Evaluation of Infraorbital Canal Anatomy and Related Anatomical Structures with Multi-Detector Ct

Ankara Üniversitesi Tıp Fakültesi Mecmuası 2016, 69 (2) DAHİLİ TIP BİLİMLERİ/ MEDICAL SCIENCES DOI: 10.1501/Tıpfak_000000924 Araștırma Makalesi / Research Article

Evaluation of Infraorbital Canal Anatomy and Related Anatomical Structures With Multi-Detector Ct

İnfraorbital Kanal Anatomisi ve Kanal ile İlișkili Anatomik Yapıların Çok-Dedektörlü BT ile Değerlendirilmesi

Çağlar Uzun1, Șaziye Eser Șanverdi2, Evren Üstüner1, Mehmet Ali Gürses2, Șafak Șalvarlı2

1 Ankara University School of Medicine, Department of Radiology 2 Integra Medical Imaging Center , Ankara, Turkey Aims: The purpose of this study is to assess the anatomic features and variations of the infraorbital canal * Bu çalışma poster olarak 2013 Avrupa Radyoloji Kongresi’nde (IOC). sunulmuştur (doi.org/10.1594/ecr2013/C-2407)

Material and method: Digitally archived paranasal sinus computed tomography (CT) images of 492 IOC of 46 adult patients (mean age; 36.7 ± 24.4 year, M/F: 154/92) were retrospectively reviewed. Course and bony

structure of the IOC, existence of anterior superior alveolar canal (ASAC) and number of the infraorbital foramen (IOF) were evaluated.

Results: IOC was observed as a groove, without a superior wall, rather than a canal in the majority of the

images (64%). Presence of a true canal was observed in the 23% of the images. IOC coursed along the superior – lateral wall of the adjacent maxillary sinus in 83% of images (n = 408). IOF was single in 88% of images

(n = 433). ASAC was detected in 44% of the images (n = 216). In comparison to IOC, ASAC had a lateral (n = 135, 62.5%) or inferior (n = 81, 37.5%) course. In the 72.6% of the patients presenting with ASAC, conjunction with IOC was detected just before the IOF.

Conclusion: Anatomic features of IOC should be demonstrated in the patients who need orbital, maxillary sinus or dental implant surgery to prevent iatrogenic trauma to neurovascular bundles within. CT can provide accurate data in the evaluation of IOC anatomy, and correlative anatomical studies would strengthen the imaging. Key Words: Infraorbital Canal, Anterior Superior Alveolar Canal, İnferior Alveolar Nerve, Multi-Detector Computed Tomography Amaç: Bu çalıșmanın amacı infraorbital kanalın (İOK) anatomik özellikleri ve varyasyonlarının değerlendiril- mesidir. Gereç ve Yöntem: Dijital olarak arșivlenmiș 246 olguya ait (ortalama yaș; 36.7 ± 24.4, E/K: 154/92) 492 İOK’nın bilgisayarlı tomografi (BT) görüntüleri retrospektif olarak gözden geçirilmiștir. İOK’nın seyri ve kemik yapısı, anterior superior alveolar kanal (ASAK) varlığı ve infraorbital foramen (İOF) sayısı değerlendirilmiștir. Bulgular: İOK incelemelerin çoğunda (%64) kanaldan çok oluk olarak görüntülenmiștir. Görüntülerin %23’ünde gerçek bir kanal görülmüștür. İOK, görüntülerin %83’ünde (n = 408) komșu maksiller sinüsün süperior-lateral duvarı boyunca seyretmiștir. Görüntülerin %88’inde (n = 433) tek İOF izlenmiștir. ASAK, görüntülerin %44’ünde (n = 216) mevcuttur. ASAK, İOK’nın lateralinde (n = 135, %62.5) ya da inferiorunda (n = 81, %37.5) görülmüștür. ASAK’ın görüldüğü olguların %72.6’sında ASAK ve İOK, İOF’nin hemen öncesinde birleșme göstermektedir. Sonuç: İçerisindeki nörovasküler yapıların iyatrojenik travmalardan korunması amacıyla orbital, maksiller ve dental cerrahi öncesi İOK’nın anatomik özelliklerinin ortaya konması gereklidir. İOK anatomisinin değerlen- dirilmesinde BT doğru bilgi sağlayabilmektedir. Görüntüleme bulgularının anatomik çalıșmalar ile korelas- yonu görüntülemenin değerini arttırabilir. Anahtar Sözcükler: İnfraorbital Kanal, Anterior Süperior Alveoler Kanal, İnferior Alveoler Sinir, Çok- Dedektörlü Bilgisayarlı Tomografi

