Surgical Anatomy and Variations of the Infraorbital Nerve

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1 The Laryngoscope VC 2015 The American Laryngological, Rhinological and Otological Society, Inc. Surgical Anatomy and Variations of the Infraorbital Nerve Elisabeth H. Ference, MD, MPH; Stephanie S. Smith, MD; David Conley, MD; Rakesh K. Chandra, MD Objectives/Hypothesis: To assess relevant variations in the anatomical course of the infraorbital nerve (ION). This understanding may reduce the risk of surgical injury. Methods: A total of 100 consecutive computed-tomography sinus studies obtained in a tertiary referral center were reviewed, and measurements were made of the 200 IONs. Anatomic variants were classified into three types based on the degree to which (if any) the nerve s course descended from the maxillary roof into the sinus lumen. Results: A total of 60.5% of IONs were entirely contained within the sinus roof. In 27.0%, the nerve canal descended below the roof but remained juxtaposed to it. In 12.5%, the ION descended into the sinus lumen. The proportion of IONs descending into the sinus significantly increased to 27.7% when an infraorbital ethmoid cell was present (chi-square P < 0.001) and to 50% when the nerve was contained within a lamella of such a cell (chi-square P < 0.001). Descended nerves terminated in a foramen located an average of mm below the infraorbital rim, significantly further below the orbit than nondescended nerves (t test P < 0.001). Descended nerves were located a mean distance of mm below the sinus roof and traversed the sinus lumen diagonally for a mean length of mm. Conclusions: Descent of the ION into the maxillary sinus is a common anatomic variant that is more prevalent in the setting of an ipsilateral infraorbital ethmoid cell. Descended nerves are associated with the foramen significantly further below the inferior orbital rim than those of nondescended nerves. These observations may help surgeons avoid iatrogenic ION injury. Key Words: Infraorbital nerve, maxillary sinus, sinus surgery. Level of Evidence: N/A. Laryngoscope, 125: , 2015 INTRODUCTION The infraorbital nerve (ION) is a terminal branch of the maxillary division of the trigeminal nerve that innervates the skin of the cheek. The maxillary nerve exits the skull base at the foramen rotundum and enters the orbit via the inferior orbital fissure. It typically courses anteriorly as the ION within a canal or groove in the orbital floor before exiting through the infraorbital foramen (IOF) into the soft tissue of the face. It is responsible for the sensory innervation to the skin of the malar area between the lower eyelid and upper lip. Transient or permanent hypoesthesia, paresthesias, or neuralgias of the face may result from iatrogenic injury to the ION. 1 Injury may consist of an avulsion injury or partial or complete disruption of the nerve. The nerve is at risk during a Caldwell-Luc procedure From the Department of Otolaryngology Head and Neck Surgery (E.H.F., S.S.S., D.C.); the Center for Healthcare Studies (S.S.S.), Northwestern University Feinberg School of Medicine, Chicago, Illinois; and the Vanderbilt Department of Otolaryngology, Bill Wilkerson Center (R.K.C.), Nashville, Tennessee, U.S.A. Editor s Note: This Manuscript was accepted for publication November 17, Presented at the American Rhinologic Society 59th Annual Meeting, Vancouver, BC, Canada September 28, The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Elisabeth Ference, MD, MPH, Department of Otolaryngology Head and Neck Surgery, Northwestern University Feinberg School of Medicine, 676 N St. Clair Suite 1325, Chicago, IL elisabeth-ference@northwestern.edu DOI: /lary when the facial flap is elevated at the IOF, or during an expanded endoscopic approach if the back wall of the maxillary sinus is removed to gain access to the infratemporal fossa. 1 Postoperative facial numbness has been reported in 2% to 9% of patients after Caldwell-Luc procedures and 44% to 67% of patients after endoscopic pterygopalatine fossa surgery. 