Figures and Tables. Citations Publications citing this paper. Victor Razafindranaly , E. Comparison of 3D C-arm-based registration to conventional pair-point registration regarding navigation accuracy in ENT surgery. Intraoperative imaging of the shoulder: A comparison of two- and three-dimensional imaging techniques. Eduardo M.
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References Publications referenced by this paper. Image-guided and computer-aided surgery in otology and neurotology: is there already a need for it?
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Thomas Lenarz , Ralf Heermann. Cone-beam computed tomography on a mobile C-arm: novel intraoperative imaging technology for guidance of head and neck surgery. Yvonne Y. Chan , Jeffrey H. Cone - beam CT on a mobile Carm : A novel intraoperative imaging technology for guidance of head and neck surgery. Design, analysis and simulation for development of the first clinical micro-CT scanner. In vitro assessment of image-guided otologic surgery: submillimeter accuracy within the region of the temporal bone.
Robert F. Labadie , Rohan J. The accuracy of computer-aided surgery in neurotologic approaches to the temporal bone: a cadaver study. Buchman , Harold C. Volume CT with a flat-panel detector on a mobile, isocentric C-arm: pre-clinical investigation in guidance of minimally invasive surgery. The panoramic image of rabbit 9 A,B shows symmetric incisor malocclusion white arrows and asymmetric premolar and molar teeth malocclusion with sharp dental points and coronal tooth elongation open arrow.
The left maxilla and mandible show apical tooth elongation, severe malangulation of the reserve crowns of the maxillary first and second molar teeth white arrow heads , and regional moth-eaten osteolysis of the alveolar bone of the maxilla. The panoramic image of rabbit 2 C,D depicts an asymmetric premolar and molar malocclusion secondary to a supernumerary right mandibular third premolar tooth with associated apical elongation and periodontal ligament space widening white arrow head.
Additionally, there is coronal elongation and a sharp dental point of the rostral most tooth white arrow. Table 2. P -values of categories detectable on the oral examination and physical examination row headers and categories detectable on cone beam computed tomography column headers. Other findings included gas opacities within the soft tissue or bone in 3 of 15 rabbits Figure 3. Twelve rabbits had gas opacities near the medial canthus of the eyes, corresponding to the entrance of the nasolacrimal duct and gas trapped under the eyelids.
Three rabbits had mineralization of the ventral nasal concha. Figure 3. Cone beam computed tomography soft tissue evaluation. A Right panoramic image of rabbit 5 showing normal incisor, premolar, and molar occlusion. Transverse image immediately rostral to the globe B and median sagittal multiplanar image C of the same rabbit showing soft tissue submandibular swelling, right-sided periocular swelling and chemosis of the nictitating membrane dotted line.
Gas opacities are present in the submandibular region and retrobulbar space open arrows and within the right maxillary first molar germinal center white arrow head. Thirteen rabbits had ventral mandibular border changes that could potentially be palpated on physical examination based on CBCT imaging. All but one rabbit had evidence of periodontal ligament space widening. Three of these 14 rabbits only had periodontal ligament space widening, whereas the other 11 also had periapical lucencies. Of the 11 rabbits with periodontal ligament space widening and periapical lucencies, nine of them also had a pattern of moth-eaten osteolysis of the alveolar bone Figure 4.
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Figure 4. Mild, moderate, and severe periodontal ligament space widening. Dorsal multiplanar MPR left column and sagittal MPR right column cone beam computed tomography images of rabbits with multiple teeth exhibiting varying degrees of periodontal ligament space widening. A,B In rabbit 8, periodontitis of the left maxillary third molar tooth is visible as subtle periodontal ligament space widening white arrows. C,D In rabbit 1, periodontitis has progressed at the left mandibular first molar tooth from widening of the periodontal ligament space white arrows to formation of periapical lucency open arrow.
E,F In rabbit 7, periodontal ligament space widening of multiple teeth white arrow is contiguous with the periapical lucency and pattern of moth-eaten osteolysis open arrow. Expansion and osteolysis of the alveolar bone is evident in this rabbit. All nine rabbits with a pattern of moth-eaten osteolysis of the alveolar bone also had inflammatory tooth resorption Figure 5. An additional three rabbits had inflammatory tooth resorption without moth-eaten osteolysis of the alveolar bone.
