Black Bone MRI for Virtual Surgical Planning in Craniomaxillofacial Surgery

Abstract

Advances in computer-aided design and computer-aided manufacturing software have improved translational applications of virtual surgical planning (VSP) in craniomaxillofacial surgery, allowing for precise and accurate fabrication of cutting guides, stereolithographic models, and custom implants. High-resolution computed tomography (CT) imaging has traditionally been the gold standard imaging modality for VSP in craniomaxillofacial surgery but delivers ionizing radiation. Black bone magnetic resonance imaging (MRI) reduces the risks related to radiation exposure and has comparable functionality when compared with CT for VSP. Our group has studied the accuracy of utilizing black bone MRI in planning and executing several types of craniofacial surgeries, including cranial vault remodeling, maxillary advancement, and mandibular reconstruction using fibular bone. Here, we review clinical applications of black bone MRI pertaining to VSP and three-dimensional (3D)-printed guide creation for craniomaxillofacial surgery. Herein, we review the existing literature and our institutional experience comparing black bone MRI and CT in VSP-generated 3D model creation in cadaveric craniofacial surgeries including cranial vault reconstruction, maxillary advancement, and mandibular reconstruction with fibular free flap. Cadaver studies have demonstrated the ability to perform VSP and execute the procedure based on black bone MRI data and achieve outcomes similar to CT when performed for cranial vault reshaping, maxillary advancement, and mandibular reconstruction with free fibula. Limitations of the technology include increased time and costs of the MRI compared with CT and the possible need for general anesthesia or sedation in the pediatric population. VSP and 3D surgical guide creation can be performed using black bone MRI with comparable accuracy to high-resolution CT scans in a wide variety of craniofacial reconstructions. Successful segmentation, VSP, and 3D printing of accurate guides from black bone MRI demonstrate potential to change the preoperative planning standard of care. Black bone MRI also reduces exposure to ionizing radiation, which is of particular concern for the pediatric population or patients undergoing multiple scans.

Craniomaxillofacial reconstruction can be particularly challenging due to the three-dimensional (3D) configuration of anatomical structures and the importance of optimizing both function (e.g., speech, mastication, swallowing, breathing, animation) and aesthetics. Virtual surgical planning (VSP) and 3D-printed surgical models and guides may help to improve operative accuracy and efficiencies, in many cases leading to reduced operative time. ¹ VSP, coupled with advancements in computer-aided design (CAD) and computer-aided modeling (CAM), have made significant impacts on craniomaxillofacial surgical planning. Furthermore, improvements in data derived from computed tomography (CT) and magnetic resonance imaging (MRI) modalities have enhanced the virtual environment and the creation of 3D models for surgical planning and manipulation. Surgeons then use these models to visualize, to analyze, and to manipulate spatial relationships for preoperative planning. ² This allows the surgeon to trial different approaches and to assess outcomes in multiple dimensions even before performing the surgery, such as when determining positions of osteotomies and bone grafts.

High-resolution CT imaging is the gold standard imaging modality for VSP and 3D-printed guide creation. The acquired CT data can then be sent digitally to a medical modeling facility where the data are segmented and processed to create a 3D virtual reconstruction. Engineers then manipulate the reconstruction in the virtual CAD/CAM environment. Surgeons collaborate closely with engineers and medical modeling groups to review 3D segments and create guides based on the images. Quantitative data such as anatomical distances, bone thickness, and volumes can be calculated to assist with planning of osteotomies and hardware placement and fixation.

Developments in medical imaging have improved the diagnosis and treatment of many diseases. For example, CT was instrumental in decreasing the number of exploratory surgeries by providing a way to review anatomy and make diagnoses—benefits which have led to the adoption and increase in utilization of CT imaging. In fact, the number of CT examinations is increasing by approximately 4% per year worldwide, with a total of approximately 300 million CT scans per year. ³

The safety of ionizing radiation has been challenged, especially in the pediatric populations ⁴ who are at risk of radiation-induced brain tumors, leukemia, and increased lifetime risk of carcinogenesis. ⁵ Furthermore, radiation in pediatric patients may have a quantitative effect on skeletal growth, leading to potential deformities and asymmetries. ⁶ Despite the well-documented evidence of adverse effects, approximately 5 to 9 million CT examinations are performed annually on children in the United States. ⁷ In addition, patients exposed to radiation at a younger age are at greater risk of cancer development compared with older patients exposed to the same radiation dose. ⁸ It has been shown that a cumulative dose of 50 to 60 mGy to the head (about the equivalent of two or three typical head CT scans in a child) increases the risk of a brain tumor threefold. ⁵ As a result, multiple centers have adopted a principle of “as low as reasonably achievable” (ALARA), creating CT protocols that minimize radiation. ^{9 10 11 12}

