Research Article Validation of the ISAAC Standardized Questionnaire Used by ...downloads.hindawi.com/archive/2013/490906.pdf · 2019. 7. 31. · Validation of the ISAAC Standardized

Hindawi Publishing CorporationEpidemiology Research InternationalVolume 2013, Article ID 490906, 6 pageshttp://dx.doi.org/10.1155/2013/490906

Research ArticleValidation of the ISAAC Standardized Questionnaire Used bySchoolchildren from Mexicali, Baja California, Mexico

Karla Gorozave-Car,1 Albino Barraza-Villarreal,1 Consuelo Escamilla-Núñez,1

Leticia Hernandez-Cadena,1 Luz Helena Sanín-Aguirre,1,2

Marlene Cortez-Lugo,1 J. Blanco-Muñoz,1 Horacio Riojas-Rodríguez,1

Hortensia Moreno-Macias,3 and Isabelle Romieu1

1 Instituto Nacional de Salud Publica, Avenida Universidad No. 655, Colonia Santa Marıa Ahuacatitlan,62100 Cuernavaca, MOR, Mexico

2Universidad Autonoma de Chihuahua, Avenida Escorza No. 900, Zona Centro, 31000 Chihuahua, CHIH, Mexico3 Universidad Autonoma Metropolitana—Iztapalapa, Avenida San Rafael Atlixco 186, Colonia Vicentina,Delegacion Iztapalapa, 09340 Mexico City, DF, Mexico

Correspondence should be addressed to Albino Barraza-Villarreal; [email protected]

Received 11 July 2013; Revised 18 October 2013; Accepted 19 October 2013

Academic Editor: David Christiani

Copyright © 2013 Karla Gorozave-Car et al. This is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properlycited.

Background. In Mexico, several studies have been conducted under the ISAACmethodology; nevertheless, no validation studies ofthe ISAAC questionnaire based on objective clinical testing in our country have been published. Aims of the Study. To validate theISAAC questionnaire, used in a study of prevalence of allergic diseases, based on medical, respiratory, and allergic evaluations ofschoolchildren being 11 to 16 years old inMexicali, Mexico.Material andMethods. We conducted a cross-sectional study to validatethe ISAAC questionnaire through the generation of an index (considered as gold standard) using pre- and postbronchodilatorspirometry test, exhaled nitric oxide measurements, and atopic evaluations. 114 schoolchildren were included (23 asthmatics withrespiratory symptoms and 91 nonasthmaticswithout respiratory symptoms) andwe evaluated the sensitivity, specificity, and positiveand negative predictive value of the questionnaire using discriminant analysis. Results. We observed sensitivity of 35.2% andspecificity of 93.3% and the positive and negative predictive values were 82.6% and 61.5%, respectively. Conclusions. Our findingsindicate that the ISAAC Mexican version questionnaire was less sensitive and more specific when compared to the gold standard;however, it is adequate and able to discriminate children with and without asthma and a useful tool to use in epidemiologicalstudies.

1. Introduction

Asthma, allergic rhinitis, and atopic dermatitis are three ofthe allergic diseases that most affect children worldwide [1–3]. Asthma is a multifactor disease characterized by chronicinflammation of the airways and a reversible obstruction ofair flow. Concern about these diseases has arisen because oftheir increase over the years, with prevalence and mortalityrates having increased worldwide [4].

The International Study of Asthma and Allergies inChildhood (ISAAC) methodology was established in 1990s[4]. This methodology is a useful and practical strategy to

most effectively identify these types of affections in children.It has been used in many countries where different languagesare spoken, as well as in countries where the language doesnot have a way to describe asthma symptoms.

The ISAAC is designed with three phases. Phase I isdesigned to assess the basic prevalence and severity ofasthma and other allergic diseases by administering targetquestionnaires. Phase II investigates possible risk factorsrelated to these diseases and those suggested in phase I.Phase III repeats phase I to assess the prevalence tendencyof these diseases and to examine the hypothesis establishedby conclusions from phase I [5].

