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Using Three-Dimensional Printing to Create Individualized Cranial Nerve Models for Skull Base Tumor Surgery
Original Article
Using Three-Dimensional Printing to Create Individualized Cranial Nerve Models for Skull Base Tumor Surgery Jiye Lin1,4, Zhenjun Zhou1, Jianwei Guan1, Yubo Zhu1, Yang Liu1, Zhilin Yang1, Bomiao Lin2, Yongyan Jiang2, Xianyue Quan2, Yiquan Ke1, Tao Xu3
OBJECTIVE: Using three-dimensional (3D) printing to create individualized patient models of the skull base, the optic chiasm and facial nerve can be previsualized to help identify and protect these structures during tumor removal surgery.
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METHODS: Preoperative imaging data for 2 cases of sellar tumor and 1 case of acoustic neuroma were obtained. Based on these data, the cranial nerves were visualized using 3D T1-weighted turbo field echo sequence and diffusion tensor imagingebased fiber tracking. Mimics software was used to create 3D reconstructions of the skull base regions surrounding the tumors, and 3D solid models were printed for use in simulation of the basic surgical steps.
CONCLUSIONS: 3D printed models of skull base tumors and nearby cranial nerves, by allowing for the surgical procedure to be simulated beforehand, facilitate preoperative planning and help prevent cranial nerve injury.
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RESULTS: The 3D printed personalized skull base tumor solid models contained information regarding the skull, brain tissue, blood vessels, cranial nerves, tumors, and other associated structures. The sphenoid sinus anatomy, saddle area, and cerebellopontine angle region could be visually displayed, and the spatial relationship between the tumor and the cranial nerves and important blood vessels was clearly defined. The models allowed for simulation of the operation, prediction of operative details, and verification of accuracy of cranial nerve reconstruction during the operation. Questionnaire assessment showed that neurosurgeons highly valued the accuracy and usefulness of these skull base tumor models.
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Key words 3D printing - Cranial nerve - Simulated surgery - Skull base surgery -
Abbreviations and Acronyms 3D: Three-dimensional CPA: Cerebellopontine angle CT: Computed tomography DTI: Diffusion tensor imaging ICA: Internal carotid artery MRI: Magnetic resonance imaging
INTRODUCTION
M
ost skull base tumors are benign, in contrast to tumors located in the brain hemispheres, and their surgical removal is often sufficient to ensure patient recovery. However, as the anatomic structure of the skull base is complex, tumor excision can often be very challenging,1 and this difficulty is further compounded by the high degree of variation among patients, which limits the usefulness of generalized anatomic models. It is therefore particularly important to develop highquality surgical training tools to improve the accuracy of preoperative diagnosis and surgical design and to reduce postoperative complications. With the advent of microneurosurgery, the focus of skull base surgery has shifted from maximizing the excision of tumor tissue to protecting the cranial nerves. Traditionally, total tumor resection and patient safety have mainly relied on the surgeon’s experience and skills, neurophysiologic monitoring, and neuronavigation, but such methods are inconvenient to use and involve significant surgical field exposure and lengthy preoperative preparation. Three-dimensional (3D) printing technology, through which scans of the patient’s brain can be recreated as a physical object, could make preoperative assessments more accurate and
From the 1National Key Clinical Specialty, Engineering Technology Research Center of Education Ministry of China, Guangdong Provincial Key Laboratory on Brain Function Repair and Regeneration, Department of Neurosurgery, and 2Department of Radiology, Zhujiang Hospital, Southern Medical University, Guangzhou; 3Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing; and 4Department of Neurosurgery, Shunde Hospital, Southern Medical University (The First People’s Hospital of Shunde Foshan), Foshan, China To whom correspondence should be addressed: Yiquan Ke, Ph.D.; Tao Xu, Ph.D. [E-mail: [email protected]; [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.236 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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surgical simulations more realistic by allowing them to be performed in the operating room rather than in virtual spaces. The application of 3D printing methods to clinical neurosurgery has been increasing; for instance, Ryan et al.2 recently used 3D printing to create a patient brain model containing 9 different features of intracranial aneurysms to simulate aneurysm clipping surgery with highly satisfactory results, as indicated by questionnaire evaluation. In another example, Thawani et al.3 printed a large 3D intracranial arteriovenous malformation model capable of accurately representing the hemodynamic characteristics of these structures. The subsequent survey showed that surgeons found the 3D printed model to be more helpful than the virtual models in diagnosing and treating complex vascular diseases. Finally, Park et al.4 described a procedure in which 3D printed titanium implants were used for the successful repair of skull defects in 21 cases. However, studies on skull base tumor models are still rare, and 3D printing research involving the cranial nerves associated with skull base tumors in particular has, to our knowledge, not been reported as of yet. The precise visualization of cranial nerves could have significant diagnostic and surgical consequences. If preoperative imaging is combined with 3D printing to show the location of the cranial nerves and the route through which they travel relative to the spatial location of the skull base tumor, it could allow the surgeon to better identify and protect these nerves during the operation and thus improve the safety and accuracy of surgical resection while shortening the length of the operation. There have been numerous reports more recently on the use of diffusion tensor imaging (DTI) to track cranial nerves, and the clinical utility of this approach has also been repeatedly verified.5-9 We also found that the combination of magnetic resonance imaging (MRI) 3D T1-weighted turbo field echo and 3D volumetric isotropic turbo spin echo acquisition sequences showed very encouraging results when used to image cranial nerves. The former in particular is a newly developed scan sequence based on classic gradient echoes and steady-state approaches. As the contrast between the water-containing nerve fiber and surrounding tissues is greatly increased when using this method, the 3D T1-weighted turbo field echo acquisition layer thickness can be reduced to 0.7e5 mm, thus making this approach more capable of spatially resolving neural structures than the spin echo sequence. The 3D volumetric isotropic turbo spin echo acquisition sequence is an MRI water imaging technique that has been demonstrated to provide a high T2-weighted cerebrospinal fluid signal in both the internal auditory canal and the cerebellopontine angle (CPA) while being able to show the relatively low-signal nerve fiber structure more prominently. We previously reported the usefulness of 3D printed models of brain and aneurysms for surgical simulations.10 In surgery for skull base tumors, our 3D-printed model of the sellar region and a CPA tumor, with the skull base rendered in transparent resin, permitted the direct visualization of structures that would otherwise have been invisible. In addition, our use of functional MRI to image the optic chiasm and facial nerve helped to effectively guide the surgeon in surgical resection and cranial nerve protection.
