Clinical Neurology and Neurosurgery 130 (2015) 162–167

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Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro

Review

Sinonasal morbidity following endoscopic endonasal skull base surgery Ahmed J. Awad a , Ahmed Mohyeldin b , Ivan H. El-Sayed c , Manish K. Aghi d,∗ a

Faculty of Medicine and Health Sciences, An-Najah National University, Nablus, Palestine Department of Neurosurgery, Ohio State University Wexner Medical Center, Columbus, USA Department of Otolaryngology-Head and Neck Surgery, University of California at San Francisco, San Francisco, USA d Department of Neurosurgery, University of California at San Francisco, San Francisco, USA b c

a r t i c l e

i n f o

Article history: Received 26 November 2014 Received in revised form 27 December 2014 Accepted 3 January 2015 Available online 14 January 2015 Keywords: Nasal morbidity Endonasal Endoscopic Skull base Quality of life

a b s t r a c t Open transcranial surgery has long served as the traditional approach for resecting tumors and other lesions in the skull base. However, endoscopic endonasal skull base surgery (EESBS) has emerged as a credible alternative. This paper provides insight on the sinonasal morbidity in patients undergoing EESBS. A literature review was performed by searches of MEDLINE database to provide further insight on sinonasal morbidity associated with EESBS, with a particular focus on published incidence rates and patterns of complication. We identified only articles that reported the incidence of sinonasal morbidity and complications as the major outcome of the studies. The most common sinonasal morbidity symptoms are nasal crusting (50.8%), nasal discharge (40.4%), nasal airflow blockage (40.1%) followed by disturbances in olfaction (26.7%). The incidence of mucocele formation is 8%, and this is significantly increased in pediatric patients up to 25% (range, 14–50%). Epistaxis appears to be a rare event, often times not found in some case series. Some studies suggested less morbidity if the middle turbinate can be preserved, a finding that must be balanced with the need for sufficient exposure on larger cases. Sinonasal morbidity following endoscopic endonasal skull base surgery has the potential to adversely impact patient quality of life, with nasal crusting and discharge being the two most common symptoms. Morbidity signs and symptoms usually resolve within 3–4 months, however symptoms can persist for longer with more complex surgeries. The rate of mucocele formation is higher in pediatric patients, with special attention required in graft positioning for this population in particular. © 2015 Elsevier B.V. All rights reserved.

Contents 1. 2.

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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Literature search . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Data extraction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Assessing types of postoperative sinonasal morbidities and their incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Intraoperative risk factors for sinonasal morbidity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Mucocele formation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Epistaxis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Impact of specific procedural alterations on sinonasal morbidity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6. Time to resolve nasal signs and symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7. Quality of life (QoL) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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∗ Corresponding author at: California Center for Pituitary Disorders and Center for Minimally Invasive Skull Base Surgery, Department of Neurological Surgery, University of California, San Francisco, 505 Parnassus Avenue, Rm M-779, San Francisco, CA 94143-0112, USA. E-mail address: [email protected] (M.K. Aghi). http://dx.doi.org/10.1016/j.clineuro.2015.01.004 0303-8467/© 2015 Elsevier B.V. All rights reserved.

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3.8. Limitations of the study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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1. Introduction Open transcranial surgery has long served the traditional approach for resecting tumors and other lesions in the skull base. However, endoscopic endonasal skull base surgery has emerged as a credible alternative to open procedures for surgical treatment of benign and malignant sinonasal and skull base lesions when patients are selected appropriately [1–3]. These procedures are typically performed by neurosurgeons and otolaryngologists working together to first establish corridors through the nasal sinuses, followed by approaches tailored for the appropriate region to best address the pathology in the skull base [4]. In this paper, we reviewed the literature to provide insight to provide further insight on sinonasal morbidity associated with endoscopic endonasal skull base surgery. While primarily the otolaryngologist member of the team often manages these morbidities, their impact on quality of life underscores its relevance for the neurosurgeon to better understand their mechanisms and develop strategies to prevent them. 2. Methods 2.1. Literature search A literature review was performed by searches of MEDLINE database for relevant articles using the search sentences “(nasal morbidity OR sinusitis OR sinonasal) AND endoscopic skull base”, “Morbidity AND (endoscopic transsphenoidal OR endoscopic endonasal)”, and “Sino-Nasal Outcome endoscopic skull base”. We identified and considered only articles that reported the incidence of sinonasal morbidity and complications as the major outcome of the studies. Case series that only reported on cerebral spinal fluid fistulas were not considered. Only articles published in English up to June 11th 2014 were included. Reports with insufficient outcome of data or series with sinonasal morbidity as not the major outcome of the articles were excluded. Case reports were also excluded. 2.2. Data extraction Data extraction was performed by A.J.A. The authors extracted methodological and demographic data including study design, population size, patient age, sinonasal morbidity symptoms post-surgery including, crusting, discharge, pain, nasal airflow (blockage), and sense of smell. Additionally, authors extracted the follow-up periods and the time period until symptoms resolution.

