Sonolucent Cranial Implants: Cadaveric Study and Clinical Findings Supporting Diagnostic and Therapeutic Transcranioplasty Ultrasound

Micah Belzberg, Netanel Ben Shalom, Edward Yuhanna, Amir Manbachi, Aylin Tekes, Judy Huang, Henry Brem, Chad R Gordon, Micah Belzberg, Netanel Ben Shalom, Edward Yuhanna, Amir Manbachi, Aylin Tekes, Judy Huang, Henry Brem, Chad R Gordon

Abstract

Background: Previously, sonographic evaluation of the intracranial contents was limited to intraoperative use following bone flap removal, with placement of the probe directly on the cortical surface or through a transsulcal tubular retractor. Cranioplasty with sonolucent implants may represent a postoperative window into the brain by allowing ultrasound to serve as a novel bedside imaging modality. The potential sonolucency of various commonly used cranial implant types was examined in this study.

Methods: A 3-phase study was comprised of cadaveric evaluation of transcranioplasty ultrasound (TCU) with cranioplasty implants of varying materials, intraoperative TCU during right-sided cranioplasty with clear implant made of poly-methyl-methacrylate (PMMA), and bedside TCU on postoperative day 5 after cranioplasty.

Results: The TCU through clear PMMA, polyether-ether-ketone, and opaque PMMA cranial implants revealed implant sonoluceny, in contrast to autologous bone and porous-polyethylene. Intraoperative ultrasound via the clear PMMA implant in a single patient revealed recognizable ventricular anatomy. Furthermore, postoperative bedside ultrasound in the same patient revealed comparable ventricular anatomy and a small epidural fluid collection corresponding to that visualized on an axial computed tomography scan.

Conclusion: Sonolucent cranial implants, such as those made of clear PMMA, hold great promise for enhanced diagnostic and therapeutic applications previously limited by cranial bone. Furthermore, as functional cranial implants are manufactured with implantable devices housed within clear PMMA, the possibility of utilizing ultrasound for real-time surveillance of intracranial pathology becomes much more feasible.

Conflict of interest statement

CG is a consultant for Stryker and Longeviti Neuro Solutions. JH and CG are stockholders of Longeviti Neuro Solutions. The remaining authors report no conflicts of interest.

Figures

FIGURE 1
FIGURE 1
Design of patient-specific custom cranial implant made of clear poly-methyl-methacrylate biomaterial. (A) Preoperative 3-dimensional (3D) reconstruction of skull defect from computed tomography (CT). (B) CT of preoperative skull defect in green with patient-specific custom design in red. (C) 3D rendering of customized cranial implant.
FIGURE 2
FIGURE 2
Photograph of clear poly-methyl-methacrylate (PMMA) implant and craniectomy defect. (A) Clear PMMA implant during reshaping process. (B) Clear PMMA implant placed within the skull defect, up against the dura. Of note, the scalp has not yet been replaced over the implant. Sonolucency was assessed using a 2.4-MHz transducer with a 3-MHz center frequency. Note that the dura can be seen directly up against the clear cranial implant.
FIGURE 3
FIGURE 3
Intraoperative photograph of skull defect, clear poly-methyl-methacrylate implant, and ultrasound probe within sterile sleeve.
FIGURE 4
FIGURE 4
Coronal ultrasound imaging of cadaver brain imaged through “scalp only” control, bone, PEEK implant, porous-polyethylene implant, opaque poly-methyl-methacrylate (PMMA) implant, and clear PMMA implant. BS, brainstem; LMF, left middle fossa; RMF, right middle fossa.
FIGURE 5
FIGURE 5
Intraoperative transcranioplasty ultrasound (TCU) through clear poly-methyl-methacrylate (PMMA) implant. (A) Ultrasound through scalp and clear PMMA implant showing right choroid plexus (CP) with probe placed on scalp. (B) Postoperative axial computed tomography (CT) showing clear PMMA implant (CI) and pneumocephalus (P). (C) Postoperative axial CT showing clear PMMA implant (CI) and extradural fluid collection (FC).
FIGURE 6
FIGURE 6
Results from postoperative day 5 bedside transcranioplasty ultrasound (TCU) through clear poly-methyl-methacrylate (PMMA) implant. (A) Ultrasound showing clear PMMA implant (CI) with small fluid collection (FC), brain parenchyma (P), and dura (D). (B) Ultrasound showing approximate coronal section with shadow artifacts (S) from titanium clips securing implant. (C) Postop day 5 axial computed tomography (CT) showing clear PMMA implant (CI) and absorption of pneumocephalus. (D) Postoperative axial CT with clear PMMA implant. Dashed region of (D) enlarged in (E). (E) Enlarged region of (D) postoperative axial CT again showing clear PMMA implant (CI) and small extradural fluid collection (FC).
FIGURE 7
FIGURE 7
Comparison of coronal sections generated with transcranioplasty ultrasound (TCU) through clear poly-methyl-methacrylate (PMMA) implant and computed tomography (CT). (A) Approximate coronal section generated with postoperative day 5 bedside TCU through clear PMMA. Image has been rotated to match standard radiographic image convention. (B) Postoperative day seven CT coronal section at approximate position as ultrasound generated image. Dashed regions of (A) and (B) enlarged and presented as (C) and (D), respectively. (C) Enlarged center portion of (A) postoperative day 5 bedside ultrasound showing right ventricle (RV), septum pellucidum (SP), and left ventricle (LV). (D) Enlarged center portion of (B) postoperative CT (day 7) showing right ventricle (RV), septum pellucidum (SP), and left ventricle (LV).

