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Home / Equine Research Bank / Anat Histol Embryol / An optimized workflow for microCT imaging of formalin-fixed ...
Anatomia, histologia, embryologia2022; 51(5); 611-623; doi: 10.1111/ahe.12834

An optimized workflow for microCT imaging of formalin-fixed and paraffin-embedded (FFPE) early equine embryos.

Abstract: Here, we describe a workflow for high-detail microCT imaging of formalin-fixed and paraffin-embedded (FFPE) equine embryos recovered on Day 34 of pregnancy (E34), a period just before placenta formation. The presented imaging methods are suitable for large animals' embryos with intention to study morphological and developmental aspects, but more generally can be adopted for all kinds of FFPE tissue specimens. Microscopic 3D imaging techniques such as microCT are important tools for detecting and studying normal embryogenesis and developmental disorders. To date, microCT imaging of vertebrate embryos was mostly done on embryos that have been stained with an X-ray dense contrast agent. Here, we describe an alternative imaging procedure that allows to visualize embryo morphology and organ development in unstained FFPE embryos. Two aspects are critical for high-quality data acquisition: (i) a proper sample mounting leaving as little as possible paraffin around the sample and (ii) an image filtering pipeline that improves signal-to-noise ratio in these inherently low-contrast data sets. The presented workflow allows overview imaging of the whole embryo proper and can be used for determination of organ volumes and development. Furthermore, we show that high-resolution interior tomographies can provide virtual histology information from selected regions of interest. In addition, we demonstrate that microCT scanned embryos remain intact during the scanning procedure allowing for a subsequent investigation by routine histology and/or immunohistochemistry. This makes the presented workflow applicable also to archival paraffin-embedded material.
© 2022 The Authors. Anatomia, Histologia, Embryologia published by Wiley-VCH GmbH.
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Publication Date: 2022-07-18 PubMed ID: 35851500PubMed Central: PMC9542120DOI: 10.1111/ahe.12834Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The researchers have developed an optimized workflow for microCT imaging of formalin-fixed and paraffin-embedded (FFPE) early horse embryos. The method is designed to provide high-detailed imaging while maintaining the integrity of the embryos for subsequent analyses.

Research Background and Objective

  • This study presents a method to improve the imaging of horse embryos fixed in formalin and embedded in paraffin, focusing primarily on embryos gathered on the 34th day of pregnancy—a crucial point just before the formation of the placenta.
  • The imaging technique is also designed for use with larger animals’ embryos or generally, any FFPE tissue specimens to examine their morphology and developmental aspects.
  • Microscopic 3D imaging techniques such as microCT are essential in studying normal embryogenesis and developmental disorders.

Improved Imaging Procedure

  • Unlike previous microCT imaging attempts on vertebrate embryos which required staining with an X-ray dense contrast agent, the technique presented here allows visualizing the morphology and organ development in unstained FFPE embryos.
  • The team paid particular attention to two considerations for high-quality data acquisition—minimizing paraffin around the sample and improving the signal-to-noise ratio through image filtering, as FFPE embryos generally produce low-contrast data sets.

Workflow and Applicability

  • The researchers developed and implemented a workflow that aids in capturing a comprehensive imaging of the embryo and assists in analyzing organ volumes and development.
  • High-resolution interior tomographies obtained using this method can also provide valuable ‘virtual histology’ information from selected regions of interest.
  • Another significant advantage of this imaging technique is that the embryos remain intact during the scanning process, thus, enabling them for additional studies using conventional histology or immunohistochemistry methods.
  • This characteristic also allows application of the workflow to archival paraffin-embedded material, hence increasing its versatility and potential uses in research.

Cite This Article

APA
Handschuh S, Okada CTC, Walter I, Aurich C, Glösmann M. (2022). An optimized workflow for microCT imaging of formalin-fixed and paraffin-embedded (FFPE) early equine embryos. Anat Histol Embryol, 51(5), 611-623. https://doi.org/10.1111/ahe.12834

Publication

Anatomia, histologia, embryologia
ISSN: 1439-0264
NlmUniqueID: 7704218
Country: Germany
Language: English
Volume: 51
Issue: 5
Pages: 611-623

Researcher Affiliations

Handschuh, Stephan
  • VetCore Facility for Research/Imaging Unit, University of Veterinary Medicine Vienna, Vienna, Austria.
Okada, Carolina T C
  • Platform Artificial Insemination and Embryo Transfer, Department for Small Animals and Horses, University of Veterinary Medicine Vienna, Vienna, Austria.
Walter, Ingrid
  • VetCore Facility for Research/VetBiobank, University of Veterinary Medicine Vienna, Vienna, Austria.
  • Institute of Morphology, University of Veterinary Medicine Vienna, Vienna, Austria.
Aurich, Christine
  • Platform Artificial Insemination and Embryo Transfer, Department for Small Animals and Horses, University of Veterinary Medicine Vienna, Vienna, Austria.
Glösmann, Martin
  • VetCore Facility for Research/Imaging Unit, University of Veterinary Medicine Vienna, Vienna, Austria.

