Anatomical Study of Critical Features on the Posterior Wall of the Maxillary Sinus: Clinical Implications

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1 The Laryngoscope VC 2014 The American Laryngological, Rhinological and Otological Society, Inc. Anatomical Study of Critical Features on the Posterior Wall of the Maxillary Sinus: Clinical Implications Liang Wang, MD; Ramazan Gun, MD; Ahmed Youssef, MD; Ricardo L. Carrau, MD; Daniel M. Prevedello, MD; Bradley A. Otto, MD; Leo Ditzel, MD Objectives/Hypothesis: Endonasal approaches to the pterygopalatine fossa for epistaxis or as part of a transpterygoid approach have been popularized somewhat by the ability to control the terminal branches of the maxillary artery (MA). Surgical landmarks are useful to identify these arteries. Therefore, identification of surface features on the posterior wall of the antrum that reflect the position of deeper structures within the pterygopalatine fossa would help predict anatomical position and orientation. Study Design: Describe the incidence of identifiable markings on the posterior wall of the maxillary sinus and ascertain their nature. Methods: An anatomical study of 18 cadaveric specimens noting and recording the presence, location, and number of prominences on the posterior wall of the antrum. After removing the bony wall, structure in the pterygopalatine fossa corresponding to the surface markings was noted. Results: Two prominences were identified. Prominence (P)1 extended from the upper part of the posterior wall of the maxillary sinus to the inferior orbit and corresponded to the infraorbital nerve. P2 was located at the middle part of the posterior wall, below P1, and corresponded to the MA. P2 was located medial to a vertical drop line where P1 connected to the posterior wall. P1 and P2 were found in 41.7% and 22.2%, respectively, of the specimens. Conclusions: This study defines features on the maxillary sinus posterior wall from an endoscopic perspective. These landmarks may be useful to identify the MA and its branches during surgery within the pterygopalatine fossa. Key Words: Maxillary sinus, sinonasal, anatomy, maxillary artery, sphenopalatine artery, infraorbital nerve, epistaxis, skull base surgery. Level of Evidence: N/A. Laryngoscope, 124: , 2014 From the Department of Otolaryngology Head and Neck Surgery (L.W., R.G., A.Y., R.L.C, B.A.O.); the Department of Neurological Surgery (D.M.P., L.D.), Wexner Medical Center, The Ohio State University, Columbus, Ohio, U.S.A.; and the Department of Otolaryngology Head and Neck Surgery (L.W.), First Affiliated Hospital, Zhengzhou University, Zhengzhou, Henan, , China Editor s Note: This Manuscript was accepted for publication March 11, The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Ricardo L. Carrau, MD, Department of Otolaryngology Head & Neck Surgery, Director of the Comprehensive Skull Base Surgery Program, Wexner Medical Center, The Ohio State University, Starling Loving Hall-Room P221, 320 West 10th Avenue, Columbus OH Ricardo.Carrau@osumc.edu DOI: /lary INTRODUCTION Ligation of the maxillary artery (MA) (previously known as internal maxillary artery) and its nasal terminal branches, namely the sphenopalatine and posterior nasal arteries (SPA & PNA, respectively) facilitate the removal of tumors of the sinonasal tract or skull base and is considered one of the most effective methods for the treatment of posterior or refractory epistaxis. These arteries are located in the pterygopalatine fossa behind the posterior wall of the maxillary sinus (PWMS); however, they present significant anatomical variation. 1,2 One disadvantage of the surgical ligation of the maxillary or sphenopalatine arteries is the potential for nerve injury (maxillary nerve, sphenopalatine ganglion, vidian nerve). 3,4 Previous studies concerning the ligation of the maxillary, sphenopalatine, and posterior nasal arteries have focused mainly on observations of the structural anatomy of the pterygopalatine fossa and measurements of the distances between these arteries and adjacent structures. 1,5 Despite these measurements and welldescribed surgical landmarks such as the crista ethmoidalis, it may be clinically difficult to guide their exposure and identification purely based on these data. In this study, we apply an endoscopic endonasal approach to make anatomical observations of the surface features on the posterior wall of the maxillary sinus and to establish their potential as landmarks for pterygopalatine fossa surgery. MATERIALS AND METHODS We dissected 18 adult specimens (36 sides) at the Anatomy Laboratory Toward Visuospatial Innovations in Otolaryngology and Neurosurgery at The Ohio State University. Specimens had been preserved in alcohol after intravascular injection with blue and red latex. Rod-lens Hopkins endoscopes of 4 mm in diameter and 18 cm in length, with 0 and 45 lenses coupled to a high-definition video camera and monitor (Karl Storz Endoscopy; Tuttlingen, Germany), were used during the dissections. Still images and video images were captured and recorded 2451

