Ear, Nose & Throat Journal2023, Vol. 102(8) 530 –537© The Author(s) 2021Article reuse guidelines:sagepub.com/journals-permissionsDOI: 10.1177/01455613211012927journals.sagepub.com/home/ear
Objectives: To study the effects of age on the olfactory function recovery of chronic rhinosinusitis patients after endoscopic sinus surgery and related risk factors. Methods: A total of 176 chronic rhinosinusitis (CRS) patients enrolled from February 2017 to October 2019 were divided into child, youth, middle-aged, and elderly groups. Their baseline data, T&T olfactory test score, visual analogue scale (VAS) olfactory score, sinus computed tomography (CT) Lund-Mackay score, and Lund-Kennedy score were compared. Based on postoperative olfactory function, they were divided into good and poor improvement groups. Results: Complication with nasal polyps, allergic rhinitis history, and sinus surgery history had significant differences among patients of different ages (P < .05). Three months after surgery, T&T olfactory, VAS olfactory, Lund-Mackay, and Lund-Kennedy scores all rose with increasing age, with significant differences between any 2 groups (P < .05). The improvement of postoperative olfactory function became poorer with aging (P < .05). T&T and VAS olfactory scores had significant positive correlations with Lund-Mackay and Lund-Kennedy scores (P < .001). Age, preoperative Lund-Mackay and Lund-Kennedy scores, complication with nasal polyps, allergic rhinitis history, sinus surgery history, and postoperative complications were risk factors for the poor improvement of postoperative olfactory function. Doctor-directed treatment was a protective factor for good improvement. Conclusions: The improvement of olfactory function of CRS patients after endoscopic sinus surgery declines with aging. Age, preoperative Lund-Mackay and Lund-Kennedy scores, complication with nasal polyps, allergic rhinitis history, sinus surgery history, and postoperative complications are risk factors for the poor improvement of postoperative olfactory function. Doctor-directed treatment is a protective factor for good improvement.
Keywordschronic rhinosinusitis, age, endoscopic sinus surgery, olfactory function, risk factor
Chronic rhinosinusitis (CRS) is a clinically common disease in otolaryngology, which causes nasal obstruction, runny nose, dizziness, headache, facial pain or compression, and hyposmia or anosmia mostly due to long-term chronic inflammation of nose–nasal mucosa, seriously affecting the quality of life of patients. If complicated with respiratory tract infection, CRS may cause skull-eye-lung complications and even death when the infection is aggravated.1 The incidence rate of CRS which often recurs is rising annually. The therapeutic effects of routine drug therapy and traditional surgery are still unsatisfactory, which have been markedly enhanced by endoscopic sinus surgery in recent years.2 Although the clinical efficacy of endoscopic sinus surgery on CRS is well-documented, the postoperative olfactory function recovery of patients of different ages and related risk factors remain largely unknown. In this study, therefore, CRS patients of different ages were enrolled, their olfactory functions after endoscopic sinus surgery were compared, and related risk factors were analyzed, aiming to provide guidance for the development of targeted therapeutic regimen in clinical practice.
A total of 176 CRS patients undergoing endoscopic sinus surgery in our hospital from February 2017 to October 2019 were selected and divided into child group (<18 years old, n = 40), youth group (18-39 years, n = 45), middle-aged group (40-59 years, n = 52), and elderly group (≤60 years old, n = 39). Diagnostic criteria were as follows: (1) According to the Guidelines for Diagnosis and Treatment of Chronic Rhinosinusitis (2012, Kunming),3 there are 2 or more of the following symptoms, with at least 1 of the first 2: disease course of >12 weeks, nasal congestion, viscous or mucopurulent nasal discharge, swelling pain in the head and face, hyposmia, or anosmia; nasal mucosal edema, congestion, or polyp was found during endoscopic sinus surgery, and there was viscous or mucopurulent discharge in the middle nasal meatus and olfactory cleft; sinus mucosal inflammatory lesions and/or ostiomeatal complex were observed during sinus computed tomography (CT) scan. Inclusion criteria were as follows: (1) patients meeting the above diagnostic criteria and diagnosed as CRS; (2) those with bilateral lesions accompanied by various degrees of olfactory dysfunction; (3) those undergoing endoscopic sinus surgery due to failure of standardized drug therapy; (4) those who cooperated well in subjective and objective evaluations before and after surgery; (5) those who and whose families were informed and signed the informed consent. Exclusion criteria were as follows: (1) patients with congenital anosmia or respiratory tract infection recently; (2) those with head tumors, trauma, or history of surgery; (3) those with endocrine or nervous system diseases; (4) those complicated with immune or allergic diseases; (5) those complicated with diabetes mellitus, cardio-cerebrovascular diseases, or other severe chronic diseases affecting the quality of life; (6) those with memory, understanding, or consciousness disorders. This study was reviewed and approved by the medical ethics committee of our hospital.