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MATERIALS AND METHODS Patient Population Two cases of sellar region tumor (a 59-year-old man with a tumor measuring 27 26 37 mm and a 40-year-old man with a tumor measuring 37 36 35) and 1 case of acoustic neuroma (a 34year-old man with a tumor measuring 26 33 24 mm) were selected for this study. 3D printing was used to create solid color cranial models that included all surgically related cranial nerves, which were used for preoperative surgical design and simulation of the tumor resection procedure. Image Acquisition Sellar Region Tumors. Contrast-enhanced computed tomography (CT) angiography scans (Brilliance CT; Philips Healthcare, Amsterdam, Netherlands) with a scanning layer thickness of 1 mm and a layer spacing of 0.5 mm were obtained together with 3.0T MRI (Ingenia R4.1; Philips Healthcare) conventional plain and enhanced scans. Magnetic resonance angiography and magnetic resonance venography scans were obtained using 3D time-of-flight spoiled gradient echo method and phase contrast method, respectively. The DTI sequence used the following settings: repetition time 7849 ms, echo time 80 ms, field of view 256 mm 256 mm, data matrix 128 128, thickness 1 mm, layer gap 0, 40 slices, and voxel size 1 1 1 mm. The number of excitations was set at 2, and the b value was 0.1000. The diffusion-sensitive gradient direction was 32. The 3D T1-weighted turbo field echo sequence parameters were repetition time 8.1 second, echo time ¼ 3.8 seconds, flip angle 7 , matrix 224 224, reconstruction matrix 256 256, field of view 256 mm 256 mm, scanning layer thickness 1 mm, layer gap 0, and number of acquisitions 1. Acoustic Neuroma. CT angiography, contrast-enhanced and plain MRI, magnetic resonance angiography, magnetic resonance venography, and DTI scans were performed as already described. 3D volumetric isotropic turbo spin echo acquisition sequence used the following settings: repetition time 2000 ms, echo time 457 ms, voxel size 1 1 1 mm, and matrix 256 256. 3D Reconstruction The imaging data of the aforementioned patients were imported into Mimics Research Version 17.0 (Materialise, Leuven, Belgium) in Digital Imaging and Communications in Medicine format. Gray scale was used to define distinct objects, following which the threshold segmentation function was used to separate different tissues from one another. Subsequent steps included separating the data with the same gray scale but belonging to different tissue, sketching out some unclear structures, and then reconstructing through the algorithm of the software. For large tumors, cranial nerves appeared unclear combined with DTI fiber tracking. Tumors, brain tissue, cranial nerves, and arteriovenous vessels were derived from MRI, and skull and arteries were derived from CT. MRI and CT data were combined based on magnetic resonance angiography and CT angiography. Finally, different colors were used to mark different tissue structures, saved in STL (stereolithography) format, and exported as 3D PDF files. The above steps were independently performed by 2 neurosurgeons (J.Y.L. and
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J.W.G.) who were familiar with the software, and the results were compared. 3D Printing Process In this study, the Connex3 Objet350 3D printer (Stratasys, Eden Prairie, Minnesota, USA), which uses PolyJet technology similar to ordinary inkjet printing, was used. Its triple jet technology allows it to mix almost all flexible, rigid, and transparent color materials by adjusting the proportions of the 3 basic materials (VeroCyan, VeroMajenta, and VeroYellow) incorporated into printed structures. The photosensitive polymeric material is sprayed layer by layer onto a build tray, and each layer of the photosensitive polymeric material is cured with ultraviolet light immediately after being ejected, creating a solid model. STL files were inserted into the printer, and elements such as material, color, transparency, and texture for various tissues or locations were set. A soft texture was selected for tumor regions, allowing the material to be easily cut and separated. With the transnasal sinus surgery model bisected along the midline, structures such as the sphenoid sinus space, arteries, and optic canal protuberance could be easily discerned. After the 3D solid model was completed, the SUP705 nontoxic gel-like photosensitive resin support material was removed using a water spray. Simulation of Surgery on 3D Printed Model We used 3-matic Version 9.0 software (Materialise) to adjust the virtual visualization skull base tumor model according to the
surgical approach to make the structure of the target region translucent, to visually understand complex anatomic relationships, and to simulate surgical procedures for tumor removal (Figure 1). Based on the experience of virtual surgical operations, the surgical plan for resecting the tumor was again simulated on the 3D printed solid models. Different surgical approaches were used to perform simulated surgery on skull base tumors to determine the best surgical route and range of skull opening windows. The critical anatomic landmarks, such as the skull, vessels, and cranial nerves, are gradually revealed during the resection process. Accurate intraoperative navigation and guidance of the surgical process were achieved.
Evaluation of Accuracy and Practicability A preliminary assessment questionnaire based on recent literature of a similar nature while taking into account the particularities of the characteristics and functions of the skull base tumor model used in this study was created.11-13 The questionnaire contained 11 items covering 3 aspects: the accuracy of the model, its practicability, and an overall evaluation. Each item was scored on a 5-point scale, with the highest score being 5. We invited 16 neurosurgeons with 3e11 years of experience (average 6.81 2.53 years), all of whom were familiar with skull base surgery, to score our 3D printed skull base tumor models using the questionnaire after they were given the opportunity to examine and manipulate the models.
Figure 1. (AeC) Simulated surgery on three-dimensional printed models.
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RESULTS
measure where drilling should be performed dimensions of the saddle (Figures 4 and 5).
Optic Chiasm and Relative Position of Sellar Region Tumor 3D printed solid models clearly showed the saddle area surgical space and directly reflected the huge tumor pushing the adjacent blood vessels and optic chiasm and the tumor destroying the skull base bone, which is consistent with the result of the virtual surgery. Via a classic frontotemporal approach, we first grinded the sphenoid ridge and made semicircular incisions into the meninges, revealing the sylvian fissure and frontal and temporal lobe. Then the superficial sylvian veins were separated from the wrapped arachnoid. Based on the relative position of the optic chiasm to the tumor, which could be classified into 1 of 3 broad categories—frontal inferior, frontal superior, and posterior superior type (Figure 2)—we selected a specific operative space (Figure 3). In the endoscopic transnasal approach, the distance from the midline was estimated using anatomic landmarks of the septum of the sphenoid sinus combined with the carotid artery protrusion and the optic nerve canal protrusion to
Figure 2. Relative locations of sellar tumors in reference to the optic chiasm. Sellar tumors fall into 1 of 3 broad categories: frontal inferior (A1 and A2),
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and
the
Cranial Nerves Surrounding Acoustic Neuromas We designed our surgical approach in this case based on the relative positions of the cranial nerves and the acoustic neuroma in the virtual model, with an emphasis on protecting the cranial nerves and vital blood vessels during simulated surgery. The asterion was first identified on the 3D printed model, and the anatomic details of the CPA region were considered from the perspective of a posterior suboccipital retrosigmoid approach. The path of the facial nerve, trigeminal nerve, glossopharyngeal nerve, and vagus nerve pushed by the tumor was gradually revealed. We then simulated grinding the inner auditory canal to remove the tumor (Figure 6). The positional relationship between facial nerves and acoustic neuromas is divided into 6 types: facial nerves are located in the anterior upper, anterior middle, anterior lower, superior, inferior, and posterior portions of the tumor (Figure 7).
frontal superior (B1 and B2), and posterior superior (A3 and B3).
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Figure 3. Simulation of a saddle area tumor resection on a three-dimensional printed model using pterional approach. (A) Bone centered on the pterion is removed to expose brain tissue. (B) The arachnoid membrane is cut at the front of the lateral septum to separate the lateral septal vein. (C) The frontal lobe and temporal lobe brain tissue are retracted, and (D) the sellar region
Clinical Evaluation Results Our models were awarded average scores of 3.94 0.60, 4.14 0.52, and 3.81 0.52 for their accuracy, practicability, and overall evaluation by the 16 neurosurgeons who were invited to complete a
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tumor and surrounding anatomic space are revealed. The internal carotid artery, optic nerve, and optic chiasm are identified. (E) A portion of the tumor is removed from the internal carotid artery and medial space of the optic nerve. (F and G) The tumors are resected in the preoptic gap. (H) The tumors are removed.
questionnaire after inspecting and handling the models (details of the survey items and the scores and comments from reviewers are provided in Table 1). These favorable scores indicate that the skull base tumor model has great potential as a neurosurgery training tool.