2 Epidemiology Research International

The ISAAC protocol maximizes the value of epidemio-logical research involving transversal studies by providing astandard tool to enable comparisons with other populations.Therefore, it is advisable to establish a mechanism to validatethe tool in order to assure the quality of information andsupport the findings. Though ISAAC validation studies havebeen conducted worldwide, some of these studies havebeen performed without considering objective clinical tests,contrasting only the responses of parents with those ofchildren or using other tests for validation [6–9]. On theother hand, different studies using this methodology havebeen conducted in Mexico [10–12]; however, there are nopublished studies that validate the ISAAC questionnaireusing objective clinical tests.Thus, the purpose of the presentstudy is to validate the ISAAC questionnaire used in a studyof prevalence and risk factors in Mexicali, Baja California,Mexico, conducted in 2004, measuring the tool’s sensitivity,specificity, and concordance by contrasting previous resultswith clinical tests for lung function and other markers inchildren.

2. Material and Methods

2.1. Design of Study Population. To validate the questionnaireusing objective clinical tests, a convenience sample of 114schoolchildren from 11 to 16 years old was chosen from a totalof 5287 schoolchildren who participated in the transversalstudy of allergic diseases during 2004 in Mexicali, BajaCalifornia, Mexico.

2.2. Data Collection. An ISAAC questionnaire was usedto collect data on sociodemographic variables, past healthhistory, and respiratory health. Each participant was assigneda personal number and was classified as asthmatic ornonasthmatic, according to information reported on thequestionnaires, which were self-administered by the parents.All procedures were explained to the parents, who signed aninformed consent form.The children also gave their informedassent. The study protocol was reviewed and approved byethics committees of the National Institute of Public Health.Of 114 children selected, 23 reported a medical diagnosis ofasthma and have respiratory symptoms in the last 12 monthsand 91 did not report symptoms in the last 12 months ormedical diagnosis of asthma.

2.3. Mechanisms Used to Validate the Questionnaire. Thequestionnaires asked two questions. Has a doctor ever diag-nosed your child as asthmatic? And have you had wheezingor whistling in the chest in the last 12 months? After childrenwere identified as asthmatic or non-asthmatic based on theanswers, different clinical tests were conducted to obtain agold standard index to validate both questions. The medicaldiagnosis of asthma reported in the ISAACquestionnaire wasvalidated based on the following tests.

2.3.1. Reversibility Test for Lung Function. A spirometry test(Easy One, Zurich, Switzerland) was administered to eachparticipant in accordance with American Thoracic Society

1994 criteria [13]. After an acceptable and reproducible testwas obtained, a 200𝜇g dose of albutherol (a short-actingB2 adrenergic receptor agonist) was administered. After 15minutes, a second spirometry was conducted to assess thechange in lung function. To determine the bronchodilatorresponse we use the degree of reversibility between pre-bronchodilator and postbronchodilator of FEV

1(≥12% and

≥200mL) according to the GINA criteria [14]; however,we also calculated the percentage of change between pre-bronchodilator and post bronchodilator test, quantified as apercent relative change value and derived from the number ofschoolchildrenwhohad a positive reversibility test using bothcriteria was almost similar, we decided to use this percentchange value for the generation of the gold standard index.

2.3.2. Exhaled Nitric Oxide (eNO) Concentrations. eNO con-centrations were measured for each child during visits to thehealth center and according to American Thoracic Societyrecommendations [15]. As recommended, the child wasasked to be seated for five minutes before and during thetest. All tests were conducted indoors to reduce possiblecontamination from environmental nitric oxide.The exhalednitric oxide was instantly measured by chemiluminescenceusing a portable NIOX MINO, with a measurement rangefrom 5 to 300 ppb and a detection limit of 5 ppb [16]. For eachparticipant, the two best tests were selected and the averageconcentration for those tests was considered.

2.3.3. Skin Test. A skin test was conducted using multitesttesting [17, 18]. This enabled identifying a specific allergenresponse to standard allergens (Dermatophagoides farinae,grass, trees, dogs, cats, and cockroaches) glycerinated in aconcentration of 1 : 10 (weight/volume) with negative controland positive to histamine (1 : 100). The test was performedby trained medical personnel. A diameter of ≤3mm for theallergens tested was considered to be a null or negative result.A positive skin test was determined by a wheel greater orequal to 3mm or equal to the same diameter of the wheelproduced by the histamine control, after 15minutes of placingthe skin test. We determined atopy status as having at leastone reaction to an antigen tested.

