Five dogs that ranged in age from 4 to 10 years (median age, 9 years) and weighed between 8.5 and 51.0 kg (18.7 and 112.2 lb) with undefined nasal masses were evaluated between 2012 and 2014 at the veterinary teaching hospital of Texas A&M University. All dogs had undergone CT of the head and nasal biopsy via a rostral rhinoscopic or unaided (blind) approach within the previous 3 weeks at the teaching hospital (2 dogs) or other referral hospitals (3 dogs). Clinical signs at evaluation included open-mouth breathing, sneezing, or unilateral epistaxis. Although the mass lesions identified via CT appeared extensive and had criteria of aggressive or malignant disease processes such as bone lysis, results of histologic evaluation of biopsy specimens suggested the nature of the lesions was inflammatory, necrotic, or hemorrhagic and those specimens were therefore believed to poorly represent the underlying disease processes.
Because of the discordance between imaging and biopsy results, a decision was made to collect additional biopsy specimens of nasal mass tissue by means of a frameless CTSBS in a manner similar to that reported for collection of brain biopsy specimens from dogs at our institution.1 For the procedure, each dog was anesthetized with an injectable agent, the choice of which was at the discretion of the attending anesthesiologist. An endotracheal tube was placed, and anesthesia was maintained by administration of an inhalant agent (isoflurane or sevoflurane).
In preparation for CT imaging, the head of each dog was secured to a custom-built stereotactic table with acrylic predrilled bite plates and thermoplastic puttya that conformed to the dentition of the dog (Figure 1). Six fiducial markers of various heights were secured to the bite plate. The head, from the nasal planum to the caudal aspect of the C2 vertebral body, was imaged with a 40-slice CT scanner,b with a slice thickness of 0.6 mm and interval (distance between 2 consecutive reconstructed images) of 0.3 mm (210 kV; 110 to 248 mA). Computed tomographic images were reconstructed in a bone algorithm in the transverse plane. The fiducialized CT images were imported into stereotactic softwarec installed on a diagnostic workstation. After image importation, a referenced image reconstruction was created.
After CT was finished and prior to transfer of dogs to the surgical suite, primary hemostasis was evaluated by measurement of buccal mucosa bleeding time with a 1.0 × 3.5-mm lancet device.d Results were considered unremarkable for all dogs (< 4 minutes and 30 seconds).2 Skin over the nasal passages and maxilla was shaved of hair, and a chlorhexidine solution was applied for preliminary antisepsis. Cefazolin (22 mg/kg [10 mg/lb], IV) was administered before the CTSBS procedure and then every 2 hours until the procedure was over. Each dog was moved to the surgical suite and positioned in front of an infrared camera.c
A digital reference frame was attached to the CT head holder, and fiducial markers affixed to the bite plate were electronically registered into the CTSBS by use of a standard probe with reflective spheres (Figure 1). The surgical field was draped in a standard fashion. A 2-mm biopsy rongeure with attached reflective spheres was electronically registered into the system. Registration of the biopsy rongeur allowed the clinician to identify the location of the instrument in relation to the nasal lesion as well as to plan the skin incision site and biopsy trajectory. An approximately 1-cm incision was made through the skin and subcutaneous tissues with a No. 11 scalpel blade to expose the underlying bone. The periosteum was reflected with periosteal elevators. Biopsy site and trajectory were established by placement of the registered biopsy rongeur on the nasal bone, with concurrent examination of the CT reconstruction (Figure 2). Biopsy site was chosen on the basis of mass extent, with care to avoid critical structures (eg, vessels or cribriform plate). A 3-mm burr hole was drilled with a pneumatic bone drill through the exposed nasal or maxillary bone. Multiple specimens of mass tissue were collected through the single created burr hole with the registered biopsy rongeur in a freehand manner while the rongeur trajectory was visually monitored via the stereotactic software. A modified geological core biopsy technique was used, in which specimens were collected from the near edge, center, and distant edge of the mass; for all dogs, at least 2 core specimens were obtained by altering rongeur trajectory through the burr.3 Factors including sizes of the mass and nasal passages, proximity of the mass to vital structures, and intraoperative evaluation of cytologic results influenced whether > 2 core specimens were obtained.
