• View in gallery
    Figure 1

    Representative images showing assessment and planning for transsphenoidal hypophysectomy using a patient-specific guide (PSG) in a dog on a 3-D computer program. A—The pituitary fossa was confirmed in a 3-D bone model with a horizontal cut of the head in a mixed-breed dog. B—The angle of the pituitary gland and the base of the maxilla were measured. C—The distance of the sphenoid bone to the pituitary gland fossa and its length were measured (blue arrow). The location of the pituitary fossa was compared with the hamular process. Cranial or caudal direction and the distance were measured (green arrow). D and E—The ventral and dorsal surfaces, respectively, of the PSG show the relationship with the mouth. F and G—Attachment of the bone model and PSG on sagittal and ventral planes, respectively, confirm the location of the pituitary gland fossa.

  • View in gallery
    Figure 2

    Representative images showing postoperative evaluation. A and B—The hole’s location on the ventral and dorsal plane, respectively, is shown for a mixed-breed dog. The cranial-caudal and left-right places were determined based on the pituitary fossa. C—The postoperative positions of the hole (pink) were recorded and compared to the preoperative position (black circle) on the dorsal plane.

  • View in gallery
    Figure 3

    Images showing the plan on CT and MRI in a Beagle. A—The boundary of the cavernous sinus was determined as the horizontal length of the surgical window on magnetic resonance angiography (MRA). B—The length of the surgical window was determined on the bone model created through CT. C—The size and the angle of the hole (radius, 2 mm) entering the pituitary gland were determined. The dorsal view of head was horizontally cut.

  • View in gallery
    Figure 4

    Images showing the modified pilot hole technique with the PSG and rigid telescope in a Beagle. A—After incision, the basisphenoid bone was revealed. B—The PSG was roughly attached to the bone. C—The pilot hole was made with a bur, and the PSG was detached. D and E—The surgical window, which was planned on CT and MRI, was made using the size of the bur. F—The shape of the surgical window and surface of the pituitary gland are shown.

  • View in gallery
    Figure 5

    Images showing the postoperative assessment of the surgical window and pituitary gland region in a live dog. A through C—The surgical window and path (red arrow) of case 1 to access the pituitary gland are identified in the axial, sagittal, and coronal MRA images, respectively. The gland was removed adequately without invasion to the surrounding vessels and venous sinus (blue arrow). D—Necropsy image of case 1 showing the resected pituitary fossa consistent with the surgical plan. E through G—Postoperative surgical windows displayed satisfactory surgical windows in the 3-D computer-aided design program in all 3 treated dogs.

  • 1.

    Snyder JM, Lipitz L, Skorupski KA, Shofer FS, Van Winkle TJ. Secondary intracranial neoplasia in the dog: 177 cases (1986–2003). J Vet Intern Med. 2008;22(1):172177. doi:10.1111/j.1939-1676.2007.0002.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Snyder JM, Shofer FS, Van Winkle TJ, Massicotte C. Canine intracranial primary neoplasia: 173 cases (1986–2003). J Vet Intern Med. 2006;20(3):669675. doi:10.1892/0891-6640(2006)20[669:cipnc]2.0.co;2

    • Search Google Scholar
    • Export Citation
  • 3.

    Tyson R, Graham JP, Bermingham E, Randall S, Berry CR. Dynamic computed tomography of the normal feline hypophysis cerebri (Glandula pituitaria). Vet Radiol Ultrasound. 2005;46(1):3338. doi:10.1111/j.1740-8261.2005.00006.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    van der Vlugt-Meijer RH, Meij BP, Voorhout G. Thin-slice three-dimensional gradient-echo magnetic resonance imaging of the pituitary gland in healthy dogs. Am J Vet Res. 2006;67(11):18651872. doi:10.2460/ajvr.67.11.1865

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Travetti O, White C, Labruyère J, Dunning M. Variation in the MRI appearance of the canine pituitary gland. Vet Radiol Ultrasound. 2021;62(2):199209. doi: 10.1111/vru.12938

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Owen TJ, Martin LG, Chen AV. Transsphenoidal surgery for pituitary tumors and other sellar masses. Vet Clin North Am Small Anim Pract. 2018;48(1):129151. doi:10.1016/j.cvsm.2017.08.006

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    O’Neill DG, Scudder C, Faire JM, et al. Epidemiology of hyperadrenocorticism among 210,824 dogs attending primary-care veterinary practices in the UK from 2009 to 2014. J Small Anim Pract. 2016;57(7):365373. doi:10.1111/jsap.12523

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    Van Rijn SJ, Galac S, Tryfonidou M, et al. The influence of pituitary size on outcome after transsphenoidal hypophysectomy in a large cohort of dogs with pituitary-dependent hypercortisolism. J Vet Intern Med. 2016;30(4):989995. doi:10.1111/jvim.14367

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Menchetti M, De Risio L, Galli G, et al. Neurological abnormalities in 97 dogs with detectable pituitary masses. Vet Q. 2019;39(1):5764. doi:10.1080/01652176.2019.1622819:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Hara Y, Teshima T, Taoda T, et al. Efficacy of transsphenoidal surgery on endocrinological status and serum chemistry parameters in dogs with Cushing’s disease. J Vet Med Sci. 2010;72(4):397404. doi:10.1292/jvms.09-0367

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Van Asselt N, Christensen N, Meier V, et al. Definitive-intent intensity-modulated radiation therapy provides similar outcomes to those previously published for definitive-intent three-dimensional conformal radiation therapy in dogs with primary brain tumors: a multi-institutional retrospective study. Vet Radiol Ultrasound. 2020;61(4):481489. doi:10.1111/vru.12868

    • Search Google Scholar
    • Export Citation
  • 12.

    Weiss N, Gilad R, Post KD. Introduction and general neurosurgery. In: Youmans and Winn Neurological Surgery, 4-Volume Set. 4th ed: Oxford University Press; 2018:131132

    • Search Google Scholar
    • Export Citation
  • 13.