MeSH Terms

  • Animals
  • Formaldehyde
  • Horses
  • Paraffin Embedding / veterinary
  • Tissue Fixation / veterinary
  • Vertebrates
  • Workflow
  • X-Ray Microtomography / methods
  • X-Ray Microtomography / veterinary

Grant Funding

  • University of Veterinary Medicine Vienna

References

This article includes 81 references
  1. Acker DA, Curran S, Bersu ET, Ginther OJ. Morphologic stages of the equine embryo proper on days 17 to 40 after ovulation.. Am J Vet Res 2001 Sep;62(9):1358-64.
    doi: 10.2460/ajvr.2001.62.1358pubmed: 11560260google scholar: lookup
  2. Aurich C, Budik S. Early pregnancy in the horse revisited - does exception prove the rule?. J Anim Sci Biotechnol 2015;6:50.
    doi: 10.1186/s40104-015-0048-6pmc: PMC4668677pubmed: 26635959google scholar: lookup
  3. Bergfelt DR, Woods JA, Ginther OJ. Role of the embryonic vesicle and progesterone in embryonic loss in mares.. J Reprod Fertil 1992 Jul;95(2):339-47.
    doi: 10.1530/jrf.0.0950339pubmed: 1517992google scholar: lookup
  4. Bergin WC. Developmental horizons and measurements useful for age determination of equine embryos and fetuses. .
  5. Betteridge KJ, Waelchli RO, Christie HL, Raeside JI, Quinn BA, Hayes MA. Relationship between the timing of prostaglandin-induced luteolysis and effects on the conceptus during early pregnancy in mares.. Reprod Fertil Dev 2012;24(3):411-24.
    doi: 10.1071/RD11132pubmed: 22401273google scholar: lookup
  6. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography.. J Bone Miner Res 2010 Jul;25(7):1468-86.
    doi: 10.1002/jbmr.141pubmed: 20533309google scholar: lookup
  7. Buie HR, Campbell GM, Klinck RJ, MacNeil JA, Boyd SK. Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis.. Bone 2007 Oct;41(4):505-15.
    doi: 10.1016/j.bone.2007.07.007pubmed: 17693147google scholar: lookup
  8. Busse M, Müller M, Kimm MA, Ferstl S, Allner S, Achterhold K, Herzen J, Pfeiffer F. Three-dimensional virtual histology enabled through cytoplasm-specific X-ray stain for microscopic and nanoscopic computed tomography.. Proc Natl Acad Sci U S A 2018 Mar 6;115(10):2293-2298.
    doi: 10.1073/pnas.1720862115pmc: PMC5877988pubmed: 29463748google scholar: lookup
  9. Cnudde V, Masschaele B, De Cock HE, Olstad K, Vlaminck L, Vlassenbroeck J, Dierick M, Witte YD, Van Hoorebeke L, Jacobs P. Virtual histology by means of high-resolution X-ray CT.. J Microsc 2008 Dec;232(3):476-85.
    doi: 10.1111/j.1365-2818.2008.02142.xpubmed: 19094024google scholar: lookup
  10. de Chiffre L, Carmignato S, Kruth JP, Schmitt R, Weckenmann A. Industrial applications of computed tomography. CIRP Journal of Manufacturing Science and Technology 63(2), 655–677.
    doi: 10.1016/j.cirp.2014.05.011google scholar: lookup
  11. de Mestre AM, Rose BV, Chang YM, Wathes DC, Verheyen KLP. Multivariable analysis to determine risk factors associated with early pregnancy loss in thoroughbred broodmares.. Theriogenology 2019 Jan 15;124:18-23.
    doi: 10.1016/j.theriogenology.2018.10.008pubmed: 30326374google scholar: lookup
  12. Deyhle H, Bikis C, Khimchenko A, Schweighauser G, Hench J, Schulz G, Muller B, Hieber SE. Visualization and Segmentation of Cells in Unstained Paraffin‐Embedded Cerebral Tissue. Microscopy and Microanalysis 24, 408–409.
  13. Dhenain M, Ruffins SW, Jacobs RE. Three-dimensional digital mouse atlas using high-resolution MRI.. Dev Biol 2001 Apr 15;232(2):458-70.
    doi: 10.1006/dbio.2001.0189pubmed: 11401405google scholar: lookup
  14. Dickinson ME, Flenniken AM, Ji X, Teboul L, Wong MD, White JK, Meehan TF, Weninger WJ, Westerberg H, Adissu H, Baker CN, Bower L, Brown JM, Caddle LB, Chiani F, Clary D, Cleak J, Daly MJ, Denegre JM, Doe B, Dolan ME, Edie SM, Fuchs H, Gailus-Durner V, Galli A, Gambadoro A, Gallegos J, Guo S, Horner NR, Hsu CW, Johnson SJ, Kalaga S, Keith LC, Lanoue L, Lawson TN, Lek M, Mark M, Marschall S, Mason J, McElwee ML, Newbigging S, Nutter LM, Peterson KA, Ramirez-Solis R, Rowland DJ, Ryder E, Samocha KE, Seavitt JR, Selloum M, Szoke-Kovacs Z, Tamura M, Trainor AG, Tudose I, Wakana S, Warren J, Wendling O, West DB, Wong L, Yoshiki A, MacArthur DG, Tocchini-Valentini GP, Gao X, Flicek P, Bradley A, Skarnes WC, Justice MJ, Parkinson HE, Moore M, Wells S, Braun RE, Svenson KL, de Angelis MH, Herault Y, Mohun T, Mallon AM, Henkelman RM, Brown SD, Adams DJ, Lloyd KC, McKerlie C, Beaudet AL, Bućan M, Murray SA. High-throughput discovery of novel developmental phenotypes.. Nature 2016 Sep 22;537(7621):508-514.