2 Fig. 1. Endoscopic view of Prominence 1 at the posterior wall of the left maxillary sinus. EMA 5 edge of maxillary antrostomy; P1 5 prominence 1; PWMS 5 posterior wall of maxillary sinus. using an AIDA digital video recorder system (Karl Storz Endoscopy; Tuttlingen, Germany). Our dissection included a pure endoscopic endonasal approach and the opening of a wide middle-meatal antrostomy, extending from the anterior aspect of the natural ostium to the level of the posterior wall of the maxillary sinus and from the superior aspect of the inferior turbinate to the inferomedial wall of the orbit. This window exposed the posterior wall of the maxillary sinus, thus allowing for its inspection with a 0 and 45 rod-lens endoscopes. We recorded the presence or absence of prominences and their location within the posterior wall of the maxillary sinus, number, and laterality. Subsequently, we dissected the mucosa off the posterior wall of the maxillary sinus and then fractured, elevated, and removed its bone with a periosteal dissector or Kerrison rongeur. The contents of the pterygopalatine fossa (PPF) were exposed after opening the posterior periosteum of the posterior wall of the maxillary sinus with scissors. Following this, we were able to ascertain which structure within the pterygopalatine fossa corresponded to the surface prominences. Fig. 3. Endoscopic view of the pterygopalatine fossa after removal of the posterior wall of the right maxillary sinus, showing that the maxillary nerve corresponds to P1 and that the position of the maxillary artery is lower than that of the maxillary nerve. EMA 5 edge of maxillary antrostomy; IMA 5 maxillary atery; IOA 5 infraorbital artery; ION- 5 infraorbital nerve; L 5 vertical line through starting point of P1 on the PMWS. RESULTS In some specimens, we identified two prominences on the posterior wall of the maxillary sinus, which we designated as P1 and P2. P1 corresponded to a seemingly vertical and elongated prominence extending from the upper part of the posterior wall of the maxillary sinus to the inferior orbital wall (i.e., superior wall of the antrum) and ultimately corresponded to the infraorbital nerve (Fig. 1 3). P2 was oriented in a horizontal axis at the middle part of the posterior wall of the maxillary sinus and corresponded to the maxillary artery (Fig. 4, Fig. 5). P1 and P2 could be further characterized as follows: Fig. 2. Endoscopic view of P1 at the posterior wall of the right maxillary sinus. L 5 vertical line through starting point of P1 on the PMWS; P1 5 prominence 1; MWM 5 medial wall of maxillary sinus; PWMS 5 posterior wall of maxillary sinus. Fig. 4. Endoscopic view of P1 and P2 at the posterior wall of the right maxillary sinus. EMA 5 edge of maxillary antrostomy; P1 5 prominence 1; P2 5 prominence 2; PWMS 5 posterior wall of maxillary sinus. 2452

3 Fig. 5. Endoscopic view demonstrating that the MA corresponds to P2, and that it is positioned lower than P1, medial of the L. EMA 5 edge of maxillary antrostomy; IMA 5 maxillary atery; P1 5 prominence 1; PWMS 5 posterior wall of maxillary sinus. 1. P1 was located in the upper part of the posterior wall of the maxillary sinus, forming a slightly inclined vertical bony ridge. It connected to the infraorbital canal in the roof of the maxillary sinus. 2. P2 was located in the middle of the posterior wall of the maxillary sinus, close to its medial wall. As a result of the great anatomical variations of the maxillary artery, the shape and position of P2 are not as constant as that of P1. 3. P2 is located below the level of P1. 