Biopsy specimens were placed in 10% formalin solution and submitted for histologic evaluation. When intraoperative cytologic findings suggested the presence of neutrophilic or pyogranulomatous inflammation (2 dogs), specimens were also prepared for bacterial and fungal culture. Hemorrhage from the burr hole was controlled with suction. Bone wax was placed in the burr hole to create a seal between the nasal cavity and subcutaneous tissues to prevent subcutaneous emphysema. The subcutaneous tissues and skin over the burr hole were closed in a routine manner. Various opiates were administered IV for immediate postoperative pain relief. Tramadol (2 to 4 mg/kg [0.9 to 1.8 mg/lb], PO, q 8 h for 7 days) was provided for at-home pain control.
Median duration of imaging for the CTSBS procedure was 35 minutes (range, 15 to 40 minutes), which included the time required for transportation from the anesthesia suite to the imaging center, acquisition of CT scans, and transportation to the surgical suite. Mass lesions were identified in all 5 dogs, with 4 dogs having a unilateral lesion and 1 having a bilateral lesion. Four dogs had a lesion at the caudal aspect of the nasal cavity, and 1 dog had a lesion at the rostral to mid aspect of the nasal cavity. Invasion of the cribriform plate was detected in 2 dogs, and 1 of those dogs also had invasion into the maxillary recess and frontal sinus.
Biopsy specimen collection, including surgical site preparation, electronic patient registration, draping, electronic instrument registration, and the actual biopsy procedure, required a median of 55 minutes (range, 38 to 84 minutes). A median of 8 biopsy specimens was collected per dog (range, 6 to 14). A board-certified clinical pathologist examined impression smears of biopsy specimens during the CTSBS procedure. If results of cytologic evaluation suggested that the biopsy specimens collected were of diagnostic quality, then specimen collection was suspended. Size of biopsy specimen varied depending on the friable nature of the mass; most specimens were approximately 3 × 2 × 1 mm, and the largest collected was 1 × 1 × 15 mm. Blood loss was estimated at < 10 mL for all dogs. Median total anesthetic duration was 285 minutes (range, 135 to 315 minutes).
All dogs were discharged from the hospital within 24 hours after the CTSBS procedure. Postoperative hemorrhage and emphysema were not reported, and all skin incisions healed without complication.
Histologic evaluation of biopsy specimens from 3 of the 5 dogs revealed findings suggestive of malignant neoplasia (Table 1). For 1 dog, CTSBS results suggested a mild mixed inflammatory response, whereas initial biopsy results suggested lymphoplasmacytic inflammation. However, the prebiopsy CT scan had revealed a large aggressive nasal mass involving the left and right nasal cavities that extended into the right maxillary recess and frontal sinus of that dog. Severe lysis of the right maxillary bone was also evident. No postbiopsy CT scan was performed on the area from which the biopsy specimen was collected.
Clinical findings associated with nasal masses in 5 dogs that underwent CT evaluation of the head and nasal biopsy via a rostral rhinoscopic or unaided (blind) approach, followed 3 weeks later by a CTSBS procedure.
