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REVIEW ARTICLE |
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| Year : 2022 | Volume
: 17
| Issue : 5 | Page : 14-20 |
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Imaging in craniofacial disorders with special emphasis on gradient echo Black-Bone and Zero Time Echo MRI sequences
Mario Ganau1, Nikolaos C Syrmos2, Shailendra A Magdum1
1 Department of Neurosurgery, Oxford University Hospitals NHS Foundation Trust, Oxford, United Kingdom
2 Department of Neurosurgery, Aristotle University of Thessaloniki, Macedonia, Greece
| Date of Submission | 04-Apr-2022 |
| Date of Acceptance | 04-Apr-2022 |
| Date of Web Publication | 19-Sep-2022 |
Correspondence Address:
Shailendra A Magdum
Department of Neurosurgery, Oxford University Hospitals NHS Foundation Trust, Oxford
United Kingdom
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/jpn.JPN_46_22
 Abstract | | |
Context: The well-known effects of ionizing radiation on brain cells have been a major driving force toward the use of non-ionizing methods of imaging in both elective and emergency settings. Pediatric neurosurgery has certainly leveraged on this shift in clinical practice, however patients with craniofacial disorders could not fully benefit from the adoption of magnetic resonance imaging (MRI) because computed tomography (CT) scans still retain superior imaging power on bone tissue. Aims: To explore the knowledge available on the use of MRI as surrogate for CT scan in the assessment of craniosynostosis. Settings and Design: A scoping review was designed to identify landmark studies and ongoing clinical trials exploring the accuracy of MRI-based bone imaging in the preoperative planning of pediatric patients with craniosynostosis. Materials and Methods: A total of 492 records were screened from Pubmed, Ovid Medline, Scopus, and Cochrane Library databases; while 55 records were retrieved from ClinicalTrials.gov register. Only clinical studies revolving around the use of Gradient Echo Black-Bone (BB) and Zero Time Echo (ZTE) MRI sequences for the preoperative planning of pediatric craniosynostosis were retained for inclusion. Results and Conclusions: This review identified only five clinical studies reporting a high accuracy of MRI-based 3D bone reconstruction in 47 pediatric candidates to surgical correction of craniosynostosis. Although promising, limited evidence (Level IV) exist that BB and ZTE MRI could help in the surgical planning for craniosynostosis management. The results of two ongoing randomized clinical trials, which are actively enrolling patients, will hopefully help answering this research question.
Keywords: 3D reconstruction, craniosynostosis, neuroradiology, pediatric neurosurgery, preoperative planning
How to cite this article:
Ganau M, Syrmos NC, Magdum SA. Imaging in craniofacial disorders with special emphasis on gradient echo Black-Bone and Zero Time Echo MRI sequences. J Pediatr Neurosci 2022;17, Suppl S1:14-20 |
| Introduction | |  |
The calvaria and craniofacial skeleton are key anatomical areas for radiation protection in view of the radiosensitive brain, lens and thyroid gland.[1] For this, radiation protection in young patients requiring neuroradiology workup has become over the years a matter of paramount importance.[2]
In pediatric neurosurgery, imaging investigations are frequently required for several cranial and craniofacial conditions, including benign ones, such as craniosynostosis (incidence 2.6–7.2 cases per 10,000 live births), which are characterized by the premature fusion of one or more sutures between the cranial vault bones.[3] However, the superior imaging quality of cortical bone on computed tomography (CT) scans and the subsequent ability to create three-dimensional (3D) reconstructions for surgical planning and navigation has largely superseded further development of non-ionizing methods, such as ultrasound (US) and magnetic resonance imaging (MRI), able to provide reliable alternatives for bone and calcified tissues.[4],[5],[6] As such, low dose CT is currently the imaging technique of choice for patients with craniosynostosis.[7]
In 2012, Eley et al. introduced a novel Gradient Echo (GRE) based MRI sequence, better known as Black Bone (BB) imaging, able to improve the natural contrast between soft tissues and bone, therefore allowing for the visualization of calvarial sutures and craniofacial skeleton.[8] Similarly ultrashort echo time and more recently zero echo time (ZTE) imaging have been used to image structures with short T2*-weighted values, including bone. Initial studies demonstrated that BB imaging, as well as ZTE imaging, can distinguish between normal and prematurely fused cranial sutures, and demonstrated segmentation success within the skull allowing for 3D reconstruction in the same way as CT.[9],[10]
As such, the emergence of those MRI sequences started to provide new opportunities for the diagnosis and preoperative planning of those patients, with the caveat of the small number of clinical reports elucidating those aspects of craniosynostosis management. This review aims at determining which progresses have been actually made in the last decade in terms of clinical applications of MRI as surrogate for CT scans in young patients with craniosynostosis, and appraise the speed of diffusion of those technical innovations.
| Materials and Methods | | |
Given the exploratory nature of our investigation a scoping review was considered as the most appropriate study design. The clinical question was well articulated according to the PICO framework: pediatric craniosynostosis as the patient and problem investigated (P); the use of BB and ZTE MRI in preoperative planning as the experimental intervention assessed (I); the comparison with 3D CT scans as control according to standard of care (C), and finally the usefulness of BB and ZTE MRI in the accuracy of surgical planning as the clinical outcome of interest (O).
