q. (2019). A Novel Model for Cutaneous Wound Healing and Scarring in the Rat. Plastic and Reconstructive Surgery. 2019;143(2):468–477. https://doi.org/10.1097/PRS.0000000000005274.
Zhu, Z., Ding, J., Shankowsky, H. A., & Tredget, E.E. (2013). The Molecular Mechanism of Hypertrophic Scar. Journal of Cell Communication and Signaling, 7(4), 239–252. https://doi.org/10.1007/s12079-013-0195-5.
Benito-Martínez, S., Pérez-Köhler, B., Rodríguez, M., Izco, J. M., Recalde, J.I., & Pascual, G. (2022). Wound Healing Modulation through the Local Application of Powder Collagen-Derived Treatments in an Excisional Cutaneous Murine Model. Biomedicines, 10(5), 960. https://doi.org/10.3390/biomedicines10050960
Boniakowski, A. E., Kimball, A. S., Jacobs, B. N. , Kunkel, S. L., & Gallagher, K. A. (2017). Macrophage-Mediated Inflammation in Normal and Diabetic Wound Healing. The Journal of Immunology : Official Journal of The American Association of Immunologists, 199(1), 17–24. https://doi.org/10.4049/jimmunol.1700223.
Brauer, E., Lippens, E., Klein, O., Nebrich, G., Schreivogel, S., Korus, G., Duda, G. N., & Petersen, A. (2019). Collagen Fibrils Mechanically Contribute to Tissue Contraction in an In Vitro Wound Healing Scenario. Advanced Science, 6(9), 1801780. https://doi.org/10.1002/advs.201801780.
Brianezi, G., Grandi, F., Bagatin, E., Enokihara, M. M. S. S., & Miot, H. A. (2015). Dermal type I collagen assessment by digital image analysis. Anais Brasileiros De Dermatologia, 90(5), 723–727. https://doi.org/10.1590/abd1806-4841.20153331.
Brien, P., De Anda C., Prokocimer, P. (2014) Comparison of Digital Planimetry and Ruler Technique to Measure ABSSSI Lesion Sizes in the ESTABLISH-1 Study.Surgical Infection. 15, 2. https://doi.org/10.1089/sur.2013.070.
Brook, I. (1995). Microbiology of Gastrostomy Site Wound Infections in Children. Journal of Medical Microbiology, 43(3), 221–223. https://doi.org/10.1099/00222615-43-3-221.
Caetano, G. F., Fronza, M., Leite, M. N., Gomes, A., & Frade, M. A. C. (2016). Comparison of collagen content in skin wounds evaluated by biochemical assay and by computer-aided histomorphometric analysis. Pharmaceutical Biology, 54 (11), 2555–2559. https://doi.org/0.3109/13880209.2016.1170861.
Caley, M.P., Martins, V. L. C., O’Toole, E.A. (2015). Metalloproteinases and Wound Healing. Advances in Wound Care, 4(4), 225–234. https://doi.org/10.1089/wound.2014.0581.
Chen, W.T. (1992). Membrane Proteases: Roles In Tissue Remodeling And Tumour Invasion. Current Opinion In Cell Biology, 4(5), 802–809. https://doi.org/10.1016/0955-0674(92)90103-j.
Chen, Y., Yu, Q., & Xu, C. B. (2017). A Convenient Method For Quantifying Collagen Fibers in Atherosclerotic Lesions by Image J Software. International Journal of Clinical and Experimental Medicine, 10(10), 14904–14910.
Chlipala, E., Bendzinski, C. M., Chu, K., Johnson, J. I., Brous, M., Copeland, K., & Bolon, B. (2020). Optical density-based image analysis method for the evaluation of hematoxylin and eosin staining precision. Journal of Histotechnology., 43(1), 29–37. https://doi.org/10.1080/01478885.2019.1708611.
Clark, R. A. F. (2003). Fibrin Is a Many Splendored Thing. Journal of Investigative Dermatology, 121(5), 21-22. https://doi.org/10.1046/j.1523-1747.2003.12575.x.