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Figure 4. Assemblable three-dimensional printed model. (A) To facilitate observation of the anatomic structure of the sphenoid sinus under the naked eye, the transsphenoidal surgical model is bisected along its midline and reassembled with an adhesive. (B) Key anatomic structures, such as the sphenoid sinus orifice
DISCUSSION In this article, we describe the application of 3D printing technology to create complex sellar region and CPA tumor solid models containing cranial nerves. Preoperatively, the position of the cranial nerves pushed or wrapped by the tumor can only be inferred. This knowledge would be very helpful for the choice of individual surgical routes and intraoperative microsurgery. A 3D printed solid model that simulates frontotemporal, endoscopic transnasal, and retrosigmoid approaches allows us to recognize and understand the most pertinent anatomic details from a completely new perspective. In particular, tracing the individual cranial nerves can help the surgeon to quickly identify and formulate strategies to protect these delicate structures. Previous 3D printed models focused only on the relationship between tumors and peripheral blood vessels, lacking the information required for cranial nerve reconstruction in microneurosurgery.14-16 Having a clear impression of the location of the sellar tumor, internal carotid artery (ICA), and optic chiasm is crucial for the
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in right half of the model, are identified. (C) The skull, being transparent, allows the internal carotid artery, optic nerve, and optic chiasm of the sphenoid sinus lateral wall to be seen. (D) The sphenoid sinus separation is clearly visible in left half of the model.
repair of lesions in the sellar and parasellar regions.17-20 Displacement of the optic chiasm by tumor changes the size of the anatomic gaps in the sellar region. Thus, precise knowledge of the position of the optic chiasm before surgery can be very helpful in choosing an appropriate surgical approach. Given that the distance between the anterior inferior chiasm and the saddle tubercle is relatively small, the raised structure of the latter can have an inordinate effect on the exposure of the suprasellar region in the case of a frontotemporal approach. As the 3D printed skull base tumor model shows the specific spatial arrangement of the tumor, optic nerve, and optic chiasm, we believe that it could play a very important role in the surgical planning once it is made widely available to surgeons. For instance, if the tumor is of a frontal inferior type, the anterior third ventricle could be thinned to allow the tumor to be more easily seen, or the laminae terminalis could be opened to expose the tumor more fully, which may be very useful for the removal of craniopharyngiomas or gliomas occurring in the third brain ventricle. If the tumor extends into the
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Figure 5. Simulation of sellar tumor resection on three-dimensional printed model using endoscopic transnasal approach. (A) Sphenoid sinus pneumatization and sequestration are shown on computed tomography angiography. (B) The sphenoid sinus orifice located in the crypts of the sphenoidal sinus is found. (C and D) The anterior sphenoid sinus is drilled. (E and F) The sphenoid
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septum is removed; the sinus cavity is washed; and anatomic landmarks including the optic nerveeinternal carotid artery internal angle, optic nerve canal protrusion, carotid artery protrusion, and slope crypt are identified. (G and H) The portion of saddle fundus that can be safely abraded away is measured; bone is removed from the center of the saddle.
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Figure 7. (A) Relative positional relationship between a tumor occurring in the cerebellopontine angle area and the facial nerve. (B) Tumor location may be classified as
side of the sella, the gap between the ICA and the optic nerve could be enlarged, and the tumor can be removed from the gap. The saddle area tumors in this study were adjacent to both ICAs and their branches, pushing the optic chiasm to a frontal superior position, with the tumor growing around the left optic nerve, extending partly into the left optic foramen. A conventional subfrontal approach in this instance would not allow adequate access to the mass via the foramen and would inevitably result in contact with the right optic nerve as well. Based on our 3D printed model, it was determined that the chiasm was in a frontal superior position, and so a left frontotemporal approach was chosen instead. In the operation, the tumors were excised mainly through the gap between the optic nerve and the ICA and the optic chiasm anterior gap, resulting in success in both cases. The structural features of the skull that are frequently used as landmarks during surgery may on certain occasions be occluded by the base of the skull. This, in combination with patient-topatient variations in anatomy, may make it difficult to achieve proper exposure of the cranial nerve. Although it is possible for an experienced surgeon to judge the position of the cranial nerves, such an approach introduces an element of error that could result
1 of 6 types: posterior (a), inferior (b), anterior lower (c), anterior middle (d), anterior upper (e), or superior (f).
in permanent visual field defects, blindness, and other catastrophic complications. In neuroendoscopic transnasal surgery, the carotid artery protrusion or optic nerve canal protrusion is sometimes not obvious, an issue that is circumvented via our use of transparent epoxy resins in our 3D models, which allows these structures to be seen. This significantly improves on the models designed by Tai et al.,21 in which the use of opaque materials in the construction of the skull caused key anatomic features, such as the ICA and the optic canal, to be hidden from view. By contrast, our model allows the spatial distance between the tumor and the ICA and the passage of the optic nerve through the skull to be easily seen. According to the spatial relationship between the sphenoid sinus, saddle fundus, and tumor, the scope of the saddle fundus can be abraded to avoid the coronal interval of the sphenoid sinus being mistaken for sphenoid posterior wall or the sagittal interval as the midline22 and occurrence of ICA or optic nerve injury. The suboccipital retrosigmoid approach is the most commonly used surgical approach for the treatment of CPA tumors. Because the affected region is adjacent to several important blood vessels, cranial nerves, and the brainstem, the
Figure 6. Simulation of acoustic neuroma resection on a 3D printed model. (A) Diffusion tensor imaging is used to visualize the facial nerve of acoustic neuroma. (B) In the skull, the asterion (star) and the bone hole of the vena emissaria occipitalis can be seen. (C) The transparent skull allows the safe distance between the transverse sinus and sigmoid sinus and the asterion (star) can be measured. (D) The brain tissue is retracted partially to reveal the tumor. Tumor tissue is separated gradually, and the adjacent cranial nerves and blood vessels are exposed. (E) The upper pole of the tumor is removed until the trigeminal nerve is visible. (F and G) Removal of the lower pole exposes the posterior cranial nerves. (H) The wall of the inner auditory canal is abraded, and (I) the tumor tissue in the inner ear is removed. (J) The tumor capsule is kept intact, as the facial nerve lies beneath the capsule.
