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Magnetic resonance imaging of the normal placenta
European Journal of Radiology 57 (2006) 256–260
Magnetic resonance imaging of the normal placenta Wibke Blaicher a,∗ , Peter C. Brugger b , Christoph Mittermayer c , Jens Schwindt c , Josef Deutinger a , Gerhard Bernaschek a , Daniela Prayer d a
c
Department of Gynecology and Obstetrics, University Hospital Vienna, Austria b Center of Anatomy and Cell Biology, University Hospital of Vienna, Austria Department of Pediatrics, Division of Neonatology and Intensive Care, University Hospital of Vienna, Austria d Department of Radiology, Division of Neuroradiology, University Hospital of Vienna, Austria Received 11 November 2005; received in revised form 14 November 2005; accepted 16 November 2005
Abstract The goal of this study was to provide a representative description of the normal placenta with contrast medium-free magnetic resonance imaging (MRI) in order to determine a standard of reference. One hundred consecutive singleton pregnancies were investigated by MRI without application of a contrast medium. The mean gestational age (GA) at the time of investigation was 29.5 weeks (range 19–40). Patients with suspected utero-placental insufficiency (UPI) or placental anomalies were excluded. Signal intensities were assessed and correlated with the respective GA. Antenatal MRI without contrast medium was able to depict placental status and morphological changes during gestation. A regular homogeneous structure was found in weeks 19–23. Subsequently, sporadic, slightly marked lobules appeared, which increased in number and markedness with ongoing gestation. Stratification of the lobules was observed after 36 weeks. The ratio of placental and amniotic fluid signal intensities decreased significantly with higher GA and with placental grading. MRI is well suited as an imaging method for the placenta. Our data may be used as a reference in the assessment of the placenta on MRI, and may have further clinical impact with respect to the determination of UPI. © 2005 Elsevier Ireland Ltd. All rights reserved. Keywords: Antenatal diagnosis; Magnetic resonance imaging; MRI; Placenta
1. Introduction Examination of the placenta and gravid uterus is an integral part of any obstetric sonographic study. Fetal well-being and growth depend on an intact utero-placental vascular supply. Prenatal management of fetuses with suspected placental insufficiency depends mainly on Doppler studies, combined with growth curves and cardiotocography. Sonography can show most macroscopic abnormalities that may adversely affect the placenta or the gravid uterus, and that may compromise the fetus or affect the mode of delivery [1]. However, sonographic visualization of the placenta can be difficult due to impaired sonographic conditions and due to the limited ∗ Corresponding author at: Department of Gynecology and Obstetrics, University Hospital Vienna, W¨ahringer G¨urtel 18-20, 1090 Vienna, Austria. Tel.: +43 1 40 400 2994; fax: +43 1 40 400 2995. E-mail address: [email protected] (W. Blaicher).
0720-048X/$ – see front matter © 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2005.11.025
soft tissue contrast. Furthermore, in cases of unclear diagnosis with ultrasound (US), additional investigation may be necessary to provide the best possible perinatal management for the mother and the fetus. MRI is a valuable adjunct in fetal evaluation [2–6]. Ultrafast MRI sequences effectively suppress fetal motion artefacts and avoid sedation. The high spatial resolution of MRI, the multiplanar capabilities, the large field of view, and the high soft tissue contrast that enables simultaneous visualization of fetal and maternal structures, have proven to be advantageous in antenatal examinations, particularly in the evaluation of the central nervous system [7–10]. MRI can demonstrate the uterine wall, placenta, amniotic fluid, and fetus with excellent contrast [11,12]. Reports of MRI of the utero-placental unit are rather rare and mostly concern pregnancies with fetal or placental pathologies [13–15], where MRI was used to confirm or elaborate findings from other diagnostic methods. Surpris-
W. Blaicher et al. / European Journal of Radiology 57 (2006) 256–260
ingly little attention has been paid to the MRI appearance of the normal placenta, though the knowledge gained might provide the basis for MRI-based diagnosis in a much wider range of utero-placental anomalies and enable a better use of this technique. The normal placenta was described using gadoliniumenhanced dynamic MRI in 1997 [16]. However, MRI of the normal placenta without contrast media has not yet been published. The purpose of this study was to provide a standard of reference for the appearance of the normal placenta on non-invasive MRI.