Clemons, T. D., Bradshaw, M., Toshniwal, P., Chaudari, N., Stevenson, A., Lynch, J., Fear, M. W., Wood, F. M., & Iyer, K. S. (2018). Coherency Image Analysis To Quantify Collagen Architecture: Implications in Scar Assessment. RSC Advances, 8(18), 9661-9669. https://doi.org/10.1039/C7RA12693J.
Cognasse, F., Hamzeh, H., Chavarin, P., Acquart, S., Genin, C., & Garraud, O. (2005). Evidence Of Toll-Like Receptor Molecules On Human Platelets. Immunology and Cell Biology, 83(2), 196–198. https://doi.org/10.1111/j.1440-1711.2005.01314.x.
Desmouliere, A., Redard, M., Darby, I., & Gabbiani, G. (1995). Apoptosis Mediates The Decrease In Cellularity During The Transition Between Granulation Tissue And Scar. The American Journal Of Pathology, 146(1), 56–66.
Dhane, D. M., Maiti, M., Mungle, T., Bar, C., Achar, A., Kolekar, M., Chakraborty, C., (2017). Fuzzy Spectral Clustering For Automated Delineation Of Chronic Wound Region Using Digital Images. Computer in Biology and Medicine, 2017; 89, 551-560. http://dx.doi.org/10.1016/j.compbiomed.2017.04.004
Dhane, D. M., Khrisna, V., Achar A., Bar, C., Sanyal, K., Chakraborty, C. (2016). Spectral Clustering for Unsupervised Segmentation of Lower Extremity Wound Beds Using Optical Images. Journal of Medical System, 2016;40(9), 207. https://doi.org/10.1007/s10916-016-0554-x
Djatumurti, D. R., Rafida, A., Manalu, A. Y. P., & Pangestiningsih, T. W. (2021). Re-epithelization and Density of Collagen Fibers on Wound Healing of Mice’s Skin (Mus musculus) That Treated with Combination of Chitosan Membrane and Eel (Monopterus albus) Mucous. BIO Web of Conferences, 33, 06005. https://doi.org/10.1051/bioconf/20213306005.
Dong, Y., Weidong, Z., Lei, X., Luo, X., Xiang, Q., Zhu, X., Pan, Q., Jin, P., & Cheng, B. (2022). Treatment of Acute Wounds With Recombinant Human-Like Collagen and Recombinant Human-Like Fibronectin in C57BL/6 Mice Individually or in Combination. Frontiers in Bioengineering and Biotechnology, 10, 908585. https://doi.org/10.3389/fbioe.2022.908585.
Duong, T. E., & Hagood, J. S. (2018). Epigenetic Regulation of Myofibroblast Phenotypes in Fibrosis. Current Pathobiology Reports, 6(1), 79–96. https://doi.org/10.1007/s40139-018-0155-0.
Enoch, S., & Leaper, D. J. (2008). Basic Science Of Wound Healing. Surgery, 23(2), 37–42. https://doi.org/10.1383/surg.23.2.37.60352
Filko, D., Nyarko, E. K. (2023). 2D/3D Wound Segmentation and Measurement Based on a Robot-Driven Reconstruction System. Sensors, 23(6), 1-23. https://doi.org/10.3390/s23063298
Folkman, J., & D’Amore, P. A. (1996). Blood vessel formation: What is its molecular basis? Cell, 87(7), 1153–1155. https://doi.org/10.1016/s0092-8674(00)81810-3
Foltynski, P., Ladyzynski P., Ciechanowska, A., Migalska-Musial, K., Judzewicz, G., Sabalinska, S. (2015). Wound Area Measurement with Digital Planimetry: Improved Accuracy and Precision with Calibration Based on 2 Rulers. PLoS ONE, 10(8), 1-13. https://doi.org/10.1371/journal.pone.0134622
Gnyawali, S., C., Sinha, M., El Masry, M., S., Wulff, B., Ghatak, S., Soto-Gonzalez, F., Wilgus, T., A., Roy, S., Sen, C., K. (2020). High Resolution Ultrasound Imaging For Repeated Measure Of Wound Tissue Morphometry, Biomechanics And Hemodynamics Under Fetal, Adult And Diabetic Conditions. PLoS ONE, 15(11), 1-23. https://doi.org/10.1371/journal.pone.0241831
Golebiewska, E. M., & Poole, A. W. (2015). Platelet Secretion: From Haemostasis To Wound Healing And Beyond. Blood Reviews, 2015;29(3), 153- 162. https://doi.org/10.1016/j.blre.2014.10.003
Golebiewska, E. M., & Poole, A.W. (2015). Platelet Secretion: From Haemostasis to Wound Healing and Beyond. Blood Reviews, 29(3), 153–162. https://doi.org/10.1016/j.blre.2014.10.003.
