O l f a c t i o n in En d o s c o p i c S i n u s a n d Sk u l l B a s e S u r ge ry Christopher F. Thompson, David B. Conley, MD
MD*,
Robert C. Kern,
MD,
KEYWORDS Endoscopic sinus surgery Anosmia Hyposmia Smell Olfaction Skull base KEY POINTS Smell loss in chronic rhinosinusitis is caused by obstruction from polyps, nasal discharge, and mucosal edema, as well as inflammatory damage to the olfactory epithelium. The effect of endoscopic sinus surgery on olfaction is difficult to predict. Addressing olfaction with patients preoperatively is recommended before endoscopic sinus and skull base surgery. If surgery is required in the olfactory cleft, then meticulous dissection is recommended to optimize olfactory function postoperatively.
INTRODUCTION
Olfactory dysfunction is a common complaint for patients visiting otolaryngology offices, with chronic rhinosinusitis (CRS) accounting for 14% to 25% of patients.1,2 Of patients with CRS, 28% to 84% complain of a decreased sense of smell.3–5 Hyposmia decreases a person’s enjoyment of food and can reduce their overall quality of life.6–8 Furthermore, the inability to detect spoiled food, fire, toxic fumes, and gas leaks can be dangerous.2 There are 2 mechanisms by which chronic rhinosinusitis decreases olfaction. First, the obstruction of the olfactory cleft from polyps, nasal discharge, and mucosal edema decreases the ability of the odorant to reach the olfactory receptors.3,9 Second, underlying epithelial inflammatory damage from CRS can affect the health of the olfactory neurons or the neurons’ ability to transmit olfaction to the brain.9 Addressing olfaction with patients who have CRS is important, because a loss of smell is correlated with a lower quality of life.6–8
Funding: No financial funding or support. Conflict of Interest: None. Department of Otolaryngology, Northwestern University, Chicago, IL, USA * Corresponding author. Department of Otolaryngology and Head & Neck Surgery, Northwestern University, 675 North St. Clair, Galter Pavilion, 15th Floor, Room 200, Chicago, IL 60611. E-mail address: [email protected] Otolaryngol Clin N Am - (2015) -–http://dx.doi.org/10.1016/j.otc.2015.05.007 0030-6665/15/$ – see front matter Ó 2015 Elsevier Inc. All rights reserved.
oto.theclinics.com
2
Thompson et al
Discussing olfaction is especially important in patients undergoing endoscopic sinus surgery (ESS) for CRS or endoscopic endonasal surgery for skull base tumors.10,11 Without clear and consistent evidence that ESS improves smell, patients’ postoperative expectations need to be addressed, which includes counseling that olfactory loss may persist or even worsen despite surgery and medical therapy.4,12–14 Addressing olfaction is also important before endoscopic endonasal skull base surgery, because smell loss may occur during tumor resection or harvest of a large nasoseptal flap for reconstruction.15–18 In a survey of practicing otolaryngologists, roughly 40% routinely discuss the potential for postoperative anosmia with patients.11 This figure is important because 17% of malpractice litigation cases from ESS pertain to smell loss or complete anosmia.10 This article reviews the anatomy and physiology of smell, presents options for olfactory testing that can be done in clinic, discusses surgical and medical considerations to optimize olfaction, and emphasizes the importance of including olfaction in the preoperative consent. OLFACTION ANATOMY AND PHYSIOLOGY
The olfactory cleft is composed of pseudostratified columnar epithelium located below the cribriform plate and extending inferiorly along the septum for about 1 cm. Parasagittally, the olfactory epithelium is roughly 2 cm in length along the superoposterior septum and can extend posteriorly to the face of the sphenoid sinus and laterally to the upper portion of the superior and middle turbinates.2,19 The olfactory epithelium contains bipolar neurons, which have ciliated dendrites that extend to the epithelial surface. The cilia have G protein–coupled and cyclic AMP–coupled receptors that are triggered by odorants. Once activated, the signal is propagated along the axons of the olfactory sensory neurons, which together form cranial nerve I. The axons pass through the cribriform plate and synapse in the olfactory bulb. Second-order neurons then send the olfactory signals to the amygdala and primary sensory cortex.9 In addition to olfactory sensory neurons, the olfactory cleft epithelium contains a balance of supporting cells and mucus-secreting glands. Any disruption in the olfaction cascade of events can lead to smell dysfunction. In CRS, either the odorant is unable to reach the receptor or the signal transduction is ineffectively relayed to the brain because of inflammatory changes in the neuroepithelium.9 OLFACTORY TESTING
