검색
검색 팝업 닫기

Ex) Article Title, Author, Keywords

Article

J Vet Clin 2022; 39(5): 246-252

https://doi.org/10.17555/jvc.2022.39.5.246

Published online October 31, 2022

Cranioplasty for Multilobular Osteochondrosarcoma Using 3-Dimensional Printing Technology in Dogs: A Report of Two Cases with a Long-Term Follow-Up

Seong-Hyeon Heo1 , Hae-Beom Lee1 , Jae-Min Jeong1 , Young-Jin Jeon1 , Dae-Hyun Kim1 , Seong-Mok Jeong1 , Yoon-Ho Roh1,2

1Department of Veterinary Surgery, College of Veterinary Medicine, Chungnam National University, Daejeon 34134, Korea
2Division of Small Animal Surgery, Department of Clinical Veterinary Medicine, Vetsuisse-Faculty, University of Bern, Bern 3012, Switzerland

Correspondence to:*202020036@g.cnu.ac.kr
Seong-Hyeon Heo and Hae-Beom Lee contributed equally to this work.

Received: April 11, 2022; Revised: August 12, 2022; Accepted: September 20, 2022

Copyright © The Korean Society of Veterinary Clinics.

Multilobular osteochondrosarcoma (MLO) reportedly has a good prognosis after complete resection. This study reports the successful treatment of MLO in two dogs using 3-dimensional (3D) printing technology. A nine-yearold castrated male Maltese (Case 1) and a five-year-old castrated male poodle (Case 2) both presented with a mass in the skull. Diagnostic imaging revealed a cranial mass arising from the cranio-orbital and parieto-occipital bones. The masses were resected using 3D-printed osteotomy guides, and the resulting defects were reconstructed using 3D-printed patient-specific implants. Histopathological results confirmed the resection of MLOs with clean margins. Patients routinely recover from surgery without complications. To date, the two patients remain alive without clinical signs of tumor recurrence at 20 and 12 months postoperatively, respectively. In the management of MLO in dogs, 3D printing technology can allow accurate tumor resection, reduced surgical time, and successful reconstruction of large defects.

Keywords: multilobular osteochondrosarcoma, 3D printing, osteotomy guide, cranioplasty, canine.

Multilobular osteochondrosarcomas (MLOs) are a rare type of malignant bone tumor that most often occur in the flat bones of a canine skull. The majority of dogs with MLOs are middle-aged to older, medium- to large-breed dogs with a median age at presentation of eight years and median weight of 29 kg (8,16). These tumors are typically slow-growing, locally invasive, and malignant, with a metastasis rate of up to 58% (8,29). The most common clinical presentation is a firm and fixed mass of the skull. However, neurological signs can appear depending on the size and location of the tumor (6).

Although chemotherapy and radiotherapy may have benefits of local control of tumors or palliation of residual tumors (13,30,31), surgery remains the treatment of choice. Clean surgical margins are strongly associated with favorable prognosis (5,7,8,16).

In a retrospective study of 39 dogs with MLO in the skull, the median disease-free times following complete and incomplete resection were 1332 days and 320 days, respectively. The metastatic rates for complete and incomplete resection are 25% and 75%, respectively (8). In that study, more than half of the diseased dogs died of local recurrence or metastasis, with a median time from the onset of recurrence or metastasis to death of 239 days. Therefore, aggressive resection of the tumor with wide margins is recommended. Wide resection of the cranium can create large defects, resulting in serious cosmetic problems, and the underlying brain becomes vulnerable to trauma or infection. Therefore, a cranioplasty should be considered (27).

Three-dimensional (3D) printing is an additive manufacturing method that converts computer-generated 3D images into physical models (22). This technology has been used extensively in surgical procedures, including surgeon-patient communication, preplanning, and custom implant fabrication (12,22,26). Recently, 3D-printed osteotomy guides have been used for malignant bone tumor surgeries, resulting in precise resection of the tumor and implantation, reduced blood loss, and reduced operation time (18,32,34). 3D-printed implants have been used to reconstruct bone defects in complex structures such as the maxilla and cranium (17,28).

To date, rare cases of cranioplasty using 3D-printed implants in dogs with MLO have been reported (5,11). This case report describes the application of 3D-printed osteotomy guides and patient-specific implants for cranioplasty in two dogs with MLOs and their favorable long-term outcomes.

Case 1

A nine-year-old, 6.7 kg castrated male Maltese presented with a firm mass in the frontal calvarium. The mass progressively enlarged over the last three months and adhered to the right fronto-orbital region on palpation. Ventrolateral deviation and hyperemia of the globe of the right eye were observed (Fig. 1A). Physical and neurological examination results were unremarkable. Radiography revealed a lobulated mass arising from the right frontal bone and extending cranially to the right orbit. Computed tomography (CT, AlexionTM, Canon Medical Systems Corporation, Otawara, Japan) confirmed a 3.3 × 2.7 × 3.1 cm mass with heterogeneous soft tissue opacity invading the right frontal sinus. On magnetic resonance imaging (MRI, 1.5 Tesla unit, Magnetom Essenza, Siemens, Germany), the mass was hypointense on T2-weighted (T2W) and isointense on T1-weighted (T1W) images, and did not invade the brain (Fig. 1B, C). The CT images of the patient were exported in Digital Imaging and Communication in Medicine format and reconstructed using a computer software (3DS Max, Autodesk, CA, USA). With the reconstructed images, the osteotomy guide was designed to provide a template for tumor resection with 5 mm lateral margins and a groove fitting to the temporal line of the right frontal bone. A titanium plate capable of reconstructing the defect was designed based on the opposite side of the skull. Anatomical bio-models of the skull and tumor were designed for preoperative planning and intraoperative inspection (Fig. 2A). The 3D osteotomy guide and bio-models were printed using a 3D printer (Finbot-Z420, TPC Mecatronics, Seoul, Korea) with a polylactic acid filament (PLA filament, Cubicon, Seongnam, Korea), and the titanium plate was printed using a 3D printer (SLM 125, SLM Solution, Germany) (Fig. 2B).

Figure 1.Preoperative and postoperative gross images and magnetic resonance imaging (MRI) of Case 1. A preoperative macroscopic image (A) and T2-weighted MRI images of transverse view (B) and sagittal view (C). A postoperative macroscopic image at two weeks postoperatively (D). Contrast-enhanced T1W MRI images of transverse view (E) and sagittal view (F) at 12 months postoperatively.
Figure 2.Preoperative planning, rehearsal surgery, and postoperative radiographic images of Case 1. Three-dimensional (3D)-reconstructed preoperative planning (A), 3D-printed biomodels with osteotomy guide and titanium plate (B), and radiographic image (C) of Case 1 at two weeks postoperatively.

