The application of the same epidemiological methods in different countries allows important comparisons between different races and cultures.
During the last decade, two large multi-centres epidemiological studies, the Portuguese Study of Allergic Diseases in Childhood (PAC study) and the International Study of Asthma and Allergies in Childhood (ISAAC study), were implemented in Portuguese speaking regions. The
main objectives were to assess and compare allergic diseases prevalence. The authors stress out the significant differences observed in schoolchildren from the three continents, with different genetic and environmental background. It was found an increase trend in the prevalence of all
allergic diseases, mainly rhinitis, in last decade. Rhinitis has been identified as an independent risk factor for asthma in Caucasian population

Gaspar, A

Morais-Almeida, M

Rosado-Pinto, J

Repositório do Centro Hospitalar de Lisboa Central, EPE

http://france.elsevier.com/direct/REVCLI/Revue française d’allergologie et d’immunologie clinique 46 (2006) 305–308* Corresponding author.E-mail address: hde.imunoalergo@ma0335-7457E/$ - see front matter © 2006Epidemiology of asthma and allergicdiseases in Portuguese speaking regionsÉpidémiologie de l’asthme et des allergiesdans les pays de langue portugaiseJ. Rosado-Pinto *, A. Gaspar, M. Morais-AlmeidaServiço de imunoalergologia, hospital Dona Estefânia, rua Jacinta Marto, Lisboa, PortugalReceived 9 January 2006; accepted 12 January 2006Available online 10 March 2006AbstractThe application of the same epidemiological methods in different countries allows important comparisons between different races and cul-tures. During the last decade, two large multi-centres epidemiological studies, the Portuguese Study of Allergic Diseases in Childhood (PACstudy) and the International Study of Asthma and Allergies in Childhood (ISAAC study), were implemented in Portuguese speaking regions. Themain objectives were to assess and compare allergic diseases prevalence. The authors stress out the significant differences observed in school-children from the three continents, with different genetic and environmental background. It was found an increase trend in the prevalence of allallergic diseases, mainly rhinitis, in last decade. Rhinitis has been identified as an independent risk factor for asthma in Caucasian population.© 2006 Elsevier SAS. All rights reserved.RésuméL’application des mêmes méthodes épidémiologiques dans plusieurs pays permet des comparaisons importantes entre des différentes races etcultures. Pendant la dernière décennie, deux centres majeurs d’études épidémiologiques, Portuguese Study of Allergic Diseases in Childhood(étude PAC) et International Study of Asthma and Allergies in Childhood (étude ISAAC), furent implantés dans des régions de langue portu-gaise. Les objectifs principaux furent de mesurer et comparer la prévalence de maladies allergiques. Les auteurs ont observé des différencessignificatives chez les enfants étudiés dans les trois continents, avec des influences génétiques et environnementales différentes. On a trouvéune tendance à l’augmentation de la prévalence de toutes les maladies allergiques, principalement de la rhinite, pendant la dernière décennie.La rhinite a été identifiée comme étant un facteur indépendant de risque pour l’asthme au sein de la population caucasienne.© 2006 Elsevier SAS. All rights reserved.Keywords: Asthma; Allergic rhinitis; Prevalence; Lifestyle; EnvironmentMots clés : Asthme ; Rhinite allergique ; Prévalence ; Mode de vie ; Environnement1. IntroductionIn the last decades there has been a worldwide increase ofallergic diseases, making them a priority to all the health caresystems [1,2]. Bronchial asthma represents an important healthproblem related with significant impact in terms of morbidityil.telepac.pt (J. Rosado-Pinto).Elsevier SAS. All rights reserved.and mortality, being with allergic rhinitis, the most frequentchildhood chronic diseases, showing also a prevalence