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Prevalence and risk factors for allergic rhinitis in primary school children
International Journal of Pediatric Otorhinolaryngology (2007) 71, 463—471
www.elsevier.com/locate/ijporl
Prevalence and risk factors for allergic rhinitis in primary school children Zeynep Tamay a,*, Ahmet Akcay b, Ulker Ones a, Nermin Guler a, Gurkan Kilic a, Mehmet Zencir c a
Department of Pediatrics, Division of Allergy and Chest Diseases, Istanbul School of Medicine, Istanbul University, Istanbul, Turkey b Department of Pediatrics, Pamukkale School of Medicine, Pamukkale University, Pamukkale, Turkey c Department of Public Health, Pamukkale School of Medicine, Pamukkale University, Pamukkale, Turkey Received 13 June 2006; received in revised form 15 November 2006; accepted 17 November 2006
KEYWORDS Allergic rhinitis; ISAAC; Risk factors; Children
Summary Objective: Allergic rhinitis is a common chronic illness of childhood. The aim of the study was to evaluate the prevalence and risk factors of allergic rhinitis in 6—12-yearold schoolchildren in Istanbul. Methods: A total of 2500 children aged between 6 and 12 years in randomly selected six primary schools of Istanbul were surveyed by using the International Study of Asthma and Allergies in Childhood (ISAAC) questionnaire between April and May 2004. Results: Of them 2387 (1185 M/1202 F) questionnaires were appropriately completed by the parents with an overall response of 95.4%. The prevalence of physiciandiagnosed allergic rhinitis was 7.9% (n = 189). A family history of atopy (aOR = 1.30, 95% CI = 1.00—1.68), frequent respiratory tract infection (aOR = 1.36, 95% CI = 1.08—1.70) and sinusitis (aOR = 2.29, 95% CI = 1.64—3.19), antibiotic use in the first year of life (aOR = 1.26, 95% CI = 1.01—1.57), cat at home in the first year of life (aOR = 2.21, 95% CI = 1.36—3.61), dampness at home (aOR = 1.31, 95% CI = 1.04— 1.65) and perianal redness (aOR = 1.26, 95% CI = 1.01—1.57) were significant for increased risk for allergic rhinitis. Frequent consumption of fruits and vegetables were inversely, and frequent consumption of lollipops and candies were positively associated with allergic rhinitis symptoms. Conclusion: Our study reconfirmed that family history of atopy, frequent respiratory tract infections, antibiotics given in the first year of life, cat at home in the first year of life, dampness at home, perianal redness and dietary habits are important
* Corresponding author at: Department of Pediatrics, Istanbul Medical Faculty, Capa 34390, Istanbul, Turkey. Tel.: +90 212 4142000/32349; fax: +90 212 6319301. E-mail address: [email protected] (Z. Tamay). 0165-5876/$ — see front matter # 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2006.11.013
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Z. Tamay et al. independent risk factors for AR. Researchers worldwide should be focused to these factors and try to develop policies for early intervention, primary and secondary preventions for allergic diseases. # 2006 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Allergic rhinitis (AR) is a very common disease in childhood as well as in adults and impairs the quality of life if left untreated [1]. AR is characterized by nasal itching, sneezing, watery rhinorrhoea and nasal obstruction [1]. The prevalence of childhood AR shows wide variation throughout the world, ranging from 0.8% to 39.7% [2]. The prevalence of allergic diseases has increased predominantly in developed countries, which indicates that environmental risk factors and life style rather than genetic predisposition seem to be the major determinants of allergic diseases [2—4]. Various risk factors have been described for AR according to different stages during life. Family history of atopy, month of birth, parental smoking, male sex, early exposure to allergens or pollutions were considered to be potential risk factors by epidemiological surveys [1,4—6]. But major determinants contributing development of AR is still not clear. The aim of the study was to evaluate the prevalence and risk factors of allergic rhinitis in 6—12year-old schoolchildren in Istanbul.
2. Methods This survey was held in children aged between 6 and 12 years in randomly selected six primary schools in Istanbul. A total of 2500 questionnaires were distributed to the children to be completed by their parents at home. The return visit to the school was done within a 2-week period to try to collect data from children formerly absent. The standardized ISAAC Phase I written core questionnaire was translated into Turkish and used. There have been quite a few studies carried out in Turkey using the ISAAC questionnaire [7—10], therefore it is well known and validated in Turkish studies. An additional questionnaire was prepared to identify demographic features and potential risk factors, including: sex, family history of atopy, the presence of physiciandiagnosed eczema or food allergy, frequent upper airway infections and sinusitis, history of tonsillectomy or adenoidectomy, antibiotic or paracetamol use in the first year of life, exposure to tobacco smoke at home, maternal and paternal smoking, cat or dog ownership in the first year of life, home
dampness, heating system, born in and living period in Istanbul, exposure to diesel trucks, perianal redness and diet. Dietary intake was estimated by using additionally a semi-quantitative food frequency questionnaire. Consumption of protective foods including starch such as potatoes, rice, cereals, pasta, vegetables, fish, other sea foods, fruits, nuts, olive oil, fish oil, and some traditional foods made from grapes and mulberries, fermented drinks made from millets and various seeds; aggravating foods including fast-food, potato chips, crackers, chocolates, lollipops, candies, cookies, muffins, margarine; other foods including eggs, animal fats, milk and dairy products, meat, polyunsaturated fatty acids (butter), sun-flower oil, corn oil, tea, olive and were asked [11]. Analysis of diet variables were determined by frequency of consumption of foods in three groups including: ‘‘never or occasionally’’, ‘‘once or twice per week’’ and ‘‘three or more times a week’’. Having a problem with sneezing or a runny, or blocked nose in the absence of a cold or a flu in the past 12 months was assessed as ‘‘current allergic rhinitis’’ [2,12]. Positive response to the question about having had allergic rhinitis diagnosed by a physician was considered to be ‘‘ever doctor-diagnosed allergic rhinitis’’. Severity of allergic rhinitis was assessed among children with current rhinitis from the responses the questions on the presence of accompanying itchy-watery eyes and about interference with daily activities because of nose problem.
2.1. Ethical consideration The study was approved by the Ethics Committee of Istanbul University, Istanbul School of Medicine.
2.2. Statistical analysis Statistical analysis included percentages, odds ratios (OR), 95% confidence interval (95% CI), chisquared test and backward logistic regression. Prevalence estimates were calculated by dividing positive responses to the given question by the total number of completed questionnaires. The 95% CI of these prevalence rates was also calculated. According to ISAAC policy, missing and inconsistent responses were included in the denominator for
Prevalence and risk factors for allergic rhinitis the prevalence calculations, but excluded from subsequent bivariate analysis [13—17]. The relation between risk factors and current AR prevalence was performed by univariate analysis using chisquared tests and univariate odds ratio (uOR) and its 95% CI. A p value less than 0.05 was considered significant. Risk factors significantly affecting current AR prevalence were family history of atopy, the presence of physician-diagnosed eczema or food allergy, frequent upper airway infections and sinusitis, history of adenoidectomy, antibiotic or paracetamol use in the first year of life, cat or dog ownership in the first year of life, home dampness, exposure to diesel trucks, perianal redness. These risk factors were tested in a backward logistic regression analysis with adjusted odds ratio (aOR) and its 95% CI. Consumption of foods were analysed by the same method, separately. The SPSS software package Version 12 was used for all statistical analyses.