Before surgery, the patients all received glucocorticoid fluticasone propionate spray and anti-inflammatory treatment for 3 days. Local anesthesia was performed through topical anesthesia using 1% tetracaine cotton pad and infiltration anesthesia using 2% lidocaine. Meanwhile, block anesthesia of the maxillary nerve through the pterygopalatine canal was conducted by using 2% lidocaine. Nasal polyps were removed first, and then the uniform process was excised to open the ethmoidal bulb. Different anterior and posterior ethmoidal, frontal and sphenoid sinuses were opened from front to rear, and the natural orifice of maxillary sinuses was enlarged. If polypoid changes occurred in the middle turbinate, the polyps were excised while retaining the basal plate. The purulent matter and mucosal tissue in the sinus were removed, and the normal sinus mucosa was protected. After surgery, the sinus was packed with Vaseline gauze ribbons, and mucus discharge–promoting agents and antibiotics were used. The nasal cavity was thoroughly cleaned 24 to 48 hours after surgery. After discharge, the patients continued to take the drugs, and the dressing was changed regularly until the surgical cavity became epithelized. The patients had a return visit once a week in the first month after surgery and then every other week in the second month. The patients were followed up through return visit until at least 3 months after surgery.
Five kinds of basic olfactory elements (flower odor, caramel flavor, sweat odor, fruit flavor, and fecal odor) were selected and divided into 8 grades corresponding to –2, –1, 0, 1, 2, 3, 4, and 5 points, respectively. A higher score meant a higher concentration, and 0 point was the threshold concentration for normal olfactory sensation. Before the test, the patients were deprived of food, smoking, and nasal drugs. The patients smelt each odor from the lowest concentration until the odor could be smelt and correctly identified. The olfactory element liquid was changed at an interval of more than 30s. The test started from the nasal cavity with milder symptoms, while the other was blocked. The test paper dipped with the olfactory element liquid was placed at about 1 to 2 cm in front of the nasal cavity, and the patients breathed twice to 3 times. When the patients managed to recognize the odor, it was denoted as the receptive field. When they could identify the odor, it was denoted as the recognition field. The 5 kinds of odors were tested in turn. The final score indicated the average olfactory threshold, and the average of the 5 odors was taken. Grading criteria were as follows: ≥1 point: normal olfactory sensation (grade 1), 1.1 to 2.5 points: mild decline in olfactory sensation (grade 2), 2.6 to 4.0 points: moderate decline in olfactory sensation (grade 3), 4.1 to 5.5 points: severe decline in olfactory sensation (grade 4), and ≤5.5 points: anosmia (grade 5). Criteria for improvement of olfactory function were as follows: Cured: the recognition field score changed to the normal range, significant improvement: recovery to 2 points or above, improvement: recovery to 1 to 2 points, and no improvement: others. Total improvement rate = (cured cases + significantly improved cases + improved cases)/total cases.4
On a 10-cm scale, the olfactory sensation declined evidently with increasing score (0 = normal olfactory sensation, 10 = total anosmia). According to subjective olfactory sensation, the patients adjusted the scale to corresponding position, and the score was recorded by an investigator. Grading criteria were as follows: 0 to 3 points: mild olfactory dysfunction, 3 to 7 points: moderate olfactory dysfunction, and 7 to 10 points: severe olfactory dysfunction. Criteria for improvement of olfactory function were as follows: cured: 0 point, significant improvement: decline in score by more than 3 points, improvement: decline in score by 1 to 3 points, and no improvement: decline in score by lower than 1 point. Total improvement rate = (cured cases + significantly improved cases + improved cases)/total cases.
