Evaluation of the effects of clearing agents, fixation, and process durations on cardiovascular tissue imaging with second harmonic generation and multi-photon modalities

IntroductionProtocols for tissue clearing have been established and optimized for the central nervous system. However, significant modifications are required for clearing different tissue types. Therefore, effective optical clearing for cardiovascular tissue remains a major challenge. The goal of th...

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Main Authors: Maedeh Makki, Zachary A. Molander, Sergio A. Pineda-Castillo, Devin W. Laurence, Shubhra Singhal, Yasmin Eltwafsha, Gerhard A. Holzapfel, Tingting Gu, Chung-Hao Lee
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Language:English
Published: Frontiers Media S.A. 2025-07-01
Series:Frontiers in Bioengineering and Biotechnology
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Online Access:https://www.frontiersin.org/articles/10.3389/fbioe.2025.1606425/full
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author Maedeh Makki
Zachary A. Molander
Sergio A. Pineda-Castillo
Devin W. Laurence
Shubhra Singhal
Yasmin Eltwafsha
Gerhard A. Holzapfel
Gerhard A. Holzapfel
Tingting Gu
Chung-Hao Lee
author_facet Maedeh Makki
Zachary A. Molander
Sergio A. Pineda-Castillo
Devin W. Laurence
Shubhra Singhal
Yasmin Eltwafsha
Gerhard A. Holzapfel
Gerhard A. Holzapfel
Tingting Gu
Chung-Hao Lee
author_sort Maedeh Makki
collection DOAJ
description IntroductionProtocols for tissue clearing have been established and optimized for the central nervous system. However, significant modifications are required for clearing different tissue types. Therefore, effective optical clearing for cardiovascular tissue remains a major challenge. The goal of this study is to better understand the responses of porcine left anterior descending artery (LADA) to label-free multiphoton imaging.MethodsTo this end, the effects of different clearing methods (i.e., benzyl alcohol benzyl benzoate–BABB and glycerol), formalin fixation, variations in formalin fixation times (0–240 min), and extended storage in BABB (up to 14 days) are investigated. We compare tissue characteristics under different conditions (e.g., tissue clearing reagent and/or tissue fixation), particularly with regard to tissue preservation and transparency across z-stacks (i.e., imaging depths).ResultsThe glycerol clearing method exhibited relatively lower tissue transparency, whereas BABB increased mean AF-AUC from 0.0035 ± 0.0009 to 0.1205 ± 0.0168 and SHG-AUC from 0.0003 ± 0.0002 to 0.0072 ± 0.0040 (p< 0.001), enabling robust signal intensities at deeper layers of LADA tissue. In addition, we observed that BABB preserves fluorescent signals even after extended tissue storage with no significant loss in integrity over 14 days. Finally, we found that formalin fixation in combination with the glycerol clearing method significantly improved tissue preservation compared to the glycerol clearing method alone. However, in combination with the BABB clearing method, fixation reduced tissue transparency and signal intensity compared to BABB clearing without fixation.DiscussionThese findings establish BABB as the superior, label-free clearing agent for deep 3D multiphoton microscopy/second harmonic generation imaging of cardiovascular tissue and underscore the necessity of tailoring fixation parameters to the chosen clearing method.
