- Email: [email protected]
The role of magnetic resonance imaging in prenatal diagnosis of fetal anomalies
European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178
The role of magnetic resonance imaging in prenatal diagnosis of fetal anomalies Mireille N. Bekker, John M.G. van Vugt* Department of Obstetrics and Gynecology, University Hospital, Vrije Universiteit, P.O. Box 7057, 1007 MB Amsterdam, The Netherlands Accepted 16 July 2000
Abstract Magnetic resonance imaging (MR) has become a useful adjuvant in evaluating fetal structural anomalies when ultrasound (US) is equivocal. It has a signi®cant promise in con®rming a US suspected abnormality and providing new information that was previously not available. The ®rst studies on prenatal MR were hindered by fetal motion and long acquisition times. This degraded imaging and, therefore, maternal or fetal sedation was needed. Since fast and ultrafast MR with scan times of <1 s have become available, the amount of motion artifacts is decreased and sedation is no longer needed. MR has proved to be especially bene®cial in detecting CNS anomalies. Agenesis of the corpus callosum, migration abnormalities and abnormalities of the posterior fossa are better seen on MR. Masses in the fetal neck and thorax can be identi®ed on MR, as some abdominal anomalies. However, the fetal skeletal is dif®cult to visualize with MR. In the future, it is most likely that real time MR will become clinically available which would improve MR imaging even more. # 2001 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Fetus; Magnetic resonance imaging; Ultrasound; Prenatal diagnosis
1. Introduction Ultrasonography (US) is the modality of choice for prenatal screening of fetal anomalies. It provides cost-effective real time imaging, has a high resolution capacity and is safe to the fetus and to the mother. However, there remain certain circumstances in which ultrasound is limited, particularly when ultrasound is indicative but not conclusive or technically dif®cult. This for example occurs in conditions as maternal obesity, oligohydramnios and unfavorable position of the fetus [1±3]. Magnetic resonance imaging (MR) may be a useful adjuvant when ultrasound is indeterminate. This article reviews the current state of MR imaging in the prenatal diagnosis of fetal structural anomalies. The ®rst reports of prenatal MR imaging appeared in the mid-80's. Magnetic resonance imaging was primarily used for evaluation of the uterus, the placenta and the umbilical cord. As more imaging was performed reports appeared documenting abnormalities of the fetus. The major limitations of these studies were consequently long acquisitions times of the standard spin-echo images (1±10 min) and fetal * Corresponding author. Tel.: 31-20-444-3234; fax: 31-20-444-2954. E-mail address: [email protected] (J.M.G. van Vugt).
motion. This degraded the images and, therefore, pharmacological intervention in the form of administration of diazepam to the mother or administration of pancuronium bromide to the fetus, was required to reduce the effects of fetal motion. However, pharmacological intervention introduces a risk to the baby as well to the mother [4±13]. In the last few years, fast and ultrafast MR have become available with scan times of <1 s. These fast and ultrafast scanning techniques decrease or eliminate the amount of motion artifacts. Therefore, maternal or fetal sedation is no longer needed. A variety of sequences have been used, ®rst echoplanar, later half-Fourier single-shot turbo spin-echo (HASTE), fast spin-echo and gradient echo sequences [2,14,15] Especially HASTE has proven to be an excellent method for imaging the human fetus [1,3,16]. Now, MR has a signi®cant promise in the prenatal evaluation of the human fetus to con®rm an US-suspected abnormality and to provide new information that was not previously available. The MR is also a useful adjuvant in de®ning maternal abnormalities and placenta praevia. The MR has several advantages over ultrasound. First MR is not affected by conditions as maternal obesity, oligohydramnios and unfavorable position. The MR has an excellent softtissue resolution and allows scanning in multiple planes, which makes a more detailed evaluation possible [1±3,17±19].
0301-2115/01/$ ± see front matter # 2001 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 3 0 1 - 2 1 1 5 ( 0 0 ) 0 0 4 5 9 - 0
174
M.N. Bekker, J.M.G. van Vugt / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178
2. Safety The MR imaging is a non-invasive procedure and does not involve ionizing radiation. At present, there is no evidence that short-term exposure to electromagnetic ®elds harms the fetus when a ®eld strength of 1.5 T or less is used [20±23]. Baker et al. [24] found no deleterious effects to the fetus in a 3-year follow-up study. Meyers et al. [25] found no adverse effects on fetal growth and birth weight. Because safety is of utmost concern in prenatal examinations, the Safety Committee of the Society for MR imaging made the following guidelines: MR imaging may be used in pregnant women if other non-ionizing forms of diagnostic images are inade-
quate or if examination provides information that would otherwise require exposure to ionizing radiation (e.g. CT, Xray). Scanning at the ®rst trimester should be avoided to minimize teratological effects [26]. 3. Fetal anomalies Table 1 represents 13 studies on the value of MR imaging in evaluating structural anomalies of the fetus using a fast or ultrafast MR sequence as come forward after consultation of Medline. Included are studies that examined a minimum of 10 fetuses.