Guo, S., & DiPietro, L. A. (2010). Critical review in oral biology & medicine: Factors affecting wound healing. Journal of Dental Research, 89(3), 219–229. https://doi.org/10.1177/0022034509359125.
Gurtner, G. C., Werner, S., Barrandon,Y., & Longaker, M. T. (2008). Wound repair and regeneration. Nature, 453(7193), 314–321. https://doi.org/10.1038/nature07039.
Ho, J.K., & Hantash, B.M. (2013). The principles of wound healing. Expert Review of Dermatology, 8(6), 639–658. https://doi.org/10.1586/17469872.2013.857161.
Huang, C., Wu, Z., Du, Y., & Ogawa, R. (2020). The Epidemiology of Keloids. In Textbook on Scar Management (pp. 20). Springer, Cham.
Huang, S.P. Wu, M., Shun, C., Wang, H., Hsieh, C., Kuo, M, & Lin, J. (2005). Cyclooxygenase-2 Increases Hypoxia-Inducible Factor-1 And Vascular Endothelial Growth Factor To Promote Angiogenesis In Gastric Carcinoma. Journal of Biomedical Science, 12(1), 229–241. https://doi.org/10.1007/s11373-004-8177-5
Jin, J., Li, H., Chen, Z., Sheng, J., Liu, T., Ma, B., Zhu, S., Xia, Z. (2018). 3-D Wound Scanner: A Novel, Effective, Reliable, And Convenient Tool For Measuring Scar Area. Burns. 44(8), 1930-1939. https://doi.org/10.1016/j.burns.2018.05.009
Jørgensen, L. B., Halekoh, U., Jemec G. B. E., Sørensen, J. A., Yderstræde, K. B. (2020) Monitoring Wound Healing of Diabetic Foot Ulcers Using Two-Dimensional and Three-Dimensional Wound Measurement Techniques: A Prospective Cohort Study. Adv Wound Care (New Rochelle), 9(10), 554–555. https://doi.org/10.1089/wound.2019.1000
Kanitakis, J. (2002). Anatomy, histology and immunohistochemistry of normal human skin. European Journal Of Dermatology, 12(4), 390–401.
Kanitakis, J. (2013). Keloidal Dermatofibroma: Report of A Rare Dermatofibroma Variant in a Young White Woman. The American Journal of Dermatopathology, 35(3), 400-401. https://doi.org/10.1097/DAD.0b013e31825d9d30.
Khorasani, H., Zheng, Z., Nguyen, C., Zara, J., Zhang, X., Wang, J., Ting, K. & Soo, C. (2011). A Quantitative Approach to Scar Analysis. American Journal of Pathology, 178(2), 621–628. https://doi.org/10.1016/j.ajpath.2010.10.019.
