Revista Chilena de Radiología, año 2016. ARTÍCULO DE REVISIÓN Fetal magnetic resonance imaging in the pre-surgical assessment of spinal dysraphism

Ximena Ortegaa,b,*, Felipe Otayzac, Diego Aranedaab, Karla Moenneb, Carolina Pérezb, Juan Antonio Escaffib, Gonzalo Corralb a Center for Rare Diseases, Clinica Las Condes, Santiago, Chile. b Child Radiology, Diagnostic Imaging Department, Clinica Las Condes, Santiago, Chile. c Department of Neurosurgery, Clinica Las Condes, Santiago, Chile.

Abstract: Spinal dysraphisms are an important indication for fetal magnetic resonance imaging (FMRI), considering the evaluation of possible candidates for intrauterine surgery. FMR has poved to be superior to 3D and 2D ultrasonography for the evaluation of the posterior fossa, brainstem, , and abnormalities of the development of the . The description and level of spinal damage, the degree of hydrocephaly, the magnitude of cerebellar herniation, and the presence of associated lesions are important variables, useful for preoperative planning and comparison with postnatal studies. Keywords: Spinal dysraphism; Magnetic resonance imaging; Ultrasonography; Prenatal; ; Fetal diseases; Prenatal diagnosis.

Introduction must be thorough; taking into account that FMR is not Ultrasound has been and will continue to be the performed as a standard procedure in patients with primary technique for the diagnosis of the central normal ultrasounds, the assessment of true or false nervous system pathology. Magnetic resonance negatives will have a questionable value1. Thus, the imaging, which has revolutionized diagnostic imaging value of the FMR in the evaluation of the central ner- in all areas of medicine, became part of the prenatal vous system pathology, has for several years, been diagnosis with the introduction of fast and ultrafast se- focused on the contribution of additional information quences, which reduced movement artifacts, allowing to ultrasound and in the way in which this information the visualization of the with multiplanar images, is capable of changing the clinical decisions2. Overall, without radiation and with a tissue contrast resolution and according to the review by Rossi and Prefumo1, not described by other techniques. it is currently estimated that in the assessment of the Efforts to improve fetal magnetic resonance central nervous system the findings can be confirmed imaging (FMR) were accompanied by innumerable postnatally (or post-mortem) in about 90% of cases, publications attempting to establish its advantages and that FMR adds findings to ultrasound in approxi- in areas in which ultrasound had been the standard. mately 18%, mainly in relation to midline anomalies, However, the debate over the superiority of images alterations of the posterior fossa, determination and with regards to ultrasound is sterile in the absence of amount of dilation of the , tumors, a quality ultrasound, which allows an early diagnostic maturation of the cerebral cortex, alterations of the suspicion that enables the study by complementary migration, ischemic lesions and hemorrhages, and techniques. Ultrasound is and will continue to be the content evaluation in the presence of hernias3-5. The standard method for screening. Therefore, the com- behavioral changes motivated by these findings are parisons on sensitivity and specificity of both methods currently estimated to be close to 30% of the cases

Ortega X, Otayza F, Araneda D, Möenne K, Pérez C, Escaffi JA, Corral C. Resonancia magnética fetal en el estudio prequirúrgico de disrafia espinal. Rev Chil Radiol 2016; 22(3): 133-139. http://dx.doi.org/10.1016/j.rchira.2016.09.004 Email: [email protected] (X. Ortega).

