Abstract
BACKGROUND:
Eczema, allergic rhinitis and asthma are common chronic allergic disorders in childhood.
AIM:
The aim of this study was to determine the prevalence of common allergic disorders among Iranian guidance schools students in Mazandaran Province, northern Iran.
METHODS:
This analytical cross-sectional study was performed on 3000 children aged 11-14 years old during 2012-13 according to ISAAC study. Of 3000 recruited children 1576 (52.54%) were female and 1424 (47.46%) were male. Data gathered by ISAAC first phase questionnaire analysed by SPSS software 20.
RESULTS:
The prevalence of wheezing, allergic rhinitis symptoms (sneezing and pruritus) and atopic dermatitis symptoms (pruritus skin lesion) were 30.5%, 30% and 15% respectively. History of pets contact and smoking was positive 6.6% and 36 % respectively. About 52% was born with caesarian section. There was wheezing in 32.5% during sport. The diagnosis of asthma, allergic rhinitis and eczema were 12.2%, 28.5% and 15% respectively. Eczema, asthma and allergic rhinitis were significantly more common in boys students (p < 0.05).
CONCLUSIONS:
The results of this study showed that asthma, allergic rhinitis and eczema have a high prevalence and they are more common in boys.
Keywords: Asthma, Allergic Rhinitis, Eczema, middle school, Students
Introduction
Asthma, allergic rhinitis (AR) and eczema or atopic dermatitis (AD) are the most common chronic diseases in childhood [1]. Allergic disorders are encountered with variable prevalence in different parts of the world. The prevalence of childhood asthma and other atopic disorders has been increased in recent decades [2]. In Previous epidemiological studies, the prevalence of asthma among elementary and guidance schools students in this region was reported 12-17% [3, 4] but in a meta-analysis, the prevalence of asthma in Iranian children was 7.6% and 10.7% in elementary and guidance school students respectively [1]. Another study estimated that asthma affects 2.7 to 35.4% of children (in average 13.4%) in Iran [5]. More than 300 million people in the world currently have asthma [5].
Clinical manifestations of AR include rhinorrhea, pruritus; sneezing and congestion and the disease is more common among children. The pooled prevalence of AR in children 6-7 years of age was 11.9% and in children aged 13-14 was 21.2 % [6].
AD is the most common chronic dermatologic disease in children associated with pruritus and marked by remissions and exacerbations. In a meta-analysis study, the prevalence of eczema in children aged 6-7 years and 13-14 years was 5.98% and 6.52%, respectively [7].
Allergic disorders pose the heavy social-economic burden on family and society. Asthma is the most common disease that observed in emergency rooms, hospital admission and abstinence of school. It has a high economic burden on patients, their family, society and healthcare resources in different countries [5].
Although the exact etiologies of allergic diseases are unknown, both genetic and environmental factors have been included [8]. In children with asthma, environmental factors especially viral infection (24-34%), indoor and outdoor includes; air pollutants, cold, tobacco smoking, moulds and pets are main trigger factors [9].
The aim of this study was to determine the prevalence of common allergic disorders including asthma, allergic rhinitis and eczema and also to evaluate a few environmental factors such as BMI, smoking and delivery among students of guidance school in the region of northern Iran.
Material and Methods
We conducted an analytic cross-sectional prospective study which has been carried out on urban guidance students (11-14 years old) in the north of Iran from September 2012 to march 2013. The children who could not complete the questionnaire were excluded. Each school was considered as a cluster, and 20 guidance schools were selected randomly. Standard ISAAC core questions for wheezing, rhinitis, and eczema was used [10]. From 3250 students, 3050 questionnaires were obtained. The questionnaire return rate was 93.84%. Finally, 3000 questionnaires (1576 for girls and 1424 for boys) were collected and analysed. Students from guidance school answered the questionnaire associated with their parents. Written informed consent was obtained from participants and schools managers. Our study approved by local ethics committee of Mazandaran University of Medical sciences.
