Quantitative Three-dimensional Imaging of Live Avian Embryonic Morphogenesis Via Micro-computed Tomography

Overview

Journal Dev Dyn

Publisher Wiley

Specialty Anatomy & Histology

Date 2011 Jul 16

PMID 21761480

Citations 28

Authors

Alyssa L Henning

Michael X Jiang

Huseyin C Yalcin

Jonathan T Butcher

Affiliations

Soon will be listed here.

Abstract

Many clinically relevant congenital malformations arise during mid to late embryonic stages. This period is challenging to image quantitatively in live embryos, necessitating the use of multiple specimens with increased experimental variability. Here we establish X-ray and blood-pool computed tomography (CT) contrast agent toxicity and teratogenesis thresholds for 3D Micro-CT imaging of live avian embryos. Day 4 chick embryos micro-injected with Visipaque™ (VP) developed for an additional 6 days without defect. X-ray radiation up to 798 mGy was nontoxic. Peak average contrast of 1,060 HU occurred within 1 hr of imaging at 50 μm resolution. VP-enhanced contrast persisted past 24 hr with delayed accumulation in the allantois. Regional volumes of VP-injected embryos were statistically identical to those of fixed embryos perfused with osmium tetroxide. We further quantified longitudinal volumetric morphogenesis of the allantois over 30 hr. These results demonstrate the safety and efficacy of contrast enhanced quantitative micro-CT imaging for live embryos.

Citing Articles

Monitoring egg fertility, embryonic morbidity, and mortality in an oviparous elasmobranch using ultrasonography.

Adams L, Wyffels J, Goodwin B, Munson R, LeBorgne L, Feldheim K Front Vet Sci. 2024; 11:1410377.

PMID: 39139603 PMC: 11319157. DOI: 10.3389/fvets.2024.1410377.

An optimized CT-dense agent perfusion and micro-CT imaging protocol for chick embryo developmental stages.

Naija A, Mutlu O, Khan T, Seers T, Yalcin H BMC Biomed Eng. 2024; 6(1):3.

PMID: 38654382 PMC: 11040921. DOI: 10.1186/s42490-024-00078-w.

Dynamic 3D morphology of chick embryos and allantois depicted nondestructively by 3.0T clinical magnetic resonance imaging.

Chen L, Wang Z, Fu X, Wang S, Feng Y, Coudyzer W Poult Sci. 2023; 102(9):102902.

PMID: 37429051 PMC: 10466300. DOI: 10.1016/j.psj.2023.102902.

Toxicological Analysis by Assessment of Vascularization and Cell Viability Using the Chicken's Chorioallantoic Membrane (CAM Assay).

Wiesmann N, Brieger J, Eckrich J Methods Mol Biol. 2023; 2644:403-421.

PMID: 37142937 DOI: 10.1007/978-1-0716-3052-5_26.

model in cancer research and tumor immunology.

Miebach L, Berner J, Bekeschus S Front Immunol. 2022; 13:1006064.

PMID: 36248802 PMC: 9556724. DOI: 10.3389/fimmu.2022.1006064.

References

Ahrens E, Srinivas M, Capuano S, Simhan H, Schatten G . Magnetic resonance imaging of embryonic and fetal development in model systems. Methods Mol Med. 2006; 124:87-101. DOI: 10.1385/1-59745-010-3:87. View

Rabin O, Perez J, Grimm J, Wojtkiewicz G, Weissleder R . An X-ray computed tomography imaging agent based on long-circulating bismuth sulphide nanoparticles. Nat Mater. 2006; 5(2):118-22. DOI: 10.1038/nmat1571. View

Graves J, Dunn B, Brown S . Embryonic chick allantois: functional isolation and development of sodium transport. Am J Physiol. 1986; 251(5 Pt 1):C787-94. DOI: 10.1152/ajpcell.1986.251.5.C787. View