Infraorbital canal (IOC) is a bony canal consists of sensorineural fibers, and that is located in the superior - lateral innervates the ipsilateral mid-face. wall of the maxillary sinus. IOC is ION has afferent fibers from the skin continuous with the inferior orbital and the conjunctiva of the ipsilateral Received : April 04,2016  Accepted: April 28, 2016 fissure and anteriorly opens into the lower eyelid; the skin and the mucosa

Corresponding Author infraorbital foramen (IOF) (Fig 1) of the nose; skin and buccal epithe- (1). IOC contains important anato- lium of the upper lip, the upper teeth Çağlar Uzun, MD, mic structures such as inferior orbital and related gingivae (1-3). E-mail:[email protected] nerve (ION) and inferior orbital ar- Phone: 508 22 60 Fax: 310 08 08 tery (IOA). ION is a branch of the Ankara University School of Medicine, Department of Radiology İbni Sina Hospital, Sıhhiye, 06100 Ankara, TURKEY maxillary nerve, which completely

Ankara Üniversitesi Tıp Fakültesi Mecmuası 2016, 69 (2)

With the posterior - superior alveolar Imaging was done with a 16 detector CT Number of IOF, the existence and artery (PSAA), IOA is the most im- scan (Siemens, Erlangen, Germany). the course of ASAC were mainly re- portant artery that supplies the maxil- Imaging frame was marked from the viewed using axial images. Coronal lary bone (4). The rich intraosseous roof of the frontal sinuses to the bot- and sagittal reformatted images were arterial anastomosis of IOA and tom of the maxillary sinuses with a referred in case of need. PSAA branches supply the maxillary 12x12 cm of field of view. The ima- sinus mucosa, bony constituents and ges were obtained with 3 mm slice Bony structure of IOC was classified the buccal epithelium (4, 5). thickness, 16 x 1 mm collimation, using the criteria employed by a pre- 200 mAs, and 120 kVp. Then, thin viously reported study (7). According Within IOC, ION provides three distinct slice reconstructions with a thickness to the developmental features of branches: middle - superior alveolar of 0.75 mm were made. Subsequ- bony walls, IOC was classified as a nerve, posterior –superior alveolar ner- ently, sagittal – oblique reformatted true canal (definite bony walls wit- ve, and anterior – superior alveolar images parallel to the course of IOC hout any defect), a canal with patchy nerve (6). Anterior – superior alveolar were obtained from these thin re- superior wall (superior wall consisted nerve (ASAN) branches from the ION constructions. of bony islets, but complete bony at the level of the 1/3 anterior portion walls in rest of the canal), as a groove of the IOC and runs within a tiny canal, Analysis was done by a radiologist expe- (absence of superior wall). The course named as anterior – superior alveolar rienced in head and neck imaging of IOC was categorized according to canal (ASAC) by Song et al. (7). ASAC (SES). The course and bony structure its location; whether the canal is might join into IOC just before the of the IOC were evaluated using the completely located in the superior - opening of IOF, or may have a separa- sagittal – oblique reformatted images. te foramen (Fig 2). lateral wall of the maxillary sinus or IOC, the canal that encases important neurovascular structures, is an area of interest in patients with intractable or pharmacologically unresponsive tri- geminal neuralgia for nerve block therapy purposes (8). In addition, ION and IOA might come under iatrogenic trauma during maxillofacial, orbital and dental surgery. To avoid iatrogenic injury, anatomic course of IOC and the topographic features of IOF should be known in patients requiring mid-facial and orbital surgery (9, 10). Therefore, preoperative assessment with multi-detector computed tomography (CT) of both IOC Figure 1a Figure 1b and IOF may help treatment plan- Figure 1: Coronal reformatted CT images; inferior orbital canals (arrows) are bilaterally seen ning and surgical management. in the floor of the orbit (a) and in the lateral wall of the maxillary sinuses (b). In this study, we aimed to investigate the anatomy of IOC and related structures with multi-detector CT in the adult population.

Material and methods A total of 492 IOC images of 246 adult patients who had been examined with paranasal sinus CT for various medical reasons were reviewed from our institutions digital picture archiving database (PACS). Mean age was 36.7 ± 24.4 years with a range of 19.6 – 56.3 years. Male to female ratio was 154 / 92. Figure 2: Infraorbital foramina (arrows) are seen in the axial CT image.