Received August 31, 2016; Accepted September 11, 2016. Available on the Internet September 29, 2016. 0717-201X/© 2016 SOCHRADI. Published by Elsevier España, S.L.U. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 133 Dra. Ximena Ortega, et al. Revista Chilena de Radiología, año 2016; 22(3): 133-139. studied in the same series, so they support their indi- other anatomical areas. This practice reduces the cost cation, as a second line examination, in the presence and time of the study, but decreases the chances of of alterations detected on ultrasound. diagnosis in the presence of previously unsuspected Open spina bifida or myelomeningocele is a alterations and which could configure a syndromic severe malformation of the central nervous system symptom, since the study through FMR enables the in which an incomplete closure of the spine exposes detection of additional findings in up to 28% of cases8. spinal cord tissue. It is located preferably in the lumbar In our center, we performed routine T2-weighted region and its incidence is estimated at approximately acquisitions on axial, coronal and sagittal planes, 1/1,000 births6. In the prenatal stage, the exposed separately for the head and fetal trunk, using HASTE nerve tissue remains in contact with the amniotic fluid (half-Fourier acquisition single-shot turbo spin-echo) and is highly vulnerable to chemical and traumatic sequences. In these images, the hyperintense cerebros- damage, which impairs the sensorineural function pinal fluid allows, with exquisite detail, the delineation toward distal. The constant loss of cerebrospinal of the ventricular system and both the convexity and fluid through the defect displaces the encephalic the perimedullary subarachnoid space and the limits structures toward the posterocaudal region of the of the vertebral column. We also performed True FISP skull, causing the descent of the posterior fossa, and T1-weighted turbo FLASH sequences of the compression of the foramen magnum and secondary fetal head, to contribute to the search for associated , which is known as Chiari malforma- alterations, with a total study time between 25 and 40 tion type II. Consequently, the affected individuals min, depending on the fetal movements. present irreversible neurological damage, paraplegia, The obtaining of a strict sagittal plane at the triventricular hydrocephalus, bladder, intestinal and encephalon level allows to delimit the contour of the sexual dysfunction, skeletal deformities of the lower cerebellum and the relationship of the tonsils to the extremities and lifetime sensorineural deterioration, foramen magnum. In the spine it is possible to spe- with consequent emotional and financial costs for the cify the defect length in a cephalocaudal direction; family and society. Although considered a non-lethal the precise determination of the involved vertebral anomaly, 15-30% of those affected with spina bifida segments in the defect has been a challenging fact die in the first years of life due to medullary nailing, in the radiological report and, obviously, of greater infection and sepsis, and renal failure. relevance considering the estimation of the level It is now recognized that the damage associated of subsequent clinical commitment of the patients. with spina bifida is not only caused by incomplete However, the difficulty of agreement in establishing neurulation but also by exposure of vulnerable nerve the level of spinal injury among different observers tissue to the intrauterine environment, which is more has already been documented. Simon and Pollock, in evident after 26 weeks of gestation. For this reason, 2004, reported differences of up to 20% in reported open spina bifida has become the first non-lethal cases9. Mangels et al, on the other hand, reported anomaly in which intrauterine surgery is considered discordances considered subtle, when they involved in order to perform neurological rescue, preservation one or two segments, in 43% of cases, and signifi- of neuromotor function and to reverse the herniation cant in 11%4. In spite of the few slices obtained in of the posterior . the trunk scan, due to the small size of the fetus, it is The randomized MOMS7 study showed that intra- possible to program sequences obtaining consecu- uterine surgery reduces the need for ventriculoperito- tive images, not overlapping or volumetric, to access neal shunting by half, significantly improves the motor reconstructions that contribute to the determination function assessed at 30 months of life compared to of the involved anatomical segments, using standard conventional neonatal surgery, and considers FMR in anatomical references. the preoperative evaluation of these patients. As is known, the contrast of the fetal tissues This new surgery during the fetal stage has al- strongly depends on the amount of free water in the ready been performed in our country, which is why structures. The initial concern about the influence of it is necessary to be aware of the findings that are the magnetic field on the developing fetus has been relevant for the perinatal team, both in the selection followed by a period lacking reports of associated de- of and in the approach to the patients. leterious effects. Currently, most studies are performed on 1.5 T resonators, a field that allows an adequate Imaging study protocol definition of contours and difference between the The test may be performed in supine or lateral signal intensities of different tissues. Recently, 3T decubitus according to the tolerance of the patient. resonators have been incorporated, equally safe for Because the indication for imaging with resonance patients, and which also allow for excellent contrast depends on ultrasound findings, many centers have images. The difference in the power of the magnetic opted for targeted evaluation, restricted to the head field should be considered in the programming of a and spine of the fetus, with little or no involvement in fetal study in 1.5 versus 3 T and the sequences require

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adjustments10. The different magnetic susceptibility The American College of Radiology recommenda- to liquids can be, on the one hand, responsible for tion regarding the practice of FMR does not consider new artifacts and on the other hand, allow the visua- the use of intravenous contrast11. Gadolinium during lization of structures, especially vascular or bone, of is considered a type C drug, which means limited representation in images obtained at less field that its safety in humans has not been sufficiently tested. strength. Table 1 summarizes the standard protocol Studies have shown that gadolinium contrasts enter used in our center with 1.5 T and the settings for 3 T. the fetal circulation, crossing the placental barrier12.

Figure 1. T2w HASTE Images in axial plane, from cephalic (A) to caudal (D). Posterior displacement of the medullary cone is observed, with neural tissue outside the medullary canal, in contact with the superficial membrane.