2. Patients and methods We reviewed the antenatal MR images of 100 pregnancies from January 2000 to August 2003. MRI was performed at the Department of Radiology, University of Vienna.
257
weighted sequences (15–19 s acquisition-time; 30 min total time per investigation) in three section planes (axial, sagittal, and coronal), and a 3–5 mm slice-thickness. Adequate anatomical visualisation of the uterus and the placentary tissue were obtained in all cases. Signal intensities were assessed in a representative area comprising the major part of the placenta by two independent investigators in each pregnancy (ImageJ 1.31a, NIH, Bethesda, MD), and the mean values of both measurements were used for statistical analysis. Signal intensities of the amniotic fluid were used as a reference for the placenta, and the ratio of placental and amniotic fluid signal intensities was correlated with placental grading and GA. Grading of placental changes was performed according to the original sonographic classification of Grannum et al. [18]. In gestations of 28 weeks and later (n = 61), the placenta was additionally subdivided into inner-lobular and homogeenous placentary tissue and signal intensities were assessed for both domains.
2.1. Patients One hundred consecutive singleton pregnancies were investigated. Indications for MRI were sonographically diagnosed fetal pathologies that were not accompanied by placental anomalies (fetal CNS and extra-CNS anomalies). Multiple pregnancies and pregnancies with suspected placental anomalies, UPI, growth-restricted fetuses (<5th percentile), abnormal Doppler studies, or aneuploidies were excluded from the study. The maternal medical histories were uneventful. Pregnancies were assessed at different GAs. The mean GA at the time of MRI investigation was 29.5 weeks (range 19–40), as determined by ultrasonographic biometry in the first trimester and by menstrual dating. Postpartum, all placentas were examined macroscopically and judged to be normal. No neonates showed any evidence of intra-uterine growth restriction (IUGR). MRI was correlated to prenatal US and postpartum appearance of the placenta. 2.2. Ultrasound Location of the placenta, anatomic structure, and grading of the changes in placental calcification were identified on US scan by the transabdominal route using a GE Logiq TM 700 ultrasound machine (GE Medical Systems, Solingen, Germany) or a Toshiba SSA-270A ultrasound machine (Toshiba Medical Systems, Wiener Neudorf, Austria) with a 3.75-MHz curved array transducer for the transabdominal route and a 5.0 MHz convex transducer for the transvaginal route. 2.3. MRI After screening for contraindications [17], MRI was performed within 1 week of the US scan. We used a 1.5 T superconducting system (Gyroscan Intera Release 9, Philips, Vienna, Austria), with a wrap-around body coil and T2-
3. Results Antenatal MRI of the normal placentas showed clear morphological changes during gestation that matched and confirmed the characteristics described with US or contrast medium by others (Figs. 1 and 2). Seventeen of 20 gestations from 19 to 23 weeks (85%) depicted regular homogeneous placental structure, corresponding to grade 0, and three placentas were graded 0–I. No grade 0 was found after week 23. A grade I appearance, with slightly marked lobules, was predominant from weeks 24 to 31. Of 43 placentas, 39 (90.7%) were classified as grade I. Three more women showed some development toward grade II, with an increase in the number and markedness of the lobules. The respective placentas were graded as I–II. In addition, the first full grade II was observed in week 31. No grade I was found after week 31. Placentas at 32–35 weeks uniformly showed a clear grade II. At 36 weeks, we found grade III development, but only one of three placentas reached a full grade III. Overall, pregnancies of 36–41 weeks tended to demonstrate a less uniform grading than observed with earlier stages and comprised placentas of grade II (n = 5), II–III (n = 6), and III (n = 4). Grade II was observed until week 38. Grade III was present in only four cases. Map-like changes in placental structure appeared in some cases, independent of the GA. These changes were interpreted as areas of normal placental infarction. The ratio of placenta/amniotic fluid signal intensity decreased significantly (p < 0.001, Spearman-rho) with GA (Fig. 3). The visual differences between inner-lobular and homogeneous placentary tissue were increasingly marked with ongoing placental maturation. Therefore, we recorded the signal intensities of both domains separately in
258
W. Blaicher et al. / European Journal of Radiology 57 (2006) 256–260
Fig. 1. Changes in placental appearance during gestation on MRI.