Table 1 Results of 13 studies of the value of MRI in evaluating fetal anomalies using a fast or ultrafast MR sequencea Study
Fetuses (n)
Indication for MR
Outcome Adding (%)
[58]
36
Maternal (n 11) Fetal (n 25): VM (n 6) Thorax (n 3) Kidney (n 7) Other (n 9)
[36]
29
CNS (n 29)
[37]
18
64b
Confirmative (%)
False ( ) (%)
False () (%)
Change of management (%)
64b
0
0
±
±
±
5.8
±
37
CNS (n 18)
39
55.6
0
5.6
39
[1]
18
Fetal anomalies (n 16)
±
±
±
±
±
[38]
14
ACC (n 14)
100
0
0
0
±
[51]
31
Maternal (n 4) Fetal (n 27): CNS (n 4) CDH (n 14) Lung masses (n 4) Giant neck masses (n 3) Twin anomalies (n 2)
±
±
±
±
±
100
0
0
0
33
50
0
0
44.4
50
5.5
0
±
±
±
±
±
[29]
25
[14]
18
[2]
13
[28]
66
CNS (n 66)
39.4
18.1
1.5
0
13.6
[33]
27
CNS (n 19) Neck (n 8)
47 75
47 12.5
0
0
±
[39]
93
CNS (n 63) Thorax (n 11) Abdomen (n 13) Skeletal (n 5)
32 37 23 40
62 54 69 20
0 0 0 0
0 0 0 0
± ±
[57]
24
Urinary Tract (n 24)
33.3
54.2
12.5
0
±
a
CNS (n 14) CDH (n 6) Miscellaneous (n 5) Thorax (n 18) CNS (n 3) CDH (n 1) Abdomen (n 9)
17
ACC Ð agencies of corpus callosum; CNS Ð central nervous system; CDH Ð congenital diaphragmatic hernia. In this study no difference was made between adding and confirming outcome. Cases in which MR was failed or was not conclusive because of motion artifacts or other reasons are not mentioned. b
M.N. Bekker, J.M.G. van Vugt / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178
The MR imaging was marked as adding when MR imaging gave additional information that was conclusive for the diagnosis. Con®rming are cases in which MR imaging was valuable in con®rming the suspected anomalies. The number of cases in which MR imaging led to a change of management is shown in the last column. 4. Central nervous system One area where MR imaging has proved to be especially bene®cial is in the evaluation of the fetal CNS [27±32]. The US evaluation of the fetal CNS is limited because of the nonspeci®c appearance of some abnormalities and ossi®cation of the fetal skull. Also some subtle parenchymal abnormalities can not be seen at US [10,33]. Ventriculomegaly is often seen on ultrasound and is associated with other anomalies in 70±85%. These anomalies are of great importance for the fetal prognosis, but are often missed on ultrasound. The MR is helpful in detecting these anomalies [14,27,28,30,34±36]. Agenesis of the corpus callosum is such an anomaly that can be missed at ultrasound. The US diagnosis of the agenesis of the corpus callosum is typically made sonographically when the ventricles have an abnormal con®guration rather than direct visualization of the region of the corpus callosum. With MR a direct visualization of the corpus callosum is possible [37]. Many studies describe the importance of MR in diagnosing complete or partial agenesis of the corpus callosum. The MR is also useful in the identi®cation of additional abnormalities like heterotopia and microgyria [10,28,38,39]. In fetuses with arachnoid and other cerebral cysts MR is contributive in de®ning the extent of the cyst and its relationship with the surrounding structures [27]. Although ultrasound can easily diagnose alobar and semilobar types of holoprosencephaly, it can be dif®cult to differ between hydrocephalus and a mild form of holoprosencephaly. The MR on the other hand can differentiate between a lobar holoprosencephaly and a hydrocephalus by showing fused thalami and rostrum [10,14]. In the third trimester sonographical evaluation of the posterior fossa is compromised due to ossi®cation of the fetal skull. Also is transabdominal scanning often impossible because the fetal head is often deeply engaged in a transverse position in the maternal pelvis in the late pregnancy. The MR is not impaired by ossi®cation of the fetal skull and clearly images the skull base, pons, third and fourth ventricles, tentorium and foramen magnum. Therefore, MR is very effective in distinguishing between a normal enlarged cisterna magna, a Dandy Walker variation, an Arnold Chiari malformation, cerebellar hypoplasia and an arachnoid cyst. Supratentorial anomalies can also seen with MR [27,28,33]. Abnormalities of neuronal migration are usually not seen on ultrasound. MS is better suited than ultrasound for the prenatal diagnosis of such anomalies, being able to detect
175
normal brain migration. Several in vitro studies have evaluated changes in sulcal and gyral maturation in relation to gestational age on MR. Anomalies seen on MR include lissenencephaly and schizencephaly, but also subtle parenchymal lesions like heterotopia and polymicrogyria have been imaged [10,40±42]. Fetal intracranial haemorrhage can be detected with MR, especially in case of intraventricular haemorraghe. The signal intensity of the blood varies with the age of the bleeding. The MR is complementary to US because it documents the extension of the lesions and the condition of the surrounding tissue. Porencephalic cavities for example can be detected with MR [19,43±45]. Neural tube defects can be well documented with ultrasound. There remain, however, cases when the de®nitive diagnosis of a neural tube defect can not be made. Under these circumstances MR is helpful. The MR is also helpful in differentiating between a sacral spine defect and a teratoma. Sacrococcygeal teratomas are one of the most common fetal tumors, which can be dif®cult to differentiate from a spine defect. Because of its high-resolution capacity it is likely that in the future MR will play a role in fetal surgery for neural tube defects [27,28,46±48]. 5. Neck Several studies report the effectiveness of MR in imaging fetal neck masses. The most common fetal neck masses are cystic hygroma and cervical teratomas. Both of these tumors can cause severe airway obstruction at birth. The MR, in contrast with ultrasound, can show the relationship of the tumor to the airway and gives an impression of the degree of displacement and compression. Such information is important for, whether immediate postnatal surgery is needed. The MR also is helpful in differentiating between a cystic hygroma and a cervical teratoma [14,33,49,50]. 6. Thorax The fetal lung and tracheobronchial tree can be well imaged with MR. They appear as hyper-intense structures that are easily distinguished from abnormal tissue. The contours of the heart and the great vessels can be imaged but an intracardiac view is not possible because of motion artifacts from the fast beating fetal heart. Therefore, MR is not helpful in evaluating congenital fetal heart disease [19]. Recent studies describe the usefulness of MR in imaging fetal chest masses [14,48,51,52]. The most common chest masses are congenital diaphragmatic hernia (CDH), congenital cystic adenomatoid malformation (CCAM), fetal hydrothorax and bronchopulmonair sequestration. CDH is the most common one, mostly occurring at the left side of the thorax. Sonographic diagnoses of CDH, however, are still missed in a signi®cant number of cases. One study
176
M.N. Bekker, J.M.G. van Vugt / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178