3. Results Of the 2500 questionnaires distributed, 2387 questionnaires were appropriately completed by the parents with an overall response of 95.4%. There were 1185 (49.6%) boys and 1202 (50.4%) girls with a M/F ratio of 0.99. The prevalence for lifetime rhinitis, rhinitis in last 12 months, rhinoconjunctivitis in last 12 months and physician-diagnosed rhinitis were 44.3%, 28.9%, 7.8% and 7.9%, respectively (Table 1). No significant relation was observed between sex and prevalence of AR ( p = 0.34, uOR = 0.92, 95% CI = 0.77—1.10). A family history of atopy ( p < 0.001, uOR = 1.78, 95% CI = 1.44—2.19), physician-diagnosed food allergy ( p = 0.005, uOR = 1.51, 95% CI = 1.13— 2.03), physician-diagnosed eczema ( p = 0.016, uOR = 1.77, 95% CI = 1.11—2.83) were significant for increased risk for AR. Of the children with AR, 62 (34.6%) had family history of atopy, 87 (48.1%) had asthma, 19 (10.6%) had eczema, and 37 (20.8%) had food allergy. Table 1 Summary of parental-completed allergic rhinitis questionnaire data
465 Frequent upper airway infection and sinusitis were significant risk factors for AR ( p < 0.001, aOR = 1.36, 95% CI = 1.08—1.70 and aOR = 2.29, 95% CI = 1.64—3.19, respectively). Of children with AR, 62.1% had frequent upper respiratory infections and 21.7% had frequent sinusitis. History of tonsillectomy was not correlated with AR. Although history of adenoidectomy was significant by univariate analysis, it lost its significance when evaluated by multivariate analysis. Antibiotic and paracetamol use in the first year of life increased the risk for development of AR by univariate analysis ( p < 0.001); antibiotic use in the first year was a significant risk factor by multivariate analysis (aOR = 1.26, 95% CI = 1.01—1.57). AR prevalence was neither associated with exposure to tobacco smoke at home nor with maternal and paternal smoking. Cat or dog ownership during the first year of life significantly affected the development of AR ( p = 0.001, uOR = 2.02, 95% CI = 1.32— 3.09 and p = 0.044, uOR = 1.91, 95% CI = 1.00—3.62, respectively). Especially cat at home during the first year of life was an independent risk factor for AR (aOR = 2.21, 95% CI = 1.36—3.61). Dampness at home was significantly and independently associated with AR ( p = 0.001, uOR = 1.42, 95% CI = 1.16—1.74 and aOR = 1.31, 95% CI = 1.04—1.65). Although exposure to diesel truck was a significant risk factor for AR ( p = 0.002, uOR = 1.35, 95% CI = 1.12—1.62) by univariate analysis, it lost its significance when it was evaluated by multivariate analysis. Heating system, born in Istanbul or time lived in Istanbul did not affect the AR prevalence. Perianal redness was a significant independent risk factor for AR ( p < 0.001, uOR = 2.21, 95% CI = 1.77—2.75 and aOR = 1.83, 95% CI = 1.43— 2.36). Risk factors for AR were shown in Table 2. Among the protective foods rice, vegetables and fruits were relatively less consumpted; among the aggravating foods lollipops, candies were relatively more consumpted and among other foods meat and sun-flower oil were consumpted three or more times a week by children with allergic rhinitis (Table 3). When these risk factors were tested in a backward logistic regression analysis with adjusted odds, only fruit, vegetable and lollipop, candy consumption were independently and significantly affected AR prevalence (Table 4).
Questionnaire
Prevalence (%)
Lifetime rhinitis
44.3
4. Discussion
12-Month prevalence Rhinitis Associated itchy eye
28.9 7.8
The present study showed that nearly one third of 6—12-year-old Turkish children had rhinitis, defined as sneezing, runny or blocked nose in the absence of a cold or the flue.
Physician-diagnosed allergic rhinitis
7.9
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Table 2 Potential risk factors for allergic rhinitis Factors
Children with current allergic rhinitis symptoms n (%)
Sex M F
332 (28.0) 358 (29.8)
Family history for atopy Yes No
192 (39.2) 485 (26.6)
aOR (95% CI)
0.92 (0.77—1.10) 1.00 <0.001
80 (37.2) 584 (28.1)
Physician-diagnosed eczema Yes No
31 (41.3) 636 (28.5)
1.78 (1.44—2.19) 1.00 0.005
370 (36.3) 302 (23.6)
Frequent sinusitis Yes No
109 (53.2) 563 (26.9)
Tonsillectomy Yes No
45 (33.1) 637 (28.8)
Adenoidectomy Yes No
61 (36.3) 624 (28.7)
1.30 (1.00—1.68) 1.00 NS
1.51 (1.13—2.03) 1.00 0.016
Frequent respiratory tract infection Yes No
NS 1.77 (1.11—2.83) 1.00
<0.001 1.85 (1.54—2.22) 1.00
1.36 (1.08—1.70) 1.00
3.09 (2.31—4.13) 1.00
2.29 (1.64—3.19) 1.00
<0.001
0.26 1.23 (0.85—1.79) 1.00 0.037
NS 1.42 (1.02—1.96) 1.00
<0.001 430 (33.2) 241 (24.1)
Paracetamol given in the first 12 months of life Yes No
503 (31.4) 171 (23.9)
Smoking at home Yes No
407 (30.4) 272 (27.1)
Smoking of child’s mother Yes No
183 (30.4) 496 (28.6)
Smoking of child’s father Yes No
408 (30.1) 267 (27.5)
Cat at home in the first 12 months of life Yes No
uOR (95% CI)
0.34
Physician-diagnosed food allergy Yes No
Antibiotics given in the first year of life Yes No
p value
1.57 (1.30—1.89) 1.00
1.26 (1.01—1.57) 1.00 NS
<0.001 1.45 (1.18—1.78) 1.00 0.08 1.18 (0.98—1.41) 1.00 0.41 1.09 (0.89—1.33) 1.00 0.17 1.14 (0.95—1.37) 1.00 0.001 40 (44.4) 640 (28.4)
2.02 (1.32—3.09) 1.00
2.21 (1.36—3.61) 1.00
Prevalence and risk factors for allergic rhinitis
467
Table 2 (Continued )
Factors
Children with current allergic rhinitis symptoms n (%)
Dog at home in the first 12 months of life Yes No
17 (43.6) 668 (28.8)
Dampness at home Yes No
200 (34.8) 477 (27.3)
Heating system Stove (wood or coal) Central heating
335 (30.3) 321 (27.2)
Born in Istanbul Yes No
568 (29.2) 113 (28.0)
Time lived in Istanbul 5 years or more 0—5 years
628 (29.3) 55 (27.6)
p value
uOR (95% CI)
0.044
aOR (95% CI)
NS 1.91 (1.00—3.62) 1.00
0.001 1.42 (1.16—1.74) 1.00
1.31 (1.04—1.65) 1.00
0.11 1.16 (0.97—1.39) 1.00 0.63 1.06 (0.84—1.35) 1.00 0.62 1.09 (0.79—1.50) 1.00
Trucks passed on weekdays Frequently almost through the day Never or seldom
247 (33.3)
0.002 1.35 (1.12—1.62)
NS
435 (27.1)
1.00
Perianal redness Yes No
180 (43.5) 486 (25.9)
<0.001 2.21 (1.77—2.75) 1.00
1.83 (1.43—2.36) 1.00
uOR, univariate odds ratio; aOR, adjusted odds ratio; CI, confidence interval; NS, no significant association in multivariate analysis.
