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Prevalence of asthma, rhinitis and eczema symptoms in rural and urban school-aged children from Oropeza Province - Bolivia: a cross-sectional study
© Solis Soto et al.; licensee BioMed Central Ltd. 2014
Received: 9 March 2013
Accepted: 5 March 2014
Published: 10 March 2014
Asthma and allergies are world-wide common chronic diseases among children and young people. Little information is available about the prevalence of these diseases in rural areas of Latin America. This study assesses the prevalence of symptoms of asthma and allergies among children in urban and rural areas at Oropeza Province in Bolivia.
The Spanish version of the ISAAC standardized questionnaire and the ISAAC video questionnaire were implemented to 2584 children attending the fifth elementary grade in 36 schools in Oropeza province (response 91%). Lifetime, 12 months and severity prevalence were determined for asthma, rhinitis and eczema symptoms. Odds ratios (OR) with 95% confidence intervals (95% CI) were calculated adjusting for age using generalized linear mixed-effects models.
Median age of children was 11 years, 74.8% attended public schools, and 52.1% were female. While children attending urban schools had lower prevalence of self-reported wheeze in the written questionnaire (adjusted OR 0.6; 95% CI 0.4-1.9), they were more likely than children attending rural schools to report wheeze in the video questionnaire (aOR 2.1; 95% CI 1.0-2.6). They also reported more frequently severe rhinoconjunctivitis (aOR 2.8; 95% CI 1.2-6.6) and severe eczema symptoms (aOR 3.3; 95% CI 1.0-11.0).
Overall in accordance with the hygiene hypothesis, children living in urban areas of Bolivia seem to have a higher prevalence of symptoms of asthma and allergies compared to children living in the country side. In order to develop primary prevention strategies, environmental factors need to be identified in future studies.
Asthma and allergies are world-wide common chronic diseases with high prevalences among children and young people and large variation between and within countries and cities . These pathologies are associated with adverse outcomes at physical, emotional, social, and professional level for both, patients and their families, interfering with normal activity and quality of life .
Among others, the International Study of Asthma and Allergies in Childhood (ISAAC) has shown a higher prevalence of symptoms of asthma and allergies in industrialized countries than in developing countries [3–5], becoming a new public health challenge for the region .
ISAAC Phase I reported that the prevalence of asthma symptoms in children from South America was as high as that reported from industrialized countries. Overall, the prevalence of recent wheeze, exercise-induced bronchospasm, and severe episodes of wheezing were 16.9%, 19.3%, and 4.6%, respectively, for children aged 13–14 years with marked differences in the prevalence of asthma symptoms between different countries . In ISAAC Phase III, after a period of 5–10 years, similar or even lower prevalences of asthma symptoms were reported in centers with high prevalence in ISAAC Phase I. This suggests that the prevalence of asthma has reached a plateau in high prevalence centers while it is still on the rise in low and intermediate prevalence centers. The same scenario was reported for rhinoconjunctivitis and eczema symptoms .
Changes in lifestyle, modernization, living conditions and dietary habits have been studied as possible explanations for such an increase . One aspect frequently shown for industrialized countries is a higher prevalence of symptoms of asthma and allergies in urban compared to rural areas. This association was confirmed for African and Asian countries [10, 11] but so far only few studies from Latin America exist [12, 13]. A higher exposure to microbial compounds in rural areas was discussed as one of the mechanisms underlying the lower prevalence of asthma and allergies in rural areas. However, a high prevalence of asthma was shown in inner city environments with high microbial load [14, 15]. Some authors have speculated that these contradictory findings might be related to different asthma phenotypes and have hypothesized that rural living protects from allergy but not from asthma [16–18]. However, recent studies do not confirm this hypothesis [19, 20].
Bolivia is the poorest country in the Latin American region with 31% of the population living in extreme poverty . Living conditions differ largely between urban and rural areas . Within the ISAAC study, the prevalence of asthma and allergies in Bolivia has only been assessed for Santa Cruz, Bolivia’s richest city . The study has shown a high prevalence of rhinoconjunctivitis [4, 6] and eczema symptoms  as compared to other Latin American countries but a moderate prevalence of asthma . So far, data on the prevalence of asthma and allergies neither exist from lower income urban areas nor from rural areas of Bolivia.