    doi: 10.1038/nature19356pmc: PMC5295821pubmed: 27626380google scholar: lookup
  15. Dudak J, Zemlicka J, Karch J, Patzelt M, Mrzilkova J, Zach P, Hermanova Z, Kvacek J, Krejci F. High-contrast X-ray micro-radiography and micro-CT of ex-vivo soft tissue murine organs utilizing ethanol fixation and large area photon-counting detector.. Sci Rep 2016 Jul 27;6:30385.
    doi: 10.1038/srep30385pmc: PMC4961961pubmed: 27461900google scholar: lookup
  16. Eckermann M, Schmitzer B, van der Meer F, Franz J, Hansen O, Stadelmann C, Salditt T. Three-dimensional virtual histology of the human hippocampus based on phase-contrast computed tomography.. Proc Natl Acad Sci U S A 2021 Nov 30;118(48).
    doi: 10.1073/pnas.2113835118pmc: PMC8640721pubmed: 34819378google scholar: lookup
  17. Ermakova O, Orsini T, Gambadoro A, Chiani F, Tocchini-Valentini GP. Three-dimensional microCT imaging of murine embryonic development from immediate post-implantation to organogenesis: application for phenotyping analysis of early embryonic lethality in mutant animals.. Mamm Genome 2018 Apr;29(3-4):245-259.
    doi: 10.1007/s00335-017-9723-6pmc: PMC5887010pubmed: 29170794google scholar: lookup
  18. Franciolli AL, Cordeiro BM, da Fonseca ET, Rodrigues MN, Sarmento CA, Ambrosio CE, de Carvalho AF, Miglino MA, Silva LA. Characteristics of the equine embryo and fetus from days 15 to 107 of pregnancy.. Theriogenology 2011 Sep 15;76(5):819-32.
    doi: 10.1016/j.theriogenology.2011.04.014pubmed: 21719090google scholar: lookup
  19. Gabner S, Böck P, Fink D, Glösmann M, Handschuh S. The visible skeleton 2.0: phenotyping of cartilage and bone in fixed vertebrate embryos and foetuses based on X-ray microCT.. Development 2020 May 29;147(11).
    doi: 10.1242/dev.187633pubmed: 32439754google scholar: lookup
  20. Gabner S, Michels C, Lanz B, Nell B, Handschuh S, Egerbacher M. Labial and buccal minor salivary glands of the dog - location, three-dimensional arrangement and histology.. Vet Ophthalmol 2021 Jul;24(4):400-407.
    doi: 10.1111/vop.12920pmc: PMC8596902pubmed: 34402569google scholar: lookup
  21. Geyer SH, Nöhammer MM, Mathä M, Reissig L, Tinhofer IE, Weninger WJ. High-resolution episcopic microscopy (HREM): a tool for visualizing skin biopsies.. Microsc Microanal 2014 Oct;20(5):1356-64.
    doi: 10.1017/S1431927614013063pubmed: 25198556google scholar: lookup
  22. Geyer SH, Weninger WJ. High‐resolution episcopic microscopy (HREM): Looking back on 13 years of successful generation of digital volume data of organic material for 3D visualisation and 3D display. Applied Sciences 9(18), 3826.
    doi: 10.3390/app9183826google scholar: lookup
  23. Gignac PM, Kley NJ, Clarke JA, Colbert MW, Morhardt AC, Cerio D, Cost IN, Cox PG, Daza JD, Early CM, Echols MS, Henkelman RM, Herdina AN, Holliday CM, Li Z, Mahlow K, Merchant S, Müller J, Orsbon CP, Paluh DJ, Thies ML, Tsai HP, Witmer LM. Diffusible iodine-based contrast-enhanced computed tomography (diceCT): an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues.. J Anat 2016 Jun;228(6):889-909.
    doi: 10.1111/joa.12449pmc: PMC5341577pubmed: 26970556google scholar: lookup
  24. Glueckert R, Johnson Chacko L, Schmidbauer D, Potrusil T, Pechriggl EJ, Hoermann R, Brenner E, Reka A, Schrott-Fischer A, Handschuh S. Visualization of the Membranous Labyrinth and Nerve Fiber Pathways in Human and Animal Inner Ears Using MicroCT Imaging.. Front Neurosci 2018;12:501.
    doi: 10.3389/fnins.2018.00501pmc: PMC6079228pubmed: 30108474google scholar: lookup