increaseas well in developed, as in developing countries [3,4]. Asthmaand rhinitis are common co-morbidities [1], although the natureof the association is still not well known. Allergic rhinitis isfrequently underestimated and undertreated, with important re-percussions in quality of life, affecting school performance inchildren.In 1992 two different epidemiological studies, under the res-ponsibility of our group, started in the Portuguese speakingTable 1PAC study–atopy and asthma prevalence (%)Country N Atopy ActiveasthmaCurrentasthmaRegionCape VerdeSal 235 6.0 10.6 2.6S. Vicente 588 11.9 7.0 4.8PortugalMadeira 1061 54.1 14.6 10.2ChinaMacao 1385 48.6a 1.3 1.1a SPT performed only in a randomly sub-sample of 743 children.J. Rosado-Pinto et al. / Revue française d’allergologie et d’immunologie clinique 46 (2006) 305–308306regions of Portugal (Europe), Cape Verde (Africa) and Macao(Asia): the global International Study of Asthma and Allergiesin Childhood (ISAAC) and the Portuguese Study of AllergicDiseases in Childhood (PAC). In these two studies, involvinga large group of investigators, performed during 10 years, weanalysed epidemiological data collected from Portuguese offi-cial language regions with different genetic, cultural and envir-onmental influences.Coincident with the application of ISAAC study, fromPhases I to III, the authors also performed, in Lisbon, a pro-spective study, in order to evaluate and correlate the impact ofallergic rhinitis in clinical outcome of childhood recurrentwheezing.2. The PAC studyThis study was performed in different Portuguese speakingregions [5,6]. The aims, similar to those described in ISAAC,were mainly to assess atopy and allergic diseases prevalenceand to obtain baseline measure for future comparisons. Ran-domly samples of schoolchildren from Madeira, Cape Verdeand Macao, were included, studied with the same methodology:● investigator-applied standard questionnaire, based onISAAC;● skin prick tests (standardised allergen extracts to commoninhalant allergens: house-dust mites, cockroaches, moulds,pets and pollens, supplied by Merck-AlIergopharma andCBF-Leti);● bronchial provocation test with methacholine (Lofarma) forthe characterisation of bronchial hyperreactivity, performedamong those who had asthma symptoms in the last year,and in matched controls (age and sex).Definitions: Atopy—at least one positive skin prick test(wheal greater than 7 mm2); Positive bronchialhyperreactivity—PD20FEV1 methacholine lower than 7.8 μmol;Active disease—symptoms last year; Current asthma—positivebronchial test and active asthma.In 1993, in Sal Island, were studied 235 children aged 6–16 years, mostly of them Black African; in 1994, a sample of588 children, aged 6–10 years, was included in S. Vicente Is-land, mostly of them Creoles (these two islands belongs to thearchipelago of Cape Verde, an African country in the Gulf ofGuinea). In 1995, 1061 Caucasian children aged 6–10 yearswere studied in Madeira Island (Portugal). In 1997, 1385 Chi-nese children aged 6–12 years, were studied in Macao (terri-tory located on the Southern Coast of China, under Portugueseadministration until 1999).The analysis of the results, revealed significant differencesof atopy and allergic diseases prevalence in the populationsstudied. In Madeira [7], we found the highest prevalence ofatopy (54%), active asthma (14.6%) and current asthma(10.2%) (Table 1).In Macao, according to the atopic status of the population(48.6%), the extremely low prevalence of active asthma (1.3%)and ever asthma (3.5%) was not expected [8], being similar todata published by Leung et al. [9] in San Bu, China, sharingthe same ethnic background, but much lower than the ratesfound in Hong Kong. Most asthmatic children had atopy(86%) and had a positive methacholine challenge test (88%).In contrast, the higher rhinitis prevalence found (24.8%), wasquite similar to those identified in Hong Kong and Madeira(22%), and much higher than the rates in China. In additionto atopy, other