gestations of 28 weeks and later. Signal intensity for both tissues decreased with increasing GA. This was significant for homogeneous tissue (p = 0.49), but not for lobular tissue.
4. Discussion
Fig. 2. Development of placental grading with ongoing gestation.
Fig. 3. Decrease in placental/amniotic fluid signal intensity ratio.
Our study underlines that fetal MRI without contrast medium is perfectly appropriate as a non-invasive method for imaging of the normal placenta. The T2-weighted images showed the placenta as moderately hyperintense and allowed differentiation between the placenta and the hypointense myometrium in most cases. With regard to the imaging of morphological changes, we confirmed the results described with the use of contrast medium [16]. The placental structure was clearly depicted, which provided a perfect basis for grading. In our series, the placenta/amniotic fluid signal ratio significantly decreased with higher GA and grading. This may carefully be attributed to morphological changes of the placenta, as suggested by the close-to-significant decrease in placental signal intensity (p = 0.051, Spearman-rho). Amniotic fluid, on the other hand, showed no correlation with either GA, placental grading, or ratio. These results may be seen as a first contribution toward a future index of placental maturity with regard to signal intensity measurements. However, the 100 placentas examined in this study comprised gestations within a range of 21 weeks. Thus, these findings should not be over-estimated. Further investigations with larger samples should be performed to validate these results.
W. Blaicher et al. / European Journal of Radiology 57 (2006) 256–260
The observed development of signal intensity may be explained by the well-known morphological changes during placental aging that lead to a loss of placental tissue density. As the placenta is increasingly “consumed” during gestation, areas of calcification and infarction appear, which may lead to reduced vascular supply. These changes are common and seem to have no adverse effect on the fetus [19]. Placental infarcts are found in approximately 25% of uncomplicated term pregnancies and appear to be of no further clinical significance. However, increasing infarction is associated with placental dysfunction and IUGR [20]. The placenta is a highly vascular organ, and placental as well as supplying blood vessels can be damaged by any process that adversely affects vessels. Rather than a single utero-placental or villous lesion, it is the accumulation of placental injury that, when present for a sufficient time interval, results in fetal growth restriction [21]. Certain maternal diseases, such as severe hypertension [22] and connective-tissue disorders (e.g., lupus, antiphospholipid antibody syndrome, scleroderma, and rheumatoid arthritis) may lead to extensive placental infarction and UPI, which is considered a major cause of IUGR and an important risk factor in the perinatal period. Progressive impairment of the utero-placental circulation increases the likelihood of preeclampsia before 32 weeks [23], and, in a study of 74 cases, it was concluded that features of maternal and fetal compromise in preterm preeclampsia are related to utero-placental vascular lesions [24]. Using quantitative three-dimensional power Doppler US, it has been shown that the fractional moving blood volume of the placenta is positively correlated with the increment of GA and fetal growth indices [25]. A particular advantage of MRI is the high soft tissue contrast. In most of our pregnancies, the visualization of the delineation between the placenta and the uterine wall was possible with T2-weighted images. However, in this regard, the administration of contrast media may be slightly advantageous. Contrast medium is rarely used in antenatal MRI, as allergic reactions may occur and because contrast media passes the placenta [7]. A number of studies have evaluated the administration of gadolinium contrast material during pregnancy and reported no obvious harmful effects [16,26]. However, administration of gadolinium contrast material to a pregnant patient, particularly in the first trimester when teratogenesis would be of greatest concern, should be considered an exceptional examination, restricted to exceptional circumstances. The only obstetric indication for gadolinium contrast material that has been suggested is the evaluation of placenta accreta [27]. MRI is well suited for the visualization of the normal placenta. It can provide clear images from multiple angles and does not expose patients to ionizing radiation. The high resolution enables fast and easy diagnosis of pathological phenomena like UPI, placental insertion defects, and tumors. MRI is superior to US in terms of limiting conditions that may impair sonography, like oligohydramnios, adipositas, or
259
adverse fetal position. In case of unclear diagnosis on US, MRI is a perfect complement that increases the confidence and diagnostic accuracy of prenatal diagnosis. In our institution, antenatal MRI has been well established for years as a second-line imaging technique and has been found to facilitate and improve perinatal management and family counseling by providing vital information about fetal malformations. In the future, we also see a role for MRI with regard to the judgement of fetus supply or in determining the optimal term for delivery. In order to make immediate and correct MRI diagnoses in fetuses with abnormal placental structure, one must be familiar with the appearance of the normal placenta. We describe the appearance of the normal placenta in the course of gestation, obtained by contrast medium-free MRI. Our data may be used as a standard of reference in the assessment of the normal placenta on MRI. Our data may have further clinical impact in the determination of UPI, abnormal placenta and exact localization of the placenta in multiple pregnancies.
Acknowledgment We would like to thank Dr. Franz Reithmayr for the revision of our paper.
References [1] Harris RD, Barth RA. Sonography of the gravid uterus and placenta: current concepts. Am J Roentgenol 1993;160:455–65. [2] Tan TY, Yeo GS. Advances in imaging in prenatal diagnosis and fetal therapy. Ann Acad Med Singapore 2003;32:289–93. [3] Kawabata I, Takahashi Y, Iwagaki S, Tamaya T. MRI during pregnancy. J Perinat Med 2003;31:449–58. [4] Levine D, Barnes PD, Edelman RR. Obstetric MR imaging. Radiology 1999;211:609–17. [5] Quinn TM, Hubbard AM, Adzick NS. Prenatal magnetic resonance imaging enhances fetal diagnosis. J Pediadr Surg 1998;33:553–8. [6] Ohgiya Y, Gokan T, Hamamizu K, Moritani T, Kushihashi T, Munechika H. Fast MRI in obstetric diagnoses. J Comput Assist Tomogr 2001;25:190–200. [7] Huisman TA, Martin E, Kubik-Huch R, Marincek B. Fetal magnetic resonance imaging of the brain: technical considerations and normal brain development. Eur Radiol 2002;12:1941–51. [8] Kubik-Huch RA, Huisman TA, Wisser J, et al. Ultrafast MR imaging of the fetus. AJR 2000;174:1599–606. [9] Raybaud C, Levrier O, Brunel H, Girard N, Farnarier P. MR imaging of fetal brain malformations. Childs Nerv Syst 2003;19:455–70. [10] Girard N, Gire C, Sigaudy S, et al. MR imaging of acquired fetal brain disorders. Childs Nerv Syst 2003;19:490–500. [11] Murphy WD, Feiglin DH, Cisar CC, al-Malt AM, Bellon EM. Magnetic resonance imaging of a third trimester abdominal pregnancy. Magn Reson Imaging 1990;8:657–9. [12] Ertl-Wagner B, Lienemann A, Strauss A, Reiser MF. Fetal magnetic resonance imaging: indications, technique, anatomical considerations and a review of fetal abnormalities. Eur Radiol 2002;12:1931– 40. [13] Verswijvel G, Grieten M, Gyselaers W, et al. MRI in the assessment of pregnancy related intrauterine bleeding: a valuable adjunct to ultrasound? JBR-BTR 2002;85:189–92.