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spelling doaj-art-9d2be43dd0bd4818a8d315de5b0a65522025-08-20T03:13:38ZengFrontiers Media S.A.Frontiers in Bioengineering and Biotechnology2296-41852025-07-011310.3389/fbioe.2025.16064251606425Evaluation of the effects of clearing agents, fixation, and process durations on cardiovascular tissue imaging with second harmonic generation and multi-photon modalitiesMaedeh Makki0Zachary A. Molander1Sergio A. Pineda-Castillo2Devin W. Laurence3Shubhra Singhal4Yasmin Eltwafsha5Gerhard A. Holzapfel6Gerhard A. Holzapfel7Tingting Gu8Chung-Hao Lee9Biomechanics and Biomaterials Design Laboratory (BBDL), Department of Bioengineering, The University of California, Riverside (UCR), Riverside, CA, United StatesBiomechanics and Biomaterials Design Laboratory (BBDL), Department of Bioengineering, The University of California, Riverside (UCR), Riverside, CA, United StatesDepartment of Biomedical Engineering, University of Minnesota, Minneapolis, MN, United StatesDepartment of Anesthesiology and Critical Care, Children’s Hospital of Philadelphia (CHOP), Philadelphia, PA, United StatesBiomechanics and Biomaterials Design Laboratory (BBDL), Department of Bioengineering, The University of California, Riverside (UCR), Riverside, CA, United StatesBiomechanics and Biomaterials Design Laboratory (BBDL), Department of Bioengineering, The University of California, Riverside (UCR), Riverside, CA, United StatesInstitute of Biomechanics, Graz University of Technology, Graz, AustriaDepartment of Structural Engineering, Norwegian University of Science and Technology (NTNU), Trondheim, NorwaySchool of Biological Sciences, The University of Oklahoma, Norman, OK, United StatesBiomechanics and Biomaterials Design Laboratory (BBDL), Department of Bioengineering, The University of California, Riverside (UCR), Riverside, CA, United StatesIntroductionProtocols for tissue clearing have been established and optimized for the central nervous system. However, significant modifications are required for clearing different tissue types. Therefore, effective optical clearing for cardiovascular tissue remains a major challenge. The goal of this study is to better understand the responses of porcine left anterior descending artery (LADA) to label-free multiphoton imaging.MethodsTo this end, the effects of different clearing methods (i.e., benzyl alcohol benzyl benzoate–BABB and glycerol), formalin fixation, variations in formalin fixation times (0–240 min), and extended storage in BABB (up to 14 days) are investigated. We compare tissue characteristics under different conditions (e.g., tissue clearing reagent and/or tissue fixation), particularly with regard to tissue preservation and transparency across z-stacks (i.e., imaging depths).ResultsThe glycerol clearing method exhibited relatively lower tissue transparency, whereas BABB increased mean AF-AUC from 0.0035 ± 0.0009 to 0.1205 ± 0.0168 and SHG-AUC from 0.0003 ± 0.0002 to 0.0072 ± 0.0040 (p< 0.001), enabling robust signal intensities at deeper layers of LADA tissue. In addition, we observed that BABB preserves fluorescent signals even after extended tissue storage with no significant loss in integrity over 14 days. Finally, we found that formalin fixation in combination with the glycerol clearing method significantly improved tissue preservation compared to the glycerol clearing method alone. However, in combination with the BABB clearing method, fixation reduced tissue transparency and signal intensity compared to BABB clearing without fixation.DiscussionThese findings establish BABB as the superior, label-free clearing agent for deep 3D multiphoton microscopy/second harmonic generation imaging of cardiovascular tissue and underscore the necessity of tailoring fixation parameters to the chosen clearing method.https://www.frontiersin.org/articles/10.3389/fbioe.2025.1606425/fullcardiovascular tissueleft anterior descending arterysecond harmonic generation imagingmulti-photon imagingbenzyl alcohol benzyl benzoate (BABB) clearingformalin fixation
spellingShingle Maedeh Makki
Zachary A. Molander
Sergio A. Pineda-Castillo
Devin W. Laurence
Shubhra Singhal
Yasmin Eltwafsha
Gerhard A. Holzapfel
Gerhard A. Holzapfel
Tingting Gu
Chung-Hao Lee
Evaluation of the effects of clearing agents, fixation, and process durations on cardiovascular tissue imaging with second harmonic generation and multi-photon modalities
Frontiers in Bioengineering and Biotechnology
cardiovascular tissue
left anterior descending artery
second harmonic generation imaging
multi-photon imaging
benzyl alcohol benzyl benzoate (BABB) clearing
formalin fixation
title Evaluation of the effects of clearing agents, fixation, and process durations on cardiovascular tissue imaging with second harmonic generation and multi-photon modalities
title_full Evaluation of the effects of clearing agents, fixation, and process durations on cardiovascular tissue imaging with second harmonic generation and multi-photon modalities
title_fullStr Evaluation of the effects of clearing agents, fixation, and process durations on cardiovascular tissue imaging with second harmonic generation and multi-photon modalities
title_full_unstemmed Evaluation of the effects of clearing agents, fixation, and process durations on cardiovascular tissue imaging with second harmonic generation and multi-photon modalities
title_short Evaluation of the effects of clearing agents, fixation, and process durations on cardiovascular tissue imaging with second harmonic generation and multi-photon modalities
title_sort evaluation of the effects of clearing agents fixation and process durations on cardiovascular tissue imaging with second harmonic generation and multi photon modalities
topic cardiovascular tissue
left anterior descending artery
second harmonic generation imaging
multi-photon imaging
benzyl alcohol benzyl benzoate (BABB) clearing
formalin fixation
url https://www.frontiersin.org/articles/10.3389/fbioe.2025.1606425/full
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