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ORIGINAL ARTICLE
Year : 2013  |  Volume : 27  |  Issue : 2  |  Page : 134-137

Correlation between nasal nitric oxide, nasal airway resistance and atopy in patients of allergic rhinitis


Department of Respiratory Allergy and Applied Immunology, Vallabhbhai Patel Chest Institute, University of Delhi, Delhi, India

Date of Web Publication4-Jan-2014

Correspondence Address:
Raj Kumar
Department of Respiratory Allergy and Applied Immunology, Vallabhbhai Patel Chest Institute, University of Delhi, Delhi - 110 007
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-6691.124396

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  Abstract 

Background: Nasal airway resistance (NAR) is dependent upon the tone of the nasal vasculature, which is regulated by endothelially derived nitric oxide (NO). Aim: The aim of this study was to investigate the relationship between nasal nitric oxide (nNO) levels, NAR and atopy in patients of allergic rhinitis (AR). Materials and Methods: The subjects were assessed for nNO levels by NIOX chemiluminescence analyzer. NAR was measured by 4-Phase-Rhinomanometry using RHINOTEST 1000. Atopy was assessed by skin prick testing against 58 common aeroallergens. Statistical Analysis: SPSS, Chicago, IL, USA, statistical package version 14 using independent sample t-test and Pearson correlation Results: In the study, 15 diagnosed cases of AR and five healthy volunteers as control were included. In the control group, the mean total NAR was 0.16 ± 0.08 kPa/l/s while in AR group mean total NAR was 0.22 ± 0.1 kPa/ l/s (P = 0.4). In AR group mean left and right NAR were 0.50 ± 0.28 kPa/l/s and 0.52 ± 0.4 kPa/l/s respectively and mean nNO levels of right and left nostrils were 291.2 ± 122.90 ppb and 251 ± 171.16 ppb (P = 0.7). No correlation was found between the left or right unilateral NAR and nNO levels, respectively. Similarly, no significant correlation of unilateral NAR and NO levels were found in the control group. Atopic AR patients had higher NAR (P = 0.001) and nNO (P = 0.06) compared with non-atopic rhinitis patients. Conclusion: In our study, AR group had higher NAR, but no correlation was found between nNO and NAR in either groups. The atopic AR patients had significantly higher NAR in comparison with non-atopic patients.

Keywords: Allergic rhinitis, nasal nitric oxide, rhinomanometry


How to cite this article:
Kumar R, Gupta N. Correlation between nasal nitric oxide, nasal airway resistance and atopy in patients of allergic rhinitis. Indian J Allergy Asthma Immunol 2013;27:134-7

How to cite this URL:
Kumar R, Gupta N. Correlation between nasal nitric oxide, nasal airway resistance and atopy in patients of allergic rhinitis. Indian J Allergy Asthma Immunol [serial online] 2013 [cited 2019 Nov 15];27:134-7. Available from: http://www.ijaai.in/text.asp?2013/27/2/134/124396


  Introduction Top


Nasal obstruction is a common condition in patients suffering from allergic rhinitis (AR). [1] The degree to which nasal obstruction causes symptoms is determined by the severity of the obstruction and by the subjective perception of obstruction to nasal airflow. In general, rhinomanometry provides information about nasal airway flow, resistance and assessment of patency of the nose. [2]],[[3]],[[4] Thus, it provides a sensitive and functional measure of nasal patency during normal breathing. Nasal nitric oxide (nNO) originates from the nasal epithelium and paranasal sinuses [5],[6] and this endothelially derived nitric oxide (NO) is an established vasodilator. Nasal airway resistance (NAR) is dependent upon the tone of the nasal vasculature, which in turn is regulated by endothelially derived NO.

After an extensive search of databases and to the best of our knowledge no study correlating the marker of nasal inflammation (nNO), NAR and atopy was found in Indian population. Hence, the present study was undertaken to study the correlation.


  Materials and Methods Top


Study population and design

The study was conducted at out-patient department between August and November 2012. The patients of AR visiting the out-patient department were included for the study. The study group consisted of total 20 subjects; 15 cases of AR and five healthy volunteers as controls. The age of the patients ranged from 18 to 36 years. The diagnosis of AR was made based on the clinical definition of AR as per Allergic Rhinitis and its impact on asthma guidelines i.e., any patient with symptoms of rhinorrhea, nasal obstruction, nasal itching and sneezing, which are reversible spontaneously or with treatment. [7]

The nNO measurements were performed by the nasal aspiration method, using chemiluminescence analyzer (NIOX Aerocrine AB, Solna, Sweden) in accordance with the 2005 American Thoracic Society/European Respiratory Society recommendations for standardized online measurements. [8] Patient exhaled through a tightly fitting nasal mask adapted to the analyzer enabling nNO measurements. The NAR was measured by 4-Phase-Rhinomanometry (4PR) using the RHINOTEST 1000, by examining flow and pressure in the upper respiratory airway. This is active anterior rhinomanometry using the 4PR software of Vogt et al.[9],[10] Skin prick test (SPT) was performed against 58 aeroallergens, routinely used for allergy testing in our department. Atopy was defined as a positive SPT (wheal diameter of >3 mm as compared to Buffer saline as control) for at least one aeroallergen. [11] A patient with negative SPT to all aeroallergens was labeled as non-atopic.