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[14] DeFriend DE, Dubbins PA, Hughes PM. Sacculation of the uterus and placenta accreta: MRI appearances. Brit J Radiol 2000;73:1323–5. [15] Maldjian C, Adam R, Pelosi M, Pelosi III M, Rudelli RD, Maldjian J. MRI appearance of placenta percreta and placenta accreta. Magn Reson Imaging 1999;17:965–71. [16] Marcos HB, Semelka RC, Worawattanakul S. Normal placenta: gadolinium-enhanced dynamic MR imaging. Radiology 1997;205:493–6. [17] Goh RH, Somers S, Jurriaans E, Yu J. Magnetic resonance imaging. Application to family practice. Can Fam Phys 1999;45:2118–28. [18] Grannum PA, Berkowitz RL, Hobbins JC. The ultrasonic changes in the maturing placenta and their relation to fetal pulmonic maturity. Am J Obstet Gynecol 1979;133:915–22. [19] Kara SA, Toppare MF, Avsar F, Caydere M. Placental aging, fetal prognosis and fetomaternal Doppler indices. Eur J Obstet Gynecol Reprod Biol 1999;82:47–52. [20] Astner A, Schwinger E, Caliebe A, Jonat W, Gembruch U. Sonographically detected fetal and placental abnormalities associated with trisomy 16 confined to the placenta. A case report and review of literature. Prenat Diagn 1998;18:1308–15.
[21] Salafia CM, Ghidini A, Lopez-Zeno JA, Pezzullo JC. Uteroplacental pathology and maternal arterial mean blood pressure in spontaneous prematurity. J Soc Gynecol Invest 1998;5:68–71. [22] Salafia CM, Pezzullo JC, Ghidini A, Lopez-Zeno JA, Whittington SS. Clinical correlations of patterns of placental pathology in preterm pre-eclampsia. Placenta 1998;19:67–72. [23] Ghidini A, Salafia CM, Pezzullo JC. Placental vascular lesions and likelihood of diagnosis of preeclampsia. Obstet Gynecol 1997;90:542–5. [24] Salafia CM. Placental pathology of fetal growth restriction. Clin Obstet Gynecol 1997;40:740–9. [25] Yu CH, Chang CH, Ko HC, Chen WC, Chang FM. Assessment of placental fractional moving blood volume using quantitative three-dimensional power doppler ultrasound. Ultrasound Med Biol 2003;29:19–23. [26] Tanaka YO, Sohda S, Shigemitsu S, Niitsu M, Itai Y. High temporal resolution dynamic contrast MRI in a high-risk group for placenta accreta. Magn Reson Imaging 2001;19:635–42. [27] Palacios Jaraquemada JM, Bruno C. Gadolinium-enhanced MR imaging in the differential diagnosis of placenta accreta and placenta percreta. Radiology 2000;216:610–1.
Magnetic resonance imaging of the normal placenta Wibke Blaicher a,∗ , Peter C. Brugger b , Christoph Mittermayer c , Jens Schwindt c , Josef Deutinger a , Gerhard Bernaschek a , Daniela Prayer d a
c
Department of Gynecology and Obstetrics, University Hospital Vienna, Austria b Center of Anatomy and Cell Biology, University Hospital of Vienna, Austria Department of Pediatrics, Division of Neonatology and Intensive Care, University Hospital of Vienna, Austria d Department of Radiology, Division of Neuroradiology, University Hospital of Vienna, Austria Received 11 November 2005; received in revised form 14 November 2005; accepted 16 November 2005
Abstract The goal of this study was to provide a representative description of the normal placenta with contrast medium-free magnetic resonance imaging (MRI) in order to determine a standard of reference. One hundred consecutive singleton pregnancies were investigated by MRI without application of a contrast medium. The mean gestational age (GA) at the time of investigation was 29.5 weeks (range 19–40). Patients with suspected utero-placental insufficiency (UPI) or placental anomalies were excluded. Signal intensities were assessed and correlated with the respective GA. Antenatal MRI without contrast medium was able to depict placental status and morphological changes during gestation. A regular homogeneous structure was found in weeks 19–23. Subsequently, sporadic, slightly marked lobules appeared, which increased in number and markedness with ongoing gestation. Stratification of the lobules was observed after 36 weeks. The ratio of placental and amniotic fluid signal intensities decreased significantly with higher GA and with placental grading. MRI is well suited as an imaging method for the placenta. Our data may be used as a reference in the assessment of the placenta on MRI, and may have further clinical impact with respect to the determination of UPI. © 2005 Elsevier Ireland Ltd. All rights reserved. Keywords: Antenatal diagnosis; Magnetic resonance imaging; MRI; Placenta