This study aimed to assess the prevalence of symptoms of asthma and allergies in urban and rural areas at Oropeza Province in Chuquisaca. In this region, the majority of people live in poverty (62%), and 66% of the population identify themselves with some ethnic group (Aymara, Quechua, Guaraní, among others) . By assessing the burden of disease this study will contribute to assess the necessity to allocate recourses to the treatment, primary and secondary prevention of asthma and allergies in a country where health resources are scarce.
A population-based prevalence study was conducted in the Oropeza Province, located in the north western part of Chuquisaca, from July 2011 to December 2011.
The estimated population of Oropeza province is around 336.218 inhabitants with 19.7% living in the rural area. Communities with less than 2000 inhabitants were considered rural .
Oropeza’s population lives at altitudes between 2000 and 4000 meters above sea level. Its climate is warm and dry, with temperatures between 15.0°C and 20.0°C, relative humidity mean annual value around 60%. Rainfall occurs predominantly in summer (average annual rainfall of 500 to 1000 cubic millimeters) .
Study population and field work
This study used a simple one-stage cluster sampling. The primary sampling units were schools selected randomly. From a total 185 school registered in the Regional Education Service (SEDUCA- Chuquisaca) (138 (75%) in urban areas and 47 (25%) in rural areas), 43 schools were selected randomly (36 (84%) in urban, 7 (16%) in rural areas). Of these, 6 urban (17%) and 1 rural school (14%) did not accept to participate due to time constraints or because of parental concern.
The secondary sampling units were all students in fifth grade. From the 36 participating schools (30 (83%) of these located in urban areas), 2584 children attending the fifth grade were invited to participate. In each sampled school, the whole fifth grade student population was studied. Schools with less than 20 pupils of this grade were excluded from the sampling frame for feasibility reasons.
The sample size was determined following ISAAC project recommendations . With 2016 participants is possible to detect differences in the prevalence of severe asthma considering 5% of significance level and 90% of statistical power.
The schools were contacted to agree upon the date of the visit, and to organize the written and video questionnaire ensuring a place to implement both questionnaires properly.
After the written questionnaire, the ISAAC video questionnaire (AVQ 3.0) was implemented according the ISAAC standard recommendations . The main researcher (MTSS) and three previously trained health professionals submitted the questionnaires.
Study instruments and variable definition
Written and video questionnaires
The Spanish version of the ISAAC standardized questionnaire (asthma, rhinitis and eczema modules) was used . This questionnaire attempts to identify children with symptoms of asthma, rhinoconjunctivitis and eczema. The written questionnaire assesses lifetime (ever) and 12 months prevalence (current symptoms) of asthma, rhinitis and eczema symptoms. In addition, severity of symptoms is assessed. In addition, the video questionnaire identifies 12 months prevalence of asthma symptoms.
The following definitions based on the ISAAC protocol were used:
Asthma symptoms: were defined as self-reported symptoms of wheezing or whistling in the chest.
Severe asthma symptoms: was considered present if children with current asthma symptoms reported: 4 or more attacks of wheeze, being woken by wheeze at one or more nights per week or wheezing severe enough to limit speech to only one or two words at a time between two breaths.
Considering the video questionnaire, wheezing, exercise-induced wheeze and dyspnea at rest occurrence were considered by affirmative response to the respective video sequences.
Rhinitis symptoms were defined as self-reported problems of sneezing, runny or blocked nose, without having a cold or influenza.
Rhino conjunctivitis symptoms were considered present if participants reported rhinitis symptoms accompanied by itchy watery eyes.
Itchy Rash was considered if the participant reported an itchy rash which was coming and going for at least six months.
Current symptoms of eczema were defined as presence of an itchy rash in the last 12 months that affected any of the following places: the folds of the elbows, behind the knees, in front of the ankles, under the buttocks, or around the neck, ears or eyes.