Fig. 1. Example of postoperative crusting after endoscopic endonasal skull base surgery. Postoperative crusting (yellow) and polyps (arrow) seen in two month follow-up office endoscopy after a lateral approach for a vidian canal schwannoma. (For interpretation of the references to color in this text, the reader is referred to the web version of the article.)

or non-infectious etiology; (iii) nasal airflow blockage (40.1%), leading to more reliance on mouth breathing; and (iv) decreased or absent sense of smell (26.7%). 3.2. Intraoperative risk factors for sinonasal morbidity In the largest two studies reporting on sinonasal morbidity following EESBS [6,9], authors performed multivariable regression analysis, adjusting for the co-variants of age, sex, and surgery type. None of these variables achieved statistical significant risk factors for nasal crusting [6,9]. However, de Almeida and colleagues, found that the only risk factor for nasal discharge was surgical complexity [6]. In 2013, de Almeida et al. [8] published an important study comparing the physical morbidity associated with skull base surgery based on surgical approach and tumor location. They studied 138 patients and divided them in 4 groups based on surgical approach (open vs. endoscopic) and tumor location (anterior vs. central). Using multivariate analyses, authors found that only patients with central tumors treated endoscopically had a statistically significant increase in nasal symptoms [8].

3. Results 3.3. Mucocele formation 3.1. Assessing types of postoperative sinonasal morbidities and their incidence Our search identified 7 series [5–11] reporting the full spectrum of sinonasal complications and their incidences. Out of the 7 series, two studies were prospective while the remaining five were retrospective as summarized in Table 1. The four most common consistent signs and symptoms reported post-operatively in order from most to least frequent were (weighted means): (i) nasal crusting (50.8%) (Fig. 1), caused by stagnation of mucus in dry nasal passages; (ii) nasal discharge (40.4%), either of infectious

Five studies [12–16] specifically addressed mucocele formation following endoscopic skull base reconstruction surgery as shown in Table 3. The incidence of mucocele formation was 8% (11 of 143) among all age groups. The incidence of mucocele formation was higher in the pediatrics age group with an incidence of 25% (range, 14–50% vs. 0–3.6% in adults). [13,15] This is because the frontal sinus is not fully formed before the age of 19 and the nasofrontal duct is tight in children, and is made even narrower by the covering flap [17]. Hence, a proper positioning of the flap is required in the endoscopic repair of frontal sinus fractures [15]. Fig. 2 shows

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Fig. 2. Example of a sinus mucocele forming after endoscopic endonasal skull base surgery. 69-Year-old female who presented with a new sphenoid sinus mucocele with 4–5 weeks of frontal/occipital headaches and sinus fullness. (A) Initial head CT including. (B) Bone window cuts demonstrating a sphenoid sinus occupying mass with distortion and thinning of the sphenoid bone consistent with a mucus retaining cystic like lesion. MRI confirmed the diagnosis (C–F) demonstrating a large heterogeneously hyperintense T1-weighted mass containing minimal areas of peripheral enhancement centered in the sphenoid sinus with invasion of the clivus and effacement of the optic nerves. (C) Sagittal T2 sequences. (D) Axial T1 without contrast. (E) Axial T1 with contrast. (F) Coronal T2 sequences.

