Prevalence of impaired lower airway function in Thai patients with allergic rhinitis

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Abstract

Background

Allergy is a chronic inflammatory disease, which may affect the upper and lower airway in reversible airflow obstruction or asthma. Spirometry is a noninvasive way to assess lower airway function routinely and to detect reversible airflow obstruction.

Objective

To determine the prevalence of abnormal spirometry in Thai patients with allergic rhinitis (AR) who did not have lower airway symptoms.

Method

Spirometry and bronchodilation testing were performed in AR patients.

Result

We included 153 patients aged from 20 to 60 years who had AR (diagnosed by clinical data and positive skin prick test) and who fulfilled the study criteria. Twenty-three patients with AR (15%) showed decreased forced expiratory volume in 1 s (FEV1) compared with normal values (FEV1 <80% of predicted value). Four patients with AR (3%) showed reversible airflow obstruction. Thirty-seven patients with AR (24%) showed decreased forced expiratory flow during 25-75 s (FEF25-75) compared with the reference value (FEF25-75 <80% of predicted value). The sensitization to both indoor and outdoor allergens was statistically and significantly associated with the decreased FEV1 (odds ratio (OR) = 7.79, 95% confidence interval (CI) 1.08-55.91, P = 0.03). The duration of AR was more than 10 years significantly affected FEF25-75 (adjusted OR = 2.6; 95%CI = 1.01-6.72, P = 0.04).

Conclusion

Impaired lower airway function and reversible airflow obstruction in patients with AR are not uncommon. Spirometry should be performed to detect lower airway impairment early in patients with AR, especially those sensitized to indoor and outdoor allergens.

Abstract

Background

Allergy is a chronic inflammatory disease, which may affect the upper and lower airway in reversible airflow obstruction or asthma. Spirometry is a noninvasive way to assess lower airway function routinely and to detect reversible airflow obstruction.

Objective

To determine the prevalence of abnormal spirometry in Thai patients with allergic rhinitis (AR) who did not have lower airway symptoms.

Method

Spirometry and bronchodilation testing were performed in AR patients.

Result

We included 153 patients aged from 20 to 60 years who had AR (diagnosed by clinical data and positive skin prick test) and who fulfilled the study criteria. Twenty-three patients with AR (15%) showed decreased forced expiratory volume in 1 s (FEV1) compared with normal values (FEV1 <80% of predicted value). Four patients with AR (3%) showed reversible airflow obstruction. Thirty-seven patients with AR (24%) showed decreased forced expiratory flow during 25-75 s (FEF25-75) compared with the reference value (FEF25-75 <80% of predicted value). The sensitization to both indoor and outdoor allergens was statistically and significantly associated with the decreased FEV1 (odds ratio (OR) = 7.79, 95% confidence interval (CI) 1.08-55.91, P = 0.03). The duration of AR was more than 10 years significantly affected FEF25-75 (adjusted OR = 2.6; 95%CI = 1.01-6.72, P = 0.04).

Conclusion

Impaired lower airway function and reversible airflow obstruction in patients with AR are not uncommon. Spirometry should be performed to detect lower airway impairment early in patients with AR, especially those sensitized to indoor and outdoor allergens.

Allergic rhinitis (AR) and allergic asthma are two common allergic diseases. The prevalence of AR worldwide, including Thailand, is 20%-40% [1, 2]. Epidemiologic studies have shown that the prevalence of asthma in patients with AR is 19%-35%, which is higher than the prevalence of asthma in the normal population [3, 4].

There are various ideas about the linkage of upper and lower airways, such as sharing similar airway epithelial lining and pathophysiology, and both conditions respond to same treatment modalities [5-7]. AR may lead to the development of asthma or aggravate an asthmatic attack. The first hypothesis is nasobronchial reflex. This reflex is considered to arise because of evidence that nasal irritation can lead to bronchoconstriction [8]. The second hypothesis is that mouth breathing as a result of AR can lead to unconditioned (cold, dry) air that passes to the lower airway, resulting in bronchial hyperactivity [4]. The third hypothesis is related to the systemic inflammation after the local nasal allergy. Allergic inflammation in the nose leads to release of cytokines and mediators especially interleukin (IL)-5 from bone marrow [9]. The fourth hypothesis is chronic irritation of lower airway from postnasal drip [9].

