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.3–5 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.13–16 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 studies13–16 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.20–22 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).
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.
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.
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.
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.
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).
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.13–15 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.20–22,30–32 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
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