During surgery, the patient was pre-medicated with midazolam (0.2 mg/kg, IV; Midazolam inj., Bukwang Pharm, Seoul, Korea). Anesthesia was induced with propofol (4 mg/kg, IV; Anepol inj., Hana Pharm, Seoul, Korea) and maintained with isoflurane (Ifran®, Hana Pharm, Seoul, Korea). A constant rate infusion (CRI) of remifentanil (5-40 µg/kg/h; Remiva inj., Hana Pharm, Seoul, Korea) was administered for analgesia. Cefazolin (22 mg/kg, IV; cefazolin inj., Chong Kun Dang, Seoul, Korea) was administered prior to skin incision and repeated every 90 min. Before tumor resection, osteotomy of the right zygomatic arch and transection of the orbital ligament were performed to allow ventral reflection of the eye globe and access to the ventral orbit. An elliptical skin incision was made along the lateral margins of the tumor. When the tumor was exposed, a 3D-printed osteotomy guide was placed around the tumor, and a surgical marking pen was used to mark the resection margin. A 2 mm pneumatic burr was used to perform craniectomy along the resection margin, extending laterally from the dorsal midline of the frontal bone to the right zygomatic process. After retracting the excised tumor, the underlying dura mater was torn, while the brain tissue was not damaged. Durectomy was performed up to the lateral margin of the tumor. Additionally, mucosa removal in the exposed frontal sinus was performed using a 2 mm pneumatic burr, and several pieces of gelatin sponges (Spongostan standard, Ethicon, USA) were inserted into the sinus for frontal sinus obliteration (19). After hemostasis of the minor bleeding, the excised dura mater was reconstructed using a synthetic dura mater substitute, ReDura (Medprin Biotech, La Mirada, CA, USA), and a 3D-printed titanium plate was placed over the defect and secured with six screws (1.5 mm self-drilling titanium).

The patient routinely recovered postoperatively. Radiographs revealed skull defect coverage and alignment of the titanium plate (Fig. 2C). Postoperatively, the CRI of remifentanil (6 µg/kg/h) was administered for three days, and cefotaxime (20 mg/kg, IV; Cefotaxime inj., Chong Kun Dang, Seoul, Korea) was administered for two weeks. Histopathological examination of the excised tumor confirmed the diagnosis of grade 1 of 3 MLO with clean lateral margins of >6 mm (Fig. 3A). A well-circumscribed, predominantly expansile, sparsely cellular mass within the subcutaneous connective tissues that partially infiltrated the underlying bone of the sinus was observed. The patient was discharged two weeks postoperatively without any complications (Fig. 1D).

Figure 3.Histopathologic microscopic examination of Cases 1 and 2. There are spindle to stellate cells forming anastomosing streams and bundles in a fibrous stroma with regularly interspersed foci of chondrus and osseous metaplasia (A, hematoxylin and eosin [H&E]; scale bars: 500 μm). Osteochondrosarcoma proliferates while maintaining the form of lobes (B, H&E; ×12.5).

At two months after discharge, the patient presented with epistaxis and purulent discharge from the right nasal orifice. An MRI scan revealed heterogeneous lesions with T2W hyperintensity and T1W isointensitiy within the nasal cavities and frontal sinuses. No tumor recurrence was detected (Fig. 1E, F). A complete blood count revealed mild neutrophilia (14,110 cells/µL, reference range: 3,900-8,000). Elevated levels of alkaline phosphatase (488 U/L, reference range: 15-127), alanine aminotransferase (175 U/L, reference range: 19-70), and aspartate aminotransferase (49 U/L, reference range: 15-43) were observed, which was considered due to recently administered prednisolone (0.5 mg/kg, PO, q12h) for dermatitis pruritis for two weeks. Bacterial culture of nasal swabs confirmed the presence of Staphylococcus aureus. The patient was diagnosed with suppurative rhinosinusitis and was prescribed doxycycline (5 mg/kg, PO, q12h; doxycycline Tab., Youngpoong Pharm, Seoul, Korea) for two weeks.

At ten months postoperatively, generalized tonic-clonic seizure was observed. The owner declined further examination, and phenobarbital administration (2.5 mg/kg PO, q12h; Phenobarbital Tab., Hana Pharm, Seoul, Korea) was started. The patient was doing well without seizures at 20 months postoperatively.

Case 2

A five-year-old, 10.7 kg castrated male poodle was brought for evaluation of a mass located in the parieto-occipital bone. Preoperative examinations, including CT, were performed (Fig. 4A). The 3D-printed osteotomy guide, titanium plate, and bio-models were designed as described for Case 1 (Fig. 4B).

Figure 4.Preoperative (A, B) and intraoperative (C, D) views of Case 2. Three-dimensional (3D) reconstructed image of preoperative computed tomography scan (A). A 3D-printed bio-model and skull of the patient (B). A defect after craniectomy (C). A 3D-printed titanium plate fixed over defect (D).

The patient was anesthetized using the same protocol as in Case 1. The temporal muscle was dissected after an elliptical incision was made on the skin. The osteotomy guide was positioned following the complete dissection of the muscle tissues, and the resection margin was marked around the tumor. Parieto-occipital craniectomy was performed using a 2 mm pneumatic burr, and the underlying dura mater was bluntly dissected with a spatula. The tumor was carefully lifted off the dura mater without damaging the dorsal sagittal sinus within the dura mater (Fig. 4C). After several lavages with sterile saline, the defect in the skull was covered with synthetic dura mater anchored to the adjacent edge of the temporal muscle. The 3D-printed titanium plate was secured over the defect with four 1.5 mm self-drilling titanium screws (Fig. 4D).

Histopathological evaluation of the excised tumor confirmed an MLO with complete lateral margins. The proliferated tumor cells had one or more distinct nucleophiles and malignant findings, such as anisokaryosis of the nucleus, and mitotic counts were rarely observed. Several osteoclasts were also observed (Fig. 3B). The patient was discharged at seven days postoperatively. No tumor complications or recurrences until the final follow-up at 12 months postoperatively were noted.

This report describes the application of 3D printing technology for cranioplasty in two dogs with MLOs. The patients had good long-term postoperative clinical results without serious complications.

For MLO, the overall recurrence rate after surgery is 47%-58% and is dependent on the completeness of surgical resection. The median disease-free interval for completely resected MLO is significantly better than that reported for incompletely resected tumors (8,16,29). However, owing to the complexity of the canine skull, obtaining an adequate surgical margin is often difficult, and early recurrence may occur (6,9,27). Recently, 3D-printed osteotomy guides for bone sarcoma resection have been reported to improve the accuracy of resection with adequate margin (1,3,18). This technique facilitates the recognition of real tumor margins and allows surgeons to overcome technical errors in treating complex bone structures. It has also been demonstrated to eliminate the need for implant trimming for cranioplasty, allowing the operator to determine the exact edge of skull tumors (24,36). Hence, the skull can be reconstructed with a 3D-printed titanium plate immediately, and the operation time can be reduced (15).