To evaluate the lower airway function, spirometry is the standard test. There are various studies from the west that have studied the prevalence of spirometric abnormalities in AR without asthmatic symptoms [10, 11]. Force expiratory volume in 1 s (FEV1) and the forced expiratory flow between 25% and 75% of forced vital capacity (FEF25_75) have been proposed as early predictors of small airway hyperresponsiveness [11]. In those studies, the risk factors, such as age, sex, duration of symptoms, type of allergen sensitization and symptom severity have been shown to affect spirometric impairment in patients with AR.

In Thailand, the prevalence of asthma associated with ARmostly derives from history taking, implying that patients already have symptoms of asthma [12]. There are limited data of impaired spirometry in AR without asthma in Asians. Although there are several articles showing the relationship between AR and the lower airway, the majority describe AR with concurrent asthma or with aggravation/worsening of asthma symptoms [12-15]. Because of the different types of allergens (e.g. grass pollens) and different clinical manifestations of AR (e.g. seasonal vs. perennial), the objective of this study was to determine the prevalence and risk factors of abnormal spirometry in Thais with AR without lower airway symptoms.

Method

The present study was a cross-sectional examination of pulmonary function in patients with AR The study was approved by the institutional review board of Siriraj hospital (certificate of approval No. Si224/2009). Written informed consent was obtained from all study participants. Patients with chronic (symptoms >1 year) rhinitis with positive allergic skin prick test (SPT) relevant to the history, 20-60 years old, and normal X-ray of the paranasal sinuses and the chest were included. SPT of common indoor allergens (house dust mite, cat, dog, and cockroach) and outdoor allergens (pollens and molds) was conducted. Once a diagnosis of AR was made, the severity of AR was classified according to the standard recommendations of the Allergic Rhinitis with its Impact on Asthma (ARIA) guidelines [16]. Exclusion criteria were pulmonary disease, asthma, current or previous smoking, severe cardiovascular disease, current use of ß-blocker drugs, pregnancy, aneurysm in the chest, aorta, or brain, previous history of ophthalmologic, abdominal or thoracic surgeries, immunodeficiency, hepatitis, and gastroesophageal reflux (by history).

Spirometry was performed using a computer assisted spirometer (Koko Spirometer, Ferraris Respiratory, Louisville, CO, USA). Patients stopped medication that may affect the spirometrie result before performing the test. The test was conducted by a single technician who is familiar with the technique recommended by the standard guidelines [17]. Two main values of spirometry including FEV and reversible airflow obstruction were considered. Airflow obstruction was defined as FEV1 values <80% of predicted [17, 18]. According to the guidelines, reversible airflow obstruction was defined as the increased FEV1 ≥12% from baseline [19]. The association between each spirometrie variable and AR parameters such as duration, severity, type of allergen sensitization were analyzed. The other variable of spirometry i.e. the force expiratory flow during 25-75 second (FEF25 75), was also recorded and analyzed because some articles proposed this value as a predictor of early airway obstruction [20-22].

Statistical analysis

Data were analyzed using STATA software (STATA version 12.0, Stata Corp, College Station, TX, USA). Age of subjects was shown in mean ± standard deviation (SD). Other baseline characteristic data including sex, duration of rhinitis symptoms, and type of allergen sensitization are expressed in number or percent.

Logistic regression analysis between spirometry and each variable/baseline parameter was analyzed. P were based on 2-sides with significant level of <0.05.

Results

We included 153 patients with AR in the present study. All patient participants fulfilled the criteria of symptoms of chronic rhinitis for one-year or more. None of them had any symptoms of asthma. Their characteristics are described in Table 1.

The mean ± SD of FEV1 and FEF25–75 was 98.89 ±11.93 and 95.64 ± 22.42, respectively. Twenty-three cases (15%) had abnormal FEV1 (Table 2). Four patients had a percent change of FEV1 higher than 12%. Thirty-seven patients had abnormal FEF25– 75. (Table 2).

