Introduction
Many people worldwide suffer from allergic rhinitis. Although medical treatment is the first choice for the treatment of allergic rhinitis, surgical intervention may be utilised for the control of resistant cases. Nishijima et al.Reference Nishijima, Kondo, Toma-Hirano, Iwasaki, Kikuta and Fujimoto1 showed that posterior nasal neurectomy reduced nasal secretion in rat models of allergic rhinitis. Although the neurovascular bundle, which emerges from the sphenopalatine foramen, contains the sphenopalatine artery and the posterior nasal nerves, Ikeda et al.Reference Ikeda, Oshima, Suzuki, Suzuki and Shimomura2 showed that resection of this neurovascular bundle inhibited nasal allergic symptoms, including sneezing, rhinorrhoea and nasal obstruction, in patients with resistant allergic rhinitis or non-allergic rhinitis secondary to eosinophilia syndrome. In order to avoid resection of the sphenopalatine artery, Takahara et al.Reference Takahara, Takeno, Hamamoto, Ishino and Hirakawa3 identified the branches of the posterior nasal nerves in the neurovascular bundle emerging from the sphenopalatine foramen, separated them and resected only the nerve branches. However, there is a risk of haemorrhage when operating around the sphenopalatine artery.
We propose that resection of the peripheral branches of the posterior nasal nerve in the inferior turbinate is a safer and more effective approach. Kobayashi et al.Reference Kobayashi, Hyodo, Nakamura, Komobuchi and Honda4 demonstrated no significant differences in improvement of nasal symptom scores between one group, who underwent resection of only branches in the inferior turbinate with turbinoplasty, and another group, who underwent resection of both the posterior nasal nerves in the neurovascular bundle emerging from the sphenopalatine foramen and posterior nasal nerve branches in the inferior turbinate with turbinoplasty. During submucosal turbinoplasty, it is possible to recognise the posterior nasal nerve branches. This approach alone is attractive, as no additional surgery is needed to find the neurovascular bundle emerging from the sphenopalatine foramen, and manipulation around the sphenopalatine artery is eliminated. However, this approach has not been well examined. To our knowledge, no previous reports have investigated the differences between resection of the branches in the inferior turbinate with turbinoplasty and turbinoplasty alone, performed to reduce allergic symptoms.
Olfactory dysfunction is one of the major symptoms of allergic rhinitisReference Moll, Klimek, Eggers and Mann5–Reference Suzuki, Yokota, Ozaki and Nakamura7 and can negatively affect a patient's quality of life.Reference Katotomichelakis, Simopoulos, Zhang, Tripsianis, Danielides and Livaditis8 Nasal secretion is a frequent cause of olfactory dysfunction.Reference Ozaki, Toida, Suzuki, Nakamura, Ohno and Ohashi9 It is unclear whether resection of the posterior nasal nerves ameliorates olfactory dysfunction or not. To our knowledge, olfactory ability has not been evaluated before or after posterior nasal nerve resection using olfactory tests.
It is important to examine the difference in efficacy between the resection of the nerve branches in the inferior turbinate with turbinoplasty and turbinoplasty alone, to understand the usefulness of resecting branches in the inferior turbinate. In order to clarify the effect of posterior nasal nerve resection on olfactory function, it is imperative to assess olfactory ability before and after posterior nasal nerve resection using objective olfactory tests. We utilised the T&T Olfactometer test in this study to assess this.
Materials and methods
Subjects
Patients who had undergone submucosal turbinoplasty or resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty were included in this study. Other inclusion criteria were the existence of perennial allergic rhinitis (the presence of perennial allergic rhinitis symptoms, and mite-specific immunoglobulin E (IgE) in serum determined using the CAP System (Pharmacia & Upjohn, Uppsala, Sweden)), and the availability of pre- and post-surgery olfactory testing results.
Patients who had undergone septoplasty were excluded. Other exclusion criteria were: the existence of any compounding nasal diseases such as sinusitis and nasal tumours or polyps; complaints of pollinosis symptoms; the presence of specific IgE for the major pollens (Japanese cedar, Japanese cypress, orchard grass or ragweed) in serum (determined using the CAP System); patients aged less than 20 years or more than 65 years; and any history of smoking or trauma.
Surgical approach
The operations were performed under local or general anaesthesia according to the request of the patient. An incision was made along the anterior margin of the inferior turbinate. After the mucosa was reflected, the bone of the inferior turbinate was removed in all patients. In the group undergoing resection of the posterior nasal nerves, we identified the peripheral branches of the posterior nasal nerves in the inferior turbinate. Haemostasis was achieved by bipolar cautery and the branches were resected (Figure 1).
Images showing the (a) identification, and (b) view after the removal, of the peripheral branches of the posterior nasal nerve in the inferior turbinate.
