Fetal Left Ventricle Function Evaluated by Two-Dimensional Speckle-Tracking Echocardiography across Clinical Stages of Severity in Growth-Restricted Fetuses
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Ultrasound Acquisition
2.3. Analysis Protocol
2.4. Statistical Analysis
3. Results
3.1. Basic Characteristics of the Study Population
3.2. Fetal Ultrasound Assessment
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Miranda, J.O.; Ramalho, C.; Henriques-Coelho, T.; Areias, J.C. Fetal Programming as a Predictor of Adult Health or Disease: The Need to Reevaluate Fetal Heart Function. Heart Fail. Rev. 2017, 22, 861–877. [Google Scholar] [CrossRef]
- Sarvari, S.I.; Rodriguez-Lopez, M.; Nuñez-Garcia, M.; Sitges, M.; Sepulveda-Martinez, A.; Camara, O.; Butakoff, C.; Gratacos, E.; Bijnens, B.; Crispi, F. Persistence of Cardiac Remodeling in Preadolescents with Fetal Growth Restriction. Circ. Cardiovasc. Imaging 2017, 10, e005270. [Google Scholar] [CrossRef]
- Figueras, F.; Gratacós, E. Update on the Diagnosis and Classification of Fetal Growth Restriction and Proposal of a Stage-Based Management Protocol. Fetal Diagn. Ther. 2014, 36, 86–98. [Google Scholar] [CrossRef]
- Crispi, F.; Sepúlveda-Martínez, Á.; Crovetto, F.; Gómez, O.; Bijnens, B.; Gratacós, E. Main Patterns of Fetal Cardiac Remodeling. Fetal Diagn. Ther. 2020, 47, 337–344. [Google Scholar] [CrossRef] [PubMed]
- Comas, M.; Crispi, F.; Cruz-Martinez, R.; Figueras, F.; Gratacos, E. Tissue Doppler Echocardiographic Markers of Cardiac Dysfunction in Small-for-Gestational Age Fetuses. Am. J. Obstet. Gynecol. 2011, 205, 57.e1–57.e6. [Google Scholar] [CrossRef] [PubMed]
- Comas, M.; Crispi, F.; Cruz-Martinez, R.; Martinez, J.M.; Figueras, F.; Gratacós, E. Usefulness of Myocardial Tissue Doppler vs. Conventional Echocardiography in the Evaluation of Cardiac Dysfunction in Early-Onset Intrauterine Growth Restriction. Am. J. Obstet. Gynecol. 2010, 203, 45.e1–45.e7. [Google Scholar] [CrossRef] [PubMed]
- Crispi, F.; Gratacos, E. Fetal Cardiac Function: Technical Considerations and Potential Research and Clinical Applications. Fetal Diagn. Ther. 2012, 32, 47–64. [Google Scholar] [CrossRef]
- DeVore, G.R.; Gumina, D.L.; Hobbins, J.C. Assessment of Ventricular Contractility in Fetuses with an Estimated Fetal Weight Less than the Tenth Centile. Am. J. Obstet. Gynecol. 2019, 221, 498.e1–498.e22. [Google Scholar] [CrossRef] [PubMed]
- Sun, X.; Zhao, B.; Chen, Y.; Pan, M.; Wang, B.; Peng, X. Preliminary Results Analysis for Left Ventricular Systolic Function in Normal Fetuses by Automated Cardiac Motion Quantitation. J. Matern. -Fetal Neonatal Med. 2021, 34, 2701–2709. [Google Scholar] [CrossRef] [PubMed]
- Day, T.G.; Charakida, M.; Simpson, J.M. Using Speckle-Tracking Echocardiography to Assess Fetal Myocardial Deformation: Are We There Yet? Ultrasound Obstet. Gynecol. 2019, 54, 575–581. [Google Scholar] [CrossRef] [PubMed]