Limandjaja, G. C., Van den Broek, L. J., Waaijman, T., Van Veen, H. A., Everts, V., Monstrey, S., Scheper, R. J., Niessen, F. B., & Gibbs, S., (2017). Increased epidermal thickness and abnormal epidermal differentiation in keloid scars. The British Journal Of Dermatology, 176(1), 116–126. https://doi.org/10.1111/bjd.14844
Mahbod, A., Ecker, R., Schaefer, G., Ellinger, I., 2021. Automatic Foot Ulcer Segmentation Using an Ensemble of Convolutional Neural Networks. https://doi.org/10.48550/arXiv.2109.01408
Mathew-Steiner, S. S., Roy, S., & Sen, C. K. (2021). Collagen in Wound Healing. Bioengineering, 8(5), 63. https://doi.org/10.3390/bioengineering8050063
Matsumoto, M., Nakagami, G., Kitamura, A., Kurita M., Suga, H., Miyake, T., Kawamoto, A., Sanada, H. (2021). Ultrasound Assessment of Deep Tissue On The Wound Bed And Periwound Skin: A Classification System Using Ultrasound Images. Journal of Tissue Viability, 30(1), 28-35. https://doi.org/10.1016/j.jtv.2020.08.002.
McGibbon, D. (2005). Rook’s Textbook of Dermatology, 7th editionClinical and Experimental Dermatology, 31(1), 178–179. https://doi.org/10.1111/j.1365-2230.2005.02034.x.
McGrath, J. A. (2020). The structure and function of skin. In McKee’s Pathology of The Skin With Clinical Correlations, 5th edition, volume 1 (pp. 26). Elsevier, Edinburgh
Moulin, V., Larochelle, S., Langlois, C., Thibault, I., Lopez-Vallé, C. A., & Roy, M. (2004). Normal Skin Wound and Hypertrophic Scar Myofibroblasts Have Differential Responses to Apoptotic Inductors. Journal of Cellular Physiology, 198(3), 350–358. https://doi.org/10.1002/jcp.10415.
Murphy, P. S., & Evans, G. R. D. (2012). Advances in Wound Healing: A Review of Current Wound Healing Products. Plastic Surgery International, 2012, 190436. https://doi.org/10.1155/2012/190436.
Naik, S., Bouladoux, N., Linehan, J. L., Han, S., Harrison, O. J., Wilhelm, C., Conlan, S., Himmelfarb, S., Byrd, A. L., Deming, C., Quinones, M., Brenchley, J. M., Kong, H. H., Tussiwand, R., Murphy, K. M., Merad. M., Segre, J. A., & Belkaid, Y. (2015). Commensal-Dendritic-Cell Interaction Specifies A Unique Protective Skin Immune Signature. Nature, 520(7545), 104-108. https://doi.org/10.1038/nature14052.
Osman, O. S., Selway, J. L., Harikumar, P.E., Jassim, S., & Langlands, K. (2014). Automated Analysis of Collagen Histology in Ageing Skin. Proceedings of The International Conference on Bioimaging (Bioimaging 2014), 41-48 https://doi.org/10.5220/0004786600410048.
Owczarzy, A., Kurasiński, R., Kulig, K., Rogóż, W., Szkudlarek, A., & Maciążek-Jurczyk, M. (2020). Collagen-structure properties and application. Engineering of Biomaterials, 2020(156), 17-23. https://doi.org/10.34821/eng.biomat.156.2020.17-23.
Petrov, V. V., Fagard, R. H., & Lijnen, P. J. (2002). Stimulation of Collagen Production by Transforming Growth Factor-Β1 During Differentiation of Cardiac Fibroblasts to Myofibroblasts. Hypertension,39(2), 258–263. https://doi.org/10.1161/hy0202.103268.
Pfisterer, K., Shaw, L. E., Symmank, D., & Weninger, W. (2021). The Extracellular Matrix in Skin Inflammation and Infection. Frontiers In Cell and Developmental Biology, 9, 682414. https://doi.org/10.3389/fcell.2021.682414.
Potekaev, N. N., Borzkyh, O. B., Medvedev, G. V., Pushkin, D. V., Petrova, M. M., Gavrilyuk, O. A., Karpova, E. I., Trefilova, V. V., Deminas, O. M., Popova, T. E. & Shanayder, N. A. (2021). Genetic and Epigenetic Aspects of Skin Collagen Fiber Turnover and Functioning. Cosmetics, 8(4), 92. https://doi.org/10.3390/cosmetics8040092.
Quan, T., & Fisher, G. J. (2015). Role of Age-Associated Alterations of The Dermal Extracellular Matrix Microenvironment in Human Skin Aging: A Mini-Review. Gerontology. 2015;61(5), 427–434. https://doi.org/10.1159/000371708.