The review of the relevant literature was conducted on the following electronic databases: Pubmed, Ovid Medline, Scopus, Cochrane Library, and US National Library of Medicine Clinical Trials Register - ClinicalTrials.gov. The following MeSH terms, including combination of them, were used: “black bone MRI”, “ZTE MRI”, “craniofacial”, “craniosynostosis”.
No language restrictions were applied, and the search was extended from 2012 up to 2021. The abstracts of all articles and clinical trials retrieved through this initial search were retained for consideration of inclusion. The initial search was conducted with the assistance of a research librarian and two authors (M.G., N.S.) participated in the triage for landmark papers. Whenever doubts arose regarding the relevance of selected papers the final decision regarding inclusion was taken through a Delphi approach involving the senior author (S.M.A.).
To ensure quality assessment of this review, its design and reporting have been conceived and conducted in agreement with the PRISMA-ScR checklist for scoping review articles,[11] a dedicated flow chart guided us through the identification, screening and inclusion stages of the search conducted through the abovementioned databases and registries [see [Figure 1]]. Accurate in the text referencing of the ClinicalTrials.gov identifier and weblink has also been provided for all trials identified and discussed in this article. | Figure 1: Flow Chart for identification of studies to be included in the scoping review from databases and registries
Click here to view |
| Results | | |
The findings from our scoping review are summarized as follows: firstly, we will provide a summary of the clinical investigations exploring the use of BB MRI; secondly, we will describe the registered clinical trials currently open for patients’ enrolment.
Clinical investigations
The initial literature search retrieved 492 articles on BB and ZTE MRI. Following an initial triage of all abstracts, the full text was obtained for 20 articles on BB MRI and 34 articles on ZTE MRI, all revolving around experimental or clinical applications in craniofacial pathologies. After screening for clinical articles relevant to our research question only 4 clinical studies on BB MRI, and 1 clinical study on ZTE MRI, were identified as suitable reports on the use of those sequences in the routine workup of a total of 47 pediatric candidates to surgical correction of craniosynostosis [see [Table 1]]. The design of those studies and their primary and secondary outcomes were fairly heterogeneous: MRI was used as stand alone preoperative investigation in most patients in only two studies,[12],[13] its imaging resolution was assessed against conventional CT scan in four studies,[13],[14],[15],[16] with evaluation of intra-rater and inter-rater reliability across multiple assessors, such as: neuroradiologists, neurosurgeons and craniofacial surgeons. Feasibility of 3D rendering was confirmed in all 4 studies on BB MRI,[12],[13],[14],[15] but not in the feasibility study on ZTE MRI, which included a wide range of pediatric neurosurgical pathologies including traumas and tumors. While the age range for craniosynostosis patients included in those five articles was 2 to 84 months, their overall mean age was just 23 months. | Table 1: Summary of clinical series identified through the scoping review protocol
Click here to view |
A meta-analysis of those data could not be performed, because all included studies had at best Level IV evidence according to the Oxford Centre for Evidence Based Medicine (OCEBM) criteria.[17] Furthermore, given the different types of craniosynostosis considered there was a slight heterogeneity of surgical rationale, technique adopted and outcome measures among the articles retrieved. Finally, a risk bias assessment could not be completed because all included studies were observational in nature.
Registered Clinical Trials
Out of 55 clinical trials on craniosynostosis registered on ClinicalTrials.gov, 3 revolves around the use of MRI in the management of pediatric patients with such diagnosis. One of those three studies was excluded at time of triaging the initial results of this scoping review because it focused on brain metabolism and monitoring of intracranial pressure, whereas the other two studies are specific to our research question and explore the accuracy of MRI as a surrogate for CT imaging in children up to 2 years of age.
The authors of the pilot study describing the BB imaging protocol have set up a multicentric clinical trial NCT04695938 sponsored by the University of Cambridge and including three highly specialized pediatric neurosurgical units from the following hospitals: Cambridge, Oxford and Great Ormond Street Hospital in London (https://clinicaltrials.gov/ct2/show/NCT04695938). The study started in 2021 and is expected to complete enrolment in 2023, its primary and secondary outcomes are accuracy of diagnosis on MRI of craniosynostosis, and automated segmentation of craniofacial MRI. Authors have calculated that a study population of 80 patients needs to be reached to achieve statistical power.