References

    1. Piazza M, Grady MS. Cranioplasty. Neurosurg Clin N Am 2017; 28:257–265.
    1. Feroze AH, Walmsley GG, Choudhri O, et al. Evolution of cranioplasty techniques in neurosurgery: historical review, pediatric considerations, and current trends. J Neurosurg 2015; 123:1098–1107.
    1. Reddy S, Khalifian S, Flores JM, et al. Clinical outcomes in cranioplasty: risk factors and choice of reconstructive material. Plast Reconstr Surg 2014; 133:864–873.
    1. Servadei F, Iaccarino C. The therapeutic cranioplasty still needs an ideal material and surgical timing. World Neurosurg 2015; 83:133–135.
    1. Gilardino MS, Karunanayake M, Al-Humsi T, et al. A comparison and cost analysis of cranioplasty techniques: autologous bone versus custom computer-generated implants. J Craniofac Surg 2015; 26:113–117.
    1. Artico M, Ferrante L, Pastore FS, et al. Bone autografting of the calvaria and craniofacial skeleton: historical background, surgical results in a series of 15 patients, and review of the literature. Surg Neurol 2003; 60:71–79.
    1. Pryor LS, Gage E, Langevin C-J, et al. Review of bone substitutes. Craniomaxillofac Trauma Reconstr 2009; 2:151–160.
    1. Malcolm JG, Mahmooth Z, Rindler RS, et al. Autologous cranioplasty is associated with increased reoperation rate: a systematic review and meta-analysis. World Neurosurg 2018; 116:60–68.
    1. van de Vijfeijken SECM, Munker TJAG, Spijker R, et al. Autologous bone is inferior to alloplastic cranioplasties: safety of autograft and allograft materials for cranioplasties, a systematic review. World Neurosurg 2018; 117:443–452.
    1. Wolff A, Santiago GF, Belzberg M, et al. Adult cranioplasty reconstruction with customized cranial implants: preferred technique, timing, and biomaterials. J Craniofac Surg 2018; 29:887–894.
    1. Zhong S, Huang GJ, Susarla SM, et al. Quantitative analysis of dual-purpose, patient-specific craniofacial implants for correction of temporal deformity. Neurosurgery 2015; 11 Suppl 2:220–229.
    1. Gordon C, Bryndza JR, Bisic T. Patient-specific craniofacial implants. United States Patent #9, 216, 084 B2. Issue December 22, 2015.
    1. Hersh DS, Kim AJ, Winkles JA, et al. Emerging applications of therapeutic ultrasound in neuro-oncology: moving beyond tumor ablation. Neurosurgery 2016; 79:643–654.
    1. Christian E, Yu C, Apuzzo MLJ. Focused ultrasound: relevant history and prospects for the addition of mechanical energy to the neurosurgical armamentarium. World Neurosurg 2014; 82:354–365.
    1. Quadri SA, Waqas M, Khan I, et al. High-intensity focused ultrasound: past, present, and future in neurosurgery. Neurosurg Focus 2018; 44:E16.
    1. Weintraub D, Elias WJ. The emerging role of transcranial magnetic resonance imaging-guided focused ultrasound in functional neurosurgery. Mov Disord 2017; 32:20–27.
    1. Carpentier A, Canney M, Vignot A, et al. Clinical trial of blood-brain barrier disruption by pulsed ultrasound. Sci Transl Med 2016; 8:343re2.
    1. Gutierrez MI, Penilla EH, Leija L, et al. Novel cranial implants of yttria-stabilized zirconia as acoustic windows for ultrasonic brain therapy. Adv Healthc Mater 2017; 6:
    1. Monteith S, Sheehan J, Medel R, et al. Potential intracranial applications of magnetic resonance-guided focused ultrasound surgery. J Neurosurg 2013; 118:215–221.