Rangaraj, A., Harding, K., & Leaper, D. (2011). Role of Collagen in Wound Management. Wounds UK, 7(2), 54–63.
Rezakhaniha, R., Agianniotis, A., Schrauwen, J. T. C., Griffa, A., Sage, D., Bouten, C. V. C., Van de Vosse, F. N., Unser, M., & Stergiopulos, N. (2012). Experimental Investigation of Collagen Waviness and Orientation in The Arterial Adventitia Using Confocal Laser Scanning Microscopy. Biomechanics and Modeling in Mechanobiology, 11(3-4):461–473. https://doi.org/10.1007/s10237-011-0325-z.
Rodrigues, M., Kosaric, N., Bonham, C. A., & Gurtner, G.C. (2019). Wound healing: A cellular perspective. Physiological Reviews, 99(1), 665–706. https://doi.org/10.1152/physrev.00067.2017.
Sabol, F., Dancakova, L, Gál, P. Vasilenko, T., Novotny, M., Smetana, K., & Lenhards, L. (2012) Immunohistological Changes in Skin Wounds During The Early Periods of Healing in a Rat Model. Veterinarni Medicina, 57, 77–82. https://doi.org/10.17221/5253-VETMED
Senejko, M., Pasek, J., Szajkowski, S., Cieślar, G., Sieroń, A. (2021). Evaluation Of The Therapeutic Efficacy Of Active Specialistic Medical Dressings In The Treatment Of Decubitus. Postepy Dermatologii i Alergologii, 38(1), 75-79. https://doi.org/10.5114/ada.2021.104282
Setiawati, A., Jang, D., Cho, D., Cho, S., Jeong, H., Park, S., Gwak, J., Ryu, S. R., Jung, W. H., Ju, B., Jung, K., Kwon, O., & Shin, K. (2021). An Accelerated Wound-Healing Surgical Suture Engineered with an Extracellular Matrix. Advanced Healthcare Materials, 10(6), 1–10. https://doi.org/10.1002/adhm.202001686.
Singer, A. J., & Clark, R. A. (1999). Cutaneous Wound Healing. The New England Journal of Medicine, 341(10), 738-746. https://doi.org/10.1056/NEJM199909023411006.
Somaiah, C., Kumar, A., Mawrie, D., Sharma, A., Patil, S. D., Bhattacharyya, J., Swaminathan, R., & Jaganathan, B. G. (2015). Collagen Promotes Higher Adhesion, Survival And Proliferation Of Mesenchymal Stem Cells. PLoS One, 10(120), 1–15. https://doi.org/10.1371/journal.pone.0145068.
Takeo, M., Lee, W., & Ito, M. (2015). Wound healing and skin regeneration. Cold Spring Habour Perspective in Medicine, ;5:a023267. https://doi.org/10.1101/cshperspect.a023267.
Tang, Y. Q., Yeaman, M. R., & Selsted, M.E. (2002). Antimicrobial Peptides from Human Platelets. Infection and Immunity, 70(12), 6524–6533. https://doi.org/10.1128/IAI.70.12.6524-6533.2002.
Theocharis, A. D., Skandalis, S. S., Gialeli, C., & Karamanos, N. K. (2016). Extracellular Matrix Structure. Advanced Drug Delivery Reviews, 1(97), 4–27. htps://doi.org/10.1016/j.addr.2015.11.001.
Velez, A. M. A, & Howard, M. S. (2012). Collagen IV in Normal and in Disease Process. North American Journal of Medical Sciences, 4(1), 1–8. https://doi.org/10.4103/1947-2714.92892.
Velnar, T., Bailey, T., & Smrkolj, V. (2009). The wound healing process: An overview of the cellular and molecular mechanisms. The Journal of International Medical Research, 37(5), 1528–1542. https://doi.org/10.1177/147323000903700531.
