Evaluation of the morphology using cone beam computed tomography Kaan Orhan, DDS, PhD,a,b Bayram U. Sakul, PhD,c Ulas Oz, DDS, PhD,d and Burak Bilecenoglu, DDS, PhD,e Ankara and Mersin, Turkey UNIVERSITY OF ANKARA, NEAR EAST UNIVERSITY, ANKARA UNIVERSITY, AND UFUK UNIVERSITY

Objective. This study consists of anatomic research of the pterygoid hamulus (PH) using 3D cone beam computed tomography (CBCT) images reconstructed from a volumetric rendering program. Study design. Three hundred ninety-six sides in the CBCT scans of 198 (115 men and 83 women) patients were retrospectively analyzed. DICOM data of the patients were transferred to a surface-rendering software so as to generate 3D hard tissue surface representations of PHs. The width, length, angle, and the distance between posterior nasal spine and tip of the PH were measured. In addition, the inclinations of PHs were also evaluated in sagittal and coronal planes of the 3D images. Pearson ␹2 and Student t test were performed for statistical analysis among age, localization, and measurements (P Ͻ .05). Results. The mean PH measurements of left and right sides were 1.72 (SD 0.94) and 1.87 (SD 1.17)-mm width, and the lengths were 5.48 (AD 1.94), and 5.40 (SD 2.0) mm, respectively, with no significant difference (P Ͼ .05). All PHs were inclined toward the lateral side in the coronal plane, whereas PHs tended to incline toward the posterior rather than anterior in the sagittal plane (ϳ78%). The results showed no statistically significant differences among age, localization, and measurements of PHs (P Ͼ .05). Conclusions. Knowledge about the morphology of these structures is helpful for the interpretation of imaging and provides valuable information in the differential diagnosis of untraceable pains in the oral cavity and pharynx. Because of potential problems owing to PH morphology and elongation, oral and maxillofacial radiologists should assess the radiographic images thoroughly. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2011;112:e48-e55)

A broad definition of pterygoid hamulus (PH) is a maxilla and oropharynx, it is of interest to all disci- hooklike projection at the inferior end of each medial plines that are involved with this region.1 plate of the pterygoid process. The medial pterygoid The position, length, and inclination of PHs are of plate of the sphenoid curves laterally at its lower great importance for the function of several muscles: extremity into a hooklike process, the PH, around tensor veli palatini, palatopharyngeus, and upper part of which the tendon of the tensor veli palatini (TVP) the upper pharyngeal constrictor, pars pterygopharyn- muscle glides. Although the PH is, because of its bi- gea. These muscles contribute to the separation of the zarre shape, a striking feature of the base, it is still oral from the nasal cavity during sucking and swallow- an unexplored region on the anatomical map.1,2 Only a ing during growth and development and into adult- few studies have been conducted on the morphology of hood.2,3 PH1-4; however, because of its close relationship to the Elongation of PH was also associated with a rare syndrome of PH that shows various and complex symp- toms in the palatal and pharyngeal regions and also causes pain and discomfort especially during swallow- a Associate Professor, Department of Oral, Tooth and Jaw Radiology, ing. The term pterygoid hamulus syndrome was first University of Ankara, Faculty of Dentistry, Ankara, Turkey. bAssociate Professor, Department of Oral, Tooth and Jaw Radiology, used to describe a pain in the palatal and pharyngeal Near East University, Faculty of Dentistry, Mersin, Turkey. regions caused by an abnormally shaped PH by Hjørt- cProfessor, Department of Anatomy, Ankara University, Faculty of ing-Hansen et al.5,6 in 1987 with about 40 cases re- Dentistry, Ankara, Turkey. ported in the literature.4-15 d Assistant Professor, Department of Orthodontics, Near East Univer- Several studies were conducted on the position and sity, Faculty of Dentistry, Mersin, Turkey. eAssistant Professor, Department of Anatomy, Ufuk University, Fac- morphology of PH in different populations. According ulty of Medicine, Ankara, Turkey. to those studies, the length of the PH was found to be Received for publication Oct 16, 2010; returned for revision Feb 17, within the range of 4.9 to 7.2 mm.1-4,10 Putz and 2011; accepted for publication Feb 22, 2011. Kroyer1 also reported the sagittal and transverse diam- 1079-2104/$ - see front matter © 2011 Mosby, Inc. All rights reserved. eter of PH as 1.4 mm and 2.3 mm, respectively, doi:10.1016/j.tripleo.2011.02.038 whereas Sasaki et al.10 also reported an elongated PH of e48 OOOOE Volume 112, Number 2 Orhan et al. e49

Fig. 1. Panoramic radiography of the patient showing no abnormality except flattening of left TMJ condyle.