The boys and girls were matched for body mass index (BMI) [11]. Also, data were collected about kitchen design (open and closed), any passive smoking at the home or non-passive smoking; delivery based on normal delivery (NVD) and cesarian section(c/s) and animal contact based on indoor or outdoor contact and without animal contact from our participants. The family numbers, room numbers including bedroom and living room and housing characteristics were considered.
Data were analysed with SPSS 20 and statistical analysis tests such as Chi-Square test and odds ratio was calculated. We used logistic regression to find the effect of explanatory variables on asthma. P- Value less than 0.05 was statistically significant.
Results
The weight of the participants was between 25-92 kg (Mean 48.42 kg) and the height of the children was 120-182 (mean155.99) cm. The BMI, family and room numbers were 9.26-43.79 (mean 19.88), 2-9 (mean 4) and 1-4 (mean 2) person respectively. Table 1 showed analysis of kitchen, smoking exposure, kind of delivery and animal contact.
Table 1.
Prevalence of allergic rhinitis, eczema and asthma in students of guidance schools
| Disease | Total sample | Number of patients | Prevalence (%) | 95% Confidence Interval | |
|---|---|---|---|---|---|
| Lower | Upper | ||||
| Allergic Rhinitis | 2979 | 847 | 28.32 | 26.82 | 30.09 |
| Eczema | 2962 | 359 | 12.12 | 10.96 | 13.35 |
| Asthma | 2969 | 362 | 12.2 | 11.04 | 13.42 |
Children who have passive smoking are 1.8 times more likely to develop asthma (PV <0.001) (OR=2.88 with CI= 2.13-3.88). Room number leads to an increase of asthma in about 44 % (PV < 0.001) (OR = 0.694, CI = 0.570-0.844).
Out of total asthma patients (362; 12.2%), 222 (15.9%) were boys and 140 (8.9%) were girls. The prevalence of asthma was more common in boys than girls (PV=0.0001) in our study. Table 2 has shown asthma symptoms based on ISAAC questionnaire.
Table 2.
Prevalence of allergic rhinitis, eczema and asthma in students of guidance schools by gender
| Disease | Gender | Total sample | Number of patients | Prevalence (%) | p-value |
|---|---|---|---|---|---|
| Allergic Rhinitis | Boys | 1003 | 406 | 40.47 | <0.001 |
| Girls | 1976 | 441 | 22.31 | ||
| Eczema | Boys | 982 | 168 | 17.10 | <0.001 |
| Girls | 1980 | 191 | 9.64 | ||
| Asthma | Boys | 984 | 144 | 14.63 | 0.006 |
| Girls | 1985 | 218 | 10.98 |
We use logistic regression to find the effect of explanatory variables on asthma. Overweight and obesity were more common in non-asthmatic patients’ 47% and 15% respectively verse 39% and 9% in asthmatic patients respectively (PV = 0.002).
Association between a family number and asthma was not significant using logistic regression. (P-Value=0.45). The relationship between asthma and BMI in all students has shown in Table 3.
Table 3.
Evaluation of environment factors in asthma prevalence using multivariate logistic regression
| environment factors | B(regression coefficients) | S.E.* | P-Value. | Odds Ratio | 95% Confidence Interval | |
|---|---|---|---|---|---|---|
| Lower | Upper | |||||
| Open kitchen (Yes/NO) | -0.111 | 0.151 | NS** | 0.895 | 0.666 | 1.202 |
| Family. Number (NO) | 0.142 | 0.087 | NS | 1.153 | 0.973 | 1.366 |
| Room. Number (NO) | -0.494 | 0.111 | 0.000 | 0.610 | 0.491 | 0.759 |
| Animal Contact(Yes/NO) | 0.051 | 0.387 | NS | 1.052 | 0.493 | 2.245 |
| Secondary Smoker (Yes/NO) | 0.609 | 0.130 | 0.000 | 1.839 | 1.425 | 2.373 |
| Born (Cesarean/Normal) | -0.12 | 0.143 | NS | 0.88 | 0.67 | 1.17 |
Standard Error of Mean;
Not Significant.