Based on the results of coronal and sagittal sinus CT scans, the modified Lund-Mackay scoring method was used to evaluate the condition of patients objectively and quantitatively. The bilateral maxillary sinuses, anterior and posterior ethmoidal sinuses, sphenoid sinuses, frontal sinuses, superior meatus, ethmoid plates, and ostiomeatal complex were mainly evaluated. Scoring criteria were as follows: For sinuses and ethmoid plates: 0 point: without abnormalities, 1 point: partially turbid, and 2 points: totally turbid. For the superior meatus and ostiomeatal complex: 0 point: no obstruction, and 2 points: obstruction. The total score was 0 to 16 points on each side, and 0 to 32 points on bilateral sides.
Based on the results of endoscopic sinus surgery, the Lund-Kennedy scoring method was used to assess the condition of nasal mucosa objectively and quantitatively, including polyps, edema, rhinorrhea, scars, and scabs. For polyps, 0 point: without polyps, 1 point: only in the middle nasal meatus, and 2 points: exceeding the middle nasal meatus. For rhinorrhea, 0 point: without rhinorrhea, 1 point: clear and thin, and 2 points: viscous and purulent. For scars and scabs, 0 point: none, 1 point: mild, and 2 points: severe. Scars and scabs were only used to assess the surgical outcomes. The score was 0 to 10 points on each side, and the total score was 0 to 20 points.
SPSS 18.0 software was used for statistical analysis. Measurement data were expressed as mean ± SD (‘χ ± s) or median (lower quartile, upper quartile; (M[P25, P75]) and compared using the t test and rank sum test. Numerical data were expressed as (n [%]) and compared using the χ2 test. Pearson correlation analysis was performed, and risk factors were analyzed through multivariate logistic regression model. α = 0.05 was set as the test level, and 2-tailed P < .05 was considered to be statistically significant.
Complication with nasal polyps, allergic rhinitis history, and sinus surgery history had significant differences among patients of different ages (P < .05). However, the patients had similar course of disease, gender, septal deviation, smoking, drinking, and nasal decongestants used (P > .05; Table 1).
Three months after surgery, T&T olfactory, visual analogue scale (VAS) olfactory, Lund-Mackay, and Lund-Kennedy scores significantly declined in all groups compared with those before surgery (P < .05). Before and 3 months after surgery, the scores all rose with increasing age, with significant differences between any 2 groups (P < .05; Table 2).
The improvement of postoperative olfactory function became poorer with increasing age. In terms of T&T olfactory score, the total improvement rate was 83.52%, and the difference was statistically significant between elderly and child groups, youth and middle-aged groups, and middle-aged and child groups (P < .05). Regarding VAS olfactory score, the total improvement rate was 82.95%, and the difference was significant between elderly and child groups, elderly and youth groups, and middle-aged and child groups (P < .05). Thus, T&T and VAS olfactory scores were consistent (Table 3).
T&T and VAS olfactory scores had significant positive correlations with Lund-Mackay and Lund-Kennedy scores (P < .001; Figure 1).
According to the improvement of postoperative olfactory function, the patients with improvement or above of both T&T and VAS olfactory scores were assigned as good improvement group, while those without improvement of T&T or VAS olfactory score were assigned as poor improvement group. The 2 groups had similar course of disease, gender, septal deviation, smoking, drinking, and nasal decongestants used (P > .05). The good improvement group had younger patients, lower preoperative Lund-Mackay and Lund-Kennedy scores, fewer cases with nasal polyps, allergic rhinitis history and sinus surgery history, milder postoperative complications, and more patients who followed the doctor’s advice, showing significant differences from those of the poor improvement group (P < .05; Table 4).
