The first full body diffusible iodine-based contrast-enhanced computed tomography dataset and teaching materials for a member of the Testudines.

3D imaging 3D modeling Testudines computed tomography diceCT natural history reptile

Journal

Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775

Informations de publication

Date de publication:
06 Jul 2023
Historique:
revised: 08 06 2023
received: 11 05 2023
accepted: 14 06 2023
medline: 6 7 2023
pubmed: 6 7 2023
entrez: 6 7 2023
Statut: aheadofprint

Résumé

Diffusible iodine-based contrast-enhanced Computed Tomography (diceCT) is now a widely used technique for imaging metazoan soft anatomy. Turtles present a particular challenge for anatomists; gross dissection is inherently destructive and irreversible, whereas their near complete shell of bony plates, covered with keratinous scutes, presents a barrier for iodine diffusion and significantly increases contrast-enhanced CT preparation time. Consequently, a complete dataset visualizing the internal soft anatomy of turtles at high resolution and in three dimensions has not yet been successfully achieved. Here we outline a novel method that augments traditional diceCT preparation with an iodine injection technique to acquire the first full body contrast-enhanced dataset for the Testudines. We show this approach to be an effective method of staining the soft tissues inside the shell. The resulting datasets were processed to produce anatomical 3D models that can be used in teaching and research. As diceCT becomes a widely employed method for nondestructively documenting the internal soft anatomy of alcohol preserved museum specimens, we hope that methods applicable to the more challenging of these, such as turtles, will contribute toward the growing stock of digital anatomy in online repositories.

Identifiants

pubmed: 37409685
doi: 10.1002/ar.25282
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Science Foundation
Organisme : University of Arizona
Organisme : University of Florida
Organisme : oVert project
ID : NSF DBI-1701714

Informations de copyright

© 2023 American Association for Anatomy.