    1. Vignon F, Shi WT, Yin X, et al. The stripe artifact in transcranial ultrasound imaging. J Ultrasound Med 2010; 29:1779–1786.
    1. Pinton G, Aubry J-F, Bossy E, et al. Attenuation, scattering, and absorption of ultrasound in the skull bone. Med Phys 2012; 39:299–307.
    1. Orman G, Benson JE, Kweldam CF, et al. Neonatal head ultrasonography today: a powerful imaging tool!. J Neuroimaging 2015; 25:31–55.
    1. van Wezel-Meijler G, Steggerda SJ, Leijser LM. Cranial ultrasonography in neonates: role and limitations. Semin Perinatol 2010; 34:28–38.
    1. Salas J, Tekes A, Hwang M, et al. Head ultrasound in neonatal hypoxic-ischemic injury and its mimickers for clinicians: a review of the patterns of injury and the evolution of findings over time. Neonatology 2018; 114:185–197.
    1. Berli JU, Thomaier L, Zhong S, et al. Immediate single-stage cranioplasty following calvarial resection for benign and malignant skull neoplasms using customized craniofacial implants. J Craniofac Surg 2015; 26:1456–1462.
    1. Gordon CR, Santiago GF, Huang J, et al. First in-human experience with complete integration of neuromodulation device within a customized cranial implant. Oper Neurosurg (Hagerstown) 2018; 15:39–45.
    1. Gordon CR, Fisher M, Liauw J, et al. Multidisciplinary approach for improved outcomes in secondary cranial reconstruction: introducing the pericranial-onlay cranioplasty technique. Neurosurgery 2014; 10:179–180.
    1. Fry FJ, Barger JE. Acoustical properties of the human skull. J Acoust Soc Am 1978; 63:1576–1590.
    1. Aubry JF, Tanter M. MR-guided transcranial focused ultrasound. In: Escoffre JM, Bouakaz A (eds) Therapeutic Ultrasound. Advances in Experimental Medicine and Biology, Vol 880. Springer, Cham, Switzerland, 2016.
    1. Janus JR, Peck BW, Tombers NM, et al. Complications after oncologic scalp reconstruction: a 139-patient series and treatment algorithm. Laryngoscope 2015; 125:582–588.
    1. Broughton E, Pobereskin L, Whitfield PC. Seven years of cranioplasty in a regional neurosurgical centre. Br J Neurosurg 2014; 28:34–39.
    1. Wachter D, Reineke K, Behm T, et al. Cranioplasty after decompressive hemicraniectomy: underestimated surgery-associated complications? Clin Neurol Neurosurg 2013; 115:1293–1297.
    1. Mursch K, Behnke-Mursch J. Polyether ether ketone cranioplasties are permeable to diagnostic ultrasound. World Neurosurg 2018; 117:142–143.
    1. Blankenberg FG, Loh NN, Bracci P, et al. Sonography, CT, and MR imaging: a prospective comparison of neonates with suspected intracranial ischemia and hemorrhage. Am J Neuroradiol 2000; 21:213–218.
    1. Bano S, Chaudhary V, Garga UC. Neonatal hypoxic-ischemic encephalopathy: a radiological review. J Pediatr Neurosci 2017; 12:1–6.
    1. Zygourakis CC, Winkler E, Pitts L, et al. Clinical utility and cost analysis of routine postoperative head CT in elective aneurysm clippings. J Neurosurg 2017; 126:558–563.
    1. Carlson JE, van Deventer J, Scolan A, Carlander C. “Frequency and temperature dependence of acoustic properties of polymers used in pulse-echo systems,” IEEE Symposium on Ultrasonics, 2003, Honolulu, HI, Vol 1, 2003, 885–888.
    1. Gordon CR. Low-profile Intercranial Device (LID). US Patent Application Publication #US2018/0338835 A1. Published November 29, 2018.

Source: PubMed

赞助者和合作者

医疗条件

药物干预

3
订阅