Various materials for cranioplasty have been described in dogs, including cortical allografts, polymethyl methacrylate (PMMA), and titanium mesh (7,20,23,27). Cortical allograft bone provides mechanical support; however, it requires aseptic harvesting and preserving techniques (23). Moreover, serious postoperative complications have been reported, including immunogenic reactivity, infection, and resorption of the implant (20). PMMA is an inexpensive and readily available material. However, it requires an intraoperative mold, which is associated with thermal tissue necrosis, infection, and prolonged surgical time (4,21). Titanium mesh has some benefits, including rigidity, availability, and resistance to infection, although intraoperative contouring is required (15,27). Custom-made titanium plates for cranioplasty have been described in human reports (28,33). A retrospective study comparing two different titanium cranioplasty methods has revealed that custom-made titanium plates had better aesthetic results, complete coverage of defects, shorter surgical times, and easier operation for the surgeon than titanium mesh (25). In our patients, the 3D-printed titanium plates were successfully secured without massive hemorrhage or prolonged procedures, resulting in good clinical outcomes.

The dorsal sagittal and transverse sinuses are the most significant vessels that may be encountered during craniectomy and lie within the dura mater (16). Damage to these structures can lead to life-threatening hemorrhage or fatal brain swelling (9). In case 1, the location of the tumor was far from the sinus; therefore, only slight bleeding occurred despite dural rupture. By contrast, the preoperative MRI scan of case 2 confirmed that the tumor was located above the dorsal sagittal sinus. This allowed the surgeon to carefully dissect the tumor from the dura mater, which may lead to favorable outcomes. Resection of the involved dura mater is considered an important component for achieving maximal resection in primary osteosarcoma of the frontal bone in humans. When dural involvement is suspected based on the intraoperative gross appearance or preoperative MRI scans, dural resection is recommended if it can be achieved with a low risk of significant morbidity (10,35). Hayes et al. have reported MLO recurrence in a dog at seven months postoperatively. They suggested that the dura mater should be considered a deep margin in cases of MLO in dogs (11). In Case 1, an intraoperative dural tear was suspected due to adhesions, which could be evidence of dural invasion of the tumor. Therefore, dural resection was performed.

Single-stage cranioplasty with osteotomy guidance is generally performed only for benign tumors because of the risk of incomplete margins. The average 3-week delay in implant manufacturing is another concern in the management of malignant tumors (14,24). However, Berli et al. described single-stage cranioplasty for malignant tumors with little morbidity (2). In veterinary medicine, single-step cranioplasty is often necessary because of the high cost of a second surgery or the owner’s preference (15). Therefore, this technique can be a reasonable option for treating malignant skull tumors, as long as the delay in implant manufacturing is minimized (2).

In our patient, craniectomy and cranioplasty for MLO were successfully performed using 3D printing technology. Based on the clinical outcomes, this technique may be feasible with limited long-term postoperative complications. Further investigation is required to confirm our preliminary findings.

Written informed consents have been obtained from all owners that donated their animals for the study.

This work was supported by the Research Scholarship of the Chungnam National University.

