Nasal floor augmentation for empty nose syndrome

Abstract Background Empty nose syndrome (ENS) can be relieved by conservative therapeutic modalities such as nasal hygiene, nasal moisturizers, or nasal irrigation; however, surgery may be required for reestablishing nasal resistance and physiologic airflow. Surgical operation for ENS is often accompanied by procedural difficulties and complications. Aims To introduce and evaluate the use of nasal floor augmentation as a simple method to increase nasal resistance and ameliorate the symptoms of ENS. Materials and methods In this prospective study, the nasal floor in six patients with ENS was augmented with pieces of auricular cartilage. Subjective symptoms were examined using questionnaire assessments performed before and 3 months after surgery. Pre- and postoperative nasal resistance was evaluated using rhinomanometry. Results The nasal floor was successfully augmented in all six cases. At 3 months after surgery, the total questionnaire score reduced, and the nasal resistance increased. Conclusions and significance The findings of this study suggest that nasal floor augmentation for ENS is effective in increasing nasal resistance and reducing the nasal symptoms causally related to ENS. Informed consent statement This study was approved by the institutional Ethics Committee Review Board. All the patients provided full written and informed consent to participate in this study. The project conforms to the Code of Ethics of the World Medical Association (Declaration of Helsinki).


Introduction
Despite the importance of maintaining normal nasal anatomy and preserving nasal mucosa to ensure normal nasal function, the inferior nasal turbinate could still be excessively reduced in turbinate surgery [1]. Empty nose syndrome (ENS), a term first coined by Kern and Stenkvist in 1994 [2,3], refers to a condition in which nasal structures, such as the nasal turbinate, are largely absent due to surgery, and nasal symptoms persist despite good nasal ventilation [2].
Patients with ENS, which is also called iatrogenic atrophic rhinitis [4], can show symptoms, such as paradoxical nasal obstruction, nasal pain, dryness of the nasal cavity, and crusting [5] weeks to years after surgery. These symptoms could be caused by turbulence owing to inferior nasal turbinate resection [6,7] or by a reduction in receptors, such as the thermal receptors of the trigeminal nerve [7]. The nasal meatuses, which are formed among the turbinates, nasal septum, and the nasal walls and floors, are narrow and limit the total airflow, thereby increasing the velocity of airflow. However, the loss of turbinates disrupts the structure of the nasal meatuses, causing turbulent and less sensate airflow [6,7]. In addition, nasal turbinates are known to be a source of nerve growth factor [8]. Excessive damage to the turbinate may therefore cause poor nerve and receptor regeneration, resulting in decreased sensation of airflow.
The reported influence of inferior turbinectomy on negative symptoms is variable. Courtiss et al. reported that 20% of the cases do not show an improvement and 8% show worsening even after inferior turbinectomy, and 8% of cases show dryness of the nasal cavity [9]. Similarly, Passali et al. reported that the symptoms of atrophic rhinitis appear in 22% of cases following inferior turbinectomy [1]. In contrast, Ophir et al. reported that symptoms do not appear during longterm observation following inferior rhinoplasty [10].
However, Hong et al. reported that a decrease in the size of the residual inferior nasal turbinate was associated with an increase in the severity of symptoms such as nasal dryness and facial pain [11]. ENS can be relieved by conservative therapeutic modalities such as nasal hygiene, nasal moisturizers, or nasal irrigation; however, surgery may be required for reestablishing nasal resistance and physiologic airflow. For ENS, autologous or artificial materials are mainly implanted in the remaining inferior nasal turbinate, nasal lateral wall, or nasal septum. Previous reports used costal and conchal cartilage [12] as autografts, acellular dermis (Alloderm V R , LifeCell, Branchburg, NJ) [13] for allografts, and porous polyethylene (Medpor V R , Stryker, Kalamazoo, MI) [14] for artificial grafts. These implants provided additional resistance to breathing and reduced the symptoms of ENS. Surgical operation is, however, often accompanied by procedural difficulties and complications, such as exposure or evacuation of the implanted materials.
This study aimed to introduce and to evaluate nasal floor augmentation as a simple method to increase nasal resistance and reduce the symptoms of ENS.