2.4. Statistical Analysis. First, the questionnaire’s reliabilitywas determined by assessing the inner consistency andconcordance of each answer using kappa statistics. Second,the quality and validity of the medical diagnoses of asthmawere assessed by comparing answerswith the index generatedaccording the clinical tests, with the latter being consideredthe gold standard. The rate was obtained by discriminantanalysis [19], which is a multivariate statistical technique thatanalyzes significant differences among groups of individualsversus variables measured in those groups. If there are anydifferences, it tries to explain them and provides systematicclassification procedures for new observations with unknownorigins in one of the groups studied. In that respect, weconsidered 3 classification variables: (1) percentage changein FEV

1or reversibility test, (2) average concentration of

FeNO levels with logarithmic units, and (3) atopic condition,

Epidemiology Research International 3

Table 1: Descriptive statistics and main outcomes of the study population according to the information obtained by ISAAC questionnaireand clinical tests.

VariablesAsthmatics(𝑛 = 23)a

Nonasthmatics(𝑛 = 91)a 𝑃 valueb

Mean (SD) Mean (SD)Age, yrs 12.7 (0.7) 12.6 (0.8) 0.613Height, m 1.6 (0.1) 1.6 (0.1) 0.586Gender (male), % 39.1 40.9 0.537Basal pulmonary function, L

FEV1 2.8 (0.4) 2.6 (0.5) 0.294FVC 3.2 (0.5) 3.1 (0.6) 0.247FEF25–75 3.2 (0.9) 3.1 (0.9) 0.719

FEV1/ FVC 0.86 (0.05) 0.86 (0.07) 0.757logFeNO 2.4 (0.7) 2.6 (0.8) 0.301%cFEV1 3.2 (5.9) 1.7 (6.3) 0.294%cFEV1 ≥ 12, % (%) 8.7 3.3 0.264Atopics % 82.6 39.6 0.000aAccording to ISAAC questionnaire.b𝑃 < 0.05.

cAverage change between pre- and postspirometry.

with 2 comparison groups (asthmatic individuals and non-asthmatic individuals) in a sample size of 114 children (23asthmatic individuals and 91 nonasthmatics individuals).Additionally and with the aim of comparing the resultsobtained, we also analyzed the information considering onlythe reversibility test according to GINA criteria as the goldstandard and tested again the sensitivity and specificity ofthe ISAAC questionnaire. Finally, a new classification wasobtained based on a constructed discriminant function,a canonic correlation, and the transformed lambda value.ANOVA tests were used as validation parameters for theclassification obtained.

3. Results

Twenty-three (20.2%) of the 114 children participating inthe research reported in the questionnaire having a medicaldiagnosis of asthma, with a higher percentage (60.9%) beingfemale, 12 to 14 years old. A total of 79.8% of schoolchildrenparticipating in the research did not report symptoms andwere considered as non-asthmatics, 59.1% of which werefemale, from 11 to 16 years old.

Table 1 presents the results of the descriptive statistics andmain outcomes, where it can be seen that the parametersfor lung function do not differ between the two groupsof individuals studied (asthmatic and non-asthmatic par-ticipants), although the FEV

1reversibility percentage was

slightly greater for the asthmatic group (𝑃 = 0.294). AverageFeNO concentrations were higher in the group of individualsthat did not report a clinical diagnosis of asthma. Differenceswere not statistically significant.

Positive skin tests were observed in 48% of the totalsample, with a higher prevalence in the asthmatic group ver-sus non-asthmatic schoolchildren (82.6% versus 39.6%, resp.,

𝑃 < 0.0001) (Table 1). The allergens that provoked a positiveresponse with greater frequency were different between thegroups. The most frequent allergens for asthmatic childrenwere trees and dermatophagoides farinae (14% and 9%, resp.)whereas for non-asthmatic children they were cockroachesand cat and grass allergens (23% and 16%, resp.) (Table 2).

A new classification of participants was obtained as aresult of the gold standard. Fifty-four of the 114 children wereclassified as asthmatic and 60 as non-asthmatic, as shown inTable 3. Nineteen of the 23 children who reported a diagnosisof asthma on the questionnaires were classified by the goldstandard (sensibility = 35.2% and positive predictive value =82.6%) and 56 of the 60 schoolchildren classified as non-asthmatic by the gold standard were identified correctly asnon-asthmatic individuals by the questionnaire (specificity =93.3% and negative predictive value = 61.5%). On the otherhand, when we use the reversibility test considering GINAguidelines only as gold standard, the sensitivity and specificitywere 22% and 81%, respectively (Table 4).