    Niebauer GW, Evans SM. Transsphenoidal hypophysectomy in the dog a new technique. Vet Surg. 1988;17:296303. doi:10.1111/j.1532-950x.1988.tb01021.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Meij BP, Voorhout G, Ingh TSVD, Hazewinkel HA, Van’t Verlaat JW. Transsphenoidal hypophysectomy in beagle dogs: evaluation of a microsurgical technique. Vet Surg. 1997;26(4):295309. doi:10.1111/j.1532-950x.1997.tb01502.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Mamelak AN, Owen TJ, Bruyette D. Transsphenoidal surgery using a high definition video telescope for pituitary adenomas in dogs with pituitary dependent hypercortisolism: methods and results. Vet Surg. 2014;43(4):369379. doi:10.1111/j.1532-950X.2014.12146.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Owen TJ, Chen AV, Frey S, Martin LG, Kalebaugh T. Transsphenoidal surgery: accuracy of an image-guided neuronavigation system to approach the pituitary fossa (sella turcica). Vet Surg. 2018;47(5):664671. doi:10.1111/vsu.12906

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Nadimi S, Molazem M, Jarolmasjed S, Nejad MRE. Volumetric evaluation of pituitary gland in dog and cat using computed tomography. Vet Res Forum. 2018;9(4):337341. doi:10.30466/vrf.2018.33073

    • Search Google Scholar
    • Export Citation
  • 18.

    Meij BP. Hypophysectomy as a treatment for canine and feline Cushing’s disease. Vet Clin North Am Small Anim Pract. 2001;31(5):10151041. doi:10.1016/s0195-5616(01)50011-x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Gao S, Stephens JD, Piatt C, et al. Overview of 3-D pringting in orthopaedics and 3-D printing in spinal surgery. In: Dipaola M, eds. 3-D Printing in Orthopaedic Surgery. Elsevier Health Sciences; 2018:85122

    • Search Google Scholar
    • Export Citation
  • 20.

    Hamilton-Bennett SE, Oxley B, Behr S. Accuracy of a patient-specific 3-D printed drill guide for placement of cervical transpedicular screws. Vet Surg. 2018;47(2):236242. doi:10.1111/vsu.12734

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Elford JH, Oxley B, Behr S. Accuracy of placement of pedicle screws in the thoracolumbar spine of dogs with spinal deformities with three-dimensionally printed patient-specific drill guides. Vet Surg. 2020;49(2):347353. doi:10.1111/vsu.13333

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Mariani CL, Zlotnick JA, Harrysson O, et al. Accuracy of three-dimensionally printed animal-specific drill guides for implant placement in canine thoracic vertebrae: a cadaveric study. Vet Surg. 2021;50(2):294302. doi:10.1111/vsu.13557

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Rho YH, Cho CW, Ryu CH, Lee JH, Jeong SM, Lee HB. Comparison between novice and experienced surgeons performing corrective osteotomy with patient-specific guides in dogs based on resulting position accuracy. Vet Sci. 2021;8(3):40. doi:10.3390/vetsci8030040

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Shinn R, Park C, DeBose K, Hsu F-C, Cecere T, Rossmeisl J. Feasibility and accuracy of 3-D printed patient-specific skull contoured brain biopsy guides. Vet Surg. 2021;50(5):933943. doi:10.1111/vsu.13641

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Fedorov A, Beichel R, Kalpathy-Cramer J, et al. 3-D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson Imaging. 2012;30(9):13231341. doi:10.1016/j.mri.2012.05.001

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    van der Vlugt-Meijer RH, Voorhout G, Meij BP. Imaging of the pituitary gland in dogs with pituitary-dependent hyperadrenocorticism. Mol Cell Endocrinol. 2002;197(1-2):8187. doi:10.1016/s0303-7207(02)00282-4

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Wininger F. Neuronavigation in small animals: development, techniques, and applications. Vet Clin North Am Small Anim Pract. 2014;44(6):12351248. doi:10.1016/j.cvsm.2014.07.015

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Wang MN, Song ZJ. Classification and analysis of the errors in neuronavigation. Neurosurgery. 2011;68(4):11311143. doi:10.1227/NEU.0b013e318209cc45

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Leblond G, Gaitero L, Moens NM, et al. Canine atlantoaxial optimal safe implantation corridors–description and validation of a novel 3-D presurgical planning method using OsiriX™. BMC Vet Res. 2016;12(1):188. doi:10.1186/s12917-016-0824-3

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Chen H, Wu D, Yang H, et al. Clinical use of 3-D printing guide plate in posterior lumbar pedicle screw fixation. Med Sci Monit. 2015;21:39483954. doi:10.12659/MSM.895597

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Beer P, Park BH, Steffen F, Smolders DLA, Pozzi A, Knell SC. Influence of a customized three-dimensionally printed drill guide on the accuracy of pedicle screw placement in lumbosacral vertebrae: an ex vivo study. Vet Surg. 2020;49(5):977988. doi:10.1111/vsu.13417

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Fujioka T, Nakata K, Nishida H, et al. A novel patient-specific drill guide template for stabilization of thoracolumbar vertebrae of dogs: cadaveric study and clinical cases. Vet Surg. 2019;48(3):336342. doi:10.1111/vsu.13140

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Kaneyama S, Sugawara T, Sumi M. Safe and accurate midcervical pedicle screw insertion procedure with the patient-specific screw guide template system. Spine. 2015;40(6):E341E348. doi:10.1097/BRS.0000000000000772

    • Crossref
    • Search Google Scholar
    • Export Citation

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Evaluation of the accuracy of three-dimensionally printed patient-specific guides for transsphenoidal hypophysectomy in small-breed dogs

Yoonho RohDepartment of Clinical Sciences, College of Veterinary Medicine, Chungnam National University, Daejeon, Korea

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Daehyun KimDepartment of Clinical Sciences, College of Veterinary Medicine, Chungnam National University, Daejeon, Korea

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Seongmok JeongDepartment of Clinical Sciences, College of Veterinary Medicine, Chungnam National University, Daejeon, Korea

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Haebeom LeeDepartment of Clinical Sciences, College of Veterinary Medicine, Chungnam National University, Daejeon, Korea

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Abstract

OBJECTIVE

To assess the accuracy of transsphenoidal hypophysectomy using 3-D printed patient-specific guides (3D-PSGs) in small-breed dogs.