reports the missing of CDH in 50% of the fetuses that got an ultrasound examination [53]. Also the presence of liver herniation into the chest has been correlated with a poor postnatal outcome. On ultrasound it is dif®cult to differentiate a herniated liver from lung tissue and bowel, because it relies on indirect signs, such as an abnormal course of the umbilical vein left to the midline or above the diaphragmatic ridge. The MR, on the other hand is not only effective in diagnosing CDH but also in identifying the position of the fetal liver and other structures in the thorax. CCAM has a variable appearance depending on whether there are macrocysts or microcysts. These lesions may enlarge rapidly or decrease in size during pregnancy. Large lesions may be associated with fetal hydrops. The MR is helpful in identifying the appearance of the CCAM and is particularly effective at estimating the amount of normal residual lung and differentiating it from the abnormal tissue. It visualizes normal compressed lung tissue and de®nes the lobar anatomy. This is important information because fetuses with large lesions should be delivered in a hospital were prompt recusciation and surgery can be performed. Other less common lesions in the thorax in which MR has been described to be helpful are bronchial occlusions and laryngeal obstruction [14,48±50]. 7. Abdomen Although the ®ne detail of the internal structures of the abdomen and pelvis is not well demonstrated with MR a gross evaluation of the visceral organs is possible. Especially the stomach, liver, urinary collecting system, the bladder and intestines can be evaluated [19]. Ultrasound is suf®cient in imaging structures and abnormalities in the abdomen. The MR can be helpful in providing anatomical localization and tissue differentiation leading to a more precise diagnosis. Abdominal anomalies in which MR has been described to be of additional value include omphalocele, gastroschisis, cloacal malformation, enterogenous cyst, fetal ascites, lymphangioma and hepatic cyst [14,48,50]. Ultrasound clearly images the fetal kidney. Nevertheless many fetal urinary tract malformations are associated with oligohydramnios which impairs sonographic visualization. Here MR may be contributive. When the fetal kidney is obstructed there is a signi®cant change in signal intensity that can be distinguished from the normal kidney [14]. Cases of MR diagnosis of autosomal recessive polycystic kidney disease in fetuses with oligohydramnios has been described [54±56]. Poutamo et al. [57] even found MR to be of additional value in cases without oligohydramnios. On the other hand, some other studies didn't found MR helpful in evaluating the kidney. They especially found renal agenesis dif®cult to diagnose with MR [58±61]. Of consideration is that, up to now, only small amounts of fetuses
have been examined in most of the studies which valued MR in evaluating kidney anomalies. 8. Skeletal The fetal skeletal is dif®cult to visualize with MR. Even with fast and ultrafast MR small amounts of fetal motion limit the ability to view the extremities in their entirety. Furthermore, when the fetus moves the suspected region may move outside the imaging plane [2,17,62]. When motion is not present assessment of even the hands and feet are possible. Anomalies that may be seen with MR include shortened, deformed or absence of extremities, but at this time no additional value to ultrasound has been reported. 9. Critical remarks Some critical remarks on the use of MR in prenatal diagnosis should be made. First claustrophobia of the mother can cause the examination to fail. Also pregnant patients may have dif®culty lying on their back for a long time, especially in the third trimester. Keeping the examination as short as possible and placing the patients in the magnet with the feet ®rst can help to minimize these problems [18]. Although fast and ultrafast MR do no longer need maternal or fetal sedation motion artifacts may still occasionally cause image degradation. This is especially true in imaging the skeletal as described above. 10. Conclusion Since the revolution of fast and ultrafast sequences prenatal MR has become a successful adjuvant to ultrasound in evaluating fetal anomalies. The MR is especially bene®cial in detecting CNS anomalies. Also masses in neck and thorax can be identi®ed or more precisely imaged with MR, as some abdominal anomalies. In the future, it is most likely that real time MR will become clinically available and motion artifacts will, therefore, be minimized. A new approach of 3D reconstruction of high quality fetal MR will be of potential value in diagnostic support of prenatal post mortem morphological examinations and in preoperative simulation of fetal surgery [63].
References [1] Yamashita Y, Namimoto T, Abe Y, et al. MR imaging of the Fetus by a HASTE Sequence. AJR 1997;168:513±19.
M.N. Bekker, J.M.G. van Vugt / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178 [2] Huppert BJ, Brandt KR, Ramin KD, et al. Single-shot fast spin-echo MR imaging of the fetus: a pictorial essay. Radiographics 1999; S215±27. [3] Levine D, Hatabu H, Gaa J, et al. Fetal anatomy revealed with fast MR sequences. AJR 1996;167:905±08. [4] Smith FW, Adam AM, Philips WDP. NMR imaging in pregnancy. Lancet 1983;1:61±2. [5] Weinreb JC, Lowe, Coen JN, et al. Human fetal anatomy: MR imaging. Radiology 1985;157:715±20. [6] Johnson II, Symonds E, Kean A, et al. Imaging of the pregnant human uterus with nuclear magnetic resonance. Am J Obstet Gynaecol 1984;148:1136±39. [7] McCarthy SM, Filly RA, Stark DD, et al. Magnetic resonance imaging of the fetal anomalies in utero: early experience. AJR 1985;677±82. [8] McCarthy SM, Filly RA, Stark DD, et al. Obstretical magnetic resonance imaging: fetal anatomy. Radiology 1985;154: 427±32. [9] Williamson RA, Weiner CP, Yuh WTC, et al. Magnetic resonance imaging of anomalous fetuses. Obstet Gynecol 1989;73:952±56. [10] Sonigo PC, Rypens FF, Carteret M, et al. MR imaging of fetal cerebral anomalies. Pediatr Radiol 1998;28:212±22. [11] Garden AS, Weindling RD, Griffiths RD, et al. Assessment of fetal growth using fast-scan magnetic resonance imaging. J Matern Fetal Invest 1991;1:7±13. [12] Garden AS, Griffiths RD, Weindling RD, et al. Fast-scan magnetic resonance imaging in fetal visualization. Obstet Gynecol 1991;164:1190±96. [13] Toshiyuki H, Ken M, Showa A, et al. Magnetic resonance imaging of the fetus: initial eperience. Gynecol Obstet Invest 1990;29:255±58. [14] Hubbard AM, Harty MP, States LJ. A new tool for prenatal diagnosis: ultrafast fetal MRI. Semin Perinatol 1999;23:437±47. [15] Kubik-Huch RA, Wisser L, Stallmach T, et al. Prenatal diagnosis of fetal malformations by ultrafast magnetic resonance imaging. Prenatal diagn 1998;18:1205±08. [16] Tsuchiya K, Katase S, Seki T, et al. Short communication: MR imaging of fetal brain abnormalities using a HASTE sequence. Br J Radiol 1996;69:668±770. [17] Levine D, Edelman RR. Fast MRI and its application in obstretics. Abdom Imaging 1997;22:589±96. [18] Levine D, Barnes PD, Edelman RR. Obstretic MR imaging. Radiology 1999;211:609±17. [19] Amin RS, Nikolaidis P, Kawashima A, et al. Normal anatomy of the fetus at MR imaging. Radiographics 1999;19:S201±14. [20] Shellock F. Biological effects and safety aspects of magnetic resonance imaging. Magn Reson Quarterly 1989;5:243±61. [21] Kanal E. Pregnancy and the safety of magnetic resonance imaging. Magn Reson Imaging Clin N Am 1994;2:309±17. [22] Mansfield P, Stehling MD, Ordige RJ, et al. Echoplanar imaging of the human fetus at 0.5 T. Br J Radiol 1990;63:833±41. [23] Poutamo J, Partanen K, Vanninen R, et al. MRI does not change fetal cardiotocographic parameters. Prenatal Diag 1998;18:1149±1154. [24] Baker PN, Johnson IR, Harvey PR, et al. A 3-year follow-up of children imaged in utero with echo-planar magnetic resonance. Am J Obstet Gynecol 1994;170:32±3. [25] Meyers C, Duncan KR, Gowland PA, et al. Failure to detect intrauterine growth restriction following in utero exposure to MRI. Br J Radiol 1998;71:549±51. [26] Shellock F, Kanal E. Policies, guidelines and recommendations for MR imaging safety and patient management. J Magn Reson Imaging 1991;1:97±100. [27] Levine D, Barnes PD, Madsen JR, et al. Fetal CNS anomalies revealed on ultrafast MR imaging. AJR 1999;172:813±18. [28] Levine D, Barnes PD, Madsen JR, et al. Central nervous system abnormalities assessed with Prenatal magnetic resonance imaging. Obstet Gynecol 1999;94:1011±119. [29] Coakley FV, Hricak H, Filly RA, et al. Complex fetal disorders: effect of MR imaging on management-preliminary clinical experience. Radiology 1999;213;691±96.