The reported prevalence rates for rhinitis ranged between 4.5% and 39.9% in different regions of Turkey in school-aged children [8—10,18—21]. Worldwide ISAAC Phase I study showed that the 12-month prevalence of allergic rhinoconjunctivitis varied between 0.8% and 39.7%. Our 12-month prevalence of allergic rhinoconjunctivitis was moderate among those values. The worldwide ISAAC Phase Three study, which was a repetition of the ISAAC Phase I study after a mean of 7 years, revealed a rising trend in allergic rhinoconjunctivitis prevalence with a range of 2.2— 45.1% in most centers [22]. Another study from Hong Kong examining the trend of allergic diseases prevalence in school children from 1995 to 2001 also showed increasing prevalence of allergic rhinitis and eczema [15]. This increasing trend of allergic diseases prevalence has been partly explained by ‘‘hygiene hypothesis’’, suggesting that declining microbial exposure in early childhood skewing the reciprocal balance between T helper 1 (Th1) and T helper 2 (Th2) towards Th2-mediated allergic disorders.
Allergic disorders are caused by a complex array of multiple gene interactions. Allergic disease develops in individuals with a genetic predisposition after they are exposed to environmental factors. Many of the genes for the cytokines and receptors that regulate allergic inflammation are clustered on certain genes [23]. Family history of atopy increases the risk of subsequent allergic diseases in children, and this has been shown in long-term prospective studies [5,24,25]. Our study also verified that family history of atopy to be a risk factor for allergic rhinitis. Frequent upper airway infections and sinusitis may be expected in respiratory allergies. Children with allergic rhinitis usually have congested nose, which causes mouth breathing leading frequent upper airway infections. Allergic children may have much tendency to upper airway tract diseases since their airways are more vulnerable due to allergic inflammation. Lee et al. [15] reported a significant correlation between AR and frequent upper respiratory infections in Chinese children. An epidemiological survey performed on Italian school children
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Z. Tamay et al.
Table 3 Univariate analysis of dietary habits of children with current allergic rhinitis symptoms
Protective foods Potatoes Rice Cereal Pasta Vegetables Fish and other sea foods Fruits Tomatoes Nuts Olive oil Fish oil Traditional foods made from grapes and mulberries Fermented drinks made from millets and various seeds Mix pickles
Never or occasionally n (%)
Once or twice per week n (%)
Three or more times a week n (%)
p value
68 114 77 97 141 409 78 99 245 257 424 308
209 247 85 273 173 171 124 136 234 147 25 172
382 299 474 289 341 43 463 424 153 179 32 132
0.093 0.028 0.103 0.851 0.021 * 0.135 0.009 * 0.122 0.708 0.439 0.233 0.406
(32.9) (35.0) (32.0) (30.4) (34.8) (30.4) (36.8) (33.2) (29.7) (30.0) (30.2) (29.2)
(26.3) (27.1) (33.6) (29.1) (28.3) (26.6) (31.6) (30.6) (29.1) (30.2) (22.5) (26.5)
(29.9) (28.9) (27.9) (28.8) (27.7) (25.6) (27.5) (27.8) (27.6) (27.3) (29.4) (29.7)
493 (29.7)
19 (31.1)
3 (15.0)
0.347
427 (29.9)
131 (29.3)
41 (30.4)
0.962
Aggravating foods Fast-food Potato cibs, crackers Chocolates Lollipops, candies Cookies, muffins Margarine
488 140 106 254 158 328
(28.7) (27.6) (27.9) (25.9) (29.5) (30.1)
95 183 191 167 197 138
(29.1) (27.2) (28.4) (30.1) (26.3) (28.9)
26 331 359 205 296 133
(28.0) (30.3) (29.9) (32.8) (30.1) (29.2)
0.973 0.305 0.915 0.009 * 0.202 0.885
Other foods Eggs Animal fats Milk, dairy products Meat Butter Sun-flower oil Corn oil Tea Olive
85 399 57 227 351 244 244 138 117
(32.8) (29.8) (32.8) (32.3) (29.3) (31.9) (28.4) (28.4) (27.5)
149 21 99 281 126 105 117 106 157
(26.5) (30) (32.1) (27.0) (28.6) (25.1) (31.0) (27.1) (32.0)
425 8 504 146 128 211 191 407 377
(29.2) (23.5) (28.1) (28.9) (29.6) (28.2) (29.2) (29.5) (28.3)
0.208 0.728 0.179 0.050 0.947 0.037 0.655 0.636 0.223
*
p < 0.05 is considered significant
emphasized the possible relationship between atopy and the upper respiratory infections [26]. Frequent antibiotic and paracetamol use early in life was examined in several studies and a possible link between antibiotic use and later asthma and rhinitis was shown in several studies [27—29]. The relation between antibiotic use and allergic diseases was explained by antibacterial-induced alterations in the intestinal flora and/or prevention of bacterial infections leading to a skewing of the immune system of young children toward an atopic phenotype [30,31]. An explanation for the association between paracetamol use and allergic disease was the ability of paracetamol to deplete antioxidant defences and promote Th2 response [32]. We found a positive relation between AR and frequent consumption of paracetamol and antibiotics, of which the latter one
was an independent risk factor. However, these associations may be explained by the reverse situation that frequent upper respiratory infections, often early symptom of asthma and allergic rhinitis, are usually treated with antibiotics and/or paracetamol [33,34]. Tonsils and adenoids are part of Waldeyer’s ring, involved in the defence against microorganisms. Surgical removal of these tissues may cause a reduction in stimulation of the Th1-type immune response and may lead to a rise in Th2-type-mediated atopic diseases according to ‘‘hygiene hypothesis’’. Although a positive relationship between adenoidectomy and tonsillectomy in childhood and the incidence of atopic disease in later childhood was shown in British National Child Developmental Study [35], no such association was found in our study,
Prevalence and risk factors for allergic rhinitis
469
Table 4 Multivariate analysis of dietary habits of children with current allergic rhinitis symptoms Children with current allergic rhinitis symptoms n (%)
Multivariant aOR (95% CI)
Fruits Never or rarely Once or twice/a week Three or more/a week
78 (36.8) 124 (31.6) 463 (27.5)
1.00 0.79 (0.53—1.53) 0.64 (0.45—0.91)
Vegetables Never or rarely Once or twice/a week Three or more/a week
141 (34.8) 173 (28.3) 341 (27.7)
Lollipops, candies Never or rarely Once or twice/a week Three or more/a week
254 (25.9) 167 (30.1) 205 (32.8)
NS
1.00 1.26 (0.99—1.59) 1.44 (1.15—1.81)
aOR, adjusted odds ratio; CI, confidence interval; NS, no significant association in multivariate analysis.