Olfactory testing has not been standardized in the literature, but testing measures are useful in documenting olfactory dysfunction in a patient complaining of smell loss. Testing can be subjective or objective. Formal subjective testing includes the 0 to 100-mm visual analog scale (VAS) or any specific item on a sinonasal-specific quality-of-life questionnaire such as item #5 on the Sinonasal Outcomes Test (SNOT)-22.20,21 For the VAS, patients rate their sense of smell from anosmia (0 mm) to perfect olfaction (100 mm).20 On the SNOT-22, smell is graded on a Likert scale from 0 (worst) to 5 (best).21 Objective olfactory testing includes threshold tests and identification tests.22 The most common threshold test is the butanol threshold test (BTT; Sigma-Aldrich, St Louis, MO). This test includes a dilutional series of butanol, with the lowest butanol concentration tested first. The patient is given 2 solution bottles, 1 with diluted butanol and 1 with water or mineral oil, and is forced to choose which bottle has the odorant.22–24 The smell threshold is determined when the bottle with the lowest butanol concentration is detected correctly 5 consecutive times.14,22–24
Olfaction in Sinus and Skull Base Surgery
Smell identification tests use common odorants in order to test how well a person can detect normal environmental odors.22 There are several smell identification tests, including the most widespread and commercially available University of Pennsylvania Smell Identification Test (UPSIT; Sensonics, Inc, Haddon Heights, NJ).25 The UPSIT was first described in 1984 and consists of 40 multiple-choice scratch-and-sniff forced-identification questions.25 There are multiple-choice answers instead of relying on free recall controls for potential failure in word recall. A score of greater than 35 is normal (range, 0–40). There are 4 answers for each question, thus a patient with anosmia should answer about 10 items correctly by chance alone. A score of 5 or less suggests malingering.25 Other odor identification tests include the Crosscultural Smell Identification Test (CCSIT; Sensonics, Haddon Heights, NJ),26 Brief Smell Identification Test (Sensonics, Inc, Haddon Heights, NJ),27 Smell Diskettes Olfaction Test (Novimed, Dietikon, Switzerland),13,15 and Barcelona Smell Test (BAST-24; Barcelona, Spain).28 Another olfaction measure used is the Sniffin’ Sticks test (Burghart, Wedel, Germany), which uses a series of pens for threshold testing, discrimination testing, and identification testing.24,29 Smell threshold is determined at the lowest butanol concentration at which a patient can correctly detect the butanol pen twice in a row. For discrimination, a patient is presented with 3 pens and asked to identify which one has an odorant. For identification testing, an odorant pen is presented to the patient, and the patient must select the correct odor from a list of 4 choices. CONDUCTIVE OLFACTORY LOSS
Patients are more likely to have smell loss when polyps, nasal discharge, and mucosal edema obstruct odorant molecules from reaching the olfactory cleft.3 This conductivetype olfactory loss is likely a major reason why patients with CRS with nasal polyps (CRSwNP) have a greater chance of smell loss than patients with CRS without nasal polyps (CRSsNP).3,30 Alt and colleagues3 found that higher scores on both the Lund-McKay Radiologic Score and the Lund-Kennedy Endoscopy Score correlated with smell loss in patients with CRSwNP. In patients with CRSsNP, the LundKennedy score only weakly correlated with smell loss, and there was no correlation with severity of Lund-McKay score. Besides overall Lund-McKay score, several investigators have shown that increased opacification on computed tomography (CT) specifically within the olfactory cleft correlates with worsening results on olfactory testing.23,26 Kim and colleagues26 graded the olfactory cleft opacification on CT scan as mild (0%–25%), moderate (25%–75%), and severe (>75%). Six months postoperatively the improvement in olfactory scores, on both the odor threshold and identification tests, was significantly better in the mild group than in the moderate or severe groups (P35), only 3 (25%) had an inflammatory response. In addition to an influx of inflammatory cells, there is a loss of normal olfactory epithelial architecture in patients with CRS and hyposmia compared with those patients with CRS and normosmia.32 Biopsy specimens in patients with CRS and anosmia have revealed an atrophic and thin olfactory epithelium, a decreased ratio of olfactory receptor neurons to supporting cells, and dendrites from olfactory neurons that are tortuous in their course to the surface. These histologic studies suggest that the olfactory dysfunction experienced by patients with CRS also results from the inflammation and damage within the olfactory epithelium in addition to the obstruction from polyps and nasal discharge. IMPACT OF ENDOSCOPIC SINUS SURGERY ON OLFACTION IN CHRONIC RHINOSINUSITIS
