Placental Shear Wave Elastography Assessment in Early and Late Fetal Growth Restriction
Abstract
1. Introduction
2. Materials and Methods
2.1. Design and Study Population
2.2. Equipment and Methods
- All FGR vs. AGA
- Early FGR vs. late FGR
- Early FGR vs. AGA
- Late FGR vs. AGA
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
SWE | Shear wave elastography |
SWV | Shear wave velocity |
FGR | Fetal growth restriction |
AGA | Appropriate (growth) for gestational age |
ISUOG | International Society for Ultrasound in Obstetrics and Gynecology |
AC | Abdominal circumference |
EFW | Estimated fetal weight |
CPR | Cerebroplacental ratio |
UA PI | Umbilical artery pulsatility index |
MCA PI | Middle cerebral artery pulsatility index |
DV PI | Ductus venosus pulsatility index |
DV PVIV | Ductus venosus peak velocity index for veins |
ROI | Region of interest |
BMI | Body mass index |
ANOVA | Analysis of Variance |
SGA | Small for gestational age |
CI | Confidence interval |
PET | Pre-eclampsia toxemia |
References
- Lawn, J.E.; Ohuma, E.O.; Bradley, E.; Idueta, L.S.; Hazel, E.; Okwaraji, Y.B.; Erchick, D.J.; Yargawa, J.; Katz, J.; Lee, A.C.C.; et al. Small babies, big risks: Global estimates of prevalence and mortality for vulnerable newborns to accelerate change and improve counting. Lancet 2023, 401, 1707–1719. [Google Scholar] [CrossRef] [PubMed]
- Triggs, T.; Crawford, K.; Hong, J.; Clifton, V.; Kumar, S. The influence of birthweight on mortality and severe neonatal morbidity in late preterm and term infants: An Australian cohort study. Lancet Reg. Health West. Pac. 2024, 45, 101054. [Google Scholar] [CrossRef]
- de Mendonça, E.L.S.S.; de Lima Macêna, M.; Bueno, N.B.; de Oliveira, A.C.M.; Mello, C.S. Premature birth, low birth weight, small for gestational age and chronic non-communicable diseases in adult life: A systematic review with meta-analysis. Early Human Dev. 2020, 149, 105154. [Google Scholar] [CrossRef] [PubMed]
- Audette, M.C.; Kingdom, J.C. Screening for fetal growth restriction and placental insufficiency. Semin. Fetal Neonatal Med. 2018, 23, 119–125. [Google Scholar] [CrossRef]
- Burton, G.J.; Jauniaux, E. Pathophysiology of placental-derived fetal growth restriction. Am. J. Obstet. Gynecol. 2018, 218, S745–S761. [Google Scholar] [CrossRef]
- Levytska, K.; Higgins, M.; Keating, S.; Melamed, N.; Walker, M.; Sebire, N.J.; Kingdom, J.C. Placental Pathology in Relation to Uterine Artery Doppler Findings in Pregnancies with Severe Intrauterine Growth Restriction and Abnormal Umbilical Artery Doppler Changes. Am. J. Perinatol. 2017, 34, 451–457. [Google Scholar] [CrossRef]
- Khong, Y.; Brosens, I. Defective deep placentation. Best Pract. Res. Clin. Obstet. Gynaecol. 2011, 25, 301–311. [Google Scholar] [CrossRef] [PubMed]
- Schiffer, V.; van Haren, A.; De Cubber, L.; Bons, J.; Coumans, A.; van Kuijk, S.M.; Spaanderman, M.; Al-Nasiry, S. Ultrasound evaluation of the placenta in healthy and placental syndrome pregnancies: A systematic review. Eur. J. Obstet. Gynecol. Reprod. Biol. 2021, 262, 45–56. [Google Scholar] [CrossRef]