ANIMALS

Heads obtained from the cadavers of 19 small-breed dogs (ex vivo portion of study) and 3 healthy adult (3 to 4 years) purpose-bred Beagles with a median body weight of 9.2 kg.

PROCEDURES

In the ex vivo study, CT images of the cadavers were collected. The position, width, and length of the pituitary fossa and the pilot hole (insertion angle and place) were measured. Using PSGs, 19 pilot holes were made for the pituitary gland fossa, and CT was performed to assess the position accuracy. In the in vivo study, 3 surgical windows from the pilot holes were made using PSGs. Repeated CT and MRI were performed to evaluate the safeness and effectiveness of PSGs, followed by necropsy.

RESULTS

In the ex vivo study, the median (interquartile range) difference between the pre- and postoperative insertion angles was 2° (0° to 3.5°) and the median deviation of the pilot hole was 0.46 mm (0 to 1.58 mm). In the in vivo study, the surrounding structures were not damaged, and favorable outcomes were evident in terms of the shape, size, and position of the surgical window.

CLINICAL RELEVANCE

3D-PSGs provided a safe and effective surgical window for transsphenoidal hypophysectomy. Our findings emphasized the applicability of PSGs in brain surgery, in terms of accuracy and effectiveness.

Abstract

OBJECTIVE

To assess the accuracy of transsphenoidal hypophysectomy using 3-D printed patient-specific guides (3D-PSGs) in small-breed dogs.

ANIMALS

Heads obtained from the cadavers of 19 small-breed dogs (ex vivo portion of study) and 3 healthy adult (3 to 4 years) purpose-bred Beagles with a median body weight of 9.2 kg.

PROCEDURES

In the ex vivo study, CT images of the cadavers were collected. The position, width, and length of the pituitary fossa and the pilot hole (insertion angle and place) were measured. Using PSGs, 19 pilot holes were made for the pituitary gland fossa, and CT was performed to assess the position accuracy. In the in vivo study, 3 surgical windows from the pilot holes were made using PSGs. Repeated CT and MRI were performed to evaluate the safeness and effectiveness of PSGs, followed by necropsy.

RESULTS

In the ex vivo study, the median (interquartile range) difference between the pre- and postoperative insertion angles was 2° (0° to 3.5°) and the median deviation of the pilot hole was 0.46 mm (0 to 1.58 mm). In the in vivo study, the surrounding structures were not damaged, and favorable outcomes were evident in terms of the shape, size, and position of the surgical window.

CLINICAL RELEVANCE

3D-PSGs provided a safe and effective surgical window for transsphenoidal hypophysectomy. Our findings emphasized the applicability of PSGs in brain surgery, in terms of accuracy and effectiveness.

Introduction

Pituitary gland tumors account for approximately 13% in dogs of all intracranial tumors.1,2 With the recent development of imaging technology, detection of pituitary lesions has been reported to increase.35 The most reported functional adenoma is corticotroph adenoma, causing pituitary dependent hyperadrenocorticism (PDH).6,7 Excessive cortisol secretion in response to excess adrenocorticotropic hormone can result in chronic stimulation of the adrenal glands, thus leading to polyphagia, polydipsia, polyuria, panting, and muscle atrophy.8 In addition, pituitary gland tumors may cause space occupying effect, such as behavioral changes, abnormal posture and gait, and cranial nerve deficits.9 In most cases of PDH in veterinary medicine, medical treatment is performed, and radiotherapy has also been applied. However, medical management treats clinical signs only and cannot reduce the size of the tumor, thus allowing persistent neurological problems.8,10 In addition, the recurrence of hormonal disease, toxicity, and side effects of the drugs used for PDH have been reported as complications.8,10,11

Surgical treatment may be recommended to increase the survival rate and reduce the recurrence of endocrine or neurologic diseases.8,10 A large pituitary mass may compress the adjacent brain7,8,12; therefore, surgical removal is considered the first choice in human medicine. Radiotherapy is recommended for an invasive primary tumor or a failed surgical option.8,10,12 Transsphenoidal resection of pituitary masses is the standard treatment in humans.12

Since the introduction of the first veterinary surgical protocols for transsphenoidal hypophysectomy (TH) in the 1980s, TH has been applied and developed successfully.13 Nevertheless, it is still challenging to perform TH successfully in dogs. First, an approach for tumor removal should be made through the mouth due to anatomical differences with human medicine.1316 Second, PDH is prevalent in small breed dogs with a small pituitary gland of an average length of 4 to 6 mm.17 The pituitary fossa is a small structure surrounded by neurovascular elements in the skull.18 Third, locating the surgical window in the skull base can be challenging because of the anatomical variations of the pituitary gland in diverse breeds.13,14 Several studies1316 have focused on identifying the location of the pituitary fossa during surgery for favorable outcomes. Meij et al14 first described the site of the pituitary fossa using CT based on the hamular processes. The surgical window was intraoperatively designated as a premeasured distance from the hamular process.14 However, this procedure is inaccurate and requires considerable experience because it is difficult to estimate the distance in the narrow space of the mouth.14,18

Recently, a video telescope-assisted 2-pilot-hole technique was developed to reduce intraoperative errors.15 The pilot hole is created as in the conventional method, after which CT is repeated to determine the distance between the pituitary fossa and the pilot hole.13 The surgical window is created based on the relation between the hamular process and the pilot hole through the video and CT images, which requires additional images intraoperatively, thus leading to increased anesthesia time.15 Moreover, this technique causes unnecessary damage because of additional holes and substantially relies on surgical experience.15 A navigation system can be used to identify surgical sites; however, it is costly and requires considerable space when conducted in dog heads. Accuracy can also be decreased by posture or manipulation during surgery.16

With the recent development of technology, 3-D printing technology has been applied to neuro-orthopedic surgery to increase accuracy.19 The surgeon can insert pins and screws at desired positions using a 3D-PSG during spinal surgery.2022 3-D printing techniques can be easily applied to clinical cases regardless of the size of the target or the surgeon’s experience.22,23 It may enable accurate location of surgical sites using PSGs in brain surgery.24 In addition, it may secure a large surgical field of view without damaging important structures during brain surgery. This necessitates the comparison and evaluation of traditional methods with methods using 3-D printing techniques; however, there are a few cases of 3-D printing applied to head surgery.24

We aimed to evaluate the accuracy of locating the surgical site for TH with a PSG by assessing the target error of the central hole prepared and its usefulness in in vivo surgery. We hypothesized that a 3D-PSG would reduce the surgical time and need for additional devices. Furthermore, we hypothesized that PSG would enable surgeons to obtain accurate and specific surgical windows for patients.

