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Endoscopic anatomy of the postganglionic pterygopalatine innervation of the posterolateral nasal mucosa.

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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: bleierb@gmail.com.
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
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