  25. Handschuh S, Baeumler N, Schwaha T, Ruthensteiner B. A correlative approach for combining microCT, light and transmission electron microscopy in a single 3D scenario.. Front Zool 2013 Aug 3;10(1):44.
    doi: 10.1186/1742-9994-10-44pmc: PMC3750762pubmed: 23915384google scholar: lookup
  26. Handschuh S, Natchev N, Kummer S, Beisser CJ, Lemell P, Herrel A, Vergilov V. Cranial kinesis in the miniaturised lizard Ablepharus kitaibelii (Squamata: Scincidae).. J Exp Biol 2019 May 10;222(Pt 9).
    doi: 10.1242/jeb.198291pubmed: 30962279google scholar: lookup
  27. Hinrichs K, Sertich PL, Palmer E, Kenney RM. Establishment and maintenance of pregnancy after embryo transfer in ovariectomized mares treated with progesterone.. J Reprod Fertil 1987 Jul;80(2):395-401.
    doi: 10.1530/jrf.0.0800395pubmed: 3116228google scholar: lookup
  28. Hutchinson JC, Shelmerdine SC, Simcock IC, Sebire NJ, Arthurs OJ. Early clinical applications for imaging at microscopic detail: microfocus computed tomography (micro-CT).. Br J Radiol 2017 Jul;90(1075):20170113.
    doi: 10.1259/bjr.20170113pmc: PMC5594989pubmed: 28368658google scholar: lookup
  29. Jiang Y, Zhao J, Liao EY, Dai RC, Wu XP, Genant HK. Application of micro-CT assessment of 3-D bone microstructure in preclinical and clinical studies.. J Bone Miner Metab 2005;23 Suppl:122-31.
    doi: 10.1007/BF03026336pubmed: 15984427google scholar: lookup
  30. Johnson JT, Hansen MS, Wu I, Healy LJ, Johnson CR, Jones GM, Capecchi MR, Keller C. Virtual histology of transgenic mouse embryos for high-throughput phenotyping.. PLoS Genet 2006 Apr;2(4):e61.
    doi: 10.1371/journal.pgen.0020061pmc: PMC1449902pubmed: 16683035google scholar: lookup
  31. Jones MG, Fabre A, Schneider P, Cinetto F, Sgalla G, Mavrogordato M, Jogai S, Alzetani A, Marshall BG, O'Reilly KM, Warner JA, Lackie PM, Davies DE, Hansell DM, Nicholson AG, Sinclair I, Brown KK, Richeldi L. Three-dimensional characterization of fibroblast foci in idiopathic pulmonary fibrosis.. JCI Insight 2016 Apr 21;1(5).
    doi: 10.1172/jci.insight.86375pmc: PMC4889020pubmed: 27275013google scholar: lookup
  32. Karreman MA, Mercier L, Schieber NL, Solecki G, Allio G, Winkler F, Ruthensteiner B, Goetz JG, Schwab Y. Fast and precise targeting of single tumor cells in vivo by multimodal correlative microscopy.. J Cell Sci 2016 Jan 15;129(2):444-56.
    doi: 10.1242/jcs.181842pmc: PMC4732291pubmed: 26659665google scholar: lookup
  33. Karreman MA, Ruthensteiner B, Mercier L, Schieber NL, Solecki G, Winkler F, Goetz JG, Schwab Y. Find your way with X-Ray: Using microCT to correlate in vivo imaging with 3D electron microscopy.. Methods Cell Biol 2017;140:277-301.
    doi: 10.1016/bs.mcb.2017.03.006pubmed: 28528637google scholar: lookup
  34. Katsamenis OL, Olding M, Warner JA, Chatelet DS, Jones MG, Sgalla G, Smit B, Larkin OJ, Haig I, Richeldi L, Sinclair I, Lackie PM, Schneider P. X-ray Micro-Computed Tomography for Nondestructive Three-Dimensional (3D) X-ray Histology.. Am J Pathol 2019 Aug;189(8):1608-1620.
    doi: 10.1016/j.ajpath.2019.05.004pmc: PMC6680277pubmed: 31125553google scholar: lookup
  35. Keklikoglou K, Faulwetter S, Chatzinikolaou E, Wils P, Brecko J, Kvaček J, Metscher B, Arvanitidis C. Micro‐computed tomography for natural history specimens: a handbook of best practice protocols. European Journal of Taxonomy 522, 1–55.
    doi: 10.5852/ejt.2019.522google scholar: lookup
  36. Laib A, Kumer JL, Majumdar S, Lane NE. The temporal changes of trabecular architecture in ovariectomized rats assessed by MicroCT.. Osteoporos Int 2001;12(11):936-41.
    doi: 10.1007/s001980170022pubmed: 11804020google scholar: lookup
  37. Lee CH, Blackband SJ, Fernandez-Funez P. Visualization of synaptic domains in the Drosophila brain by magnetic resonance microscopy at 10 micron isotropic resolution.. Sci Rep 2015 Mar 10;5:8920.
    doi: 10.1038/srep08920pmc: PMC4649768pubmed: 25753480google scholar: lookup