  1. Bellanova L, Paul L, Docquier PL. Surgical guides (patient-specific instruments) for pediatric tibial bone sarcoma resection and allograft reconstruction. Sarcoma 2013; 2013: 787653.
    Pubmed KoreaMed CrossRef
  2. Berli JU, Thomaier L, Zhong S, Huang J, Quinones A, Lim M, 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.
    Pubmed CrossRef
  3. Blakeney WG, Day R, Cusick L, Smith RL. Custom osteotomy guides for resection of a pelvic chondrosarcoma. Acta Orthop 2014; 85: 438-441.
    Pubmed KoreaMed CrossRef
  4. Bryant KJ, Steinberg H, McAnulty JF. Cranioplasty by means of molded polymethylmethacrylate prosthetic reconstruction after radical excision of neoplasms of the skull in two dogs. J Am Vet Med Assoc 2003; 223: 67-72, 59.
    Pubmed CrossRef
  5. Choi S, Honnami M, Liu IL, Yamamoto K, Ohba S, Echigo R, et al. Cranioplasty with custom-made artificial bone after resection of multilobular bone tumor in a dog. J Vet Clin 2014; 31: 46-50.
    CrossRef
  6. Cook S, Civello A, Lam R, Fenn J, Neilson D, Priestnall S, et al. Rapid postoperative recurrence of a cranial multilobular tumor of bone in a young dog. Clin Case Rep 2017; 5: 1995-1999.
    Pubmed KoreaMed CrossRef
  7. de Casterlé AD, Van Goethem B, Kitshoff A, Bhatti S, Gielen I, Bosmans T. Titanium mesh reconstruction of a dog’s cranium after multilobular osteochondrosarcoma resection. Vlaams Diergeneeskd Tijdsch 2017; 86: 232-240.
    CrossRef
  8. Dernell WS, Straw RC, Cooper MF, Powers BE, LaRue SM, Withrow SJ. Multilobular osteochondrosarcoma in 39 dogs: 1979-1993. J Am Anim Hosp Assoc 1998; 34: 11-18.
    Pubmed CrossRef
  9. Gallegos J, Schwarz T, McAnulty JF. Massive midline occipitotemporal resection of the skull for treatment of multilobular osteochondrosarcoma in two dogs. J Am Vet Med Assoc 2008; 233: 752-757.
    Pubmed CrossRef
  10. Hadley C, Gressot LV, Patel AJ, Wang LL, Flores RJ, Whitehead WE, et al. Osteosarcoma of the cranial vault and skull base in pediatric patients. J Neurosurg Pediatr 2014; 13: 380-387.
    Pubmed CrossRef
  11. Hayes GM, Demeter EA, Choi E, Oblak M. Single-stage craniectomy and cranioplasty for multilobular osteochondrosarcoma managed with a custom additive manufactured titanium plate in a dog. Case Rep Vet Med 2019; 2019: 6383591.
    Pubmed KoreaMed CrossRef
  12. Hespel AM, Wilhite R, Hudson J. Invited review--applications for 3D printers in veterinary medicine. Vet Radiol Ultrasound 2014; 55: 347-358.
    Pubmed CrossRef
  13. Holmes ME, Keyerleber MA, Faissler D. Prolonged survival after craniectomy with skull reconstruction and adjuvant definitive radiation therapy in three dogs with multilobular osteochondrosarcoma. Vet Radiol Ultrasound 2019; 60: 447-455.
    Pubmed CrossRef
  14. Jalbert F, Boetto S, Nadon F, Lauwers F, Schmidt E, Lopez R. One-step primary reconstruction for complex craniofacial resection with PEEK custom-made implants. J Craniomaxillofac Surg 2014; 42: 141-148.
    Pubmed CrossRef
  15. James J, Oblak ML, Zur Linden AR, James FMK, Phillips J, Parkes M. Schedule feasibility and workflow for additive manufacturing of titanium plates for ranioplasty in canine skull tumors. BMC Vet Res 2020; 16: 180.
    Pubmed KoreaMed CrossRef
  16. Kudnig ST, Séguin B. Veterinary surgical oncology. New York: John Wiley & Sons. 2012.
    CrossRef
  17. Kuipers von Lande RG, Worth AJ, Peckitt NS, Cave NJ, Tang L. Rapid prototype modeling and customized titanium plate fabrication for correction of a persistent hard palate defect in a dog. J Am Vet Med Assoc 2012; 240: 1316-1322.
    Pubmed CrossRef
  18. Ma L, Zhou Y, Zhu Y, Lin Z, Wang Y, Zhang Y, et al. 3D-printed guiding templates for improved osteosarcoma resection. Sci Rep 2016; 6: 23335.
    Pubmed KoreaMed CrossRef
  19. Meetze K, Palmer JN, Schlosser RJ. Frontal sinus complications after frontal craniotomy. Laryngoscope 2004; 114: 945-948.
    Pubmed CrossRef
  20. Moissonnier P, Devauchelle P, Delisle F. Cranioplasty after en bloc resection of calvarial chondroma rodens in two dogs. J Small Anim Pract 1997; 38: 358-363.
    Pubmed CrossRef
  21. Mouatt JG. Acrylic cranioplasty and axial pattern flap following calvarial and cerebral mass excision in a dog. Aust Vet J 2002; 80: 211-215.
    Pubmed CrossRef
  22. Mulford JS, Babazadeh S, Mackay N. Three-dimensional printing in orthopaedic surgery: review of current and future applications. ANZ J Surg 2016; 86: 648-653.
    Pubmed CrossRef
  23. O’Brien CS, Bagley RS, Hicks DG, Chen AV, Wininger FA, Brumitt JW. Gamma-irradiated calvarium allograft cranioplasty in a cat following brain tumor removal. J Am Anim Hosp Assoc 2010; 46: 268-273.
    Pubmed CrossRef
  24. Oji T, Sakamoto Y, Miwa T, Nakagawa Y, Yoshida K, Kishi K. Usefulness of an osteotomy template for skull tumorectomy and simultaneous skull reconstruction. J Craniofac Surg 2016; 27: 1565-1567.
    Pubmed CrossRef
  25. Policicchio D, Casu G, Dipellegrini G, Doda A, Muggianu G, Boccaletti R. Comparison of two different titanium cranioplasty methods: custom-made titanium prostheses versus precurved titanium mesh. Surg Neurol Int 2020; 11: 148.
    Pubmed KoreaMed CrossRef
  26. Pucci JU, Christophe BR, Sisti JA, Connolly ES Jr. Three-dimensional printing: technologies, applications, and limitations in neurosurgery. Biotechnol Adv 2017; 35: 521-529.
    Pubmed CrossRef
  27. Rosselli DD, Platt SR, Freeman C, O’Neill J, Kent M, Holmes SP. Cranioplasty using titanium mesh after skull tumor resection in five dogs. Vet Surg 2017; 46: 67-74.
    Pubmed CrossRef
  28. Rotaru H, Stan H, Florian IS, Schumacher R, Park YT, Kim SG, et al. Cranioplasty with custom-made implants: analyzing the cases of 10 patients. J Oral Maxillofac Surg 2012; 70: e169-e176.
    Pubmed CrossRef
  29. Straw RC, LeCouteur RA, Powers BE, Withrow SJ. Multilobular osteochondrosarcoma of the canine skull: 16 cases (1978-1988). J Am Vet Med Assoc 1989; 195: 1764-1769.
  30. Sweet KA, Nolan MW, Yoshikawa H, Gieger TL. Stereotactic radiation therapy for canine multilobular osteochondrosarcoma: eight cases. Vet Comp Oncol 2020; 18: 76-83.
    Pubmed CrossRef
  31. Vancil JM, Henry CJ, Milner RJ, McCoig AM, Lattimer JC, Villamil JA, et al. Use of samarium Sm 153 lexidronam for the treatment of dogs with primary tumors of the skull: 20 cases (1986-2006). J Am Vet Med Assoc 2012; 240: 1310-1315.
    Pubmed CrossRef
  32. Wang F, Zhu J, Peng X, Su J. The application of 3D printed surgical guides in resection and reconstruction of malignant bone tumor. Oncol Lett 2017; 14: 4581-4584.
    Pubmed KoreaMed CrossRef
  33. Williams LR, Fan KF, Bentley RP. Custom-made titanium cranioplasty: early and late complications of 151 cranioplasties and review of the literature. Int J Oral Maxillofac Surg 2015; 44: 599-608.
    Pubmed CrossRef
  34. Wong KC, Sze LKY, Kumta SM. Complex joint-preserving bone tumor resection and reconstruction using computer navigation and 3D-printed patient-specific guides: a technical note of three cases. J Orthop Translat 2021; 29: 152-162.
    Pubmed KoreaMed CrossRef
  35. Wu G, Liang Q, Liu Y. Primary osteosarcoma of frontal bone: a case report and review of literature. Medicine (Baltimore) 2017; 96: e9392.
    Pubmed KoreaMed CrossRef
  36. Yashin KS, Ermolaev AY, Ostapyuk MV, Kutlaeva MA, Rasteryaeva MV, Mlyavykh SG, et al. Case report: simultaneous resection of bone tumor and CAD/CAM titanium cranioplasty in fronto-orbital region. Front Surg 2021; 8: 718725.
    Pubmed KoreaMed CrossRef

Article

Case Report

J Vet Clin 2022; 39(5): 246-252

Published online October 31, 2022 https://doi.org/10.17555/jvc.2022.39.5.246

Copyright © The Korean Society of Veterinary Clinics.

Cranioplasty for Multilobular Osteochondrosarcoma Using 3-Dimensional Printing Technology in Dogs: A Report of Two Cases with a Long-Term Follow-Up

Seong-Hyeon Heo1 , Hae-Beom Lee1 , Jae-Min Jeong1 , Young-Jin Jeon1 , Dae-Hyun Kim1 , Seong-Mok Jeong1 , Yoon-Ho Roh1,2

1Department of Veterinary Surgery, College of Veterinary Medicine, Chungnam National University, Daejeon 34134, Korea
2Division of Small Animal Surgery, Department of Clinical Veterinary Medicine, Vetsuisse-Faculty, University of Bern, Bern 3012, Switzerland

Correspondence to:*202020036@g.cnu.ac.kr
Seong-Hyeon Heo and Hae-Beom Lee contributed equally to this work.