a symptomatic mucocele filling the sphenoid sinus in a patient treated for a sellar adenoma via an endoscopic endonasal approach. 3.4. Epistaxis Epistaxis, typically from the sphenopalatine artery, is a rare but potentially significant sinonasal morbidity after EESBS. Our searches identified only three series [5,18,19] studying epistaxis rate following EESBS. Two studies reported 0% incidence of epistaxis following EESBS. Koren et al. studied 20 patients treated with endoscopic endonasal approaches for pituitary tumors [5], while Griffiths et al. studied 161 patients with 174 operations using a bilateral “rescue flap” technique to preserve the mucosa containing a nasal–septal vascular pedicles [19]. In contrast, the third study reported an incidence of 3% in 330 patients within 30 days of EESBS for various pathologies [18]. Overall, these studies collectively suggest epistaxis to be a rare sinonasal complication after EESBS. 3.5. Impact of specific procedural alterations on sinonasal morbidity In investigating the impact of potential modifications to the endoscopic endonasal approach or closure on sinonasal morbidity, our searches identified two prospective studies reported the impact of middle turbinate preservation or removal on the incidence of sinonasal morbidity [10,20]. The nasal turbinates in particular the middle turbinate plays an important role in humidifying, filtering and regulating temperature of airflow before entering the lower airway tract. Historically, many surgeons sacrifice one or both middle turbinates in order to improve exposure and surgical access during EESBS [21,22]. Nyquist and colleagues conducted a prospective study evaluating the impact of preserving the middle turbinate in 160 of 163 (98%) cases of purely endoscopic endonasal transsphenoidal surgeries [20]. During a median of 16 months follow-up, no patients (0%) developed frontal sinusitis [20]. The authors concluded that

preserving the middle turbinate is associated with better sinonasal function while still providing good surgical access [20]. In another series, Sowerby et al. studied the impact of sacrificing a unilateral middle turbinate and its effect on olfactory and sinonasal outcomes in endoscopic transsphenoidal skull-base surgery [10]. They found that out of 22 patients treated, 10 (45%) had improvement in olfaction, while 9 (41%) had a decrease in olfactory function [10]. More recently, Thompson and colleagues published an interesting study where they employed technical modifications on a cohort and compared it with their prior study [23,24]. They discontinued routine resection of the middle turbinate, maxillary antrostomies, and nasoseptal flaps [23]. The new cohort achieved a significant improvement (p < 0.05) in SinoNasal Outcome Test scores and less sinonasal morbidity compared to their prior study [23]. Despite the lack of randomized comparisons, it is certainly reasonable based on these findings for the surgeon to remove the middle turbinate only when absolutely necessary for exposure rather than performing routine turbinectomy for surgical access [20,23].

3.6. Time to resolve nasal signs and symptoms Quality of life transiently worsens in the early period following surgery, but significantly improves in the months later [25,26]. Out of the 7 series we identified as reporting the spectrum of sinonasal morbidities after EESBS, only 3 reported the time for sinonasal signs and symptoms resolution as shown in Table 2. Two of these studies have reported most morbidities to take 3–4 months to resolve [6,11], while, a third study, which was retrospective, reported that 51% of patients with nasal crusting, 66% of patients with nasal discharge, and 51% of patients with decrease olfaction had their symptoms resolved in less than 4 weeks [9]. Two studies showed duration of 101–126 days for nasal crusting resolution after EESBS [6,11]. More specifically, in a prospective study, de Almeida and colleagues found that nasal crusting was

0 – – – – – – 4 (20%) – – – – – – 2 (10%) – – – – – – 4 (20%) 10 (9%) – – – – – – – – – – – 21 (17%) – 22 (20%) 16 (25.4%) – – – – – – 13 (20%) – – – – – – 3 (4.8%) – – – 59 (48%) – – 1 (1.6%) – – – 11 (9%) – – 29 (46%) 20 (49%) – – 53 (43%) 20 109 63 41 22 65 124 Koren (1999) Pant (2010) de Almeida (2011) Cavel (2012) Sowerby (2013) de Almeida (2013) Gallagher (2014)

Retrospective Retrospective Prospective Retrospective Prospective Retrospective Retrospective

– – 45 55 49 48 55

– – 5–35 – – 33 15 (8–28)

– – – – – 52 (80%) –

2 (10%) – 62 (98%) – – – 53 (43%)

2 (10%) – 5 (8%) 19 (46%) 9 (41%) – 32 (26%)

Complete Nasal airflow loss of smell (blockage) Decrease sense of smell Nasal discharge Crusting Post op nasal symptoms Followup (months) Age (years) Patient # Study design Author (year)

Table 1 Summary of series reported sinonasal morbidity following endoscopic endonasal skull base surgery as the major outcome.