Materials and Methods

Ex vivo study

Specimens—Overall, 19 small and toy-breed canine cadavers were obtained for this study through donations after euthanasia at an animal shelter for reasons unrelated to the study. None of the dogs displayed abnormalities on radiographic examination. The cadavers were stored at –20 °C and thawed at room temperature for imaging and surgery.

Imaging and 3-D guides production—Skull CT (AlexionTM; Canon Medical Systems Corp) images of the dogs were obtained with a slice thickness of 1 mm, using bone filters with operating parameters of 120 kV and 12 mA. The DICOM images were imported to a computer image processing and modeling software (3-D Slicer 4.10).25 We segmented skulls without mandibles and created 3-D bone models using stereolithography files. Every process, from the analysis of bones to the production of PSGs, was performed using a computer-aided design software (3-DS Max; Autodesk). We measured the length of the pituitary fossa and the depth of the sphenoid bone. The location of the pituitary gland was assessed cranially or caudally to the hamular process, and distances between them were calculated on the sagittal images. We planned the trajectories for the intended burr in a software program using a cylinder function (Figure 1). All outcomes were assessed by a single investigator (YHR).

Figure 1
Figure 1

Representative images showing assessment and planning for transsphenoidal hypophysectomy using a patient-specific guide (PSG) in a dog on a 3-D computer program. A—The pituitary fossa was confirmed in a 3-D bone model with a horizontal cut of the head in a mixed-breed dog. B—The angle of the pituitary gland and the base of the maxilla were measured. C—The distance of the sphenoid bone to the pituitary gland fossa and its length were measured (blue arrow). The location of the pituitary fossa was compared with the hamular process. Cranial or caudal direction and the distance were measured (green arrow). D and E—The ventral and dorsal surfaces, respectively, of the PSG show the relationship with the mouth. F and G—Attachment of the bone model and PSG on sagittal and ventral planes, respectively, confirm the location of the pituitary gland fossa.

Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.09.0154

The PSGs were designed to accommodate a burr to create a hole in the pituitary fossa (Figure 2). These holes were planned at the center of the pituitary fossa. The aforementioned 3-D guides were designed to fit the anatomical features of maxillary molars. To ensure a precise and appropriate fit of the drill guide to the bone surface, the ventral surface was designed to represent an inverted virtual representation of the molars and the ventral surface of the sphenoid bone (Figure 1). The production time, that is the time required to complete the design of the 3-D guide in the program, was measured. We printed the bone model and PSGs using a 3-D printer (Style NEO-A22C; Cubicon) and polylactic acid filament (PLA filament; Cubicon). All models were made with the following resolution of print: layer height, 0.2 mm; wall line count, 2; top layers, 4; bottom layers, 4; nozzle size, 0.4 mm; infill density, 20%; infill overlap percentage, 15%; and build plate adhesion type, brim.

Figure 2
Figure 2

Representative images showing postoperative evaluation. A and B—The hole’s location on the ventral and dorsal plane, respectively, is shown for a mixed-breed dog. The cranial-caudal and left-right places were determined based on the pituitary fossa. C—The postoperative positions of the hole (pink) were recorded and compared to the preoperative position (black circle) on the dorsal plane.

Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.09.0154

Ex vivo surgery

This surgical technique was modified from previous reports.13,14,26 The 19 cadavers were thawed and positioned in sternal recumbency with an open mouth. The maxillary canine teeth were fixed with a rope to the holding bar, and the mandible was pulled downward.15,18 We incised the soft palate in the midline between the hamular processes. The PSG was manually placed on the molar and sphenoid bones (Figure 1), following the soft tissue dissection of the mucosa. A 2 mm diamond burr (Stryker Corp) was used to create a bicortical tract in the sphenoid bone. The surgery time was measured from the moment the PSGs were attached to the bone to the moment a hole was made using a burr. After penetrating the sphenoid bone, CT of the skull was performed using values identical to the preoperative set.

Assessment of burr tract accuracy

Triangulated mesh representations of the head were obtained from postoperative DICOM images. We used the postoperative 3-D skull model to analyze the accuracy of the bur tract corridors. Accuracy was then evaluated by measuring the deviation from the pituitary fossa, the trajectory of the burr tract, and the breach of the pituitary fossa in the modeling software. We recorded the divergence of holes as cranial-caudal and left-right at the center of the pituitary fossa (Figure 2). Breach of the pituitary fossa was defined as interruption of the skull base bone surrounding the pituitary fossa by the burr and graded as follows: grade 0, no breach; grade 1, 0-2 mm; grade 2, 2-4 mm; and grade 3, > 4 mm. All outcomes were assessed by a single investigator (YR). The calculated measurements are expressed as median (IQR).

In vivo study

Animals—This study was approved by the Institutional Animal Care and Use Committee of Chungnam National University (No. 202012A-CNU-196). Three purpose-bred healthy adult (3 to 4 years old) Beagles (2 females and 1 male) with a median weight of 9.2 kg (interquartile [25th to 75th percentile] range [IQR], 8.6 to 9.35 kg) were used in this study. All dogs (cases 1 through 3) underwent a thorough neurological and orthopedic examination to confirm the absence of any preexisting disease. They were individually housed in kennels (1.5 X 2 X 2.5 m) and fed with a commercially available maintenance diet.