13 mm. Recently, it was found that the length increased on cone beam computed tomography (CBCT) imaging in adult age and then decreased significantly again in with generated 3D skull representations using a sur- the elderly population. Moreover, all studies reported face-rendering program to identify and investigate PH. that the positions of PHs are inclined laterally in the Thus, this study consists of anatomic research of PH coronal plane.1-2 using 3D CBCT images reconstructed form a volumet- This information is important especially in tracing an ric rendering program. unusual pain in the soft palate and pharyngeal region. Such a symptom in that area may be forming a complex MATERIAL AND METHODS that can include hearing disorders, difficulties in swal- In the case that guided us to this research, a 26-year- lowing, headache, pain and clicking in the temporo- old female was referred to our outpatient clinic because mandibular joints (TMJs), uncontrolled movements of of painful and burning sensations in the soft palate and the facial muscles, impacted teeth, trigeminal and glos- pharynx of 9 months’ duration. The patient’s history sopharyngeal neuralgia, stylo-hyoid ligament calcifica- revealed that the symptoms started after traumatic re- tion, stylo-mandibular ligament inflammation, tumors, moval of the right maxillary third molar. For this pain, cysts, herpes simplex, infection, otitis media, and so she stated that she was referred to 10 to 15 different forth; thus, consideration of the PH as a pain-inducing consultants, including ear, nose, and throat and maxil- factor should be included in the diagnosis.4,8,11 There- lofacial surgeons, and various diagnoses were made, fore, it is important to know the average length, shape, such as temporomandibular disorder (TMD) and glos- and morphology of PHs for the population that guided sopharyngeal neuralgia. The patient received nonsteroi- us to conduct this research. dal anti-inflammatory drugs and also an occlusal splint The detection of this area can be achieved by radi- for TMD. However, the painful sensation was not re- ography (cephalometric radiography, submentovertex, solved during the 9 months. Waters view, and so forth); however, identification of Initial panoramic radiography of the patient showed these structures by conventional radiography is exceed- neither a carious lesion nor any root fragment in the ingly difficult because of superimposition and distor- extraction site (Fig. 1) with slight degeneration on the tion. Today, computed tomography (CT) can be per- left TMJ condyle. Intraorally, pain and a firm swelling formed in axial and coronal planes with 3-dimensional were noted in palpation of the region. A decision was (3D) views for diagnosis and treatment.8 The 3D CT made to perform CBCT to obtain a more precise view avoids superimposition and problems owing to magni- of the region. Axial CBCT scan did not demonstrate fication and offers visualization of the craniofacial any abnormality; however, coronal sections showed structures with more precision than the 2D conven- elongated PH in the right side. The 3D reconstructed tional methods.16-19 CBCT images also showed an elongated PH (9.7 mm in Despite various studies that were conducted on length) with a sickle shape (Fig. 2). Infiltration of local shape, length, and position of the PH, the anatomical anesthesia to the PH subsided pain; however, the symp- relations of PH and the surrounding structures are toms returned after the anesthetic was metabolized. A rarely investigated.1-4 Moreover, no studies were found diagnosis of hamular pain was made. The patient was OOOOE e50 Orhan et al. August 2011

Fig. 2. a, Axial CBCT scan showed no abnormality, whereas in b and c, coronal CBCT images showed elongated PH on the right side (arrows) with a normal PH on the left side (arrowhead). d, e, 3D reconstructed CBCT images also showed elongated PH (9.7 mm in length) with a sickle shape (arrow).