Allergic rhinitis
Sneezing and rhinorrhea were seen in 29.8% of our allergic rhinitis patients in 12 last months but ever sneezing and rhinorrhea was seen in 22.4%. Nasal pruritus and eye involvement such as redness, Lacrimation was observed in 35.6% (Table 4).
Table 4.
Asthma symptoms according ISSAC questionnaire in guidance school students
| Asthma symptoms | Boys (%) | Girls (%) | Total (%) | P-value |
|---|---|---|---|---|
| Ever Wheeze | ||||
| Yes | 596 (20) | 153 (5) | 749 (25) | < 0.001 |
| No | 803 (27) | 1420 (48) | 1503 (75) | |
| Total | 1399 (47) | 1573 (53) | 2972 (100) | |
| Current Wheeze | ||||
| Yes | 812 (27) | 102 (4) | 914 (31) | < 0.001 |
| No | 586 (20) | 146 (49) | 2053 (69) | |
| Total | 1398 (47) | 1570 (53) | 2968 (100) | |
| Sleepdisturbance relatedWheeze | ||||
| Yes | 847 (29) | 70 (3) | 917 (32) | < 0.001 |
| No | 548 (18) | 1490 (50) | 2038 (68) | |
| Total | 1395 (47) | 1560 (53) | 2955 (100) | |
| Speech Disorder | ||||
| Yes | 286 (10) | 151 (5) | 437 (15) | < 0.001 |
| No | 1113 (37) | 1415 (48) | 2528 (85) | |
| Total | 1399 (47) | 1566 (53) | 2965 (100) | |
| Ever asthma | ||||
| Yes | 222 (8) | 140 (5) | 362 (13) | < 0.001 |
| No | 1176 (39) | 1431 (48) | 2607 (87) | |
| Total | 1398 (47) | 1571 (53) | 2969 (100) | |
| Exerciserelated Wheeze | ||||
| Yes | 837 (29) | 139 (5) | 976 (34) | < 0.001 |
| No | 558 (18) | 1425 (48) | 1983 (66) | |
| Total | 1395 (47) | 1564 (53) | 2959 (100) | |
| Dry cough at night | ||||
| Yes | 542 (18) | 308 (11) | 850 (29) | < 0.001 |
| No | 855 (29) | 1254 (42) | 2109 (71) | |
| Total | 1397 (47) | 1562 (53) | 2959 (100) |
The prevalence of allergic rhinitis was more common in boys (n = 736, 51.7%: vs.; n = 174, 11%), PV = 0.0001. Association between using an open kitchen and allergic rhinitis was significant and persons who had open Kitchen had odds ratio 1.868 times more than others to have allergic rhinitis (P < 0.001).
Association between smoking and allergic rhinitis was significant and secondary smoker had odds ratio 3.11 times more than others to have allergic rhinitis (P <0.001). There was no significant relationship between others explanatory variables and allergic rhinitis.
Eczema
There was no relationship between BMI and prevalence of eczema (PV = 0.052). Association between smoking and eczema was significant and secondary smoker had 2.96 times more odds than others to have eczema using logistic regression (P < 0.001). There were no significant association between others explanatory variables and Eczema.
Discussion
Asthma
Asthma is the most common chronic disease in the pediatric population [12]. The prevalence of asthma has doubled over the past several decades [13]. In the present study, the prevalence of asthma was more common among boys than girls (2:1 ratio) similar other studies [1, 3, 4]. Also, in the present study, the prevalence of asthma was higher than the other studies such as Thailand [13]. The prevalence of asthma was more variations between countries than within countries (15). The higher prevalence of asthma was reported in United Kingdom, New Zealand, and Australia but the lowest asthma prevalence reported from several eastern European countries, China, and some other countries in Southeast Asia. Generally, asthma was more common in affluent countries than in more developing countries [16].