3-D planning and printing—CT images were used to develop PSGs, and MRI was performed to confirm the limitation of the surgical window as follows: cavernous sinus, internal carotid artery, third ventricle, and communicating artery affecting the dimension of the pituitary gland. We performed MRI using a 1.5-T open magnet (Vantage Elan; Canon Medical Systems) and small coil and with dogs in sternal recumbency. Contiguous slices of the pituitary gland were obtained with a T2-weighted (T2W) 3-D FASE3-D sequence (flash, 3-D; time of repetition, 3500 msec; echo time, 352 msec; slab thickness, 1 mm; rectangular field of view, 144 X 144 mm) and magnetic resonance angiography (MRA) 3-D 8fc_WET sequence (flash, 3-D; time of repetition, 30 msec; echo time, 8 msec; slab thickness, 1 mm; rectangular field of view, 147 X 147 mm), without the use of contrast agents. Multiplanar reformation (MPR) was performed using a dedicated computer software (ZeTTA PACS; TaeYong Soft). Dorsal and transverse reconstruction were composed of sagittal series.

We assessed the shape and anatomy surrounding the pituitary gland with hyperintense signals. While the length of the pituitary gland was measured on CT, the width was measured between the edge of the cavernous sinus on MRI (Figure 3). We conducted preoperative 3-D planning based on the method applied in the ex vivo study to measure the anatomic landmark. The surgical windows in the shape of a rectangular box centering on the pilot hole (6 mm width and 8 mm length) were planned in the modeling software considering the insertion angle and size of the bur, shape of the pituitary gland fossa, and cavernous sinus. Using the PSG, pilot holes were planned to be positioned at the center of the pituitary gland. After marking the pilot holes with a 2-mm burr, the surgical window was expanded 4 mm cranially, 2 mm caudally, and 2 mm sideways. The bone model and PSGs were printed using the 3-D printer.

Figure 3
Figure 3

Images showing the plan on CT and MRI in a Beagle. A—The boundary of the cavernous sinus was determined as the horizontal length of the surgical window on magnetic resonance angiography (MRA). B—The length of the surgical window was determined on the bone model created through CT. C—The size and the angle of the hole (radius, 2 mm) entering the pituitary gland were determined. The dorsal view of head was horizontally cut.

Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.09.0154

Procedure—Three transsphenoidal surgeries were performed by veterinary surgeons (2 cases by HL and 1 case by YR) using PSGs similar to the ex vivo study. Each dog was positioned in sternal recumbency, and hair was clipped over the head. The hair around the mouth and head was removed, and the skin was disinfected using 10% iodine and 0.5% chlorhexidine, respectively. The dogs were stabilized with fluid therapy and premedicated with hydromorphone (0.1 mg/kg, IV) and midazolam (0.2 mg/kg, IV). General anesthesia was induced with propofol (4 mg/kg, IV) and maintained with 2% isoflurane in oxygen. For prophylaxis, cefazolin (22 mg/kg, IV) was administered at 90-minute intervals throughout the surgery. A 10-mm, 0°, rigid telescope with a high-definition camera system (Stryker Endoscopy, Stryker Corp) was used for magnifying the surgical site (Figure 4). The telescope was held in position by a mechanical endoscope holder fixed to the side rail of the surgical table.

Figure 4
Figure 4

Images showing the modified pilot hole technique with the PSG and rigid telescope in a Beagle. A—After incision, the basisphenoid bone was revealed. B—The PSG was roughly attached to the bone. C—The pilot hole was made with a bur, and the PSG was detached. D and E—The surgical window, which was planned on CT and MRI, was made using the size of the bur. F—The shape of the surgical window and surface of the pituitary gland are shown.

Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.09.0154

Following dissection of the soft tissue on the sphenoid bone, 2-mm pilot holes were created using PSGs. The surgical window was expanded to create rectangular windows. Surgery time was measured from the moment the PSGs were attached to the bone to the moment surgical windows were completed. Following the complete removal of the pituitary gland, CT and MRI were performed for postoperative assessment during anesthesia (Figure 5). Euthanasia was performed in all dogs during anesthesia after obtaining the images.

Assessment of the surgical windows—Necropsy was performed posteuthanasia. The postoperative surgical windows were assessed on necropsy images, 3-D skull models on a 3-D computer program, and MRI (Figure 5). The size, figure, and position of the surgical windows were evaluated by comparing the surgical plan and postoperative outcomes. Then, MRI was used to confirm the breach of the pituitary fossa. All results were assessed by a single investigator (YR).

Statistical analysis

In the ex vivo study, statistical analyses were carried out using the SPSS software version 24.0 (IBM Corp). Descriptive data (eg, median and IQR) were recorded for each outcome measure. The deviation of the holes and the angle difference between the preoperative plans and postoperative measurements were evaluated for normality using the Shapiro-Wilk test. The data were compared using Wilcoxon signed-rank test. Statistical significance was set at P < 0.05.

For the in vivo study, we performed an a priori power analysis using statistical software (G*Power V3.1.9.2x) to estimate the number of dogs required for the study. A sample size of 3 dogs was evaluated as follows: α = 0.05, power = 0.8, and estimated effect size = 1.0040748 (which was calculated using the mean and SD values of the location of the center of the surgical site created following TH in a pilot study and this ex vivo study14).

Results

Ex vivo study evaluation

The heads used in the ex vivo study had been obtained from cadavers of 7 Cocker Spaniels, 6 mixed-breed dogs, 3 Pomeranians, 1 Miniature Poodle, 1 Spitz, and 1 Maltese. All dogs were female (sexually intact), with a median weight of 6.25 kg (range, 1.7 to 8.5 kg), and a median body condition score of 4 (range, 1 to 9).

Perioperative measurements were summarized (Table 1). The pituitary fossa was located cranially from the hamular process in 1 of the 19 dogs. We identified 5 breaches; only grade 1 breach (0 to 2 mm) was observed, and the violations comprised partial penetration of the lateral limits of the pituitary fossa. However, the center of the bur was within the boundary of the fossa. Although the P values for deviation of the holes and the angle difference were < 0.05, there was no significant difference in surgical outcome.