Often cited is the advantage of CT to delineate bone from soft tissue when compared with standard MRI ( Fig. 1 ). In 2012, Eley et al ¹³ termed “black bone MRI” which provided a low flip angle, gradient echo (GRE) MRI sequence which provided a high image contrast between bone and other tissues ( Fig. 2 ). Black bone MRI is a nonionizing alternative for surgical planning that does not require exposure to radiation and has been found to have comparable functionality when compared with CT for surgical planning in multiple settings. MRI-generated surgical guides have the potential to replace CT-generated guides and the risk of ionizing radiation exposure associated with CT scans. Our group has previously studied the accuracy of black bone MRI compared with CT scan in VSP and 3D surgical guide creation for multiple indications. In 2018, we reported that black bone MRI had comparable accuracy for VSP and 3D surgical guides when compared with CT for cranial vault remodeling. ¹⁴ For clinical care in pediatric patients undergoing black bone MRI, coordination of care is necessary to avoid recurring sedation.

Fig. 1.

Standard computed tomography (CT) ( left ) and magnetic resonance imaging (MRI) ( right ).

Fig. 2.

Black bone magnetic resonance imaging (MRI) utilizes a low flip angle MRI technique that can clearly distinguish bone. ( A ) Coronal. ( B ) Sagittal. ( C ) Axial. ( D ) Three-dimensional (3D) reformatting.

Methods

Herein, we report our institutional experience comparing black bone MRI and CT in VSP-generated 3D model creation in cadaveric craniofacial surgeries including cranial vault reconstruction, maxillary advancement, and mandibular reconstruction with fibular free flap, and review and discuss the existing literature related to black bone MRI. Our group has previously evaluated the use of MRI and CT in VSP-generated 3D model creation for craniofacial surgery. ^{1 2}

Cadaveric Dissections

In previous studies, black bone MRI was compared with CT for three common mock craniofacial surgeries performed in cadaveric specimens (cranial vault reconstruction, ¹⁴ mandibular reconstruction with fibular free flap, ¹⁵ maxillary advancement ¹⁶ ). For each surgical procedure, 10 cadaver heads were used. We created 3D-printed guides for five specimens using black bone MRI versus five with CT scans ( Fig. 3 ). Following these mock surgical reconstructions, all specimens underwent a postoperative CT scan. 3D reconstruction was performed and surgical accuracy was compared with the plan and assessed using GeoMagic Wrap (3D Systems Corporation), assessing average postoperative deviation from plan. Our results are further detailed below.

Fig. 3.

Study design. Black bone magnetic resonance imaging (MRI) and computed tomography (CT) was used to create a three-dimensional (3D) guide using virtual surgical planning (VSP) in cadaveric specimens. Mock craniofacial surgeries were performed (cranial vault reconstruction, maxillary advancement, and mandibular reconstruction with fibular free flap) and postoperative CTs were performed to compare the imaging modalities.

MRI was performed in our studies with a 3.0-T, 750-w Discovery Scanner using a 12-channel GEM Head Coil (GE Healthcare, Waukesha, WI). Specimens were positioned inside the coil in the head-first supine position. The 3D axial black bone sequence was then acquired covering the entire specimen's anatomy. The sequence was optimized for 3.0-T MRI (field of view, 24 cm; flip angle, 5 degrees; repetition time, 6.7 ms; echo time, 2.2 ms; matrix, 320 × 320; bandwidth, 31.25; number of excitations, 1; scan time 7 minutes 50 seconds; zero filling interpolation processing, 512). ^{14 15}

Maxillary Advancement

In one study, we compared whether 3D-printed surgical guides created from black bone MRI are comparable in accuracy to those created from CT scans for maxillary advancement. ¹⁴ A mock single-segment maxillary advancement using LeFort 1 osteotomy was virtually planned and performed in 10 fresh cadavers. VSP-derived 3D-printed guides and splints were created from five fresh cadaver specimens using black bone MRI and five fresh cadaver specimens using CT scan. Reconstructed skulls underwent CT scans with 3D reconstruction and accuracy was compared with that of virtually planned surgery. In all surgeries, the guides created from black bone MRI demonstrated high accuracy to the surgical plan. Furthermore, average deviation of postoperative anatomy from preoperative plan was not significantly different between black bone MRI versus CT. Our findings demonstrated that VSP and 3D segmentation and surgical guides could be created with high fidelity using black bone MRI and with comparable accuracy to CT.