2 8 Although injury to the nerve is rare in routine endoscopic surgery of the maxillary sinus, the course of the nerve makes it susceptible to surgical trauma during clearance of disease from the roof of the maxillary sinus, particularly if the nerve is low-lying, running within a septation, or contained within the lamellae of an infraorbital ethmoid cell. 9 Fine-cut computed tomography (CT) technology with triplanar reconstruction has enhanced our ability to delineate the course of the infraorbital nerve through its bony canal. In the literature, few publications are available concerning the prevalence of descent of the ION within the maxillary sinus and variations in the location of the IOF. We aim to describe the relevant variations in the anatomical course of the ION in order to aid surgeons in preventing injury to a low-lying ION nerve. MATERIALS AND METHODS This study was approved by the Northwestern University Institutional Review Board. One hundred consecutive CT sinus studies obtained in a tertiary referral center s outpatient clinic between April 29, 2013, and May 25, 2013, were reviewed using a volumetric flat panel scanner, which obtained 0.4-mm voxels (volumetric pixels). Images of 200 IONs were viewed in the axial, coronal, and parasagittal planes. Measurements were

2 Type 3 nerves are hereafter referred to as descended nerves, whereas type 1 and type 2 nerves are not. T tests, chisquare, analysis of variance (ANOVA), and kappa coefficient analyses were performed using SAS Version 9.2 (SAS Institute Inc, Cary, NC). Fig. 1. Measurement of the vertical distance between the infraorbital nerve and maxillary sinus roof, demonstrated on a type 3 nerve. White bar 5 maximum vertical distance from the nerve to the sinus roof; white arrow 5 uncinate. made in the parasagittal plane of the maximum vertical distance from the center of the IOF to the inferior orbital rim, and of the maximum length of nerve exposed in the sinus from the point of emergence from the orbital floor to the IOF. In the coronal plane, measurements were made of the maximum vertical distance from the nerve to the sinus roof as it crossed the sinus (Fig. 1). The maximum horizontal distance from the center of the IOF to the center of the canine root was also measured by drawing a line in the coronal plane through the IOF and measuring the distance in the axial plane from the line to the canine root. Data was collected on gender, side, the presence of an infraorbital ethmoid cell, and the relationship of the nerve to the lamellae of such cells. Using a new classification scheme devised by the authors, anatomic variants were categorized into three types based on the degree (if any) to which the nerve s course descended from the maxillary roof into the sinus lumen (Fig. 2): Type 1: Nerve entirely contained within the sinus roof Type 2: Nerve canal located below the roof but remaining juxtaposed to it Type 3: Nerve descending into the sinus lumen, suspended from the sinus roof within a septation or the lamella of an infraorbital ethmoid cell RESULTS CT scans were obtained from 45 males and 55 females for a total of 200 IONs. An ipsilateral infraorbital ethmoid cell was present in 47 sinuses, and 24 of these cells contained the ION within their lamellae. One hundred and twenty-one (60.5%) of the IONs were categorized as type 1, 54 (27.0%) as type 2, and 25 (12.5%) IONs as type 3 (Table I). Of the type 3 IONs, 12 were contained within the lamellae of an infraorbital ethmoid cell, one was not contained within a present ipsilateral infraorbital ethmoid cell, and 12 traveled within a septation with no ipsilateral infraorbital ethmoid cell present. The proportion of nerves within the sinus significantly increased from 7.8% in cases without an ipsilateral infraorbital ethmoid cell to 27.7% when a cell was present (v , P < 0.001) and to 50% when the nerve was contained within a lamella of such a cell (v , P < 0.001) (Table I). The mean distance from the foramen to the orbital rim increased parallel to the degree of descension of the nerve s course from the sinus roof (ANOVA P value < 0.001) Among all 200 nerves, the average distance below the infraorbital rim was mm. Type 1 nerves were located mm; type 2 were located mm; and type 3 were located mm below the infraorbital rim. There was no significant difference in location of ION below the infraorbital