Ensuring that patients understand the goals of ESS during the surgeon’s preoperative discussion is critical, so that reasonable expectations can be achieved. When conservative medical management fails, ESS is an excellent treatment modality to improve sinonasal drainage, remove obstructing polyps and debris, and allow better access for topical medications and irrigations to reach the sinus cavities. Ample evidence in the literature supports ESS, because overall quality of life is better, endoscopic scores are improved, and patients’ symptoms are better controlled.24,27,33–35 An improvement in sinonasal symptoms, such as thick nasal discharge and nasal obstruction, can reasonably be achieved with appropriate surgery and postoperative care.35 However, the return of olfaction is difficult to predict. The only significant prognostic factor that seems consistent across several studies is that patients with CRSwNP have a better chance for improvement in smell compared with those patients with CRSsNP.12,36,37 Removing polyps alleviates obstruction, improves nasal airflow, and allows odorant molecules a better chance to reach the olfactory receptors. There is no gold standard by which olfaction is tested or reported. Testing measures used to assess outcomes after surgery are generally combinations of the previously mentioned subjective questionnaires and objective odor threshold or identification tests. The outcomes vary widely, and olfactory improvement is unpredictable, ranging from roughly 5% to 85%.4,12–14,30,38 In a study of 70 patients undergoing ESS, Jiang and colleagues4 reported no significant differences in UPSIT or BTT scores before or at least 6 months after surgery, because only 6% of patients noted an improvement in their smell. A 1996 study using the UPSIT showed that 52% of patients have an improvement in smell after surgery and 48% do not at an average of 18 months after
Olfaction in Sinus and Skull Base Surgery
surgery.38 Pade and Hummel12 used Sniffin’ Sticks and found that, 4 months following sinus surgery, smell improved in 23%, did not change in 65%, and decreased in 9% of patients. In a long-term study of smell outcomes 5 years after ESS, Briner and colleagues13 reported that 27 of 34 (79%) patients improved on the 100-mm VAS from 28.4 mm before surgery to 58.5 mm. On the BTT, 85% of patients improved, 9% had no improvement, and 6% had deterioration of smell. In evaluating patients based on polyp status with the VAS, Oka and colleagues30 found that those with CRSwNP improved from 14.0 mm before surgery to 57.9 mm at 3 months, 59.1 mm at 6 months, 32.3 mm at 12 months, and 45.3 mm at 24 months. Those patients with CRSsNP had a higher preoperative score of 30.9 mm, which improved to 53.8 mm at 3 months, 54.4 mm at 6 months, 48.9 mm at 12 months, and 54.2 mm at 24 months. Several studies examined whether the degree of smell loss preoperatively can predict recovery after surgery. Litvack and colleagues36 compared the improvement in smell for hyposmics and anosmics and found that only anosmics have a significant improvement in olfaction after ESS. The 40-item UPSIT was used as the objective measure; men with scores of 19 to 33 and women with scores of 19 to 34 were considered hyposmics, and anosmics were men and women with scores of 6 to 18. Anosmics significantly improved on the UPSIT from a preoperative mean of 9.7 to 21.3 6 months after surgery, and this improvement was sustained at 12 months after surgery (mean, 21.7). Regarding hyposmics, there was no significant change in the UPSIT scores from before surgery (28.8) to 6 months (30.0) or 12 months (29.5) after surgery. A second study also suggested that patients with anosmia may be more likely to benefit from ESS than those with hyposmia, but the difference in smell recovery between the two groups was not significant. Using the UPSIT, 60.6% of anosmics improved compared with 42.4% of hyposmics.39 PERIOPERATIVE CONSIDERATIONS FOR OLFACTORY PRESERVATION DURING ENDOSCOPIC SINUS SURGERY FOR CHRONIC RHINOSINUSITIS
Because the predominant location of olfactory sensory neurons has been established to be along the superoposterior septum and upper portion of the turbinates, preservation of these structures is generally recommended when possible. Meticulous dissection should be used near turbinates and the superior septum to lessen the chance of mucosal stripping, unintentional turbinectomies, and damage to the cribriform. Despite the turbinates’ potential contribution to olfaction, turbinate resection may be considered when they severely obstruct the nasal airflow, impede postoperative debridements, or are degenerated from the inflammatory process.40 Careful debulking of polyps medial to the turbinate may also be considered by experienced surgeons who have carefully reviewed the anatomy, so as not to strip the olfactory epithelium or disrupt the skull base causing a cerebrospinal fluid (CSF) leak.41 Several studies have evaluated whether turbinate resection and debulking olfactory cleft polyps affects olfaction.41–44 Turbinates play a normal role in maintenance of laminar airflow and humidification of inhaled air.40 However, several studies show that partial resection of the superior turbinate or removal of the middle turbinate does not have a negative impact on olfaction.42,43 Resection of the inferior third of the superior turbinate is often done during a transethmoid sphenoidotomy to visualize and access the natural sphenoid ostium.45 Say and colleagues42 analyzed whether this partial resection of the superior turbinate affects smell. In 55 partial superior turbinate specimens, only 9 (16%) contained olfactory nerve fibers. Postoperatively, none of these 9 nostrils had a decrease in smell as measured by the 12-item CCSIT (Sensonics, Inc, Haddon Heights, NJ). Regarding