Dog | CT results | Initial biopsy results | CTSBS collection site | CTSBS results |
---|---|---|---|---|
1 | 23 × 19 × 43-mm soft tissue mass in the left nasal cavity, with destruction of the cribriform plate | Neutrophilic inflammation | Dorsal midline region over caudal portion of nasal bone | Hemangiopericytoma |
2 | 33 × 28 × 92-mm soft tissue mass occupying the right nasal cavity, with extension into the right frontal sinus; cribriform plate involvement suspected | Inflamed granulation tissue or an inflamed vascular tumor (first biopsy procedure); necrosis (second biopsy procedure) | Right dorsal paramedian region over caudal maxillary bone | Undifferentiated sarcoma |
3 | 44 × 27 × 82-mm space-occupying soft tissue mass occupying most of the right nasal cavity | Lymphoplasmacytic and eosinophilic inflammation | Right dorsal paramedian region over caudal maxillary bone | Chondrosarcoma |
4 | 18 × 34 × 61-mm bilateral soft tissue mass of entire nasal cavity (worse on right), with facial bone lysis | Lymphoplasmacytic inflammation | Right dorsal paramedian region over caudal maxillary bone | Mild mixed-cell inflammation |
5 | 18 × 23 × 36-mm soft tissue mass of the right caudal nasal cavity | Vascular hamartoma | Right dorsal paramedian region over caudal maxillary bone | Vascular hamartoma |
In another dog, 2 masses were identified. The most rostrally located mass was situated at the nasal planum and was diagnosed by the referring veterinarian as squamous cell carcinoma on the basis of results of cytologic evaluation. A second and larger mass was identified incidentally on CT scan and was associated with the ventral mid to caudal aspect of the right nasal passage. Focal turbinate destruction was identified in the region of the second mass; however, there was no evidence of maxillary bone destruction. The referring veterinarian had obtained a biopsy specimen of this second mass via a rostral rhinoscopic approach. Malignant neoplasia was not identified as a result of this initial biopsy. Histologic findings for the initial biopsy specimen suggested a vascular hamartoma or arterial-venous nevus, and subsequent use of the CTSBS confirmed this diagnosis for the second mass. For the dog with hamartoma, a CT scan of the nasal cavity was performed 2 weeks after the CTSBS procedure was performed. That CT scan revealed that the biopsy specimens collected via CTSBS guidance had been collected directly from the center of the second mass (Figure 3). This dog was the only patient in which a postoperative CT scan was performed.
Discussion
Chronic nasosinal disease is common in dogs.4 Clinical signs include sneezing, nasal discharge, obstruction, epistaxis, and facial deformity. Underlying etiologies include lodged foreign material, mite infestation, fungal infection, lymphoplasmacytic rhinitis, and neoplasia. Diagnostic options include imaging (radiography, CT, and MRI) and collection of a biopsy specimen from the nasal passages or sinuses.
Reported diagnostic yield associated with etiologic evaluation of nasal disease in dogs is variable, ranging from 64% to 91%.5,6 Traditional methods for collection of nasal biopsy specimens include blind collection via a rostral approach, endoscopic collection via a rostral or retroflexed approach, nasal hydropulsion, or open rhinotomy.4,7,8 Specimens collected blindly may not reflect the disease process, and hemorrhage may limit the collection of representative biopsy specimens via a rhinoscopic approach. Although specimens obtained with nasal hydropulsion can be large, not all tumors can be dislodged in this manner, and complications may arise if the cribriform plate lacks integrity. When specimens with insufficient quality for diagnosis are obtained via rhinoscopy or blind nasal biopsy, open rhinotomy is traditionally considered as a next step to obtain high-quality specimens.
Open rhinotomy is able to provide large, good-quality biopsy specimens; however, complications are common.9–11 During the procedure, a section of bone is removed to provide access to the nasal cavity. If postoperative radiation therapy is a possibility, then the bony window is not replaced and the opening to the nasal passage is closed only with the overlying skin. Therefore, air from the nasal passage frequently causes subcutaneous emphysema. In addition to subcutaneous emphysema, hemorrhage is a common complication following open rhinotomy. Nasal turbinates are well vascularized, and removal of large pieces of nasal turbinates to access and collect specimens from a mass is likely to result in postoperative hemorrhage. In some dogs, the nasal cavity is packed with gauze and remains packed for 12 to 24 hours to provide hemostasis. Complications of subcutaneous emphysema and postoperative hemorrhage were not reported and no postoperative treatment or intraoperative packing was necessary in the dogs of the present report.
In some dogs, focal lesions are located in more caudal aspects of the nasal passages, limiting the feasibility of traditional methods for biopsy specimen collection. Additionally, hemorrhage or inflammation related to tumor growth may limit the diagnostic yield of specimens collected in a manner that precludes direct visibility of the mass. Failure to obtain a definitive diagnosis for a dog with neoplastic disease may delay the delivery of appropriate treatment and impact patient outcome.