Figure 1

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Figure 1

Study flow chart AR = Allergic rhinitis, CXR = chest x-ray, PNS = film paranasal sinus, FEV1 = force expiratory volume in 1 s.

Citation: Asian Biomedicine 10, 1; 10.5372/1905-7415.1001.467

Table 1

Patient characteristics

CharacteristicsNumber (percent)
Age (years)
 Mean ± standard deviation34.4 ±10.5 (range 20-59)
Sex
 Male/Female46 (30%)/107 (70%)
Duration of symptoms
 ≤ 5 years62 (41%)
 5-10 years52 (34%)
 ≥ 10 years39 (26%)
Severity of allergic rhinitis
 Mild intermittent38 (25%)
 Moderate/severe intermittent37 (24%)
 Mild persistent19 (12%)
 Moderate/severe persistent59 (39%)
Allergic to indoor allergens25 (16%)
Allergic to outdoors allergens16 (11%)
Allergic to both indoor and outdoor allergens112 (73%)
Table 2

Prevalence of abnormal pulmonary function test results

FEV1= Force expiratory volume in 1 second, FEF25–75 = force expiratory flow during 25-75 s

Number (percent)
Abnormal FEV123 (15%)
Abnormal % change of FEV14 (3%)
Abnormal FEF25–7537 (24%)

In 23 patients who had FEV1 less than 80% of predicted value, half had moderate to severe persistent symptom severity. The majority were sensitized to both indoor and outdoor allergens (Table 3).

Table 3

Prevalence of abnormal pulmonary function (Force expiratory volume in 1 s <80%), duration of allergy, severity of allergic symptoms, and sensitization to allergens

NumberPrevalence (%)
Overall prevalence15323 (15)
Duration of allergy
 ≤ 5 years6210 (16)
 5-10 years527 (14)
 ≥ 10 years396 (15)
Severity of allergic symptoms
 Mild intermittent384 (11)
 Moderate/severe intermittent375 (14)
 Mild persistent192 (11)
 Moderate/severe persistent5912 (20)
Sensitization to indoor allergens251 (4)
Sensitization to outdoor allergens161 (6)
Sensitization to both indoor and outdoor allergens11221 (19)

The sensitization to both groups of allergens was significantly associated with FEV1 abnormality (odds ratio = 7.79, 95%confidence interval (CI) 1.08-55.91, P < 0.03). There was no association between FEV1 abnormality and other variables such as duration of allergy, symptom severity, sensitization to indoor allergens only and sensitization to outdoor allergens only (Table 4).

Table 4

Clinical characteristics and their relation to FEV1

OR = odds ratio, CI = confidence interval, FEV1= force expiratory volume in 1 s

CharacteristicsTotalSubject with FEV1 < 80%OR95%CIP
Duration of allergy (y)
 ≤ 56210 (16%)1-
 5-10527 (14%)0.830.34-2.040.691
 ≥ 10396 (15%)0.950.38-2.420.921
Severity of allergic symptoms-
 Mild intermittent384 (11%)1-
 Moderate/severe intermittent375 (14%)1.280.37-4.410.691
 Mild persistent192 (11%)10.20-4.981.000
 Moderate/severe persistent5912 (20%)1.930.67-5.550.203
Sensitization to indoor allergens591 (4%)0.230.08-1.650.09
Sensitization to outdoor allergens161 (6%)0.390.06-2.690.29
Sensitization to indoor and outdoor allergens11221 (19%)7.791.08-55.91*0.03

Four patients had the percent changes of FEV1 ≥12% after bronchodilator administration. There was no association between abnormal percent change of FEV1 and the duration of allergy, symptom severity, type of allergen sensitization (Table 5).