Références

Akpan, J., & Strayer, J. (2010). Which comes first the use of computer simulation of frog dissection or conventional dissection as academic exercise? Journal of Computers in Mathematics and Science Teaching, 29(2), 113-138.
Boyer, D. M., Gunnell, G. F., Kaufman, S., & McGeary, T. M. (2016). Morphosource: Archiving and sharing 3-d digital specimen data. The Paleontological Society Papers, 22, 157-181.
Broeckhoven, C., El Adak, Y., Hui, C., Van Damme, R., & Stankowich, T. (2018). On dangerous ground: The evolution of body Armour in cordyline lizards. Proceedings of the Royal Society B, 285(1880), 20180513.
Buser, T. J., Boyd, O. F., Cortés, Á., Donatelli, C. M., Kolmann, M. A., Luparell, J. L., Pfeiffenberger, J. A., Sidlauskas, B. L., & Summers, A. P. (2020). The natural historian's guide to the CT galaxy: Step-by-step instructions for preparing and analyzing computed tomographic (CT) data using cross-platform, open access software. Integrative Organismal Biology, 2(1), obaa009.
Clemann, N., Rowe, K. M. C., Rowe, K. C., Raadik, T., Gomon, M., Menkhorst, P., Sumner, J., Bray, D., Norman, M., & Melville, J. (2014). Value and impacts of collecting vertebrate voucher specimens, with guidelines for ethical data collection. Memoirs of Museum Victoria, 72, 141-151.
Croghan, J. A. (2019). Two turtles, two diets, two biomechanical strategies: Jaw biomechanics in a generalist versus a Durophagous species of Emydid. Society of Integrative and Comparative Biology Abstracts, P1-P27. https://sicb.org/wp-content/uploads/2021/02/2019-SICB-Abstract-Book.pdf
Dawood, Y., Hagoort, J., Siadari, B. A., Ruijter, J. M., Gunst, Q. D., Lobe, N. H. J., Strijkers, G. J., de Bakker, B. S., & van den Hoff, M. J. B. (2021). Reducing soft-tissue shrinkage artefacts caused by staining with Lugol's solution. Scientific Reports, 11(1), 1-12.
Dawood, Y., Hagoort, J., Siadari, B. A., Ruijter, J. M., Gunst, Q. D., Lobe, N. H. J., Strijkers, G. J., de Bakker, B. S., & van den Hoff, M. J. B. (2022). Author correction: Reducing soft-tissue shrinkage artefacts caused by staining with Lugol's solution. Scientific Reports, 12, 2366. https://doi.org/10.1038/s41598-022-06160-4
Early, C. M., Morhardt, A. C., Cleland, T. P., Milensky, C. M., Kavich, G. M., & James, H. F. (2020). Chemical and molecular effects of diffusion-based iodine contrast enhancing stains on fluid-preserved avian specimens. PLoS One, 15(9), e0238783.
Erolin, C. (2019). Interactive 3D digital models for anatomy and medical education. Biomedical Visualisation, 2, 1-6.
Evers, S. W., Neenan, J. M., Ferreira, G. S., Werneburg, I., Barrett, P. M., & Benson, R. B. J. (2019). Neurovascular anatomy of the protostegid turtles Rhinochelys pulchriceps and comparisons of membranous and endosseous labyrinth shape in an extant turtle. Zoological Journal of the Linnean Society, 187, 800-828. https://doi.org/10.1093/zoolinnean.zlz063
Evers, S. W., Ponstein, J., Gray, J. A., Jansen, M. A., & Fröbisch, J. (2022). A systematic compendium of turtle mandibular anatomy using digital dissections of soft tissue and osteology. The Anatomical Record, 306(6), 1228-1303. https://doi.org/10.1002/ar.25037
Ferreira, G. S., Werneburg, I., Lautenschlager, S., & Evers, S. W. (2023). Chapter 4: Contrasting brains and bones: Neuroanatomical evolution of turtles (Testudinata). In M. T. Dozo, A. Paulina-Carabajal, T. E. Macrini, & S. Walsh (Eds.), Paleoneurology of amniotes: New directions in the study of fossil endocasts. Springer. https://doi.org/10.1007/978-3-031-13983-3_4
Forghani, R., De Man, B., & Gupta, R. (2017). Dual-energy computed tomography: physical principles, approaches to scanning, usage, and implementation: part 1. Neuroimaging Clinics. 27(3), 371-84.
Gignac, P. M., & Kley, N. J. (2014). Iodine-enhanced micro-CT imaging: Methodological refinements for the study of the soft-tissue anatomy of post-embryonic vertebrates. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 322(3), 166-176.
Gignac, P. M., Kley, N. J., Clarke, J. A., Colbert, M. W., Morhardt, A. C., Cerio, D., Cost, I. N., Cox, P. G., Daza, J. D., Early, C. M., & Echols, M. S. (2016). Diffusible iodine-based contrast-enhanced computed tomography (diceCT): An emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. Journal of Anatomy, 228(6), 889-909.
Gignac, P. M., O'Brien, H. D., Sanchez, J., & Vazquez-Sanroman, D. (2021). Multiscale imaging of the rat brain using an integrated diceCT and histology workflow. Brain Structure and Function, 226(7), 2153-2168.
Handschuh, S., Natchev, N., Kummer, S., Beisser, C. J., Lemell, P., Herrel, A., & Vergilov, V. (2019). Cranial kinesis in the miniaturised lizard Ablepharus kitaibelii (Squamata: Scincidae). Journal of Experimental Biology, 222(9), jeb198291.