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Table 1. Three-Dimensional Printed Skull Base Tumor Model Evaluation Survey Results from 16 Neurosurgeons Survey Items
Score
Other Comments
3.94 0.60
Accuracy* Skull
4.18 0.72
Brain tissue
3.75 0.55
Not soft enough and fragile
Artery
3.87 0.48
Lack of flowing blood Lack of flowing blood
Vein
3.81 0.63
Optic nerve or facial nerve
4.00 0.50
Tumor
4.06 0.55 4.14 0.52
Practicabilityy Identify bony landmarks (sphenoid sinus, pterion, cerebellopontine angle)
4.25 0.55
Identify optic chiasma position
4.12 0.59
Identify facial nerve position
4.06 0.42
Simulate tumor resection
4.12 0.48
Can see inside the structure through the transparent skull
No blood flow after excision The arachnoid adhesions around tumor cannot be simulated
3.81 0.52
Overall evaluationz
*Don’t know ¼ 1; Mostly inaccurate ¼ 2; Basically accurate, but lacks some details ¼ 3; More accurate ¼ 4; Highly accurate, no changes needed ¼ 5. yDon’t know ¼ 1; No help ¼ 2; Little help ¼ 3; Some help ¼ 4; Very helpful ¼ 5. zDon’t know ¼ 1; Need much improvement ¼ 2; Need some adjustment ¼ 3; Need a little improvement ¼ 4; Excellent, no changes needed ¼ 5.
operating space available is quite narrow. Accurately estimating the scope of excision in the internal auditory canal and the relative positions of the facial nerve and the tumor is thus very important.23,24 With the 3D printed CPA tumor model, we can now precisely determine the location of the asterion and the size of the window that needs to be created in the skull to obtain the optimal operating space via simulation. As most tumors in the region tend to be schwannomas, opening the internal auditory canal and resecting the residual tumor tissue is an important means to prevent disease recurrence. However, owing to large variations in individual anatomy and the close apposition of the bony semicircular canal and the vestibule with the posterior wall of the internal auditory canal, there is a significant risk that tumor removal may not be complete if the surgeon is too conservative or that the semicircular canal may be damaged if the ablation process is too excessive. In such an instance, a patient-specific 3D model with an auditory canal that can be removed from the bony structures that enclose it could be very helpful. 3D printed models could also be useful for locating where the cranial nerve passes close to the tumor within the CPA and help reduce intraoperative damage to the facial nerve, in addition to shortening the length of the operation. Surgeons with experience in acoustic neuroma surgery are well acquainted with the normal orientation of the facial nerve and would be able to roughly infer the position of the facial nerve based on neurophysiologic monitoring. However, it is challenging to determine accurately whether the facial nerve in each patient is located below or above the ventral aspect of the tumor, or if it passes by its lower or (in very rare cases) dorsal pole.6 By recreating the cranial nerves in the CPA in resin based on imaging data, this problem may be effectively nullified.
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Therefore, we propose that the 3D printed skull base tumor model be used as a “living textbook” for skull base anatomy that can be used by junior physicians to learn and design neurosurgical strategies or as practical training tools to be used in simulated surgeries. Our preliminary questionnaire evaluation indicated that the 3D print model is capable of providing enough detail regarding the 3D anatomy of structures surrounding the tumor. The blood vessels and cranial nerves were found to be particularly useful signposts to gauge the progress and scope of surgery, and the models were judged to be better than the traditional twodimensional tomography in this regard. It was also mentioned that simulated surgeries conducted with the models may be helpful for procedures involving areas close to the cranial nerves or to critical vasculature. Finally, the models may also facilitate the prediction of complications that may occur during procedures and allow for contingency plans to be put in place ahead of time. This is in agreement with previous studies, which have also concluded that high-quality 3D printing models could have a positive impact on the skills of surgeons by providing them with more realistic simulations.11-13 Limitations and Future Directions In practice, we found that the shape of the cranial nerves in the 3D printed models were not always completely consistent with the actual shape seen during the operation and that the models were currently mainly useful only for determining the traveling and position of the fiber bundles and the degree to which they are displaced by the tumor. This may be due to the fact that extended compression of the nerve fibers by the tumor leads to changes in the density, parallelism, and integrity of the myelin sheath, which alters how water diffuses through the fiber. As DTI is based on the
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fractional anisotropy of water molecules,25 these changes could interfere with achieving an ideal spatial resolution and signal-tonoise ratio for nerves that are thus affected. In addition, the release of cerebrospinal fluid during surgery causes brain tissue to retract and shift within the cranium. As our model is composed of materials that are comparatively more rigid, it is difficult to simulate this dynamic process. Therefore, future designs will focus on solving these problems by increasing blood circulation and altering the model so that intracranial pressure changes can be replicated. In addition, as MRI currently can capture only major vascular structures, there will still be a need for intraoperative monitoring of bleeding from small blood vessels <1 mm in diameter that are invisible to this imaging technique to minimize the incidence of complications. Finally, this study examined a small patient population. To more thoroughly study the value of 3D printing in skull base tumor surgery, randomized controlled
REFERENCES 1. Maroon JC. Skull base surgery: past, present, and future trends. Neurosurg Focus. 2005;19:E1. 2. Ryan JR, Almefty KK, Nakaji P, Frakes DH. Cerebral aneurysm clipping surgery simulation using patient-specific 3D printing and silicone casting. World Neurosurg. 2016;88:175-181. 3. Thawani JP, Pisapia JM, Singh N, Petrov D, Schuster JM, Hurst RW, et al. Three-dimensional printed modeling of an arteriovenous malformation including blood flow. World Neurosurg. 2016; 90:675-683.e2. 4. Park EK, Lim JY, Yun IS, Kim JS, Woo SH, Kim DS, et al. Cranioplasty enhanced by threedimensional printing: custom-made threedimensional-printed titanium implants for skull defects. J Craniofac Surg. 2016;27:943-949. 5. Hodaie M, Quan J, Chen DQ. In vivo visualization of cranial nerve pathways in humans using diffusion-based tractography. Neurosurgery. 2010; 66:788-795 [discussion: 795-796]. 6. Song F, Hou Y, Sun G, Chen X, Xu B, Huang JH, et al. In vivo visualization of the facial nerve in patients with acoustic neuroma using diffusion tensor imaging-based fiber tracking. J Neurosurg. 2016;125:787-794. 7. Yoshino M, Kin T, Ito A, Saito T, Nakagawa D, Ino K, et al. Combined use of diffusion tensor tractography and multifused contrast-enhanced FIESTA for predicting facial and cochlear nerve positions in relation to vestibular schwannoma. J Neurosurg. 2015;123:1480-1488. 8. Yoshino M, Abhinav K, Yeh FC, Panesar S, Fernandes D, Pathak S, et al. Visualization of cranial nerves using high-definition fiber tractography. Neurosurgery. 2016;79:146-165. 9. Hilly O, Chen JM, Birch J, Hwang E, Lin VY, Aviv RI, et al. Diffusion tensor imaging tractography of the facial nerve in patients with cerebellopontine angle tumors. Otol Neurotol. 2016;37: 388-393.
trials involving large sample sizes derived from multiple centers will need to be conducted. CONCLUSIONS Our 3D printed skull base tumor model incorporates cranial nerve structures and is a very realistic neurosurgical training tool. Simulation performed on the solid model can be used to optimize the surgical strategy. These models help facilitate intraoperative navigation and positioning, allowing surgeons to rapidly identify the cranial nerves that are severely displaced by tumors and can effectively reduce intraoperative cranial nerve damage and ensure the safety and efficiency of the procedures. ACKNOWLEDGMENTS We thank the surgeons who participated in this study.