177
[30] Garel C, Brisse H, Sebag G, et al. Magnetic resonance imaging of the fetus. Pediatr Radiol 1998;28:201±11. [31] Resta M, Burdi N, Medicamento N. Magnetic resonance imaging of normal and pathologic fetal brain. Childs Nerv Syst 1998;14:151±4. [32] Yuh WTC, Nguyen HD, Fisher DJ, et al. MR of fetal central nervous system abnormalities. AJNR 1994;14:459±64. [33] Poutamo J, Vanninen R, Partanen K, et al. Magnetic resonance imaging supplements ultrasonographic imaging of the posterior fossa, pharynx and neck in malformed fetuses. Ultrasound Obstet Gynecol 1999;13:327±34. [34] Nicolaides K, Berry S, Snijders R, et al. Fetal lateral ventriculomegaly: associated malformations and chromosomal defects. Fetal Diagn Ther 1990;5:5±14. [35] Dinh DH, Wright RM, Hanigan WC. The use of magnetic resonance imaging for the diagnosis of fetal intracranial anomalies. Childs Nerv Syst 1990;6:212±5. [36] Lair-Milan F, Gelot A, Baron JM, et al. Prenatal MRI of the brain. Retrospective study apropos of 34 tests. J Radiol 1997;78: 499±500. [37] Levine D, Barnes PD, Madsen JR, et al. Fetal central nervous system anomalies: MR imaging augments sonographic diagnosis. Radiology 1997;204:635±42 [38] D'Ercole C, Girard N, Cravello L, et al. Prenatal diagnosis of fetal corpus callosum agencies by ultrasonography and magnetic resonance imaging. Prenat Diagn 1998;18:247±253. [39] Vimercati A, Greco P, Vera L, et al. The diagnostic role of in utero magnetic resonance imaging. J Perinatol Med 1999;27:303±08. [40] Levine D, Barens PD. Cortical maturation in normal and abnormal fetuses as assessed with prenatal MR imaging. Radiology 1999;210:751±8. [41] Lan LM, Yamashita Y, Tang Y, et al. Normal fetal brain development: MR imaging with a half-Fourier rapid acquisition with relaxation enhancement sequence. Radiology 2000;215:205±10. [42] Girard J, Raybaud C, Poncet M. Vivo MR study of brain maturation in normal fetuses. AJNR 1995;16:407±13. [43] Kirkinen P, Partanen K, Orden MR. Fetal intracranial hemorraghe: imaging by ultrasound and magnetic resonance imaging. J Reprod Med 1997;42:467±72. [44] Canapicchi R, Cioni G, Strigini Fal, et al. Prenatal diagnosis of periventricular hemorraghe by fetal brain magnetic resonance imaging. Childs Nerv Syst 1998;14:689±92. [45] Fusch C, Ozdoba C, Kuhn P, et al. Perinatal ultrasonography and magnetic resonance imaging findings in congenital hydrocephalus associated with fetal intraventricular hemorraghe. Am J Obstet Gynecol 1997;177:512±18. [46] Olutoye OO, Adzick NS. Fetal surgery for meningocele. Semin Perinatol 1999;23:462±73. [47] Magram G. Fetal surgery for spin bifida. Lancet 1999;353:406±7. [48] Adzick NS, Sutton LN, Cromblehome TM, et al. Succesful fetal surgery for spina bifida. Lancet 1998;352:1675±77. [49] Hubbard AM, Harty P. Prenatal magnetic resonance imaging of fetal anomalies. Semin Roentgenol 1999;34(1):41±7. [50] Tsuda H, Matsumoto M, Yamamoto K, et al. Usefulness of ultrasonography and magnetic resonance imaging for prenatal diagnosis of fetal teratoma of the neck. J Clin Ultrasound 1996;24:217±19. [51] Quinn TM, Hubbard AM, Adzick NS, et al. Prenatal magnetic resonance imaging enhances fetal diagnosis. J Ped Surg 1998;33:553±8. [52] Hubbard AM, Adzick NS, Cromblehome TM, et al. Congenital chest lesions: diagnosis and characterization with prenatal MR imaging. Radiology 1999;212:43±8. [53] Lewis D, Reickert C, Bowerman R, et al. Prenatal ultrasonography frequently fails to diagnose congential diaphragmatic hernia. J Pediatr Surg 1997;32:352±6. [54] Takeuchi K, Moriyama T, Funakoshi T, et al. Prenatal diagnosis of fetal urogenital abnormalities with oligohydramnios by magnetic
178
[55] [56] [57] [58]
M.N. Bekker, J.M.G. van Vugt / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178 resonance imaging using turbo spin echo technique. J Perinat Med 1998;26:56±61. Nishi T. Magnetic resonance imaging of autosomal recessive polycystic kidney disease in utero. J Obstet Gynaecol 1995;21:471±4. Nishi T. Prenatal diagnosis of urinary tract abnormalities. Acta Obstet Gynecol Scand 1997;76:409±13. Poutamo J, Vanninen R, Kirkinen P. Diagnosing fetal urinary tract abnormalities: benefits of MRI compared to ultrasonography. Acta Obstet Gynecol Scand 2000;79:65±71. Kirkinen P, Partanen K, Vainio P, et al. MRI in obstetrics: a supplementary method for ultrasonography. Ann Med 1996;28:131± 136.
[59] Coletti PM. Computer-assisted imaging of the fetus with magnetic resonance imaging. Elsevier Sci 1996;20:491±496. [60] DeCleijn K, Degryse H, Slangen T, et al. MRI in the prenatal diagnosis of bilateral renal agencies. Fortschr Rontgenst Ger 1989;150:140±145. [61] Garden AS, Weindling AM, Griffiths RD, et al. Fast-scan magnetic resonance imaging of fetal anomalies. Br J Obstet Gynecol 1991;98:1217±1222. [62] Levine D, Barnes PD, Sher S, et al. Fetal fast MR imaging: reproducibility, technical quality and conspicuity of anatomy. Radiology 1998;206:549±54. [63] Brookes JAS, Deng J, Wilkinson ID, et al. Three-dimensional imaging of the postmorem fetus by MRI: early experience. Fetal Diagn Therapy 1999;14:166±71.