Two of these rabbits had periodontal ligament space widening and periapical lucencies, whereas the remaining one rabbit only had periodontal ligament space widening. Of the 12 total rabbits with inflammatory tooth root resorption, six of them had such severe resorption that the teeth fragmented. Three of the 15 rabbits had true tooth fractures. Eight of the 15 rabbits already had missing teeth. Figure 5. Inflammatory tooth resorption. A Irregular margins and lucency indicative of resorption of the right maxillary first molar tooth white arrow. A normal tooth that is not fully within the plane of the image open arrow can appear lucent and irregular as though it has resorption due to volume average artifact.
Similarly, if the teeth are angled, the transverse image may show the clinical crown of one tooth, but the reserve crown of an adjacent tooth white arrow head , creating the artifactual appearance of tooth resorption or fragmentation. B Tooth resorption may be more evident on dorsal multiplanar images white arrow.
C,D In these panoramic images of rabbit 11, tooth resorption is severely affecting the right premolar and molar teeth, but not the left. Additionally, there is elongation of the right maxillary premolar and molar teeth with resorption of the third premolar tooth open arrow head. Increased opacity is visible superimposed on the apices of the right maxillary first and second molars open arrow due to elongation and malangulation of the reserve crowns. Mineralization of the left nasal cavity white arrow was an incidental finding. The present study is the first to demonstrate the feasibility and yield of CBCT in evaluating maxillofacial features and dentition in rabbits with dental disease.
The results of this study support our hypothesis that CBCT will detect dental pathology that cannot be observed or predicted by physical and oral examinations alone. Additionally, abnormalities detected on physical and oral examinations are not necessarily associated with the presence of dental abnormalities, such as periodontal ligament space widening, periapical lucencies, moth-eaten osteolysis of the alveolar bone, or inflammatory tooth resorption that will influence the choice of treatment.
Therefore, advanced imaging is required when dental disease is suspected to fully characterize the extent and nature of the dental pathology and inform appropriate therapy. Widening of the periodontal ligament can progress to periapical lucency and then to a pattern of moth-eaten osteolysis of the alveolar bone. There was a relatively even distribution of rabbits with mild four rabbits , moderate five rabbits , and severe dental disease six rabbits. The known duration of the dental disease did not necessarily match the severity of the dental disease.
For example, rabbits 12 and 14 had severe dental disease, but the duration of known clinical signs was 3. Thus, it is likely that rabbits with severe or moderate dental disease, and short duration of clinical signs, may have had dental disease for longer than the duration clinical signs were noticed by the client. Incisor malocclusion is more visually evident to the client, but it is important for the veterinarian to also evaluate the premolar and molar teeth when performing an oral evaluation.
The current literature states that incisor malocclusion is common in pet rabbits and that incisor malocclusion without premolar and molar abnormalities may be relatively rare, especially in older rabbits 4 , Only one rabbit had incisor malocclusion in the absence of premolar and molar malocclusion. Previous literature supports that if incisor malocclusion occurs as an isolated entity at an early age, it is probably due to maxillary brachygnathia, which has a genetic origin 4 , 18 — The one rabbit with isolated incisor malocclusion was a 3.
She was one of the four youngest rabbits in this study, which may indicate that her incisor malocclusion was genetic in origin, but evaluation of her CBCT scan does not show maxillary brachygnathia. Malocclusion and fracture of the right maxillary first incisor tooth may have been secondary to trauma or iatrogenic trauma associated with incisor trimming, as she was not reported to have incisor malocclusion in the years previous. There were 10 rabbits with premolar and molar malocclusion that did not have incisor malocclusion. Once explanation of this finding is that these rabbits were having incisor trimmings without proper premolar and molar adjustments, thereby skewing our data.
In contrast, the current literature states that incisor malocclusion may be secondary to, or occur concomitantly with, premolar and molar malocclusion. Additionally, incisor malocclusion that prevents normal mastication may lead to premolar and molar malocclusion It is also possible that cases presenting to the VMTH and the relatively small number of rabbits included in this study may not be representative of the larger population of rabbits presenting to general practitioners for dental maintenance.