Table 1

Perioperative measurements in the ex vivo (n = 19 cadaveric dog heads) and in vivo (3 healthy adult Beagles) studies.

Value, by study Preoperative Operative Postoperative
DHP (mm) DSB (mm) LPF (mm) PA (°) PT (min) ST (min) DH (min) Breach (grade) PAD (degree)
Ex vivo
Median 2.09 5.21 4.68 64.00 24.00 5.67 0.46 0.00 2.00
IQR 1.52–3.96 3.86–6.10 4.17–5.29 59–65 22.0–27.5 4.9–6.17 0–1.58 0–0.5 0–3.5
In vivo
Median 6.47 6.49 7.02 59.0 20.0 24.0
IQR 6.47–6.86 6.23–6.81 7.00–7.24 58–59.5 16–25 22.5–30

— = Not applicable. DH = Deviation of the hole. DHP = Distance from the hamular process to the pituitary fossa. DSB = Depth of the sphenoid bone. IQR = Interquartile (25th to 75th percentile) range. LPF = Length of the pituitary fossa. PA = Preoperative angle. PAD = Postoperative angle difference. PT = Production time. ST = Surgical time.

In vivo study evaluation

Preoperative values were measured on the 3-D bone model using a computer-aided design software (Table 1). We identified the location of the pituitary gland by considering the dorsum sellae, optic nerve, and internal carotid artery on dorsal MRA. The border of the cavernous sinus was determined on the dorsal and transverse images obtained by 3-D T2W and MRA. The preoperatively planned size of the surgical window in 3 dogs was 6 mm width and 8 mm length in the modeling software. All three dogs had satisfactory surgical windows, similar to those of the preoperative plan. The median postoperative size of the surgical window was 5.17 mm in width and 7.51 mm in length (7.07 and 7.51 mm for case 1, 5.01 and 7.13 mm for case 2, and 5.17 and 7.57 mm for case 3). There was no damage to the surrounding structures, including the cavernous sinus, optic nerve, and internal carotid artery on the dorsal and transverse images obtained by 3-D T2W and MRA (Figure 5).

Figure 5
Figure 5

Images showing the postoperative assessment of the surgical window and pituitary gland region in a live dog. A through C—The surgical window and path (red arrow) of case 1 to access the pituitary gland are identified in the axial, sagittal, and coronal MRA images, respectively. The gland was removed adequately without invasion to the surrounding vessels and venous sinus (blue arrow). D—Necropsy image of case 1 showing the resected pituitary fossa consistent with the surgical plan. E through G—Postoperative surgical windows displayed satisfactory surgical windows in the 3-D computer-aided design program in all 3 treated dogs.

Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.09.0154

Discussion

This study evaluated the applicability and accuracy of 3-D printed PSGs for transsphenoidal hypophysectomy in canine cadavers and 3 live Beagles. The 3D-PSG located the accurate position of the pilot hole, and there was no significant difference in determining the location and size of the surgical window between the planned and postoperative outcomes. Most of the holes were placed in the pituitary fossa in the ex vivo study, and the median deviation of the holes was 0.46 mm (IQR, 0 to 1.58 mm). The median difference between the pre- and postoperative entry angles was 2° (IQR, 0° to 3.5°). Therefore, the PSG guide allowed us to create the pilot hole in the sphenoid bone, exactly where it corresponded to the pituitary gland fossa. All postoperative surgical outcomes in the in vivo study were favorable. There was no significant difference in size of surgical windows between preoperative plan (6 mm in width and 8 mm in length) and postoperative assessment (median size, 5.17 mm and 7.51 mm). There was no invasion of the neurovascular structure encompassing the pituitary gland during surgery.

Identifying the surgical site is essential for TH because the surgery aims to remove small structures in the brain.13,14 Perioperative effects, such as edema, bleeding, and trauma from manipulation during surgery can lead to catastrophic consequences.12 The conventional method of locating the surgical site involves using the hamular process as a landmark.1315 However, the position of the pituitary gland in relation to the hamular process and the long axis distance of the pituitary fossa differ among dog breeds.13,14,18,26 In the ex vivo study, the location of the pituitary gland fossa differed among the dogs, and the median distance from the hamular process to the pituitary fossa was 2.09 mm (IQR, 1.52 to 3.96 mm).

Researchers have developed modified techniques to improve the localization of the pituitary fossa and visualization of the surgical site, including the pilot hole technique with a high-definition video telescope and neuronavigation system15,16; however, these methods have certain limitations. With the pilot hole technique, 2 holes should be created to designate the surgical window to improve accuracy.15,16 Calculating the exact distance between the holes and the hamular process during surgery requires expertise. In addition, it is inconvenient to perform CT during surgery. However, PSGs permit the placement of the surgical window on the preoperative plane without measuring the distance from the hamular process during surgery and creating additional holes. Moreover, the surgical time to fit the PSG with the bone was short (median, 24 minutes) in the present study. In neuronavigation systems, the surgical field can be limited by the frame or external fiducial markers in small-breed dogs.27 A previous study27 reported a median of 0.89 mm in the accuracy of applying frameless neuronavigation in dogs. Nonetheless, a change in posture during image acquisition and procedures can cause errors in localization.16,28 Variation in size, shape, and thickness of the skull conformation also makes the neuronavigation system application difficult. In contrast, PSGs are easily manipulated and can be created in small sizes for their application in small breed dogs.29 The accuracy can be maintained regardless of variations in skull conformation among breeds; therefore, PSGs can prevent the complicated procedure of TH.