Double-entry of data and congruence checking was performed using the statistical analysis software EpiInfo V. 3.5.3 for Windows to avoid possible mistakes. Data was exported to SPSS v.17 for descriptive analysis and to R v. 3.0.1  software for statistical models.
Intraclass correlation coefficient (ICC) was computed  to analyze the relationship of cases within a cluster (schools) for each of the outcomes. ICC is around 4% for outcomes reported by written questionnaire and around 20% for outcomes reported by Video questionnaire. Considering that, all analyzes were adjusted by cluster sampling.
Absolute and relative frequencies were calculated. The Rao-Scott adjusted chi-square test  was computed to assess differences in prevalence of symptoms between rural and urban areas. In addition crude and adjusted odds ratios as well as their corresponding 95% confidence intervals were calculated using generalized linear mixed-effects models . The adjusted models included variables which were statistically significant (p value ≤ 0.05) in the bivariate analysis.
The study was approved by the National Research Ethics Committee from San Andres University at La Paz–Bolivia; also a permission to apply the questionnaire was obtained from the Regional Education Service (SEDUCA- Chuquisaca). International ethical research guidelines were considered at all research steps. A written informed consent form as well as a letter explaining the importance of the study was sent to parents or legal guardians of the children one week before the visit to the school. Voluntary participation from children was respected.
Descriptive data by for place of living (N = 2340)
(N = 1727)
(N = 613)
≤ 10 years
≥ 12 years
Type of school
Private and public with private Infrastructure
Prevalence, unadjusted and adjusted odds ratios comparing self-reported asthma, rhinitis and eczema in school aged children from rural and urban areas
Written questionnaire (N = 2340)
Wheeze (12 months prevalence)
Severe asthmaa (12 months prevalence)
Video questionnaire (N = 2300)
Wheezing (12 months prevalence)
Exercise-induced wheeze (12 months prevalence)
Dyspnoea at rest (12 months prevalence)
RHINITIS SYMPTOMS (N = 2327)
Rhinitis (12 months prevalence)
Rhinoconjunctivitisd (12 months prevalence)
Severe Rhinoconjunctivitise (12 months prevalence)
ECZEMA SYMPTOMS (N = 2303)
Itchy rash (ever)
Itchy rash (12 months prevalence)
Eczemaf (12 months prevalence)
Severe Eczemag (12 months prevalence)
The prevalence of rhinitis symptoms was high with a 12-months prevalence of rhinoconjunctivitis symptoms of 22% in children from urban and 24% in children from rural schools. Only for severe rhinoconjunctivitis symptoms the 12-months prevalence differed between urban and rural schools (aOR 2.8; 95% CI 1.2-6.6; Table 2).
The 12-months prevalence of current itchy rash was higher in urban than in rural schools (12% vs. 9%; Table 2). The 12-months prevalence of severe eczema was very low (1.6% in children from urban schools, 0.5% in children from rural schools). Only the 12-months severe eczema symptoms was statistically significantly higher in children from urban compared with children from rural schools (aOR 3.3; 95% CI 1.0-11.0).
Our study for the first time assessed the prevalence of symptoms of asthma and allergies in rural and urban areas of Bolivia. The prevalence found in this study was within the range reported for South America [4, 6, 24]. Difference between rural and urban areas indicated higher prevalences for urban areas compatible with the hygiene hypothesis, although the difference was smaller in comparison with previous studies .
This is the first study in Bolivia comparing the prevalence of symptoms of asthma and allergies in a representative sample of children in this region using standardized methods. The study showed an optimal response rate (91%), which is similar to the one reported from other studies following the ISAAC protocol in Latin America .
However, 7 out of the selected 43 schools did not agree to participate (16%). Most of these schools were from urban areas. The main reason for non-participation was the frequent implementation of different governmental programs which interrupt the education schedule. It is not assumed that this might have resulted in selection bias.
Although cluster effect was not expected to be large in ISAAC studies , methods for correlated data were computed as recommended when cluster sampling is implemented . In our study, even if we found an ICC of 20% in some cases, huge variations between logistic regression models (considering independent data) and generalized linear mixed-effects models (considering the correlation between schools) were not founded.