1. Introduction Examination of the placenta and gravid uterus is an integral part of any obstetric sonographic study. Fetal well-being and growth depend on an intact utero-placental vascular supply. Prenatal management of fetuses with suspected placental insufficiency depends mainly on Doppler studies, combined with growth curves and cardiotocography. Sonography can show most macroscopic abnormalities that may adversely affect the placenta or the gravid uterus, and that may compromise the fetus or affect the mode of delivery [1]. However, sonographic visualization of the placenta can be difficult due to impaired sonographic conditions and due to the limited ∗ Corresponding author at: Department of Gynecology and Obstetrics, University Hospital Vienna, W¨ahringer G¨urtel 18-20, 1090 Vienna, Austria. Tel.: +43 1 40 400 2994; fax: +43 1 40 400 2995. E-mail address: [email protected] (W. Blaicher).
0720-048X/$ – see front matter © 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2005.11.025
soft tissue contrast. Furthermore, in cases of unclear diagnosis with ultrasound (US), additional investigation may be necessary to provide the best possible perinatal management for the mother and the fetus. MRI is a valuable adjunct in fetal evaluation [2–6]. Ultrafast MRI sequences effectively suppress fetal motion artefacts and avoid sedation. The high spatial resolution of MRI, the multiplanar capabilities, the large field of view, and the high soft tissue contrast that enables simultaneous visualization of fetal and maternal structures, have proven to be advantageous in antenatal examinations, particularly in the evaluation of the central nervous system [7–10]. MRI can demonstrate the uterine wall, placenta, amniotic fluid, and fetus with excellent contrast [11,12]. Reports of MRI of the utero-placental unit are rather rare and mostly concern pregnancies with fetal or placental pathologies [13–15], where MRI was used to confirm or elaborate findings from other diagnostic methods. Surpris-
W. Blaicher et al. / European Journal of Radiology 57 (2006) 256–260
ingly little attention has been paid to the MRI appearance of the normal placenta, though the knowledge gained might provide the basis for MRI-based diagnosis in a much wider range of utero-placental anomalies and enable a better use of this technique. The normal placenta was described using gadoliniumenhanced dynamic MRI in 1997 [16]. However, MRI of the normal placenta without contrast media has not yet been published. The purpose of this study was to provide a standard of reference for the appearance of the normal placenta on non-invasive MRI.
2. Patients and methods We reviewed the antenatal MR images of 100 pregnancies from January 2000 to August 2003. MRI was performed at the Department of Radiology, University of Vienna.
257
weighted sequences (15–19 s acquisition-time; 30 min total time per investigation) in three section planes (axial, sagittal, and coronal), and a 3–5 mm slice-thickness. Adequate anatomical visualisation of the uterus and the placentary tissue were obtained in all cases. Signal intensities were assessed in a representative area comprising the major part of the placenta by two independent investigators in each pregnancy (ImageJ 1.31a, NIH, Bethesda, MD), and the mean values of both measurements were used for statistical analysis. Signal intensities of the amniotic fluid were used as a reference for the placenta, and the ratio of placental and amniotic fluid signal intensities was correlated with placental grading and GA. Grading of placental changes was performed according to the original sonographic classification of Grannum et al. [18]. In gestations of 28 weeks and later (n = 61), the placenta was additionally subdivided into inner-lobular and homogeenous placentary tissue and signal intensities were assessed for both domains.