referred for surgery of elongated PH. Following this views by the NewTom 3G. Depending on the size of case, we decided to conduct further research regarding the patient and the extent of beam attenuation, a vari- PH morphology in our population. ation in exposure of up to 40% was possible. For this purpose, 396 sides of 198 subjects (115 men The axial slice thickness was 0.3 mm, and the voxels and 83 women) ranging in age from 22 to 75 years were isotropic. The axial images were exported as a (mean: 35.54) who had craniofacial CBCT scans were 512 ϫ 512 matrix in DICOM file format and then were retrospectively investigated. CBCT images were taken imported in Maxilim software version 2.3.0 (Medicim, for various purposes, such as preimplant imaging, para- Mechelen, Belgium). All constructions and measure- nasal sinus examinations, or orthodontic purposes. The ments were performed on a 21.3-inch flat-panel color study’s protocol was carried out according to the prin- active matrix TFT medical display monitor (Nio Color ciples described in the Declaration of Helsinki, includ- 3MP, Barco, Belgium) with a resolution of 2048 ϫ ing all amendments and revisions. Only the investiga- 1536 at 76 Hz and 0.2115-mm dot pitch operated at 10 tors had access to the collected data. The institutional b. A consultant experienced in 3D imaging made high- review board of the faculty reviewed and approved quality 3D hard tissue surface representations com- informed consent forms. There was no preference about puted from the patients’ CBCT data set in several gender regarding sample choice, however only Turkish stages similar to previous studies20-22 and examined all patients were included in the study. Only high-quality scans were included. Images of low quality, such as images. scattering or insufficient accuracy of bony borders were First, the bone and soft tissue surfaces were seg- excluded. mented by applying a threshold on the acquired image CBCT scans were made with a Newtom 3G (Quan- volume of radiographic densities. An attempt was made titative Radiology s.r.l., Verona, Italy). The imaging to reduce noise without reducing actual osseous anat- protocol used a 9-inch field of view to include the omy. The were rendered as high-quality 3D hard mandibular and maxillary anatomy. X-ray parameters tissue surface representations that were computed from of kV and ma are automatically determined from scout the patients’ CBCT data set. The axial, sagittal, and OOOOE Volume 112, Number 2 Orhan et al. e51

using rotation and translation of the rendered images. Landmarks were identified by using a cursor-driven pointer. The width and the length of the PH together with the distance and the angles between posterior nasal spine (PNS) and tip of the PH were measured (Fig. 3, a, b, and c). To standardize the measurements, refer- ence points were chosen. The length measurements were taken from the junction of medial pterygoid plate and PH through the tip, similar to Putz and Kroyer’s study.1 First a line was drawn from the junction of medial pterygoid plate and PH parallel to the horizontal plane. Following the identification of the midpoint of this line, the length was measured starting from this point to the tip of the PH. The width of the PH was measured as the distance between the most prominence points of the PH in the coronal plane (Fig. 3, c). In addition, the inclinations of PHs were evaluated in sagittal and coronal planes of the 3D images. The average degrees of inclinations in the sagittal and cor- onal planes were also calculated by means of the soft- ware according to horizontal plane following Putz and Kroyer’s study1 (Fig. 4). The inclinations in the sagittal plane were also classified visually as anterior and pos- terior (Fig. 5), whereas inclinations in the coronal plane were classified as lateral or medial. All measurements were done 3 times by the same observer and the mean of these measurements were noted for analysis. The observer also performed the study 2 times with an interval of 2 weeks so as to detect intraobserver vari- ability. Statistical analyses were carried out using the SPSS 12.0.1 (SPSS, Chicago, IL) software program. To as- sess intraobserver reliability, Wilcoxon matched-pairs signed-ranks test was used for repeated measurements of the observer. Pearson ␹2 and Student t test were performed for statistical analysis among age, localiza- tion, and measurements (P Ͻ .05).

RESULTS Repeated measurement of CBCTs indicated no sig- nificant intraobserver difference (P Ͼ .05). Intraob- Fig. 3. a, b, Figure showing the measurements performed in server consistency was rated at 95% between 2 mea- the study that were made on a generated 3D image from surements. A total of 396 left and right sides of PHs volumetric rendering software with superimposed coronal were measured in 198 3D CBCT images. The findings slices over reconstructed 3D image taken from CBCT data. c, are presented in Table I. The mean measurements of Cropped image showing the length and width measurement in both left and right sides were 1.72 (SD 0.94) and 1.87 detail. w, width; l, length. (SD 1.17)-mm width, respectively whereas the lengths were 5.48 (SD 1.94) and 5.40 (SD 2.0) mm, respec- tively without any significant difference (P Ͼ .05). There were also no statistically significant differences coronal CT radiographic slices were also superimposed between left and right measurements between posterior over reconstructed 3D images (Fig. 3). nasal spine and tip of the PH of sides (P Ͼ .05). Measurements of 3D images were located and In the coronal plane, it was found that all PHs were marked on the 3D surface-rendered volumetric image inclined toward the lateral side (Fig. 3). However, in OOOOE e52 Orhan et al. August 2011