Received: April 11, 2022; Revised: August 12, 2022; Accepted: September 20, 2022

This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Multilobular osteochondrosarcoma (MLO) reportedly has a good prognosis after complete resection. This study reports the successful treatment of MLO in two dogs using 3-dimensional (3D) printing technology. A nine-yearold castrated male Maltese (Case 1) and a five-year-old castrated male poodle (Case 2) both presented with a mass in the skull. Diagnostic imaging revealed a cranial mass arising from the cranio-orbital and parieto-occipital bones. The masses were resected using 3D-printed osteotomy guides, and the resulting defects were reconstructed using 3D-printed patient-specific implants. Histopathological results confirmed the resection of MLOs with clean margins. Patients routinely recover from surgery without complications. To date, the two patients remain alive without clinical signs of tumor recurrence at 20 and 12 months postoperatively, respectively. In the management of MLO in dogs, 3D printing technology can allow accurate tumor resection, reduced surgical time, and successful reconstruction of large defects.

Keywords: multilobular osteochondrosarcoma, 3D printing, osteotomy guide, cranioplasty, canine.

Introduction

Multilobular osteochondrosarcomas (MLOs) are a rare type of malignant bone tumor that most often occur in the flat bones of a canine skull. The majority of dogs with MLOs are middle-aged to older, medium- to large-breed dogs with a median age at presentation of eight years and median weight of 29 kg (8,16). These tumors are typically slow-growing, locally invasive, and malignant, with a metastasis rate of up to 58% (8,29). The most common clinical presentation is a firm and fixed mass of the skull. However, neurological signs can appear depending on the size and location of the tumor (6).

Although chemotherapy and radiotherapy may have benefits of local control of tumors or palliation of residual tumors (13,30,31), surgery remains the treatment of choice. Clean surgical margins are strongly associated with favorable prognosis (5,7,8,16).

In a retrospective study of 39 dogs with MLO in the skull, the median disease-free times following complete and incomplete resection were 1332 days and 320 days, respectively. The metastatic rates for complete and incomplete resection are 25% and 75%, respectively (8). In that study, more than half of the diseased dogs died of local recurrence or metastasis, with a median time from the onset of recurrence or metastasis to death of 239 days. Therefore, aggressive resection of the tumor with wide margins is recommended. Wide resection of the cranium can create large defects, resulting in serious cosmetic problems, and the underlying brain becomes vulnerable to trauma or infection. Therefore, a cranioplasty should be considered (27).

Three-dimensional (3D) printing is an additive manufacturing method that converts computer-generated 3D images into physical models (22). This technology has been used extensively in surgical procedures, including surgeon-patient communication, preplanning, and custom implant fabrication (12,22,26). Recently, 3D-printed osteotomy guides have been used for malignant bone tumor surgeries, resulting in precise resection of the tumor and implantation, reduced blood loss, and reduced operation time (18,32,34). 3D-printed implants have been used to reconstruct bone defects in complex structures such as the maxilla and cranium (17,28).

To date, rare cases of cranioplasty using 3D-printed implants in dogs with MLO have been reported (5,11). This case report describes the application of 3D-printed osteotomy guides and patient-specific implants for cranioplasty in two dogs with MLOs and their favorable long-term outcomes.

Case Report

Case 1

A nine-year-old, 6.7 kg castrated male Maltese presented with a firm mass in the frontal calvarium. The mass progressively enlarged over the last three months and adhered to the right fronto-orbital region on palpation. Ventrolateral deviation and hyperemia of the globe of the right eye were observed (Fig. 1A). Physical and neurological examination results were unremarkable. Radiography revealed a lobulated mass arising from the right frontal bone and extending cranially to the right orbit. Computed tomography (CT, AlexionTM, Canon Medical Systems Corporation, Otawara, Japan) confirmed a 3.3 × 2.7 × 3.1 cm mass with heterogeneous soft tissue opacity invading the right frontal sinus. On magnetic resonance imaging (MRI, 1.5 Tesla unit, Magnetom Essenza, Siemens, Germany), the mass was hypointense on T2-weighted (T2W) and isointense on T1-weighted (T1W) images, and did not invade the brain (Fig. 1B, C). The CT images of the patient were exported in Digital Imaging and Communication in Medicine format and reconstructed using a computer software (3DS Max, Autodesk, CA, USA). With the reconstructed images, the osteotomy guide was designed to provide a template for tumor resection with 5 mm lateral margins and a groove fitting to the temporal line of the right frontal bone. A titanium plate capable of reconstructing the defect was designed based on the opposite side of the skull. Anatomical bio-models of the skull and tumor were designed for preoperative planning and intraoperative inspection (Fig. 2A). The 3D osteotomy guide and bio-models were printed using a 3D printer (Finbot-Z420, TPC Mecatronics, Seoul, Korea) with a polylactic acid filament (PLA filament, Cubicon, Seongnam, Korea), and the titanium plate was printed using a 3D printer (SLM 125, SLM Solution, Germany) (Fig. 2B).

Figure 1. Preoperative and postoperative gross images and magnetic resonance imaging (MRI) of Case 1. A preoperative macroscopic image (A) and T2-weighted MRI images of transverse view (B) and sagittal view (C). A postoperative macroscopic image at two weeks postoperatively (D). Contrast-enhanced T1W MRI images of transverse view (E) and sagittal view (F) at 12 months postoperatively.
Figure 2. Preoperative planning, rehearsal surgery, and postoperative radiographic images of Case 1. Three-dimensional (3D)-reconstructed preoperative planning (A), 3D-printed biomodels with osteotomy guide and titanium plate (B), and radiographic image (C) of Case 1 at two weeks postoperatively.

During surgery, the patient was pre-medicated with midazolam (0.2 mg/kg, IV; Midazolam inj., Bukwang Pharm, Seoul, Korea). Anesthesia was induced with propofol (4 mg/kg, IV; Anepol inj., Hana Pharm, Seoul, Korea) and maintained with isoflurane (Ifran®, Hana Pharm, Seoul, Korea). A constant rate infusion (CRI) of remifentanil (5-40 µg/kg/h; Remiva inj., Hana Pharm, Seoul, Korea) was administered for analgesia. Cefazolin (22 mg/kg, IV; cefazolin inj., Chong Kun Dang, Seoul, Korea) was administered prior to skin incision and repeated every 90 min. Before tumor resection, osteotomy of the right zygomatic arch and transection of the orbital ligament were performed to allow ventral reflection of the eye globe and access to the ventral orbit. An elliptical skin incision was made along the lateral margins of the tumor. When the tumor was exposed, a 3D-printed osteotomy guide was placed around the tumor, and a surgical marking pen was used to mark the resection margin. A 2 mm pneumatic burr was used to perform craniectomy along the resection margin, extending laterally from the dorsal midline of the frontal bone to the right zygomatic process. After retracting the excised tumor, the underlying dura mater was torn, while the brain tissue was not damaged. Durectomy was performed up to the lateral margin of the tumor. Additionally, mucosa removal in the exposed frontal sinus was performed using a 2 mm pneumatic burr, and several pieces of gelatin sponges (Spongostan standard, Ethicon, USA) were inserted into the sinus for frontal sinus obliteration (19). After hemostasis of the minor bleeding, the excised dura mater was reconstructed using a synthetic dura mater substitute, ReDura (Medprin Biotech, La Mirada, CA, USA), and a 3D-printed titanium plate was placed over the defect and secured with six screws (1.5 mm self-drilling titanium).