which was in agreement with Dutch longitudinal birth cohort study [36]. The presence of a cat home has been found to be a significant risk factor for AR in Turkish children, although the rate of pet ownership is extremely low in our population. The association between pet ownership in childhood and subsequent allergic diseases and sensitization is very controversial. Intriguing, but contradictory, reports have caused considerable uncertainty [37—39]. Keeping a cat in the home provides high-dose exposure to cat allergens and increases the risk of sensitization to cat in susceptible children. On the other hand, endotoxin may be abundant in house dust particularly in houses with cats and dogs, and protect against allergen sensitization by enhancing Th1 immunity. Contradictory results may be due to heterogeneity of the population, different immune response to antigens in susceptible individuals. Some investigators found a negative significant association between the prevalence of allergic rhinitis and exposure to tobacco and parental smoking [40,41]. This inverse relation was also explained by ‘‘hygiene hypothesis’’. Passive smoking might lead to high infection rates in infancy, resulting with the dominance of Th1-type immune response and less allergic diseases. On the contrary, a positive association between tobacco smoke and rhinitis was reported in a number of studies [6,40,42]. According to a meta-analysis data, no consistent association emerged between parental smoking and allergic rhinitis, which was compatible with our results [41]. Moisture at home may increase sensitization to mould in susceptible children by stimulating Th2immune response. Moisture-related problems in buildings were found to be a risk factor for asthma and allergic symptoms among preschool children
[43]. In our study, home dampness was significantly associated with symptoms of AR. Istanbul is the biggest city of Turkey, with more than 10 million inhabitants. Western lifestyle is predominant in this city and adaptation of immigrants to this lifestyle can quickly occur. In our study, born in or living in Istanbul was not significantly increased the risk for AR. Not classifying the patients according to urban and rural parts of the city might affect our results. Motor vehicle exhaust from freeways could have an inverse effect on respiratory health of children. van Vliet et al. reported that cough, wheeze, runny nose and asthma were more frequent in children living within 100 m from the freeway, where exposure to diesel truck too much [44]. Exposure to diesel truck may have irritant effect on airways facilitating penetrating allergens to airways. In our study, frequent exposure to diesel truck was more frequently reported by parents of children with symptoms of AR, but it was not an independent significant risk factor. Perianal redness has not been evaluated as a risk factor for allergic diseases before. Iacono et al. found that chronic constipation with perianal fissures or perianal erythema can be a manifestation of cow’s milk intolerance [45]. We think that perianal erythema can be a clue of mucosal inflammation due to food allergy in infants and young children according to our clinical observations. In our study, perianal redness was a significant risk factor for AR. Although there are other factors such as fungal infections, thread worms that cause perianal redness, it may be also a sign of mucosal inflammation due to concomitant subclinic food allergy in children with AR. Several studies have suggested that the increasing prevalence of symptoms of allergic diseases
470 could be associated with changes in the diet [46— 48]. Changes in the diet may mediate an effect, through changes in gut flora. Intestinal flora of allergic children differs from healthy children [49]; different intestinal flora may induce Th2-type immune response against antigens and preservation of intestinal mucosal integrity by ‘‘healthy’’ gut flora may be a protective factor against atopy and atopic diseases [50]. Besides this effect, nutrients like antioxidants, polyunsaturated fatty acids may be needed for healthy immune system development. In our study, a significant inverse relationship was found between symptoms of AR and the intake of fruits and vegetables. Our results were in agreement with the previous studies [47,48]. Frequent consumption of fruits and vegetables may be protective against allergic diseases due to their antioxidant effects [47,48]. We also found a dosedependent association between frequent consumption lollipops, candies and symptoms of AR. Although allergies to food additives are rarely seen in children, food additives existing in lollipops and candies may act as non-specific adjuvant factors in the development of allergic diseases. There are several strengths of this study. First, ISAAC questionnaire has been validated in a number of Turkish studies. Second, the data is large enough to reflect Istanbul population. Since potential risk factors are influenced by the same social and environmental conditions and can also interact with each other, they may affect the situation only when they exist together. This may be the reason of the difference between the results of the univariate and the multivariate analyses, which may be a limitation of the study. In conclusion our study reconfirmed that family history of atopy, frequent respiratory tract infections, antibiotics given in the first year of life, cat at home in the first year of life, dampness at home, perianal redness and dietary habits are important independent risk factors for AR. Researchers worldwide should be focused to these factors and try to develop policies for early intervention, primary and secondary preventions for allergic diseases.