10. Lan Q, Chen A, Zhang T, Li G, Zhu Q, Fan X, et al. Development of three-dimensional printed craniocerebral models for simulated neurosurgery. World Neurosurg. 2016;91:434-442. 11. Ryan JR, Chen T, Nakaji P, Gonzalez LF. Ventriculostomy simulation using patient-specific ventricular anatomy, 3D printing, and hydrogel casting. World Neurosurg. 2015;84:1333-1339. 12. Da CM, Francis HW. Face and content validation of a novel three-dimensional printed temporal bone for surgical skills development. J Laryngol Otol. 2015;129(suppl 3):S23-S29. 13. Mashiko T, Otani K, Kawano R, Konno T, Kaneko N, Ito Y, et al. Development of threedimensional hollow elastic model for cerebral aneurysm clipping simulation enabling rapid and low cost prototyping. World Neurosurg. 2015;83: 351-361. 14. Muelleman TJ, Peterson J, Chowdhury NI, Gorup J, Camarata P, Lin J. Individualized surgical approach planning for petroclival tumors using a 3D printer. J Neurol Surg B Skull Base. 2016;77: 243-248. 15. Spottiswoode BS, van den Heever DJ, Chang Y, Engelhardt S, Du Plessis S, Nicolls F, et al. Preoperative three-dimensional model creation of magnetic resonance brain images as a tool to assist neurosurgical planning. Stereotact Funct Neurosurg. 2013;91:162-169. 16. Kondo K, Harada N, Masuda H, Sugo N, Terazono S, Okonogi S, et al. A neurosurgical simulation of skull base tumors using a 3D printed rapid prototyping model containing mesh structures. Acta Neurochir (Wien). 2016;158:1213-1219. 17. Zhang Y, Yang W, Zhang H, Liu M, Yin X, Zhang L, et al. Internal carotid artery and its relationship with structures in sellar region: anatomic study and clinical applications. World Neurosurg. 2018;110:e6-e19. 18. Griessenauer CJ, Raborn J, Mortazavi MM, Tubbs RS, Cohen-Gadol AA. Relationship between the pituitary stalk angle in prefixed, normal, and postfixed optic chiasmata: an anatomic study with microsurgical application. Acta Neurochir (Wien). 2014;156:147-151.
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19. Salma A, Alkandari A, Sammet S, Ammirati M. Lateral supraorbital approach vs pterional approach: an anatomic qualitative and quantitative evaluation. Neurosurgery. 2011;68(2 Suppl Operative):364-372 [discussion: 371-372]. 20. Theodosopoulos PV, Cebula H, Kurbanov A, Cabero AB, Osorio JA, Zimmer LA, et al. The medial extra-sellar corridor to the cavernous sinus: anatomic description and clinical correlation. World Neurosurg. 2016;96:417-422. 21. Tai BL, Wang AC, Joseph JR, Wang PI, Sullivan SE, McKean EL, et al. A physical simulator for endoscopic endonasal drilling techniques: technical note. J Neurosurg. 2016;124: 811-816. 22. Zada G, Kim AH, Governale LS, Laws ER. Midline filum of the sellar dura: a useful landmark during endoscopic transsphenoidal pituitary surgery. Neurosurgery. 2010;67:391-394. 23. Grahnke K, Garst JR, Martin B, Leonetti JP, Anderson DE. Prognostic indices for predicting facial nerve outcome following the resection of large acoustic neuromas. J Neurol Surg B Skull Base. 2017;78:454-460. 24. McBrayer KL, Wanna GB, Dawant BM, Balachandran R, Labadie RF, Noble JH. Resection planning for robotic acoustic neuroma surgery. J Med Imaging (Bellingham). 2017;4:025002. 25. Price SJ, Burnet NG, Donovan T, Green HA, Peña A, Antoun NM, et al. Diffusion tensor imaging of brain tumours at 3T: a potential tool for assessing white matter tract invasion? Clin Radiol. 2003;58:455-462. Conflict of interest statement: Funding for this project was received from the Science and Technology Project of Guangzhou (Grant No. 1565000177). Received 18 April 2018; accepted 26 July 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.236 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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Using Three-Dimensional Printing to Create Individualized Cranial Nerve Models for Skull Base Tumor Surgery Jiye Lin1,4, Zhenjun Zhou1, Jianwei Guan1, Yubo Zhu1, Yang Liu1, Zhilin Yang1, Bomiao Lin2, Yongyan Jiang2, Xianyue Quan2, Yiquan Ke1, Tao Xu3
OBJECTIVE: Using three-dimensional (3D) printing to create individualized patient models of the skull base, the optic chiasm and facial nerve can be previsualized to help identify and protect these structures during tumor removal surgery.
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METHODS: Preoperative imaging data for 2 cases of sellar tumor and 1 case of acoustic neuroma were obtained. Based on these data, the cranial nerves were visualized using 3D T1-weighted turbo field echo sequence and diffusion tensor imagingebased fiber tracking. Mimics software was used to create 3D reconstructions of the skull base regions surrounding the tumors, and 3D solid models were printed for use in simulation of the basic surgical steps.
CONCLUSIONS: 3D printed models of skull base tumors and nearby cranial nerves, by allowing for the surgical procedure to be simulated beforehand, facilitate preoperative planning and help prevent cranial nerve injury.
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RESULTS: The 3D printed personalized skull base tumor solid models contained information regarding the skull, brain tissue, blood vessels, cranial nerves, tumors, and other associated structures. The sphenoid sinus anatomy, saddle area, and cerebellopontine angle region could be visually displayed, and the spatial relationship between the tumor and the cranial nerves and important blood vessels was clearly defined. The models allowed for simulation of the operation, prediction of operative details, and verification of accuracy of cranial nerve reconstruction during the operation. Questionnaire assessment showed that neurosurgeons highly valued the accuracy and usefulness of these skull base tumor models.
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Key words 3D printing - Cranial nerve - Simulated surgery - Skull base surgery -
Abbreviations and Acronyms 3D: Three-dimensional CPA: Cerebellopontine angle CT: Computed tomography DTI: Diffusion tensor imaging ICA: Internal carotid artery MRI: Magnetic resonance imaging
INTRODUCTION
M
ost skull base tumors are benign, in contrast to tumors located in the brain hemispheres, and their surgical removal is often sufficient to ensure patient recovery. However, as the anatomic structure of the skull base is complex, tumor excision can often be very challenging,1 and this difficulty is further compounded by the high degree of variation among patients, which limits the usefulness of generalized anatomic models. It is therefore particularly important to develop highquality surgical training tools to improve the accuracy of preoperative diagnosis and surgical design and to reduce postoperative complications. With the advent of microneurosurgery, the focus of skull base surgery has shifted from maximizing the excision of tumor tissue to protecting the cranial nerves. Traditionally, total tumor resection and patient safety have mainly relied on the surgeon’s experience and skills, neurophysiologic monitoring, and neuronavigation, but such methods are inconvenient to use and involve significant surgical field exposure and lengthy preoperative preparation. Three-dimensional (3D) printing technology, through which scans of the patient’s brain can be recreated as a physical object, could make preoperative assessments more accurate and
From the 1National Key Clinical Specialty, Engineering Technology Research Center of Education Ministry of China, Guangdong Provincial Key Laboratory on Brain Function Repair and Regeneration, Department of Neurosurgery, and 2Department of Radiology, Zhujiang Hospital, Southern Medical University, Guangzhou; 3Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing; and 4Department of Neurosurgery, Shunde Hospital, Southern Medical University (The First People’s Hospital of Shunde Foshan), Foshan, China To whom correspondence should be addressed: Yiquan Ke, Ph.D.; Tao Xu, Ph.D. [E-mail: [email protected]; [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.236 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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surgical simulations more realistic by allowing them to be performed in the operating room rather than in virtual spaces. The application of 3D printing methods to clinical neurosurgery has been increasing; for instance, Ryan et al.2 recently used 3D printing to create a patient brain model containing 9 different features of intracranial aneurysms to simulate aneurysm clipping surgery with highly satisfactory results, as indicated by questionnaire evaluation. In another example, Thawani et al.3 printed a large 3D intracranial arteriovenous malformation model capable of accurately representing the hemodynamic characteristics of these structures. The subsequent survey showed that surgeons found the 3D printed