Table 5

Clinical characteristics and their relation to percent changes of FEV1

OR = Odds ratio, CI = Confidence interval, FEV1= force expiratory volume in 1 s

CharacteristicsTotalSubject with percent change FEV1≥ 12%OR95%CIP
Duration of allergy (y)
 ≤ 5620 (0%)--
 5-10523 (5.8%)--0.06
 ≥ 10391 (2.6%)--0.21
Severity of allergic symptoms
 Mild intermittent381 (2.63%)1-
 Moderate/severe intermittent371 (2.7%)1.030.07-15.820.99
 Mild persistent190 (0%)0-0.48
 Moderate/severe persistent592 (3.39%)1.280.12-13.710.83
Sensitization to indoor allergens252 (8%)5.120.75-34.660.06
Sensitization to outdoor allergens160 (0%)000.48
Sensitization to indoor and outdoor allergens1122 (1.79%)0.360.05-2.510.28

Thirty-seven patients had the value of FEF25–75 <80% of predicted value. From the univariate analysis, moderate/severe intermittent symptom severity seemed to affect FEF25–75. Therefore, in the multivariate analysis of symptom severity was not significant.

The duration of allergic symptoms >10 y significantly affected FEF25–75. Multivariate analysis found duration significantly affected FEF25–75 (adjusted OR = 2.07; 95%CI = 1.01-4.25, P < 0.05). There was no influence of abnormal percent change of FEF25–75 on sensitization to indoor or outdoor allergens (Table 6).

Table 6

Clinical characteristics and their relation to FEF25–75

OR = odds ratio, CI = confidence interval, FEV1= force expiratory volume in 1 s, FEF25–75 = force expiratory flow during 25-75 second, *P < 0.05

CharacteristicsTotalParticipant with FEF2–75<80%OR95%CIP
Duration of allergy (y)
 ≤ 56210 (16%)1-
 5-105214 (27%)1.670.81-3.040.16
 ≥ 103913 (33%)2.071.01-4.25*0.04
Severity of allergic symptoms
 Mild intermittent3810 (26%)1-
 Moderate/severe intermittent379 (24%)0.920.42-2.010.04
 Mild persistent194 (21%)0.800.28-2.210.66
 Moderate/severe persistent5914 (24%)0.900.44-1.810.77
Sensitization to indoor allergens258 (32%)1.410.73-2.710.31
Sensitization to outdoor allergens166 (38%)1.660.82-3.350.19
Sensitization to both indoor and outdoor allergens11223 (21%)0.600.34-1.050.08

Discussion

International Study of Asthma and Allergies in Childhood (ISAAC) standardized questionnaire showed that the prevalence of asthmatic symptoms ranged from 2.1% to 32.2% [2]. In Thailand, the ISAAC phase three survey showed that 13.9%–25% of children with rhinitis had asthma [1]. Recently, we reported 16.1 % of our patients with AR treated at the ear, nose, and throat (ENT) allergy clinic had concomitant symptoms of asthma [12]. In that study, 15 percent of patients with AR (23 of 153 patients) had abnormal FEV, even though they did not have any lower airway symptoms. Our 15% prevalence of FEV1 abnormality differs from the finding reported by Ciprandi et al. (8% prevalence) even though the standard criteria, the value of FEV, <80% of predicted value was used as the outcome parameter [11]. These 23 cases of our series have been followed up regularly in our ENT allergy clinic to monitor the possibility of lower airway involvement.

Because the definition of asthma is a reversible airway condition, some studies considered ≥ 12 percent change of FEV, after bronchodilator administration as another variable by which to diagnose asthma [23]. In our study, only 4 patients showed >12 percent changes of FEV,.

Ciprandi et al. proposed the FEF25–75 as an early indicator of lower airway involvement [20, 24, 25]. The various cut-off value of FEF25_75 has been proposed, but the consensus of cut-off value has not yet been established. When using the criteria of FEF25–75 less than 80% of predicted value as suggested [26], the prevalence of abnormal FEF25–75 was 24.2% (37/153 patients) in our study. The prevalence of our abnormal FEV25–75 was higher than the finding of Ciprandi et al. (11%) in 2009.