However, our results emphasize the importance of performing a full oral examination on a regular basis. The CBCT evaluation of the rabbits in this study demonstrated that oral examination alone is not enough to fully diagnose dental disease. The panoramic image of rabbit 10 Figures 1 A,B demonstrates how incisor, premolar, and molar occlusion can appear normal, but dental pathology can be present including severe apical elongation, a missing tooth, inflammatory tooth resorption, and moth-eaten pattern of osteolysis of the alveolar bone.
The transverse image of rabbit 10 shows a normal 10 occlusal angle on the right and a flat occlusal angle on the left Figure 1 C. This subtle change in occlusal angulation could easily be missed on conscious oral examination. When occlusal angle and dental charting are normal, subtle changes to the dentition can only be detected with advanced imaging. It is established in the literature that some form of imaging should be performed in rabbits with dental disease 1 , 4 , 8 — 11 ; however, this is the first study to recommend the use of CBCT.
In feline and canine patients, the diagnostic yield of full-mouth dental radiography has been quantified 21 , 22 , but this has not yet been performed in rabbits with skull radiography or CT. Our study compared CBCT findings that could be detected on conscious oral examination vs. Except for the association between coronal and apical tooth elongation, our results indicate that oral examination findings are poor indicators of additional dental pathology and that diagnostic imaging, such as CBCT, is an essential part of fully characterizing dental disease in rabbits.
Our group has separately found CBCT to be superior to conventional CT for evaluation of normal dentition in rabbits 12 and direct comparison of the diagnostic yield of oral endoscopy, skull radiographs, conventional CT, and CBCT should be the basis of future studies investigating rabbit dental disease.
Overall, it is important to perform diagnostic imaging in rabbits suspected to have dental disease, despite a normal oral examination. Malocclusion may be symmetric or asymmetric and the clinical signs may not fully represent the severity of the disease. For instance, rabbit 9 was reported by the client to be eating well and healthy overall but the panoramic image revealed symmetric incisor malocclusion and asymmetric premolar and molar malocclusion Figures 2 A,B.
The left maxilla and mandible show apical tooth elongation, coronal tooth elongation, and moth-eaten osteolysis of the alveolar bone. In contrast, rabbit 2 had relatively mild dental disease but severe clinical signs including decreased fecal output, gastrointestinal stasis, ptyalism, and anorexia. The panoramic image of rabbit 2 depicts an asymmetric premolar and molar malocclusion secondary to a supernumerary right mandibular third premolar tooth Figures 2 C,D.
The severity of the apical elongation and the palpable changes to the right ventral mandibular border indicate that this had been a chronic problem, despite the acute nature of the clinical signs. The discrepancy between severity of clinical signs and the extent of underlying dental disease suggests that diagnostic imaging is indicated even for patients with mild clinical signs. Sharp dental points are an important clinical problem in rabbits and can lead to buccal and lingual ulcers 4 , 8 , 9.
We found the evaluation of dental points via CBCT to be difficult, because all maxillary premolar and molar teeth have slightly pointed buccal aspects and mandibular premolar and molar teeth have slightly pointed lingual aspects due to the natural wear of the teeth associated with anisognathism. Although we report 12 of 15 rabbits as having CBCT evidence of sharp dental points, there was poor agreement between CBCT findings and oral examination findings with respect to the presence of sharp dental points.
One limitation of our study is that several different clinicians performed oral examinations for the rabbits in this study, and reporting of sharp dental points was not standardized. Variation in the reporting of dental points by different clinicians may have contributed to the poor agreement between CBCT and oral examination for detecting dental points, but it is important to consider that CBCT may be limited in its ability to accurately detect potentially significant dental points. For example, the right panoramic image of rabbit 5 shows normal incisor and premolar and molar occlusion Figure 3 A , whereas the sagittal MPR Figure 3 B and transverse images Figure 3 C reveal the submandibular swelling, right-sided periocular swelling and chemosis of the nictitating membrane, and gas opacities in the submandibular region, retrobulbar space, and right maxillary first molar germinal center.
CBCT scan is optimized to image the osseous maxillofacial features rather than the soft tissue, but evaluation of the soft tissue is still possible.
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Despite the poorer contrast resolution of CBCT compared to conventional CT, contrast enhancement of small blood vessels in an experimentally induced lesion can be detected following intravenous iodinated contrast administration in rabbits The utility of contrast administration for CBCT of clinical rabbit patients with naturally occurring disease has not yet been described. The improved spatial resolution of CBCT compared to conventional CT may enhance visualization of small, strongly contrast-enhancing lesions and normal structures such as blood vessels, but subtle contrast enhancement may not be detected by CBCT.