Fig. 4. a, 3D images showing angle and orientation of PH in the coronal plane, b, in the sagittal plane, and c, the angle between the posterior nasal spine and tip of the PH. HoP indicates horizontal plane.

Fig. 5. 3D reconstructed images showing a, anterior inclination and b, posterior inclination of PH (arrows).

Table I. Measurements of PH (mm) and standard deviations (SD) together with inclination of PH in coronal and sagittal planes Left Right Total Male Female Total Male Female Measurements (mean Ϯ SD) (mean Ϯ SD) (mean Ϯ SD) (mean Ϯ SD) (mean Ϯ SD) (mean Ϯ SD) (mean Ϯ SD) Width of the PH in coronal plane 1.72 Ϯ 0.94 1.73 Ϯ 0.83 1.70 Ϯ 1.07 1.87 Ϯ 1.17 1.93 Ϯ 1.44 1.79 Ϯ 0.60 Length of the PH 5.48 Ϯ 1.94 5.49 Ϯ 1.95 5.45 Ϯ 1.91 5.40 Ϯ 2.00 5.38 Ϯ 1.99 5.43 Ϯ 2.01 Posterior nasal spine to tip of PH 21.35 Ϯ 2.45 21.46 Ϯ 2.47 21.19 Ϯ 2.42 21.18 Ϯ 3.09 21.3 Ϯ 3.35 21.02 Ϯ 2.70 The average inclination in 52.5° Ϯ 2.57° 53.2° Ϯ 2.18° 51.9° Ϯ 1.96° 53.9° Ϯ 2.01° 54.1° Ϯ 2.33° 53.8° Ϯ 2.16° coronal plane The average inclination in 82.6° Ϯ 3.08° 82.8° Ϯ 3.19° 82.4° Ϯ 2.90° 81.9° Ϯ 3.25° 81.8° Ϯ 3.40° 82.0° Ϯ 2.99° sagittal plane Number of inclinations of PH in Lateral Lateral coronal plane 198 115 83 198 115 83 Medial Medial 000000 Number of inclinations of PH in Anterior Anterior sagittal plane 43 (21.7%) 21 (18.3%) 22 (26.5%) 45 (22.7%) 28 (24.3%) 17 (20.5%) Posterior Posterior 155 (78.3%) 94 (81.7%) 61 (73.5%) 153 (77.3%) 87 (75.7%) 66 (79.5%) PH, pterygoid hamulus. the sagittal plane, 43 (21.7%) PHs were inclined The average inclination in the sagittal plane and in toward the anterior whereas 155 (78.3%) PHs tended the coronal plane showed no statistically significant to posterior on the left side. Similarly, on the right difference (P Ͼ .05) (Table I). The angles between side, 45 (22.7%) PHs were inclined toward the an- posterior nasal spine and tip of the PH were also mea- terior, whereas 153 (77.3%) PHs tended to the pos- sured. The average degree for the left was 33.4° (SD terior (Fig. 5). 2.34) and 34.3° (SD 2.18) for right. Overall results also OOOOE Volume 112, Number 2 Orhan et al. e53