In contrast to the original ISAAC protocol, we included children in the 5th grade (age range 9–15 years). The reason for that was that in the following school grades the drop-out rate in Bolivian schools is substantial most likely affecting the representativeness of the results . We considered that these children are able to understand and adequately respond the questionnaire. The alternative to select 1st grade pupils and use the International Study of Asthma and Allergies in Childhood parental questionnaire was omitted due the overall low literacy level among adults in this region.
Another limitation of our study is related to the cross-sectional design, with the exposure and outcome being measured simultaneously, thus it is not possible to determine the temporality of the association or the causality. Although this design is prone to induce recall bias, we assume that blinding the participants to the hypothesis under investigation minimized this concern.
In accordance with previous studies, we have found a low agreement between written and video questionnaire for asthma with much higher prevalences in the written than in the video questionnaire . Given the extremely high prevalence in the written asthma questionnaire as compared to the video questionnaire and to other studies in Latin America  one might assume that the results reported by video questionnaire could be more reliable than those from written questionnaire.
The video questionnaire has been described as being sensitive to language, culture, or literacy differences [37, 38]. Even given that the video questionnaire has been validated only in children 13 to 14 year olds, it is unlikely that its validity decreases so much with age (median age of our population: 11 years). Even if this would be the case it is expected to result in non-differential bias which might lower the risk estimates towards the null.
Overall, the prevalence of current asthma symptoms (6.4%) were lower than the Latin American average (10.3%), especially those reported from the neighboring countries (17.1% in Peru, 12.1% in Chile, 10.4% in Paraguay and 8.1% in Argentina) .
Although the questionnaire has been proven to be valid for eczema and rhinitis symptoms [39, 40] it is possible that the results were also affected by interpretation problems related to cultural and educational background differences especially in rural areas. However, the prevalence of rhinitis and eczema symptoms was comparable to previous Latin American studies .
Several studies explored the possible relation between ethnicity, poverty, environmental pollution, level of industrialization, health conditions, helminthiasis or genetic factors and the prevalence of asthma and allergies symptoms. The real impact of such factors remains unclear since large differences have been described specially in Latin America , but there is common agreement about the importance of environmental factors for the development of asthma and allergic symptoms . Based on the video questionnaire we found a lower prevalence of asthma and allergy symptoms in rural areas where extreme poverty is above 70%, with more than 40% of the population engaged in agricultural activities, more than 90% of the population identifying themselves with native Quechua ethnicity  and high percentage of acute respiratory infections and diarrhea in children under 5 years .
Overall in accordance with the hygiene hypothesis, children living in urban areas of Bolivia seem to have a higher prevalence of asthma and atopic symptoms compared to children living in the country side. More research is needed assessing the role of environmental factors in the development of asthma and allergies trying to explain the differences in rural and urban areas. It will help to design future primary prevention strategies in order to avoid the rapid increase of these diseases in this region.
The authors would like to thank Javier Mallol and Julian Crane for providing the Spanish validated questionnaires and a copy of the video questionnaire (AVQ 3.0) respectively and a special gratitude for all the study participants for their cooperation.