2.1. Patients One hundred consecutive singleton pregnancies were investigated. Indications for MRI were sonographically diagnosed fetal pathologies that were not accompanied by placental anomalies (fetal CNS and extra-CNS anomalies). Multiple pregnancies and pregnancies with suspected placental anomalies, UPI, growth-restricted fetuses (<5th percentile), abnormal Doppler studies, or aneuploidies were excluded from the study. The maternal medical histories were uneventful. Pregnancies were assessed at different GAs. The mean GA at the time of MRI investigation was 29.5 weeks (range 19–40), as determined by ultrasonographic biometry in the first trimester and by menstrual dating. Postpartum, all placentas were examined macroscopically and judged to be normal. No neonates showed any evidence of intra-uterine growth restriction (IUGR). MRI was correlated to prenatal US and postpartum appearance of the placenta. 2.2. Ultrasound Location of the placenta, anatomic structure, and grading of the changes in placental calcification were identified on US scan by the transabdominal route using a GE Logiq TM 700 ultrasound machine (GE Medical Systems, Solingen, Germany) or a Toshiba SSA-270A ultrasound machine (Toshiba Medical Systems, Wiener Neudorf, Austria) with a 3.75-MHz curved array transducer for the transabdominal route and a 5.0 MHz convex transducer for the transvaginal route. 2.3. MRI After screening for contraindications [17], MRI was performed within 1 week of the US scan. We used a 1.5 T superconducting system (Gyroscan Intera Release 9, Philips, Vienna, Austria), with a wrap-around body coil and T2-
3. Results Antenatal MRI of the normal placentas showed clear morphological changes during gestation that matched and confirmed the characteristics described with US or contrast medium by others (Figs. 1 and 2). Seventeen of 20 gestations from 19 to 23 weeks (85%) depicted regular homogeneous placental structure, corresponding to grade 0, and three placentas were graded 0–I. No grade 0 was found after week 23. A grade I appearance, with slightly marked lobules, was predominant from weeks 24 to 31. Of 43 placentas, 39 (90.7%) were classified as grade I. Three more women showed some development toward grade II, with an increase in the number and markedness of the lobules. The respective placentas were graded as I–II. In addition, the first full grade II was observed in week 31. No grade I was found after week 31. Placentas at 32–35 weeks uniformly showed a clear grade II. At 36 weeks, we found grade III development, but only one of three placentas reached a full grade III. Overall, pregnancies of 36–41 weeks tended to demonstrate a less uniform grading than observed with earlier stages and comprised placentas of grade II (n = 5), II–III (n = 6), and III (n = 4). Grade II was observed until week 38. Grade III was present in only four cases. Map-like changes in placental structure appeared in some cases, independent of the GA. These changes were interpreted as areas of normal placental infarction. The ratio of placenta/amniotic fluid signal intensity decreased significantly (p < 0.001, Spearman-rho) with GA (Fig. 3). The visual differences between inner-lobular and homogeneous placentary tissue were increasingly marked with ongoing placental maturation. Therefore, we recorded the signal intensities of both domains separately in
258
W. Blaicher et al. / European Journal of Radiology 57 (2006) 256–260
Fig. 1. Changes in placental appearance during gestation on MRI.
gestations of 28 weeks and later. Signal intensity for both tissues decreased with increasing GA. This was significant for homogeneous tissue (p = 0.49), but not for lobular tissue.
4. Discussion
Fig. 2. Development of placental grading with ongoing gestation.
Fig. 3. Decrease in placental/amniotic fluid signal intensity ratio.
Our study underlines that fetal MRI without contrast medium is perfectly appropriate as a non-invasive method for imaging of the normal placenta. The T2-weighted images showed the placenta as moderately hyperintense and allowed differentiation between the placenta and the hypointense myometrium in most cases. With regard to the imaging of morphological changes, we confirmed the results described with the use of contrast medium [16]. The placental structure was clearly depicted, which provided a perfect basis for grading. In our series, the placenta/amniotic fluid signal ratio significantly decreased with higher GA and grading. This may carefully be attributed to morphological changes of the placenta, as suggested by the close-to-significant decrease in placental signal intensity (p = 0.051, Spearman-rho). Amniotic fluid, on the other hand, showed no correlation with either GA, placental grading, or ratio. These results may be seen as a first contribution toward a future index of placental maturity with regard to signal intensity measurements. However, the 100 placentas examined in this study comprised gestations within a range of 21 weeks. Thus, these findings should not be over-estimated. Further investigations with larger samples should be performed to validate these results.