Although the prevalence of asthma in some studies was different between urban and rural areas [17, 18, 19] but the results of our study in the same region in the north of Iran and the results reported by others were similar between the two areas [4, 20]. The prevalence of asthma in guidance school was 29.9% in rural area in this region [20]. Therefore there is no significant difference between rural and urban in asthma prevalence in our region that was similar the study by Gunner et al [21]. Urban and rural areas in our region are not substantially different climate. Environmental factors such as allergens, viral infections, pollutants, lifestyle, socioeconomic status, geographical area, diet, have been similar between two areas in this region.
Our study showed that the prevalence of wheezing in a 12 months period was 30.5%, so about one-fourth of our children had probability asthma. Our study showed that ever and current wheezing prevalence decreased with increasing age. Asthma diagnosis was 12.2 percent in our study. It has moderate prevalent in Iran and Middle East. In another study by Ghaffari et al., 12% of elementary school students had asthma with predominantly in boys [22]. Based on the previous studies in this region, the prevalence of asthma is more common in guidance school children than in elementary school students.
The prevalence of asthma is an average of 9 and 13 percent in Iran [1]). The average prevalence rate of asthma in the Middle East is 10.7% (11% in Oman and Palestine and around 17% in Kuwait) [1]. The prevalence of asthma in the north of Iran is more common than other regions of Iran and also it is more common or the same as some other countries such as United Kingdom (14.9%) and Malaysia (13 %) and less than other countries such as Austria (32%), United States of America (24.4%), and Singapore (27.4%) [1]. There is evidence that overweight and obesity are associated with children asthma [23]. It has been suggested that obesity results more severe, increased exacerbation, and poorer control asthma. Obesity rates have increased significantly in children in the world. A study showed that the risk of obese children having asthma was two times higher than for children with normal body weight. But our study showed that overweight and obesity were lower in asthmatic or in patients with wheezing (p = 0.002) [23]. Also, Alvarez Zallo et al study showed no relationship between obesity and asthma in the guidance school children group [24]. There is more conflict in a relation between overweight and obesity with asthma in children. More studies are needed in children and adolescents to confirm the relation between overweight and obesity with asthma and better understand how body fat distribution impacts the obesity-asthma relationship.
Sleep disturbance related wheeze, speech disorder, exercise related wheeze and dry cough at night were more common in boys than girls (p < 0.001). The asthma prevalence was more common in boys than girls in our study (significantly, PV = 0.0001). Susceptibility to developing asthma among passive smoking guidance school children were 2.8 times more common than the non-passive smokers children (CI, 95% = 2.13-3.88) (PV = 0.001). Therefore, exposure to passive smoking is a significant risk factor for developing asthma. Of course, reversely, also for a room asthma leads to an increase of about 44% (P < 0.001). (OR = 0.694, CI = 0.570-0.844). In our study, kind of kitchen, type of delivery and contact with pets could not find any association with children asthma.
Allergic rhinitis
The prevalence of allergic rhinitis was 30% in our study. Based on a meta-analysis study in Iran, the prevalence of allergic rhinitis in children of aged 13-14 was 21.2%. Therefore AR is more common in the north of Iran with high humidity and warm weather. In another study in this region, the prevalence of allergic rhinitis in guidance school was 18.1% and 21.7% in rural and urban areas in this region respectively [6, 20]. Prevalence of AR is not more common in urban than the rural area.
In this study, the prevalence of rhinitis symptoms in the both age groups was higher than children in Croatia, city of Zagreb and is lowers than in children in Thailand [20]. Wide variations in the prevalence of rhinitis were observed across centres with a higher prevalence in Austria, Madrid, Cartagena and Bilbao, lower prevalences were reported from Barcelona, Castellon and Pamplona [20]. Our results showed that 12-month and lifetime prevalence rates of allergic nasal symptoms and hay fever, particularly in the older age group was even higher. One study in the global ISAAC Phase reported more than fourfold worldwide variation in the prevalence of allergic nasal symptoms in both age groups [17]. However, we believe that 12- month prevalence of nasal symptoms (not the combination of nasal symptoms) in a great majority of children living in our region is sensitised to house dust mite. It may be expected that many of them have perennial allergic rhinitis without associated significant conjunctival symptoms [18]. The incidence of allergic rhinitis has been increasing for the last few decades in the world [20]. AR is a major risk factor for developing asthma. Our study showed the similar results. AR and asthma have had significant effects on quality of life and other numerous complications.