Hedrick, B. P., Heberling, J. M., Meineke, E., Turner, K. G., Grassa, C. J., Park, D., Kennedy, J., Clarke, J., Cook, J., Blackburn, D. C., Edwards, S. V., & Davis, C. C. (2020). Digitization and the future of natural history collections. Bioscience, 70, 243-251.
Holyoak, A. (2022). Dissection of the red-eared turtle. Department of Biology, BYU Idaho. https://www.youtube.com/watch?v=8NgP5Wh5ZRY
Humason, G. L. (1962). Animal Tissue Techniques.
Jones, M. E. H., Werneburg, I., Curtis, N., Penrose, R., O'Higgins, P., Fagan, M. J., & Evans, S. E. (2012). The head and neck anatomy of sea turtles (Cryptodira: Chelonioidea) and skull shape in Testudines. PLoS One, 7(11), e47852.
Joyce, W. G., & Bourque, J. R. (2016). A review of the fossil record of turtles of the clade Pan-Kinosternoidea. Bulletin of the Peabody Museum of Natural History, 57(1), 57-95.
Ketcham, R. A., & Carlson, W. D. (2001). Acquisition, optimization and interpretation of X-ray computed tomographic imagery: Applications to the geosciences. Computational Geosciences, 27, 381-400.
Kinzie, M. B., Strauss, R., & Foss, J. (1993). The effects of an interactive dissection simulation on the performance and achievement of high school biology students. Journal of Research in Science Teaching, 30(8), 989-1000.
Kolmann, M. A., Nagesan, R. S., Andrews, J. V., Borstein, S., Figueroa, R. T., Singer, R., Friedman, M., & López-Fernández, H. (2023). DiceCT for fishes: Recommendations for pairing iodine contrast agents with μCT to visualize soft tissues in fishes. Journal of Fish Biology, 102(4), 893-903.
Liem, K., Bemis, W., Walker, W. F., & Grande, L. (2001). Functional anatomy of the vertebrates: An evolutionary perspective (3rd ed.). Cengage Learning.
Nasoori, A. (2020). Formation, structure, and function of extra-skeletal bones in mammals. Biological Reviews, 95(4), 986-1019.
Perilli, E., Baruffaldi, F., Bisi, M. C., Cristofolini, L., & Cappello, A. (2006). A physical phantom for the calibration of three-dimensional X-ray microtomography examination. Journal of Microscopy, 222(2), 124-134.
Rhodin, A. G. J., Iverson, J. B., Bour, R., Fritz, U., Georges, A., Shaffer, H. B., & Van Dijk, P. P. (2021). Turtles of the world, annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status (9th ed.). Turtle Taxonomy Working Group. Chelonian Research Foundation and Turtle Conservancy.
Ricciardi, M., Franchini, D., Valastro, C., Ciccarelli, S., Caprio, F., Assad, A. E., & Di Bello, A. (2019). Multidetector computed tomographic anatomy of the lungs in the loggerhead sea turtle (Caretta caretta). The Anatomical Record, 302(9), 1658-1665.
Rolfe, S. M., Whikehart, S. M., & Maga, A. M. (2022). Deep learning enabled multi-organ segmentation of mouse embryos. bioRxiv, 26, 2022-08.
Schmidbaur, H., Keklikoglou, K., Metscher, B. D., & Faulwetter, S. (2015). Exploring methods to remove iodine and phosphotungstic acid stains from zoological specimens. Bruker microCT User Mtg Abstracts, 21, 1-8.
Simmons, J. E. (2014). Fluid preservation: A comprehensive reference. Rowman & Littlefield.
Stock SR. Microcomputed tomography: methodology and applications. CRC press; 2018.
Stone, M. D., & Turner, A. J. (2012). Use of dual-energy X-ray absorptiometry (DXA) with non-human vertebrates: Application, challenges, and practical considerations for research and clinical practice. A Birds Eye View of Veterinary Medicine, 100-116. https://doi.org/10.5772/30510
Watkins-Colwell, G. J., Love, K., Randall, Z., Boyer, D. M., Winchester, J. M., Staley, E. L., & Blackburn, D. C. (2018). The walking dead: Status report, data workflow and best practices of the oVertThematic collections network. Biodiversity Information Science and Standards, 2, e26078.
Wolke, R. E., & George, A. (1981). Sea turtle necropsy manual. National Oceanic and Atmospheric Administration. Technical Memorandum NMFS-SEFC-24.
Zheng, H., Motch Perrine, S. M., Pitirri, M. K., Kawasaki, K., Wang, C., Richtsmeier, J. T., & Chen, D. Z. (2020). Cartilage segmentation in high-resolution 3d micro-ct images via uncertainty-guided self-training with very sparse annotation. In Medical image computing and computer assisted intervention-MICCAI 2020: 23rd international conference, Lima, Peru, October 4-8, 2020, Proceedings, Part I 23 (pp. 802-812). Springer International Publishing.

Auteurs

Jaimi A Gray (JA)

Florida Museum of Natural History, Gainesville, Florida, USA.

Paul M Gignac (PM)

University of Arizona, Tucson, Arizona, USA.

Edward L Stanley (EL)

Florida Museum of Natural History, Gainesville, Florida, USA.

Classifications MeSH