Craniosynostosis

In another study, we compared whether 3D-printed surgical guides created from black bone MRI are comparable in accuracy to those created from CT scans for craniosynostosis. ¹⁵ A mock craniosynostosis surgery translocating four calvarial segments was virtually planned and performed in 10 cadavers ( Fig. 4 ). VSP-derived 3D-printed guides and splints were created from five specimens using black bone MRI and five specimens using CT scan ( Fig. 5 ). Reconstructed skulls underwent CT scans with 3D reconstruction and accuracy was compared with that of virtually planned surgery. Importantly, postoperative reconstructions deviated from preoperative plans by less than 1.5 mm, independent of which modality was used for planning, and there was no statistically significant difference in deviation from the plan between the two modalities. These results further demonstrate that black bone MRI is reliable for the creation of surgical guides in calvarial procedures compared with CT without the risk of radiation exposure.

Fig. 4.

A mock craniosynostosis surgery translocating four calvarial segments was virtually planned and performed in 10 cadavers.

Fig. 5.

A mock craniosynostosis surgery was performed in five fresh cadaver specimens using virtual surgical planning (VSP) three-dimensional (3D) guides derived from black bone magnetic resonance imaging (MRI) and five specimens from computed tomography (CT) scan. Black bone MRI was found to be comparable to CT for the creation of surgical guides without the risk of radiation exposure.

Free Fibula Flap Mandibular Reconstruction

Our group also applied black bone MRI to VSP for free fibula reconstruction for mandibular defects. VSP-derived 3D-printed guides were created from five fresh cadaver specimens using black bone MRI and five fresh cadaver specimens using CT scan ( Fig. 5 ). Statistical analysis shows the positive or negative deviation between CT and black bone MRI-based reconstruction was not statistically significant in the whole plated mandible. Upon analyzing individual segments of the mandible in an effort to acknowledge positional error that could be introduced from plating of the segments, no statistical significance was found, except for a negative deviation in the right mandible segment and positive deviation in the left mandible segment. However, the average differences between CT and black bone MRI in these deviations were 0.25 and 0.14 mm. This study demonstrated the ability of black bone MRI to be reliably used in the VSP of surgeries of the long bone, allowing it to be expanded to the use of other osteocutaneous flaps, including the radial forearm free flap and scapular free flap. ¹⁶

Hoving et al ¹⁷ published a study on the optimization of lower jaw resection margin planning by using an added sequence of black bone MRI instead of a CT scan and therefore avoiding the 1- to 2-mm margin of error that can accompany CT and MRI fusion. They found that surface comparison with 3D CT-based models showed average deviation errors between 0.6 and 0.8 mm, signifying it was possible to plan surgical resection guides and reconstruction plates from MRI data. Two cases in the study proceeded with MRI-based surgical planning and MRI-based patient-specific reconstruction plates with successful outcomes, further clarifying the role of MRI-based VSP in this indication.

Literature Review

3D Printing of Anatomic Models

3D printing of models from imaging is an important clinical application which allows for surgical planning, guide fabrication, and patient education. Using previously acquired black bone MRI of an adult and infant with craniosynostosis, Eley et al printed 3D craniofacial models using black bone MRI and CT scan. ¹⁸ Analysis found that 3D models produced from black bone MRI data had reduced discrepancy from the measurements of models produced from CT data, thereby providing a viable imaging alternative in this indication.

Craniosynostosis

Craniosynostosis results from premature fusion of one or more sutures of the calvarium resulting in morphological abnormalities in the craniofacial skeleton. Surgical correction aims to expand intracranial volume, to reduce risk of developing increased intracranial pressure to allow normal brain growth, and to normalize head shape and appearance. The use of VSP and prefabricated cutting guides allow surgical osteotomies to be planned using a 3D template, permitting precise and accurate placement of calvarial bone segments without the need for subjective assessment of the desired calvarial shape. This process also allows patients and families to have a better understanding of the disease process and process through virtual surgery, thereby aligning expectations of parents and surgeons. ¹⁹ Despite added costs of VSP, previous studies have demonstrated cost-effectiveness due to decreased operating room time and improved outcomes. ²⁰ CT has long remained the gold standard imaging modality for diagnosis of craniosynostosis and VSP of calvarial operations.