4. A perpendicular line L was marked where P1 connected with the posterior wall of the maxillary sinus. P2 was located medial to L ; thus, all the terminal branches of the internal maxillary artery were always located in the medial side of L (Fig. 1 5). P1 (infraorbital nerve) was identified in 15 of 18 specimens (36 sides) for an incidence of 41.7%, with six of 18 specimens (33.3%) on the right side and nine of 18 specimens (50%) on the left side. Three of the 18 specimens had prominences bilaterally (16.7%). P2 (maxillary artery) was identified in eight of 18 specimens (36 sides) for an incidence of 22.2%, with five of 18 specimens (28%) on the right side and three of 18 specimens (16.7%) on the left side. Two specimens had prominences bilaterally (11.1%) (Table I). DISCUSSION Clinical concerns regarding the maxillary artery and its terminal branches mainly focus on their relevance as part of a surgical approach to remove tumors of the sinonasal tract or skull base or for the treatment of posterior or refractory epistaxis. Therefore, the main clinical application is the elective ligation during surgery of tumors of the nasal cavity, sinus, pterygopalatine fossa and other parts of the skull base or in lieu of a posterior packing to control posterior epistaxis. Transpterygoid approaches are the keystone for lateral and posterior extensions of extended endonasal endoscopic approaches because control of the vascular compartment of the pterygopalatine fossa is fundamental to the surgery. Approaches that transgress the pterygopalatine fossa (PPS) are useful to control lesions that arise or extend to the fossa or as a route to areas posterior or lateral to it, such as the lateral recess of the sphenoid sinus. 6,7 Pathologic processes in these areas are relatively rare; however, one may encounter juvenile nasopharyngeal angiofibromas, neurogenic tumors such as schwannomas, perineural extension of sinonasal malignancies, and meningoencephaloceles. The approach can be also performed to reach the cavernous sinus and middle cranial fossa for the surgical management of meningiomas, schwannomas, and invasive pituitary adenomas. In addition, it can be part of the approach to resect lesions of the petrous bone and the posterior fossa such as chordomas and chondrosarcomas. Surgeons have traditionally used open approaches such as midfacial degloving or lateral rhinotomy/medial maxillectomy and preauricular temporal subtemporal approaches to treat these lesions. Compared with these options, endoscopic endonasal transpterygoid approaches obviate the need for external incisions, osteotomies, and incidental injury to normal structures within the path of the corridor. Endoscopic endonasal transpterygoid approaches have paved the way for minimally invasive treatment of these lesions, providing excellent visualization and reducing morbidity. 8,9 Treatment of posterior epistaxis has always been a challenge for otolaryngologists. The terminal branches of the maxillary artery provide the main blood supply to the posterior nasal cavity; therefore, they are a target for surgical treatment. There are three main approaches for the surgical control of posterior epistaxis by ligating the main trunk of the maxillary artery or its terminal branches. The first is the transantral approach, which was first described by Sieffert 10 in 1928, reintroduced by Chandler and Serrins 11 in This approach is TABLE I. Incidence of P1 and P2 Markings on the Posterior Wall of Maxillary Sinus. Left Side Right Side Bilateral Total P1 P2 P1 P2 P1 P2 P1 P2 6/18 5/18 9/18 3/18 3/18 2/18 15/36 8/ % 28% 50% 16.7% 16.7% 11.1% 41.7% 22.2% 2453

4 technically challenging because the maxillary artery and its terminal branches are subject to significant anatomical variation. Chiu described three common configurations of the maxillary artery in the pterygopalatine fossa: a single looped form (18%) and two double-looped forms E (51%) and M (31%). 12 Although surgical failures are most commonly technical in nature and avoidable, at least 40% may be attributable to the surgeon s inability to locate the maxillary artery and its terminal branches within the pterygomaxillary fossa. 13 In addition, this approach is associated with cheek paresthesias as well as sensory problems secondary to inadvertent trauma to the maxillary nerve, sphenopalatine ganglion, or vidian nerve. The second approach is the intraoral ligation of maxillary artery is described by Maceri, 14 who effectively applied this approach to ligate the maxillary artery on 14 patients. The intraoral technique is versatile, relatively fast, effective, and does not require the operating microscope. However, its main disadvantages are the ensuing postoperative swelling of the cheek and trismus, experienced by four of his 14 patients (recovered 3 months after surgery). These complications hindered the popularization of this