  38. Maire E, Withers PJ. Quantitative X‐ray tomography. International Materials Reviews 59(1), 1–43.
    doi: 10.1179/1743280413y.0000000023google scholar: lookup
  39. Markel M, Ginzel M, Peukert N, Schneider H, Haak R, Mayer S, Suttkus A, Lacher M, Kluth D, Gosemann JH. High resolution three-dimensional imaging and measurement of lung, heart, liver, and diaphragmatic development in the fetal rat based on micro-computed tomography (micro-CT).. J Anat 2020 Dec 2;238(4):1042-54.
    doi: 10.1111/joa.13355pmc: PMC7930770pubmed: 33289078google scholar: lookup
  40. Marxen JC, Prymak O, Beckmann F, Neues F, Epple M. Embryonic shell formation in the snail Biomphalaria glabrata: A comparison between scanning electron microscopy (SEM) and synchrotron radiation micro computer tomography (SR mu CT). Journal of Molluscan Studies 74, 19–26.
    doi: 10.1093/mollus/eym044google scholar: lookup
  41. Metscher BD. MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues.. BMC Physiol 2009 Jun 22;9:11.
    doi: 10.1186/1472-6793-9-11pmc: PMC2717911pubmed: 19545439google scholar: lookup
  42. Metscher BD. MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions.. Dev Dyn 2009 Mar;238(3):632-40.
    pubmed: 19235724doi: 10.1002/dvdy.21857google scholar: lookup
  43. Mizutani R, Suzuki Y. X-ray microtomography in biology.. Micron 2012 Feb;43(2-3):104-15.
    doi: 10.1016/j.micron.2011.10.002pubmed: 22036251google scholar: lookup
  44. Morales AG, Stempinski ES, Xiao X, Patel A, Panna A, Olivier KN, McShane PJ, Robinson C, George AJ, Donahue DR, Chen P, Wen H. Micro-CT scouting for transmission electron microscopy of human tissue specimens.. J Microsc 2016 Jul;263(1):113-7.
    doi: 10.1111/jmi.12385pmc: PMC4907811pubmed: 26854176google scholar: lookup
  45. Müller M, Kimm MA, Ferstl S, Allner S, Achterhold K, Herzen J, Pfeiffer F, Busse M. Nucleus-specific X-ray stain for 3D virtual histology.. Sci Rep 2018 Dec 14;8(1):17855.
    doi: 10.1038/s41598-018-36067-ypmc: PMC6294809pubmed: 30552357google scholar: lookup
  46. Okada CTC, Kaps M, Scarlet D, Handschuh S, Gautier C, Melchert M, Aurich J, Aurich C. Low plasma progestin concentration during the early postovulatory phase impairs equine conceptus development in the late preimplantation phase. Reproduction Fertility and Development 32(13), 1156–1167.
    doi: 10.1071/RD20116google scholar: lookup
  47. Pauwels E, Van Loo D, Cornillie P, Brabant L, Van Hoorebeke L. An exploratory study of contrast agents for soft tissue visualization by means of high resolution X-ray computed tomography imaging.. J Microsc 2013 Apr;250(1):21-31.
    doi: 10.1111/jmi.12013pubmed: 23432572google scholar: lookup
  48. Pitrone PG, Schindelin J, Stuyvenberg L, Preibisch S, Weber M, Eliceiri KW, Huisken J, Tomancak P. OpenSPIM: an open-access light-sheet microscopy platform.. Nat Methods 2013 Jul;10(7):598-9.
    doi: 10.1038/nmeth.2507pmc: PMC7450513pubmed: 23749304google scholar: lookup
  49. Quintana L, Sharpe J. Optical projection tomography of vertebrate embryo development.. Cold Spring Harb Protoc 2011 Jun 1;2011(6):586-94.
    doi: 10.1101/pdb.top116pubmed: 21632785google scholar: lookup
  50. Rawson SD, Maksimcuka J, Withers PJ, Cartmell SH. X-ray computed tomography in life sciences.. BMC Biol 2020 Feb 27;18(1):21.
    doi: 10.1186/s12915-020-0753-2pmc: PMC7045626pubmed: 32103752google scholar: lookup
  51. Ritman EL. Micro-computed tomography-current status and developments.. Annu Rev Biomed Eng 2004;6:185-208.
    doi: 10.1146/annurev.bioeng.6.040803.140130pubmed: 15255767google scholar: lookup
  52. Ritman EL. Current status of developments and applications of micro-CT.. Annu Rev Biomed Eng 2011 Aug 15;13:531-52.
    doi: 10.1146/annurev-bioeng-071910-124717pubmed: 21756145google scholar: lookup
  53. Rodgers G, Tanner C, Schulz G, Migga A, Kuo W, Bikis C, Scheel M, Kurtcuoglu V, Weitkamp T, Müller B. Virtual histology of an entire mouse brain from formalin fixation to paraffin embedding. Part 2: Volumetric strain fields and local contrast changes.. J Neurosci Methods 2022 Jan 1;365:109385.