Statistically significant factors in univariate analysis were employed as the independent variables, and the good/poor improvement of postoperative olfactory function was used as the dependent variable. Values were assigned to the independent variables as follows: age: ≤45 years = 1, <45 years = 0; preoperative Lund-Mackay score: ≤11.69 = 1, <11.69 = 0, with the median as the cutoff value; preoperative Lund-Kennedy score: ≤4.88 = 1, <4.88 = 0, with the median as the cutoff value; nasal polyps: Yes = 1, No = 0; allergic rhinitis history: Yes = 1, No = 0; sinus surgery history: Yes = 1, No = 0; doctordirected treatment: Yes = 1, No = 0; and postoperative complications: Yes = 1, No = 0. The results of multivariate logistic regression analysis revealed that age, preoperative Lund-Mackay and Lund-Kennedy scores, complication with nasal polyps, allergic rhinitis history, sinus surgery history, and postoperative complications were risk factors for the poor improvement of postoperative olfactory function of CRS patients. Doctor-directed treatment was a protective factor for good improvement (Table 5).
Olfactory sensation is one of the important sensory functions of human body. Olfactory dysfunction can affect the quality of life, and anosmia may make people unable to escape from a dangerous environment promptly. About 65% to 80% of CRS patients are plagued by various degrees of olfactory dysfunction.5 The olfactory dysfunction of CRS patients is aggravated with aging, which is consistent with changes in the preoperative T&T and VAS olfactory scores of CRS patients of different ages in this study.6 It has been confirmed that the age at which patients are most prone to allergic rhinitis is below 35 years, while nasal polyps are more common among adults aged above 30. Therefore, a younger age corresponds to higher incidence rate of allergic rhinitis and lower incidence rate of nasal polyps.7 Zhang et al found that the proportion of CRS patients with allergic rhinitis or asthma in youth group was significantly higher than those of middle-aged and elderly groups, while the proportion of cases with nasal polyps significantly decreased in youth group.8 Their findings are in accordance with those in this study.
The mechanism of olfactory sensation development is complicated, but it is well-accepted that olfactory elements, airflow, and olfactory system are necessary. Olfactory elements reach the olfactory area with the airflow and bind olfactory receptors, as the basis for olfactory sensation development. In CRS patients, the nasal cavity and sinuses have anatomic abnormalities, and there are swelling, polyps, and inflammation in the nasal mucosa, as well as obstruction of nasal discharge, all of which suppress ventilation and drainage, so gas molecules are no longer able to reach the olfactory area. At the same time, inflammatory response also causes damages to the olfactory epithelium and nerve, atrophy, and decrease of olfactory cells, resulting in olfactory dysfunction or even anosmia. Endoscopic sinus surgery, as one of the crucial treatment methods for CRS, can improve the olfactory function by 23% to 85%.9 Similarly, the total improvement rate herein was 83.52% in terms of T&T olfactory score and 82.95% in terms of VAS olfactory score. As the age increased, the improvement of postoperative olfactory function became poorer, which may be related to decline in the sensitivity of various sensory organs in the elderly. Moreover, older patients have worse recovery and prolonged course of disease, thus harming the improvement of postoperative olfactory function. It has previously been reported that apoptotic genes expressed in the olfactory epithelium of elderly rats significantly increased, thereby promoting the death of olfactory receptor neurons.10 Notably, the changes of T&T and VAS olfactory scores had consistency in this study.
The sinus CT Lund-Mackay score is currently the most recognized index for objectively assessing the lesion range of CRS. It is well-documented that a higher preoperative Lund-Mackay score means severer olfactory dysfunction of patients.11 However, the lesions of the superior meatus and ethmoid plates are not evaluated in the scoring criteria. From the anatomical viewpoint, the olfactory nerve epithelium is distributed in some areas of the superior turbinate, middle turbinate, ethmoid plates, and nasal septum. Therefore, the modified Lund-Mackay score was employed in this study. The Lund-Kennedy scoring system can be used to quantify the visible structure of the nasal cavity under a nasal endoscope to assess the efficacy of endoscopic sinus surgery. This scoring method focuses more on evaluation of the overall morphological changes in the nasal cavity, failing to determine the specific sites affecting the olfactory function. Regardless, the Lund-Kennedy score has been positively correlated with the degree of olfactory dysfunction.12 Likewise, T&T and VAS olfactory scores had correlations with Lund-Mackay and Lund-Kennedy scores in this study.