5
6
Thompson et al
middle turbinates, Friedman and colleagues46 found no significant difference in the postoperative change in UPSIT scores in 38 patients who had partial middle turbinate resection and 26 patients who did not as part of their ESS. In the multi-institutional study by Soler and colleagues,43 patients who had bilateral middle turbinate resection were more likely to have worse CRS burden on CT and nasal endoscopy. Patients with bilateral middle turbinate resection had a more significant improvement in smell identification test scores than those who had the middle turbinates preserved. In these more severe CRS cases, removal of the likely degenerated middle turbinates potentially allowed better access for odorants to reach the olfactory cleft.43 Contrary to these studies, Nguyen and colleagues44 found that, in revision sinus surgery, a history of middle turbinate resection was a negative prognostic indicator for smell improvement after surgery. Although the results of these studies analyzing turbinate resection are inconsistent, middle turbinate resection may be considered when disease burden is high and the turbinates are degenerated. If the middle turbinate is appears normal on endoscopy, turbinate preservation is recommended. Polyps medial to the middle turbinates block odorants from reaching the olfactory cleft, but are located intimately with the olfactory epithelium along the cribriform plate, middle turbinate, superior turbinate, and superior septum.41 These polyps can often be left, without any attempt at debulking the obstructive load, for fear that removal would damage the cribriform, decrease smell, or cause a CSF leak. Masaki and Tanaka41 described having a low threshold for septoplasty and carefully lateralizing the middle turbinate before olfactory cleft surgery in order to widen the area for polyp removal. They recommended olfactory cleft polypectomy or debulking because up to a third of polyps can arise from the olfactory cleft.41 No complications were reported and olfaction was not analyzed. In evaluating olfaction after olfactory cleft surgery, Nguyen and colleagues44 reported that either debulking of nasal polyps or removal of respiratory epithelial adenomatoid hamartomas can improve smell. The Sniffin’ Sticks test was used. All patients with normosmia before olfactory cleft surgery conserved their sense of smell postoperatively. Of the patients with hyposmia or anosmia preoperatively, 45% had an improvement in smell and 55% had no change after surgery. No complications were reported, and none of the 74 patients in the study had a CSF leak. PERIOPERATIVE CONSIDERATIONS IN THE ENDONASAL APPROACH TO THE SKULL BASE
The endoscopic endonasal approach to anterior skull base lesions is growing in popularity because of the enhanced visualization and decreased morbidity.47 Despite its increased use, normal anatomic structures are often removed or altered in order to endoscopically access the skull base and allow a 4-hand technique or to reconstruct the surgical defect. When approaching the skull base, limiting the disruption along the nasal corridor and only using nasoseptal flaps when necessary for reconstruction may lessen the postoperative morbidity and nasal symptoms.48 A recent study compared postoperative olfaction with the Smell Diskettes Olfaction Test (Novimed, Dietikon, Switzerland) in patients who had pituitary tumors removed via the transseptal microscopic approach versus the endoscopic endonasal approach.15 At 6 months after surgery, 13 of 25 patients had hyposmia and 5 of 25 patients had anosmia in the microscopic approach group. None of the patients in the endoscopic approach group had smell dysfunction. This difference in smell recovery between the two groups was significant (P
MD*,
Robert C. Kern,
MD,
KEYWORDS Endoscopic sinus surgery Anosmia Hyposmia Smell Olfaction Skull base KEY POINTS Smell loss in chronic rhinosinusitis is caused by obstruction from polyps, nasal discharge, and mucosal edema, as well as inflammatory damage to the olfactory epithelium. The effect of endoscopic sinus surgery on olfaction is difficult to predict. Addressing olfaction with patients preoperatively is recommended before endoscopic sinus and skull base surgery. If surgery is required in the olfactory cleft, then meticulous dissection is recommended to optimize olfactory function postoperatively.