    doi: 10.1016/j.jneumeth.2021.109385pubmed: 34637810google scholar: lookup
  54. Rodrigues RF, Rodrigues MN, Franciolli ALR, Carvalho RC, Rigoglio N, Jacob JCF, Gastal EL, Miglino MA. Embryonic and fetal development of the cardiorespiratory apparatus in horses (Equus Caballus) from 20 to 115 days of gestation. Journal of Cytology & Histology 5(4), 1.
    doi: 10.4172/2157-7099.1000240google scholar: lookup
  55. Ruffins SW, Martin M, Keough L, Truong S, Fraser SE, Jacobs RE, Lansford R. Digital three-dimensional atlas of quail development using high-resolution MRI.. ScientificWorldJournal 2007 May 11;7:592-604.
    doi: 10.1100/tsw.2007.125pmc: PMC5901279pubmed: 17525824google scholar: lookup
  56. Santi PA. Light sheet fluorescence microscopy: a review.. J Histochem Cytochem 2011 Feb;59(2):129-38.
    doi: 10.1369/0022155410394857pmc: PMC3201139pubmed: 21339178google scholar: lookup
  57. Schwaha TF, Handschuh S, Ostrovsky AN, Wanninger A. Morphology of the bryozoan Cinctipora elegans (Cyclostomata, Cinctiporidae) with first data on its sexual reproduction and the cyclostome neuro-muscular system.. BMC Evol Biol 2018 Jun 14;18(1):92.
    doi: 10.1186/s12862-018-1206-1pmc: PMC6000935pubmed: 29898669google scholar: lookup
  58. Scott AE, Vasilescu DM, Seal KA, Keyes SD, Mavrogordato MN, Hogg JC, Sinclair I, Warner JA, Hackett TL, Lackie PM. Three dimensional imaging of paraffin embedded human lung tissue samples by micro-computed tomography.. PLoS One 2015;10(6):e0126230.
    doi: 10.1371/journal.pone.0126230pmc: PMC4452358pubmed: 26030902google scholar: lookup
  59. Sengle G, Tufa SF, Sakai LY, Zulliger MA, Keene DR. A correlative method for imaging identical regions of samples by micro-CT, light microscopy, and electron microscopy: imaging adipose tissue in a model system.. J Histochem Cytochem 2013 Apr;61(4):263-71.
    doi: 10.1369/0022155412473757pmc: PMC3636687pubmed: 23264636google scholar: lookup
  60. Senter-Zapata M, Patel K, Bautista PA, Griffin M, Michaelson J, Yagi Y. The Role of Micro-CT in 3D Histology Imaging.. Pathobiology 2016;83(2-3):140-7.
    doi: 10.1159/000442387pubmed: 27100885google scholar: lookup
  61. Sharpe J. Optical projection tomography.. Annu Rev Biomed Eng 2004;6:209-28.
    doi: 10.1146/annurev.bioeng.6.040803.140210pubmed: 15255768google scholar: lookup
  62. Sharpe J, Ahlgren U, Perry P, Hill B, Ross A, Hecksher-Sørensen J, Baldock R, Davidson D. Optical projection tomography as a tool for 3D microscopy and gene expression studies.. Science 2002 Apr 19;296(5567):541-5.
    doi: 10.1126/science.1068206pubmed: 11964482google scholar: lookup
  63. Sombke A, Lipke E, Michalik P, Uhl G, Harzsch S. Potential and limitations of X-Ray micro-computed tomography in arthropod neuroanatomy: a methodological and comparative survey.. J Comp Neurol 2015 Jun 1;523(8):1281-95.
    doi: 10.1002/cne.23741pmc: PMC4409823pubmed: 25728683google scholar: lookup
  64. Stock SR. X‐ray microtomography of materials. International Materials Reviews 44(4), 141–164.
    doi: 10.1179/095066099101528261google scholar: lookup
  65. Stock SR. Microcomputed tomography: methodology and applications. .
  66. Stock SR, Barss J, Dahl T, Veis A, Almer JD, Carlo F. Synchrotron X-ray studies of the keel of the short-spined sea urchin Lytechinus variegatus: absorption microtomography (microCT) and small beam diffraction mapping.. Calcif Tissue Int 2003 May;72(5):555-66.
    doi: 10.1007/s00223-002-1037-2pubmed: 12721775google scholar: lookup
  67. Tafforeau P, Boistel R, Boller E, Bravin A, Brunet M, Chaimanee Y, Cloetens P, Feist M, Hoszowska J, Jaeger JJ, Kay RF, Lazzari V, Marivaux L, Nel A, Nemoz C, Thibault X, Vignaud P, Zabler S. Applications of X‐ray synchrotron microtomography for non‐destructive 3D studies of paleontological specimens. Applied Physics A‐Materials Science & Processing 83(2), 195–202.
    doi: 10.1007/s00339-006-3507-2google scholar: lookup