135 Dra. Ximena Ortega, et al. Revista Chilena de Radiología, año 2016; 22(3): 133-139.

Figure 2. Spinal dysraphism, with posterior defect and different sized sac. Sagittal T2w HASTE images with large sac (A), small (B) and absent (C).

Later they are filtered by the kidneys and eliminated presence of cutaneous stigmas. to the amniotic fluid, where it could be swallowed Meningocele and myelomeningocele correspond to again by the fetus, in a cycle whose duration has not pathologies that are suspected in the uterus. In addition been determined. to initially confirming the alteration, the imaging study focuses on fetal surgery as a potential indication. In Findings this way, the focus on the analysis and reporting of Changes to the dorsal induction correspond to a the findings should center on the following points. spectrum of alterations occurring during the first 4-5 Description of the spinal injury weeks of gestation, when the neural tube, the noto- Failure in the closure of the neural tube determines chord, the spine and the skull are formed. From the the separation of the posterior aspect of the vertebra point of view of imaging diagnosis, these alterations with herniation of the and can be divided into spina bifida occulta, meningocele outside the canal (Figure 1). The position of the neural and myelomeningocele3. placode with respect to the level of the skin surface 9 Spina bifida occulta is not usually diagnosed with allows to distinguish the type of open defect . If the prenatal ultrasound, so these patients do not go as hernia sac contains nerve structures, it corresponds far as a second opinion with magnetic resonance to myelomeningocele; if it only comprises fat and imaging. The diagnosis of this alteration occurs during connective tissue, it corresponds to a meningocele the postnatal period, generally associated with the (Figure 2).

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Figure 3. Dorsal myelomeningocele, in axial (A) and sagittal (B) T2w HASTE images.

Figure 4. Colpocephaly, with prominence of posterior horns of , in coronal (A), axial (B) and sagittal (C) T2w HASTE images. 137 Dra. Ximena Ortega, et al. Revista Chilena de Radiología, año 2016; 22(3): 133-139.

Spinal injury level small. Myelomeningocele is often accompanied by Often the alterations will compromise the lumbar or brain anomalies, which include the descent of the lumbosacral region. However, it is necessary to keep in cerebellar tonsils through the foramen magnum. The mind that the defects could be high and even multiple strict sagittal images allow the delimitation of the fo- (Figure 3). Once the defect is identified, it is necessary ramen and the quantification of the herniated tissue to determine the length taking into consideration that towards the caudal region (Figure 5). more extensive commitments will obviously involve a greater number of vertebral segments, depending on Associated injuries the size of the fetus. Recognising the dorsolumbar The detection of associated lesions can immedia- junction is key in the determination of the compromised tely differentiate candidates for prenatal surgery from structural level, in the presence of an adequate defini- those who will not be. The presence of alterations in tion of the bone contours. The dorsolumbar junction the spectrum of spinal dysraphism is described in maintains in its fetal life its habitual relationship with several syndromes and summarized in Table 2. The the ribs, the posterior insertion of the diaphragm and search for alterations of the other segments and organs the superior pole of the kidneys. must therefore be routine and exhaustive (Figure 6). Degree of hydrocephalus Coronal images are useful in the general evalua- Ethical responsibilities tion of the state of the ventricular system and of the Protection of people and animals. The authors convexity subarachnoid space. The determination of declare that no experiments have been performed the bifrontal diameter could be routine in resonance, on humans or animals for this research. considering that it is an easy determination to obtain Confidentiality of the data. The authors declare with ultrasound after birth, enhancing the follow up. that they have followed the protocols of their work The characterization and quantification of the lateral center on the publication of patient data. ventricle dilation is less evaluated in axial images, Right to privacy and informed consent. The authors where it is possible to obtain reproducible measure- declare that no patient data appears in this article. ments of the posterior horns, for example (Figure 4). Conflict of interests Degree of cerebellum herniation The authors declare that there are no conflicts The posterior fossa in these patients is usually of interest.

Figure 5. Spinal dysraphism, with normal posterior fossa and normal amplitude subarachnoid space in sagittal T2w HASTE (A) images and with diminished subarachnoid space (B) associated with a descent of cerebellar tonsils through the foramen magnum. 138 Revista Chilena de Radiología, año 2016. ARTÍCULO DE REVISIÓN

tiple pathologies. Its usefulness in relation to spinal dysraphism in particular goes beyond the confirmation of the findings suspected with ultrasound. In addition to the ability to detect associated alterations that may make surgery not recommendable, resonance has an important role in the description of the defect, the presence and characteristics of the sac and its rela- tionship with neural tissue, for the adequate planning of the neurorrhaphy.

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