INTRODUCTION
Olfactory dysfunction is a common complaint for patients visiting otolaryngology offices, with chronic rhinosinusitis (CRS) accounting for 14% to 25% of patients.1,2 Of patients with CRS, 28% to 84% complain of a decreased sense of smell.3–5 Hyposmia decreases a person’s enjoyment of food and can reduce their overall quality of life.6–8 Furthermore, the inability to detect spoiled food, fire, toxic fumes, and gas leaks can be dangerous.2 There are 2 mechanisms by which chronic rhinosinusitis decreases olfaction. First, the obstruction of the olfactory cleft from polyps, nasal discharge, and mucosal edema decreases the ability of the odorant to reach the olfactory receptors.3,9 Second, underlying epithelial inflammatory damage from CRS can affect the health of the olfactory neurons or the neurons’ ability to transmit olfaction to the brain.9 Addressing olfaction with patients who have CRS is important, because a loss of smell is correlated with a lower quality of life.6–8
Funding: No financial funding or support. Conflict of Interest: None. Department of Otolaryngology, Northwestern University, Chicago, IL, USA * Corresponding author. Department of Otolaryngology and Head & Neck Surgery, Northwestern University, 675 North St. Clair, Galter Pavilion, 15th Floor, Room 200, Chicago, IL 60611. E-mail address: [email protected] Otolaryngol Clin N Am - (2015) -–http://dx.doi.org/10.1016/j.otc.2015.05.007 0030-6665/15/$ – see front matter Ó 2015 Elsevier Inc. All rights reserved.
oto.theclinics.com
2
Thompson et al
Discussing olfaction is especially important in patients undergoing endoscopic sinus surgery (ESS) for CRS or endoscopic endonasal surgery for skull base tumors.10,11 Without clear and consistent evidence that ESS improves smell, patients’ postoperative expectations need to be addressed, which includes counseling that olfactory loss may persist or even worsen despite surgery and medical therapy.4,12–14 Addressing olfaction is also important before endoscopic endonasal skull base surgery, because smell loss may occur during tumor resection or harvest of a large nasoseptal flap for reconstruction.15–18 In a survey of practicing otolaryngologists, roughly 40% routinely discuss the potential for postoperative anosmia with patients.11 This figure is important because 17% of malpractice litigation cases from ESS pertain to smell loss or complete anosmia.10 This article reviews the anatomy and physiology of smell, presents options for olfactory testing that can be done in clinic, discusses surgical and medical considerations to optimize olfaction, and emphasizes the importance of including olfaction in the preoperative consent. OLFACTION ANATOMY AND PHYSIOLOGY
The olfactory cleft is composed of pseudostratified columnar epithelium located below the cribriform plate and extending inferiorly along the septum for about 1 cm. Parasagittally, the olfactory epithelium is roughly 2 cm in length along the superoposterior septum and can extend posteriorly to the face of the sphenoid sinus and laterally to the upper portion of the superior and middle turbinates.2,19 The olfactory epithelium contains bipolar neurons, which have ciliated dendrites that extend to the epithelial surface. The cilia have G protein–coupled and cyclic AMP–coupled receptors that are triggered by odorants. Once activated, the signal is propagated along the axons of the olfactory sensory neurons, which together form cranial nerve I. The axons pass through the cribriform plate and synapse in the olfactory bulb. Second-order neurons then send the olfactory signals to the amygdala and primary sensory cortex.9 In addition to olfactory sensory neurons, the olfactory cleft epithelium contains a balance of supporting cells and mucus-secreting glands. Any disruption in the olfaction cascade of events can lead to smell dysfunction. In CRS, either the odorant is unable to reach the receptor or the signal transduction is ineffectively relayed to the brain because of inflammatory changes in the neuroepithelium.9 OLFACTORY TESTING
Olfactory testing has not been standardized in the literature, but testing measures are useful in documenting olfactory dysfunction in a patient complaining of smell loss. Testing can be subjective or objective. Formal subjective testing includes the 0 to 100-mm visual analog scale (VAS) or any specific item on a sinonasal-specific quality-of-life questionnaire such as item #5 on the Sinonasal Outcomes Test (SNOT)-22.20,21 For the VAS, patients rate their sense of smell from anosmia (0 mm) to perfect olfaction (100 mm).20 On the SNOT-22, smell is graded on a Likert scale from 0 (worst) to 5 (best).21 Objective olfactory testing includes threshold tests and identification tests.22 The most common threshold test is the butanol threshold test (BTT; Sigma-Aldrich, St Louis, MO). This test includes a dilutional series of butanol, with the lowest butanol concentration tested first. The patient is given 2 solution bottles, 1 with diluted butanol and 1 with water or mineral oil, and is forced to choose which bottle has the odorant.22–24 The smell threshold is determined when the bottle with the lowest butanol concentration is detected correctly 5 consecutive times.14,22–24