rim based on gender (ANOVA P value 0.88) or side (ANOVA P value 0.19). Type 3 nerves terminated in a foramen significantly further below the orbit than the nondescended nerves (Table II). Mean maximum distance between a type 3 nerve and the sinus roof was mm, and descended nerves traversed the sinus lumen diagonally for a mean length of mm. Overall, the foramen was a mean distance of mm lateral to the canine root, and this did not significantly vary according to descent type (ANOVA TABLE I. Anatomic Variation of V2 Nerve Course in the Maxillary Sinus Based on Demographic and Anatomic Characteristics. Type 1 Type 2 Type 3 n % n % n % Chi Square P Value Male (n 5 90) Female (n 5 110) Right nerve (n 5 100) Left nerve (n 5 100) Ipsilateral Haller cell present (n 5 47) < Nerve within a Haller cell (n 5 24) < Total (N 5 200)

3 TABLE II. Measurements for Nondescended (Type 1 and 2) and Descended (Type 3) Nerves. Distance from infraorbital foramen to orbital rim Diagonal length of nerve exposed in maxillary sinus Distance from nerve canal to sinus roof SD 5 standard deviation. Type Mean (mm) SD (mm) 1 & P value < measurement has been used in multiple prior studies, although never in the setting of a nerve descended within the maxillary sinus We also measured the horizontal distance from the center of the IOF to a line drawn through the center of the canine root and found that the IOF in all of our subjects was lateral to the canine root. The horizontal distance of approximately 1 cm did not vary based on descension; therefore, it may serve as an additional landmark if the nerve is difficult to find during dissection. The availability of endoscopic technology has decreased the indications for the Caldwell Luc approach during routine management of chronic inflammatory P value 0.36). There was a moderate concordance between nerve category on the left compared to on the right (weighted kappa 0.49; 95% confidence interval ; two-sided P value < 0.001). DISCUSSION Descension of the ION within the maxillary sinus is a common anatomic variant present in 12.5% of nerves, and is more prevalent in the setting of an ipsilateral infraorbital ethmoid cell, especially if the nerve is contained within the lamellae of the cell. The foramen of descended nerves is on average 2.9-mm inferior to the location of the foramen of nondescended nerves, and descended nerves are located on average 8.6 mm below the maxillary sinus roof within the sinus cavity. The increased distance from the IOF to the orbital rim at the foramen may be important during Caldwell Luc procedures, whereas the distance of the ION to the maxillary sinus roof and the length of exposed nerve within the sinus may be important during endoscopic surgery. During routine endoscopic sinus surgery with simple maxillary antrostomy via removal of the uncinate process and enlargement of the natural ostium, a descended nerve will not be at increased risk of injury. However, any surgical attempt to clear mucosal disease from the roof of the maxillary sinus, or to break down septations or the lamellae of an infraorbital ethmoid cell, may cause infraorbital nerve injury. 1,9,10 For example, approximately 40% of inverted papillomas occur in the maxillary sinus, and during resection the mucosal lining must be deliberately stripped and the wall addressed with a burr or cautery, placing a descended ION at risk When the attachment of the papilloma is far lateral or anterior in the sinus, endoscopic resection may need to be supplemented with a targeted external Caldwell-Luc approach or antral trephination Our study also found an association between descended nerves and increased distance between the IOF and the inferior orbital rim, which may pose an increased risk of injury during a Caldwell-Luc approach. 9 Although the distance to a superior based landmark is not exactly the same perspective as one would need to consider for a sublabial approach, surgeons tend to palpate the inferior orbital rim while doing a Caldwell Luc procedure or infraorbital block. This 1298 Fig. 2. Coronal and parasagittal examples of anatomic variants based on descent of the infraorbital nerve from the maxillary sinus roof, with arrows indicating nerve.