Several clinical parameters may influence the abnormality of spirometry. For example, duration of rhinitis had been shown to be moderately correlated (Pearson’s correlation coefficient = 0.36) with the abnormality of FEV1 [26]. Our data showed the longer duration of AR (especially a duration >10 y) affected the FEF25–75. This data is consistent that reported by Ciprandi et al. in 2010, who found that patients with a long duration of AR were more likely to develop small airway obstruction [26].

The nasal symptom severity (as measured by total nasal symptom score) has been shown to affect nasal airflow and FEV1 [27]. When nasal symptom severity was classified according to ARIA classification, the majority of our patients were categorized as the moderate-severe/persistent group [16, 28]. The symptom severity, according to ARIA classification, did not show influence on spirometric values either FEV1, percent change of FEV1 or FEF25–75 in our study.

Spirometry can show sensitization to outdoor and indoor allergens. Ciprandi etal. [26] showed significant influence of pollen allergen (P < 0.01) and barely significant of perennial allergens (P < 0.05) on FEV1 and FEF25–75. In the present study, sensitization to indoor and outdoor allergens significantly influenced FEV1 (P < 0.05). By contrast with the studies from Europe, pollen sensitization or allergy showed no influence on FEV1 in our patient participants [29, 30].

An explanation for the differences in prevalence of spirometric abnormalities and risk factors between our present study and the various studies conducted in Europe are proposed as follows. First, allergens in Thailand differ from those in Europe or North America, for instance birch, hazel, and olive trees are rare in Thailand. Second, the severity of AR has been classified according to ARIA instead of a visual analog scale. Last, in tropical countries, a pattern of perennial AR is more prevalent than seasonal AR.

Although the present study provides information regarding the prevalence of abnormal spirometry

results in patients with AR, it has some limitations. First, patients may not be presenting lower airway obstruction on the occasion of the examination, but on different occasions bronchospasm may develop. The application of allergen-specific nasal provocation tests in combination with spirometry in patients with AR showed that allergic nasal reactions may lead to the development of upper and/or lower ventilation obstruction in patients with AR and previously normal spirometry [31, 32]. Second, other spirometry variables such as forced vital capacity (FVC) or the ratio of FEV1 to FVC were not included in the interpretation. Third, the possibility that other unrecognized lower airway conditions (such as occult bronchiectasis) might interfere with interpretation of spirometrie abnormality cannot be excluded. Nevertheless, this study included the patients with AR without any lower airway symptoms, without abnormal chest x-ray, and who were nonsmokers. Moreover, all participants stopped antiallergic medication for one week before the day of spirometry, because of the allergen skin prick test was performed on the same day. These modalities would reduce the possibility of confounding factors affecting pulmonary function test interpretation.

Conclusion

In patients with AR who had no symptoms of lower airway, the prevalence of abnormal FEV1 (<80% of predicted value) and abnormal percent change of FEV1 (≥12%) after bronchodilator were 15% and 2.6% respectively. The early predictor of small airway obstruction (FEF25–75) was abnormal in 24.2%. The sensitization to both indoor and outdoor allergens significantly affected FEV1 abnormality. A duration of allergy more than 10 y significantly affected FEF25–75. When patients with AR seek treatment, the lower airway status should always be evaluated. Awareness of upper and lower airway linkage will lead to early and proper treatment before significant deterioration of lower airway function occurs. A suspicion of bronchial asthma should be raised especially in patients from an AR subgroup.

Acknowledgments

The authors would like to thank Dr. Premyos Nguathepprutharam, Ms. Jeerapa Kerdnoppakhun, and Mr. Wannachai Kaewkeb for the data collection. This study was supported by the research grant from the Siriraj Research Fund and the National Research Fund (NRU) of Mahidol University.

Conflict of interest statement: The authors have no conflicts of interest to declare.

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Footnotes

*

P < 0.05

*

P < 0.05

1

Trakultivakorn M, Sangsupawanich P, Vichyanond P. Time trends of the prevalence of asthma, rhinitis and eczema in Thai children-ISAAC (International Study of Asthma and Allergies in Childhood) Phase Three. J Asthma. 2007; 44:609-11.