The role of magnetic resonance imaging in prenatal diagnosis of fetal anomalies Mireille N. Bekker, John M.G. van Vugt* Department of Obstetrics and Gynecology, University Hospital, Vrije Universiteit, P.O. Box 7057, 1007 MB Amsterdam, The Netherlands Accepted 16 July 2000
Abstract Magnetic resonance imaging (MR) has become a useful adjuvant in evaluating fetal structural anomalies when ultrasound (US) is equivocal. It has a signi®cant promise in con®rming a US suspected abnormality and providing new information that was previously not available. The ®rst studies on prenatal MR were hindered by fetal motion and long acquisition times. This degraded imaging and, therefore, maternal or fetal sedation was needed. Since fast and ultrafast MR with scan times of <1 s have become available, the amount of motion artifacts is decreased and sedation is no longer needed. MR has proved to be especially bene®cial in detecting CNS anomalies. Agenesis of the corpus callosum, migration abnormalities and abnormalities of the posterior fossa are better seen on MR. Masses in the fetal neck and thorax can be identi®ed on MR, as some abdominal anomalies. However, the fetal skeletal is dif®cult to visualize with MR. In the future, it is most likely that real time MR will become clinically available which would improve MR imaging even more. # 2001 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Fetus; Magnetic resonance imaging; Ultrasound; Prenatal diagnosis
1. Introduction Ultrasonography (US) is the modality of choice for prenatal screening of fetal anomalies. It provides cost-effective real time imaging, has a high resolution capacity and is safe to the fetus and to the mother. However, there remain certain circumstances in which ultrasound is limited, particularly when ultrasound is indicative but not conclusive or technically dif®cult. This for example occurs in conditions as maternal obesity, oligohydramnios and unfavorable position of the fetus [1±3]. Magnetic resonance imaging (MR) may be a useful adjuvant when ultrasound is indeterminate. This article reviews the current state of MR imaging in the prenatal diagnosis of fetal structural anomalies. The ®rst reports of prenatal MR imaging appeared in the mid-80's. Magnetic resonance imaging was primarily used for evaluation of the uterus, the placenta and the umbilical cord. As more imaging was performed reports appeared documenting abnormalities of the fetus. The major limitations of these studies were consequently long acquisitions times of the standard spin-echo images (1±10 min) and fetal * Corresponding author. Tel.: 31-20-444-3234; fax: 31-20-444-2954. E-mail address: [email protected] (J.M.G. van Vugt).
motion. This degraded the images and, therefore, pharmacological intervention in the form of administration of diazepam to the mother or administration of pancuronium bromide to the fetus, was required to reduce the effects of fetal motion. However, pharmacological intervention introduces a risk to the baby as well to the mother [4±13]. In the last few years, fast and ultrafast MR have become available with scan times of <1 s. These fast and ultrafast scanning techniques decrease or eliminate the amount of motion artifacts. Therefore, maternal or fetal sedation is no longer needed. A variety of sequences have been used, ®rst echoplanar, later half-Fourier single-shot turbo spin-echo (HASTE), fast spin-echo and gradient echo sequences [2,14,15] Especially HASTE has proven to be an excellent method for imaging the human fetus [1,3,16]. Now, MR has a signi®cant promise in the prenatal evaluation of the human fetus to con®rm an US-suspected abnormality and to provide new information that was not previously available. The MR is also a useful adjuvant in de®ning maternal abnormalities and placenta praevia. The MR has several advantages over ultrasound. First MR is not affected by conditions as maternal obesity, oligohydramnios and unfavorable position. The MR has an excellent softtissue resolution and allows scanning in multiple planes, which makes a more detailed evaluation possible [1±3,17±19].
0301-2115/01/$ ± see front matter # 2001 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 3 0 1 - 2 1 1 5 ( 0 0 ) 0 0 4 5 9 - 0
174
M.N. Bekker, J.M.G. van Vugt / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178
2. Safety The MR imaging is a non-invasive procedure and does not involve ionizing radiation. At present, there is no evidence that short-term exposure to electromagnetic ®elds harms the fetus when a ®eld strength of 1.5 T or less is used [20±23]. Baker et al. [24] found no deleterious effects to the fetus in a 3-year follow-up study. Meyers et al. [25] found no adverse effects on fetal growth and birth weight. Because safety is of utmost concern in prenatal examinations, the Safety Committee of the Society for MR imaging made the following guidelines: MR imaging may be used in pregnant women if other non-ionizing forms of diagnostic images are inade-
quate or if examination provides information that would otherwise require exposure to ionizing radiation (e.g. CT, Xray). Scanning at the ®rst trimester should be avoided to minimize teratological effects [26]. 3. Fetal anomalies Table 1 represents 13 studies on the value of MR imaging in evaluating structural anomalies of the fetus using a fast or ultrafast MR sequence as come forward after consultation of Medline. Included are studies that examined a minimum of 10 fetuses.