4 disease, but the procedure is occasionally required for the resection of neoplasms, ligation of the internal maxillary artery, and repair of the orbital floor. 9 The ION can be injured during a Caldwell-Luc procedure when a facial flap is elevated at the point where the nerve exits the IOF. Therefore, preoperative identification of anatomic variations and intraoperative identification of the nerve, if appropriate, is important to decrease the risk of iatrogenic injury during surgery of the midface and maxillofacial skeleton. Once injury occurs, the management is conservative. 1 Injury may have a significant impact on patient s quality of life because it may result in permanent soreness and paresthesias or hypoesthesias of the cheek, a complication relatively frequent after facial trauma with fracture of the orbital floor or anterior maxillary wall. 1 Various studies have estimated that between 60% to 80% of patients with maxillary fractures have paresthesias immediately after the trauma, and between 15% to 30% have permanent sensory disturbances Nerve function must be evaluated and documented following any midface trauma or prior to any surgery on the midface or paranasal sinuses, particularly when dissection of the roof of the maxillary sinus or a Caldwell- Luc approach is planned. Iatrogenic injury may prompt medicolegal action against the surgeon. It is important for the radiologist to mention anatomical variations in the course of the ION in any sinonasal preoperative report and for the surgeon to be aware of any anatomic variant. Prevention of infraorbital nerve injury during endoscopic surgery may be achieved by identifying a descended ION on the preoperative CT scan; localizing the aberrant nerve during surgery through the use of angled scopes or an image-guidance system, when available; and minimizing instrumentation along the roof of the sinus. The overall mean of the maximum vertical distance between the infraorbital rim and the IOF was mm, which is in keeping with the surgical literature that analyzed CT scans. A prior study using CT imaging estimated the distance at mm on the left and mm on the right. 19 Prior studies using dried skulls or cadaver skulls estimated the distances to be slightly less, between mm and mm, possibly due to differences in measurement techniques and volume averaging by CT imaging In studies that looked at gender and side, using either CT imaging or cadaver skulls, no significant difference was seen either when comparing between right and left or male and female. 14,15,19 We could find no prior study in the literature that discussed increase in the vertical distance between the infraorbital rim and the IOF based on the course of the nerve. Other studies have looked at the morphological structure of the infraorbital canal of volunteers or cadaveric skulls using three-dimensional reconstructions from CT data. 19,23,24 However, none of these articles looked at the effects of the course of the nerve on the distance from the IOF to the orbital rim or canine, and none quantified the extent to which the nerve descended into the sinus. Prior articles have focused on the angles and landmarks needed to perform adequate nerve blocks for local anesthesia rather than surgical anatomy relevant to the endoscopic surgeon. During a review of the literature, only one prior case study by Chandra and Kennedy was found documenting the ION traversing the lumen of the maxillary sinus within the lamella of an infraorbital cell, whereas another article by Mailleux et al. documented two cases of the ION traveling within maxillary sinus septations. 9,10 We could identify no prior reports of the prevalence of these anatomic variants. To our knowledge, this is the first study to use CT sinus scans to measure the length of nerve exposed in the sinus, the length of descent below the infraorbital rim, and the distance of the IOF to the infraorbital rim among patients with anatomic variations in the course of the ION. CONCLUSION The ION traversing the lumen of the maxillary sinus rather than remaining within a canal in the orbital floor is a common anatomic variant and is more prevalent in the setting of an ipsilateral infraorbital ethmoid cell, especially if the nerve is contained within the lamellae of the cell. Descended nerves are associated