- Domínguez-Gallardo, C.; Ginjaume-Garcia, N.; Ullmo, J.; Trilla, C.; Medina, M.C.; Vazquez, A.; Cruz-Lemini, M.; Llurba, E. Gestational Age-Adjusted Reference Ranges for Fetal Left Ventricle Longitudinal Strain by Automated Cardiac Motion Quantification between 24–37 Weeks’ Gestation. Fetal Diagn. Ther. 2022, 49, 311–320. [Google Scholar] [CrossRef] [PubMed]
- Barker, P.C.A.; Houle, H.; Li, J.S.; Miller, S.; Herlong, J.R.; Camitta, M.G.W. Global Longitudinal Cardiac Strain and Strain Rate for Assessment of Fetal Cardiac Function: Novel Experience with Velocity Vector Imaging. Echocardiography 2009, 26, 28–36. [Google Scholar] [CrossRef] [PubMed]
- Devore, G.R.; Polanco, B.; Satou, G.; Sklansky, M. Two-Dimensional Speckle Tracking of the Fetal Heart. J. Ultrasound Med. 2016, 35, 1765–1781. [Google Scholar] [CrossRef] [PubMed]
- Domínguez-Gallardo, C.; Ginjaume-García, N.; Ullmo, J.; Fernández-Oliva, A.; Parra, J.; Vázquez, A.; Cruz-Lemini, M.; Llurba, E. Longitudinal Behavior of Left-Ventricular Strain in Fetal Growth Restriction. Diagnostics 2023, 13, 1252. [Google Scholar] [CrossRef] [PubMed]
- Bijnens, B.; Cikes, M.; Butakoff, C.; Sitges, M.; Crispi, F. Myocardial Motion and Deformation: What Does It Tell Us and How Does It Relate to Function? Fetal Diagn. Ther. 2012, 32, 5–16. [Google Scholar] [CrossRef]
- van Oostrum, N.H.M.; Derks, K.; van der Woude, D.A.A.; Clur, S.A.; Oei, S.G.; van Laar, J.O.E.H. Two-Dimensional Speckle Tracking Echocardiography in Fetal Growth Restriction: A Systematic Review. Eur. J. Obstet. Gynecol. Reprod. Biol. 2020, 254, 87–94. [Google Scholar] [CrossRef]
- Robinson, H.P.; Sweet, E.M.; Adam, A.H. The Accuracy of Radiological Estimates of Gestational Age Using Early Fetal Crown-Rump Length Measurements By Ultrasound As a Basis for Comparison. BJOG Int. J. Obstet. Gynaecol. 1979, 86, 525–528. [Google Scholar] [CrossRef] [PubMed]
- Figueras, F.; Meler, E.; Iraola, A.; Eixarch, E.; Coll, O.; Figueras, J.; Francis, A.; Gratacos, E.; Gardosi, J. Customized Birthweight Standards for a Spanish Population. Eur. J. Obstet. Gynecol. Reprod. Biol. 2008, 136, 20–24. [Google Scholar] [CrossRef]
- Crispi, F.; Hernandez-Andrade, E.; Pelsers, M.M.A.L.; Plasencia, W.; Benavides-Serralde, J.A.; Eixarch, E.; Le Noble, F.; Ahmed, A.; Glatz, J.F.C.; Nicolaides, K.H.; et al. Cardiac Dysfunction and Cell Damage across Clinical Stages of Severity in Growth-Restricted Fetuses. Am. J. Obstet. Gynecol. 2008, 199, 254.e1–254.e8. [Google Scholar] [CrossRef]
- Hernandez-andrade, E.; Andres, J. Evaluation of Conventional Doppler Fetal Cardiac Function Parameters: E/A Ratios, Outflow Tracts, and Myocardial Performance Index. Fetal Diagn. Ther. 2012, 32, 22–29. [Google Scholar] [CrossRef]
- Naujorks, A.A.; Zielinsky, P.; Beltrame, P.A.; Castagna, R.C.; Petracco, R.; Busato, A.; Nicoloso, A.L.H.; Piccoli, A.; Manica, J.L. Myocardial Tissue Doppler Assessment of Diastolic Function in the Growth-Restricted Fetus. Ultrasound Obstet. Gynecol. 2009, 34, 68–73. [Google Scholar] [CrossRef]
- Germanakis, I.; Gardiner, H. Assessment of Fetal Myocardial Deformation Using Speckle Tracking Techniques. Fetal Diagn. Ther. 2012, 32, 39–46. [Google Scholar] [CrossRef]