We found no significant relationship between BMI and guidance school children with or without AR in our study (Table 4), P = 0.281). In another study, there was evidence that overweight and obesity was not associated with children AR [23]. Our research showed that prevalence of AR was more common (significantly, P = 0.0001) in boys than girls. We found that kind of kitchen, type of delivery and contact with pets could not find any association with children AR.
Eczema
Atopic dermatitis (AD) is an increasingly chronic dermatologic disease. Fifteen percent of our cases have had eczema. The pooled prevalence of eczema in children in guidance school age was 6.52% (range 4.1 to 24.3%) in Iran [7].
The prevalence of eczema in our study is much higher than the average in our country. A previous study in this region showed that the prevalence of eczema was 5.5% among rural guidance school children [20]. But in another study in urban guidance school children the prevalence of eczema was 8.2% in this region [6]. Our results related to the eczema symptoms in both age groups are higher than previously reported study in former socialist Europe and lower than that in Scandinavia and the United Kingdom [20].
Similar to our study, Hogewoning et al.’s in Ghana, Gabon and Rwanda and also Guner et al in Turkey reported that the prevalence of eczema had no significant difference in urban and rural areas [21, 25]. Our study showed no significant relation between BMI and guidance school students with or without eczema. There is evidence that overweight and obesity are associated with children eczema [23]. In addition, our study revealed that the eczema prevalence was more common in guidance school`s boys than girls (P = 0.0001). We found that kind of kitchen, type of delivery and contact with pets had any association with children eczema.
In conclusion, it can be concluded that the prevalence of asthma, allergic rhinitis, and eczema symptoms (except a dry cough at night) in boys were higher than in girls. This study also shows that asthma, allergic rhinitis, and eczema in guidance schools children from the capital of Mazandaran province northern Iran are more common than an average of our country. A major possible limitation of the study is parental reporting on disorder symptoms (asthma, AR and eczema) could be influenced in data analysis.
Authors` contributions
SB participated in the conception of the study and acquisition of the data. ST contributed to acquisition of the data and distribution of questionnaires. DZ contributed to conception, design, acquisition of the data, and distribution of questionnaires. JY contributed to analysis, interpretation of data and drafting, and JGH contributed in conception, design, drafting and final approval.
Footnotes
Funding: This study was supported financially by Research vice chancellor of Mazandaran University of Medical Sciences.
Competing Interests: The authors have declared that no competing interests exist.