  68. Teplov A, Tabata K, Fu X, Uraoka N, Roehrl M, Ntiamoah P, Humm JL, Sirintrapun SJ, Murray MP, Shia J, Travis WD, Brogi E, Hameed M, Yagi Y. Development of standard operating procedure (SOP) of Micro‐computed tomography (micro‐CT) in pathology. Diagnostic Pathology 5, 273.
    doi: 10.17629/www.diagnosticpathology.eugoogle scholar: lookup
  69. Töpperwien M, Markus A, Alves F, Salditt T. Contrast enhancement for visualizing neuronal cytoarchitecture by propagation-based x-ray phase-contrast tomography.. Neuroimage 2019 Oct 1;199:70-80.
    doi: 10.1016/j.neuroimage.2019.05.043pubmed: 31129306google scholar: lookup
  70. Töpperwien M, van der Meer F, Stadelmann C, Salditt T. Three-dimensional virtual histology of human cerebellum by X-ray phase-contrast tomography.. Proc Natl Acad Sci U S A 2018 Jul 3;115(27):6940-6945.
    doi: 10.1073/pnas.1801678115pmc: PMC6142271pubmed: 29915047google scholar: lookup
  71. Toro-Ramos T, Paley C, Pi-Sunyer FX, Gallagher D. Body composition during fetal development and infancy through the age of 5 years.. Eur J Clin Nutr 2015 Dec;69(12):1279-89.
    doi: 10.1038/ejcn.2015.117pmc: PMC4680980pubmed: 26242725google scholar: lookup
  72. Vasarhelyi L, Konya Z, Kukovecz A, Vajtai R. Microcomputed tomography‐based characterization of advanced materials: A review. Materials Today Advances 8, 100084.
    doi: 10.1016/j.mtadv.2020.100084google scholar: lookup
  73. Walter A, Paul-Gilloteaux P, Plochberger B, Sefc L, Verkade P, Mannheim JG, Slezak P, Unterhuber A, Marchetti-Deschmann M, Ogris M, Buehler K, Fixler D, Geyer SH, Weninger WJ, Gloesmann M, Handschu S, Wanek T. Correlated multimodal imaging in life sciences: expanding the biomedical horizon. Frontiers in Physics 8, 1–28.
    doi: 10.3389/fphy.2020.00047google scholar: lookup
  74. Walton LA, Bradley RS, Withers PJ, Newton VL, Watson RE, Austin C, Sherratt MJ. Morphological Characterisation of Unstained and Intact Tissue Micro-architecture by X-ray Computed Micro- and Nano-Tomography.. Sci Rep 2015 May 15;5:10074.
    doi: 10.1038/srep10074pmc: PMC4650804pubmed: 25975937google scholar: lookup
  75. Weber M, Mickoleit M, Huisken J. Light sheet microscopy.. Methods Cell Biol 2014;123:193-215.
    doi: 10.1016/B978-0-12-420138-5.00011-2pubmed: 24974029google scholar: lookup
  76. Weninger WJ, Maurer-Gesek B, Reissig LF, Prin F, Wilson R, Galli A, Adams DJ, White JK, Mohun TJ, Geyer SH. Visualising the Cardiovascular System of Embryos of Biomedical Model Organisms with High Resolution Episcopic Microscopy (HREM).. J Cardiovasc Dev Dis 2018 Dec 15;5(4).
    doi: 10.3390/jcdd5040058pmc: PMC6306920pubmed: 30558275google scholar: lookup
  77. Wong MD, Dazai J, Walls JR, Gale NW, Henkelman RM. Design and implementation of a custom built optical projection tomography system.. PLoS One 2013;8(9):e73491.
    doi: 10.1371/journal.pone.0073491pmc: PMC3762719pubmed: 24023880google scholar: lookup
  78. Wong MD, Maezawa Y, Lerch JP, Henkelman RM. Automated pipeline for anatomical phenotyping of mouse embryos using micro-CT.. Development 2014 Jun;141(12):2533-41.
    doi: 10.1242/dev.107722pmc: PMC4050698pubmed: 24850858google scholar: lookup
  79. Wong MD, Spring S, Henkelman RM. Structural stabilization of tissue for embryo phenotyping using micro-CT with iodine staining.. PLoS One 2013;8(12):e84321.
    doi: 10.1371/journal.pone.0084321pmc: PMC3875560pubmed: 24386367google scholar: lookup
  80. Zamyadi M, Baghdadi L, Lerch JP, Bhattacharya S, Schneider JE, Henkelman RM, Sled JG. Mouse embryonic phenotyping by morphometric analysis of MR images.. Physiol Genomics 2010 Oct;42A(2):89-95.
    doi: 10.1152/physiolgenomics.00091.2010pmc: PMC2957795pubmed: 20682847google scholar: lookup
  81. Ziegler A, Bock C, Ketten DR, Mair RW, Mueller S, Nagelmann N, Pracht ED, Schröder L. Digital three‐dimensional imaging techniques provide new analytical pathways for malacological research. American Malacological Bulletin 36(2), 248–273.
    doi: 10.4003/006.036.0205google scholar: lookup