- Chambers Gurson, S. Advances in Fetal Echocardiography: Myocardial Deformation Analysis, Cardiac MRI and Three-Dimensional Printing. Curr. Opin. Cardiol. 2019, 34, 35–40. [Google Scholar] [CrossRef]
- de Waal, K.; Phad, N. A Comparison between Philips and Tomtec for Left Ventricular Deformation and Volume Measurements in Neonatal Intensive Care Patients. Echocardiography 2018, 35, 375–379. [Google Scholar] [CrossRef] [PubMed]
- Crispi, F.; Bijnens, B.; Figueras, F.; Bartrons, J.; Eixarch, E.; Le Noble, F.; Ahmed, A.; Gratacós, E. Fetal Growth Restriction Results in Remodeled and Less Efficient Hearts in Children. Circulation 2010, 121, 2427–2436. [Google Scholar] [CrossRef]
- Patey, O.; Carvalho, J.S.; Thilaganathan, B. Perinatal Changes in Cardiac Geometry and Function in Growth-Restricted Fetuses at Term. Ultrasound Obstet. Gynecol. 2019, 53, 655–662. [Google Scholar] [CrossRef] [PubMed]
- Girsen, A.; Ala-Kopsala, M.; Mäkikallio, K.; Vuolteenaho, O.; Räsänen, J. Cardiovascular Hemodynamics and Umbilical Artery N-Terminal Peptide of ProB-Type Natriuretic Peptide in Human Fetuses with Growth Restriction. Ultrasound Obstet. Gynecol. 2007, 29, 296–303. [Google Scholar] [CrossRef]
- Hobbs, F.D.R. Reliability of N-Terminal pro-Brain Natriuretic Peptide Assay in Diagnosis of Heart Failure: Cohort Study in Representative and High Risk Community Populations. BMJ 2002, 324, 1498. [Google Scholar] [CrossRef]
- Baschat, A.A.; Cosmi, E.; Bilardo, C.M.; Wolf, H.; Berg, C.; Rigano, S.; Germer, U.; Moyano, D.; Turan, S.; Hartung, J.; et al. Predictors of Neonatal Outcome in Early-Onset Placental Dysfunction. Obstet. Gynecol. 2007, 109, 253–261. [Google Scholar] [CrossRef] [PubMed]
Variable | SGA (n = 5) | FGR I (n = 30) | FGR ≥ II (n = 5) | p |
---|---|---|---|---|
Clinical characteristics | ||||
Maternal age, years | 35 ± 6 | 34 ± 6 | 31 ± 2 | 0.473 |
Caucasian | 100 (5) | 80 (24) | 40 (2) | 0.195 |
Latin-American | 0 (0) | 10 (3) | 40 (2) | 0.195 |
Body mass index at inclusion, kg/m2 | 25.8 ± 5.8 | 23.6 ± 4.8 | 25.2 ± 3.6 | 0.564 |
Nulliparity | 100 (5) | 53.3 (16) | 40 (2) | 0.104 |
Pregnancy outcome | ||||
Neonatal male sex | 20 (1) | 33.3 (10) | 100 (5) | 0.012 |
Preeclampsia | 20 (1) | 10 (3) | 20 (1) | 0.710 |
GA at delivery | 39.2 ± 1.4 | 37.1 ± 2.8 | 29.7 ± 3.1 *† | <0.001 |
Vaginal delivery | 80 (4) | 66.6 (20) | 0 (0) | 0.032 |
Caesarean delivery | 20 (1) | 33.3 (10) | 100 (5) | 0.032 |
Birth weight, g | 2577 ± 210 | 2215 ± 488 | 1233 ± 464 *† | <0.001 |
Birth weight centile APGAR 1′ APGAR 5′ Neonatal intensive care unit admission | 3 ± 1 8 ± 2 9 ± 2 25 (1) | 2 ± 3 8 ± 1 9 ± 2 22 (6) | 1 ± 2 6 ± 2 8 ± 1 100 (5) | 0.463 0.071 0.473 0.003 |
Perinatal mortality | 0 (0) | 3.3 (1) | 40 (2) | 0.012 |
Variable | SGA (n = 5) | FGR I (n = 30) | FGR ≥ II (n = 5) | p |
---|---|---|---|---|
Fetoplacental US | ||||
GA at US (weeks) | 31.2 ± 0.6 | 30.9 ± 3.5 | 28.7 ± 2.6 | 0.317 |
EFW (g) | 1433 ± 75 | 1353 ± 531 | 943 ± 365 | 0.171 |
EFW (centile) | 5 ± 2 | 2 ± 2 | 1 ± 2 * | 0.027 |
UA-PI (Zs) | 0.09 ± 0.67 | 0.62 ± 1.20 | 3.93 ± 1.90 *† | <0.001 |