References
- 1.Ghaffari J, Aarabi M. The prevalence of paediatric asthma in the Islamic Republic of Iran: A systematic review and meta-analysis. J Pediatr Rev. 2013;1(1):2–11. [Google Scholar]
- 2.Gessner BD, Neeno T. Trends in asthma prevalence, hospitalization risk, and inhaled corticosteroid use among Alaska native and nonnative Medicaid recipients younger than 20 years. Annals of Allergy, Asthma & Immunology. 2005;94(3):372–9. doi: 10.1016/S1081-1206(10)60990-8. http://dx.doi.org/10.1016/S1081-1206(10)60990-8 . [DOI] [PubMed] [Google Scholar]
- 3.Ghaffari J, Mohammadzadeh I, Khalilian AR, Rafatpanah H, Mohammadjafari H, Davoudi A. Prevalence of asthma, allergic rhinitis and eczema in elementary schools in Sari (Iran) Caspian J Intern Med. 2012;3(1):372–376. PMid: 26557289. PMCid: PMC4600135. [PMC free article] [PubMed] [Google Scholar]
- 4.Mohammadzadeh I, Ghafari J, Barari Savadkoohi R, Tamaddoni A, Esmaeili Dooki MR, Alizadeh Navaei R. The Prevalence of Asthma, Allergic Rhinitis and Eczema in North of Iran: the International Study of Asthma and Allergies in Childhood (ISAAC) Iran J Pediatr. 2008;18(2):117–122. [Google Scholar]
- 5.Ghaffari J, Hadian A, Daneshpoor SM, Khademloo M. Asthma Burden in the Hospitalized Patients in North of Iran. International Journal of Pediatrics. 2014;2(4.1):257–66. [Google Scholar]
- 6.Mohammadzadeh I, Barari-Savadkoohi R, Alizadeh-Navaei R. The prevalence of allergic rhinitis in Iranian children: A systematic review and descriptive meta-analysis. J Pediatr Rev. 2013;1(2):19–24. [Google Scholar]
- 7.Ghaffari J, Navaeifar MR, Alizadeh-Navaei R. The prevalence of Eczema in Iranian children: A systematic review and meta-analysis. J Pediatr Rev. 2014;2(1):2–9. [Google Scholar]
- 8.Vervloet D, Williams AE, Lloyd A, Clark TJH. Costs of managing asthma as defined by a derived Asthma Control TestTM score in seven European countries. Eur Respir Rev. 2006;15(98):17–23. http://dx.doi.org/10.1183/09059180.06.00009803 . [Google Scholar]
- 9.FaridHossaini R, Ghaffari J, Ranjbar AR, Haghshenas MR, Rafatpanah H. Infections in Children with Asthma. J Pediatr Rev. 2013;1(1):34–45. [Google Scholar]
- 10.Wang XS, Tan TN, Shek LPC, et al. The prevalence of asthma and allergies in Singapore;data from two ISAAC surveys seven years apart. Arch Dis Child. 2004;89(5):423–6. doi: 10.1136/adc.2003.031112. http://dx.doi.org/10.1136/adc.2003.031112 . PMid: 15102631. PMCid: PMC1719913. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Kudzyte J, Griska E, Bojarskas J. Time trends in the prevalence of asthma and allergy among 6–7-year-old children: results from ISAAC phase I and III studies in Kaunas, Lithuania. Medicina (Kaunas) 2008;44(12):944–52. [PubMed] [Google Scholar]
- 12.Gessner BD, Neeno T. Trends in asthma prevalence, hospitalization risk, and inhaled corticosteroid use among Alaska native and nonnative Medicaid recipients younger than 20 years. Annals of Allergy, Asthma & Immunology. 2005;94(3):372–9. doi: 10.1016/S1081-1206(10)60990-8. http://dx.doi.org/10.1016/S1081-1206(10)60990-8 . [DOI] [PubMed] [Google Scholar]
- 13.Teeratakulpisarn J, Wiangnon S, Kosalaraksa P, Heng S. Surveying the prevalence of asthma, allergic rhinitis and eczema in school-children in Khon Kaen, Northeastern Thailand using the ISAAC questionnaire: phase III. Asian Pac J Allergy Immunol. 2004;22(4):175–81. PMid: 15783129. [PubMed] [Google Scholar]