Olfactory testing
Olfactory testing was performed using the T&T Olfactometer (Daiichi Yakuhin Sangyo, Tokyo, Japan), following a previously reported protocol.Reference Azuma, Uchiyama, Tanigawa, Bamba, Azuma and Takano10–Reference Suzuki, Saito, Min, Vladau, Toida and Itoh12 This test consists of five standard odours: roses, burning, sweat, fruits and vegetable chips. Eight concentrations of samples were prepared (categorised as –2 to 5) except for the burning odour, for which seven concentrations were prepared (–2 to 4). The minimum concentration at which patients detected and recognised an odour was defined as the detection threshold and recognition threshold, respectively. When the highest concentration was not identified, the score was denoted as 6, except in the case of the burning odour, for which the score was denoted as 5. The detection threshold and recognition threshold means for all five odours were calculated.
Symptom score
A questionnaire was administered to all participants to assess rhinitis symptoms. Symptom severity was evaluated using the Japanese guidelines for allergic rhinitis.Reference Okubo, Kurono, Ichimura, Enomoto, Okamoto and Kawauchi13 The frequency of sneezing was classified as 0, 1–5, 6–10, 11–20, or more than 21 times per day, with scores of 0–4, respectively. The frequency of nose blowing, which represents the degree of nasal secretion, was classified as 0, 1–5, 6–10, 11–20, or more than 21 times per day, with scores of 0–4, respectively. Nasal obstruction was classified as none, a feeling of obstruction but mouth breathing not required, obstruction that required mouth breathing sometimes, obstruction that required mouth breathing most of the day, and obstruction requiring mouth breathing for the entire day; these were scored as 0–4, respectively. Subjective olfactory dysfunction was classified as none, mild, moderate, severe and anosmia, with scores of 0–4, respectively.
Statistical analysis
Data are expressed as mean ± standard error of the mean. A statistical comparison of the results between the two groups was performed using the chi-square test for sex and the Mann–Whitney test for the other parameters. The Wilcoxon signed-rank test was used for comparison of the results before and after treatment. A probability of p < 0.05 was considered statistically significant.
This study was approved by the Nagoya City University Ethics Committee and was performed in accordance with the Declaration of Helsinki.
Results
Patients’ characteristics
The study comprised: 21 patients (12 women and 9 men) who underwent resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty (mean age of 43.9 ± 2.9 years (range of 22–63 years)), and 19 patients (10 women and 9 men) who underwent submucosal turbinoplasty only (mean age of 39.1 ± 3.2 years (range of 21–63 years)). There were no significant differences in age or sex between the two groups.
Effects of surgery on nasal symptoms
We compared changes in nasal symptoms, including sneezing, rhinorrhoea and nasal obstruction, in patients who underwent resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty versus those who underwent submucosal turbinoplasty alone, before and after surgery (Table 1).
Sneezing, rhinorrhoea and nasal obstruction pre- and post-surgery
Data represent mean ± standard error values. *P < 0.01 versus pre-surgery; †p < 0.05 versus turbinoplasty alone
The amount of sneezing after resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty was significantly lower than that before this surgery, while there was no significant difference in sneezing before and after submucosal turbinoplasty alone.
Additionally, there was no significant difference in the severity of nasal obstruction between the two groups before or after surgery. However, the severity of nasal obstruction after submucosal turbinoplasty and after resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty was significantly lower than that before each procedure.
Furthermore, the frequency of nose blowing after resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty was significantly lower than that before this surgery, while there was no significant difference in the frequency of nose blowing before and after submucosal turbinoplasty alone. The frequency of nose blowing after resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty was significantly lower than that after simple submucosal turbinoplasty, although no significant differences were observed before the surgery.
Effects of surgery on olfactory dysfunction
Table 2 reports the changes in subjective olfactory dysfunction and results of olfactory testing in patients who underwent resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty versus those who underwent submucosal turbinoplasty alone, before and after surgery.
Olfactory dysfunction pre- and post-surgery
Data represent mean ± standard error values. *P < 0.01 versus pre-surgery; †p < 0.01 versus turbinoplasty alone
Several patients complained of anosmia before surgery, including 3 (15.8 per cent) of the 19 patients who underwent simple submucosal turbinoplasty, and 4 (19.0 per cent) of the 21 patients who underwent resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty. The number of patients with subjective anosmia decreased after surgery; just one patient in the submucosal turbinoplasty only group had anosmia, and no patients had anosmia after posterior nasal nerve resection.
Subjective olfactory dysfunction severity was significantly reduced following resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty, but not in patients who underwent submucosal turbinoplasty alone.
The resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty significantly decreased the detection and recognition thresholds of olfactory testing, while submucosal turbinoplasty alone did not. The detection and recognition thresholds after resection of the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty were significantly lower than those after submucosal turbinoplasty alone, though no significant differences were observed between these groups pre-operatively.
Complications and safety of resection
We evaluated the safety of resecting the posterior nasal nerve branches in the inferior turbinate with submucosal turbinoplasty and of submucosal turbinoplasty alone. There were no major complications, such as post-operative bleeding, facial swelling, hypoesthesia or dry eye, in the two groups.