- Mallol J, Crane J, Von Mutius E, Odhiambo J, Keil U, Stewart A: The International Study of Asthma and Allergies in Childhood (ISAAC) phase three: a global synthesis. Allergol Immunopathol (Madr). 2013, 41 (2): 73-85. 10.1016/j.aller.2012.03.001.View ArticleGoogle Scholar
- Lobo F, Lobo B: Quality of life in asthmatic outpatients. J Asthma. 2008, 45: 27-32. 10.1080/02770900701815495.View ArticleGoogle Scholar
- Lai CK, Beasley R, Crane J, Foliaki S, Shah J, Weiland S: Global variation in the prevalence and severity of asthma symptoms: phase three of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax. 2009, 64 (6): 476-483. 10.1136/thx.2008.106609.View ArticlePubMedGoogle Scholar
- Ait-Khaled N, Pearce N, Anderson HR, Ellwood P, Montefort S, Shah J: Global map of the prevalence of symptoms of rhinoconjunctivitis in children: The International Study of Asthma and Allergies in Childhood (ISAAC) Phase Three. Allergy. 2009, 64 (1): 123-148. 10.1111/j.1398-9995.2008.01884.x.View ArticlePubMedGoogle Scholar
- Odhiambo JA, Williams HC, Clayton TO, Robertson CF, Asher MI: Global variations in prevalence of eczema symptoms in children from ISAAC Phase Three. J Allergy Clin Immunol. 2009, 124 (6): 1251-1258. e1223. 10.1016/j.jaci.2009.10.009.View ArticlePubMedGoogle Scholar
- Chong Neto HJ, Rosario NA, Sole D: Asthma and Rhinitis in South America: How Different They are From Other Parts of the World. Allergy Asthma Immunol Res. 2012, 4 (2): 62-67. 10.4168/aair.2012.4.2.62.View ArticlePubMedGoogle Scholar
- Mallol J, Sole D, Asher I, Clayton T, Stein R, Soto-Quiroz M: Prevalence of asthma symptoms in Latin America: the International Study of Asthma and Allergies in Childhood (ISAAC). Pediatric pulmonology. 2000, 30 (6): 439-444. 10.1002/1099-0496(200012)30:6<439::AID-PPUL1>3.0.CO;2-E.View ArticlePubMedGoogle Scholar
- Pearce N, Aït-Khaled N, Beasley R, Mallol J, Keil U, Mitchell E, Robertson C: Worldwide trends in the prevalence of asthma symptoms: phase III of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax. 2007, 62 (9): 758-10.1136/thx.2006.070169.View ArticlePubMedPubMed CentralGoogle Scholar
- Wehrmeister FC, Menezes AM, Cascaes AM, Martinez-Mesa J, Barros AJ: Time trend of asthma in children and adolescents in Brazil, 1998–2008. Revista de saude publica. 2012, 46 (2): 242-250. 10.1590/S0034-89102012005000008.View ArticlePubMedGoogle Scholar
- Morcos MM, Morcos WM, Ibrahim MA, Shaheen MA: Environmental exposure to endotoxin in rural and urban Egyptian school children and its relation to asthma and atopy. Minerva pediatrica. 2011, 63 (1): 19-26.PubMedGoogle Scholar
- Lee SY, Kwon JW, Seo JH, Song YH, Kim BJ, Yu J, Park KS, Kim H, Kim EJ, Lee JS, Hong SJ: Prevalence of atopy and allergic diseases in Korean children: associations with a farming environment and rural lifestyle. Int Arch Allergy Immunol. 2012, 158 (2): 168-174. 10.1159/000330820.View ArticlePubMedGoogle Scholar
- Rodriguez A, Vaca M, Oviedo G, Erazo S, Chico ME, Teles C, Barreto ML, Rodrigues LC, Cooper PJ: Urbanisation is associated with prevalence of childhood asthma in diverse, small rural communities in Ecuador. Thorax. 2011, 66 (12): 1043-1050. 10.1136/thoraxjnl-2011-200225.View ArticlePubMedPubMed CentralGoogle Scholar
- Robinson CL, Baumann LM, Gilman RH, Romero K, Combe JM, Cabrera L, Hansel NN, Barnes K, Gonzalvez G, Wise RA, Breysse PN, Checkley W: The Peru Urban versus Rural Asthma (PURA) Study: methods and baseline quality control data from a cross-sectional investigation into the prevalence, severity, genetics, immunology and environmental factors affecting asthma in adolescence in Peru. BMJ open. 2012, 2 (1): e000421-View ArticlePubMedPubMed CentralGoogle Scholar