risk factors, as lifestyle, should be importanton allergic disease expression in these regions. We showed thatit is possible to have a very strong expression of atopy withvery low asthma prevalence. Comparing our data from Macaoand Madeira, we found an 11-fold variation in active asthmaprevalence (1.3 vs. 14.6%), but also a 20-fold variation in ma-ternal smoking (0.5 vs. 10%). The importance of passive tobac-co smoke exposure in childhood is well known.In Cape Verde [10], active asthma had a similar prevalenceto most European countries, but much lower prevalence of al-lergen sensitisation. Different wheezing phenotypes could beimplicated, even in 6–16-year-old patients, and recurrent res-piratory infections may play a major role. The low prevalenceof atopy in Cape Verde was not related with lower allergenexposure [5]. The high mean value of serum total IgE foundin Cape Verde, even in non-atopic individuals, probably relatedto the parasite load of this population, could be important onthe modulation of the allergic response [11]. The different re-sults found in the two Cape Verde Islands studied, namely thedifferences of atopy and current asthma, with important ethnicvariations, point out the importance of genetics.In order to assess trends in the prevalence of atopy and al-lergic diseases in Cape Verde, in 1999, it was randomly se-lected in Sal Island a new sample of 175 children aged 6–10 years [6]; the epidemiological methods were the same andit was possible to correlate the results with those obtained inthe same age group 6 years earlier. The atopy prevalence raisedthreefolds (6 to 18%) and the allergic rhinitis prevalence(symptoms last year) doubled from 11 to 22%. The prevalenceof active asthma was unchanged (15 to 16%) but the preva-lence of atopic asthma (asthmatics with positive skin pricktests) raised from 2 to 5%. That is probably the price paid forprogress, related with the improved Capeverdian populationwell being.3. The ISAAC studyThis study was performed under the national coordinationof José Rosado-Pinto, by questionnaire modules, in several re-J. Rosado-Pinto et al. / Revue française d’allergologie et d’immunologie clinique 46 (2006) 305–308 307gions of Portugal, between 1993 and 2002, involving morethan 40,000 schoolchildren of two age groups: 6–7 and 13–14 years old [12]. The objectives of this international study[3,13], not yet completely published, and divided into threephases were:● to describe the prevalence and severity of allergic diseasesin children living in different places, allowing comparisonswithin and between countries;● to obtain baseline measures for the assessment of futuretrends in allergic diseases prevalence and severity;● to provide a framework for further etiological research intolifestyle, environmental, genetic and health care factors af-fecting these diseases.In Portugal, this study involved in Phase I 207 schools for6–7 years old and 84 for 13–14 years old and in Phase III 408and 142 schools, respectively, for the same age groups [12].Comparing the data obtained in Phase I and Phase III(Tables 2 and 3)—(data on file), we found a statistically sig-nificant increasing trend in rhinitis (cumulative and last yearsymptoms) and eczema (last year) prevalence, for both theage groups studied. Regarding the last year wheezing preva-lence, in the group of 6–7 years, 9 years later we found thesame prevalence 12.9%, but in the 13–14 years group wefound a statistically significant increasing from 9.2 to 11.8%,particularly in the two urban regions corresponding to the Por-tuguese largest cities: Lisbon (10.9 to 14.6%; P < 0.001) andOporto (7.2 to 13.1%; P < 0.001). The same trend was found,Table 2ISAAC study in Portugal–allergic diseases prevalence in 6–7-year-old childrenAllergic diseases prevalence Phase I(1993/1994)Phase III(2002)P-valueN % N %WheezingWheezing ever 1420 28.2 1512 28.1 0.94Wheezing last year 649 12.9 692 12.9 0.98RhinitisRhinitis ever 1198 23.8 1565 29.1 < 0.001Rhinitis last year 1003 19.9 1291 24.0 < 