The patient routinely recovered postoperatively. Radiographs revealed skull defect coverage and alignment of the titanium plate (Fig. 2C). Postoperatively, the CRI of remifentanil (6 µg/kg/h) was administered for three days, and cefotaxime (20 mg/kg, IV; Cefotaxime inj., Chong Kun Dang, Seoul, Korea) was administered for two weeks. Histopathological examination of the excised tumor confirmed the diagnosis of grade 1 of 3 MLO with clean lateral margins of >6 mm (Fig. 3A). A well-circumscribed, predominantly expansile, sparsely cellular mass within the subcutaneous connective tissues that partially infiltrated the underlying bone of the sinus was observed. The patient was discharged two weeks postoperatively without any complications (Fig. 1D).

Figure 3. Histopathologic microscopic examination of Cases 1 and 2. There are spindle to stellate cells forming anastomosing streams and bundles in a fibrous stroma with regularly interspersed foci of chondrus and osseous metaplasia (A, hematoxylin and eosin [H&E]; scale bars: 500 μm). Osteochondrosarcoma proliferates while maintaining the form of lobes (B, H&E; ×12.5).

At two months after discharge, the patient presented with epistaxis and purulent discharge from the right nasal orifice. An MRI scan revealed heterogeneous lesions with T2W hyperintensity and T1W isointensitiy within the nasal cavities and frontal sinuses. No tumor recurrence was detected (Fig. 1E, F). A complete blood count revealed mild neutrophilia (14,110 cells/µL, reference range: 3,900-8,000). Elevated levels of alkaline phosphatase (488 U/L, reference range: 15-127), alanine aminotransferase (175 U/L, reference range: 19-70), and aspartate aminotransferase (49 U/L, reference range: 15-43) were observed, which was considered due to recently administered prednisolone (0.5 mg/kg, PO, q12h) for dermatitis pruritis for two weeks. Bacterial culture of nasal swabs confirmed the presence of Staphylococcus aureus. The patient was diagnosed with suppurative rhinosinusitis and was prescribed doxycycline (5 mg/kg, PO, q12h; doxycycline Tab., Youngpoong Pharm, Seoul, Korea) for two weeks.

At ten months postoperatively, generalized tonic-clonic seizure was observed. The owner declined further examination, and phenobarbital administration (2.5 mg/kg PO, q12h; Phenobarbital Tab., Hana Pharm, Seoul, Korea) was started. The patient was doing well without seizures at 20 months postoperatively.

Case 2

A five-year-old, 10.7 kg castrated male poodle was brought for evaluation of a mass located in the parieto-occipital bone. Preoperative examinations, including CT, were performed (Fig. 4A). The 3D-printed osteotomy guide, titanium plate, and bio-models were designed as described for Case 1 (Fig. 4B).

Figure 4. Preoperative (A, B) and intraoperative (C, D) views of Case 2. Three-dimensional (3D) reconstructed image of preoperative computed tomography scan (A). A 3D-printed bio-model and skull of the patient (B). A defect after craniectomy (C). A 3D-printed titanium plate fixed over defect (D).

The patient was anesthetized using the same protocol as in Case 1. The temporal muscle was dissected after an elliptical incision was made on the skin. The osteotomy guide was positioned following the complete dissection of the muscle tissues, and the resection margin was marked around the tumor. Parieto-occipital craniectomy was performed using a 2 mm pneumatic burr, and the underlying dura mater was bluntly dissected with a spatula. The tumor was carefully lifted off the dura mater without damaging the dorsal sagittal sinus within the dura mater (Fig. 4C). After several lavages with sterile saline, the defect in the skull was covered with synthetic dura mater anchored to the adjacent edge of the temporal muscle. The 3D-printed titanium plate was secured over the defect with four 1.5 mm self-drilling titanium screws (Fig. 4D).

Histopathological evaluation of the excised tumor confirmed an MLO with complete lateral margins. The proliferated tumor cells had one or more distinct nucleophiles and malignant findings, such as anisokaryosis of the nucleus, and mitotic counts were rarely observed. Several osteoclasts were also observed (Fig. 3B). The patient was discharged at seven days postoperatively. No tumor complications or recurrences until the final follow-up at 12 months postoperatively were noted.

Discussion

This report describes the application of 3D printing technology for cranioplasty in two dogs with MLOs. The patients had good long-term postoperative clinical results without serious complications.

For MLO, the overall recurrence rate after surgery is 47%-58% and is dependent on the completeness of surgical resection. The median disease-free interval for completely resected MLO is significantly better than that reported for incompletely resected tumors (8,16,29). However, owing to the complexity of the canine skull, obtaining an adequate surgical margin is often difficult, and early recurrence may occur (6,9,27). Recently, 3D-printed osteotomy guides for bone sarcoma resection have been reported to improve the accuracy of resection with adequate margin (1,3,18). This technique facilitates the recognition of real tumor margins and allows surgeons to overcome technical errors in treating complex bone structures. It has also been demonstrated to eliminate the need for implant trimming for cranioplasty, allowing the operator to determine the exact edge of skull tumors (24,36). Hence, the skull can be reconstructed with a 3D-printed titanium plate immediately, and the operation time can be reduced (15).

Various materials for cranioplasty have been described in dogs, including cortical allografts, polymethyl methacrylate (PMMA), and titanium mesh (7,20,23,27). Cortical allograft bone provides mechanical support; however, it requires aseptic harvesting and preserving techniques (23). Moreover, serious postoperative complications have been reported, including immunogenic reactivity, infection, and resorption of the implant (20). PMMA is an inexpensive and readily available material. However, it requires an intraoperative mold, which is associated with thermal tissue necrosis, infection, and prolonged surgical time (4,21). Titanium mesh has some benefits, including rigidity, availability, and resistance to infection, although intraoperative contouring is required (15,27). Custom-made titanium plates for cranioplasty have been described in human reports (28,33). A retrospective study comparing two different titanium cranioplasty methods has revealed that custom-made titanium plates had better aesthetic results, complete coverage of defects, shorter surgical times, and easier operation for the surgeon than titanium mesh (25). In our patients, the 3D-printed titanium plates were successfully secured without massive hemorrhage or prolonged procedures, resulting in good clinical outcomes.