model to be more helpful than the virtual models in diagnosing and treating complex vascular diseases. Finally, Park et al.4 described a procedure in which 3D printed titanium implants were used for the successful repair of skull defects in 21 cases. However, studies on skull base tumor models are still rare, and 3D printing research involving the cranial nerves associated with skull base tumors in particular has, to our knowledge, not been reported as of yet. The precise visualization of cranial nerves could have significant diagnostic and surgical consequences. If preoperative imaging is combined with 3D printing to show the location of the cranial nerves and the route through which they travel relative to the spatial location of the skull base tumor, it could allow the surgeon to better identify and protect these nerves during the operation and thus improve the safety and accuracy of surgical resection while shortening the length of the operation. There have been numerous reports more recently on the use of diffusion tensor imaging (DTI) to track cranial nerves, and the clinical utility of this approach has also been repeatedly verified.5-9 We also found that the combination of magnetic resonance imaging (MRI) 3D T1-weighted turbo field echo and 3D volumetric isotropic turbo spin echo acquisition sequences showed very encouraging results when used to image cranial nerves. The former in particular is a newly developed scan sequence based on classic gradient echoes and steady-state approaches. As the contrast between the water-containing nerve fiber and surrounding tissues is greatly increased when using this method, the 3D T1-weighted turbo field echo acquisition layer thickness can be reduced to 0.7e5 mm, thus making this approach more capable of spatially resolving neural structures than the spin echo sequence. The 3D volumetric isotropic turbo spin echo acquisition sequence is an MRI water imaging technique that has been demonstrated to provide a high T2-weighted cerebrospinal fluid signal in both the internal auditory canal and the cerebellopontine angle (CPA) while being able to show the relatively low-signal nerve fiber structure more prominently. We previously reported the usefulness of 3D printed models of brain and aneurysms for surgical simulations.10 In surgery for skull base tumors, our 3D-printed model of the sellar region and a CPA tumor, with the skull base rendered in transparent resin, permitted the direct visualization of structures that would otherwise have been invisible. In addition, our use of functional MRI to image the optic chiasm and facial nerve helped to effectively guide the surgeon in surgical resection and cranial nerve protection.
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MATERIALS AND METHODS Patient Population Two cases of sellar region tumor (a 59-year-old man with a tumor measuring 27 26 37 mm and a 40-year-old man with a tumor measuring 37 36 35) and 1 case of acoustic neuroma (a 34year-old man with a tumor measuring 26 33 24 mm) were selected for this study. 3D printing was used to create solid color cranial models that included all surgically related cranial nerves, which were used for preoperative surgical design and simulation of the tumor resection procedure. Image Acquisition Sellar Region Tumors. Contrast-enhanced computed tomography (CT) angiography scans (Brilliance CT; Philips Healthcare, Amsterdam, Netherlands) with a scanning layer thickness of 1 mm and a layer spacing of 0.5 mm were obtained together with 3.0T MRI (Ingenia R4.1; Philips Healthcare) conventional plain and enhanced scans. Magnetic resonance angiography and magnetic resonance venography scans were obtained using 3D time-of-flight spoiled gradient echo method and phase contrast method, respectively. The DTI sequence used the following settings: repetition time 7849 ms, echo time 80 ms, field of view 256 mm 256 mm, data matrix 128 128, thickness 1 mm, layer gap 0, 40 slices, and voxel size 1 1 1 mm. The number of excitations was set at 2, and the b value was 0.1000. The diffusion-sensitive gradient direction was 32. The 3D T1-weighted turbo field echo sequence parameters were repetition time 8.1 second, echo time ¼ 3.8 seconds, flip angle 7 , matrix 224 224, reconstruction matrix 256 256, field of view 256 mm 256 mm, scanning layer thickness 1 mm, layer gap 0, and number of acquisitions 1. Acoustic Neuroma. CT angiography, contrast-enhanced and plain MRI, magnetic resonance angiography, magnetic resonance venography, and DTI scans were performed as already described. 3D volumetric isotropic turbo spin echo acquisition sequence used the following settings: repetition time 2000 ms, echo time 457 ms, voxel size 1 1 1 mm, and matrix 256 256. 3D Reconstruction The imaging data of the aforementioned patients were imported into Mimics Research Version 17.0 (Materialise, Leuven, Belgium) in Digital Imaging and Communications in Medicine format. Gray scale was used to define distinct objects, following which the threshold segmentation function was used to separate different tissues from one another. Subsequent steps included separating the data with the same gray scale but belonging to different tissue, sketching out some unclear structures, and then reconstructing through the algorithm of the software. For large tumors, cranial nerves appeared unclear combined with DTI fiber tracking. Tumors, brain tissue, cranial nerves, and arteriovenous vessels were derived from MRI, and skull and arteries were derived from CT. MRI and CT data were combined based on magnetic resonance angiography and CT angiography. Finally, different colors were used to mark different tissue structures, saved in STL (stereolithography) format, and exported as 3D PDF files. The above steps were independently performed by 2 neurosurgeons (J.Y.L. and
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J.W.G.) who were familiar with the software, and the results were compared. 3D Printing Process In this study, the Connex3 Objet350 3D printer (Stratasys, Eden Prairie, Minnesota, USA), which uses PolyJet technology similar to ordinary inkjet printing, was used. Its triple jet technology allows it to mix almost all flexible, rigid, and transparent color materials by adjusting the proportions of the 3 basic materials (VeroCyan, VeroMajenta, and VeroYellow) incorporated into printed structures. The photosensitive polymeric material is sprayed layer by layer onto a build tray, and each layer of the photosensitive polymeric material is cured with ultraviolet light immediately after being ejected, creating a solid model. STL files were inserted into the printer, and elements such as material, color, transparency, and texture for various tissues or locations were set. A soft texture was selected for tumor regions, allowing the material to be easily cut and separated. With the transnasal sinus surgery model bisected along the midline, structures such as the sphenoid sinus space, arteries, and optic canal protuberance could be easily discerned. After the 3D solid model was completed, the SUP705 nontoxic gel-like photosensitive resin support material was removed using a water spray. Simulation of Surgery on 3D Printed Model We used 3-matic Version 9.0 software (Materialise) to adjust the virtual visualization skull base tumor model according to the
surgical approach to make the structure of the target region translucent, to visually understand complex anatomic relationships, and to simulate surgical procedures for tumor removal (Figure 1). Based on the experience of virtual surgical operations, the surgical plan for resecting the tumor was again simulated on the 3D printed solid models. Different surgical approaches were used to perform simulated surgery on skull base tumors to determine the best surgical route and range of skull opening windows. The critical anatomic landmarks, such as the skull, vessels, and cranial nerves, are gradually revealed during the resection process. Accurate intraoperative navigation and guidance of the surgical process were achieved.
Evaluation of Accuracy and Practicability A preliminary assessment questionnaire based on recent literature of a similar nature while taking into account the particularities of the characteristics and functions of the skull base tumor model used in this study was created.11-13 The questionnaire contained 11 items covering 3 aspects: the accuracy of the model, its practicability, and an overall evaluation. Each item was scored on a 5-point scale, with the highest score being 5. We invited 16 neurosurgeons with 3e11 years of experience (average 6.81 2.53 years), all of whom were familiar with skull base surgery, to score our 3D printed skull base tumor models using the questionnaire after they were given the opportunity to examine and manipulate the models.