Verhaegen, P. D. H. M, Van Zujilen, P. P. M., Pennings, N. M., Van Marle, J., Niessen, F. B., Van der Horst, C. M. A. M., & Middelkoop, E. (2009). Differences in Collagen Architecture Between Keloid, Hypertrophic Scar, Normotrophic Scar, and Normal Skin: An Objective Histopathological Analysis. Wound Repair And Regeneration: Official Publication of The Wound Healing Society [and] The European Tissue Repair Society, 17(5), 649–656. https://doi.org/10.1111/j.1524-475X.2009.00533.x.
Wang, H. (2021). A Review of The Effects of Collagen Treatment in Clinical Studies. Polymers, 13(22), 3868. https://doi.org/10.3390/polym13223868
Wang, C., Anisuzzaman, D., M., Williamson, V., Dhar, M., K., Rostami, B., Niezgoda, J., Gopalakrishnan, S., Zeyun, Y. (2020). Fully Automatic Wound Segmentation With Deep Convolutional Neural Networks. Scientific Reports, 10(1), 1-9. https://doi.org/10.1038/s41598-020-78799-w
Wershof, E., Park, D., Barry, D. J., Jenkins, R. P., Rulan, A., Wilkins, A., Schlegelmilch, K, Roxanis, I, Anderson, K. I., Bates, P. A., & Sahai, E. (2021). A FIJI Macro for Quantifying Pattern in Extracellular Matrix. Life Science Alliance, 4(3), 1–11. https://doi.org/10.26508/lsa.202000880.
Whittaker, P., Kloner, R. A., Boughner, D. R., & Pickering, J. G. (1994). Quantitative Assessment of Myocardial Collagen with Picrosirius Red Staining and Circularly Polarized Light. Basic Res Cardiol. 89(5), 397–410. https://doi.org/10.1007/BF00788278
Wilkinson, H. N., & Hardman, M. J. (2020). Wound Healing: Cellular Mechanisms And Pathological Outcomes. Open Biology, 10. 200223. https://doi.org/10.1098/rsob.200223.
Wolfram, D., Tzankov, A., Pülzl, P., & Piza-Katzer, H. (2009). Hypertrophic Scars and Keloids - A Review of Their pathophysiology, Risk Factors, and Therapeutic Management. Dermatologic Surgery: Official Publication For American Society For Dermatologic Surgery, 35(2), 171-181. https://doi.org/171–181. 10.1111/j.1524-4725.2008.34406.x.
Xue, M., & Jackson, C. J. (2015). Extracellular Matrix Reorganization During Wound Healing and Its Impact on Abnormal Scarring. Advances in Wound Care, 4(3), 119–136. https://doi.org/10.1089/wound.2013.0485.
Yang, H. J., & Kang, S.Y. (2019). The Clinical Uses of Collagen-Based Matrices in the Treatment of Chronic Wounds. Journal of Wound Management and Research, 15(2), 103-108. https://doi.org/10.22467/jwmr.2019.00640.
Zaidi, A., & Green, L. (2019). Physiology of Haemostasis. Anaesthesia and Intensive Care Medicine, 20(3), 152–158. https://doi.org/10.1016/j.mpaic.2019.01.005.
Zhou, S., Wang, W., Zhou, S., Zhang, G., He, J., & Li, Q. (2019). A Novel Model for Cutaneous Wound Healing and Scarring in the Rat. Plastic and Reconstructive Surgery. 2019;143(2):468–477. https://doi.org/10.1097/PRS.0000000000005274.
Zhu, Z., Ding, J., Shankowsky, H. A., & Tredget, E.E. (2013). The Molecular Mechanism of Hypertrophic Scar. Journal of Cell Communication and Signaling, 7(4), 239–252. https://doi.org/10.1007/s12079-013-0195-5.
Published
2024-06-10
How to Cite
Santoso, C. N., Widyantara, K. A., Kencana, N. B. W., Setyajati, F. D. E., & Setiawati, A. (2024). Advances in Quantitative and Qualitative Assessment of Collagen in Cutaneous Wound Healing. Indonesian Journal of Pharmacy, 35(2), 194-210. https://doi.org/10.22146/ijp.9773
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Section
Review Article
