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Published in: European Radiology 12/2023

19-07-2023 | Magnetic Resonance Imaging | Magnetic Resonance

Longitudinal assessment of placental perfusion in normal and hypertensive pregnancies using pseudo-continuous arterial spin–labeled MRI: preliminary experience

Authors: Christina L. Herrera, Yiming Wang, Durga Udayakumar, Yin Xi, Quyen N. Do, Matthew A. Lewis, David M. Owen, Baowei Fei, Catherine Y. Spong, Diane M. Twickler, Ananth J. Madhuranthakam

Published in: European Radiology | Issue 12/2023

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Abstract

Objectives

To evaluate longitudinal placental perfusion using pseudo-continuous arterial spin–labeled (pCASL) MRI in normal pregnancies and in pregnancies affected by chronic hypertension (cHTN), who are at the greatest risk for placental-mediated disease conditions.

Methods

Eighteen normal and 23 pregnant subjects with cHTN requiring antihypertensive therapy were scanned at 3 T using free-breathing pCASL-MRI at 16–20 and 24–28 weeks of gestational age.

Results

Mean placental perfusion was 103.1 ± 48.0 and 71.4 ± 18.3 mL/100 g/min at 16–20 and 24–28 weeks respectively in normal pregnancies and 79.4 ± 27.4 and 74.9 ± 26.6 mL/100 g/min in cHTN pregnancies. There was a significant decrease in perfusion between the first and second scans in normal pregnancies (p = 0.004), which was not observed in cHTN pregnancies (p = 0.36). The mean perfusion was not statistically different between normal and cHTN pregnancies at both scans, but the absolute change in perfusion per week was statistically different between these groups (p = 0.044). Furthermore, placental perfusion was significantly lower at both time points (p = 0.027 and 0.044 respectively) in the four pregnant subjects with cHTN who went on to have infants that were small for gestational age (52.7 ± 20.4 and 50.4 ± 20.9 mL/100 g/min) versus those who did not (85 ± 25.6 and 80.0 ± 25.1 mL/100 g/min).

Conclusion

pCASL-MRI enables longitudinal assessment of placental perfusion in pregnant subjects. Placental perfusion in the second trimester declined in normal pregnancies whereas it remained unchanged in cHTN pregnancies, consistent with alterations due to vascular disease pathology. Perfusion was significantly lower in those with small for gestational age infants, indicating that pCASL-MRI-measured perfusion may be an effective imaging biomarker for placental insufficiency.

Clinical relevance statement

pCASL-MRI enables longitudinal assessment of placental perfusion without administering exogenous contrast agent and can identify placental insufficiency in pregnant subjects with chronic hypertension that can lead to earlier interventions.