Figure 1. (AeC) Simulated surgery on three-dimensional printed models.
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RESULTS
measure where drilling should be performed dimensions of the saddle (Figures 4 and 5).
Optic Chiasm and Relative Position of Sellar Region Tumor 3D printed solid models clearly showed the saddle area surgical space and directly reflected the huge tumor pushing the adjacent blood vessels and optic chiasm and the tumor destroying the skull base bone, which is consistent with the result of the virtual surgery. Via a classic frontotemporal approach, we first grinded the sphenoid ridge and made semicircular incisions into the meninges, revealing the sylvian fissure and frontal and temporal lobe. Then the superficial sylvian veins were separated from the wrapped arachnoid. Based on the relative position of the optic chiasm to the tumor, which could be classified into 1 of 3 broad categories—frontal inferior, frontal superior, and posterior superior type (Figure 2)—we selected a specific operative space (Figure 3). In the endoscopic transnasal approach, the distance from the midline was estimated using anatomic landmarks of the septum of the sphenoid sinus combined with the carotid artery protrusion and the optic nerve canal protrusion to
Figure 2. Relative locations of sellar tumors in reference to the optic chiasm. Sellar tumors fall into 1 of 3 broad categories: frontal inferior (A1 and A2),
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and
the
Cranial Nerves Surrounding Acoustic Neuromas We designed our surgical approach in this case based on the relative positions of the cranial nerves and the acoustic neuroma in the virtual model, with an emphasis on protecting the cranial nerves and vital blood vessels during simulated surgery. The asterion was first identified on the 3D printed model, and the anatomic details of the CPA region were considered from the perspective of a posterior suboccipital retrosigmoid approach. The path of the facial nerve, trigeminal nerve, glossopharyngeal nerve, and vagus nerve pushed by the tumor was gradually revealed. We then simulated grinding the inner auditory canal to remove the tumor (Figure 6). The positional relationship between facial nerves and acoustic neuromas is divided into 6 types: facial nerves are located in the anterior upper, anterior middle, anterior lower, superior, inferior, and posterior portions of the tumor (Figure 7).
frontal superior (B1 and B2), and posterior superior (A3 and B3).
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Figure 3. Simulation of a saddle area tumor resection on a three-dimensional printed model using pterional approach. (A) Bone centered on the pterion is removed to expose brain tissue. (B) The arachnoid membrane is cut at the front of the lateral septum to separate the lateral septal vein. (C) The frontal lobe and temporal lobe brain tissue are retracted, and (D) the sellar region
Clinical Evaluation Results Our models were awarded average scores of 3.94 0.60, 4.14 0.52, and 3.81 0.52 for their accuracy, practicability, and overall evaluation by the 16 neurosurgeons who were invited to complete a
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tumor and surrounding anatomic space are revealed. The internal carotid artery, optic nerve, and optic chiasm are identified. (E) A portion of the tumor is removed from the internal carotid artery and medial space of the optic nerve. (F and G) The tumors are resected in the preoptic gap. (H) The tumors are removed.
questionnaire after inspecting and handling the models (details of the survey items and the scores and comments from reviewers are provided in Table 1). These favorable scores indicate that the skull base tumor model has great potential as a neurosurgery training tool.
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Figure 4. Assemblable three-dimensional printed model. (A) To facilitate observation of the anatomic structure of the sphenoid sinus under the naked eye, the transsphenoidal surgical model is bisected along its midline and reassembled with an adhesive. (B) Key anatomic structures, such as the sphenoid sinus orifice
DISCUSSION In this article, we describe the application of 3D printing technology to create complex sellar region and CPA tumor solid models containing cranial nerves. Preoperatively, the position of the cranial nerves pushed or wrapped by the tumor can only be inferred. This knowledge would be very helpful for the choice of individual surgical routes and intraoperative microsurgery. A 3D printed solid model that simulates frontotemporal, endoscopic transnasal, and retrosigmoid approaches allows us to recognize and understand the most pertinent anatomic details from a completely new perspective. In particular, tracing the individual cranial nerves can help the surgeon to quickly identify and formulate strategies to protect these delicate structures. Previous 3D printed models focused only on the relationship between tumors and peripheral blood vessels, lacking the information required for cranial nerve reconstruction in microneurosurgery.14-16 Having a clear impression of the location of the sellar tumor, internal carotid artery (ICA), and optic chiasm is crucial for the
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in right half of the model, are identified. (C) The skull, being transparent, allows the internal carotid artery, optic nerve, and optic chiasm of the sphenoid sinus lateral wall to be seen. (D) The sphenoid sinus separation is clearly visible in left half of the model.
repair of lesions in the sellar and parasellar regions.17-20 Displacement of the optic chiasm by tumor changes the size of the anatomic gaps in the sellar region. Thus, precise knowledge of the position of the optic chiasm before surgery can be very helpful in choosing an appropriate surgical approach. Given that the distance between the anterior inferior chiasm and the saddle tubercle is relatively small, the raised structure of the latter can have an inordinate effect on the exposure of the suprasellar region in the case of a frontotemporal approach. As the 3D printed skull base tumor model shows the specific spatial arrangement of the tumor, optic nerve, and optic chiasm, we believe that it could play a very important role in the surgical planning once it is made widely available to surgeons. For instance, if the tumor is of a frontal inferior type, the anterior third ventricle could be thinned to allow the tumor to be more easily seen, or the laminae terminalis could be opened to expose the tumor more fully, which may be very useful for the removal of craniopharyngiomas or gliomas occurring in the third brain ventricle. If the tumor extends into the
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Figure 5. Simulation of sellar tumor resection on three-dimensional printed model using endoscopic transnasal approach. (A) Sphenoid sinus pneumatization and sequestration are shown on computed tomography angiography. (B) The sphenoid sinus orifice located in the crypts of the sphenoidal sinus is found. (C and D) The anterior sphenoid sinus is drilled. (E and F) The sphenoid
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septum is removed; the sinus cavity is washed; and anatomic landmarks including the optic nerveeinternal carotid artery internal angle, optic nerve canal protrusion, carotid artery protrusion, and slope crypt are identified. (G and H) The portion of saddle fundus that can be safely abraded away is measured; bone is removed from the center of the saddle.