Olfaction in Sinus and Skull Base Surgery
Smell identification tests use common odorants in order to test how well a person can detect normal environmental odors.22 There are several smell identification tests, including the most widespread and commercially available University of Pennsylvania Smell Identification Test (UPSIT; Sensonics, Inc, Haddon Heights, NJ).25 The UPSIT was first described in 1984 and consists of 40 multiple-choice scratch-and-sniff forced-identification questions.25 There are multiple-choice answers instead of relying on free recall controls for potential failure in word recall. A score of greater than 35 is normal (range, 0–40). There are 4 answers for each question, thus a patient with anosmia should answer about 10 items correctly by chance alone. A score of 5 or less suggests malingering.25 Other odor identification tests include the Crosscultural Smell Identification Test (CCSIT; Sensonics, Haddon Heights, NJ),26 Brief Smell Identification Test (Sensonics, Inc, Haddon Heights, NJ),27 Smell Diskettes Olfaction Test (Novimed, Dietikon, Switzerland),13,15 and Barcelona Smell Test (BAST-24; Barcelona, Spain).28 Another olfaction measure used is the Sniffin’ Sticks test (Burghart, Wedel, Germany), which uses a series of pens for threshold testing, discrimination testing, and identification testing.24,29 Smell threshold is determined at the lowest butanol concentration at which a patient can correctly detect the butanol pen twice in a row. For discrimination, a patient is presented with 3 pens and asked to identify which one has an odorant. For identification testing, an odorant pen is presented to the patient, and the patient must select the correct odor from a list of 4 choices. CONDUCTIVE OLFACTORY LOSS
Patients are more likely to have smell loss when polyps, nasal discharge, and mucosal edema obstruct odorant molecules from reaching the olfactory cleft.3 This conductivetype olfactory loss is likely a major reason why patients with CRS with nasal polyps (CRSwNP) have a greater chance of smell loss than patients with CRS without nasal polyps (CRSsNP).3,30 Alt and colleagues3 found that higher scores on both the Lund-McKay Radiologic Score and the Lund-Kennedy Endoscopy Score correlated with smell loss in patients with CRSwNP. In patients with CRSsNP, the LundKennedy score only weakly correlated with smell loss, and there was no correlation with severity of Lund-McKay score. Besides overall Lund-McKay score, several investigators have shown that increased opacification on computed tomography (CT) specifically within the olfactory cleft correlates with worsening results on olfactory testing.23,26 Kim and colleagues26 graded the olfactory cleft opacification on CT scan as mild (0%–25%), moderate (25%–75%), and severe (>75%). Six months postoperatively the improvement in olfactory scores, on both the odor threshold and identification tests, was significantly better in the mild group than in the moderate or severe groups (P35), only 3 (25%) had an inflammatory response. In addition to an influx of inflammatory cells, there is a loss of normal olfactory epithelial architecture in patients with CRS and hyposmia compared with those patients with CRS and normosmia.32 Biopsy specimens in patients with CRS and anosmia have revealed an atrophic and thin olfactory epithelium, a decreased ratio of olfactory receptor neurons to supporting cells, and dendrites from olfactory neurons that are tortuous in their course to the surface. These histologic studies suggest that the olfactory dysfunction experienced by patients with CRS also results from the inflammation and damage within the olfactory epithelium in addition to the obstruction from polyps and nasal discharge. IMPACT OF ENDOSCOPIC SINUS SURGERY ON OLFACTION IN CHRONIC RHINOSINUSITIS