MCA-PI (Zs) | −0.17 ± 0.91 | −0.20 ± 1.13 | −1.56 ± 0.59 *† | 0.035 |
CPR (Zs) | −0.64 ± 1.04 | −1.02 ± 1.15 | −3.18 ± 0.50 *† | 0.002 |
UtA-PI (Zs) | 0.75 ± 0.67 † | 1.93 ± 1.60 | 3.53 ± 0.78 * | 0.008 |
LV strain values (Zs) | ||||
GLS | −1.85 ± 1.44 | −2.54 ± 2.06 | −5.27± 2.43 *† | <0.05 |
BAL | −0.49 ± 1.42 | −0.08 ± 1.23 | −1.98 ± 3.05 † | <0.05 |
MAL | 0.20 ± 0.78 | 0.34 ± 0.90 | 1.37 ± 0.94 | 0.053 |
AAL | −1.04 ± 1.36 | −1.90 ± 2.10 | −2.74 ± 2.45 | 0.369 |
BIS | 0.31 ± 0.85 | 1.15 ± 1.17 | −0.34 ± 0.68 | 0.093 |
MIS | 0.62 ± 1.97 | −0.29 ± 1.40 | −1.20 ± 0.89 | 0.324 |
AIS | −2.29 ± 2.33 | −1.92 ± 2.75 | −5.04 ± 2.64 | 0.065 |
EF | −0.43 ± 1.39 | −0.52 ± 2.32 | −1.90 ± 1.99 | 0.410 |
Differences in Least Squares Means | |||
---|---|---|---|
LV Strain Evaluation (Zs) | Group | Estimate (SE) | Adj p |
GLS Zs | |||
SGA vs. FGR I | 1.03 (0.56) | 0.167 | |
SGA vs. FGR ≥ II | 3.27 (0.96) | 0.003 | |
FGR I vs. FGR ≥ II | 2.24 (0.85) | 0.029 | |
BIS Zs | |||
SGA vs. FGR I | 0.13 (0.33) | 0.913 | |
SGA vs. FGR ≥ II | 0.17 (0.54) | 0.944 | |
FGR I vs. FGR ≥ II | 0.04 (0.48) | 0.996 | |
MIS Zs | |||
SGA vs. FGR I | 0.64 (0.37) | 0.209 | |
SGA vs. FGR ≥ II | 1.57 (0.64) | 0.046 | |
FGR I vs. FGR ≥ II | 0.93 (0.57) | 0.247 | |
AIS Zs | |||
SGA vs. FGR I | 0.95 (0.74) | 0.409 | |
SGA vs. FGR ≥ II | 2.77 (1.24) | 0.075 | |
FGR I vs. FGR ≥ II | 1.82 (1.11) | 0.238 | |
BAL Zs | |||
SGA vs. FGR I | −1.04 (0.41) | 0.035 | |
SGA vs. FGR ≥ II | −0.29 (0.69) | 0.909 | |
FGR I vs. FGR ≥ II | 0.76 (0.62) | 0.442 | |
MAL Zs | |||
SGA vs. FGR I | −0.03 (0.22) | 0.992 | |
SGA vs. FGR ≥ II | −0.66 (0.38) | 0.203 | |
FGR I vs. FGR ≥ II | −0.64 (0.34) | 0.159 | |
AAL Zs | |||
SGA vs. FGR I | 1.46 (0.49) | 0.012 | |
SGA vs. FGR ≥ II | 3.15 (0.85) | 0.001 | |
FGR I vs. FGR ≥ II | 1.68 (0.76) | 0.078 | |
EF Zs | |||
SGA vs. FGR I | 0.46 (0.49) | 0.623 | |
SGA vs. FGR ≥ II | 3.12 (0.90) | 0.003 | |
FGR I vs. FGR ≥ II | 3.59 (0.80) | 0.000 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Domínguez-Gallardo, C.; Ginjaume-García, N.; Ullmo, J.; Parra, J.; Vázquez, A.; Cruz-Lemini, M.; Llurba, E. Fetal Left Ventricle Function Evaluated by Two-Dimensional Speckle-Tracking Echocardiography across Clinical Stages of Severity in Growth-Restricted Fetuses. Diagnostics 2024, 14, 548. https://doi.org/10.3390/diagnostics14050548
Domínguez-Gallardo C, Ginjaume-García N, Ullmo J, Parra J, Vázquez A, Cruz-Lemini M, Llurba E. Fetal Left Ventricle Function Evaluated by Two-Dimensional Speckle-Tracking Echocardiography across Clinical Stages of Severity in Growth-Restricted Fetuses. Diagnostics. 2024; 14(5):548. https://doi.org/10.3390/diagnostics14050548
Chicago/Turabian StyleDomínguez-Gallardo, Carla, Nuria Ginjaume-García, Johana Ullmo, Juan Parra, Ana Vázquez, Mónica Cruz-Lemini, and Elisa Llurba. 2024. "Fetal Left Ventricle Function Evaluated by Two-Dimensional Speckle-Tracking Echocardiography across Clinical Stages of Severity in Growth-Restricted Fetuses" Diagnostics 14, no. 5: 548. https://doi.org/10.3390/diagnostics14050548