The literature on MRI with zero echo-time (ZTE) that uses proton density differences rather than T2 relaxation time differences to achieve contrast is relatively rich and extends to several surgical specialties from maxillo-facial surgery to orthopedic surgery. Almost all types of craniosynostosis have also been at the center of the attention, hence the rationale for the comparative clinical trial NCT04704284 sponsored by Mayo Clinic in Rochester, MN, USA, (https://clinicaltrials.gov/ct2/show/NCT04704284) started in 2020 and forecasted to enroll patients until 2022. The goal of the research team is to identify 90% or greater concordance between ZTE MRI and standard CT findings in at least 37 consecutive pediatric patients.
| Discussion | | |
This scoping review highlighted the progressed made in recent years with the identification of MRI sequences meant to allow for a visualization of bone structures with a quality of imaging compatible to conventional CT scans. Despite the scientific literature on such area of imaging investigations touches upon a number of pathological conditions (including those affecting long bones, spine, pelvis, etc.), our attention toward congenital craniofacial pathologies led to a specific focus on pediatric patients with craniosynostosis.
Craniosynostosis and their surgical management
The human skull develops from plates of bone separated from each other by growth lines, consisting of fibrous bands of tissue also known as cranial sutures, which remain open for about 18–24 months. An early fusion of one or more of these sutures leads to abnormally shaped skull.[18]
Craniosynostosis are usually classified according to their incidence, type of suture/s involved and pathogenesis.[19] The most common type of craniosynostosis is scaphocephaly, which is caused by the premature closure of the sagittal suture running between the parietal bones.[20] The unilateral fusion of the coronal suture running between the frontal and parietal bones leads to anterior plagiocephaly, it represents the second most common type of craniosynostosis, and is certainly less complex than the bilateral fusion of both coronal sutures, commonly known as brachycephaly, which causes the baby’s head to grow broad and short.[21] The most rare forms of craniosynostosis include posterior plagiocephaly, caused by the early fusion of the lambdoid sutures, running between the parietal and occipital bones, and trigonocephaly, caused by fusion of the metopic suture running from the baby’s nose to the sagittal suture at the top of the head.[22],[23],[24] Craniosynostosis can also be classified according to their pathogenesis in non-syndromic and syndromic: in fact, they may represent an isolated finding in an otherwise normally developed newborn, or they may occur in the context of complex genetic syndromes and be associated to many other types of cranial and extra-cranial malformations.[25],[26]
In the five studies identified through our scoping review protocol 18 patients had been diagnosed with Posterior Plagiocephaly, 16 patients had Scaphocephaly, 7 patients had Trigonocephaly, 4 patients had Anterior Plagiocephaly, only 4 patients had syndromic craniosynostosis, including: 1 case of Apert Syndrome, 2 cases of Crouzon Syndrome, and 1 case of Saethre-Chotzen Syndrome.
Whilst in many cases the abnormal head shape provides pediatricians and neurosurgeons with the underlying diagnosis, a thorough neuroradiological workup is required to achieve a conclusive diagnosis and establish a treatment plan. Employing MRI protocols in this workup would allow for concomitant visualization of other intracranial structures (often affected by concomitant malformations),[27] cerebrospinal fluid dynamics (often altered by coexistent hydrocephalus),[28] and radiological features of raised intracranial pressure (commonly dictating the urgency of craniosynostosis management).[29] Of note, the authors of all five articles included in this review highlighted such specific aspect. This is not surprising: without going into the complex details of surgical strategies for craniosynostosis, it is worth mentioning that there is a growing body of tools to guide surgical decision-making: in that respect, the greatest recent breakthrough meant to improve the diagnosis and surgical planning has been the use of 3D reconstruction and the availability of new MRI based diagnostic modalities to reduce radiation exposure.[30],[31] Conversely, it must be acknowledged that the use of MRI in such a young patient population would often oblige the treating team to consider sedation or even general anesthesia to conduct those investigations and limit movement artifacts.[32],[33]
MRI protocols as surrogate of CT
Over the last decade the widespread appetite for 3D imaging and printing has also fuelled the high clinical expectations for automated segmentation methods, irrespective of the intrinsic limitations of various imaging methodology. The unrivalled benefits of soft tissue imaging of MRI combined with a desire to avoid ionizing radiation exposure have led to a quest for rapid bone imaging techniques which can obviate the need for CT scans.[4] In an attempt to acquire strong bone signal a combination of GRE techniques were developed to enhance the bone/soft tissue boundary, in doing that scientists leveraged on a combination of short time echo (4 ms) and short repetition time (8 ms), and a low flip angle (5 degrees).[8],[15]