In this study, age, preoperative Lund-Mackay and Lund-Kennedy scores, complication with nasal polyps, allergic rhinitis history, sinus surgery history, and postoperative complications were risk factors for the poor improvement of postoperative olfactory function of CRS patients, while doctordirected treatment was a protective factor for good improvement, being consistent with the study of Wang et al.13 In addition to adults aged above 18 years, children aged below 18 years were also included herein. Chronic rhinosinusitis can be induced by allergic rhinitis. In CRS patients complicated with allergic rhinitis, a large amount of histamine is released to stimulate mastocytes under the mediation of IgE, so considerable inflammatory cytokines are released to directly act on the nasal mucosa, leading to nasal vasodilation, and increasing the vascular permeability and nasal glandular secretion. Moreover, mucosal epithelial thickening, proliferative changes, and nasal polyps may also be directly caused, thereby resulting in epithelization of the mucosal tissues of the nasal cavity receiving surgery and ultimately olfactory dysfunction.14 The incidence rate of olfactory cleft polyps in CRS patients is 52%, and the incidence rate of olfactory dysfunction in these patients is far higher than that of patients without olfactory cleft polyps.15 Nasal polyps block the olfactory cleft area, so the inhaled air cannot enter, which leads to decline in olfactory sensation or anosmia. In the case of larger nasal polyp, the obstruction of the olfactory area and decline in olfactory function are severer. The olfactory function of most patients can be greatly improved after surgical excision of nasal polyps. In addition, hormones allow the inhaled air to reach the olfactory cleft area smoothly through reducing nasal polyps and relieving mucosal swelling, thereby improving the olfactory function. Using glucocorticoids after endoscopic sinus surgery has local anti-allergic, anti-inflammatory, and anti-edema effects, and effectively protects the physiological structure and function of the nasal cavity. Meanwhile, the postoperative recurrence rate is low.16 Before surgery, the patients herein all received glucocorticoid fluticasone propionate spray and anti-inflammatory treatment for 3 days, so the effects of glucocorticoids on olfactory function were not assessed.
Higher preoperative Lund-Mackay and Lund-Kennedy scores mean larger lesions of nasal sinuses and mucosa, as well as severer nasal congestion, leading to poor drainage and inflammation. Chronic inflammation causes irritation and damage to the olfactory mucosa, thereby aggravating olfactory dysfunction. The history of sinus surgery indicates recurrence due to the unsatisfactory effect of previous surgery, and scar hyperplasia and nasal tissue adhesion may have already occurred. Re-surgery may aggravate the damage to the nasal mucosa and alter the main anatomical structure of the nasal cavity, thus reducing the defense ability. During doctor-directed treatment, the nasal cavity is cleaned before and after surgery, and the accumulation of nasal secretions is reduced, so the incidence rates of postoperative mucosal inflammatory lesions, adhesions, and granulation hyperplasia decrease. In addition, the reduction of postoperative complications is conducive to the recovery of patients.
In conclusion, the improvement of olfactory function of CRS patients after endoscopic sinus surgery declines with increasing age. Age, preoperative Lund-Mackay and Lund-Kennedy scores, complication with nasal polyps, allergic rhinitis history, sinus surgery history, and postoperative complications are risk factors for the poor improvement of postoperative olfactory function of CRS patients. Doctor-directed treatment is a protective factor for good improvement.
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
The author(s) received no financial support for the research, authorship, and/or publication of this article.
Weihuan Ma https://orcid.org/0000-0001-8320-6503
1 Department of ENT, Baoji Central Hospital, Baoji, Shaanxi Province, China
2 Department of Burn and Plastic Surgery, Baoji Central Hospital, Baoji, Shaanxi Province, China
Received: February 08, 2021; revised: March 30, 2021; accepted: April 06, 2021
Corresponding Author:Weihuan Ma, Department of Burn and Plastic Surgery, Baoji Central Hospital, Baoji, Shaanxi Province 721008, China.Email: asabgooca1983@web.de