Patients
A total of 11 sides in six patients (one woman and five men, mean age: 52 ± 16 years) were operated on; surgeries were performed on both sides in five patients and on one side in one patient. All the patients had undergone partial inferior turbinectomy involving bone on both sides at other clinics. The patients subsequently complained of occurrence or exacerbation of nasal obstruction, nasal pain, rhinorrhea, or postnasal drips following the surgery. Five patients complained of nasal symptoms on both sides, while one patient complained of nasal symptoms on one side alone. Nasal hygiene, nasal moisturizers, nasal irrigation, application of ointment and antiallergic drugs were ineffective for all patients. Patients who did not want surgery were excluded.
This study is a prospective project approved by the institutional Ethics Committee Review Board. All the patients gave their full written and informed consent to participate in this study. The project conforms to the Code of Ethics of the World Medical Association (Declaration of Helsinki).

Examinations
Reduction of the bilateral or unilateral inferior nasal turbinate was confirmed on inspection under a nasal endoscope and sinus computed tomography. Patients were asked to complete a questionnaire, including questions from the Sino-Nasal Outcome Test 20 (SNOT-20) [15], SNOT-25 [14], and Empty Nose Syndrome 6-item Questionnaire (ENS6Q) [16,17], to examine their subjective symptoms before and 3 months after surgery (Table 1). Each item is scored from 0 (no symptoms) to 5 (severe symptoms). We have obtained permission to use the questionnaires.
The in-office cotton test [18] was performed by placing a cotton plug on the nasal floor near the site of tissue loss to predict the effect of the surgery. The results of the cotton test were considered positive when nasal symptoms such as nasal obstruction and nasal pain reduced. Nasal floor augmentation was indicated in patients with reduced unilateral or bilateral inferior nasal turbinates and positive results in the cotton test. Patients who did not experience any benefits in the cotton test were not considered as candidates for nasal floor augmentation.
Rhinomanometry (Rhinorheograph MPR-3100; Nihon Kohden, Tokyo, Japan) by the mask anterior method during normal inspiration and expiration was performed before and after surgery to assess changes in nasal resistance. Bilateral nasal resistance at a nasal pressure of 100 Pa was recorded three times, and the mean value was used for the analysis. Rhinomanometry can measure the airflow velocity through the nasal cavity and the difference in pressure between the nostril and nasal choana during normal inspiration and expiration through the nose. Based on the hydrodynamic equation (resistance ¼pressure difference/velocity of flow), the nasal resistance was calculated.

Statistical analyses
IBM SPSS software version 22.0 (IBM, Tokyo, Japan) was used for statistical analysis. Pre-and postoperative scores in assessments with SNOT-20, SNOT-25, and ENS6Q were compared using paired t-tests. Preand postoperative nasal resistance at 100 Pa of nasal pressure were compared using the Wilcoxon signed rank test. The normality of the data was tested using the Kolmogorov-Smirnov test. A of p-value <.05 was considered statistically significant.

Surgical methods
All surgical procedures were performed under general anesthesia. First, several pieces of cartilage approximately 8 mm Â 12 mm in size were removed from the auricle. A 10-15-mm incision was made on the skin-mucosal transition area at the nasal floor ( Figure 1(a)), and a mucosal flap was created from the bony nasal floor with the posterior end 20 mm posterior to the incision (Figure 1(b)). Next, four to five removed pieces of cartilage were stacked in the space between the nasal floor bone (Figure 1(c)), where symptomatic relief was obtained in the preoperative cotton test. After confirming sufficient augmentation of the nasal floor ( Figure 1(d)), the incisions were closed with nonabsorbable sutures.
Polyvinyl alcohol foam (Ivaron V R , First Aid Bandage Company, New London, CT) was placed in the nasal cavity for 2 days to compress the surgical wound and to prevent hematoma formation.

Representative case report
The patient was a 40-year-old man who had undergone bilateral nasal septorhinoplasty and inferior turbinectomy at another clinic, but experienced exacerbation of bilateral nasal obstruction following the surgery. Assessments performed at the other clinic revealed that he had almost no inferior nasal turbinate on both sides. He visited our clinic to seek consultation and treatment for ENS. His inferior nasal turbinates were excessively reduced (Figure 2(a)). Conservative treatments, including nasal hygiene, nasal moisturizers, and nasal irrigation, were ineffective. The cotton test could effectively reduce nasal obstruction and nasal pain. Therefore, the patient underwent nasal floor augmentation. Three months following the surgery, the questionnaire scores for Table 1. SNOT-20, SNOT-25, and ENS6Q assessments pre-and post-surgery.    Average score  e  g  n  a  h  c  f  o  t  n  u  o  m  A  s  m  o  t  p  m  y  s  Q  6  S  N  E  d  n  a  ,  5  2  -T  O  N  S  ,  0  2  -T  O  N  S p -value SNOT-20 Shaded areas indicate factors that were significant (p < .05).
nasal and general symptoms had reduced, the nasal floor was successfully augmented (Figure 2(b)), and bilateral nasal resistance on rhinomanometry was greater than that before surgery.