Key Points

Arterial spin–labeled (ASL) magnetic resonance imaging (MRI) enables longitudinal assessment of placental perfusion without administering exogenous contrast agent.
ASL-MRI-measured placental perfusion decreased significantly between 16-20 week and 24-28 week gestational age in normal pregnancies, while it remained relatively constant in hypertensive pregnancies, attributed to vascular disease pathology.
ASL-MRI-measured placental perfusion was significantly lower in subjects with hypertension who had a small for gestational age infant at 16–20-week gestation, indicating perfusion as an effective biomarker of placental insufficiency.
Literature
1.
go back to reference Harris LK, Benagiano M, D’Elios MM, Brosens I, Benagiano G (2019) Placental bed research: II. Functional and immunological investigations of the placental bed. Am J Obstet Gynecol 221:457–469CrossRefPubMed Harris LK, Benagiano M, D’Elios MM, Brosens I, Benagiano G (2019) Placental bed research: II. Functional and immunological investigations of the placental bed. Am J Obstet Gynecol 221:457–469CrossRefPubMed
2.
go back to reference Fisher S, McMaster M, Roberts JM (2015) The placenta in normal pregnancy and preeclampsia. In: Taylor RNRJ, Cunningham FG, Lindheimer MD (eds) Chesley’s hypertensive disorders in pregnancy. Elsevier, San Diego Fisher S, McMaster M, Roberts JM (2015) The placenta in normal pregnancy and preeclampsia. In: Taylor RNRJ, Cunningham FG, Lindheimer MD (eds) Chesley’s hypertensive disorders in pregnancy. Elsevier, San Diego
3.
go back to reference Combs CA, Katz MA, Kitzmiller JL, Brescia RJ (1993) Experimental preeclampsia produced by chronic constriction of the lower aorta: validation with longitudinal blood pressure measurements in conscious rhesus monkeys. Am J Obstet Gynecol 169:215–223CrossRefPubMed Combs CA, Katz MA, Kitzmiller JL, Brescia RJ (1993) Experimental preeclampsia produced by chronic constriction of the lower aorta: validation with longitudinal blood pressure measurements in conscious rhesus monkeys. Am J Obstet Gynecol 169:215–223CrossRefPubMed
4.
go back to reference Papageorghiou AT, Yu CK, Nicolaides KH (2004) The role of uterine artery Doppler in predicting adverse pregnancy outcome. Best Pract Res Clin Obstet Gynaecol 18:383–396CrossRefPubMed Papageorghiou AT, Yu CK, Nicolaides KH (2004) The role of uterine artery Doppler in predicting adverse pregnancy outcome. Best Pract Res Clin Obstet Gynaecol 18:383–396CrossRefPubMed
5.
go back to reference Myatt L, Clifton RG, Roberts JM et al (2012) The utility of uterine artery Doppler velocimetry in prediction of preeclampsia in a low-risk population. Obstet Gynecol 120:815–822CrossRefPubMedPubMedCentral Myatt L, Clifton RG, Roberts JM et al (2012) The utility of uterine artery Doppler velocimetry in prediction of preeclampsia in a low-risk population. Obstet Gynecol 120:815–822CrossRefPubMedPubMedCentral
6.
go back to reference Zun Z, Zaharchuk G, Andescavage NN, Donofrio MT, Limperopoulos C (2017) Non-invasive placental perfusion imaging in pregnancies complicated by fetal heart disease using velocity-selective arterial spin labeled MRI. Sci Rep 7:16126CrossRefPubMedPubMedCentral Zun Z, Zaharchuk G, Andescavage NN, Donofrio MT, Limperopoulos C (2017) Non-invasive placental perfusion imaging in pregnancies complicated by fetal heart disease using velocity-selective arterial spin labeled MRI. Sci Rep 7:16126CrossRefPubMedPubMedCentral
8.
go back to reference Shao X, Liu D, Martin T et al (2018) Measuring human placental blood flow with multidelay 3D GRASE pseudocontinuous arterial spin labeling at 3T. J Magn Reson Imaging 47:1667–1676CrossRefPubMed Shao X, Liu D, Martin T et al (2018) Measuring human placental blood flow with multidelay 3D GRASE pseudocontinuous arterial spin labeling at 3T. J Magn Reson Imaging 47:1667–1676CrossRefPubMed
9.
go back to reference Liu D, Shao X, Danyalov A et al (2020) Human placenta blood flow during early gestation with pseudocontinuous arterial spin labeling MRI. J Magn Reson Imaging 51:1247–1257CrossRefPubMed Liu D, Shao X, Danyalov A et al (2020) Human placenta blood flow during early gestation with pseudocontinuous arterial spin labeling MRI. J Magn Reson Imaging 51:1247–1257CrossRefPubMed
10.