90 Evaluation of Infraorbital Canal Anatomy and Related Anatomical Structures With Multi-Detector Ct Journal Of Ankara University Faculty of Medicine 2016, 69 (2)

partially located in the lateral wall and Table 1: Bony structure of the IOC Table 2: Course of ASAC partially located in the cavity of the Number and ASAC Number and percentage of maxillary sinus. The relation of ASAC IOC percentage of images and IOC such as conjunction points, images Course Lateral, n = 135 (62.5%) True bony canal 64 (13%) (according Inferior, n = 81 (37.5%) opening features of the canals whet- Patchy superior wall 113 (23%) to IOC) her separately or together, and num- Groove 315 (64%) ASAC: anterior – superior alveolar canal, ber of IOF were also evaluated. Age IOC: inferior orbital canal and gender differentiations were IOC coursed through the superior - IOF was single in 88% of the images (n analyzed. lateral wall of the adjacent maxillary = 433). Double IOF was detected in Patients with maxillofacial trauma and sinus in 83% of the images (n = 408). 59 (12%) images, one belonging to abnormality, and the examinations In the 17% of images (n = 84), 1/3 IOC and the other to ASAC (Table with motion artifacts were not inclu- anterior portion of IOC was within 3). In the group of the patients with ded in the study. the sinus cavity, while 2/3 posterior ASAC, conjunction with IOC just be- portion was coursing in the maxillary fore IOF was noted (n=157, 72.6%). Local ethical committee approval was sinus wall. Neither bony structure, obtained for this study. nor course of IOC revealed any signi- Neither course, nor existence of ASAC ficant correlation with age or gender revealed any significant correlation Statistical analyses were made by SPSS (P > 1, for each pair). with age or gender (P >1, for each 15.0 version for Windows (SPSS, pair). No statistical correlation was Chicago, Ill). Descriptive statistics In this study, ASAC was identified as a found between the number of IOF were used for general distribution ac- distinct canal in the 216 of the images and age or gender, either (P > 1, for cording to age and gender. One way (44%). According to the localization of each pair). analysis (ANOVA) was used to ob- IOC, ASAC revealed two different co- Table 3: Number of IOF tain the differences between two urses; lateral (n = 135, 62.5%) and inferior (n = 81, 37.5%) (Fig 4) (Table 2). Number and percen- IOF genders. Fisher’s Exact test was per- tage of images formed to analyze the relation Double 59 (12%) between the age and features of IOC Single 433 (88%) and IOF. Threshold for the statistical IOF: Infraorbital foramen analyses was set as P<0.05. Discussion Results Mid-face is the cornerstone for plastic IOC was observed as a groove, without a and aesthetic interventions, dental superior wall, rather than a canal in implantation, maxillary sinus explora- the majority of the images (n = 315, tion and orbital procedures. Relati- 64%). In 23% of the images (n = 113) vely thin skin and subcutaneous fat a deficient bony roof was detected tissue in comparison to other body (Fig 3). True canal was only noted in Figure 4a parts provide easy access to impor- the 13% of the images (n = 64) tant vascular structures and neural (Table 1). plexuses in that area. Intense neurovascular supply of mid-face tends that area vulnerable to iatrogenic trauma. IOF, the opening of ION and IOA and the anatomical structure that is most superficially located in mid-face have been studied in many previous studies (11-13). In this study we mainly analyzed the association of foramina of IOC and ASAC in regard to their courses. In the 3 dimensional CT study that has Figure 4b been reported by Lee et al. (12) The Figure 3: Sagittal - oblique reformatted CT Figure 4: Inferior orbital canal (white arrow) course and the shape of the IOC, and image, infraorbital canal (arrows) is seen with and anterior-superior alveolar canal (black the anatomical landmarks adjacent to arrow) are seen in the axial (a) and in the patchy osseous appearance of the superior coronal reformatted (b) CT image IOF were analyzed. In the study of wall of maxillary sinus. Hindy and Abdel-Raouf (11), which