In a study of nine patients with clinical craniosynostosis, both black bone MRI and 3D CT were performed and images were evaluated by a multidisciplinary group including a craniofacial surgeon, pediatric neurosurgeon, and neuroradiologists. ²¹ The affected synostotic sutures were identified in both modalities in all patients with high intrarater and interrater reliability for rating the calvarial sutures. However, reliability for rating intracranial impressions was low by both imaging methods. Eley et al ²² also compared CT versus black bone MRI in 13 children with clinical diagnosis of craniosynostosis. Patent cranial sutures were identified on black bone MRI with high interrater reliability. Patients with craniosynostosis were consistently identified even by nonexpert assessors as not having a suture line visible, further proving the utility of black bone MRI in this condition.

A retrospective review of six consecutive patients with nonsyndromic craniosynostosis treated in a craniofacial center in Germany demonstrated the utility of “black bone” sequence in CAD/CAM techniques and 3D VSP for preoperative planning. ²³ Black bone MRI was used to generate guides for six patients with trigonocephaly who underwent successful fronto-orbital advancement, demonstrating safety, feasibility, and superior imaging quality of intracranial structures.

Plagiocephaly

Plagiocephaly is a condition characterized by an asymmetrical distortion or flattening of the skull. The current gold standard of diagnosis of posterior plagiocephaly is CT scan, which exposes an infant to ionizing radiation. Through serial assessments, the patient receives a high dose of radiation exposure. A team in Helsinki ²⁴ used black bone MRI in 15 patients with severe posterior plagiocephaly with neurological symptoms, who were without improvement at 18 months of age. Two patients with scaphocephaly were also scanned using black bone MRI and CT imaging to further confirm the diagnostic value of MRI. Accurate images were acquired in all patients, with visualization of brain cortex in other MRI sequences done in the same session. In the scaphocephalic patients, the cranial sutures were identified on both imaging modalities as areas of decreased signal intensity. These sutures were absent in craniosynostosis patients at the site of the pathology, with confirmation on CT scan. The authors commended the quality of black bone MRI sequencing as being sufficient for diagnosis.

Skull Fractures

In a retrospective comparison of two-dimensional head CT and brain MRI with black bone sequence for the detection of skull fractures, MR had lower sensitivity and specificity for the detection of traumatic skull fractures, with cranial sutures being incorrectly interpreted as fractures by pediatric neuroradiologists. The group noted limitations in detection in young children or in fractures of aerated bone. ²⁵

In another study, pediatric patients were evaluated for potential abusive head trauma with noncontrast CT and black bone MRI (both with 3D reconstruction) by two independent pediatric neuroradiologists. ²⁶ Among the 20 skull fractures found on head CT, black bone MRI comparatively demonstrated 83% sensitivity, 100% specificity, 100% positive predictive value, and 97% negative predictive value and accuracy for diagnosis of skull fracture, and detected 95% (19/20) of the skull fractures detected by CT.

Cephalometry

Eley et al compared measurements derived from black bone MRI to those derived from lateral cephalograms in eight patients. ²⁷ The overall mean discrepancy between distance measurements between the modalities was 1 to 2 mm, justifying black bone MRI as a reliable and accurate method for 3D cephalometrics.

Kupka et al ²⁸ studied the use of black bone MRI in cephalometry of the mandible and facial skeleton in 10 children with pathologies of the temporomandibular joint. Although they noted that images required processing for inversion of signal intensity and removal of air, there was excellent intra- and interreader agreement in the 60 linear and 40 angle measurements taken per patient, comparable to cone beam CT, CT, and orthopantomograms. These images were also found to be more accurate than lateral cephalogram radiographs.

Intraosseous Visualization of Inferior Alveolar Nerve

Black bone MRI sequencing has also been used to delineate the anatomy of the inferior alveolar nerve and lingual nerves in healthy volunteers, allowing for differentiation of the tissue composition of the neurovascular bundle inside the mandibular canal. ²⁹ This could have favorable implications on procedures of the mandible and dental implant placement. For example, in mandibular fractures, CT or cone beam CT is used to visualize the mandibular canal, but cannot determine fascicular continuity of the inferior alveolar nerve. Burian et al ³⁰ investigated the use of black bone MRI sequences in 15 mandibular fractures and 15 healthy volunteers and noted the superiority of the imaging modality compared with CT or cone beam CT. Not only was the black bone MRI able to visualize osseous structures comparable to CT, but it was able to depict features of nerve damage, such as edema, involvement of nerve sheaths and fascicular structures, and internal neuroma formation or Wallerian degeneration, thereby allowing for rapid assessment in urgent settings.