- Abramowicz, J.S.; Sheiner, E. Ultrasound of the placenta: A systematic approach. Part I: Imaging. Placenta 2008, 29, 225–240. [Google Scholar] [CrossRef]
- Abramowicz, J.S.; Sheiner, E. Ultrasound of the placenta: A systematic approach. Part II: Functional assessment (Doppler). Placenta 2008, 29, 921–929. [Google Scholar] [CrossRef]
- Lees, C.C.; Stampalija, T.; Baschat, A.; da Silva Costa, F.; Ferrazzi, E.; Figueras, F.; Hecher, K.; Kingdom, J.; Poon, L.C.; Salomon, L.J.; et al. ISUOG Practice Guidelines: Diagnosis and management of small-for-gestational-age fetus and fetal growth restriction. Ultrasound Obstet. Gynecol. 2020, 56, 298–312. [Google Scholar] [CrossRef] [PubMed]
- Brosens, I.; Pijnenborg, R.; Vercruysse, L.; Romero, R. The “Great Obstetrical Syndromes” are associated with disorders of deep placentation. Am. J. Obstet. Gynecol. 2011, 204, 193–201. [Google Scholar] [CrossRef] [PubMed]
- Sigrist, R.M.S.; Liau, J.; Kaffas, A.E.; Chammas, M.C.; Willmann, J.K. Ultrasound Elastography: Review of Techniques and Clinical Applications. Theranostics 2017, 7, 1303–1329. [Google Scholar] [CrossRef] [PubMed]
- Cosgrove, D.; Piscaglia, F.; Bamber, J.; Bojunga, J.; Correas, J.M.; Gilja, O.H.; Klauser, A.S.; Sporea, I.; Calliada, F.; Cantisani, V.; et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall Med. 2013, 34, 238–253. [Google Scholar] [CrossRef]
- Ferraioli, G.; Parekh, P.; Levitov, A.B.; Filice, C. Shear wave elastography for evaluation of liver fibrosis. J. Ultrasound Med. 2014, 33, 197–203. [Google Scholar] [CrossRef]
- Özkaya, N.; Leger, D.; Goldsheyder, D.; Nordin, M. Mechanical Properties of Biological Tissues. In Fundamentals of Biomechanics: Equilibrium, Motion, and Deformation; Özkaya, N., Leger, D., Goldsheyder, D., Nordin, M., Eds.; Springer International Publishing: Cham, Switzerlands, 2017; pp. 361–387. [Google Scholar]
- Shiina, T.; Nightingale, K.R.; Palmeri, M.L.; Hall, T.J.; Bamber, J.C.; Barr, R.G.; Castera, L.; Choi, B.I.; Chou, Y.H.; Cosgrove, D.; et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 1: Basic principles and terminology. Ultrasound Med. Biol. 2015, 41, 1126–1147. [Google Scholar] [CrossRef]
- Ferraioli, G.; Wong, V.W.-S.; Castera, L.; Berzigotti, A.; Sporea, I.; Dietrich, C.F.; Choi, B.I.; Wilson, S.R.; Kudo, M.; Barr, R.G. Liver Ultrasound Elastography: An Update to the World Federation for Ultrasound in Medicine and Biology Guidelines and Recommendations. Ultrasound Med. Biol. 2018, 44, 2419–2440. [Google Scholar] [CrossRef]
- Edwards, C.; Cavanagh, E.; Kumar, S.; Clifton, V.; Fontanarosa, D. The use of elastography in placental research—A literature review. Placenta 2020, 99, 78–88. [Google Scholar] [CrossRef]
- Ohmaru, T.; Fujita, Y.; Sugitani, M.; Shimokawa, M.; Fukushima, K.; Kato, K. Placental elasticity evaluation using virtual touch tissue quantification during pregnancy. Placenta 2015, 36, 915–920. [Google Scholar] [CrossRef]