An effective surgery without complications, including bleeding and edema, necessitates determining the morphology, size, and exact location of the pituitary gland.18 Surgery in the present study was directed toward the anterior lobe of the pituitary gland to obtain the maximum surgical window because the pituitary stalk of domestic animals is directed caudoventrally.18 In addition, we created the surgical windows considering the morphology of individuals, including the insertion angle to the sphenoid bone, the length and width of the pituitary fossa, and the neurovascular structures regardless of the position of the dog. This is because the surgical window should not invade major blood vessels, such as the cavernous sinus and internal carotid artery around the pituitary fossa.18 Thin-sliced 3-D gradient-echo MRI reportedly visualizes differentiation between the pituitary gland and surrounding structures.4 In the present study, MRA and 3-D T2W-MRI without contrast medium injection generated images with an improved definition of the border between the pituitary gland and surrounding structures, such as the cavernous sinuses. Therefore, the horizontal length of cavernous sinus measured on MRI was determined to be the horizontal length of the surgical window to obtain a safe and maximum surgical window. The surgery ended safely without important bleeding while securing the surgical windows, which were similar to the preoperative plans. The pituitary glands were removed entirely, and there was no invasive damage to the surrounding structure on the 3-D-T2 and MRA images. Therefore, the application of PSG resulted in accurate and safe surgical outcomes for TH.

The present study had some limitations. Press fit between a bone and PSG is warranted to reduce errors in localizing the surgical site.2022,3032 Slight deviation of the target during spinal surgery with PSGs can result in devastating consequences, such as canal penetration.20,22,30 Temporary K-wires could be inserted to prevent slipping during orthopedic surgeries; however, they cannot be applied in spinal and head surgery.33 Therefore, PSGs were held to press fit during the creating of the pilot hole. Further studies on more stable PSG designs are needed for stability and accuracy. Moreover, this study was not conducted in a patient with a pituitary gland tumor, which can lead to the altered location of surrounding structure including cavernous sinus and artery and excessive bleeding.6,8,12 Clear methods and criteria are needed to identify vascular structures around the pituitary gland on CT and MRI. We did not perform clinical follow-up, postoperative biochemical tests, or pituitary function tests. Despite the surgical accuracy observed in the ex vivo and in vivo studies, unexpected complications might occur in clinical patients.

Innovations in devices and techniques could modify the surgical strategy for TH in veterinary medicine. We demonstrated that PSGs provide the advantage of securing a more accurate location. The patient-specific surgical window for clear visualization of the pituitary gland provided safe and adequate tumor resection; therefore, excellent surgical outcomes are anticipated with the use of PSGs. The results can be used as a background for the application of PSGs in future clinical studies and other brain surgeries.

Acknowledgments

Author Contributions—Author 1: co-conceived the study, performed surgical procedures, data collection, interpretation of the results, manuscript preparation, critical review of the article, and approval of the final manuscript; Author 2: interpretation of the results, manuscript preparation, critical review of the article, and approval of the final manuscript; Author 3: interpretation of the results, manuscript preparation, critical review of the article, and approval of the final manuscript; Author 4: co-conceived the study, performed surgical procedures, data collection, interpretation of the results, manuscript preparation, critical review of the article, and approval of the final manuscript.

Funded by the National Research Foundation of Korea (grant No. NRF-2020R1A2C1101286).

The authors declare that there were no conflicts of interest.

References

  • 1.

    Snyder JM, Lipitz L, Skorupski KA, Shofer FS, Van Winkle TJ. Secondary intracranial neoplasia in the dog: 177 cases (1986–2003). J Vet Intern Med. 2008;22(1):172177. doi:10.1111/j.1939-1676.2007.0002.x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Snyder JM, Shofer FS, Van Winkle TJ, Massicotte C. Canine intracranial primary neoplasia: 173 cases (1986–2003). J Vet Intern Med. 2006;20(3):669675. doi:10.1892/0891-6640(2006)20[669:cipnc]2.0.co;2

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Tyson R, Graham JP, Bermingham E, Randall S, Berry CR. Dynamic computed tomography of the normal feline hypophysis cerebri (Glandula pituitaria). Vet Radiol Ultrasound. 2005;46(1):3338. doi:10.1111/j.1740-8261.2005.00006.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    van der Vlugt-Meijer RH, Meij BP, Voorhout G. Thin-slice three-dimensional gradient-echo magnetic resonance imaging of the pituitary gland in healthy dogs. Am J Vet Res. 2006;67(11):18651872. doi:10.2460/ajvr.67.11.1865

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Travetti O, White C, Labruyère J, Dunning M. Variation in the MRI appearance of the canine pituitary gland. Vet Radiol Ultrasound. 2021;62(2):199209. doi: 10.1111/vru.12938

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Owen TJ, Martin LG, Chen AV. Transsphenoidal surgery for pituitary tumors and other sellar masses. Vet Clin North Am Small Anim Pract. 2018;48(1):129151. doi:10.1016/j.cvsm.2017.08.006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    O’Neill DG, Scudder C, Faire JM, et al. Epidemiology of hyperadrenocorticism among 210,824 dogs attending primary-care veterinary practices in the UK from 2009 to 2014. J Small Anim Pract. 2016;57(7):365373. doi:10.1111/jsap.12523

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Van Rijn SJ, Galac S, Tryfonidou M, et al. The influence of pituitary size on outcome after transsphenoidal hypophysectomy in a large cohort of dogs with pituitary-dependent hypercortisolism. J Vet Intern Med. 2016;30(4):989995. doi:10.1111/jvim.14367

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Menchetti M, De Risio L, Galli G, et al. Neurological abnormalities in 97 dogs with detectable pituitary masses. Vet Q. 2019;39(1):5764. doi:10.1080/01652176.2019.1622819:

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Hara Y, Teshima T, Taoda T, et al. Efficacy of transsphenoidal surgery on endocrinological status and serum chemistry parameters in dogs with Cushing’s disease. J Vet Med Sci. 2010;72(4):397404. doi:10.1292/jvms.09-0367

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Van Asselt N, Christensen N, Meier V, et al. Definitive-intent intensity-modulated radiation therapy provides similar outcomes to those previously published for definitive-intent three-dimensional conformal radiation therapy in dogs with primary brain tumors: a multi-institutional retrospective study. Vet Radiol Ultrasound. 2020;61(4):481489. doi:10.1111/vru.12868

    • Search Google Scholar
    • Export Citation
  • 12.