Table 1 Results of 13 studies of the value of MRI in evaluating fetal anomalies using a fast or ultrafast MR sequencea Study
Fetuses (n)
Indication for MR
Outcome Adding (%)
[58]
36
Maternal (n 11) Fetal (n 25): VM (n 6) Thorax (n 3) Kidney (n 7) Other (n 9)
[36]
29
CNS (n 29)
[37]
18
64b
Confirmative (%)
False ( ) (%)
False () (%)
Change of management (%)
64b
0
0
±
±
±
5.8
±
37
CNS (n 18)
39
55.6
0
5.6
39
[1]
18
Fetal anomalies (n 16)
±
±
±
±
±
[38]
14
ACC (n 14)
100
0
0
0
±
[51]
31
Maternal (n 4) Fetal (n 27): CNS (n 4) CDH (n 14) Lung masses (n 4) Giant neck masses (n 3) Twin anomalies (n 2)
±
±
±
±
±
100
0
0
0
33
50
0
0
44.4
50
5.5
0
±
±
±
±
±
[29]
25
[14]
18
[2]
13
[28]
66
CNS (n 66)
39.4
18.1
1.5
0
13.6
[33]
27
CNS (n 19) Neck (n 8)
47 75
47 12.5
0
0
±
[39]
93
CNS (n 63) Thorax (n 11) Abdomen (n 13) Skeletal (n 5)
32 37 23 40
62 54 69 20
0 0 0 0
0 0 0 0
± ±
[57]
24
Urinary Tract (n 24)
33.3
54.2
12.5
0
±
a
CNS (n 14) CDH (n 6) Miscellaneous (n 5) Thorax (n 18) CNS (n 3) CDH (n 1) Abdomen (n 9)
17
ACC Ð agencies of corpus callosum; CNS Ð central nervous system; CDH Ð congenital diaphragmatic hernia. In this study no difference was made between adding and confirming outcome. Cases in which MR was failed or was not conclusive because of motion artifacts or other reasons are not mentioned. b
M.N. Bekker, J.M.G. van Vugt / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178
The MR imaging was marked as adding when MR imaging gave additional information that was conclusive for the diagnosis. Con®rming are cases in which MR imaging was valuable in con®rming the suspected anomalies. The number of cases in which MR imaging led to a change of management is shown in the last column. 4. Central nervous system One area where MR imaging has proved to be especially bene®cial is in the evaluation of the fetal CNS [27±32]. The US evaluation of the fetal CNS is limited because of the nonspeci®c appearance of some abnormalities and ossi®cation of the fetal skull. Also some subtle parenchymal abnormalities can not be seen at US [10,33]. Ventriculomegaly is often seen on ultrasound and is associated with other anomalies in 70±85%. These anomalies are of great importance for the fetal prognosis, but are often missed on ultrasound. The MR is helpful in detecting these anomalies [14,27,28,30,34±36]. Agenesis of the corpus callosum is such an anomaly that can be missed at ultrasound. The US diagnosis of the agenesis of the corpus callosum is typically made sonographically when the ventricles have an abnormal con®guration rather than direct visualization of the region of the corpus callosum. With MR a direct visualization of the corpus callosum is possible [37]. Many studies describe the importance of MR in diagnosing complete or partial agenesis of the corpus callosum. The MR is also useful in the identi®cation of additional abnormalities like heterotopia and microgyria [10,28,38,39]. In fetuses with arachnoid and other cerebral cysts MR is contributive in de®ning the extent of the cyst and its relationship with the surrounding structures [27]. Although ultrasound can easily diagnose alobar and semilobar types of holoprosencephaly, it can be dif®cult to differ between hydrocephalus and a mild form of holoprosencephaly. The MR on the other hand can differentiate between a lobar holoprosencephaly and a hydrocephalus by showing fused thalami and rostrum [10,14]. In the third trimester sonographical evaluation of the posterior fossa is compromised due to ossi®cation of the fetal skull. Also is transabdominal scanning often impossible because the fetal head is often deeply engaged in a transverse position in the maternal pelvis in the late pregnancy. The MR is not impaired by ossi®cation of the fetal skull and clearly images the skull base, pons, third and fourth ventricles, tentorium and foramen magnum. Therefore, MR is very effective in distinguishing between a normal enlarged cisterna magna, a Dandy Walker variation, an Arnold Chiari malformation, cerebellar hypoplasia and an arachnoid cyst. Supratentorial anomalies can also seen with MR [27,28,33]. Abnormalities of neuronal migration are usually not seen on ultrasound. MS is better suited than ultrasound for the prenatal diagnosis of such anomalies, being able to detect
175
normal brain migration. Several in vitro studies have evaluated changes in sulcal and gyral maturation in relation to gestational age on MR. Anomalies seen on MR include lissenencephaly and schizencephaly, but also subtle parenchymal lesions like heterotopia and polymicrogyria have been imaged [10,40±42]. Fetal intracranial haemorrhage can be detected with MR, especially in case of intraventricular haemorraghe. The signal intensity of the blood varies with the age of the bleeding. The MR is complementary to US because it documents the extension of the lesions and the condition of the surrounding tissue. Porencephalic cavities for example can be detected with MR [19,43±45]. Neural tube defects can be well documented with ultrasound. There remain, however, cases when the de®nitive diagnosis of a neural tube defect can not be made. Under these circumstances MR is helpful. The MR is also helpful in differentiating between a sacral spine defect and a teratoma. Sacrococcygeal teratomas are one of the most common fetal tumors, which can be dif®cult to differentiate from a spine defect. Because of its high-resolution capacity it is likely that in the future MR will play a role in fetal surgery for neural tube defects [27,28,46±48]. 5. Neck Several studies report the effectiveness of MR in imaging fetal neck masses. The most common fetal neck masses are cystic hygroma and cervical teratomas. Both of these tumors can cause severe airway obstruction at birth. The MR, in contrast with ultrasound, can show the relationship of the tumor to the airway and gives an impression of the degree of displacement and compression. Such information is important for, whether immediate postnatal surgery is needed. The MR also is helpful in differentiating between a cystic hygroma and a cervical teratoma [14,33,49,50]. 6. Thorax The fetal lung and tracheobronchial tree can be well imaged with MR. They appear as hyper-intense structures that are easily distinguished from abnormal tissue. The contours of the heart and the great vessels can be imaged but an intracardiac view is not possible because of motion artifacts from the fast beating fetal heart. Therefore, MR is not helpful in evaluating congenital fetal heart disease [19]. Recent studies describe the usefulness of MR in imaging fetal chest masses [14,48,51,52]. The most common chest masses are congenital diaphragmatic hernia (CDH), congenital cystic adenomatoid malformation (CCAM), fetal hydrothorax and bronchopulmonair sequestration. CDH is the most common one, mostly occurring at the left side of the thorax. Sonographic diagnoses of CDH, however, are still missed in a signi®cant number of cases. One study
176
M.N. Bekker, J.M.G. van Vugt / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178