- 14.Suh M, Kim HH, Sohn MH, et al. Prevalence of allergic diseases among Korean school-age children: a nationwide cross-sectional questionnaire study. J Korean Med Sci. 2011;26(3):332–8. doi: 10.3346/jkms.2011.26.3.332. http://dx.doi.org/10.3346/jkms.2011.26.3.332 . PMid: 21394299. PMCid: PMC3051078. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Ma Y, Zhao J, Han ZR, et al. Very low prevalence of asthma and allergies in school children from rural Beijing, China. Pediatr Pulmonol. 2009;44(8):793–9. doi: 10.1002/ppul.21061. http://dx.doi.org/10.1002/ppul.21061 . PMid: 19603531. [DOI] [PubMed] [Google Scholar]
- 16.Mohammadzadeh I, Jafarian A, Ghaffari J, Alizadeh-navaei R. The Prevalence of Allergy symptoms in Students in Rural Area. Caspian J Pediatr. 2014;1(2):35–38. [Google Scholar]
- 17.Guner SN, Gokturk B, Kilic M, Ozkiraz S. The prevalences of allergic diseases in rural and urban areas are similar. Allergol Immunopathol (Madr) 2011;39(3):140–4. doi: 10.1016/j.aller.2010.05.004. PMid: 21208714. http://dx.doi.org/10.1016/j.aller.2010.05.004 . [DOI] [PubMed] [Google Scholar]
- 18.Ghaffari J, Mohammadzadeh I, Khalilian A, Rafatpanah H, Mohammadjafari H, Davoudi A. Prevalence of asthma, allergic rhinitis and eczema in elementary schools in Sari (Iran) Caspian journal of internal medicine. 2012;3(1):372. PMid: 26557289. PMCid: PMC4600135. [PMC free article] [PubMed] [Google Scholar]
- 19.Kumar GS, Roy G, Subitha L, Sahu SK. Prevalence of bronchial asthma and its associated factors among school children in urban Puducherry, India. J Nat Sci Biol Med. 2014;5(1):59–62. doi: 10.4103/0976-9668.127289. http://dx.doi.org/10.4103/0976-9668.127289 . PMid: 24678199. PMCid: PMC3961954. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Asher MI, Anderson HR, Stewart AW, Crane J. Worldwide variations in the prevalence of asthma symptoms: the International Study of Asthma and Allergies in Childhood (ISAAC) Eur Respir J. 1998;12(2):315–35. doi: 10.1183/09031936.98.12020315. http://dx.doi.org/10.1183/09031936.98.12020315 . PMid: 9727780. [DOI] [PubMed] [Google Scholar]
- 21.Beasley R, Ellwood P, Asher I. International patterns of the prevalence of pediatric asthma the ISAAC program. Pediatr Clin North Am. 2003;50(3):539–53. doi: 10.1016/s0031-3955(03)00050-6. http://dx.doi.org/10.1016/S0031-3955(03)00050-6 . [DOI] [PubMed] [Google Scholar]
- 22.Suglia SF, Chambers EC, Rosario A, et al. Asthma and obesity in three-year-old urban children: role of sex and home environment. J Pediatr. 2011;159:14–20.e1. doi: 10.1016/j.jpeds.2011.01.049. http://dx.doi.org/10.1016/j.jpeds.2011.01.049 . PMid: 21392787. PMCid: PMC3115396. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Weinmayr G, Forastiere F, Büchele G, Jaensch A, Strachan DP, Nagel G ISAAC Phase Two Study Group. Overweight/Obesity and Respiratory and Allergic Disease in Children: International Study of Asthma and Allergies in Childhood (ISAAC) Phase Two. PLoS One. 2014;9(12):e113996. doi: 10.1371/journal.pone.0113996. http://dx.doi.org/10.1371/journal.pone.0113996 . PMid: 25474308. PMCid: PMC4256390. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Álvarez Zallo N, Guillen Grima F, Aguinaga-Ontoso I, Hermoso-de-Mendoza-Cantón J, Marín Fernández B, Serrano-Monzó I, Azcona San Julián C. [Study of prevalence and association between asthma symptoms and obesity in the pediatric population of pamplona] Nutr Hosp. 2014;30(3):519–25. doi: 10.3305/nh.2014.30.3.7434. PMid: 25238826. [DOI] [PubMed] [Google Scholar]
- 25.Hogewoning AA, Bouwes Bavinck JN, Amoah AS, et al. Point and period prevalences of eczema in rural and urban schoolchildren in Ghana, Gabon and Rwanda. J Eur Acad Dermatol Venereol. 2012;26(4):488–94. doi: 10.1111/j.1468-3083.2011.04106.x. http://dx.doi.org/10.1111/j.1468-3083.2011.04106.x . PMid: 21575064. [DOI] [PubMed] [Google Scholar]