Z. Tamay et al.
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471 [36] E.S. van Hattum, W.A. Balemans, M.M. Rovers, G.A. Zielhuis, A.G. Schilder, C.K. van der Ent, Adenoidectomy and/or tonsillectomy in childhood is not associated with atopic disease later in life, Clin. Exp. Allergy 36 (2006) 40—43. [37] F. Kurosaka, Y. Nakatani, T. Terada, A. Tanaka, H. Ikeuchi, A. Hayakawa, et al., Current cat ownership may be associated with the lower prevalence of atopic dermatitis, allergic rhinitis, and Japanese cedar pollinosis in schoolchildren in Himeji, Japan, Pediatr. Allergy Immunol. 17 (2006) 22—28. [38] A. Simpson, A. Custovic, Pets and the development of allergic sensitization, Curr. Allergy Asthma Rep. 5 (2005) 212—220. [39] C. Almqvist, High allergen exposure as a risk factor for asthma and allergic disease, Clin. Rev. Allergy Immunol. 28 (2005) 25—41. [40] E.A. Mitchell, A.W. Stewart, ISAAC Phase One Study Group. International Study of Asthma and Allergy in Childhood, The ecological relationship of tobacco smoking to the prevalence of symptoms of asthma and other atopic diseases in children: the International Study of Asthma and Allergies in Childhood (ISAAC), Eur. J. Epidemiol. 17 (2001) 667—673. [41] D.P. Strachan, D.G. Cook, Health effects of passive smoking. 5. Parental smoking and allergic sensitisation in children, Thorax 53 (1998) 117—123. [42] H.J. Wittig, E.T. Mclaughlin, K.L. Leifer, J.D. Belloit, Risk factors for the development of allergic disease: analysis of 2190 patient records, Ann. Allergy 41 (1978) 84—88. [43] C.G. Bornehag, J. Sundell, L. Hagerhed-Engman, T. Sigsggard, S. Janson, Aberg N, D.B.H. Study Group, ‘‘Dampness’’ at home and its association with airway, nose, and skin symptoms among 10,851 preschool children in Sweden: a cross-sectional study, Indoor Air 15 (2005) 48—55. [44] P. van Vliet, M. Knape, J. de Hartog, N. Janssen, H. Harssema, B. Brunekreef, Motor vehicle exhaust and chronic respiratory symptoms in children living near freeways, Environ. Res. 74 (1997) 122—132. [45] G. Iacono, F. Cavataio, G. Montalto, A. Florena, M. Tumminello, M. Soresi, et al., Intolerance of cow’s milk and chronic constipation in children, N. Engl. J. Med. 339 (1998) 1100— 1104. [46] A. Seaton, D.J. Codden, K. Brown, Increase in asthma: a more toxic environment or a more susceptible population? Thorax 49 (1994) 171—174. [47] P. Ellwood, M.I. Asher, B. Bjorksten, M. Burr, N. Pearce, C.F. Robertson, Diet and asthma, allergic rhinoconjunctivitis and atopic eczema symptom prevalence: an ecological analysis of the International Study of Asthma and Allergies in Childhood (ISAAC) data. ISAAC Phase One Study Group, Eur. Respir. J. 17 (2001) 436—443. [48] Y. Miyake, S. Sasaki, Y. Ohya, S. Miyamoto, I. Matsunaga, T. Yoshida, et al., Soy, isoflavones, and prevalence of allergic rhinitis in Japanese women: the Osaka Maternal and Child Health Study, J. Allergy Clin. Immunol. 115 (2005) 1176—1183. [49] B. Bjorksten, P. Naaber, E. Sepp, M. Mikelsaar, The intestinal microflora of Estonian and Swedish 2-year-old children, Clin. Exp. Allergy 29 (1999) 342—346. [50] S.F. Bloomfield, R. Stanwell-Smith, R.W.R. Crevel, J. Pickup, Too clean, or not too clean: the Hygiene Hypothesis and home hygiene, Clin. Exp. Allergy 36 (2006) 402—425.
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Prevalence and risk factors for allergic rhinitis in primary school children Zeynep Tamay a,*, Ahmet Akcay b, Ulker Ones a, Nermin Guler a, Gurkan Kilic a, Mehmet Zencir c a
Department of Pediatrics, Division of Allergy and Chest Diseases, Istanbul School of Medicine, Istanbul University, Istanbul, Turkey b Department of Pediatrics, Pamukkale School of Medicine, Pamukkale University, Pamukkale, Turkey c Department of Public Health, Pamukkale School of Medicine, Pamukkale University, Pamukkale, Turkey Received 13 June 2006; received in revised form 15 November 2006; accepted 17 November 2006
KEYWORDS Allergic rhinitis; ISAAC; Risk factors; Children
Summary Objective: Allergic rhinitis is a common chronic illness of childhood. The aim of the study was to evaluate the prevalence and risk factors of allergic rhinitis in 6—12-yearold schoolchildren in Istanbul. Methods: A total of 2500 children aged between 6 and 12 years in randomly selected six primary schools of Istanbul were surveyed by using the International Study of Asthma and Allergies in Childhood (ISAAC) questionnaire between April and May 2004. Results: Of them 2387 (1185 M/1202 F) questionnaires were appropriately completed by the parents with an overall response of 95.4%. The prevalence of physiciandiagnosed allergic rhinitis was 7.9% (n = 189). A family history of atopy (aOR = 1.30, 95% CI = 1.00—1.68), frequent respiratory tract infection (aOR = 1.36, 95% CI = 1.08—1.70) and sinusitis (aOR = 2.29, 95% CI = 1.64—3.19), antibiotic use in the first year of life (aOR = 1.26, 95% CI = 1.01—1.57), cat at home in the first year of life (aOR = 2.21, 95% CI = 1.36—3.61), dampness at home (aOR = 1.31, 95% CI = 1.04— 1.65) and perianal redness (aOR = 1.26, 95% CI = 1.01—1.57) were significant for increased risk for allergic rhinitis. Frequent consumption of fruits and vegetables were inversely, and frequent consumption of lollipops and candies were positively associated with allergic rhinitis symptoms. Conclusion: Our study reconfirmed that family history of atopy, frequent respiratory tract infections, antibiotics given in the first year of life, cat at home in the first year of life, dampness at home, perianal redness and dietary habits are important
* Corresponding author at: Department of Pediatrics, Istanbul Medical Faculty, Capa 34390, Istanbul, Turkey. Tel.: +90 212 4142000/32349; fax: +90 212 6319301. E-mail address: [email protected] (Z. Tamay). 0165-5876/$ — see front matter # 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2006.11.013
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Z. Tamay et al. independent risk factors for AR. Researchers worldwide should be focused to these factors and try to develop policies for early intervention, primary and secondary preventions for allergic diseases. # 2006 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Allergic rhinitis (AR) is a very common disease in childhood as well as in adults and impairs the quality of life if left untreated [1]. AR is characterized by nasal itching, sneezing, watery rhinorrhoea and nasal obstruction [1]. The prevalence of childhood AR shows wide variation throughout the world, ranging from 0.8% to 39.7% [2]. The prevalence of allergic diseases has increased predominantly in developed countries, which indicates that environmental risk factors and life style rather than genetic predisposition seem to be the major determinants of allergic diseases [2—4]. Various risk factors have been described for AR according to different stages during life. Family history of atopy, month of birth, parental smoking, male sex, early exposure to allergens or pollutions were considered to be potential risk factors by epidemiological surveys [1,4—6]. But major determinants contributing development of AR is still not clear. The aim of the study was to evaluate the prevalence and risk factors of allergic rhinitis in 6—12year-old schoolchildren in Istanbul.
2. Methods This survey was held in children aged between 6 and 12 years in randomly selected six primary schools in Istanbul. A total of 2500 questionnaires were distributed to the children to be completed by their parents at home. The return visit to the school was done within a 2-week period to try to collect data from children formerly absent. The standardized ISAAC Phase I written core questionnaire was translated into Turkish and used. There have been quite a few studies carried out in Turkey using the ISAAC questionnaire [7—10], therefore it is well known and validated in Turkish studies. An additional questionnaire was prepared to identify demographic features and potential risk factors, including: sex, family history of atopy, the presence of physiciandiagnosed eczema or food allergy, frequent upper airway infections and sinusitis, history of tonsillectomy or adenoidectomy, antibiotic or paracetamol use in the first year of life, exposure to tobacco smoke at home, maternal and paternal smoking, cat or dog ownership in the first year of life, home
dampness, heating system, born in and living period in Istanbul, exposure to diesel trucks, perianal redness and diet. Dietary intake was estimated by using additionally a semi-quantitative food frequency questionnaire. Consumption of protective foods including starch such as potatoes, rice, cereals, pasta, vegetables, fish, other sea foods, fruits, nuts, olive oil, fish oil, and some traditional foods made from grapes and mulberries, fermented drinks made from millets and various seeds; aggravating foods including fast-food, potato chips, crackers, chocolates, lollipops, candies, cookies, muffins, margarine; other foods including eggs, animal fats, milk and dairy products, meat, polyunsaturated fatty acids (butter), sun-flower oil, corn oil, tea, olive and were asked [11]. Analysis of diet variables were determined by frequency of consumption of foods in three groups including: ‘‘never or occasionally’’, ‘‘once or twice per week’’ and ‘‘three or more times a week’’. Having a problem with sneezing or a runny, or blocked nose in the absence of a cold or a flu in the past 12 months was assessed as ‘‘current allergic rhinitis’’ [2,12]. Positive response to the question about having had allergic rhinitis diagnosed by a physician was considered to be ‘‘ever doctor-diagnosed allergic rhinitis’’. Severity of allergic rhinitis was assessed among children with current rhinitis from the responses the questions on the presence of accompanying itchy-watery eyes and about interference with daily activities because of nose problem.