Statistical analysis

All data analysis was performed using SPSS statistical package version 14.0 for windows (SPSS, Chicago, IL, USA) and Prism 6.0. The univariate analyses of factors associated with nNO was done using Pearson correlation. The measurements for nNO were compared between groups using the independent sample t-test.


  Results Top


The study included 15 diagnosed cases of AR and five healthy volunteers as controls. The age ranged from 18 to 36 years, mean being 21.26 years. There were 11 atopic and four non-atopic patients in AR group; the control group had only non-atopic subjects. In AR group mean total NAR was 0.22 ± 0.1 kPa/l/s and in the control group the mean total NAR was 0.16 ± 0.08 kPa/l/s. The AR group had higher NAR in comparison with control group, the difference was not statistically significant (P = 0.24). In AR group, mean left and right NAR were 0.50 ± 0.28 kPa/l/s and 0.52 ± 0.4 kPa/l/s respectively (P = 0.9) and mean nNO levels from the left and right nostrils were 251 ± 171.16 ppb and 291.2 ± 122.90 ppb (P = 0.7). The difference between the levels of NAR and nNO from either nostril were not significant.

In patients of AR on evaluation of the left or right unilateral NAR and nNO levels respectively, no correlation was found between these measurements from either nose (right nose r = 0.378, P = 0.16; left nose r = −0.46, P = 0.869). Similarly, the mean nNO levels and NAR did not show any significant correlation [Figure 1] in AR group. Furthermore, there was no significant correlation between total NAR and the left nNO levels (r = −0.002, P = 0.9) or total NAR and right nNO levels (r = 0.101, P = 0.7) in AR patients. Atopic AR patients had significantly higher NAR as compared to non-atopic patients (0.24 ± 0.05 vs. 0.17 ± 0.02; P = 0.001) [Figure 2], also the nNO levels in atopic rhinitis were higher as compared with non-atopic rhinitis (292.13 ± 154.1 vs. 213.25 ± 42.3, P = 0.06) [Figure 3]. In the control group, no correlation was found between the right or left unilateral NAR and NO levels respectively (right r = −0.562, P = 0.178; left r = −0.423, P = 0.478). Similarly, no correlation was found between mean nNO levels and NAR in the control group [Figure 4].
Figure 1: Correlation between mean nasal nitric oxide and nasal airway resistance in allergic rhinitis

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Figure 2: The nasal nitric oxide levels in atopic and non-atopic allergic rhinitis

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Figure 3: The nasal airway resistance in atopic and non-atopic allergic rhinitis

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Figure 4: Correlation between mean nasal nitric oxide and nasal airway resistance in control group

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  Discussion Top


Nasal obstruction is a dominant symptom associated with all types of rhinitis; [12] it is an indirect marker of nasal inflammation, subjecting to the condition that there are no significant permanent nasal anatomical abnormalities which contribute to reduced nasal airflow. The disease processes or drugs cause dilation of nasal blood vessels, thus leading to swelling of the nasal venous sinuses, will be associated with nasal obstruction. In subjects with no signs or symptoms of nasal disease, the NAR has been observed to be ranging between 0.15 and 0.39 Pa/cm 3 /s. [13] However, to distinguish between skeletal stenosis and mucosal swelling, it is imperative to have reference values for NAR for the technique that is being used. However, generally usable validated normal data for NAR is still lacking and that is a major problem.

In a study by Ferguson [14] on 123 healthy volunteers, no relationship was found to exist between nNO concentration and total NAR. Similarly, the study did not found any correlation between the left or right unilateral NAR and left or right nNO concentration, respectively. In our study results, no correlation was found between nNO and NAR in both AR patients and healthy volunteers. However a study by Imada et al. [15] on healthy volunteers proposed that nNO may be involved in the control of NAR.

In a cross-sectional study of 200 subjects, 112 suffering from nasal disease and 88 normal subjects by Suzina et al., [16] the mean total NAR was significantly higher in patients with nasal disease (0.33 Pa/cm 3 /s) as compared with normal subjects (0.24 Pa/cm 3 /s). However, there was no significant difference in total NAR between patients with symptoms of nasal obstruction and those without the symptoms (P = 0.42). Our study also showed higher NAR in AR group as compared with the healthy group, though not statistically significant.

The nNO levels in AR and control group were 274.40 ± 132.23 ppb and 130.20 ± 100.12 ppb respectively. The AR group had significantly higher nNO levels (P = 0.03). In a study by Kharitonov et al., [17] the mean nNO levels in AR were significantly (P < 0.001) elevated in patients with untreated rhinitis (1527 ± 87 ppb, n = 12) compared with normal individuals (996 ± 39 ppb, n = 46).