Malodorous discharge

Hypothesia

Pain

Synechia

Septal perforation

Postnasal drip

Epistaxis

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resolved within a median of 101 days [6]. Further, these authors found that time to absence of nasal crusting was longer in patients who had complex approaches compared with those who had simple approaches. Moreover, patients who had nasoseptal flaps or fat grafts did not have a significantly longer time to achieve absence of nasal crusting compared to those without, suggesting that nasoseptal flap harvest and the resulting denuded cartilage was not a risk factor for postoperative crusting [6]. These results are consistent with a retrospective study conducted by Pant and colleagues [11]. Those authors evaluated the sinonasal complications in 109 patients underwent EESBS and found that the use of nasoseptal flap did not affect the duration of nasal crusting. However, it should be noted that the two studies are from the same center and likely have overlapping patients. In contrast, Gallagher and colleagues observed different results of patient-reported nasal morbidity following EESBS [9]. One hundred and twenty four patients were interviewed with a median follow-up of 15 months. The authors observed that 51% of patients with nasal crusting and 66% with nasal discharge had their symptoms resolved in less than 4 weeks [9]. The authors noticed that, of patients who did not use sinus rinse, none reported nasal pain or discharge but all reported nasal crusting. Additionally, the authors found there was no statistical significant difference in nasal pain, crusting or blockage between patients undergoing pituitary surgery or other anterior skull base surgeries. However, patients having surgeries for non-pituitary anterior skull base lesions were statistically more likely to experience prolonged nasal discharge and anosmia post-surgery [9]. EESBS sometimes involves the application of pressure to anatomical structures containing olfactory neuroepithelium. Hence, the sense of smell maybe affected transiently or permanently following EESBS. According to our review, the incidence of decrease of smell following EESBS is 25%. Gallagher et al. reported that more than 50% of patients had their decrease of olfaction resolved in less than 4 weeks [9]. Hart et al. evaluated olfaction dysfunction in 57 patients using the University of Pennsylvania Smell Identification Test [27]. They found that although there was olfactory dysfunction at on month post-surgery, there was no significant difference in olfactory function between baseline and at 3 months following surgery [27]. 3.7. Quality of life (QoL) Quality of life assessment is an important outcome measure in skull base surgery patients due to the complexity of surgery and associated significant morbidity. Several questionnaires and tools have been introduced and used in clinical studies of endoscopic skull base surgery to assess QoL morbidity and sinonasal outcomes. These include Short Form-36 (SF-36), Anterior Skull Base Questionnaire (ASBQ), Rhinosinusitis Outcome Measure (RSOM)31, Sinonasal Outcome Test (SNOT)-20, SNOT-22, and many others [6,7,24,26,28–33]. However, due to several different questionnaires and no standardized definition for QoL, it is hard to compare different studies. A recent systemic review of QoL after anterior skull base surgery found that QoL of patients undergoing endoscopic surgery is greater and manifest earlier compared with open surgery [34]. Importantly, it appears that there is no clear long-term deleterious effect on sinonasal outcomes compared with open surgery [34]. 3.8. Limitations of the study This systematic review is limited by retrospective study design of the series included, the limited granularity of individual patient characteristics, the single center nature of many of the studies, and overlapping data between studies [6,11]. Importantly, sinonasal complications are not always going to resolve completely and the

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Table 2 Time for sinonasal signs and symptoms resolution. Author (year)

Study design

Patient #

Age (years)

Follow-up (months)

Time to absence of crusting

Time to absence of nasal discharge

Time for olfactory dysfunction resolution

Pant (2010) de Almeida (2011) Gallagher (2014)

Retrospective Prospective Retrospective

109 63 124

– 45 55

– 5–35 15 (8–28)

126 days (mean) 101 days (median) 27/53 (51%) in

Sinonasal morbidity following endoscopic endonasal skull base surgery.

Open transcranial surgery has long served as the traditional approach for resecting tumors and other lesions in the skull base. However, endoscopic en...
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