Yalcin H, Shekhar A, Nishimura N, Rane A, Schaffer C, Butcher J . Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects. Am J Physiol Heart Circ Physiol. 2010; 299(5):H1728-35. DOI: 10.1152/ajpheart.00495.2010. View

van Soest G, Goderie T, Regar E, Koljenovic S, van Leenders G, Gonzalo N . Atherosclerotic tissue characterization in vivo by optical coherence tomography attenuation imaging. J Biomed Opt. 2010; 15(1):011105. DOI: 10.1117/1.3280271. View

Yalcin H, Shekhar A, Rane A, Butcher J . An ex-ovo chicken embryo culture system suitable for imaging and microsurgery applications. J Vis Exp. 2010; (44). PMC: 3185626. DOI: 10.3791/2154. View

Gargesha M, Jenkins M, Wilson D, Rollins A . High temporal resolution OCT using image-based retrospective gating. Opt Express. 2009; 17(13):10786-99. PMC: 2748662. DOI: 10.1364/oe.17.010786. View

Pallares P, Fernandez-Valle M, Gonzalez-Bulnes A . In vivo virtual histology of mouse embryogenesis by ultrasound biomicroscopy and magnetic resonance imaging. Reprod Fertil Dev. 2009; 21(2):283-92. DOI: 10.1071/rd08124. View

Zhang W, Chen Y, Swift M, Tassi E, Stylianou D, Gibby K . Effect of FGF-binding protein 3 on vascular permeability. J Biol Chem. 2008; 283(42):28329-37. PMC: 2568920. DOI: 10.1074/jbc.M802144200. View

10.

Metscher B . MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol. 2009; 9:11. PMC: 2717911. DOI: 10.1186/1472-6793-9-11. View

11.

Hogers B, van der Weerd L, Olofsen H, van der Graaf L, DeRuiter M, Gittenberger-de Groot A . Non-invasive tracking of avian development in vivo by MRI. NMR Biomed. 2008; 22(4):365-73. DOI: 10.1002/nbm.1346. View

12.

Liebling M, Forouhar A, Gharib M, Fraser S, Dickinson M . Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences. J Biomed Opt. 2005; 10(5):054001. DOI: 10.1117/1.2061567. View

13.

Aristizabal O, Ketterling J, Turnbull D . 40-MHz annular array imaging of mouse embryos. Ultrasound Med Biol. 2006; 32(11):1631-7. PMC: 1858655. DOI: 10.1016/j.ultrasmedbio.2006.05.020. View

14.

Hornberger L, Need L, Benacerraf B . Development of significant left and right ventricular hypoplasia in the second and third trimester fetus. J Ultrasound Med. 1996; 15(9):655-9. DOI: 10.7863/jum.1996.15.9.655. View

15.

ROMANOFF A . Membrane growth and function. Ann N Y Acad Sci. 1952; 55(2):288-301. DOI: 10.1111/j.1749-6632.1952.tb26545.x. View

16.

Paulus M, Gleason S, Kennel S, Hunsicker P, Johnson D . High resolution X-ray computed tomography: an emerging tool for small animal cancer research. Neoplasia. 2000; 2(1-2):62-70. PMC: 1531867. DOI: 10.1038/sj.neo.7900069. View

17.

Zamir E, Czirok A, Cui C, Little C, Rongish B . Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements. Proc Natl Acad Sci U S A. 2006; 103(52):19806-11. PMC: 1705812. DOI: 10.1073/pnas.0606100103. View

18.

de la Cruz M, CAMPILLO-SAINZ C, MUNOZ-ARMAS S . Congenital heart defects in chick embryos subjected to temperature variations. Circ Res. 1966; 18(3):257-62. DOI: 10.1161/01.res.18.3.257. View

19.

Nieman B, Turnbull D . Ultrasound and magnetic resonance microimaging of mouse development. Methods Enzymol. 2010; 476:379-400. PMC: 3160173. DOI: 10.1016/S0076-6879(10)76021-3. View

20.

Duce S, Morrison F, Welten M, Baggott G, Tickle C . Micro-magnetic resonance imaging study of live quail embryos during embryonic development. Magn Reson Imaging. 2010; 29(1):132-9. PMC: 3006493. DOI: 10.1016/j.mri.2010.08.004. View