    Weiss N, Gilad R, Post KD. Introduction and general neurosurgery. In: Youmans and Winn Neurological Surgery, 4-Volume Set. 4th ed: Oxford University Press; 2018:131132

    • Search Google Scholar
    • Export Citation
  • 13.

    Niebauer GW, Evans SM. Transsphenoidal hypophysectomy in the dog a new technique. Vet Surg. 1988;17:296303. doi:10.1111/j.1532-950x.1988.tb01021.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Meij BP, Voorhout G, Ingh TSVD, Hazewinkel HA, Van’t Verlaat JW. Transsphenoidal hypophysectomy in beagle dogs: evaluation of a microsurgical technique. Vet Surg. 1997;26(4):295309. doi:10.1111/j.1532-950x.1997.tb01502.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Mamelak AN, Owen TJ, Bruyette D. Transsphenoidal surgery using a high definition video telescope for pituitary adenomas in dogs with pituitary dependent hypercortisolism: methods and results. Vet Surg. 2014;43(4):369379. doi:10.1111/j.1532-950X.2014.12146.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Owen TJ, Chen AV, Frey S, Martin LG, Kalebaugh T. Transsphenoidal surgery: accuracy of an image-guided neuronavigation system to approach the pituitary fossa (sella turcica). Vet Surg. 2018;47(5):664671. doi:10.1111/vsu.12906

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Nadimi S, Molazem M, Jarolmasjed S, Nejad MRE. Volumetric evaluation of pituitary gland in dog and cat using computed tomography. Vet Res Forum. 2018;9(4):337341. doi:10.30466/vrf.2018.33073

    • Search Google Scholar
    • Export Citation
  • 18.

    Meij BP. Hypophysectomy as a treatment for canine and feline Cushing’s disease. Vet Clin North Am Small Anim Pract. 2001;31(5):10151041. doi:10.1016/s0195-5616(01)50011-x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Gao S, Stephens JD, Piatt C, et al. Overview of 3-D pringting in orthopaedics and 3-D printing in spinal surgery. In: Dipaola M, eds. 3-D Printing in Orthopaedic Surgery. Elsevier Health Sciences; 2018:85122

    • Search Google Scholar
    • Export Citation
  • 20.

    Hamilton-Bennett SE, Oxley B, Behr S. Accuracy of a patient-specific 3-D printed drill guide for placement of cervical transpedicular screws. Vet Surg. 2018;47(2):236242. doi:10.1111/vsu.12734

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Elford JH, Oxley B, Behr S. Accuracy of placement of pedicle screws in the thoracolumbar spine of dogs with spinal deformities with three-dimensionally printed patient-specific drill guides. Vet Surg. 2020;49(2):347353. doi:10.1111/vsu.13333

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Mariani CL, Zlotnick JA, Harrysson O, et al. Accuracy of three-dimensionally printed animal-specific drill guides for implant placement in canine thoracic vertebrae: a cadaveric study. Vet Surg. 2021;50(2):294302. doi:10.1111/vsu.13557

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Rho YH, Cho CW, Ryu CH, Lee JH, Jeong SM, Lee HB. Comparison between novice and experienced surgeons performing corrective osteotomy with patient-specific guides in dogs based on resulting position accuracy. Vet Sci. 2021;8(3):40. doi:10.3390/vetsci8030040

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Shinn R, Park C, DeBose K, Hsu F-C, Cecere T, Rossmeisl J. Feasibility and accuracy of 3-D printed patient-specific skull contoured brain biopsy guides. Vet Surg. 2021;50(5):933943. doi:10.1111/vsu.13641

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Fedorov A, Beichel R, Kalpathy-Cramer J, et al. 3-D Slicer as an image computing platform for the Quantitative Imaging Network. Magn Reson Imaging. 2012;30(9):13231341. doi:10.1016/j.mri.2012.05.001

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    van der Vlugt-Meijer RH, Voorhout G, Meij BP. Imaging of the pituitary gland in dogs with pituitary-dependent hyperadrenocorticism. Mol Cell Endocrinol. 2002;197(1-2):8187. doi:10.1016/s0303-7207(02)00282-4

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Wininger F. Neuronavigation in small animals: development, techniques, and applications. Vet Clin North Am Small Anim Pract. 2014;44(6):12351248. doi:10.1016/j.cvsm.2014.07.015

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Wang MN, Song ZJ. Classification and analysis of the errors in neuronavigation. Neurosurgery. 2011;68(4):11311143. doi:10.1227/NEU.0b013e318209cc45

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Leblond G, Gaitero L, Moens NM, et al. Canine atlantoaxial optimal safe implantation corridors–description and validation of a novel 3-D presurgical planning method using OsiriX™. BMC Vet Res. 2016;12(1):188. doi:10.1186/s12917-016-0824-3

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Chen H, Wu D, Yang H, et al. Clinical use of 3-D printing guide plate in posterior lumbar pedicle screw fixation. Med Sci Monit. 2015;21:39483954. doi:10.12659/MSM.895597

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Beer P, Park BH, Steffen F, Smolders DLA, Pozzi A, Knell SC. Influence of a customized three-dimensionally printed drill guide on the accuracy of pedicle screw placement in lumbosacral vertebrae: an ex vivo study. Vet Surg. 2020;49(5):977988. doi:10.1111/vsu.13417

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Fujioka T, Nakata K, Nishida H, et al. A novel patient-specific drill guide template for stabilization of thoracolumbar vertebrae of dogs: cadaveric study and clinical cases. Vet Surg. 2019;48(3):336342. doi:10.1111/vsu.13140

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Kaneyama S, Sugawara T, Sumi M. Safe and accurate midcervical pedicle screw insertion procedure with the patient-specific screw guide template system. Spine. 2015;40(6):E341E348. doi:10.1097/BRS.0000000000000772

    • Crossref
    • Search Google Scholar
    • Export Citation

Contributor Notes

Corresponding author: Dr. Lee (seatiger76@cnu.ac.kr)