Results
The cotton test revealed bilaterally positive results in five cases with ENS symptoms on both sides and unilaterally positive results in one case with ENS  In the questionnaire assessments, reductions were observed in the nasal scores for the need to blow nose, runny nose, facial pain/pressure, dryness, difficulty with nasal breathing, nasal crusting, and nasal burning (Table 1). Moreover, score reductions were observed for general symptoms such as difficulty falling asleep, waking up at night, lack of good night's sleep, frustration/restlessness/irritability, sadness, and embarrassment ( Table 1). The total scores reduced in assessments with SNOT-20 (p ¼ .03), SNOT-25 (p ¼ .03), and ENS6Q (p ¼ .04) ( Table 1).
In the assessments performed with rhinomanometry, the postoperative nasal resistance at 100 Pa of nasal pressure (mean ± SD: 0.16 ± 0.02 Pa/cm 3 /s) increased from the preoperative value (0.13 ± 0.03 Pa/ cm 3 /s) in all six patients (Figure 3). Pre-(p ¼ .83) and postoperative (p ¼ .62) nasal resistance were normally distributed and the difference between them was significant (p ¼ .02).

Discussion
To alleviate the symptoms of ENS, it is important to augment the volume at the surgically reduced sites in the nasal cavity or increase the nasal pressure, although this objective is often challenging. Therefore, in this study, we augmented the nasal floor instead of the reduced inferior nasal turbinate. The nasal floor augmentation proved to be effective in reducing the symptoms of ENS and increasing the nasal pressure.

Features of nasal floor augmentation with cartilages
Previous reports have primarily described the implantation of autologous or artificial materials in the remaining inferior nasal turbinate, nasal lateral wall, or nasal septum for ENS [4]. However, nasal floor augmentation may offer a few advantages over the previous methods.
First, nasal floor augmentation involves very easy manipulations. Furthermore, we believe that augmentation for the reduced inferior nasal turbinate is more physiological and ideal for correcting the nasal cavity closer to its normal shape. In ENS, however, the inferior nasal turbinate and, in many cases, the nasal septum have undergone treatment in the previous surgeries. After surgical manipulation, the nasal mucosa becomes hard and difficult to stretch. Moreover, an excessively reduced inferior nasal turbinate contains limited space for augmentation between the nasal mucosa and the bone, and the mucosa of the left and right sides of the corrected nasal septum may be tightly adhered. These postoperative changes complicate implantation of autologous or artificial materials, and the materials could be exposed or evacuated as a result. On the other hand, nasal floor augmentation can be performed in a series of easy steps, i.e. removing some pieces of the auricular cartilage, incising the anterior nasal floor, creating the mucosal flap from the bony nasal floor, stacking the pieces of the cartilage, and suturing the incision. In addition, a previously unoperated nasal floor is relatively flexible and unbreakable and unlikely to expose the implanted cartilage pieces. Furthermore, augmentation of the lateral wall of the inferior nasal meatus may result in nasolacrimal duct obstruction. On the other hand, no such concerns are associated with nasal floor augmentation, unless the floor is stacked with a very large number of cartilage pieces.
Second, nasal floor augmentation may help restore normal nasal airflow. The normal inferior turbinate modulates the amount of nasal airflow and increases the airflow velocity upward [6] toward the middle nasal meatus [6,7]. However, when the inferior turbinate is removed, almost the entire airflow converges into the enlarged nasal cavity along the nasal floor, and the airflow is not elevated or deflected into the higher regions of the nose [6]. In this scenario, augmentation of the nasal floor, which forms the lower  part of the nasal cavity, may facilitate this function, since the anterior prominence of the nasal floor may also direct airflow into the higher regions of the nose. Nasal floor augmentation could be less physiological than enlargement of the reduced inferior nasal turbinate itself. However, alternating development of mounds of mucosal hypertrophy was reported in the nasal floor, nasal septum, and inferior meatus owing to the excessively reduced inferior turbinate in ENS [17]. Thus, nasal floor augmentation is also considered reasonable.
Third, in cases where an excessively high number of cartilage pieces were stacked, the number of pieces can be reduced after surgery. The appropriate extent of augmentation is difficult to achieve because the surgery is performed under general anesthesia, although a preoperative cotton test is performed to predict the proper location and size of the augmentation. Certainly, even if the surgery is performed under local anesthesia, an appropriate extent of augmentation may be difficult to achieve because the nasal mucosa is anesthetized. The volume of the nasal cavity cannot be corrected postoperatively if a large single cartilage [12] or bone or artificial materials [13] are implanted under the nasal mucosa. In contrast, although excessive stacking of cartilage in our nasal floor augmentation technique can result in a more intense nasal obstruction after surgery, since the cartilage pieces are only stacked under the mucosa on the nasal floor, some pieces can be removed under local anesthesia as needed. Nevertheless, none of the six cases in this report required removal of the cartilage pieces, even though the number of pieces was sufficient to avoid causing auricular deformity.
SNOT-20, SNOT-25, and ENS6Q questionnaires ENS is a condition in which nasal symptoms occur despite good nasal ventilation [4]. Considering the subjective nature of ENS symptoms, questionnaire assessments evaluating changes in symptoms before and after surgery are important. The assessments with the SNOT-20 [15], SNOT-25 [14], and ENS6Q [16,17] questionnaires showed a significant reduction in the total score, suggesting that nasal floor augmentation was effective in reducing ENS-related symptoms. Although assessments based solely on ENS6Q [16,17] may be sufficient for evaluation of the nasal symptoms of ENS, as reported by Velasquez et al. [16], SNOT-20 [15] and SNOT-25 [14] are more detailed and also showed a significant reduction in the total score. Moreover, the scores before (mean SNOT-20 score ¼ 48.8, mean SNOT-25 score ¼ 63.3) and after surgery (mean SNOT-20 score ¼ 30.2, mean SNOT-25 score ¼ 38.4) were approximately within the range of the scores obtained in six previous studies that reported score changes after surgery (before surgery, mean ¼ 39.3-68.3; after surgery, mean ¼ 19.8-38.3) [12][13][14]. Thus, the effectiveness of nasal floor augmentation for improving nasal airflow was comparable to that reported previously.
On reviewing the scores for the individual questions, the symptoms related to nasal breathing, nasal discharge, and nasal pain, which showed high preoperative scores, were reduced. Improvements in these symptoms are preferable since they are the common complaints of patients with ENS. On the other hand, postnasal discharge and thick nasal discharge did not reduce despite the high preoperative scores. Postnasal discharge and thick nasal discharge may be hard to cure, or they may not be symptoms causally related to ENS. The symptoms related to anxiety, depressive tendencies, and sleep were also reduced despite the low preoperative scores. ENS influences patients' quality of life, although it is not a mental illness. Thus, nasal floor augmentation can be effective for improving patients' mental health.