2.1. Ethical consideration The study was approved by the Ethics Committee of Istanbul University, Istanbul School of Medicine.
2.2. Statistical analysis Statistical analysis included percentages, odds ratios (OR), 95% confidence interval (95% CI), chisquared test and backward logistic regression. Prevalence estimates were calculated by dividing positive responses to the given question by the total number of completed questionnaires. The 95% CI of these prevalence rates was also calculated. According to ISAAC policy, missing and inconsistent responses were included in the denominator for
Prevalence and risk factors for allergic rhinitis the prevalence calculations, but excluded from subsequent bivariate analysis [13—17]. The relation between risk factors and current AR prevalence was performed by univariate analysis using chisquared tests and univariate odds ratio (uOR) and its 95% CI. A p value less than 0.05 was considered significant. Risk factors significantly affecting current AR prevalence were family history of atopy, the presence of physician-diagnosed eczema or food allergy, frequent upper airway infections and sinusitis, history of adenoidectomy, antibiotic or paracetamol use in the first year of life, cat or dog ownership in the first year of life, home dampness, exposure to diesel trucks, perianal redness. These risk factors were tested in a backward logistic regression analysis with adjusted odds ratio (aOR) and its 95% CI. Consumption of foods were analysed by the same method, separately. The SPSS software package Version 12 was used for all statistical analyses.
3. Results Of the 2500 questionnaires distributed, 2387 questionnaires were appropriately completed by the parents with an overall response of 95.4%. There were 1185 (49.6%) boys and 1202 (50.4%) girls with a M/F ratio of 0.99. The prevalence for lifetime rhinitis, rhinitis in last 12 months, rhinoconjunctivitis in last 12 months and physician-diagnosed rhinitis were 44.3%, 28.9%, 7.8% and 7.9%, respectively (Table 1). No significant relation was observed between sex and prevalence of AR ( p = 0.34, uOR = 0.92, 95% CI = 0.77—1.10). A family history of atopy ( p < 0.001, uOR = 1.78, 95% CI = 1.44—2.19), physician-diagnosed food allergy ( p = 0.005, uOR = 1.51, 95% CI = 1.13— 2.03), physician-diagnosed eczema ( p = 0.016, uOR = 1.77, 95% CI = 1.11—2.83) were significant for increased risk for AR. Of the children with AR, 62 (34.6%) had family history of atopy, 87 (48.1%) had asthma, 19 (10.6%) had eczema, and 37 (20.8%) had food allergy. Table 1 Summary of parental-completed allergic rhinitis questionnaire data
465 Frequent upper airway infection and sinusitis were significant risk factors for AR ( p < 0.001, aOR = 1.36, 95% CI = 1.08—1.70 and aOR = 2.29, 95% CI = 1.64—3.19, respectively). Of children with AR, 62.1% had frequent upper respiratory infections and 21.7% had frequent sinusitis. History of tonsillectomy was not correlated with AR. Although history of adenoidectomy was significant by univariate analysis, it lost its significance when evaluated by multivariate analysis. Antibiotic and paracetamol use in the first year of life increased the risk for development of AR by univariate analysis ( p < 0.001); antibiotic use in the first year was a significant risk factor by multivariate analysis (aOR = 1.26, 95% CI = 1.01—1.57). AR prevalence was neither associated with exposure to tobacco smoke at home nor with maternal and paternal smoking. Cat or dog ownership during the first year of life significantly affected the development of AR ( p = 0.001, uOR = 2.02, 95% CI = 1.32— 3.09 and p = 0.044, uOR = 1.91, 95% CI = 1.00—3.62, respectively). Especially cat at home during the first year of life was an independent risk factor for AR (aOR = 2.21, 95% CI = 1.36—3.61). Dampness at home was significantly and independently associated with AR ( p = 0.001, uOR = 1.42, 95% CI = 1.16—1.74 and aOR = 1.31, 95% CI = 1.04—1.65). Although exposure to diesel truck was a significant risk factor for AR ( p = 0.002, uOR = 1.35, 95% CI = 1.12—1.62) by univariate analysis, it lost its significance when it was evaluated by multivariate analysis. Heating system, born in Istanbul or time lived in Istanbul did not affect the AR prevalence. Perianal redness was a significant independent risk factor for AR ( p < 0.001, uOR = 2.21, 95% CI = 1.77—2.75 and aOR = 1.83, 95% CI = 1.43— 2.36). Risk factors for AR were shown in Table 2. Among the protective foods rice, vegetables and fruits were relatively less consumpted; among the aggravating foods lollipops, candies were relatively more consumpted and among other foods meat and sun-flower oil were consumpted three or more times a week by children with allergic rhinitis (Table 3). When these risk factors were tested in a backward logistic regression analysis with adjusted odds, only fruit, vegetable and lollipop, candy consumption were independently and significantly affected AR prevalence (Table 4).
Questionnaire
Prevalence (%)
Lifetime rhinitis
44.3
4. Discussion
12-Month prevalence Rhinitis Associated itchy eye
28.9 7.8
The present study showed that nearly one third of 6—12-year-old Turkish children had rhinitis, defined as sneezing, runny or blocked nose in the absence of a cold or the flue.