Ensuring that patients understand the goals of ESS during the surgeon’s preoperative discussion is critical, so that reasonable expectations can be achieved. When conservative medical management fails, ESS is an excellent treatment modality to improve sinonasal drainage, remove obstructing polyps and debris, and allow better access for topical medications and irrigations to reach the sinus cavities. Ample evidence in the literature supports ESS, because overall quality of life is better, endoscopic scores are improved, and patients’ symptoms are better controlled.24,27,33–35 An improvement in sinonasal symptoms, such as thick nasal discharge and nasal obstruction, can reasonably be achieved with appropriate surgery and postoperative care.35 However, the return of olfaction is difficult to predict. The only significant prognostic factor that seems consistent across several studies is that patients with CRSwNP have a better chance for improvement in smell compared with those patients with CRSsNP.12,36,37 Removing polyps alleviates obstruction, improves nasal airflow, and allows odorant molecules a better chance to reach the olfactory receptors. There is no gold standard by which olfaction is tested or reported. Testing measures used to assess outcomes after surgery are generally combinations of the previously mentioned subjective questionnaires and objective odor threshold or identification tests. The outcomes vary widely, and olfactory improvement is unpredictable, ranging from roughly 5% to 85%.4,12–14,30,38 In a study of 70 patients undergoing ESS, Jiang and colleagues4 reported no significant differences in UPSIT or BTT scores before or at least 6 months after surgery, because only 6% of patients noted an improvement in their smell. A 1996 study using the UPSIT showed that 52% of patients have an improvement in smell after surgery and 48% do not at an average of 18 months after
Olfaction in Sinus and Skull Base Surgery
surgery.38 Pade and Hummel12 used Sniffin’ Sticks and found that, 4 months following sinus surgery, smell improved in 23%, did not change in 65%, and decreased in 9% of patients. In a long-term study of smell outcomes 5 years after ESS, Briner and colleagues13 reported that 27 of 34 (79%) patients improved on the 100-mm VAS from 28.4 mm before surgery to 58.5 mm. On the BTT, 85% of patients improved, 9% had no improvement, and 6% had deterioration of smell. In evaluating patients based on polyp status with the VAS, Oka and colleagues30 found that those with CRSwNP improved from 14.0 mm before surgery to 57.9 mm at 3 months, 59.1 mm at 6 months, 32.3 mm at 12 months, and 45.3 mm at 24 months. Those patients with CRSsNP had a higher preoperative score of 30.9 mm, which improved to 53.8 mm at 3 months, 54.4 mm at 6 months, 48.9 mm at 12 months, and 54.2 mm at 24 months. Several studies examined whether the degree of smell loss preoperatively can predict recovery after surgery. Litvack and colleagues36 compared the improvement in smell for hyposmics and anosmics and found that only anosmics have a significant improvement in olfaction after ESS. The 40-item UPSIT was used as the objective measure; men with scores of 19 to 33 and women with scores of 19 to 34 were considered hyposmics, and anosmics were men and women with scores of 6 to 18. Anosmics significantly improved on the UPSIT from a preoperative mean of 9.7 to 21.3 6 months after surgery, and this improvement was sustained at 12 months after surgery (mean, 21.7). Regarding hyposmics, there was no significant change in the UPSIT scores from before surgery (28.8) to 6 months (30.0) or 12 months (29.5) after surgery. A second study also suggested that patients with anosmia may be more likely to benefit from ESS than those with hyposmia, but the difference in smell recovery between the two groups was not significant. Using the UPSIT, 60.6% of anosmics improved compared with 42.4% of hyposmics.39 PERIOPERATIVE CONSIDERATIONS FOR OLFACTORY PRESERVATION DURING ENDOSCOPIC SINUS SURGERY FOR CHRONIC RHINOSINUSITIS
Because the predominant location of olfactory sensory neurons has been established to be along the superoposterior septum and upper portion of the turbinates, preservation of these structures is generally recommended when possible. Meticulous dissection should be used near turbinates and the superior septum to lessen the chance of mucosal stripping, unintentional turbinectomies, and damage to the cribriform. Despite the turbinates’ potential contribution to olfaction, turbinate resection may be considered when they severely obstruct the nasal airflow, impede postoperative debridements, or are degenerated from the inflammatory process.40 Careful debulking of polyps medial to the turbinate may also be considered by experienced surgeons who have carefully reviewed the anatomy, so as not to strip the olfactory epithelium or disrupt the skull base causing a cerebrospinal fluid (CSF) leak.41 