0.001EczemaEczema ever 938 18.6 1129 21.0 0.002Eczema last year 698 13.9 838 15.6 0.013Table 3ISAAC study in Portugal–allergic diseases prevalence in 13–14-year-oldchildrenAllergic diseases prevalence Phase I(1993/1994)Phase III(2002)P-valueN % N %WheezingWheezing ever 2082 18.2 2576 21.8 < 0.001Wheezing last year 1049 9.2 1398 11.8 < 0.001RhinitisRhinitis ever 3455 30.2 4383 37.1 < 0.001Rhinitis last year 2417 21.2 3131 26.5 < 0.001EczemaEczema ever 1460 12.8 1573 13.3 0.22Eczema last year 869 7.6 1032 8.7 0.002in the 13–14 years group, in the cumulative prevalence ofwheezing, from 18.2 to 21.8%.In the ISAAC Phase III, the questionnaire included severallifestyle items. The most relevant results at national level re-ferred in the 13–14 years age group were: fast-food once aweek or more in 49%; physical activities three or more timesa week in only 22.5%; 3 or more hours/day watching TV in52.2%; no smoker at home in only 34.3% (father smoking in42.3%, and mother smoking in 22.8%).4. The prospective study of risk factors for active asthma atschool ageThe authors [14] performed an 8-year prospective study, inorder to correlate clinical outcome of recurrent wheezing in thefirst years of life with prognostic risk factors, including evalua-tion of the impact of allergic rhinitis. A cohort of 308 childrenwith recurrent wheezing, aged less than 7 years, was enrolledin 1993, studied with clinical questionnaire (adapted fromISAAC), skin prick tests (standardised allergen extracts tocommon inhalant allergens, house-dust mites, pollens, moulds,cockroaches and pets supplied by Merck-AlIergopharma andCBF-Leti, and food allergens, cow’s milk proteins, egg, fishand wheat supplied by Stallergènes), and serum total IgE.Eight years later, it was possible to re-evaluate 81% of the ini-tial sample (N = 249), repeating skin prick tests and performinglung function tests (spirometry with assessment of broncho-dilator response).By logistic regression analysis, personal history of allergicrhinitis was identified as an independent risk factor for activeasthma at school age, with an adjusted odds ratio of 15.8 (95%CI = 6.1–40.8). In the children with allergic rhinitis, 85% hadactive asthma, compared to 21% of those without rhinitis(P < 0.001). Similar results were found, in adults, by otherauthors. Leynaert et al. [15], by investigating cross-sectionaldata from the European Community Respiratory Health Sur-vey, found an adjusted odds ratio for association between rhi-nitis and asthma of 8.1 among atopic and 11.6 among non-ato-pic subjects 20–40 years old. Guerra et al. [16], using data thatwas collected as part of the Tucson Epidemiologic Study ofObstructive Lung Diseases, identified rhinitis as a significantand independent risk factor for adult-onset asthma, with anodds ratio of 4.13. There is certainly more than just a causalrelation between asthma and rhinitis, but it is yet to be deter-mined if asthma is the natural progression of a common airwaydisease.5. ConclusionThe significant differences found in atopy and allergic di-seases prevalence in schoolchildren populations from African,Asiatic and European Portuguese speaking regions studied inthe PAC study, point out the importance of genetics, linked torace, in the pathogenesis of these diseases, although it will bestrongly modulated by environmental and lifestyle variables.Comparing the results obtained from Phase I and Phase IIIof ISAAC study in Portuguese schoolchildren, an increasing[4][5][6][7][8][9][10[11[12[13[14[15[16J. Rosado-Pinto et al. / Revue française d’allergologie et d’immunologie clinique 46 (2006) 305–308308trend in the prevalence of all allergic diseases during the lastdecade was revealed, mainly in relation to rhinitis in both agegroups studied, with a slight increase also in asthma and atopiceczema symptoms during the last year. Some lifestyle changesin our children, such as western diet habits, absence of physicalactivities, high indoor habits (watching TV or playing withcomputer) and tobacco smoke