Physician-diagnosed allergic rhinitis
7.9
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Table 2 Potential risk factors for allergic rhinitis Factors
Children with current allergic rhinitis symptoms n (%)
Sex M F
332 (28.0) 358 (29.8)
Family history for atopy Yes No
192 (39.2) 485 (26.6)
aOR (95% CI)
0.92 (0.77—1.10) 1.00 <0.001
80 (37.2) 584 (28.1)
Physician-diagnosed eczema Yes No
31 (41.3) 636 (28.5)
1.78 (1.44—2.19) 1.00 0.005
370 (36.3) 302 (23.6)
Frequent sinusitis Yes No
109 (53.2) 563 (26.9)
Tonsillectomy Yes No
45 (33.1) 637 (28.8)
Adenoidectomy Yes No
61 (36.3) 624 (28.7)
1.30 (1.00—1.68) 1.00 NS
1.51 (1.13—2.03) 1.00 0.016
Frequent respiratory tract infection Yes No
NS 1.77 (1.11—2.83) 1.00
<0.001 1.85 (1.54—2.22) 1.00
1.36 (1.08—1.70) 1.00
3.09 (2.31—4.13) 1.00
2.29 (1.64—3.19) 1.00
<0.001
0.26 1.23 (0.85—1.79) 1.00 0.037
NS 1.42 (1.02—1.96) 1.00
<0.001 430 (33.2) 241 (24.1)
Paracetamol given in the first 12 months of life Yes No
503 (31.4) 171 (23.9)
Smoking at home Yes No
407 (30.4) 272 (27.1)
Smoking of child’s mother Yes No
183 (30.4) 496 (28.6)
Smoking of child’s father Yes No
408 (30.1) 267 (27.5)
Cat at home in the first 12 months of life Yes No
uOR (95% CI)
0.34
Physician-diagnosed food allergy Yes No
Antibiotics given in the first year of life Yes No
p value
1.57 (1.30—1.89) 1.00
1.26 (1.01—1.57) 1.00 NS
<0.001 1.45 (1.18—1.78) 1.00 0.08 1.18 (0.98—1.41) 1.00 0.41 1.09 (0.89—1.33) 1.00 0.17 1.14 (0.95—1.37) 1.00 0.001 40 (44.4) 640 (28.4)
2.02 (1.32—3.09) 1.00
2.21 (1.36—3.61) 1.00
Prevalence and risk factors for allergic rhinitis
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Table 2 (Continued )
Factors
Children with current allergic rhinitis symptoms n (%)
Dog at home in the first 12 months of life Yes No
17 (43.6) 668 (28.8)
Dampness at home Yes No
200 (34.8) 477 (27.3)
Heating system Stove (wood or coal) Central heating
335 (30.3) 321 (27.2)
Born in Istanbul Yes No
568 (29.2) 113 (28.0)
Time lived in Istanbul 5 years or more 0—5 years
628 (29.3) 55 (27.6)
p value
uOR (95% CI)
0.044
aOR (95% CI)
NS 1.91 (1.00—3.62) 1.00
0.001 1.42 (1.16—1.74) 1.00
1.31 (1.04—1.65) 1.00
0.11 1.16 (0.97—1.39) 1.00 0.63 1.06 (0.84—1.35) 1.00 0.62 1.09 (0.79—1.50) 1.00
Trucks passed on weekdays Frequently almost through the day Never or seldom
247 (33.3)
0.002 1.35 (1.12—1.62)
NS
435 (27.1)
1.00
Perianal redness Yes No
180 (43.5) 486 (25.9)
<0.001 2.21 (1.77—2.75) 1.00
1.83 (1.43—2.36) 1.00
uOR, univariate odds ratio; aOR, adjusted odds ratio; CI, confidence interval; NS, no significant association in multivariate analysis.
The reported prevalence rates for rhinitis ranged between 4.5% and 39.9% in different regions of Turkey in school-aged children [8—10,18—21]. Worldwide ISAAC Phase I study showed that the 12-month prevalence of allergic rhinoconjunctivitis varied between 0.8% and 39.7%. Our 12-month prevalence of allergic rhinoconjunctivitis was moderate among those values. The worldwide ISAAC Phase Three study, which was a repetition of the ISAAC Phase I study after a mean of 7 years, revealed a rising trend in allergic rhinoconjunctivitis prevalence with a range of 2.2— 45.1% in most centers [22]. Another study from Hong Kong examining the trend of allergic diseases prevalence in school children from 1995 to 2001 also showed increasing prevalence of allergic rhinitis and eczema [15]. This increasing trend of allergic diseases prevalence has been partly explained by ‘‘hygiene hypothesis’’, suggesting that declining microbial exposure in early childhood skewing the reciprocal balance between T helper 1 (Th1) and T helper 2 (Th2) towards Th2-mediated allergic disorders.
Allergic disorders are caused by a complex array of multiple gene interactions. Allergic disease develops in individuals with a genetic predisposition after they are exposed to environmental factors. Many of the genes for the cytokines and receptors that regulate allergic inflammation are clustered on certain genes [23]. Family history of atopy increases the risk of subsequent allergic diseases in children, and this has been shown in long-term prospective studies [5,24,25]. Our study also verified that family history of atopy to be a risk factor for allergic rhinitis. Frequent upper airway infections and sinusitis may be expected in respiratory allergies. Children with allergic rhinitis usually have congested nose, which causes mouth breathing leading frequent upper airway infections. Allergic children may have much tendency to upper airway tract diseases since their airways are more vulnerable due to allergic inflammation. Lee et al. [15] reported a significant correlation between AR and frequent upper respiratory infections in Chinese children. An epidemiological survey performed on Italian school children
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Table 3 Univariate analysis of dietary habits of children with current allergic rhinitis symptoms
Protective foods Potatoes Rice Cereal Pasta Vegetables Fish and other sea foods Fruits Tomatoes Nuts Olive oil Fish oil Traditional foods made from grapes and mulberries Fermented drinks made from millets and various seeds Mix pickles
Never or occasionally n (%)
Once or twice per week n (%)
Three or more times a week n (%)
p value
68 114 77 97 141 409 78 99 245 257 424 308
209 247 85 273 173 171 124 136 234 147 25 172
382 299 474 289 341 43 463 424 153 179 32 132
0.093 0.028 0.103 0.851 0.021 * 0.135 0.009 * 0.122 0.708 0.439 0.233 0.406
(32.9) (35.0) (32.0) (30.4) (34.8) (30.4) (36.8) (33.2) (29.7) (30.0) (30.2) (29.2)
(26.3) (27.1) (33.6) (29.1) (28.3) (26.6) (31.6) (30.6) (29.1) (30.2) (22.5) (26.5)
(29.9) (28.9) (27.9) (28.8) (27.7) (25.6) (27.5) (27.8) (27.6) (27.3) (29.4) (29.7)
493 (29.7)
19 (31.1)
3 (15.0)
0.347
427 (29.9)
131 (29.3)
41 (30.4)
0.962
Aggravating foods Fast-food Potato cibs, crackers Chocolates Lollipops, candies Cookies, muffins Margarine
488 140 106 254 158 328
(28.7) (27.6) (27.9) (25.9) (29.5) (30.1)
95 183 191 167 197 138
(29.1) (27.2) (28.4) (30.1) (26.3) (28.9)
26 331 359 205 296 133
(28.0) (30.3) (29.9) (32.8) (30.1) (29.2)
0.973 0.305 0.915 0.009 * 0.202 0.885
Other foods Eggs Animal fats Milk, dairy products Meat Butter Sun-flower oil Corn oil Tea Olive
85 399 57 227 351 244 244 138 117
(32.8) (29.8) (32.8) (32.3) (29.3) (31.9) (28.4) (28.4) (27.5)
149 21 99 281 126 105 117 106 157
(26.5) (30) (32.1) (27.0) (28.6) (25.1) (31.0) (27.1) (32.0)
425 8 504 146 128 211 191 407 377
(29.2) (23.5) (28.1) (28.9) (29.6) (28.2) (29.2) (29.5) (28.3)
0.208 0.728 0.179 0.050 0.947 0.037 0.655 0.636 0.223
*
p < 0.05 is considered significant
emphasized the possible relationship between atopy and the upper respiratory infections [26]. Frequent antibiotic and paracetamol use early in life was examined in several studies and a possible link between antibiotic use and later asthma and rhinitis was shown in several studies [27—29]. The relation between antibiotic use and allergic diseases was explained by antibacterial-induced alterations in the intestinal flora and/or prevention of bacterial infections leading to a skewing of the immune system of young children toward an atopic phenotype [30,31]. An explanation for the association between paracetamol use and allergic disease was the ability of paracetamol to deplete antioxidant defences and promote Th2 response [32]. We found a positive relation between AR and frequent consumption of paracetamol and antibiotics, of which the latter one