- Akinbami LJ, Moorman JE, Bailey C, Zahran HS, King M, Johnson CA, Liu X: Trends in asthma prevalence, health care use, and mortality in the United States, 2001–2010. NCHS data brief. 2012, 94: 1-8.PubMedGoogle Scholar
- Robinson CL, Baumann LM, Romero K, Combe JM, Gomez A, Gilman RH, Cabrera L, Gonzalvez G, Hansel NN, Wise RA, Barnes KC, Breysse PN, Checkley W: Effect of urbanisation on asthma, allergy and airways inflammation in a developing country setting. Thorax. 2011, 66 (12): 1051-1057. 10.1136/thx.2011.158956.View ArticlePubMedGoogle Scholar
- Cooper PJ, Rodrigues LC, Barreto ML: Influence of poverty and infection on asthma in Latin America. Curr Opin Allergy Clin Immunol. 2012, 12 (2): 171-178. 10.1097/ACI.0b013e3283510967.View ArticlePubMedGoogle Scholar
- Weinmayr G, Weiland SK, Bjorksten B, Brunekreef B, Buchele G, Cookson WO, Garcia-Marcos L, Gotua M, Gratziou C, Van Hage M, Von Mutius E, Riikjarv MA, Rzehak P, Stein RT, Strachan DP, Tsanakas J, Wickens K, Wong GW: Atopic sensitization and the international variation of asthma symptom prevalence in children. Am J Respir Crit Care Med. 2007, 176 (6): 565-574. 10.1164/rccm.200607-994OC.View ArticlePubMedGoogle Scholar
- Moncayo AL, Vaca M, Oviedo G, Erazo S, Quinzo I, Fiaccone RL, Chico ME, Barreto ML, Cooper PJ: Risk factors for atopic and non-atopic asthma in a rural area of Ecuador. Thorax. 2010, 65 (5): 409-416. 10.1136/thx.2009.126490.View ArticlePubMedPubMed CentralGoogle Scholar
- Fuchs O, Genuneit J, Latzin P, Buchele G, Horak E, Loss G, Sozanska B, Weber J, Boznanski A, Heederik D, Braun-Fahrlander C, Frey U, Von Mutius E: Farming environments and childhood atopy, wheeze, lung function, and exhaled nitric oxide. J Allergy Clin Immunol. 2012, 130 (2): 382-388 e386. 10.1016/j.jaci.2012.04.049.View ArticlePubMedGoogle Scholar
- Boneberger A, Haider D, Baer J, Kausel L, Von Kries R, Kabesch M, Radon K, Calvo M: Environmental risk factors in the first year of life and childhood asthma in the Central South of Chile. J Asthma. 2011, 48 (5): 464-469. 10.3109/02770903.2011.576740.View ArticlePubMedGoogle Scholar
- Economic Comission for Latin America and the Caribbean (ECLAC). Statistical Yearbook for Latin America and the Caribbean. 2011, Santiago, Chile: United NationsGoogle Scholar
- National Report on Human Development in Bolivia: Lifestyles, inequality and urban social mobility strategies. The changes behind the change, inequality and social mobility in Bolivia. Edited by: United Nations Development Programme (PNUD). 2010, Bolivia: National Report on Human Development in BoliviaGoogle Scholar
- United Nations Development Programme: Santa Cruz: current status, evaluation and perspectives. Millennium Development Goals (In Spanish). 2007, La Paz, Bolivia: United Nations Development ProgrammeGoogle Scholar
- Solé D, Mallol J, Wandalsen G, Aguirre V, Latin American ISAAC Phase 3 Study Group: Prevalence of symptoms of eczema in Latin America: results of the International Study of Asthma and Allergies in Childhood (ISAAC) Phase 3. J Investig Allergol Clin Immunol. 2010, 20 (4): 311-323.PubMedGoogle Scholar
- United Nations Development Programme, Social and Economic Policies Analysis unit. Human Development in Chuquisaca (In Spanish). 2010Google Scholar
- National Statistical Institute: Population and Housing Census (In Spanish). 2001Google Scholar
- Bolivia: relative humidity by Seasons 1999–2008 (In Spanish). http://www.ine.gob.bo,