The atopic AR patients also had higher nNO levels in comparison to non-atopic patients (292.13 ± 154.10 ppb vs. 213.25 ± 42.3 ppb), though the result was not statistically significant (P = 0.06). Kharitonov et al., in another study [18] showed higher nNO levels in atopic subjects exposed to pollens during the pollen season. Our study also showed significantly higher levels of NAR in atopic subjects compared with non-atopic subjects of allergic. However, to the best of our knowledge we could not found a study directly correlating the atopy and NAR. Thus, role of atopy in NAR measurements needs further evaluation. The limitation of our study is a small sample size and hence further large scale longitudinal studies are required for the generalization of results to the larger population.


  Conclusion Top


In our study, AR group had higher NAR, but no correlation was found between nNO and NAR in either AR group or control group. Furthermore, the atopic AR patients had significantly higher NAR in comparison to non-atopic patients.

 
  References Top

1.Jessen M, Malm L. Definition, prevalence and development of nasal obstruction. Allergy 1997;52:3-6.  Back to cited text no. 1
    
2.Empey DW. Assessment of the nasal passages. Br J Clin Pharmacol 1980;9:317-9.  Back to cited text no. 2
    
3.McCaffrey TV. Rhinomanometry and diagnosis of nasal obstruction. Facial Plast Surg 1990;7:266-73.  Back to cited text no. 3
    
4.Eccles R. Rhinomanometry and nasal challenge. In: Mackay IS, Bull TR, editors. Scott-Brown′s Otolaryngology. 5 th ed. London: Butter-worth-Heinemann; 1987. p. 40-53.  Back to cited text no. 4
    
5.Furukawa K, Harrison DG, Saleh D, Shennib H, Chagnon FP, Giaid A. Expression of nitric oxide synthase in the human nasal mucosa. Am J Respir Crit Care Med 1996;153:847-50.  Back to cited text no. 5
    
6.Lundberg JO, Farkas-Szallasi T, Weitzberg E, Rinder J, Lidholm J, Anggåard A, et al. High nitric oxide production in human paranasal sinuses. Nat Med 1995;1:370-3.  Back to cited text no. 6
    
7.Bousquet J, Khaltaev N, Cruz AA, Denburg J, Fokkens W, Togias A, et al. Allergic rhinitis and its impact on asthma 2008. Allergy 2008;63:1-91.  Back to cited text no. 7
    
8.American Thoracic Society, European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med 2005;171:912-30.  Back to cited text no. 8
    
9.Vogt K, Jalowayski AA, Althaus W, Cao C, Han D, Hasse W, et al. 4-phase-rhinomanometry (4PR) - Basics and practice 2010. Rhinol Suppl 2010;21:1-50.  Back to cited text no. 9
    
10.Vogt K, Zhang L. Airway assessment by four-phase rhinomanometry in septal surgery. Curr Opin Otolaryngol Head Neck Surg 2012;20:33-9.  Back to cited text no. 10
    
11.Gaur SN, Singh BP, Singh AB, Vijayan VK, Agarwal MK. Guidelines for practice of allergen immunotherapy in India. Indian J Allergy Asthma Appl Immunol 2009;23:1-20.  Back to cited text no. 11
    
12.Eccles R. Nasal airflow and decongestants. In: Naclerio RM, Durham SR, Mygind N, editors. Rhinitis Mechanisms and Management. New York: Marcel Dekker; 1999. p. 291-312.  Back to cited text no. 12
    
13.Morris S, Jawad MS, Eccles R. Relationships between vital capacity, height and nasal airway resistance in asymptomatic volunteers. Rhinology 1992;30:259-64.  Back to cited text no. 13
    
14.Ferguson EA, Eccles R. Relationship between nasal nitric oxide concentration and nasal airway resistance. Rhinology 1997;35:120-3.  Back to cited text no. 14
    
15.Imada M, Iwamoto J, Nonaka S, Kobayashi Y, Unno T. Measurement of nitric oxide in human nasal airway. Eur Respir J 1996;9:556-9.  Back to cited text no. 15
    
16.Suzina AH, Hamzah M, Samsudin AR. Objective assessment of nasal resistance in patients with nasal disease. J Laryngol Otol. 2003;117:609-13.  Back to cited text no. 16
    
17.Kharitonov SA, Gonio F, Kelly C, Meah S, Barnes PJ. Reproducibility of exhaled nitric oxide measurements in healthy and asthmatic adults and children. Eur Respir J 2003;21:433-8.  Back to cited text no. 17
    
18.Kharitonov SA, Rajakulasingam K, O′Connor B, Durham SR, Barnes PJ. Nasal nitric oxide is increased in patients with asthma and allergic rhinitis and may be modulated by nasal glucocorticoids. J Allergy Clin Immunol 1997;99:58-64.  Back to cited text no. 18
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]



 

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