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Figure 7. (A) Relative positional relationship between a tumor occurring in the cerebellopontine angle area and the facial nerve. (B) Tumor location may be classified as
side of the sella, the gap between the ICA and the optic nerve could be enlarged, and the tumor can be removed from the gap. The saddle area tumors in this study were adjacent to both ICAs and their branches, pushing the optic chiasm to a frontal superior position, with the tumor growing around the left optic nerve, extending partly into the left optic foramen. A conventional subfrontal approach in this instance would not allow adequate access to the mass via the foramen and would inevitably result in contact with the right optic nerve as well. Based on our 3D printed model, it was determined that the chiasm was in a frontal superior position, and so a left frontotemporal approach was chosen instead. In the operation, the tumors were excised mainly through the gap between the optic nerve and the ICA and the optic chiasm anterior gap, resulting in success in both cases. The structural features of the skull that are frequently used as landmarks during surgery may on certain occasions be occluded by the base of the skull. This, in combination with patient-topatient variations in anatomy, may make it difficult to achieve proper exposure of the cranial nerve. Although it is possible for an experienced surgeon to judge the position of the cranial nerves, such an approach introduces an element of error that could result
1 of 6 types: posterior (a), inferior (b), anterior lower (c), anterior middle (d), anterior upper (e), or superior (f).
in permanent visual field defects, blindness, and other catastrophic complications. In neuroendoscopic transnasal surgery, the carotid artery protrusion or optic nerve canal protrusion is sometimes not obvious, an issue that is circumvented via our use of transparent epoxy resins in our 3D models, which allows these structures to be seen. This significantly improves on the models designed by Tai et al.,21 in which the use of opaque materials in the construction of the skull caused key anatomic features, such as the ICA and the optic canal, to be hidden from view. By contrast, our model allows the spatial distance between the tumor and the ICA and the passage of the optic nerve through the skull to be easily seen. According to the spatial relationship between the sphenoid sinus, saddle fundus, and tumor, the scope of the saddle fundus can be abraded to avoid the coronal interval of the sphenoid sinus being mistaken for sphenoid posterior wall or the sagittal interval as the midline22 and occurrence of ICA or optic nerve injury. The suboccipital retrosigmoid approach is the most commonly used surgical approach for the treatment of CPA tumors. Because the affected region is adjacent to several important blood vessels, cranial nerves, and the brainstem, the
Figure 6. Simulation of acoustic neuroma resection on a 3D printed model. (A) Diffusion tensor imaging is used to visualize the facial nerve of acoustic neuroma. (B) In the skull, the asterion (star) and the bone hole of the vena emissaria occipitalis can be seen. (C) The transparent skull allows the safe distance between the transverse sinus and sigmoid sinus and the asterion (star) can be measured. (D) The brain tissue is retracted partially to reveal the tumor. Tumor tissue is separated gradually, and the adjacent cranial nerves and blood vessels are exposed. (E) The upper pole of the tumor is removed until the trigeminal nerve is visible. (F and G) Removal of the lower pole exposes the posterior cranial nerves. (H) The wall of the inner auditory canal is abraded, and (I) the tumor tissue in the inner ear is removed. (J) The tumor capsule is kept intact, as the facial nerve lies beneath the capsule.
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Table 1. Three-Dimensional Printed Skull Base Tumor Model Evaluation Survey Results from 16 Neurosurgeons Survey Items
Score
Other Comments
3.94 0.60
Accuracy* Skull
4.18 0.72
Brain tissue
3.75 0.55
Not soft enough and fragile
Artery
3.87 0.48
Lack of flowing blood Lack of flowing blood
Vein
3.81 0.63
Optic nerve or facial nerve
4.00 0.50
Tumor
4.06 0.55 4.14 0.52
Practicabilityy Identify bony landmarks (sphenoid sinus, pterion, cerebellopontine angle)
4.25 0.55
Identify optic chiasma position
4.12 0.59
Identify facial nerve position
4.06 0.42
Simulate tumor resection
4.12 0.48
Can see inside the structure through the transparent skull
No blood flow after excision The arachnoid adhesions around tumor cannot be simulated
3.81 0.52
Overall evaluationz
*Don’t know ¼ 1; Mostly inaccurate ¼ 2; Basically accurate, but lacks some details ¼ 3; More accurate ¼ 4; Highly accurate, no changes needed ¼ 5. yDon’t know ¼ 1; No help ¼ 2; Little help ¼ 3; Some help ¼ 4; Very helpful ¼ 5. zDon’t know ¼ 1; Need much improvement ¼ 2; Need some adjustment ¼ 3; Need a little improvement ¼ 4; Excellent, no changes needed ¼ 5.
operating space available is quite narrow. Accurately estimating the scope of excision in the internal auditory canal and the relative positions of the facial nerve and the tumor is thus very important.23,24 With the 3D printed CPA tumor model, we can now precisely determine the location of the asterion and the size of the window that needs to be created in the skull to obtain the optimal operating space via simulation. As most tumors in the region tend to be schwannomas, opening the internal auditory canal and resecting the residual tumor tissue is an important means to prevent disease recurrence. However, owing to large variations in individual anatomy and the close apposition of the bony semicircular canal and the vestibule with the posterior wall of the internal auditory canal, there is a significant risk that tumor removal may not be complete if the surgeon is too conservative or that the semicircular canal may be damaged if the ablation process is too excessive. In such an instance, a patient-specific 3D model with an auditory canal that can be removed from the bony structures that enclose it could be very helpful. 3D printed models could also be useful for locating where the cranial nerve passes close to the tumor within the CPA and help reduce intraoperative damage to the facial nerve, in addition to shortening the length of the operation. Surgeons with experience in acoustic neuroma surgery are well acquainted with the normal orientation of the facial nerve and would be able to roughly infer the position of the facial nerve based on neurophysiologic monitoring. However, it is challenging to determine accurately whether the facial nerve in each patient is located below or above the ventral aspect of the tumor, or if it passes by its lower or (in very rare cases) dorsal pole.6 By recreating the cranial nerves in the CPA in resin based on imaging data, this problem may be effectively nullified.
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Therefore, we propose that the 3D printed skull base tumor model be used as a “living textbook” for skull base anatomy that can be used by junior physicians to learn and design neurosurgical strategies or as practical training tools to be used in simulated surgeries. Our preliminary questionnaire evaluation indicated that the 3D print model is capable of providing enough detail regarding the 3D anatomy of structures surrounding the tumor. The blood vessels and cranial nerves were found to be particularly useful signposts to gauge the progress and scope of surgery, and the models were judged to be better than the traditional twodimensional tomography in this regard. It was also mentioned that simulated surgeries conducted with the models may be helpful for procedures involving areas close to the cranial nerves or to critical vasculature. Finally, the models may also facilitate the prediction of complications that may occur during procedures and allow for contingency plans to be put in place ahead of time. This is in agreement with previous studies, which have also concluded that high-quality 3D printing models could have a positive impact on the skills of surgeons by providing them with more realistic simulations.11-13 Limitations and Future Directions In practice, we found that the shape of the cranial nerves in the 3D printed models were not always completely consistent with the actual shape seen during the operation and that the models were currently mainly useful only for determining the traveling and position of the fiber bundles and the degree to which they are displaced by the tumor. This may be due to the fact that extended compression of the nerve fibers by the tumor leads to changes in the density, parallelism, and integrity of the myelin sheath, which alters how water diffuses through the fiber. As DTI is based on the
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ORIGINAL ARTICLE JIYE LIN ET AL.
3D PRINTED INDIVIDUALIZED CRANIAL NERVE MODELS
fractional anisotropy of water molecules,25 these changes could interfere with achieving an ideal spatial resolution and signal-tonoise ratio for nerves that are thus affected. In addition, the release of cerebrospinal fluid during surgery causes brain tissue to retract and shift within the cranium. As our model is composed of materials that are comparatively more rigid, it is difficult to simulate this dynamic process. Therefore, future designs will focus on solving these problems by increasing blood circulation and altering the model so that intracranial pressure changes can be replicated. In addition, as MRI currently can capture only major vascular structures, there will still be a need for intraoperative monitoring of bleeding from small blood vessels <1 mm in diameter that are invisible to this imaging technique to minimize the incidence of complications. Finally, this study examined a small patient population. To more thoroughly study the value of 3D printing in skull base tumor surgery, randomized controlled
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