Stereotactic biopsy techniques were first described almost 100 years ago.12 In essence, stereotactic surgery involves first mapping the anatomic area of interest in a 3-D coordinate system. With an MRI or CT scan and a 3-D computer workstation, surgeons can accurately target the anatomic area of interest in stereotactic space. Historically, in human medicine, frame-based stereotactic systems were routinely used to facilitate mass removal and biopsy in the nasal sinuses.13,14 More recently, frameless stereotactic technologies have been developed.15–18 These systems involve fiducial markers, 3-D image sets, and infrared cameras to permit intraoperative lesion localization. Compared with frame-based systems, frameless technology likely enhances patient comfort because bone-grasping head holders are not required. Frameless systems also allow for better adaption to the various canine skull shapes and unobstructed access for surgical biopsy.1
Although use of a CTSBS for collection of intracranial tissue from dogs reportedly results in diagnostic yields > 90% and few adverse events,19–21 the present report is the first in which a CTSBS was used within the nasal passages of dogs with mass lesions. Two cadaver studies1,22 have demonstrated the Pythagorean application accuracy of frameless stereotactic biopsy in brains of dogs; mean needle placement error ranged from 0.9 to 2.9 mm. This technology permitted collection of diagnostically high-yield biopsy specimens from 4 of 5 dogs of the present report that had previously undergone traditional rhinoscopic biopsy procedures. A definitive diagnosis of malignant neoplasia was established for 3 of these 4 dogs in which a definitive diagnosis was obtained (Table 1), permitting determination of appropriate treatment plans and establishment of valuable prognostic information.
In 1 dog of the present report, histopathologic findings for biopsy specimens obtained via the CTSBS did not match the clinical signs and results of advanced imaging. This dog had an extensive, bilateral, caudally located nasal mass, with evidence of bony destruction on CT. The lesion identified via CT likely included both a true neoplasm and a substantial amount of adjacent inflammation or hemorrhage. It may be prudent to select ≥ 2 sites for biopsy specimen collection from dogs with apparently extensive disease to avoid this limitation. This dog was one of the smaller dogs that underwent biopsy, and patient size may have had an impact on outcome. Also, user error could have affected the accuracy of specimen collection. Examples of user errors include disturbance of the digital reference frame during or following the electronic registration process, patient movement within the frameless head positioner following imaging or registration, failure to tightly secure reflective spheres to the biopsy instrument, or lack of surgeon ability to target lesions on the basis of 3-D computer reconstructions.1 The dog of the present report received palliative radiation therapy for the suspected neoplastic nasal mass, with a progression-free interval of ≥ 8 months.
For another dog of the present report, histologic findings obtained via the CTSBS (hamartoma) matched those of the biopsy specimens obtained rhinoscopically. Loss of typical healthy architecture adjacent to the mass and malignant neoplasia was suspected. Benign disease was detected when the CTSBS was used (Table 1). In this situation, a CT scan was performed 2 weeks after the CTSBS procedure, revealing that biopsy specimens had been collected from the central portion of the lesion. On the basis of those findings, periodic monitoring of the mass via CT scan but no further treatment was recommended. Squamous cell carcinoma of the nasal planum was treated with 5 fractions of neoadjuvant radiation therapy, followed by nasal planectomy. Results of subsequent histologic evaluation revealed that surgical margins were tumor free. This particular dog has received no additional imaging, and no clinical signs attributable to the hamartoma have been reported.
None of the 5 dogs of the present report developed any major complications related to the CTSBS procedure, suggesting that use of a CTSBS was a safe technique for collection of nasal biopsy specimens. Hemorrhage was minimal, and all incisions healed in the expected manner. The degree of postprocedural pain appeared to be mild and was easily managed with opiate administration.
The findings reported here pertained to only 5 dogs, and research is needed to determine the impact of patient size, lesion location, or nasal conformation on the clinical usefulness of a CTSBS for dogs with nasal tumors and other types of spontaneous nasal disease. However, biopsy specimens were safely collected during a CTSBS procedure from masses within the nasal and sinus passages of the dogs of the present report. The CTSBS described should be considered for use in situations in which other less equipment-intensive methods have failed to facilitate a definitive diagnosis. The CTSBS may be a more suitable first choice than traditional methods if a mass is identified in the caudal portion of the nasal cavity or the nasal sinuses.
ABBREVIATIONS
CTSBS | Computed tomography–guided stereotactic biopsy system |
Footnotes
VP Mix, Henry Schein Inc, Melville, NY.
Siemens Somatom Definition AS, Siemens, Malvern, Pa.
Radionics OmniSight EXcell, Integra Radionics, Burlington, Mass.
