Noninvasive Tracking of Embryonic Cardiac Dynamics and Development with Volumetric Optoacoustic Spectroscopy

Overview

Journal Adv Sci (Weinh)

Specialty Biomedical Engineering

Date 2024 Mar 25

PMID 38526147

Authors

Maryam Hatami

Ali Ozbek

Xose Luis Dean-Ben

Jessica Gutierrez

Alexander Schill

Daniel Razansky

Kirill V Larin

Affiliations

Soon will be listed here.

Abstract

Noninvasive monitoring of cardiac development can potentially prevent cardiac anomalies in adulthood. Mouse models provide unique opportunities to study cardiac development and disease in mammals. However, high-resolution noninvasive functional analyses of murine embryonic cardiac models are challenging because of the small size and fast volumetric motion of the embryonic heart, which is deeply embedded inside the uterus. In this study, a real time volumetric optoacoustic spectroscopy (VOS) platform for whole-heart visualization with high spatial (100 µm) and temporal (10 ms) resolutions is developed. Embryonic heart development on gestational days (GDs) 14.5-17.5 and quantify cardiac dynamics using time-lapse-4D image data of the heart is followed. Additionally, spectroscopic recordings enable the quantification of the blood oxygenation status in heart chambers in a label-free and noninvasive manner. This technology introduces new possibilities for high-resolution quantification of embryonic heart function at different gestational stages in mammalian models, offering an invaluable noninvasive method for developmental biology.

Citing Articles

Diagnostic and therapeutic optical imaging in cardiovascular diseases.

Pang W, Yuan C, Zhong T, Huang X, Pan Y, Qu J iScience. 2024; 27(11):111216.

PMID: 39569375 PMC: 11576408. DOI: 10.1016/j.isci.2024.111216.

Noninvasive Tracking of Embryonic Cardiac Dynamics and Development with Volumetric Optoacoustic Spectroscopy.

Hatami M, Ozbek A, Dean-Ben X, Gutierrez J, Schill A, Razansky D Adv Sci (Weinh). 2024; 11(22):e2400089.

PMID: 38526147 PMC: 11165471. DOI: 10.1002/advs.202400089.

References

Phoon C, Aristizabal O, Turnbull D . 40 MHz Doppler characterization of umbilical and dorsal aortic blood flow in the early mouse embryo. Ultrasound Med Biol. 2000; 26(8):1275-83. DOI: 10.1016/s0301-5629(00)00278-7. View

Lin H, Dean-Ben X, Ivankovic I, Kimm M, Kosanke K, Haas H . Characterization of Cardiac Dynamics in an Acute Myocardial Infarction Model by Four-Dimensional Optoacoustic and Magnetic Resonance Imaging. Theranostics. 2017; 7(18):4470-4479. PMC: 5695143. DOI: 10.7150/thno.20616. View

Ozsoy C, Ozbek A, Reiss M, Dean-Ben X, Razansky D . Ultrafast four-dimensional imaging of cardiac mechanical wave propagation with sparse optoacoustic sensing. Proc Natl Acad Sci U S A. 2021; 118(45). PMC: 8609330. DOI: 10.1073/pnas.2103979118. View

Lindsey M, Kassiri Z, Virag J, de Castro Bras L, Scherrer-Crosbie M . Guidelines for measuring cardiac physiology in mice. Am J Physiol Heart Circ Physiol. 2018; 314(4):H733-H752. PMC: 5966769. DOI: 10.1152/ajpheart.00339.2017. View

Laufer J, Norris F, Cleary J, Zhang E, Treeby B, Cox B . In vivo photoacoustic imaging of mouse embryos. J Biomed Opt. 2012; 17(6):061220. DOI: 10.1117/1.JBO.17.6.061220. View

Li M, Tang Y, Yao J . Photoacoustic tomography of blood oxygenation: A mini review. Photoacoustics. 2018; 10:65-73. PMC: 6033062. DOI: 10.1016/j.pacs.2018.05.001. View