Çağlar Uzun, Șaziye Eser Șanverdi, Evren Üstüner, Mehmet Ali Gürses, Șafak Șalvarlı 91 Ankara Üniversitesi Tıp Fakültesi Mecmuası 2016, 69 (2)

had been conducted on dry skulls, the might be associated with the pneuma- (16.25%) in their anthropometric course of IOC, and the distance from tization features of the maxillary si- human skull study in a distinct ethnic the center of IOF to the lateral nasal nus. However, involvement of other group, South Indians. In the study of border and to the inferior border of possible factors such as genetic and Bressan et al (16). anatomical features the orbit were evaluated. According environmental factors cannot be ru- of IOF have been analyzed in 1064 to the evaluation parameters, except led out. human skulls, and accessory IOF rate the distances between IOF and rela- have been reported as 4.7%. They ted anatomical structures, our study is We found a distinct ASAC in the 216 of have stated a slight male dominancy quite close to the study by Hindy and the images (44%). According to the (5.4% in male and 4.26% in female) Abdel-Raouf. localization of the IOC, ASAC revea- in contrast to this study. Since these led two different courses as laterally studies were conducted on different We analyzed the bony texture of IOC in (n = 135, 62.5%) and inferiorly (n ethnic populations (South Indian, Ita- regard to the authors’ classification =81, 37.5%). Song et al (7). have also lian and Turkish people, respectively) mentioned above; and we found true reported that lateral course of ASAC wide range of findings reminded us bony canal in 13%, a patchy superior according to IOC was more frequent. genetic factors might be responsible. wall in 23%, and a groove configura- In their cadaveric study lateral course In the studies that have analyzed the tion in 64% of CT images. IOC was of ASAC was reported as 57.5% and anatomical features of IOF in Tur- classified in the study of Hindy and inferior course as 37.5%. They have kish population reported by Kazkaya- Abdel-Raouf (11) as true canal in 25%, stated medial course of ASAC in 2 si et al (17). and Canan et al (20)., the patchy wall in 15%, and a groove in patients in their series. But they have prevalence of double IOF was repor- 60% Frequency of true bony canal was also declared that medially coursed ted as 5% and 11.5%, respectively. In lower in our study in comparison to ASAC finally joined to the IOC. In this study, prevalence of double IOF the study of Hindy and Abdel-Raouf. the micro-computed tomography was found as 12%, and this value was We suggest that the higher resolution study of cadavers by Song et al. the considered to be in the range provi- provided by the multi-detector CT number and the association of ASAC ded by the worldwide literature. We technology in our study might have led and IOC were analyzed. They repor- believe that the studies with larger se- to the detailed evaluation of the supe- ted multiple ASACs in some cases. ries in various ethnical populations rior wall of the IOC. They have also stated that ASACs and meta-analysis of literature would frequently aroused from the 1/5-1/2 be helpful to clarify the issue. We also evaluated the course of IOC anterior portion of IOC with an angle within the maxillary sinus. In 408 of of 37 degree (7). In this study we did Absence of cadaveric correlation of CT the images (83%), IOC coursed in not find multiple ASACs. Moreover findings is the limitation of our study. the superior - lateral wall of the we identified ASAC in some of the But previous comparative studies ha- maxillary sinus. In the remaining 84 images, not in all sinuses. Findings ve already shown that CT could be images (17%), IOC coursed in the showed that ASAC evaluation carried used as a reliable technique in the superior - lateral wall of the maxillary out with CT scanners provide higher planning of mid-face, orbital and den- sinus posteriorly, and in the maxillary resolution. tal surgery. sinus cavity anteriorly. In the latter group, approximately 2/3 of IOC In this study single IOF was found in The current study has revealed the detai- was encountered by the maxillary si- 433 of the images (88%). In the rema- led anatomy of IOC and related ana- nus wall whereas 1/3 anterior portion ining images (n = 59, 12%) double tomical structures. In the patients showed free course in the sinus ca- IOF with two distinct foramina one who will undergo orbital, maxillofa- vity. In 74 patients, one IOC revealed belonging to IOC and the other to cial, or dental surgery, it is important intra-osseous course and the other ASAC was observed. In the English to know detailed anatomy of IOC to revealed partially intra-osseous and literature the prevalence of double protect neurovascular structures wit- partially intra-sinus course. According IOF has been reported as 2.2% to hin. CT can provide accurate and re- to the best of our knowledge, there is 18.2% (11-12, 14-19). Hindy and Ab- liable guidance regarding this issue, no study in the English literature that del-Raouf (11) have found double correlation with anatomical studies has investigated the course of IOC IOF in the 10% of their study popu- would strengthen the imaging fin- within the maxillary sinus. In the light lation that consisted of Egyptians. dings. of statistical analyses we thought that Boopathi et al (15). have reported ac- variations in the course of the IOC cessory IOF in 13 of the 80 samples