Citations

This article has been cited 5 times.
  1. Kraus N, Placzek F, Metscher B. OCT Meets micro-CT: A Subject-Specific Correlative Multimodal Imaging Workflow for Early Chick Heart Development Modeling. J Cardiovasc Dev Dis 2022 Nov 3;9(11).
    doi: 10.3390/jcdd9110379pubmed: 36354778google scholar: lookup
  2. Handschuh S, Glösmann M. Mouse embryo phenotyping using X-ray microCT. Front Cell Dev Biol 2022;10:949184.
    doi: 10.3389/fcell.2022.949184pubmed: 36187491google scholar: lookup
  3. Rzhepakovsky I, Piskov S, Avanesyan S, Sizonenko M, Timchenko L, Shakhbanov M, Nassali G, Kiryowa I, Nagdalian A. Rapid 3D phenotyping of chick embryo liver development at HH22-HH41 embryonic stages using X-ray microcomputed tomography with PTA staining. PLoS One 2025;20(10):e0333995.
    doi: 10.1371/journal.pone.0333995pubmed: 41144470google scholar: lookup
  4. Sagar MMR, D'Amico L, Longo E, Persson IM, Deyhle R Jr, Tromba G, Bayat S, Alves F, Dullin C. Air artifact suppression in phase contrast micro-CT using conditional generative adversarial networks. J Synchrotron Radiat 2025 May 1;32(Pt 3):678-689.
    doi: 10.1107/S1600577525001511pubmed: 40138215google scholar: lookup
  5. Dizbay Sak S, Sevim S, Buyuksungur A, Kayı Cangır A, Orhan K. The Value of Micro-CT in the Diagnosis of Lung Carcinoma: A Radio-Histopathological Perspective. Diagnostics (Basel) 2023 Oct 20;13(20).
    doi: 10.3390/diagnostics13203262pubmed: 37892083google scholar: lookup
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