Li L, Zhu L, Ma C, Lin L, Yao J, Wang L . Single-impulse Panoramic Photoacoustic Computed Tomography of Small-animal Whole-body Dynamics at High Spatiotemporal Resolution. Nat Biomed Eng. 2018; 1(5). PMC: 5766044. DOI: 10.1038/s41551-017-0071. View

Amadei G, Handford C, Qiu C, De Jonghe J, Greenfeld H, Tran M . Embryo model completes gastrulation to neurulation and organogenesis. Nature. 2022; 610(7930):143-153. PMC: 9534772. DOI: 10.1038/s41586-022-05246-3. View

Lin H, Dean-Ben X, Reiss M, Schottle V, Wahl-Schott C, Efimov I . Ultrafast Volumetric Optoacoustic Imaging of Whole Isolated Beating Mouse Heart. Sci Rep. 2018; 8(1):14132. PMC: 6148063. DOI: 10.1038/s41598-018-32317-1. View

10.

Lara-Canton I, Badurdeen S, Dekker J, Davis P, Roberts C, Te Pas A . Oxygen saturation and heart rate in healthy term and late preterm infants with delayed cord clamping. Pediatr Res. 2022; 96(3):604-609. PMC: 11499272. DOI: 10.1038/s41390-021-01805-y. View

11.

Rocha L, Rolo L, Araujo Junior E . How to perform a functional assessment of the fetal heart: a pictorial review. Ultrasonography. 2019; 38(4):365-373. PMC: 6773963. DOI: 10.14366/usg.18065. View

12.

Dean-Ben X, Razansky D . On the link between the speckle free nature of optoacoustics and visibility of structures in limited-view tomography. Photoacoustics. 2017; 4(4):133-140. PMC: 5200938. DOI: 10.1016/j.pacs.2016.10.001. View

13.

Pizzo E, Berrettoni S, Kaul R, Cervantes D, Stefano V, Jain S . Heart Rate Variability Reveals Altered Autonomic Regulation in Response to Myocardial Infarction in Experimental Animals. Front Cardiovasc Med. 2022; 9:843144. PMC: 9108187. DOI: 10.3389/fcvm.2022.843144. View

14.

MacGrogan D, Munch J, de la Pompa J . Notch and interacting signalling pathways in cardiac development, disease, and regeneration. Nat Rev Cardiol. 2018; 15(11):685-704. DOI: 10.1038/s41569-018-0100-2. View

15.

Wallenstein M, Harper L, Odibo A, Roehl K, Longman R, Macones G . Fetal congenital heart disease and intrauterine growth restriction: a retrospective cohort study. J Matern Fetal Neonatal Med. 2011; 25(6):662-5. DOI: 10.3109/14767058.2011.597900. View

16.

Markel M, Ginzel M, Peukert N, Schneider H, Haak R, Mayer S . 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; . PMC: 7930770. DOI: 10.1111/joa.13355. View

17.

Keller B, MacLennan M, Tinney J, Yoshigi M . In vivo assessment of embryonic cardiovascular dimensions and function in day-10.5 to -14.5 mouse embryos. Circ Res. 1996; 79(2):247-55. DOI: 10.1161/01.res.79.2.247. View

18.

Lee F, Marini D, Seed M, Sun L . Maternal hyperoxygenation in congenital heart disease. Transl Pediatr. 2021; 10(8):2197-2209. PMC: 8429855. DOI: 10.21037/tp-20-226. View

19.

Meilhac S, Buckingham M . The deployment of cell lineages that form the mammalian heart. Nat Rev Cardiol. 2018; 15(11):705-724. DOI: 10.1038/s41569-018-0086-9. View

20.

Zhou Y, Foster F, Parkes R, Adamson S . Developmental changes in left and right ventricular diastolic filling patterns in mice. Am J Physiol Heart Circ Physiol. 2003; 285(4):H1563-75. DOI: 10.1152/ajpheart.00384.2003. View