Rhinomanometry
Rhinomanometry was performed before and after surgery to assess the changes in nasal resistance. A larger nasal resistance indicates a smaller cross-sectional area, whereas a smaller nasal resistance indicates a larger cross-sectional area. Postoperative nasal resistance increased from the preoperative levels in all six cases included, suggesting that the cross-sectional area of the nasal cavity was successfully reduced. In rhinomanometry, the approximate normal range of nasal resistance is 0.25 ± 0.10 Pa/cm 3 /s in the Japanese population, and the nasal resistance of the cases included was around the lower limit of the normal range both before and after surgery. Thus, the crosssectional area of the nasal cavity in our cases was slightly large even after surgery. The intensity of nasal obstruction symptoms does not correlate well with the actual nasal volume or cross-sectional area. Thus, the postoperative nasal resistance may have been large enough for the cases included, or the symptoms may have been weakened by the postoperative increase in nasal resistance. In a study of patients who underwent nasal and/or sinus surgery, Naito et al. reported that the nasal width and nasal resistance showed an inverse correlation [19]. On the other hand, McCaffrey and Kern reported that there was no correlation between the nasal width and nasal resistance [20]. Our results were consistent with those of the latter study. The intensity of nasal obstruction may not correlate well with actual nasal volume or nasal resistance in ENS.

Methodological considerations/limitations
This study was limited by the small number of cases and short follow-up duration. Moreover, there is a limit to the amount of auricular cartilage and, consequently, the size of the augmented nasal floor. Future studies are warranted to accumulate more cases and follow patients over a longer term.
In conclusion, nasal floor augmentation for ENS is effective, at least in part, because it increases nasal resistance and reduces the nasal symptoms causally related to ENS, although there is a limit to the amount of auricular cartilage and, consequently, the size of the augmented nasal floor. Nevertheless, we believe that nasal floor augmentation could help treat patients with ENS without decreasing their quality-oflife post-surgery.