- Arioz Habibi, H.; Alici Davutoglu, E.; Kandemirli, S.G.; Aslan, M.; Ozel, A.; Kalyoncu Ucar, A.; Zeytun, P.; Madazli, R.; Adaletli, I. In vivo assessment of placental elasticity in intrauterine growth restriction by shear-wave elastography. Eur. J. Radiol. 2017, 97, 16–20. [Google Scholar] [CrossRef]
- Akbas, M.; Koyuncu, F.M.; Artunç-Ulkumen, B. Placental elasticity assessment by point shear wave elastography in pregnancies with intrauterine growth restriction. J. Perinat. Med. 2019, 47, 841–846. [Google Scholar] [CrossRef] [PubMed]
- Anuk, A.T.; Tanacan, A.; Erol, S.A.; Alkan, M.; Altinboga, O.; Celen, S.; Keskin, H.L.; Sahin, D. Value of shear-wave elastography and cerebral-placental-uterine ratio in women diagnosed with preeclampsia and fetal growth restriction in prediction of adverse perinatal outcomes. J. Matern. Fetal Neonatal Med. 2022, 35, 10001–10009. [Google Scholar] [CrossRef] [PubMed]
- Menon, A.; Meena, J.; Manchanda, S.; Singhal, S.; Shivhare, S.; Kumar, S. Role of Placental Vascularization Indices and Shear Wave Elastography in Fetal Growth Restriction. J. Obstet. Gynaecol. India 2023, 73, 75–82. [Google Scholar] [CrossRef]
- Imtiaz, S.; Naz, N.; Walid, A.; Rahim, A.; Waseem, H.F. Role Of Shear Wave Elastography In Assessment Of Placental Elasticity In Normal And High-Risk Pregnancies In Third Trimester. J. Pak. Med. Assoc. 2023, 73, 2205–2208. [Google Scholar] [CrossRef] [PubMed]
- Ansar, M.; Ali, M.A.; Ali, N.; Haider, Z.; Latif, A.; Tazeen, A.; Fatima, Z.; Anjum, M.N. Ultrasound shear wave elastography of the placenta: A potential tool for early detection of fetal growth restriction. Clin. Imaging 2024, 116, 110329. [Google Scholar] [CrossRef]
- Hasegawa, T.; Kuji, N.; Notake, F.; Tsukamoto, T.; Sasaki, T.; Shimizu, M.; Mukaida, K.; Ito, H.; Isaka, K.; Nishi, H. Ultrasound elastography can detect placental tissue abnormalities. Radiol. Oncol. 2018, 52, 129–135. [Google Scholar] [CrossRef]
- Gordijn, S.J.; Beune, I.M.; Thilaganathan, B.; Papageorghiou, A.; Baschat, A.A.; Baker, P.N.; Silver, R.M.; Wynia, K.; Ganzevoort, W. Consensus definition of fetal growth restriction: A Delphi procedure. Ultrasound Obstet. Gynecol. 2016, 48, 333–339. [Google Scholar] [CrossRef]
- World Medical Association. World Medical Association Declaration of Helsinki: Ethical Principles for Medical Research Involving Human Subjects. JAMA 2013, 310, 2191–2194. [Google Scholar] [CrossRef]
- Khalil, A.; Sotiriadis, A.; D’Antonio, F.; Da Silva Costa, F.; Odibo, A.; Prefumo, F.; Papageorghiou, A.T.; Salomon, L.J. ISUOG Practice Guidelines: Performance of third-trimester obstetric ultrasound scan. Ultrasound Obstet. Gynecol. 2024, 63, 131–147. [Google Scholar] [CrossRef]
- Hadlock, F.P.; Harrist, R.B.; Sharman, R.S.; Deter, R.L.; Park, S.K. Estimation of fetal weight with the use of head, body, and femur measurements--a prospective study. Am. J. Obstet. Gynecol. 1985, 151, 333–337. [Google Scholar] [CrossRef]
- Flatley, C.; Kumar, S.; Greer, R.M. Reference centiles for the middle cerebral artery and umbilical artery pulsatility index and cerebro-placental ratio from a low-risk population—A Generalised Additive Model for Location, Shape and Scale (GAMLSS) approach. J. Matern. Fetal Neonatal Med. 2019, 32, 2338–2345. [Google Scholar] [CrossRef] [PubMed]