The different nature of BB and ZTE, and their related limitations, suggest a possible synergy between those sequences. In the case of BB MRI, fully automated segmentation methods are complicated due to the uncertainty between air from paranasals sinuses and bone tissue voxels, both yielding no detectable signal; on the other hand, ZTE MRI can easily detect the signal from bone tissue and thus distinguish it from air. However, the latter is characterized by a radial k-space acquisition pattern (which is not time efficient), as well as low flip angles, requiring multiple averages to achieve sufficient signal-to-noise ratio for segmentation purposes: as such, the image resolutions that can be effectively achieved by ZTE MRI in clinical practice are currently lower than BB sequences and limited to ~ 1 mm3.[4] For these reasons the ultimate frontier of MRI-based bone imaging is moving toward two ambitious areas of clinical application. One consists in the potential enhancement of BB sequences by using the high contrast of ZTE to drive segmentation of high resolution GRE based data: basically, ZTE could be used to discern bone from air and soft tissues, whereas BB would offer high resolution to segment bone in those regions of interest.[4] The other consists in the application of segmentation processes to conventional MRI sequences not originally conceived for bone imaging, such as FIESTA (Fast Imaging Employing Steady-State Acquisition) or CISS (Constrictive Interference Steady State).[8],[34]
The development of better contrast and non contrast based imaging protocols able to expand the scope and improve the accuracy of existing imaging methodologies is an excellent example of translational research in neuroradiology.[2] Unsurprisingly, most of the clinical studies identified by this scoping review are translational in nature, in fact, they represent the ultimate expression of a local coexistence, in renowned academic hubs, of strong neuroimaging research teams and busy clinical/surgical units. In fact, the two RCT identified are both conducted by research teams, who are leading the development of those MRI sequences and their continuous refinement, and whose initial clinical experience has been captured by our review of the literature.[15],[16]
Despite the ongoing debate about the most appropriate MRI protocol and segmentation technique to increase the natural contrast between bone and surrounding galea/dura/brain structures, several positive externalities emerging from this research field deserve attention. First, research in pediatric MRI is certainly welcome because, from a radiation protection perspective, there are no known long-term risks associated with MRI, and no contrast medium is required for the purposes of visualizing the calvaria and its open sutures which spontaneously appear hyperintense, and well distinguishable from closed ones.[35] Second, the implementation of protocols revolving around ZTE sequences, and the emergence of silent ZTE MRI, has allowed decreasing the acoustic noise intrinsic of MRI machine, hence bringing hopes of improving patients’ compliance with such type of investigation.[36] Third, this type of research is fostering the ease of 3D rendering of MRI images through commonly available imaging software, either proprietary ones, such as: OsiriX (Pixmeo) and MicroDicom (Microsoft), or free open source ones, such as: Horos, 3D Slicer, Miele-LXIV, InVesalius 3, Weasis. 3DimViewer, etc.
Limitations of this scoping review
Two types of limitations, both considered and accepted at time of designing it, affect this study: one is related to the limited diffusion of BB MRI beyond neurosurgical departments involved in clinical research, and the other regards the very narrow clinical application investigated. Those limitations are interconnected because the limited diffusion is currently providing only Level IV evidence according to OCEBM criteria, therefore there would be significant medico-legal implications in adopting such MRI protocols outside the boundaries of well-defined Institutional Review Board (IRB) approved prospective studies and internationally registered clinical trials. Although this review was not exploring various human factors and technical aspects intrinsic to the theory of diffusion of technology,[37] the importance of the following drivers:
- -relative advantage (to conventional CT),
- -compatibility (with conventional MRI machines),
- -complexity (image acquisition and processing),
- -trialability (ease of use by new adopters among radiographers and radiologist),
- -observability (the degree in which the results brought by the adoption of those MRI sequences can be seen by others likely to adopt them),[38]
should not be underestimated in any future study about BB MRI, ZTE MRI or any other manipulation of MRI sequences meant to expand the scope of this neuroimaging modality.
| Conclusion | | |
The review of the literature provided in this article offers an update on the use of various MRI sequences available as alternative to CT scan for the preoperative planning of pediatric patients diagnosed with craniosynostosis.
Whereas the promising preliminary data from the clinical studies published so far indicate the potential of BB and ZTE MRI sequences as an alternative to low dose 3D CT scan, the low quality evidence achieved so far seems to suggest that it will take some time before such MRI sequences will be officially considered as a reliable diagnostic option in the growing pediatric neuroradiology armamentarium.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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[Figure 1]
[Table 1]
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