The dorsal sagittal and transverse sinuses are the most significant vessels that may be encountered during craniectomy and lie within the dura mater (16). Damage to these structures can lead to life-threatening hemorrhage or fatal brain swelling (9). In case 1, the location of the tumor was far from the sinus; therefore, only slight bleeding occurred despite dural rupture. By contrast, the preoperative MRI scan of case 2 confirmed that the tumor was located above the dorsal sagittal sinus. This allowed the surgeon to carefully dissect the tumor from the dura mater, which may lead to favorable outcomes. Resection of the involved dura mater is considered an important component for achieving maximal resection in primary osteosarcoma of the frontal bone in humans. When dural involvement is suspected based on the intraoperative gross appearance or preoperative MRI scans, dural resection is recommended if it can be achieved with a low risk of significant morbidity (10,35). Hayes et al. have reported MLO recurrence in a dog at seven months postoperatively. They suggested that the dura mater should be considered a deep margin in cases of MLO in dogs (11). In Case 1, an intraoperative dural tear was suspected due to adhesions, which could be evidence of dural invasion of the tumor. Therefore, dural resection was performed.

Single-stage cranioplasty with osteotomy guidance is generally performed only for benign tumors because of the risk of incomplete margins. The average 3-week delay in implant manufacturing is another concern in the management of malignant tumors (14,24). However, Berli et al. described single-stage cranioplasty for malignant tumors with little morbidity (2). In veterinary medicine, single-step cranioplasty is often necessary because of the high cost of a second surgery or the owner’s preference (15). Therefore, this technique can be a reasonable option for treating malignant skull tumors, as long as the delay in implant manufacturing is minimized (2).

Conclusions

In our patient, craniectomy and cranioplasty for MLO were successfully performed using 3D printing technology. Based on the clinical outcomes, this technique may be feasible with limited long-term postoperative complications. Further investigation is required to confirm our preliminary findings.

Source of Funding

This study was supported by the research fund of Chungnam National University.

Informed Consent Statement

Written informed consents have been obtained from all owners that donated their animals for the study.

Acknowledgements

This work was supported by the Research Scholarship of the Chungnam National University.

Conflicts of Interest

The authors have no conflicting interests.

Fig 1.

Figure 1.Preoperative and postoperative gross images and magnetic resonance imaging (MRI) of Case 1. A preoperative macroscopic image (A) and T2-weighted MRI images of transverse view (B) and sagittal view (C). A postoperative macroscopic image at two weeks postoperatively (D). Contrast-enhanced T1W MRI images of transverse view (E) and sagittal view (F) at 12 months postoperatively.
Journal of Veterinary Clinics 2022; 39: 246-252https://doi.org/10.17555/jvc.2022.39.5.246

Fig 2.

Figure 2.Preoperative planning, rehearsal surgery, and postoperative radiographic images of Case 1. Three-dimensional (3D)-reconstructed preoperative planning (A), 3D-printed biomodels with osteotomy guide and titanium plate (B), and radiographic image (C) of Case 1 at two weeks postoperatively.
Journal of Veterinary Clinics 2022; 39: 246-252https://doi.org/10.17555/jvc.2022.39.5.246

Fig 3.

Figure 3.Histopathologic microscopic examination of Cases 1 and 2. There are spindle to stellate cells forming anastomosing streams and bundles in a fibrous stroma with regularly interspersed foci of chondrus and osseous metaplasia (A, hematoxylin and eosin [H&E]; scale bars: 500 μm). Osteochondrosarcoma proliferates while maintaining the form of lobes (B, H&E; ×12.5).
Journal of Veterinary Clinics 2022; 39: 246-252https://doi.org/10.17555/jvc.2022.39.5.246

Fig 4.

Figure 4.Preoperative (A, B) and intraoperative (C, D) views of Case 2. Three-dimensional (3D) reconstructed image of preoperative computed tomography scan (A). A 3D-printed bio-model and skull of the patient (B). A defect after craniectomy (C). A 3D-printed titanium plate fixed over defect (D).
Journal of Veterinary Clinics 2022; 39: 246-252https://doi.org/10.17555/jvc.2022.39.5.246