approach. The third approach is the endonasal endoscopic ligation of sphenopalatine artery. The microsurgical ligature of the sphenopalatine artery was introduced by Prades 15 in 1976 and subsequently reported in 1987 by Sulsenti et al. 16 In 1992, Budrovich and Saetti 17 were the first to report the endoscopic approach to ligation of the sphenopalatine artery. Bolger et al. 18 reported on the use of the crista ethmoidalis, a small crest arising from the palatine bone anterior to the sphenopalatine artery, as a surgical landmark. However, the ethmoidal crest is not always well developed or may not be readily identified. In addition, there are some anatomical variations, such as the existence of an accessory foramen, which are found in approximately 10% of anatomical specimens or in variable branching of the artery. 19,20 All variations can lead to failure of the sphenopalatine and posterior nasal arteries ligation. Since its emergence, the use of rod-lens nasal endoscopy in sinonasal surgery has been increasing. In recent years, its use has been expanded further into skull-base surgery applications. Endoscopic ligation of the terminal branches of the maxillary artery is now a common surgery. Traditionally, maxillary artery ligation for epistaxis was performed via transantral or transoral approach. A transantral approach adopts a modified Caldwell-Luc technique that is familiar to most otolaryngologists. It is relatively straightforward and can be performed in case of an emergency where endoscopic equipment is not available or when significant trauma or tumor impedes an endonasal approach. Compared to surgeries via the transantral approach, surgeries via transoral approach are conceptually simpler 21 and are possible in cases when transantral or endonasal approach is not available, such as severe maxillary fracture, select pediatric patients, and tumor invasion in the maxillary sinus. Wang et al. 22 performed a ligation of the internal maxillary artery through transoral 2454 approach before completing a total maxillectomy for the treatment of sinonasal tumors, reducing intraoperative bleeding significantly. Every otolaryngologist who performs ligation of the maxillary artery should be familiar with intraoral and transantral techniques. References in the literature about P1 and P2 features are sparse; however, we speculate that these structures may affect the pneumatization and development of the maxillary sinus. Ossification of the maxilla commences in the sixth or seventh week of embryonic life as one center. Subsequently, extensions develop into the orbital, alveolar, and palatine processes. The infraorbital vessel and nerve occupy for some time a mere groove on the orbital surface of the maxilla, later to become encased by a lamina of bone. 23 In its lateral development, the average maxillary sinus at the end of the first year has come into close relation with the infraorbital nerve. During the second year, the most lateral portion of the sinus passes beneath the nerve, leaving a ridge on the roof of the sinus that distinctly indicates the course of the nerve in its canal. The degree of prominence that the ridge may assume varies greatly. 24 This is the first study to describe the anatomical features of the posterior wall of the maxillary sinus and their clinical implications. Anatomical features of the posterior wall of the maxillary sinus can be used to locate the maxillary artery and its terminal branches. P2 always lies inferior and medial to P1. Therefore, as long as we dissect below P1, damage to the infraorbital nerve and maxillary nerve will be avoided. An operation being performed within the medial side of L line will ensure the exposure of the trunk of the internal maxillary artery. These prominences can also function as landmarks to identify structures like foramen rotundum and the pterygoid (vidian) canal. However, these prominences are not always present, which to some extent limits their clinical application. CONCLUSION This is the first study to define the surface features on the posterior wall of maxillary sinus from an endoscopic perspective. These findings have clinical significance for the ligation of the maxillary artery or its branches during surgery for refractory epistaxis and for surgery addressing tumors of the nasal cavity, paranasal sinuses, and pterygopalatine fossa. BIBLIOGRAPHY 1. Shires CB, Boughter JD, Sebelik ME. Sphenopalatine artery ligation: a cadaver anatomic study. 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