Table II. Measurements of PH (mm) and standard within the sulcus hamulus is responsible for the gliding deviations (SD) according to age of the tendon. It reduces friction caused by movement Measurements 22-55 y Ͼ55 y of the tendon of the TVP muscle around the PH. (mean Ϯ SD) Total (mean Ϯ SD) Total (mean Ϯ SD) The position, inclination, and especially the length of Width of the PH in 1.85 Ϯ 0.88 1.73 Ϯ 1.07 PHs are of great importance for the function of the coronal plane muscles that are located here. When these muscles Length of the PH 6.38 Ϯ 1.93 4.50 Ϯ 1.72 contract, the nasal and oral cavities separate from each Posterior nasal spine to 21.73 Ϯ 2.54 20.8 Ϯ 2.85 tip of PH other during swallowing and sucking. This separation is The average inclination in 53.9° Ϯ 2.18° 52.5° Ϯ 2.17° accomplished by the evaluation of soft palate following coronal plane LVP contraction and Tubar part of TVP for stretching The average inclination in 82.8° Ϯ 2.99° 81.7° Ϯ 3.05° the palatal aponeurosis.2,7,8 TVP also produces tension sagittal plane and elevation of soft palate, which the Tubar part is Number of inclinations of Lateral Lateral PH in coronal plane 166 32 fixed to the hamulus. The position and morphology of Medial Medial PH are closely related to TVP function, which directly 00affects the width of the hard plate during swallowing. Number of inclinations of Anterior Anterior The inclination of the PH is also responsible for better PH in sagittal plane 39 4 tension of palatal apounerosis.2 Krmpotic´-Nemanic´et Posterior Posterior 2 127 28 al. pointed out that if the hamulus remains short as in newborns, the surrounding muscles do not have firm support, which leads to uncontrolled narrowing of the upper pharynx, thus causing snoring and sleep apnea. showed no statistically significant differences among Besides, the elongated PH can also be the reason for 10 gender, localization, and measurements of PHs (P Ͼ pain and discomfort in the soft palate and pharynx. Such 15 .05). cases have been previously reported. Gores was the first As a further evaluation, we divided the study group to report the presence of pain caused by a long PH. The into 2 age groups, 22 to 55 and older than 55 years, so term pterygoid hamulus syndrome was then used to de- as to detect any differences according to age group. scribe a pain in the palatal and pharyngeal regions with 4-14 Table II shows the data according to age group. The about 40 cases reported in the literature. length of PH differed among the age groups. The pa- There is no consensus for the etiology of this syndrome. tient group older than 55 had shorter PH length than the Previously, several etiologic factors stated bursitis of TVP 4,9-12,14 4,10 22- to 55-year-olds (P ϭ .054) (Table II). No further or an osteophyte, elongation of PH, or consis- 13 statistically significant difference was found among age tent minimal trauma to the overlying structure. The and all measurements (P Ͼ .05). trauma from swallowing a large bolus of food or from an overextended denture, anesthesia intubations, trauma dur- DISCUSSION ing tooth brushing, bulimic patients, and “fellatio” in child Anatomically, the PH and the edge of the medial abuse seem to be the cause of this syndrome.10,11 In our pterygoid plate immediately superior to the PH, give case, the patient had her third molar extracted and the rise to the origin of the superior constrictor muscle of symptoms started after this operation. the pharynx. The palate pharyngeus muscle originates Patients suffering from this syndrome have clinical in layers from the PHs, as well as from the border of the signs, including pain and sensation of strangeness, hard palate, and from fibers of the levator veli palatine burning and swelling of the hard/soft palate, elevated muscle (LVP). It is generally stated that the lowest and noise sensitivity, dysphagia, dysfunction of muscles, most anterior fibers of LVP arise from the base of the and difficulty in swallowing. Clinically, the PH region pterygoid process and reach up to and a little beyond usually appears erythematous; sometimes the PH can the base of the PH. In addition, TVP originating from be palpated as firm swelling or recognized as an en- the scaphoid , the spine of palatal aponeurosis, largement under the mucosa of the soft palate.9-11 Fur- and the lateral wall of the cartilaginous auditory tube ther, the PH may have tenderness to palpation, which winds its tendon around the PH in a groove with a will be eliminated after anesthetic infiltration of the synovial bursa between the tendon and the bone, inserts area. In our case, no erythematous appearance was soft palate. The separation of the oral from the nasal seen; however, a firm swelling was noted and pain cavity is accomplished by the elevation of soft palate subsided after anesthetic infiltration. with constriction of these muscles.3,8,22,23 As the ten- The differential diagnosis of pain in the hard/soft don of the TVP winds around the PH, a synovial bursa palate and pharynx should include tumors, cysts, infec- is