reports the missing of CDH in 50% of the fetuses that got an ultrasound examination [53]. Also the presence of liver herniation into the chest has been correlated with a poor postnatal outcome. On ultrasound it is dif®cult to differentiate a herniated liver from lung tissue and bowel, because it relies on indirect signs, such as an abnormal course of the umbilical vein left to the midline or above the diaphragmatic ridge. The MR, on the other hand is not only effective in diagnosing CDH but also in identifying the position of the fetal liver and other structures in the thorax. CCAM has a variable appearance depending on whether there are macrocysts or microcysts. These lesions may enlarge rapidly or decrease in size during pregnancy. Large lesions may be associated with fetal hydrops. The MR is helpful in identifying the appearance of the CCAM and is particularly effective at estimating the amount of normal residual lung and differentiating it from the abnormal tissue. It visualizes normal compressed lung tissue and de®nes the lobar anatomy. This is important information because fetuses with large lesions should be delivered in a hospital were prompt recusciation and surgery can be performed. Other less common lesions in the thorax in which MR has been described to be helpful are bronchial occlusions and laryngeal obstruction [14,48±50]. 7. Abdomen Although the ®ne detail of the internal structures of the abdomen and pelvis is not well demonstrated with MR a gross evaluation of the visceral organs is possible. Especially the stomach, liver, urinary collecting system, the bladder and intestines can be evaluated [19]. Ultrasound is suf®cient in imaging structures and abnormalities in the abdomen. The MR can be helpful in providing anatomical localization and tissue differentiation leading to a more precise diagnosis. Abdominal anomalies in which MR has been described to be of additional value include omphalocele, gastroschisis, cloacal malformation, enterogenous cyst, fetal ascites, lymphangioma and hepatic cyst [14,48,50]. Ultrasound clearly images the fetal kidney. Nevertheless many fetal urinary tract malformations are associated with oligohydramnios which impairs sonographic visualization. Here MR may be contributive. When the fetal kidney is obstructed there is a signi®cant change in signal intensity that can be distinguished from the normal kidney [14]. Cases of MR diagnosis of autosomal recessive polycystic kidney disease in fetuses with oligohydramnios has been described [54±56]. Poutamo et al. [57] even found MR to be of additional value in cases without oligohydramnios. On the other hand, some other studies didn't found MR helpful in evaluating the kidney. They especially found renal agenesis dif®cult to diagnose with MR [58±61]. Of consideration is that, up to now, only small amounts of fetuses
have been examined in most of the studies which valued MR in evaluating kidney anomalies. 8. Skeletal The fetal skeletal is dif®cult to visualize with MR. Even with fast and ultrafast MR small amounts of fetal motion limit the ability to view the extremities in their entirety. Furthermore, when the fetus moves the suspected region may move outside the imaging plane [2,17,62]. When motion is not present assessment of even the hands and feet are possible. Anomalies that may be seen with MR include shortened, deformed or absence of extremities, but at this time no additional value to ultrasound has been reported. 9. Critical remarks Some critical remarks on the use of MR in prenatal diagnosis should be made. First claustrophobia of the mother can cause the examination to fail. Also pregnant patients may have dif®culty lying on their back for a long time, especially in the third trimester. Keeping the examination as short as possible and placing the patients in the magnet with the feet ®rst can help to minimize these problems [18]. Although fast and ultrafast MR do no longer need maternal or fetal sedation motion artifacts may still occasionally cause image degradation. This is especially true in imaging the skeletal as described above. 10. Conclusion Since the revolution of fast and ultrafast sequences prenatal MR has become a successful adjuvant to ultrasound in evaluating fetal anomalies. The MR is especially bene®cial in detecting CNS anomalies. Also masses in neck and thorax can be identi®ed or more precisely imaged with MR, as some abdominal anomalies. In the future, it is most likely that real time MR will become clinically available and motion artifacts will, therefore, be minimized. A new approach of 3D reconstruction of high quality fetal MR will be of potential value in diagnostic support of prenatal post mortem morphological examinations and in preoperative simulation of fetal surgery [63].
References [1] Yamashita Y, Namimoto T, Abe Y, et al. MR imaging of the Fetus by a HASTE Sequence. AJR 1997;168:513±19.
M.N. Bekker, J.M.G. van Vugt / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178 [2] Huppert BJ, Brandt KR, Ramin KD, et al. Single-shot fast spin-echo MR imaging of the fetus: a pictorial essay. Radiographics 1999; S215±27. [3] Levine D, Hatabu H, Gaa J, et al. Fetal anatomy revealed with fast MR sequences. AJR 1996;167:905±08. [4] Smith FW, Adam AM, Philips WDP. NMR imaging in pregnancy. Lancet 1983;1:61±2. [5] Weinreb JC, Lowe, Coen JN, et al. Human fetal anatomy: MR imaging. Radiology 1985;157:715±20. [6] Johnson II, Symonds E, Kean A, et al. Imaging of the pregnant human uterus with nuclear magnetic resonance. Am J Obstet Gynaecol 1984;148:1136±39. [7] McCarthy SM, Filly RA, Stark DD, et al. Magnetic resonance imaging of the fetal anomalies in utero: early experience. AJR 1985;677±82. [8] McCarthy SM, Filly RA, Stark DD, et al. Obstretical magnetic resonance imaging: fetal anatomy. Radiology 1985;154: 427±32. [9] Williamson RA, Weiner CP, Yuh WTC, et al. Magnetic resonance imaging of anomalous fetuses. Obstet Gynecol 1989;73:952±56. [10] Sonigo PC, Rypens FF, Carteret M, et al. MR imaging of fetal cerebral anomalies. Pediatr Radiol 1998;28:212±22. [11] Garden AS, Weindling RD, Griffiths RD, et al. Assessment of fetal growth using fast-scan magnetic resonance imaging. J Matern Fetal Invest 1991;1:7±13. [12] Garden AS, Griffiths RD, Weindling RD, et al. Fast-scan magnetic resonance imaging in fetal visualization. Obstet Gynecol 1991;164:1190±96. [13] Toshiyuki H, Ken M, Showa A, et al. Magnetic resonance imaging of the fetus: initial eperience. Gynecol Obstet Invest 1990;29:255±58. [14] Hubbard AM, Harty MP, States LJ. A new tool for prenatal diagnosis: ultrafast fetal MRI. Semin Perinatol 1999;23:437±47. [15] Kubik-Huch RA, Wisser L, Stallmach T, et al. Prenatal diagnosis of fetal malformations by ultrafast magnetic resonance imaging. Prenatal diagn 1998;18:1205±08. [16] Tsuchiya K, Katase S, Seki T, et al. Short communication: MR imaging of fetal brain abnormalities using a HASTE sequence. Br J Radiol 1996;69:668±770. [17] Levine D, Edelman RR. Fast MRI and its application in obstretics. Abdom Imaging 1997;22:589±96. [18] Levine D, Barnes PD, Edelman RR. Obstretic MR imaging. Radiology 1999;211:609±17. [19] Amin RS, Nikolaidis P, Kawashima A, et al. Normal anatomy of the fetus at MR imaging. Radiographics 1999;19:S201±14. [20] Shellock F. Biological effects and safety aspects of magnetic resonance imaging. Magn Reson Quarterly 1989;5:243±61. [21] Kanal E. Pregnancy and the safety of magnetic resonance imaging. Magn Reson Imaging Clin N Am 1994;2:309±17. [22] Mansfield P, Stehling MD, Ordige RJ, et al. Echoplanar imaging of the human fetus at 0.5 T. Br J Radiol 1990;63:833±41. [23] Poutamo J, Partanen K, Vanninen R, et al. MRI does not change fetal cardiotocographic parameters. Prenatal Diag 1998;18:1149±1154. [24] Baker PN, Johnson IR, Harvey PR, et al. A 3-year follow-up of children imaged in utero with echo-planar magnetic resonance. Am J Obstet Gynecol 1994;170:32±3. [25] Meyers C, Duncan KR, Gowland PA, et al. Failure to detect intrauterine growth restriction following in utero exposure to MRI. Br J Radiol 1998;71:549±51. [26] Shellock F, Kanal E. Policies, guidelines and recommendations for MR imaging safety and patient management. J Magn Reson Imaging 1991;1:97±100. [27] Levine D, Barnes PD, Madsen JR, et al. Fetal CNS anomalies revealed on ultrafast MR imaging. AJR 1999;172:813±18. [28] Levine D, Barnes PD, Madsen JR, et al. Central nervous system abnormalities assessed with Prenatal magnetic resonance imaging. Obstet Gynecol 1999;94:1011±119. [29] Coakley FV, Hricak H, Filly RA, et al. Complex fetal disorders: effect of MR imaging on management-preliminary clinical experience. Radiology 1999;213;691±96.