References

  1. Bellanova L, Paul L, Docquier PL. Surgical guides (patient-specific instruments) for pediatric tibial bone sarcoma resection and allograft reconstruction. Sarcoma 2013; 2013: 787653.
    Pubmed KoreaMed CrossRef
  2. Berli JU, Thomaier L, Zhong S, Huang J, Quinones A, Lim M, 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.
    Pubmed CrossRef
  3. Blakeney WG, Day R, Cusick L, Smith RL. Custom osteotomy guides for resection of a pelvic chondrosarcoma. Acta Orthop 2014; 85: 438-441.
    Pubmed KoreaMed CrossRef
  4. Bryant KJ, Steinberg H, McAnulty JF. Cranioplasty by means of molded polymethylmethacrylate prosthetic reconstruction after radical excision of neoplasms of the skull in two dogs. J Am Vet Med Assoc 2003; 223: 67-72, 59.
    Pubmed CrossRef
  5. Choi S, Honnami M, Liu IL, Yamamoto K, Ohba S, Echigo R, et al. Cranioplasty with custom-made artificial bone after resection of multilobular bone tumor in a dog. J Vet Clin 2014; 31: 46-50.
    CrossRef
  6. Cook S, Civello A, Lam R, Fenn J, Neilson D, Priestnall S, et al. Rapid postoperative recurrence of a cranial multilobular tumor of bone in a young dog. Clin Case Rep 2017; 5: 1995-1999.
    Pubmed KoreaMed CrossRef
  7. de Casterlé AD, Van Goethem B, Kitshoff A, Bhatti S, Gielen I, Bosmans T. Titanium mesh reconstruction of a dog’s cranium after multilobular osteochondrosarcoma resection. Vlaams Diergeneeskd Tijdsch 2017; 86: 232-240.
    CrossRef
  8. Dernell WS, Straw RC, Cooper MF, Powers BE, LaRue SM, Withrow SJ. Multilobular osteochondrosarcoma in 39 dogs: 1979-1993. J Am Anim Hosp Assoc 1998; 34: 11-18.
    Pubmed CrossRef
  9. Gallegos J, Schwarz T, McAnulty JF. Massive midline occipitotemporal resection of the skull for treatment of multilobular osteochondrosarcoma in two dogs. J Am Vet Med Assoc 2008; 233: 752-757.
    Pubmed CrossRef
  10. Hadley C, Gressot LV, Patel AJ, Wang LL, Flores RJ, Whitehead WE, et al. Osteosarcoma of the cranial vault and skull base in pediatric patients. J Neurosurg Pediatr 2014; 13: 380-387.
    Pubmed CrossRef
  11. Hayes GM, Demeter EA, Choi E, Oblak M. Single-stage craniectomy and cranioplasty for multilobular osteochondrosarcoma managed with a custom additive manufactured titanium plate in a dog. Case Rep Vet Med 2019; 2019: 6383591.
    Pubmed KoreaMed CrossRef
  12. Hespel AM, Wilhite R, Hudson J. Invited review--applications for 3D printers in veterinary medicine. Vet Radiol Ultrasound 2014; 55: 347-358.
    Pubmed CrossRef
  13. Holmes ME, Keyerleber MA, Faissler D. Prolonged survival after craniectomy with skull reconstruction and adjuvant definitive radiation therapy in three dogs with multilobular osteochondrosarcoma. Vet Radiol Ultrasound 2019; 60: 447-455.
    Pubmed CrossRef
  14. Jalbert F, Boetto S, Nadon F, Lauwers F, Schmidt E, Lopez R. One-step primary reconstruction for complex craniofacial resection with PEEK custom-made implants. J Craniomaxillofac Surg 2014; 42: 141-148.
    Pubmed CrossRef
  15. James J, Oblak ML, Zur Linden AR, James FMK, Phillips J, Parkes M. Schedule feasibility and workflow for additive manufacturing of titanium plates for ranioplasty in canine skull tumors. BMC Vet Res 2020; 16: 180.
    Pubmed KoreaMed CrossRef
  16. Kudnig ST, Séguin B. Veterinary surgical oncology. New York: John Wiley & Sons. 2012.
    CrossRef
  17. Kuipers von Lande RG, Worth AJ, Peckitt NS, Cave NJ, Tang L. Rapid prototype modeling and customized titanium plate fabrication for correction of a persistent hard palate defect in a dog. J Am Vet Med Assoc 2012; 240: 1316-1322.
    Pubmed CrossRef
  18. Ma L, Zhou Y, Zhu Y, Lin Z, Wang Y, Zhang Y, et al. 3D-printed guiding templates for improved osteosarcoma resection. Sci Rep 2016; 6: 23335.
    Pubmed KoreaMed CrossRef
  19. Meetze K, Palmer JN, Schlosser RJ. Frontal sinus complications after frontal craniotomy. Laryngoscope 2004; 114: 945-948.
    Pubmed CrossRef
  20. Moissonnier P, Devauchelle P, Delisle F. Cranioplasty after en bloc resection of calvarial chondroma rodens in two dogs. J Small Anim Pract 1997; 38: 358-363.
    Pubmed CrossRef
  21. Mouatt JG. Acrylic cranioplasty and axial pattern flap following calvarial and cerebral mass excision in a dog. Aust Vet J 2002; 80: 211-215.
    Pubmed CrossRef
  22. Mulford JS, Babazadeh S, Mackay N. Three-dimensional printing in orthopaedic surgery: review of current and future applications. ANZ J Surg 2016; 86: 648-653.
    Pubmed CrossRef
  23. O’Brien CS, Bagley RS, Hicks DG, Chen AV, Wininger FA, Brumitt JW. Gamma-irradiated calvarium allograft cranioplasty in a cat following brain tumor removal. J Am Anim Hosp Assoc 2010; 46: 268-273.
    Pubmed CrossRef
  24. Oji T, Sakamoto Y, Miwa T, Nakagawa Y, Yoshida K, Kishi K. Usefulness of an osteotomy template for skull tumorectomy and simultaneous skull reconstruction. J Craniofac Surg 2016; 27: 1565-1567.
    Pubmed CrossRef
  25. Policicchio D, Casu G, Dipellegrini G, Doda A, Muggianu G, Boccaletti R. Comparison of two different titanium cranioplasty methods: custom-made titanium prostheses versus precurved titanium mesh. Surg Neurol Int 2020; 11: 148.
    Pubmed KoreaMed CrossRef
  26. Pucci JU, Christophe BR, Sisti JA, Connolly ES Jr. Three-dimensional printing: technologies, applications, and limitations in neurosurgery. Biotechnol Adv 2017; 35: 521-529.
    Pubmed CrossRef
  27. Rosselli DD, Platt SR, Freeman C, O’Neill J, Kent M, Holmes SP. Cranioplasty using titanium mesh after skull tumor resection in five dogs. Vet Surg 2017; 46: 67-74.
    Pubmed CrossRef
  28. Rotaru H, Stan H, Florian IS, Schumacher R, Park YT, Kim SG, et al. Cranioplasty with custom-made implants: analyzing the cases of 10 patients. J Oral Maxillofac Surg 2012; 70: e169-e176.
    Pubmed CrossRef
  29. Straw RC, LeCouteur RA, Powers BE, Withrow SJ. Multilobular osteochondrosarcoma of the canine skull: 16 cases (1978-1988). J Am Vet Med Assoc 1989; 195: 1764-1769.
  30. Sweet KA, Nolan MW, Yoshikawa H, Gieger TL. Stereotactic radiation therapy for canine multilobular osteochondrosarcoma: eight cases. Vet Comp Oncol 2020; 18: 76-83.
    Pubmed CrossRef
  31. Vancil JM, Henry CJ, Milner RJ, McCoig AM, Lattimer JC, Villamil JA, et al. Use of samarium Sm 153 lexidronam for the treatment of dogs with primary tumors of the skull: 20 cases (1986-2006). J Am Vet Med Assoc 2012; 240: 1310-1315.
    Pubmed CrossRef
  32. Wang F, Zhu J, Peng X, Su J. The application of 3D printed surgical guides in resection and reconstruction of malignant bone tumor. Oncol Lett 2017; 14: 4581-4584.
    Pubmed KoreaMed CrossRef
  33. Williams LR, Fan KF, Bentley RP. Custom-made titanium cranioplasty: early and late complications of 151 cranioplasties and review of the literature. Int J Oral Maxillofac Surg 2015; 44: 599-608.
    Pubmed CrossRef
  34. Wong KC, Sze LKY, Kumta SM. Complex joint-preserving bone tumor resection and reconstruction using computer navigation and 3D-printed patient-specific guides: a technical note of three cases. J Orthop Translat 2021; 29: 152-162.
    Pubmed KoreaMed CrossRef
  35. Wu G, Liang Q, Liu Y. Primary osteosarcoma of frontal bone: a case report and review of literature. Medicine (Baltimore) 2017; 96: e9392.
    Pubmed KoreaMed CrossRef
  36. Yashin KS, Ermolaev AY, Ostapyuk MV, Kutlaeva MA, Rasteryaeva MV, Mlyavykh SG, et al. Case report: simultaneous resection of bone tumor and CAD/CAM titanium cranioplasty in fronto-orbital region. Front Surg 2021; 8: 718725.
    Pubmed KoreaMed CrossRef

Vol.39 No.5 2022-10-31

qrcode
qrcode
The Korean Society of Veterinary Clinics

pISSN 1598-298X
eISSN 2384-0749

Stats or Metrics

Share this article on :

  • line