2

ISAAC, Steering Committee. Worldwide variations in the prevalence of asthma symptoms: the International Study of Asthma and Allergies in Childhood (ISAAC). Euro Respir J. 1998; 12:315-35.

3

Kämpe M, Stolt I, Lampinen M, Janson C, Stälenheim G, Carlson M. Patients with allergic rhinitis and allergic asthma share the same pattern of eosinophil and neutrophil degranulation after allergen challenge. Clin Mol Allergy. 2011; 9:3. doi:10.1186/1476-7961-9-3.

4

Pedersen PA, Weeke ER. Asthma and allergic rhinitis in the same patients. Allergy. 1983; 38:25-9.

5

Garcia-Marcos L, Rubi Ruiz T, Garcia-Hernandez G, Suarez-Varela MM, Valverde-Molina J, Sanchez-Solis M. Asthma and rhinoconjunctivitis comorbidity: united airway disease or inherited target organs? Pediatr Allergy Immunol. 2010; 21:e142-8.

6

Hens G, Vanaudenaerde BM, Bullens DM, Piessens M, Decramer M, Dupont LJ, et al. Sinonasal pathology in nonallergic asthma and COPD: ‘united airway disease’ beyond the scope of allergy. Allergy. 2008;63: 261-7.

7

Rimmer J, Ruhno JW. 6: Rhinitis and asthma: united airway disease. Med J Australia. 2006; 185:565-71.

8

Kaufman J, Wright GW. The effect of nasal and nasopharyngeal irritation on airway resistance in man. Am Rev Respir Dis. 1969; 100:626-30.

9

Braunstahl GJ, Fokkens W. Nasal involvement in allergic asthma. Allergy. 2003; 58:1235-43.

10

Bavbek S, Saryal S, Karabiyikoglu G, Misirligil Z. Pulmonary function parameters in patients with allergic rhinitis. J Investig Allergol Clin Immunol. 2003; 13:252-8.

11

Ciprandi G, Signori A, Tosca MA, Cirillo I. Spirometric abnormalities in patients with allergic rhinitis: Indicator of an “asthma march” Am J Rhinol Allergy. 2011; 25:e181-5.

12

Bunnag C, Jareoncharsri P, Tantilipikorn P, Vichyanond P, Pawankar R. Epidemiology and current status of allergic rhinitis and asthma in Thailand- ARIA Asia-Pacific Workshop report. Asian Pac J Allergy Immunol. 2009; 27:79-86.

13

Koh YI, Choi IS. Relationship between nasal and bronchial responsiveness in perennial allergic rhinitic patients with asthma. Int Arch Allergy Immunol. 2002; 129:341-7.

14

El-Helaly N, Samy SM, Ibrahim TS, Morcos WM, El- Hoshy HM, Mohamed DA. Pulmonary function changes in allergic rhinitis with or without bronchial asthma. J Am Science. 2012; 8:110-4.

15

Deb A, Mukherjee S, Saha BK, Sarkar BS, Pal J, Pandey N, et al. Profile of patients with allergic rhinitis (AR): a clinic based cross-sectional study from Kolkata, India. J Clin Diagn Res. 2014; 8:67-70.

16

Brozek JL, Bousquet J, Baena-Cagnani CE, Bonini S, Canonica GW, Casale TB, et al. Allergic Rhinitis and its Impact on Asthma (ARIA) guidelines: 2010 Revision. J Allergy Clin Immunol. 2010; 126:466-76.

17

Standardized lung function testing. Official statement of the European Respiratory Society. Euro Respir J Supp. 1993;16:1-100.

18

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Journal Information


IMPACT FACTOR 2017: 0.209
5-year IMPACT FACTOR: 0.243

CiteScore 2017: 0.24

SCImago Journal Rank (SJR) 2017: 0.162
Source Normalized Impact per Paper (SNIP) 2017: 0.173

Figures

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    Study flow chart AR = Allergic rhinitis, CXR = chest x-ray, PNS = film paranasal sinus, FEV1 = force expiratory volume in 1 s.

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