Endoscopic anatomy of the postganglionic pterygopalatine innervation of the posterolateral nasal mucosa.код для вставкиСкачать
ORIGINAL ARTICLE Endoscopic anatomy of the postganglionic pterygopalatine innervation of the posterolateral nasal mucosa Benjamin S. Bleier, MD1 Rodney J. Schlosser, MD2 Background: Recent anatomic dissections have redeﬁned the sinonasal parasympathetic pathway suggesting that individual rami project from the pterygopalatine ganglion (PPG) to innervate the nasal mucosa via multiple small nerve fascicles. The purpose of this study is correlate these anatomic descriptions with endoscopic ﬁndings and to deﬁne the paern and location of the posterolateral neurovascular rami. Methods: Eight cadaver heads were utilized for a total of 16 individual sides. A lateral nasal submucosal ﬂap was elevated while preserving all neurovascular bundles perforating the palatine bone. All nerves were traced proximally to conﬁrm their origin. Results: Excluding the sphenopalatine foraminal contents, accessory posterolateral nerves were noted in 87.5% (14/16) of specimens, 50% (7/14) of which contained greater than one. All nerves could be traced directly to the PPG or greater palatine nerve. Of the 25 accessory nerves iden- V idian neurectomy for the management of vasomotor rhinitis was first described in 19571 based upon studies of pterygopalatine anatomy performed a century prior. This procedure represents a nonselective autonomic denervation of the pterygopalatine ganglion (PPG) and, though effective, it is associated with significant and perhaps unnecessary risks including loss of reflex tearing and its attendant morbidities. Recent microanatomic studies 1 Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston, MA.; 2 Medical University of South Carolina, Charleston, SC Correspondence to: Benjamin S. Bleier, M.D., Massachusetts Eye and Ear Infirmary, 243 Charles St., Boston MA, 02114; e-mail: firstname.lastname@example.org. This work was performed at the Medical University of South Carolina, Charleston, SC. Podium presentation at the American Rhinologic Society Meeting, September 25, 2010, Boston, MA. Potential conflict of interest: None reported. Received: 10 August 2010; Accepted: 11 September 2010 DOI: 10.1002/alr.20011 View this article online at wileyonlinelibrary.com. 113 International Forum of Allergy & Rhinology, Vol. 1, No. 2, March/April 2011 tiﬁed, the most common location was posterosuperior to the horizontal aachment of the inferior turbinate (40%, 10/25). Conclusion: This study supports prior work suggesting that neurons project from the PPG via multiple individual postganglionic rami to supply the nasal mucosa. This new anatomic insight may be exploited to selectively lesion these nerve fascicles in patients with vasomotor rhinitis to improve outcomes while avoiding the morbidities associated with vidian neurectomy. C 2011 ARS-AAOA, LLC. Key Words: vidian neurectomy; vasomotor rhinitis; neurogenic rhinitis; pterygopalatine fossa; parasympathetic innervation How to Cite this Article: Bleier BS, Schlosser RJ. Endoscopic anatomy of the postganglionic pterygopalatine innervation of the posterolateral nasal mucosa. Int Forum Allergy Rhinol, 2011; 1:113–117 have redefined the parasympathetic pathway suggesting a direct route of postganglionic lacrimal and mucosal secretomotor innervation by multiple groups of small yet independent nerve fascicles. The identification of these nerves via an endoscopic approach would lend support to these findings and may provide an opportunity to improve upon the current surgical management of vasomotor rhinitis. The traditional understanding of the pterygopalatine autonomic pathways derive from studies performed by Lushka2 , Jendrassik3 , and Goldheizer4 in the latter half of the 19th century. Based on both anatomic and clinical observations, the postganglionic parasympathetic fibers were thought to travel exclusively with arborizations of the trigeminal nerve. This work provided not only an enhanced understanding of skull base anatomy but was also used to develop functional surgical approaches such as the vidian neurectomy for the treatment of neurogenic mediated pathologies. These studies perpetuated the idea that autonomic fibers projected to the sinonasal mucosa via the Bleier and Schlosser FIGURE 1. Endoscopic view of a left cadaveric pterygopalatine fossa dissection. The black outline depicts the course of the GPN along with its medial projections through the palatine bone. The DPA is outlined in white, along with its medial projections joining the accessory posterolateral neurovascular bundles. DPA = descending palatine artery; GPC = greater palatine canal; GPN = greater palatine nerve; PPF = pterygopalatine fossa. sphenopalatine neurovascular bundle. An additional consequence of this understanding was the unusually complex lacrimal pathway, in which secretomotor fibers created an anastomosis between the maxillary and zygomatic branches of the second and first trigeminal divisions through a communicating nerve.5 Recent microanatomic dissection of the pterygopalatine fossa (PPF) have redefined the secretomotor pathway. These studies have shifted the paradigm from individual named postganglionic autonomic nerves in favor of a multiplicity of efferent rami that project from the PPG to innervate the orbit and nasal mucosa via numerous groups of small nerve fascicles.5,6 The purpose of this study is correlate these microanatomic descriptions with endoscopic findings and to define the pattern and location of the postganglionic pterygopalatine fibers innervating the posterolateral nasal mucosa. Materials and methods Eight cadaver heads were obtained from the Department of Anatomy at Medical University of South Carolina (MUSC; Charleston, SC), for a total of 16 individual sides. A complete sphenoethmoidectomy and maxillary antrostomy was performed on each side, ensuring that the posterior fontanelle was resected to the level of the posterior maxillary wall. A mucoperiosteal flap was then elevated from the orbital process of the palatine bone down to the nasal FIGURE 2. Endoscopic view of right accessory posterolateral nerve dissections. (A-E) demonstrate examples of successively increasing numbers of accessory nerves found in different specimens (short white arrows indicate nerves, black oval indicates sphenopalatine foramen). (F) Demonstrates the presence of 4 individual nerves (short white arrows) along with an anastomotic loop (long white arrow). floor, taking care to preserve all neurovascular bundles perforating through the underlying bone. The lateral surface of the flap was probed to expose any anastomotic loops between individual nerve fascicles. The perpendicular plate of the palatine bone was then resected with a Kerrison rongeur to expose the contents of the PPF and greater palatine canal. The descending palatine artery (DPA) was dissected off the greater palatine nerve up to the level of the PPG. The sphenopalatine artery was ligated and reflected laterally to expose the entire PPG. All neurovascular bundles were then traced proximally to confirm their origin (Fig. 1). Results Exclusive of the sphenopalatine foramen (SPF) contents, additional posterolateral neurovascular rami were noted in 87.5% (14/16) of specimens, 50% (7/14) of which contained greater than 1 (Fig. 2). Of the 25 additional posterolateral nerves identified, the most common location (40%, International Forum of Allergy & Rhinology, Vol. 1, No. 2, March/April 2011 114 Innervation of the posterolateral nasal mucosa FIGURE 3. Illustration of medial aspect of the left palatine bone indicating the location of all 25 accessory posterolateral nerves identified. The closed dots represent nerves traversing directly through the bone whereas the open circles represent nerves that were associated with distinct foramina. 10/25) was within 1 cm posterosuperior to the horizontal attachment of the inferior turbinate; however, 28% (7/25) were noted within 5 mm anteroinferior to this attachment (Fig. 3). In 40% (10/25) of cases, the nerves exited the palatine bone via a foramen distinct from the SPF. Interfascicle anastomotic loops were identified in 13% (2/16) of specimens, all of which were associated with at least 3 accessory nerves. Intraspecimen symmetry was noted in only 1 in 8 (13%) of the heads. In all cases, each accessory nerve could be proximally traced directly to the PPG or greater palatine nerve. Discussion Within the past decade, microanatomic and histologic studies of the PPF have redefined our understanding of orbital and nasal parasympathetic pathways. In contrast to the traditional 19th century–derived teaching, these studies reveal that secretomotor fibers emanate from the PPG via multiple rami. These nerves project through the PPF and orbit as individual fascicles to innervate their targets without formally joining the trigeminal neural scaffold.5,6 The sympathetic pathways have also been reexamined utilizing tyrosine hydroxylase labeling, which has revealed duel pathways derived from both the vidian nerve as well as internal maxillary periarteriolar plexi.7 The postganglionic parasympathetic mucosal secretomotor fibers may be divided into 2 principal groups, the rami sphenoethmoidalis and the rami orbitonasalis, which innervate the posterior and ante- 115 International Forum of Allergy & Rhinology, Vol. 1, No. 2, March/April 2011 rior mucosa, respectively. Of note, the rami orbitonasalis gain access to the nasal cavity via the anterior ethmoidal foramen, thereby providing the opportunity for selective anterior or posterior parasympathectomies. This new anatomic framework also provides for a more intuitive understanding of the innervation of the lacrimal gland. A third group of secretomotor fibers, the rami lacrimales, project dorsally from the PPG toward the orbital apex, where they join the retro-orbital plexus before passing anteriorly to synapse on the lacrimal gland. Recognition of this pathway therefore obviates the need to invoke the presence of the controversial “communicating nerve,” which is both absent in other mammals and inconsistent in humans.5 Knowledge of the pterygopalatine autonomic pathways was exploited as early as 1935 by Ziegelman8 , who developed the transcranial greater superficial petrosal neurectomy1 in attempt to manage patients with vasomotor rhinitis. The transnasal vidian neurectomy was not described by Malcolmson9 until 1957, although it is generally attributed to Golding-Wood, who described his series of 40 patients in 1961.1 Predating modern endoscopic techniques, these early procedures were largely performed blindly and met with varying success. Recent studies have suggested success rates between 50% and 88%10,11 in the treatment of rhinorrhea, with other ancillary benefits including improvements in symptoms of sneezing and nasal obstruction. These subjective symptomatic improvements have also been correlated to histologic mucosal changes with reductions in stromal edema, eosinophilic cellular Bleier and Schlosser infiltration, mast cell levels, and histamine concentrations in denervated mucosa.11 Despite the reported clinical and histologic efficacy of vidian neurectomy, it has failed to gain widespread acceptance largely due to the morbidities associated with its lack of anatomic and autonomic selectivity. The site of the lesion involves the preganglionic secretomotor fibers to the lacrimal gland and thus loss of reflex tearing has been reported in 35% to 50% of cases.11,12 This decrease