- Kessler, J.; Rasmussen, S.; Hanson, M.; Kiserud, T. Longitudinal reference ranges for ductus venosus flow velocities and waveform indices. Ultrasound Obstet. Gynecol. 2006, 28, 890–898. [Google Scholar] [CrossRef] [PubMed]
- Cavoretto, P.I.; Salmeri, N.; Candiani, M.; Farina, A. Reference ranges of uterine artery pulsatility index from first to third trimester based on serial Doppler measurements: Longitudinal cohort study. Ultrasound Obstet. Gynecol. 2023, 61, 474–480. [Google Scholar] [CrossRef] [PubMed]
- Edwards, C.; Cavanagh, E.; Kumar, S.; Clifton, V.L.; Borg, D.J.; Priddle, J.; Wille, M.L.; Drovandi, C.; Fontanarosa, D. Changes in placental elastography in the third trimester—Analysis using a linear mixed effect model. Placenta 2021, 114, 83–89. [Google Scholar] [CrossRef]
- Cavanagh, E.; Crawford, K.; Hong, J.G.S.; Fontanarosa, D.; Edwards, C.; Wille, M.L.; Hong, J.; Clifton, V.L.; Kumar, S. The Relationship between Placental Shear Wave Elastography and Fetal Weight-A Prospective Study. J. Clin. Med. 2024, 13, 4432. [Google Scholar] [CrossRef]
- Weiher, M.; Richtering, F.G.; Dörffel, Y.; Müller, H.P. Simplification of 2D shear wave elastography by enlarged SWE box and multiple regions of interest in one acquisition. PLoS ONE 2022, 17, e0273769. [Google Scholar] [CrossRef]
- Edwards, C.; Cavanagh, E.; Kumar, S.; Clifton, V.; Fontanarosa, D. Intra-system reliability assessment of 2-dimensional shear wave elastography. Appl. Sci. 2021, 11, 2992. [Google Scholar] [CrossRef]
- O’Hara, S.; Zelesco, M.; Rocke, K.; Stevenson, G.; Sun, Z. Reliability Indicators for 2-Dimensional Shear Wave Elastography. J. Ultrasound Med. 2019, 38, 3065–3071. [Google Scholar] [CrossRef]
- AIUM. Recommended Maximum Scanning Times for Displayed Thermal Index (TI) Values. Available online: https://www.aium.org/resources/official-statements/view/recommended-maximum-scanning-times-for-displayed-thermal-index-(ti)-values (accessed on 4 August 2023).
- Harris, P.A.; Taylor, R.; Thielke, R.; Payne, J.; Gonzalez, N.; Conde, J.G. Research electronic data capture (REDCap)—A metadata-driven methodology and workflow process for providing translational research informatics support. J. Biomed. Inform. 2009, 42, 377–381. [Google Scholar] [CrossRef]
- Harris, P.A.; Taylor, R.; Minor, B.L.; Elliott, V.; Fernandez, M.; O’Neal, L.; McLeod, L.; Delacqua, G.; Delacqua, F.; Kirby, J.; et al. The REDCap consortium: Building an international community of software platform partners. J. Biomed. Inform. 2019, 95, 103208. [Google Scholar] [CrossRef]
- Wolff, R.F.; Moons, K.G.M.; Riley, R.D.; Whiting, P.F.; Westwood, M.; Collins, G.S.; Reitsma, J.B.; Kleijnen, J.; Mallett, S. PROBAST: A Tool to Assess the Risk of Bias and Applicability of Prediction Model Studies. Ann. Intern. Med. 2019, 170, 51–58. [Google Scholar] [CrossRef]
- Heinze, G.; Wallisch, C.; Dunkler, D. Variable selection—A review and recommendations for the practicing statistician. Biom. J. 2018, 60, 431–449. [Google Scholar] [CrossRef]