W. Blaicher et al. / European Journal of Radiology 57 (2006) 256–260
The observed development of signal intensity may be explained by the well-known morphological changes during placental aging that lead to a loss of placental tissue density. As the placenta is increasingly “consumed” during gestation, areas of calcification and infarction appear, which may lead to reduced vascular supply. These changes are common and seem to have no adverse effect on the fetus [19]. Placental infarcts are found in approximately 25% of uncomplicated term pregnancies and appear to be of no further clinical significance. However, increasing infarction is associated with placental dysfunction and IUGR [20]. The placenta is a highly vascular organ, and placental as well as supplying blood vessels can be damaged by any process that adversely affects vessels. Rather than a single utero-placental or villous lesion, it is the accumulation of placental injury that, when present for a sufficient time interval, results in fetal growth restriction [21]. Certain maternal diseases, such as severe hypertension [22] and connective-tissue disorders (e.g., lupus, antiphospholipid antibody syndrome, scleroderma, and rheumatoid arthritis) may lead to extensive placental infarction and UPI, which is considered a major cause of IUGR and an important risk factor in the perinatal period. Progressive impairment of the utero-placental circulation increases the likelihood of preeclampsia before 32 weeks [23], and, in a study of 74 cases, it was concluded that features of maternal and fetal compromise in preterm preeclampsia are related to utero-placental vascular lesions [24]. Using quantitative three-dimensional power Doppler US, it has been shown that the fractional moving blood volume of the placenta is positively correlated with the increment of GA and fetal growth indices [25]. A particular advantage of MRI is the high soft tissue contrast. In most of our pregnancies, the visualization of the delineation between the placenta and the uterine wall was possible with T2-weighted images. However, in this regard, the administration of contrast media may be slightly advantageous. Contrast medium is rarely used in antenatal MRI, as allergic reactions may occur and because contrast media passes the placenta [7]. A number of studies have evaluated the administration of gadolinium contrast material during pregnancy and reported no obvious harmful effects [16,26]. However, administration of gadolinium contrast material to a pregnant patient, particularly in the first trimester when teratogenesis would be of greatest concern, should be considered an exceptional examination, restricted to exceptional circumstances. The only obstetric indication for gadolinium contrast material that has been suggested is the evaluation of placenta accreta [27]. MRI is well suited for the visualization of the normal placenta. It can provide clear images from multiple angles and does not expose patients to ionizing radiation. The high resolution enables fast and easy diagnosis of pathological phenomena like UPI, placental insertion defects, and tumors. MRI is superior to US in terms of limiting conditions that may impair sonography, like oligohydramnios, adipositas, or
259
adverse fetal position. In case of unclear diagnosis on US, MRI is a perfect complement that increases the confidence and diagnostic accuracy of prenatal diagnosis. In our institution, antenatal MRI has been well established for years as a second-line imaging technique and has been found to facilitate and improve perinatal management and family counseling by providing vital information about fetal malformations. In the future, we also see a role for MRI with regard to the judgement of fetus supply or in determining the optimal term for delivery. In order to make immediate and correct MRI diagnoses in fetuses with abnormal placental structure, one must be familiar with the appearance of the normal placenta. We describe the appearance of the normal placenta in the course of gestation, obtained by contrast medium-free MRI. Our data may be used as a standard of reference in the assessment of the normal placenta on MRI. Our data may have further clinical impact in the determination of UPI, abnormal placenta and exact localization of the placenta in multiple pregnancies.
Acknowledgment We would like to thank Dr. Franz Reithmayr for the revision of our paper.
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