Surgicutt Junior, ITC, Edison, NJ.
2-mm cup 6-inch Grasping & Biopsy Roungeur, Sontec Instruments, Centennial, Colo.
References
1. Taylor AR, Cohen ND, Fletcher S, et al. Application and machine accuracy of a new frameless computed tomography-guided stereotactic brain biopsy system in dogs. Vet Radiol Ultrasound 2013; 54: 332–342.
2. Forsyth LT, Willis SE. Evaluating oral mucosa bleeding times in healthy dogs using a spring-loaded device. Can Vet J 1989; 30: 344–345.
3. Owen CM, Linskey ME. Frame-based stereotaxy in a frameless era: current capabilities, relative role, and the positive- and negative predictive values of blood through the needle. J Neurooncol 2009; 93: 139–149.
4. Cohn LA. Canine nasal disease. Vet Clin North Am Small Anim Pract 2013; 44: 75–89.
5. Meler E, Dunn M, Lecuyer M. A retrospective study of canine persistent nasal disease: 80 cases (1998–2003). Can Vet J 2008; 49: 71–76.
6. Tasker S, Knottenbelt CM, Munro EAC, et al. Aetiology and diagnosis of persistent nasal disease in the dog: a retrospective study of 42 cases. J Small Anim Pract 1999; 40: 473–478.
7. Ashbaugh EA, McKiernan BC, Miller CJ, et al. Nasal hydropulsion: a novel tumor biopsy technique. J Am Anim Hosp Assoc 2011; 47: 312–316.
8. Pietra M, Spinella G, Pasquali F, et al. Clinical findings, rhinoscopy and histological evaluation of 54 dogs with chronic nasal disease. J Vet Sci 2010; 11: 249–255.
9. Withrow SJ. Tumors of the respiratory system. In: Vail SJ, Vail DM, Page RL, eds. Withrow & MacEwen's small animal clinical oncology. 4th ed. St Louis: WB Saunders Co, 2007;511–539.
10. Malinowski C. Canine and feline nasal neoplasia. Clin Tech Small Anim Pract 2006; 21: 89–94. 21.
11. Moores A, Walker D. Canine nasal disease: investigation and management. In Pract 2013; 35: 197–211.
12. Gildenberg PL. The history of stereotactic neurosurgery. Neurosurg Clin N Am 1990; 1: 765–780.
13. Rosenfeld JV, Wallace D, Klug GL, et al. Transnasal stereotactic biopsy of a clivus tumor. Technical note. J Neurosurg 1992; 76: 878–879.
14. Metyolkina L, Peresedov V. Transnasal stereotactic surgery of pituitary adenomas concomitant with acromegaly. Stereotact Funct Neurosurg 1995; 65: 184–186.
15. Koele W, Stammberger H, Lackner A, et al. Image guided surgery of paranasal sinuses and anterior skull base—five years experience with the InstaTrak-System. Rhinology 2002; 40: 1–9.
16. Tabaee A, Kacker A, Kassenoff TL, et al. Outcome of computer-assisted sinus surgery: a 5-year study. Am J Rhinol 2003; 17: 291–297.
17. Wise SK, DelGaudio JM. Computer-aided surgery of the paranasal sinuses and skull base. Expert Rev Med Devices 2005; 2: 395–408.
18. Fried MP, Morrison PR. Computer-augmented endoscopic sinus surgery. Otolaryngol Clin North Am 1998; 31: 331–340.
19. Moissonnier P, Blot S, Devauchelle P, et al. Stereotactic CT-guided brain biopsy in the dog. J Small Anim Pract 2002; 43: 115–123.
20. Koblik PD, LeCouteur RA, Higgins RJ, et al. CT-guided brain biopsy using a modified Pelorus Mark III stereotactic system: experience with 50 dogs. Vet Radiol Ultrasound 1999; 40: 434–440.
21. Clark AC, Lopez FR, Levine JM, et al. Intracranial migration of Eucoleus (Capillaria) boehmi in a dog. J Small Anim Pract 2013; 54: 99–103.
22. Troxel MT, Vite CH. CT-guided stereotactic brain biopsy using the Kopf stereotactic system. Vet Radiol Ultrasound 2008; 49: 438–443.