- Edwards, C.; Cavanagh, E.; Kumar, S.; Clifton, V.L.; Borg, D.J.; Priddle, J.; Marie-Luise, W.; Drovandi, C.; Fontanarosa, D. Relationship between placental elastography, maternal pre-pregnancy body mass index and gestational weight gain. Placenta 2022, 121, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Mansournia, M.A.; Nazemipour, M. Recommendations for accurate reporting in medical research statistics. Lancet 2024, 403, 611–612. [Google Scholar] [CrossRef] [PubMed]
- von Elm, E.; Altman, D.G.; Egger, M.; Pocock, S.J.; Gøtzsche, P.C.; Vandenbroucke, J.P. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for reporting observational studies. J. Clin. Epidemiol. 2008, 61, 344–349. [Google Scholar] [CrossRef] [PubMed]
- Saw, S.N.; Dai, Y.; Yap, C.H. A Review of Biomechanics Analysis of the Umbilical-Placenta System With Regards to Diseases. Front. Physiol. 2021, 12, 587635. [Google Scholar] [CrossRef]
- Altunkeser, A.; Alkan, E.; Günenç, O.; İsmet, T.; Körez, M.K. Evaluation of a Healthy Pregnant Placenta with Shear Wave Elastography. Iran. J. Radiol. 2019, 16, e68280. [Google Scholar] [CrossRef]
- Townsend, R.; Khalil, A.; Premakumar, Y.; Allotey, J.; Snell, K.I.E.; Chan, C.; Chappell, L.C.; Hooper, R.; Green, M.; Mol, B.W.; et al. Prediction of pre-eclampsia: Review of reviews. Ultrasound Obstet. Gynecol. 2019, 54, 16–27. [Google Scholar] [CrossRef]
- Xiao, R.; Sorensen, T.K.; Williams, W.A.; Luthy, D.A. Influence of pre-eclampsia on fetal growth. J. Matern.-Fetal Neonatal Med. 2003, 13, 157–162. [Google Scholar] [CrossRef]
- Burton, G.J.; Jauniaux, E. What is the placenta? Am. J. Obstet. Gynecol. 2015, 213, S6.e1–S6.e4. [Google Scholar] [CrossRef]
- Abramowicz, J.S.; Sheiner, E. In utero imaging of the placenta: Importance for diseases of pregnancy. Placenta 2007, 28 (Suppl. A), S14–S22. [Google Scholar] [CrossRef] [PubMed]
- Kingdom, J.C.; Audette, M.C.; Hobson, S.R.; Windrim, R.C.; Morgen, E. A placenta clinic approach to the diagnosis and management of fetal growth restriction. Am. J. Obstet. Gynecol. 2018, 218, S803–S817. [Google Scholar] [CrossRef] [PubMed]
- Brosens, I.; Puttemans, P.; Benagiano, G. Placental bed research: I. The placental bed: From spiral arteries remodeling to the great obstetrical syndromes. Am. J. Obstet. Gynecol. 2019, 221, 437–456. [Google Scholar] [CrossRef]
- Morley, L.C.; Debant, M.; Walker, J.J.; Beech, D.J.; Simpson, N.A.B. Placental blood flow sensing and regulation in fetal growth restriction. Placenta 2021, 113, 23–28. [Google Scholar] [CrossRef] [PubMed]
Total | Early FGR | Late FGR | AGA | p-Value | |
---|---|---|---|---|---|
N = 222 | N = 56 | N = 33 | N = 133 | ||
Age | 31 ± 6 | 33 ± 5 | 30 ± 5 | 31 ± 6 | 0.058 |
Body Mass Index at recruitment (kg/m2) | 25 (21, 31) | 26 (23, 31) | 24 (21, 27) | 24 (21, 31) | 0.062 |
Mean Arterial Pressure at time of recruitment (mmHg) | 82 (77, 88) | 83 (77, 93) | 82 (78, 87) | 82 (77, 87) | 0.190 |
Nulliparous | 86 (38.7%) | 24 (42.9%) | 14 (42.4%) | 48 (36.1%) | 0.610 |