Based on the data obtained, we can observe that theprobability that the questionnaire correctly classifies a child asasthmatic (sensibility) was lower than the probability of cor-rectly classifying him or her as non-asthmatic (specificity).Table 5 shows the characteristics of individuals according tothe gold standard classification.

With the ROCanalysis, a probability of 64%was observedfor asthmatic and non-asthmatic individuals and both groupswere correctly classified by the discriminant analysis. Con-cordance (kappa test) for both tests was 65.8.

4. Discussion

The ISAAC study and its phases have been developed in ourcountry [10–12]; the prevalence and risk factors associated


Table 2: Frequency of positive skin prick tests according to most common sensitivities allergens tested in the study population.

Asthmatica Nonasthmatica𝑃 value

Frequency (%) Frecuency (%)Allergens

Tree 14 (70.0) 0 (0.0) 0.000Dermatophagoides farinae 9 (45.0) 10 (15.6) 0.012Lawn 4 (19.1) 16 (25.4) 0.769Dog 0 (0.0) 8 (12.7) 0.189Cockroach 6 (30.0) 23 (34.9) 0.791Cat 4 (20.0) 16 (23.9) 1.000Atopic positive 19 (82.6) 36 (39.6) 0.000

aAccording to ISAAC questionnaire.

Table 3: Classification of the study population according to gold standard (percentage change in FEV1, average concentration of FeNO levels,and atopic condition).

Clinical test (gold standard) TotalAsthmatics Nonasthmatics

Questionnaire ISAAC Asthmatics 19 4 23Nonasthmatics 35 56 91

Total 54 60 114Sensitivity: (19/54) ∗ 100 = 35.2; specificity: (56/60) ∗ 100 = 93.3.Predictive positive value: (19/23) ∗ 100 = 82.6; predictive negative value: (56/91) ∗ 100 = 61.5.

Table 4: Classification of the study population considering the reversibility test as gold standard.

Reversibility test GINA guidelines (% FEV1 ≥ 12%) TotalAsthmatics Nonasthmatics

Questionnaire ISAAC Asthmatics 13 10 23Nonasthmatics 46 45 91

Total 59 55 114Sensitivity: (13/59) ∗ 100 = 22.0; specificity: (45/55) ∗ 100 = 81.8.Predictive positive value: (13/23) ∗ 100 = 56.5; predictive negative value: (45/91) ∗ 100 = 49.5.

with allergic diseases among schoolchildren are known.Nevertheless, to our knowledge the present study is the firstconducted in our country to validate the ISAAC question-naire through objective clinical testing.

Our results indicate that 54 of the 114 children partici-pating in the research were classified as asthmatic accordingto the gold standard (percentage change in FEV

1, average

of FeNO concentrations, and skin test positive). Meanwhile,according to the questionnaires, 23 individuals reportedhaving an asthmatic condition, which represents a very lowsensibility (35.2%) of the instrument compared to otherstudies. This could indicate that interpreting all recentsymptoms in the questionnaire was not adequate and mayresult in subestimating the prevalence of childhood asthma;that is, the 35 schoolchildren classified as negative false bythe questionnaire are probably those who are not familiarwith the term of wheezing and did not correctly report therespiratory noises and sensations, and the 4 schoolchildrenwho were found as positive false had some respiratorydisease or respiratory symptoms when the questionnairewas applied. On the other hand, we observed that our goldstandard classified 60 children as non-asthmatics versus 91

who were reported as healthy by the questionnaire, resultingin specificity of 93.3%. Similarly, the positive predictive valueof the questionnaire was high (82.6%). These results are veryimportant in public health because this tool can be used withconfidence to identify the health situation in communities.

With regard to validation studies conducted worldwide,specifically among the Latino school population, it is impor-tant to point out that, unlike themajority of studies published,our research is one of the first studies to use several clinicaltests (spirometry with bronchodilatation, measurement ofFeNO levels, and skin tests). Other studies validate question-naires mainly by contrasting responses of parents with thoseof children or by exclusively using spirometry.