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One example of subtle findings identifiable on CBCT images is change to the periodontal ligament space. The periodontal ligament should not be evaluated on 3D reconstruction or panoramic images, as previously discussed in part one Periodontitis starts with the inflammation, infection, and widening of the periodontal ligament and loss of the adjacent alveolar bone 5.
Figure 4 demonstrates the spectrum of periodontal ligament space changes observed in this study, from subtle periodontal ligament space widening Figures 4 A,B , to periapical lucency suggestive of abscessation Figures 4 C,D , to osteolysis and expansion of the alveolar bone Figures 4 E,F.
Periapical abscessation and expansion of the alveolar bone can be palpated as a contour change to the ventral mandibular border or present as exophthalmia with decreased ocular retropulsion 24 , and detection of these changes on physical examination provide indications that further evaluation of the dentition is necessary. In areas with loss of alveolar bone secondary to inflammatory conditions such as periodontitis and abscessation, loss of dental substance can occur in the form of inflammatory tooth resorption.
Tooth resorption can be difficult to evaluate solely from transverse images, because a tooth that is not fully within the plane of the image can appear as though it is partially resorbed Figure 5 A. Worsening inflammatory resorption can cause tooth fragmentation, making extraction difficult. Pre-extraction evaluation of the teeth with CBCT can alert the practitioner to the presence of fragments that may complicate extraction.
Previous studies showed preference for the use of transverse CT images for the diagnosis of dental pathology 3 , 9 , 10 , 25 ; however, in this study, we found that using specialized software to create panoramic, custom MPR, and 3D reconstructed images aided in visualization of specific dental abnormalities. The panoramic and 3D reconstructed images were helpful in evaluating the overall occlusion and the relationship of the teeth to one another.
The occlusal angles between the maxillary premolar and molar and the mandibular premolar and molar teeth were visible on transverse images. Transverse images were also useful for delineating the orbit and nasal cavity. The panoramic views provided images of the skull without superimposition of the right and left sides as occurs with skull radiography.
Panoramic and sagittal MPR images were useful in evaluating for coronal and apical elongation. To evaluate each individual tooth for dental pathology as well as to assess the soft tissue structures, the transverse and custom MPR images were required. Widening of the periodontal ligament space was more easily identified on dorsal MPR images. Dorsal MPR views also aid in assessment of the orbit, nasal cavity, and sinuses. Inflammatory tooth resorption was more apparent on sagittal and dorsal MPR images and could be confirmed on the transverse images.
The short scanning time, decreased cost, and high-resolution images without the superimposition of anatomic structures make CBCT an appealing method for evaluating rabbit dental disease. Independent of the method of imaging used, this study, as well as multiple other studies, substantiate the need to perform advanced imaging when dental disease is suspected. Oral and physical examination is not enough to fully diagnose dental disease. GR: study concept and design; acquisition of data; analysis and interpretation of data; and drafting of manuscript.
DC: analysis and interpretation of data; critical revision of the manuscript for important intellectual content; and study supervision. BA: study concept and design; analysis and interpretation of data; critical revision of the manuscript for important intellectual content; administrative, technical, or material support; study supervision; and obtaining funding.
DH: critical revision of the manuscript for important intellectual content. PK: statistical analysis. AZ: acquisition of data. FV: study concept and design; analysis and interpretation of data; critical revision of the manuscript for important intellectual content; administrative, technical, or material support; study supervision; and obtaining funding. FV: full access to all of the data in the study and took responsibility for the integrity of the data and the accuracy of the data analysis. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors thank John Doval and Chrisoula Toupadakis for the artwork. Gorrel C. Veterinary Dentistry for the General Practitioner. Edinburgh: Elsevier Saunders Google Scholar. Dental and oral diseases in lagomorphs. J Vet Dent —7. Rabbit and Rodent Dentistry Handbook. Lake Worth: Zoological Education Network Dentistry in pet rabbits. Comp Cont Educ Pract 27 9 — Crossley DA. Oral biology and disorders of lagomorphs.
Computed tomography and cross-sectional anatomy of the head in healthy rabbits. Am J Vet Res 71 3 — Harcourt-Brown FM. The progressive syndrome of acquired dental disease in rabbits.