Born in Australia | 94 (42.3%) | 21(37.5% | 13 (39.4%) | 60 (45.1%) | 0.890 |
Born outside Australia | 128 (57.7%) | 35 (62.5%) | 20 (60.6%) | 73 (55.9%) | 0.720 |
Mode of Conception | 0.066 | ||||
Spontaneous | 205 (92.3%) | 48 (85.7%) | 30 (90.9%) | 127 (95.5%) | |
Assisted Reproductive Technology | 17 (7.7%) | 8 (14.3%) | 3 (9.1%) | 6 (4.5%) | |
Smoking during pregnancy | 21 (9.5%) | 5 (8.9%) | 7 (21.2%) | 9 (6.8%) | 0.039 |
Alcohol during pregnancy | 3 (1.4%) | 2 (3.6%) | 0 (0.0%) | 1 (0.8%) | 0.240 |
History of SGA baby | 73 (32.9%) | 22 (39.3%) | 11 (33.3%) | 40 (30.1%) | 0.470 |
Previous stillbirth | 15 (6.8%) | 5 (8.9%) | 0 (0.0%) | 10 (7.5%) | 0.230 |
Previous preterm birth | 27 (12.2%) | 12 (21.4%) | 4 (12.1%) | 11 (8.3%) | 0.041 |
Hypertension in current pregnancy | 43 (19.4%) | 18 (32.1%) | 4 (12.1%) | 21 (15.8%) | 0.018 |
Pre-eclampsia in current pregnancy | 36 (16.2%) | 21 (37.5%) | 4 (12.1%) | 11 (8.3%) | <0.001 |
Low dose aspirin use | 62 (27.9%) | 22 (39.3%) | 3 (9.1%) | 37 (27.8%) | 0.009 |
Connective tissue disease in pregnancy | 4 (1.8%) | 3 (5.4%) | 0 (0.0%) | 1 (0.8%) | 0.066 |
Low Molecular Weight Heparin use | 12 (5.4%) | 7 (12.5%) | 0 (0.0%) | 5 (3.8%) | 0.020 |
Diabetes in pregnancy | 65 (29.3%) | 25 (44.6%) | 5 (15.2%) | 35 (26.3%) | 0.006 |
Renal disease in pregnancy | 3 (1.4%) | 1 (1.8%) | 0 (0.0%) | 2 (1.5%) | 0.76 |
Gestational age at last scan before 32 weeks’ gestation | 28 (26, 30) | 28 (26, 30) | 31 (30, 31) | 28 (25, 30) | 0.021 |
Gestational age at last scan before birth | 35 (32, 36) | 33 (30, 35) | 36 (35, 37) | 36 (32, 36) | <0.001 |
EFW at last scan before 32 weeks’ gestation | 1126 (764, 1418) | 844 (628, 1223) | 1420 (1252, 1480) | 1171 (776, 1485) | 0.003 |
EFW at last scan before birth | 2190 (1627, 2493) | 1571 (1106, 1968) | 2136 (1895, 2288) | 2371 (1964, 2622) | <0.001 |
Gestational age at birth | 38 (37, 39) | 37 (32, 37) | 37 (37, 38) | 38 (37, 39) | <0.001 |
Mean SWV at last scan before 32 weeks’ gestation (m/s2) | 1.30 (1.22, 1.41) | 1.35 (1.22, 1.45) | 1.23 (1.19, 1.32) | 1.30 (1.21, 1.40) | 0.330 |
Mean SWV at last scan before delivery (m/s2) | 1.29 (1.21, 1.41) | 1.29 (1.22, 1.38) | 1.26 (1.20, 1.35) | 1.32 (1.21, 1.45) | 0.360 |
Average depth of SWV sample at last scan before 32 weeks’ gestation (cm) | 4.78 (3.82, 5.51) | 4.54 (3.65, 5.72) | 4.88 (4.26, 5.14) | 4.90 (3.87, 5.60) | 0.640 |
Average depth of SWV sample at last scan before delivery (cm) | 4.48 (3.80, 5.22) | 4.30 (3.68, 5.02) | 4.20 (3.72, 5.00) | 4.67 (3.90, 5.42) | 0.280 |
Model 1 | FGR vs. AGA (Last Scan Before 32-Weeks’ Gestation) | |
---|---|---|
Univariable Coefficient (95% CI) | p-Value | |
FGR | 0.13 (−0.25, 0.51) | 0.51 |
Model 2 | Early FGR vs. No early FGR (last scan before 32 weeks’ gestation) | |
Univariable coefficient (95% CI) | p-value | |
Early FGR | 0.27 (−0.13, 0.66) | 0.18 |
Model 3 | FGR vs. AGA (last scan before delivery) | |
Univariable coefficient (95% CI) | p-value | |
FGR | −0.09 (−0.36, 0.18) | 0.52 |
Model 4 | Early FGR vs. AGA (last scan before delivery) | |