was an independent risk factor. However, these associations may be explained by the reverse situation that frequent upper respiratory infections, often early symptom of asthma and allergic rhinitis, are usually treated with antibiotics and/or paracetamol [33,34]. Tonsils and adenoids are part of Waldeyer’s ring, involved in the defence against microorganisms. Surgical removal of these tissues may cause a reduction in stimulation of the Th1-type immune response and may lead to a rise in Th2-type-mediated atopic diseases according to ‘‘hygiene hypothesis’’. Although a positive relationship between adenoidectomy and tonsillectomy in childhood and the incidence of atopic disease in later childhood was shown in British National Child Developmental Study [35], no such association was found in our study,
Prevalence and risk factors for allergic rhinitis
469
Table 4 Multivariate analysis of dietary habits of children with current allergic rhinitis symptoms Children with current allergic rhinitis symptoms n (%)
Multivariant aOR (95% CI)
Fruits Never or rarely Once or twice/a week Three or more/a week
78 (36.8) 124 (31.6) 463 (27.5)
1.00 0.79 (0.53—1.53) 0.64 (0.45—0.91)
Vegetables Never or rarely Once or twice/a week Three or more/a week
141 (34.8) 173 (28.3) 341 (27.7)
Lollipops, candies Never or rarely Once or twice/a week Three or more/a week
254 (25.9) 167 (30.1) 205 (32.8)
NS
1.00 1.26 (0.99—1.59) 1.44 (1.15—1.81)
aOR, adjusted odds ratio; CI, confidence interval; NS, no significant association in multivariate analysis.
which was in agreement with Dutch longitudinal birth cohort study [36]. The presence of a cat home has been found to be a significant risk factor for AR in Turkish children, although the rate of pet ownership is extremely low in our population. The association between pet ownership in childhood and subsequent allergic diseases and sensitization is very controversial. Intriguing, but contradictory, reports have caused considerable uncertainty [37—39]. Keeping a cat in the home provides high-dose exposure to cat allergens and increases the risk of sensitization to cat in susceptible children. On the other hand, endotoxin may be abundant in house dust particularly in houses with cats and dogs, and protect against allergen sensitization by enhancing Th1 immunity. Contradictory results may be due to heterogeneity of the population, different immune response to antigens in susceptible individuals. Some investigators found a negative significant association between the prevalence of allergic rhinitis and exposure to tobacco and parental smoking [40,41]. This inverse relation was also explained by ‘‘hygiene hypothesis’’. Passive smoking might lead to high infection rates in infancy, resulting with the dominance of Th1-type immune response and less allergic diseases. On the contrary, a positive association between tobacco smoke and rhinitis was reported in a number of studies [6,40,42]. According to a meta-analysis data, no consistent association emerged between parental smoking and allergic rhinitis, which was compatible with our results [41]. Moisture at home may increase sensitization to mould in susceptible children by stimulating Th2immune response. Moisture-related problems in buildings were found to be a risk factor for asthma and allergic symptoms among preschool children
[43]. In our study, home dampness was significantly associated with symptoms of AR. Istanbul is the biggest city of Turkey, with more than 10 million inhabitants. Western lifestyle is predominant in this city and adaptation of immigrants to this lifestyle can quickly occur. In our study, born in or living in Istanbul was not significantly increased the risk for AR. Not classifying the patients according to urban and rural parts of the city might affect our results. Motor vehicle exhaust from freeways could have an inverse effect on respiratory health of children. van Vliet et al. reported that cough, wheeze, runny nose and asthma were more frequent in children living within 100 m from the freeway, where exposure to diesel truck too much [44]. Exposure to diesel truck may have irritant effect on airways facilitating penetrating allergens to airways. In our study, frequent exposure to diesel truck was more frequently reported by parents of children with symptoms of AR, but it was not an independent significant risk factor. Perianal redness has not been evaluated as a risk factor for allergic diseases before. Iacono et al. found that chronic constipation with perianal fissures or perianal erythema can be a manifestation of cow’s milk intolerance [45]. We think that perianal erythema can be a clue of mucosal inflammation due to food allergy in infants and young children according to our clinical observations. In our study, perianal redness was a significant risk factor for AR. Although there are other factors such as fungal infections, thread worms that cause perianal redness, it may be also a sign of mucosal inflammation due to concomitant subclinic food allergy in children with AR. Several studies have suggested that the increasing prevalence of symptoms of allergic diseases
470 could be associated with changes in the diet [46— 48]. Changes in the diet may mediate an effect, through changes in gut flora. Intestinal flora of allergic children differs from healthy children [49]; different intestinal flora may induce Th2-type immune response against antigens and preservation of intestinal mucosal integrity by ‘‘healthy’’ gut flora may be a protective factor against atopy and atopic diseases [50]. Besides this effect, nutrients like antioxidants, polyunsaturated fatty acids may be needed for healthy immune system development. In our study, a significant inverse relationship was found between symptoms of AR and the intake of fruits and vegetables. Our results were in agreement with the previous studies [47,48]. Frequent consumption of fruits and vegetables may be protective against allergic diseases due to their antioxidant effects [47,48]. We also found a dosedependent association between frequent consumption lollipops, candies and symptoms of AR. Although allergies to food additives are rarely seen in children, food additives existing in lollipops and candies may act as non-specific adjuvant factors in the development of allergic diseases. There are several strengths of this study. First, ISAAC questionnaire has been validated in a number of Turkish studies. Second, the data is large enough to reflect Istanbul population. Since potential risk factors are influenced by the same social and environmental conditions and can also interact with each other, they may affect the situation only when they exist together. This may be the reason of the difference between the results of the univariate and the multivariate analyses, which may be a limitation of the study. In conclusion our study reconfirmed that family history of atopy, frequent respiratory tract infections, antibiotics given in the first year of life, cat at home in the first year of life, dampness at home, perianal redness and dietary habits are important independent risk factors for AR. Researchers worldwide should be focused to these factors and try to develop policies for early intervention, primary and secondary preventions for allergic diseases.
Z. Tamay et al.
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