92 Evaluation of Infraorbital Canal Anatomy and Related Anatomical Structures With Multi-Detector Ct Journal Of Ankara University Faculty of Medicine 2016, 69 (2)

REFERENCES

1. Xu H, Guo Y, Lv D, et al. Morphological the infraorbital foramen. Aesthet Surg J asurements and surgical relevance. J Med structure of the infraorbital canal using 2013;33:13-18. Assoc Thai 2006;89:675-682. three-dimensional reconstruction. J Cra- niofac Surg 2012;23:1166-1168. 9. Ella B, Sedarat C, Noble Rda C, et al. 15. Boopathi S, Chakravarthy Marx S, Dha- Vascular connections of the lateral wall of lapathy SL, et al. Anthropometric analysis 2. Hwang K, Suh MS, Chung IH. Cutaneous the sinus: surgical effect in sinus augmen- of the infraorbital foramen in a South In- distribution of infraorbital nerve. J Crani- tation. Int J Oral Maxillofac Implants dian population. Singapore Med J ofac Surg 2004;15:3-5. 2008;23:1047-1052. 2010;51:730-735.

3. Moore K, Dalley A. Clinically oriented 10. Rosano G, Taschieri S, Gaudy JF, et al. 16. Bressan C, Geuna S, Malerba G, et al. anatomy. 4th ed. Philadelphia: Lippincott Maxillary sinus vascular anatomy and its Descriptive and topographic anatomy of Williams & Wilkins; 1999:903-905. relation to sinus lift surgery. Clin Oral the accessory infraorbital foramen. Clini- 4. Traxler H, Windisch A, Geyerhofer U, et Implants Res 2011;22:711-715. cal implications in maxillary surgery. Mi- al. Arterial blood supply of the maxillary nerva Stomatol 2004;53:495-505. 11. Hindy AM, Abdel-Raouf F. A study of sinus. Clin Anat 1999;12:417-421. infraorbital foramen, canal and nerve in 17. Kazkayasi M, Ergin A, Ersoy M, et al. 5. Solar P, Geyerhofer U, Traxler H, et al. adult Egyptians. Egypt Dent J Microscopic anatomy of the infraorbital Blood supply to the maxillary sinus rele- 1993;39:573-580. canal, nerve, and foramen. Otolaryngol vant to sinus floor elevation procedures. Head Neck Surg 2003;129:692-697. Clin Oral Implants Res 1999;10:34-44. 12. Lee T, Lee H, Baek S. A three- dimensional computed tomographic mea- 18. Leo JT, Cassell MD, Bergman RA. Varia- 6. Drake R, Vogl A, Mitchell A. Gray’s Ana- surement of the location of infraorbital tion in human infraorbital nerve, canal tomy for Students. Philadelphia: Churchill foramen in East Asians. J Craniofac Surg and foramen. Ann Anat 1995;177:93-95. Livingstone; 2010:933-942. 2012;23:1169-1173. 19. Sato I, Kawai T, Yoshida S, et al. Obser- 7. Song WC, Kim JN, Yoo JY, et al. Micro- 13. Lee UY, Nam SH, Han SH, et al. Morp- ving the bony canal structure of the hu- anatomy of the infraorbital canal and its hological characteristics of the infraorbi- man maxillary sinus in Japanese cadavers connecting canals in the maxilla using 3- tal foramen and infraorbital canal using using cone beam CT. Okajimas Folia D reconstruction of microcomputed to- three-dimensional models. Surg Radiol Anat Jpn 2010;87:123-128. mographic images. J Craniofac Surg Anat 2006;28:115-120. 2012;23:1184-1187. 20. Canan S, Asim OM, Okan B, et al. Ana- 14. Apinhasmit W, Chompoopong S, Met- tomic variations of the infraorbital fora- 8. Raschke R, Hazani R, Yaremchuk MJ. hathrathip D, et al. .Supraorbital Notch/ men. Ann Plast Surg 1999;43:613-617. Identifying a safe zone for midface aug- Foramen, Infraorbital Foramen and Men- mentation using anatomic landmarks for tal Foramen in Thais:anthropometric me-

Çağlar Uzun, Șaziye Eser Șanverdi, Evren Üstüner, Mehmet Ali Gürses, Șafak Șalvarlı 93