with IOF significantly further below the inferior orbital rim than those of nondescended nerves. Preoperative recognition of anatomic variants and meticulous attention during the procedure is therefore necessary to preserve the nerve during management of infraorbital ethmoid cells, maxillary septations, and mucosal disease along the orbital floor or while performing a Caldwell- Luc approach. BIBLIOGRAPHY 1. Tewfik MA, Wormald P-J. Chapter 9: Complications in Endoscopic Sinus Surgeyr. In: Bernal-Sprekelsen M, Carrau RL, Dazert S, et al., eds. Complications in Otolaryngology Head and Neck Surgery. New York, NY: Thieme; Cutler JL, Duncavage JA, Matheny K, Cross JL, Miman MC, Oh CK. Results of Caldwell-Luc after failed endoscopic middle meatus antrostomy in patients with chronic sinusitis. Laryngoscope 2003;113: DeFreitas J, Lucente FE. The Caldwell-Luc procedure: institutional review of 670 cases: Laryngoscope 1988;98: DelGaudio JM. Endoscopic transnasal approach to the pterygopalatine fossa. Arch Otolaryngol Head Neck Surg 2003;129: El-Sayed I, Pletcher S, Russell M, McDermott M, Parsa A. Endoscopic anterior maxillotomy: infratemporal fossa via transnasal approach. Laryngoscope 2011;121: Har-El G. Combined endoscopic transmaxillary-transnasal approach to the pterygoid region, lateral sphenoid sinus, and retrobulbar orbit. Ann Otol Rhinol Laryngol 2005;114: Kim E, Duncavage JA. Prevention and management of complications in maxillary sinus surgery. Otolaryngol Clin North Am 2010;43: Stefansson P, Andreasson L, Jannert M. Caldwell-Luc operation: long-term results and sequelaes. Acta Otolaryngol Suppl 1988;449: Chandra RK, Kennedy DW. Surgical implications of an unusual anomaly of the infraorbital nerve. Ear Nose Throat J 2004;83: Mailleux P, Desgain O, Ingabire MI. Ectopic infraorbital nerve in a maxillary sinus septum: another potentially dangerous variant for sinus surgery. Jbr-Btr 2010;93: Busquets JM, Hwang PH. Endoscopic resection of sinonasal inverted papilloma: a meta-analysis. Otolaryngol Head Neck Surg 2006;134: Kamel R, Khaled A, Kandil T. Inverted papilloma: new classification and guidelines for endoscopic surgery. Am J Rhinol 2005;19: Schneyer MS, Milam BM, Payne SC. Sites of attachment of Schneiderian papilloma: a retrospective analysis. Int Forum Allergy Rhinol 2011;1:

5 14. Agthong S, Huanmanop T, Chentanez V. Anatomical variations of the supraorbital, infraorbital, and mental foramina related to gender and side. J Oral Maxillofac Surg 2005;63: Aziz SR, Marchena JM, Puran A. Anatomic characteristics of the infraorbital foramen: a cadaver study. J Oral Maxillofac Surg 2000;58: Cutright B, Quillopa N, Schubert W. An anthropometric analysis of the key foramina for maxillofacial surgery. J Oral Maxillofac Surg 2003;61: Hindy AM, Abdel-Raouf F. A study of infraorbital foramen, canal and nerve in adult Egyptians. Egypt Dent J 1993;39: Kazkayasi M, Ergin A, Ersoy M, Bengi O, Tekdemir I, Elhan A. Certain anatomical relations and the precise morphometry of the infraorbital foramen canal and groove: an anatomical and cephalometric study. Laryngoscope 2001;111: Xu H, Guo Y, Lv D, et al. Morphological structure of the infraorbital canal using three-dimensional reconstruction. J Craniofac Surg 2012;23: Jungell P, Lindqvist C. Paraesthesia of the infraorbital nerve following fracture of the zygomatic complex. Int J Oral Maxillofac Surg 1987;16: Schultze-Mosgau S, Erbe M, Rudolph D, Ott R, Neukam FW. Prospective study on post-traumatic and postoperative sensory disturbances of the inferior alveolar nerve and infraorbital nerve in mandibular and midfacial fractures. J Craniomaxillofac Surg 1999;27: Taicher S, Ardekian L, Samet N, Shoshani Y, Kaffe I. Recovery of the infraorbital nerve after zygomatic complex fractures: a preliminary study of different treatment methods. Int J Oral Maxillofac Surg 1993; 22: Lee UY, Nam SH, Han SH, Choi KN, Kim TJ. Morphological characteristics of the infraorbital foramen and infraorbital canal using threedimensional models. Surg Radiol Anat 2006;28: Song WC, Kim JN, Yoo JY, et al. Microanatomy of the infraorbital canal and its connecting canals in the maxilla using 3-D reconstruction of microcomputed tomographic images. J Craniofac Surg 2012;23:

PTERYGOPALATINE FOSSA

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