Univariable coefficient (95% CI) | p-value | |
Early FGR | 0.09 (−0.22, 0.39) | 0.57 |
Model 5 | Late FGR vs. AGA (last scan before delivery) | |
Univariable coefficient (95% CI) | p-value | |
Late FGR | −0.29 (−0.65, 0.07) | 0.12 |
Model 1 | FGR vs. AGA (Last Scan Before 32-Weeks’ Gestation) | |
---|---|---|
Variable | Multivariable Coefficient (95% CI) | p-Value |
FGR | 0.21 (−0.17, 0.60) | 0.28 |
Pre-eclampsia | 1.48 (0.69, 2.27) | <0.001 |
FGR # Pre-eclampsia | −1.37 (−2.32, −0.42) | 0.005 |
BMI | 0.06 (0.03, 0.08) | <0.001 |
Model 2 | Early FGR vs. No early FGR (last scan before 32 weeks’ gestation) | |
Variable | Multivariable coefficient (95% CI) | p-value |
Early FGR | 0.36 (−0.06, 0.77) | 0.09 |
Pre-eclampsia | 1.50 (0.72, 2.28) | <0.001 |
FGR # Pre-eclampsia | −1.52 (−2.47, −0.56) | 0.002 |
BMI | 0.06 (0.03, 0.08) | <0.001 |
Model 3 | FGR vs. AGA (last scan before delivery) | |
Variable | Multivariable coefficient (95% CI) | p-value |
FGR | −0.002 (−0.28, 0.28) | 0.99 |
Pre-eclampsia | 1.10 (0.54, 1.66) | <0.001 |
FGR # Pre-eclampsia | −1.09 (−1.80, −0.38) | 0.003 |
BMI | 0.05 (0.03, 0.07) | <0.001 |
Model 4 | Early FGR vs. AGA (last scan before delivery) | |
Variable | Multivariable coefficient (95% CI) | p-value |
Early FGR | 0.13 (−0.21, 0.46) | 0.46 |
Pre-eclampsia | 0.90 (0.41, 1.39) | <0.001 |
FGR # Pre-eclampsia | −1.06 (−1.76, −0.36) | 0.003 |
BMI | 0.05 (0.03, 0.07) | <0.001 |
Model 5 | Late FGR vs. AGA (last scan before delivery) | |
Variable | Multivariable coefficient (95% CI) | p-value |
Late FGR | −0.13 (−0.48, 0.22) | 0.47 |
Pre-eclampsia | 1.10 (0.57, 1.63) | <0.001 |
FGR # Pre-eclampsia | −0.71 (−1.74, 0.33) | 0.18 |
BMI | 0.05 (0.03, 0.07) | <0.001 |
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. |
© 2025 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
Cavanagh, E.; Crawford, K.; Hong, J.; Fontanarosa, D.; Edwards, C.; Wille, M.-L.; Hong, J.; Clifton, V.L.; Kumar, S. Placental Shear Wave Elastography Assessment in Early and Late Fetal Growth Restriction. J. Clin. Med. 2025, 14, 4980. https://doi.org/10.3390/jcm14144980
Cavanagh E, Crawford K, Hong J, Fontanarosa D, Edwards C, Wille M-L, Hong J, Clifton VL, Kumar S. Placental Shear Wave Elastography Assessment in Early and Late Fetal Growth Restriction. Journal of Clinical Medicine. 2025; 14(14):4980. https://doi.org/10.3390/jcm14144980
Chicago/Turabian StyleCavanagh, Erika, Kylie Crawford, Jesrine Hong, Davide Fontanarosa, Christopher Edwards, Marie-Luise Wille, Jennifer Hong, Vicki L. Clifton, and Sailesh Kumar. 2025. "Placental Shear Wave Elastography Assessment in Early and Late Fetal Growth Restriction" Journal of Clinical Medicine 14, no. 14: 4980. https://doi.org/10.3390/jcm14144980
APA StyleCavanagh, E., Crawford, K., Hong, J., Fontanarosa, D., Edwards, C., Wille, M.-L., Hong, J., Clifton, V. L., & Kumar, S. (2025). Placental Shear Wave Elastography Assessment in Early and Late Fetal Growth Restriction. Journal of Clinical Medicine, 14(14), 4980. https://doi.org/10.3390/jcm14144980