Several studies have evaluated whether turbinate resection and debulking olfactory cleft polyps affects olfaction.41–44 Turbinates play a normal role in maintenance of laminar airflow and humidification of inhaled air.40 However, several studies show that partial resection of the superior turbinate or removal of the middle turbinate does not have a negative impact on olfaction.42,43 Resection of the inferior third of the superior turbinate is often done during a transethmoid sphenoidotomy to visualize and access the natural sphenoid ostium.45 Say and colleagues42 analyzed whether this partial resection of the superior turbinate affects smell. In 55 partial superior turbinate specimens, only 9 (16%) contained olfactory nerve fibers. Postoperatively, none of these 9 nostrils had a decrease in smell as measured by the 12-item CCSIT (Sensonics, Inc, Haddon Heights, NJ). Regarding
5
6
Thompson et al
middle turbinates, Friedman and colleagues46 found no significant difference in the postoperative change in UPSIT scores in 38 patients who had partial middle turbinate resection and 26 patients who did not as part of their ESS. In the multi-institutional study by Soler and colleagues,43 patients who had bilateral middle turbinate resection were more likely to have worse CRS burden on CT and nasal endoscopy. Patients with bilateral middle turbinate resection had a more significant improvement in smell identification test scores than those who had the middle turbinates preserved. In these more severe CRS cases, removal of the likely degenerated middle turbinates potentially allowed better access for odorants to reach the olfactory cleft.43 Contrary to these studies, Nguyen and colleagues44 found that, in revision sinus surgery, a history of middle turbinate resection was a negative prognostic indicator for smell improvement after surgery. Although the results of these studies analyzing turbinate resection are inconsistent, middle turbinate resection may be considered when disease burden is high and the turbinates are degenerated. If the middle turbinate is appears normal on endoscopy, turbinate preservation is recommended. Polyps medial to the middle turbinates block odorants from reaching the olfactory cleft, but are located intimately with the olfactory epithelium along the cribriform plate, middle turbinate, superior turbinate, and superior septum.41 These polyps can often be left, without any attempt at debulking the obstructive load, for fear that removal would damage the cribriform, decrease smell, or cause a CSF leak. Masaki and Tanaka41 described having a low threshold for septoplasty and carefully lateralizing the middle turbinate before olfactory cleft surgery in order to widen the area for polyp removal. They recommended olfactory cleft polypectomy or debulking because up to a third of polyps can arise from the olfactory cleft.41 No complications were reported and olfaction was not analyzed. In evaluating olfaction after olfactory cleft surgery, Nguyen and colleagues44 reported that either debulking of nasal polyps or removal of respiratory epithelial adenomatoid hamartomas can improve smell. The Sniffin’ Sticks test was used. All patients with normosmia before olfactory cleft surgery conserved their sense of smell postoperatively. Of the patients with hyposmia or anosmia preoperatively, 45% had an improvement in smell and 55% had no change after surgery. No complications were reported, and none of the 74 patients in the study had a CSF leak. PERIOPERATIVE CONSIDERATIONS IN THE ENDONASAL APPROACH TO THE SKULL BASE
The endoscopic endonasal approach to anterior skull base lesions is growing in popularity because of the enhanced visualization and decreased morbidity.47 Despite its increased use, normal anatomic structures are often removed or altered in order to endoscopically access the skull base and allow a 4-hand technique or to reconstruct the surgical defect. When approaching the skull base, limiting the disruption along the nasal corridor and only using nasoseptal flaps when necessary for reconstruction may lessen the postoperative morbidity and nasal symptoms.48 A recent study compared postoperative olfaction with the Smell Diskettes Olfaction Test (Novimed, Dietikon, Switzerland) in patients who had pituitary tumors removed via the transseptal microscopic approach versus the endoscopic endonasal approach.15 At 6 months after surgery, 13 of 25 patients had hyposmia and 5 of 25 patients had anosmia in the microscopic approach group. None of the patients in the endoscopic approach group had smell dysfunction. This difference in smell recovery between the two groups was significant (P