177
[30] Garel C, Brisse H, Sebag G, et al. Magnetic resonance imaging of the fetus. Pediatr Radiol 1998;28:201±11. [31] Resta M, Burdi N, Medicamento N. Magnetic resonance imaging of normal and pathologic fetal brain. Childs Nerv Syst 1998;14:151±4. [32] Yuh WTC, Nguyen HD, Fisher DJ, et al. MR of fetal central nervous system abnormalities. AJNR 1994;14:459±64. [33] Poutamo J, Vanninen R, Partanen K, et al. Magnetic resonance imaging supplements ultrasonographic imaging of the posterior fossa, pharynx and neck in malformed fetuses. Ultrasound Obstet Gynecol 1999;13:327±34. [34] Nicolaides K, Berry S, Snijders R, et al. Fetal lateral ventriculomegaly: associated malformations and chromosomal defects. Fetal Diagn Ther 1990;5:5±14. [35] Dinh DH, Wright RM, Hanigan WC. The use of magnetic resonance imaging for the diagnosis of fetal intracranial anomalies. Childs Nerv Syst 1990;6:212±5. [36] Lair-Milan F, Gelot A, Baron JM, et al. Prenatal MRI of the brain. Retrospective study apropos of 34 tests. J Radiol 1997;78: 499±500. [37] Levine D, Barnes PD, Madsen JR, et al. Fetal central nervous system anomalies: MR imaging augments sonographic diagnosis. Radiology 1997;204:635±42 [38] D'Ercole C, Girard N, Cravello L, et al. Prenatal diagnosis of fetal corpus callosum agencies by ultrasonography and magnetic resonance imaging. Prenat Diagn 1998;18:247±253. [39] Vimercati A, Greco P, Vera L, et al. The diagnostic role of in utero magnetic resonance imaging. J Perinatol Med 1999;27:303±08. [40] Levine D, Barens PD. Cortical maturation in normal and abnormal fetuses as assessed with prenatal MR imaging. Radiology 1999;210:751±8. [41] Lan LM, Yamashita Y, Tang Y, et al. Normal fetal brain development: MR imaging with a half-Fourier rapid acquisition with relaxation enhancement sequence. Radiology 2000;215:205±10. [42] Girard J, Raybaud C, Poncet M. Vivo MR study of brain maturation in normal fetuses. AJNR 1995;16:407±13. [43] Kirkinen P, Partanen K, Orden MR. Fetal intracranial hemorraghe: imaging by ultrasound and magnetic resonance imaging. J Reprod Med 1997;42:467±72. [44] Canapicchi R, Cioni G, Strigini Fal, et al. Prenatal diagnosis of periventricular hemorraghe by fetal brain magnetic resonance imaging. Childs Nerv Syst 1998;14:689±92. [45] Fusch C, Ozdoba C, Kuhn P, et al. Perinatal ultrasonography and magnetic resonance imaging findings in congenital hydrocephalus associated with fetal intraventricular hemorraghe. Am J Obstet Gynecol 1997;177:512±18. [46] Olutoye OO, Adzick NS. Fetal surgery for meningocele. Semin Perinatol 1999;23:462±73. [47] Magram G. Fetal surgery for spin bifida. Lancet 1999;353:406±7. [48] Adzick NS, Sutton LN, Cromblehome TM, et al. Succesful fetal surgery for spina bifida. Lancet 1998;352:1675±77. [49] Hubbard AM, Harty P. Prenatal magnetic resonance imaging of fetal anomalies. Semin Roentgenol 1999;34(1):41±7. [50] Tsuda H, Matsumoto M, Yamamoto K, et al. Usefulness of ultrasonography and magnetic resonance imaging for prenatal diagnosis of fetal teratoma of the neck. J Clin Ultrasound 1996;24:217±19. [51] Quinn TM, Hubbard AM, Adzick NS, et al. Prenatal magnetic resonance imaging enhances fetal diagnosis. J Ped Surg 1998;33:553±8. [52] Hubbard AM, Adzick NS, Cromblehome TM, et al. Congenital chest lesions: diagnosis and characterization with prenatal MR imaging. Radiology 1999;212:43±8. [53] Lewis D, Reickert C, Bowerman R, et al. Prenatal ultrasonography frequently fails to diagnose congential diaphragmatic hernia. J Pediatr Surg 1997;32:352±6. [54] Takeuchi K, Moriyama T, Funakoshi T, et al. Prenatal diagnosis of fetal urogenital abnormalities with oligohydramnios by magnetic
178
[55] [56] [57] [58]
M.N. Bekker, J.M.G. van Vugt / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 173±178 resonance imaging using turbo spin echo technique. J Perinat Med 1998;26:56±61. Nishi T. Magnetic resonance imaging of autosomal recessive polycystic kidney disease in utero. J Obstet Gynaecol 1995;21:471±4. Nishi T. Prenatal diagnosis of urinary tract abnormalities. Acta Obstet Gynecol Scand 1997;76:409±13. Poutamo J, Vanninen R, Kirkinen P. Diagnosing fetal urinary tract abnormalities: benefits of MRI compared to ultrasonography. Acta Obstet Gynecol Scand 2000;79:65±71. Kirkinen P, Partanen K, Vainio P, et al. MRI in obstetrics: a supplementary method for ultrasonography. Ann Med 1996;28:131± 136.
[59] Coletti PM. Computer-assisted imaging of the fetus with magnetic resonance imaging. Elsevier Sci 1996;20:491±496. [60] DeCleijn K, Degryse H, Slangen T, et al. MRI in the prenatal diagnosis of bilateral renal agencies. Fortschr Rontgenst Ger 1989;150:140±145. [61] Garden AS, Weindling AM, Griffiths RD, et al. Fast-scan magnetic resonance imaging of fetal anomalies. Br J Obstet Gynecol 1991;98:1217±1222. [62] Levine D, Barnes PD, Sher S, et al. Fetal fast MR imaging: reproducibility, technical quality and conspicuity of anatomy. Radiology 1998;206:549±54. [63] Brookes JAS, Deng J, Wilkinson ID, et al. Three-dimensional imaging of the postmorem fetus by MRI: early experience. Fetal Diagn Therapy 1999;14:166±71.