in lacrimation may be permanent and in severe cases can be associated with vision loss.12 The complete autonomic denervation associated with vidian neurectomy not only contributes to its resultant morbidities but may also limit its efficacy. While the goal of vidian neurectomy in patients with vasomotor rhinitis is a reduction in rhinorrhea, the complete parasympathetic denervation of the submucosal glands and goblet cells may be excessive leading to complaints of nasal dryness and crusting in up to 30% of patients.11 Similarly, effecting a simultaneous complete sympathectomy is likely counterproductive in the management of these patients given that it may actually contribute to symptoms of nasal obstruction and rhinorrhea.1 Long-term failure has also been reported as a significant risk associated with vidian neurectomy.11 While this may be attributable to poor anatomic localization and incomplete nerve sectioning in many of the early reports, the proximal location of the neural injury relative to the target end organ may also be implicated. Recent appreciation of the passage of postganglionic pterygopalatine fibers through the retroorbital plexus provides the theoretical opportunity for aberrant re-innervation through both the cavernous autonomic plexus and otic ganglion projections traveling with the accessory meningeal artery. Each of these reported risks may be directly attributable to the nonspecific site of autonomic denervation in vidian neurectomy. Consequently, shifting the site of lesion to the postganglionic parasympathetic rami would achieve the same physiologic effect while avoiding collateral injury to the lacrimal and sympathetic fibers. This idea has been adopted in a series of studies by Ikeda et al.,13.14 who describe the selective sectioning of the “posterior nasal nerve” in conjunction with inferior turbinate submucous resection. In these studies, the posterior nasal nerve is described as being comprised of both sympathetic and parasympathetic fibers that consistently and exclusively traverse the SPF to innervate the mucosa. While the authors report favorable success rates and mucosal histologic changes, this procedure is dependent on a traditional understanding of the postganglionic parasympathetic pathway. Our findings suggest that 90% of the patients in this study would have retained intact accessory secretomotor fibers to the posterolateral mucosa, which may serve to explain why 42% of patients reported submaximal improvement in symptom scores. The results of our dissection support prior microanatomic studies suggesting that the nasal mucosa is innervated by an array of small neurovascular fascicles. These fibers may be termed accessory posterolateral nerves to differentiate them from the contributions traversing the SPF. Our findings suggest that these rami are transmitted through multiple fissures and foramina throughout the palatine bone and may demonstrate anastomotic loops with both the SPF and other accessory nerves. The fact that these neurovascular bundles may be identified endoscopically provides the opportunity to isolate and completely transect these fibers. This selective postganglionic pterygopalatine parasympathectomy (SP3), would achieve a similar therapeutic effect to that of vidian neurectomy while sparing the rami lacrimales, thereby eliminating the risk of dry eye. This approach could also decrease the rate of postoperative nasal crusting and dryness by allowing for the ability to titrate the degree of anterior denervation through judicious sparing of the rami orbitonasalis. Furthermore, the SP3 technique would preserve a portion of the sympathetic contributions from the both the deep petrosal nerve and internal maxillary periarteriolar plexi. This would result in a relative preponderance of sympathetic tone, which may allow for improved outcomes with respect to nasal obstruction. Finally, the distal location of the site of lesion permits a complete resection of all anastomotic loops, which may help to reduce the rate of long-term re-innervation. One critique of this study is that while each of the accessory fibers were traced directly back to either the greater palatine nerve or PPG, in the absence of histologic data one cannot definitively prove that these nerves contain autonomic fibers. This inference is made, however, based on histologic studies which confirm that secretomotor fibers do project from the PPG in multiple individual fascicles, coupled with the fact that the greater palatine canal is known to transmit a portion of these autonomic fibers to innervate the hard palate. Future efforts will be directed toward exploring the role of these accessory posterolateral nerves through histologic and functional studies. Conclusion This study supports recent challenges to the traditional view of the pterygopalatine autonomic pathway by corroborating the existence of multiple individual postganglionic rami. This enhanced understanding of the complex neuroanatomy of the PPF may be exploited to help improve outcomes in the surgical management of neurogenic sinonasal disease while limiting morbidity. International Forum of Allergy & Rhinology, Vol. 1, No. 2, March/April 2011 116 Innervation of the posterolateral nasal mucosa References 1. 2. 3. 4. 5. 117 Golding-Wood PH. Observations on petrosal and vidian neurectomy in chronic vasomotor rhinitis. J Laryngol Otol. 1961;75:232–247. Luschka H. Die Nervi spheno-ethmoidalis. Müllers Arch Anat Physiol. 1857;313–326. Jendrássik E. Közlemény az egyetemi II belklinikáról. Az arczideg viszonyáról a Könnyelválasztáshoz. Orv Hétil. 1893;31:367–368. Goldheizer W. Beitrag zur Physiologie der Thränensecretion. Arch Augenheilk. 1894;28:7–21. Ruskell GL. 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