Discussion
Kobayashi et al.Reference Kobayashi, Hyodo, Nakamura, Komobuchi and Honda4 showed no significant differences in nasal symptom scores between a group who underwent resection of the branches in the inferior turbinate with turbinoplasty and a group who underwent resection of the posterior nasal nerve branches in both the neurovascular bundle emerging from the sphenopalatine foramen and in the inferior turbinate with turbinoplasty. This suggests the superior usefulness of posterior nasal nerve branch resection in the inferior turbinate. However, submucosal inferior turbinoplasty is necessary to find the peripheral branch of the posterior nasal nerves in the maxilla. Whether resection of the posterior nasal nerve inferior branches in the inferior turbinate has more influence on the inhibition of rhinitis symptoms than turbinoplasty alone remains controversial, and we examined this in the present study.
The present study showed that resection of the posterior nasal nerve inferior branches in the inferior turbinate with turbinoplasty inhibited nasal allergic symptoms, including sneezing, rhinorrhoea and nasal obstruction. Conversely, turbinoplasty alone significantly inhibited only nasal obstruction, and not sneezing or rhinorrhoea. This suggests the superior efficacy of resecting the posterior nasal nerve inferior branches in the inferior turbinate for the control of allergic rhinitis. It is important to find the peripheral branch of the posterior nasal nerves in the inferior turbinate and resect it, to obtain maximum inhibition of allergic symptoms.
We previously established a mouse model of allergic rhinitis with olfactory dysfunction.Reference Ozaki, Toida, Suzuki, Nakamura, Ohno and Ohashi9 In this mouse model, the number and size of the glands in the olfactory mucosa were found to be increased. The findings suggested that mucin and rhinorrhoea in the olfactory cleft and nasal mucosa contribute to olfactory dysfunction in allergic rhinitis. Additionally, the present study indicates that resection of the posterior nasal nerves inhibits rhinorrhoea and olfactory dysfunction. Considering this, resection of the posterior nasal nerves may inhibit olfactory dysfunction through the reduction of rhinorrhoea.
• Resection of the peripheral branch of the posterior nasal nerves in the inferior turbinate has been recently used to treat allergic rhinitis
• There are few detailed studies on resection of the posterior nasal nerves in the inferior turbinate
• Resection of the peripheral branch of the posterior nasal nerves in the inferior turbinate is safe
• Such resection is an effective method to treat nasal discharge and olfactory dysfunction in allergic rhinitis patients
Ikeda et al.Reference Ikeda, Oshima, Suzuki, Suzuki and Shimomura2 resected the neurovascular bundle containing the sphenopalatine vessels and the posterior nasal nerves using an ultrasonic coagulator. In Ikeda's study, post-operative epistaxis occurred in one patient, and one patient complained of transient hypoesthesia of the soft palate and dry eye. However, with resection of the peripheral branches of the posterior nasal nerves in the inferior turbinate, the sphenopalatine artery and foramen are avoided, suggesting improved safety with this method. Additionally, there were no post-operative complications such as epistaxis, hypoesthesia or dry eye in this study. Thus, resection of the inferior turbinate branches may be considered a safe approach.
Ikeda et al.Reference Ikeda, Oshima, Suzuki, Suzuki and Shimomura2 reported that subjective anosmia improved in four of eight patients, while the other four patients experienced no improvement after the resection of posterior nasal nerves. This suggests that resection of the posterior nasal nerves may improve olfactory dysfunction. However, the results were obtained through subjective assessment, not olfactory testing. Detailed examinations of the effects of posterior nasal nerve resection on olfactory function have not been reported using olfactory testing, despite the importance of investigating olfaction objectively. This study demonstrated, for the first time, that resection of the posterior nasal nerves ameliorated olfactory dysfunction (determined using the T&T Olfactometer test).
A recognition threshold of −2.0 to 1.0 is defined as normal, while a recognition threshold of 1.1 to 5.8 indicates olfactory dysfunction.Reference Azuma, Uchiyama, Tanigawa, Bamba, Azuma and Takano10,Reference Oka, Tsuzuki, Takebayashi, Kojima, Daimon and Sakagami11 In this study, the mean recognition threshold before turbinoplasty alone (2.56) and before the resection of posterior nasal nerves with turbinoplasty (2.44) was greater than 1.0, indicating olfactory dysfunction. There was no significant difference in recognition threshold before and after turbinoplasty alone. However, the mean recognition threshold (0.89) after resection of the peripheral branches of the posterior nasal nerves in the inferior turbinate was less than 1.0, indicating normal function. This suggests that posterior nasal nerve resection can alleviate olfactory dysfunction.
In conclusion, this study showed that resection of the peripheral branches of the posterior nasal nerves in the inferior turbinate is a safe and useful surgical procedure. It demonstrated that resection of the posterior nasal nerves inhibited olfactory dysfunction. However, there are limitations of this study, such as small sample size. Further studies are needed to develop this approach.
Competing interests
None declared