Fetal MRI

Fetal MRI is an established imaging modality for abnormalities of the central nervous system and its use has gradually been expanded to evaluate other fetal systems. However, the inability of traditional MRI to delineate bone from soft tissue makes evaluation of the skeletal system challenging. A 2021 study from the United Kingdom looked at the utility of black bone MRI for evaluating fetal skeletal systems. ³¹ Fifty images (from 17 patients) were scored by four blinded observers for images derived from optimized T2-weighted GRE sequence to other “black bone sequences.” The authors found that optimized T2-weighted GRE sequences they had developed offered adequate to excellent image quality in 63% of cases and scored higher than other comparative sequences from the same patient. Image quality was also found to be dependent on gestational age with good image quality achieved on almost all patients after 26 weeks. T2-weighted GRE was proposed to provide adequate fetal “black bone” contrast due to good bone-soft tissue contrast and minimal motion artifacts. These findings could perhaps be extrapolated to allow for imaging in utero for the diagnosis of craniofacial abnormalities and early surgical planning for any associated defects.

Limitations

Although black bone MRI offers advantages in reducing radiation exposure in susceptible populations, it is not without limitations. Absolute contraindications to any MRI are the same as traditional MRI, such as pacemakers, metallic foreign body in the eye, and any implanted magnetic devices. MRI scans are often time consuming and expensive, requiring the subject to lie still for an extended period of time, which may be challenging in many clinical scenarios including in infants, young children, or patients with claustrophobia. Infants and young children may require sedation or general anesthesia for 6 to 8 minutes to achieve images of satisfactory quality. Feeding infants may prompt them to fall asleep so scanning can be performed, but timing of the feed-sleep cycle can make this method unpredictable and challenging. A “black bone” sequence can be added to an MRI scan done under general anesthesia for younger children, but it is difficult to justify the risks of general anesthesia or sedation against the risks of radiation exposure in acute scenarios such as trauma. Older children may often be able to lie still for the duration of the exam, especially with behavioral training or MRI-compatible video goggles. ^{32 33} Discussion with the neurologist or pediatric anesthetist may help to analyze the risk–benefit ratios on a case-by-case basis. Black bone MRI sequencing may also not be as accurate when the subject is of 6 months or younger. The thin bone and higher water content causes the bone to not appear black, leading to difficulty in image segmentation of the skull.

Black bone MRI is also limited by the lack of automated software for 3D reconstruction. ³⁴ Although our group reported no difference in planning time between MRI and CT-based methods, some groups report that MRI reconstruction can take up to three times that of CT. With growing popularity, manufacturers and engineers may collaborate to create widely available software for fast reconstruction. Eley et al ³⁵ have published an algorithm which can perform this automated segmentation.

Although black bone MRI sequencing delineates bone and soft tissue adequately, bone and air have similar appearances due to the signal void of cortical bone, and complete signal loss in air. As a result, portions of the craniofacial skeleton such as paranasal sinuses, floor of the orbit, and mastoid portion of the temporal bone are often difficult to visualize. This has been rectified adequately by Eley et al, ³⁶ by the modification of the GRE black bone with zero echo time, with improvements in image quality of the air/bone interface and dense muscular attachments on 3D reconstructions.

VSP also has inherent limitations, including the time for imaging, planning sessions, coordination of services, manufacturing of models, guides, and implant s . ^{1 2 36 37} Timely planning and logistical improvements can capitalize on the advantages of VSP. VSP is also conditional on multiple processes, subjecting it to potential errors such as miscommunication among teams, or limitations in software incompatibility and imaging formatting which may require reimaging.

Conclusion

Black bone MRI is useful in VSP and 3D guide creation, leading to surgical accuracy similar to computed tomographic scans and eliminating the risk of ionizing radiation exposure. Our group has evaluated the use of MRI and CT in VSP-generated 3D model creation and routinely uses VSP for complex craniofacial surgeries. We have also found black bone MRI to be comparable to CT for several craniofacial surgeries performed in cadaveric studies, including maxillary advancement, cranial vault reconstruction, and mandibular reconstruction with fibular free flap. Our institutional experience and our review of the black bone MRI literature attempts to summarize the known clinical applications of black bone MRI and its implications in reducing exposure to ionizing radiation.