go back to reference Harteveld AA, Hutter J, Franklin SL et al (2020) Systematic evaluation of velocity-selective arterial spin labeling settings for placental perfusion measurement. Magn Reson Med 84:1828–1843CrossRefPubMedPubMedCentral Harteveld AA, Hutter J, Franklin SL et al (2020) Systematic evaluation of velocity-selective arterial spin labeling settings for placental perfusion measurement. Magn Reson Med 84:1828–1843CrossRefPubMedPubMedCentral
11.
12.
go back to reference Zeeman GG, McIntire DD, Twickler DM (2003) Maternal and fetal artery Doppler findings in women with chronic hypertension who subsequently develop superimposed pre-eclampsia. J Matern Fetal Neonatal Med 14:318–323CrossRefPubMed Zeeman GG, McIntire DD, Twickler DM (2003) Maternal and fetal artery Doppler findings in women with chronic hypertension who subsequently develop superimposed pre-eclampsia. J Matern Fetal Neonatal Med 14:318–323CrossRefPubMed
13.
go back to reference Browne JC, Veall N (1953) The maternal placental blood flow in normotensive and hypertensive women. J Obstet Gynaecol Br Emp 60:141–147CrossRefPubMed Browne JC, Veall N (1953) The maternal placental blood flow in normotensive and hypertensive women. J Obstet Gynaecol Br Emp 60:141–147CrossRefPubMed
14.
go back to reference Brosens JJ, Pijnenborg R, Brosens IA (2002) The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: a review of the literature. Am J Obstet Gynecol 187:1416–1423CrossRefPubMed Brosens JJ, Pijnenborg R, Brosens IA (2002) The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: a review of the literature. Am J Obstet Gynecol 187:1416–1423CrossRefPubMed
15.
go back to reference ACOG (2017) Committee opinion no 700: methods for estimating the due date. Obstet Gynecol 129:e150–e154CrossRef ACOG (2017) Committee opinion no 700: methods for estimating the due date. Obstet Gynecol 129:e150–e154CrossRef
16.
go back to reference ACOG (2020) Practice bulletin no 222: gestational hypertension and preeclampsia. Obstet Gynecol 135:1492–1495CrossRef ACOG (2020) Practice bulletin no 222: gestational hypertension and preeclampsia. Obstet Gynecol 135:1492–1495CrossRef
17.
go back to reference ACOG (2021) Practice bulletin no 227: fetal growth restriction. Obstet Gynecol 137:385–387CrossRef ACOG (2021) Practice bulletin no 227: fetal growth restriction. Obstet Gynecol 137:385–387CrossRef
18.
go back to reference Duryea EL, Hawkins JS, McIntire DD, Casey BM, Leveno KJ (2014) A revised birth weight reference for the United States. Obstet Gynecol 124:16–22CrossRefPubMed Duryea EL, Hawkins JS, McIntire DD, Casey BM, Leveno KJ (2014) A revised birth weight reference for the United States. Obstet Gynecol 124:16–22CrossRefPubMed
19.
go back to reference Chappell LC, Enye S, Seed P, Briley AL, Poston L, Shennan AH (2008) Adverse perinatal outcomes and risk factors for preeclampsia in women with chronic hypertension: a prospective study. Hypertension 51:1002–1009CrossRefPubMed Chappell LC, Enye S, Seed P, Briley AL, Poston L, Shennan AH (2008) Adverse perinatal outcomes and risk factors for preeclampsia in women with chronic hypertension: a prospective study. Hypertension 51:1002–1009CrossRefPubMed
21.
go back to reference Hughes EJ, Price AN, McCabe L et al (2021) The effect of maternal position on venous return for pregnant women during MRI. NMR Biomed 34:e4475CrossRefPubMed Hughes EJ, Price AN, McCabe L et al (2021) The effect of maternal position on venous return for pregnant women during MRI. NMR Biomed 34:e4475CrossRefPubMed
22.
go back to reference Alsop DC, Detre JA, Golay X et al (2015) Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 73:102–116CrossRefPubMed Alsop DC, Detre JA, Golay X et al (2015) Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 73:102–116CrossRefPubMed
23.
go back to reference Greer JS, Wang X, Wang Y et al (2019) Robust pCASL perfusion imaging using a 3D Cartesian acquisition with spiral profile reordering (CASPR). Magn Reson Med 82:1713–1724CrossRefPubMedPubMedCentral Greer JS, Wang X, Wang Y et al (2019) Robust pCASL perfusion imaging using a 3D Cartesian acquisition with spiral profile reordering (CASPR). Magn Reson Med 82:1713–1724CrossRefPubMedPubMedCentral
24.