- Ellwood P, Asher M, Beasley R, Clayton T, Stewart A: The International Study of Asthma and Allergies in Childhood (ISAAC): phase three rationale and methods research methods. Int J Tubercul Lung Dis. 2005, 9 (1): 10-16.Google Scholar
- Gibson PG, Henry R, Shah S, Toneguzzi R, Francis JL, Norzila MZ, Davies H: Validation of the ISAAC video questionnaire (AVQ3.0) in adolescents from a mixed ethnic background. Clin Exp Allergy. 2000, 30 (8): 1181-1187. 10.1046/j.1365-2222.2000.00882.x.View ArticlePubMedGoogle Scholar
- Mata Fernandez C, Fernandez-Benitez M, Perez Miranda M, Guillen Grima F: Validation of the Spanish version of the Phase III ISAAC questionnaire on asthma. J Investig Allergol Clin Immunol. 2005, 15 (3): 201-210.PubMedGoogle Scholar
- R Core Team: R: A language and environment for statistical computing. R Foundation for Statistical Computing. 2013, Vienna, Austria: R Core Team: R, url: http://www.R-project.org ISBN 3-900051-07-0 ,Google Scholar
- Zeger SL, Liang KY, Albert PS: Models for longitudinal data: a generalized estimating equation approach. Biometrics. 1988, 44 (4): 1049-1060. 10.2307/2531734.View ArticlePubMedGoogle Scholar
- Thomas DR, Decady YJ: Testing for association using multiple response survey data: approximate procedures based on the Rao-Scott approach. Int J Test. 2004, 4 (1): 43-59. 10.1207/s15327574ijt0401_3.View ArticleGoogle Scholar
- Bates D, Maechler M, Bolker MB, Suggests mlmRev M: Package ‘lme4’. 2013Google Scholar
- Zyzanski SJ, Flocke SA, Dickinson LM: On the nature and analysis of clustered data. Ann Fam Med. 2004, 2 (3): 199-200. 10.1370/afm.197.View ArticlePubMedPubMed CentralGoogle Scholar
- Ministry of Education: Education in Bolivia: indicators, numbers and results (in Spanish). Bolivia. 2004Google Scholar
- Crane J, Mallol J, Beasley R, Stewart A, Asher MI: Agreement between written and video questions for comparing asthma symptoms in ISAAC. Eur Respir J. 2003, 21 (3): 455-461. 10.1183/09031936.03.00041403.View ArticlePubMedGoogle Scholar
- Rahimi Rad MH, Hejazi ME: Agreement between written and video asthma symptoms questionnaires in school children in Urmia, Iran. Iran J Allergy Asthma Immunol. 2007, 6 (1): 21-25.PubMedGoogle Scholar
- Flohr C, Weinmayr G, Addo Yobo E, Annesi Maesano I, Björkstén B, Bråbäck L, Büchele G, Chico M, Cooper P, Clausen M: How well do questionnaires perform compared with physical examination in detecting flexural eczema? Findings from the International Study of Asthma and Allergies in Childhood (ISAAC) Phase Two. Br J Dermatol. 2009, 161 (4): 846-853. 10.1111/j.1365-2133.2009.09261.x.View ArticlePubMedGoogle Scholar
- Asher M, Keil U, Anderson H, Beasley R, Crane J, Martinez F, Mitchell E, Pearce N, Sibbald B, Stewart A: International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods. Eur Respir J. 1995, 8 (3): 483-491. 10.1183/09031936.95.08030483.View ArticlePubMedGoogle Scholar
- Mallol J: Asthma in Latin America: where the asthma causative/protective hypotheses fail. Allergol Immunopathol (Madr). 2008, 36 (3): 150-153. 10.1016/S0301-0546(08)72540-0.View ArticleGoogle Scholar
- Mallol J: Satellite symposium: asthma in the world. Asthma among children in Latin America. Allergol Immunopathol (Madr). 2004, 32 (3): 100-103.View ArticleGoogle Scholar
- Ministry of Health, National Institute of Statistics: Demographic and Health Surveys (DHS) 2008 (In Spanish). La Paz, Bolivia. 2009Google Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2466/14/40/prepub
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