situated between the tendon and the bone. This bursa tions, foreign bodies, elongated styloid syndrome, third OOOOE e54 Orhan et al. August 2011 molar eruption, TMJ diseases, muscular dysfunction, structures by conventional radiography is exceedingly and also elongated PH.4,10,11 difficult because of superimposition and distortion. To- Several studies were conducted on the morphology day, CT can be performed in axial and coronal planes of PH in different populations. Eyrich et al.4 found the with 3D views for diagnosis and treatment of this mean length of the left hamulus to be 5 mm and region.7-8,24 The 3D CT avoids the superimposition and the right to be 4.9 mm. Putz and Kroyer1 reported the problems owing to magnification and offers visualization average length to be 7.2 mm and the sagittal and of the craniofacial structures with more precision than the transverse diameter to be 1.4 mm and 2.3 mm, respec- 2D conventional methods.17-19,25 Despite these advan- tively. Sasaki et al.10 also reported an average PH tages, the effective dose of CT is much higher than the length of 6.8 mm (SD 1.4 mm). Our results showed the conventional radiographs and also expensive procedures mean length of PHs for left and right sides were 5.48 and scanners are not easily accessible.19,26,27 (SD 1.94) and 5.40 (SD 2.0) mm, respectively which is In the past decade, CBCT was proposed for maxillo- similar to other studies.1,4,10 There was no significant craniofacial imaging.28-31 The advantages of this imag- difference according to gender and location. Sasaki et ing modality are the following: lower radiation dose al.10 reported an elongated PH case of 13 mm. Our than traditional CT, the possibility of individualized longest PH case was 10.9 mm in a male patient. overlap-free reconstructions, and DICOM data can be Recently Krmpotic´-Nemanic´ et al.2 conducted an imported and exported for other applications.28 Dental extensive study on PH. They investigated the PH CBCT can be recommended as a dose-sparing tech- among 3 age groups: children (0-9), adults (21-59), and nique compared with alternative standard medical CT elderly (60-100). They found that children had the scans for common oral and maxillofacial radiographic shortest PH length, on average 3.6 mm. The length imaging tasks. Effective dose (ICRP 2007) from a increased in adults (6.9 mm) and then decreased sig- standard dental protocol scan with the traditional CT nificantly again to 5.0 mm in the elderly group. They was from 1.5 to 12.3 times greater than comparable 32 also found no statistical difference for gender and for medium field of view dental CBCT scans. It was also left and right sides. stated that effective dose and dose to the main portions Although no statistically significant difference was of the head and neck were higher for traditional CT observed between the age groups, the P value was .054. than for CBCT. Image quality of CBCT was judged to From a numerical point of view, it can be concluded be equivalent to that of traditional CT for visualizing 33-37 that older patients had shorter PH length than the the maxillofacial structures. younger patients. This is in line with Krmpotic´- From the radiation point of view, CBCT examina- Nemanic´et al.’s2 study, but does not coincide with Putz tions can be used instead of CT to evaluate this region. and Kroyer’s1 study, which reported that the PH in- When 3D imaging is required to visualize anatomic creases in length to the beginning of adulthood, and structures, such as processes of , hard/ thereafter remains unchanged throughout life. soft palate, and oropharynx, CBCT should be preferred There was only one study regarding the width and over a CT image. the inclination of the PH.1 Putz and Kroyer1 measured the sagittal diameter of PH as 1.4 mm, which is con- CONCLUSIONS sistent with our width (sagittal diameter) measure- Knowledge about the morphology of these structures ments: 1.72 (SD 0.94) and 1.87 (SD 1.17) mm for left is helpful for the interpretation of imaging and provides and right, respectively. The inclinations in their study valuable information in the differential diagnosis of were 75° in the sagittal plane and 58° in the coronal untraceable pains in the oral cavity and pharynx. Be- plane, which is also similar to our results (Table II). cause of potential problems owing to PH morphology Each hamulus in this study was inclined laterally, as in and elongation, oral and maxillofacial radiologists previous studies.1-2 The results showed no statistically should assess the radiographic images thoroughly. Sim- significant differences among gender, localization, and ilar studies will provide useful information to better understand the anatomy and diseases regarding the PH. measurements of PHs (P Ͼ .05). The elongated PH can be responsible for atypical REFERENCES pain in the soft palate and pharynx region. Radiographs 1. Putz R, Kroyer A. Functional morphology in the pterygoid of the PH and pterygomaxillary region should be ob- hamulus. 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