go back to reference Robson PM, Madhuranthakam AJ, Dai W, Pedrosa I, Rofsky NM, Alsop DC (2009) Strategies for reducing respiratory motion artifacts in renal perfusion imaging with arterial spin labeling. Magn Reson Med 61:1374–1387CrossRefPubMedPubMedCentral Robson PM, Madhuranthakam AJ, Dai W, Pedrosa I, Rofsky NM, Alsop DC (2009) Strategies for reducing respiratory motion artifacts in renal perfusion imaging with arterial spin labeling. Magn Reson Med 61:1374–1387CrossRefPubMedPubMedCentral
25.
go back to reference Zhang Y, Kapur P, Yuan Q et al (2016) Tumor vascularity in renal masses: correlation of arterial spin-labeled and dynamic contrast-enhanced magnetic resonance imaging assessments. Clin Genitourin Cancer 14:e25-36CrossRefPubMed Zhang Y, Kapur P, Yuan Q et al (2016) Tumor vascularity in renal masses: correlation of arterial spin-labeled and dynamic contrast-enhanced magnetic resonance imaging assessments. Clin Genitourin Cancer 14:e25-36CrossRefPubMed
26.
go back to reference Wang X, Greer JS, Dimitrov IE, Pezeshk P, Chhabra A, Madhuranthakam AJ (2018) Frequency offset corrected inversion pulse for B0 and B1 insensitive fat suppression at 3T: application to MR neurography of brachial plexus. J Magn Reson Imaging 48:1104–1111CrossRefPubMed Wang X, Greer JS, Dimitrov IE, Pezeshk P, Chhabra A, Madhuranthakam AJ (2018) Frequency offset corrected inversion pulse for B0 and B1 insensitive fat suppression at 3T: application to MR neurography of brachial plexus. J Magn Reson Imaging 48:1104–1111CrossRefPubMed
27.
go back to reference Gowland PA, Francis ST, Duncan KR et al (1998) In vivo perfusion measurements in the human placenta using echo planar imaging at 0.5 T. Magn Reson Med 40:467–473CrossRefPubMed Gowland PA, Francis ST, Duncan KR et al (1998) In vivo perfusion measurements in the human placenta using echo planar imaging at 0.5 T. Magn Reson Med 40:467–473CrossRefPubMed
28.
go back to reference Brosens I, Pijnenborg R, Vercruysse L, Romero R (2011) The “great obstetrical syndromes” are associated with disorders of deep placentation. Am J Obstet Gynecol 204:193–201CrossRefPubMed Brosens I, Pijnenborg R, Vercruysse L, Romero R (2011) The “great obstetrical syndromes” are associated with disorders of deep placentation. Am J Obstet Gynecol 204:193–201CrossRefPubMed
29.
go back to reference Brosens I, Puttemans P, Benagiano G (2019) Placental bed research: I. The placental bed: from spiral arteries remodeling to the great obstetrical syndromes. Am J Obstet Gynecol 221:437–456CrossRefPubMed Brosens I, Puttemans P, Benagiano G (2019) Placental bed research: I. The placental bed: from spiral arteries remodeling to the great obstetrical syndromes. Am J Obstet Gynecol 221:437–456CrossRefPubMed
30.
go back to reference Shahedi M, Spong CY, Dormer JD et al (2021) Deep learning-based segmentation of the placenta and uterus on MR images. J Med Imaging (Bellingham) 8:054001PubMed Shahedi M, Spong CY, Dormer JD et al (2021) Deep learning-based segmentation of the placenta and uterus on MR images. J Med Imaging (Bellingham) 8:054001PubMed
31.
go back to reference Morris D, Wright C, Dobbs M et al (2012) Arterial spin labelling in the human placenta–mapping perfusion Proc 20th Annual Meeting ISMRM, Melbourne Morris D, Wright C, Dobbs M et al (2012) Arterial spin labelling in the human placenta–mapping perfusion Proc 20th Annual Meeting ISMRM, Melbourne
32.
go back to reference Link D, Avisdris N, Shao X et al (2021) Multi-parametric functional and structural assessment of the placenta at late gestational ages using MRI. Proc 2021 Annual Meeting ISMRM, Virtual, p 3883 Link D, Avisdris N, Shao X et al (2021) Multi-parametric functional and structural assessment of the placenta at late gestational ages using MRI. Proc 2021 Annual Meeting ISMRM, Virtual, p 3883
Metadata
Title
Longitudinal assessment of placental perfusion in normal and hypertensive pregnancies using pseudo-continuous arterial spin–labeled MRI: preliminary experience
Authors
Christina L. Herrera
Yiming Wang
Durga Udayakumar
Yin Xi
Quyen N. Do
Matthew A. Lewis
David M. Owen
Baowei Fei
Catherine Y. Spong
Diane M. Twickler
Ananth J. Madhuranthakam
Publication date
19-07-2023
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 12/2023
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-023-09945-x

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