Research conducted in a Latino population in Los Ange-les, CA, USA, [20] evaluated the validation of responses to aquestionnaire using spirometry and children’s responses.Thestudy compared parents’ responses with children’s responsesregarding asthma diagnosis. The more accurate report wasobtained from children, for which 47% of children reportedas asthmatic in the questionnaire were observed to be positiveby at least one of four spirometries conducted.

Epidemiology Research International 5

Table 5: Descriptive statistics and main outcomes of the study population according to the classification obtained by gold standard index.

Asthmatics (𝑛 = 54) Nonasthmatics (𝑛 = 60)𝑃 valuea

Mean (SD) Mean (SD)P (asthmatics)b, % 67.4 (7.5) 23.4 (7.7) 0.000Discriminant scores 1.1 (0.4) −0.9 (0.4) 0.000FeNO (ppb), median (P25, P75)

c 10.8 (7.5, 16.0) 13.5 (9.3, 27.5) 0.017logFeNO (ppb) 2.4 (0.7) 2.8 (0.8) 0.009FEV1 (L)

d 2.2 (6.0) 1.9 (6.4) 0.766Atopics, % 98.2 3.3 0.000a𝑃 < 0.05.

bP (asthmatics): probability of being in the asthmatic group.cMann-Whitney test.dAverage change between pre- and postspirometry test.

Another validation study was conducted with Spanishspeakers in Spain [21]. This study demonstrated how muchvariability an event can present, such as bronchial hyperre-activity, when compared with other studies performed in thesame country.

In addition, a multicentric validation study conducted in40 countries and 90 centers was performed by comparingresponses before and after children were shown a video toidentify respiratory diseases. This study found that teenagersinterpreted asthmatic symptoms differently. In 20 centersthere was concordance of ≥0.4, indicating that the question-naires should obtain the same results when administeredusing different modalities, at different times, and by differentobservers [22]. Thus, total validation of the questionnaireis a strategy that more greatly guarantees obtaining reliabledata. In the present research, the same questionnaire wasadministered to an additional subsample at two differentbut consecutive moments. According to kappa statistics, thatverified the reliability and quality of the instrument, weobserved a questionnaire reproducibility of 66%.

With regard to the classification of asthma in this studyusing the ISAAC questionnaire, it is important to mentionthat this was obtained mainly with two questions. Has a doc-tor ever diagnosed your child as asthmatic? And during thelast 12 months has your child observed wheezing? Therefore,we are probably excluding children with wheezing duringanother period of life, which could indicate an asthmaticcondition.

A limitation of this study may be that the gold standardwas based on three different tests; therefore the sensitivity ofthe questionnaire could be affected. For this reason, addition-ally we used only the reversibility test considering the GINAguidelines [14] as gold standard and the sensitivity of theISAAC questionnaire was low; JenkinsMA and collaboratorsfound sensitivity of 0.39 (0.21–0.61) in adults and 0.54 (0.48–0.67) in children using the bronchial hyperresponsiveness(BHR) as gold standard for asthma, noting that the BHRwas highly specific but not sensitive [23]. Nevertheless, theliterature has reported that the tests that we used can be usedfor the diagnosis of asthma.Therefore, we believe that, in thiscase, lack of affirmative criteria to diagnose asthma wouldunderestimate the sensibility of questionnaire. Finally, our

sample size is small which may have limited the power of ourstudy.

5. Conclusions

In summary, our findings indicate that the ISAAC Mexicanversion questionnaire was less sensitive and more specificwhen compared to the gold standard; however it is adequateand able to discriminate children with and without asthmaand a useful tool to use in epidemiological studies. Neverthe-less, to improve the consistency and quality of information,measurement instruments need to be continuously validatedbecause, though they are the standardized ones, it is impor-tant to remember that language, culture, and accessibility canaffect the results.This will enable verifying the authenticity ofthe data and assuring that the efforts of governmental, social,and scientific institutions benefit high-risk populations.

Conflict of Interests

The authors declare they have no competing conflict ofinterests.

Acknowledgments

We want to extend our gratitude to the schoolchildren thatparticipated in the study. This research was supported by aresearch grant from the National Center for EnvironmentalHealth, Center for Disease Control and Prevention, Atlanta,GA.

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Research Article Validation of the ISAAC Standardized Questionnaire Used by ...downloads.hindawi.com/archive/2013/490906.pdf · 2019. 7. 31. · Validation of the ISAAC Standardized