exposure, seem to play a role.Early diagnosis of bronchial asthma is important to planadequate treatment and prevention. Although several clinicalstudies suggest that upper respiratory tract dysfunction may af-fect the lower airways, the diagnosis of rhinitis is frequentlyunderestimated by non-specialist physicians, namely in paedia-tric age. The authors have identified rhinitis as an independentrisk factor for asthma in Caucasian population.The worldwide increasing of asthma and allergic diseasesobserved in the last decades demands for a global health strate-gy [1–3]. As a consequence of these large epidemiological pro-jects, it will be possible to plan health care programs at na-tional and international levels for better prevention, educationand treatment of allergic diseases, whose direct and indirectcosts will certainly strongly increase in this Century.References[1] Bousquet J, Van Cauwenberge P, Khaltaev N, Aria Workshop Group,World Health Organization. Allergic rhinitis and its impact on asthma. JAllergy Clin Immunol 2001;108(Suppl. 5):147–334.[2] Global Strategy for Asthma Management and Prevention. National Insti-tutes of Health, National Heart, Lung, and Blood Institute. Guidelines forthe diagnosis and management of asthma, NIH, Publication Number 02-3659; 2002.[3] ISAAC Steering Committee. Worldwide variation in prevalence of symp-toms of asthma, allergic rhinoconjunctivitis, and atopic eczema: ISAAC.Lancet 1998;351:1225–32.Bousquet J, Ndiaye M, Ait-Khaled N, Annesi-Maesano I, Vignola AM.Management of chronic respiratory and allergic diseases in developingcountries. Focus on sub-Saharan Africa. Allergy 2003;58:265–83.Morais Almeida M, Rosado Pinto J. Bronchial asthma in children: clin-ical and epidemiologic approach in different Portuguese speaking coun-tries. Pediatr Pulmonol Suppl 1999;18:49–53.Morais Almeida M, Gaspar A, Rosado Pinto J. Epidemiology of asthmain Portugal, Cape Verde and Macao. Pediatr Pulmonol 2001(Suppl. 23):35–7.Morais Almeida M, Câmara R, Marques A, Ornelas P, Romeira J, Neu-parth N, et al. Prevalence of asthma and atopy in Madeira Archipelagoschoolchildren. Eur Respir J 1996;9(Suppl. 23):232s.Morais Almeida M, Andrade I, Ieong KM, Gaspar A, Andrade N, Hum-berto J, et al. Epidemiology of childhood allergic diseases and atopy inMacau (Southern Coast of China). Eur Respir J 1998;12(Suppl. 28):13s.Leung R, Ho P, Lam CWK, Lai CKW. Sensitization to inhaled allergensas a risk factor for asthma and allergic diseases in Chinese population. JAllergy Clin Immunol 1997;99:594–9.] Neuparth N, Morais Almeida M, Santa Marta C, Pires G, Vieira LopesD, Tavares C, et al. Prevalence of childhood asthma and atopy in CapeVerde: preliminary results. Eur Respir J 1995;8(Suppl. 19):495s.] Abreu Nogueira JM, Pinto PL, Morais Almeida M, Tavares C, Lopes D,Loureiro V, et al. Alatop-RIA in the screening of atopy in a non Cauca-sian population. Allerg Immunol (Paris) 1997;9:274–8.] Nunes C, Ladeira S, Rosado Pinto J. Definição, epidemiologia e classifi-cação da asma na criança. In: Rosado Pinto J, Morais de Almeida M,editors. A criança asmática no mundo da alergia. Lisboa: Euromédice;2003. p. 35–56.] Asher MI, Keil U, Anderson HR, Beasley R, Crane J, Martinez F, et al.International study of asthma and allergies in childhood (ISAAC). Ratio-nale and methods. Eur Respir J 1995;8:483–91.] Morais-Almeida M, Gaspar A, Rosado-Pinto J. Risk factors for activeasthma at school age: an 8-year prospective study. Allergy Asthma Proc2006 (in press).] Leynaert B, Bousquet J, Neukirch C, Liard R, Neukirch F. Perennial rhi-nitis: an independent risk factor for asthma in nonatopic subjects: resultsfrom the European Community Respiratory Health Survey. J AllergyClin Immunol 1999;104:301–4.] Guerra S, Sherrill DL, Martinez FD, Barbee RA. Rhinitis as an indepen-dent risk factor for adult-onset asthma. J Allergy Clin Immunol 2002;109:419–25.

Épidémiologie de l’Asthme et des Allergies dans les Pays de Langue Portugaise

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