Date post: | 04-Dec-2023 |
Category: |
Documents |
Upload: | independent |
View: | 0 times |
Download: | 0 times |
Delivered by Publishing Technology to: Hinari - Cameroon IP: 190.221.48.174 On: Sat, 04 Sep 2010 16:19:41Copyright (c) Oceanside Publications, Inc. All rights reserved.
For permission to copy go to www.copyright.com
Factors associated with allergic rhinitis in children andadolescents from northern Mexico: International Study ofAsthma and Allergies in Childhood Phase IIIB
Sandra N. Gonzalez-Díaz, Ph.D.,1 Blanca E. Del Río-Navarro, M.D.,2
Dino R. Pietropaolo-Cienfuegos, M.D.,2 Alberto J. Escalante-Domínguez, M.D.,3
Roberto G. García-Almaraz, M.D.,4 Valente Merida-Palacio, M.D.,5 andArturo Berber, M.D., Ph.D.6
ABSTRACT
The epidemiology of allergic diseases has not been studied extensively in Mexico. The present study, based on theInternational Study of Asthma and Allergies in Childhood Phase IIIB survey, reports the prevalence of allergic rhinitisand the associated risk factors in the pediatric population in four cities in northern Mexico. Children (6 –7 years old) andadolescents (13–14 years old) in public elementary and secondary schools were surveyed in 2002 and 2003. The subjectswere chosen randomly from Ciudad Victoria, Mexicali, Monterrey, and Tijuana. The following categories were analyzed:occurrence of rhinitis symptoms (currently or in the last 12 months), rhinoconjunctivitis symptoms, a previous diagnosisof allergic rhinitis, and relevant environmental factors. Factors associated with rhinitis that were identified previouslywith the chi-squared test were analyzed using logistic regression. The number of valid questionnaires was 10,892 forschoolchildren and 12,299 for adolescents. In 6- to 7-year-old children, the following frequencies were determined: rhinitis(ever), 27.9%; current rhinitis, 24.2%; rhinoconjunctivitis, 9.2%; and diagnosis of allergic rhinitis, 5.5%. The corre-sponding frequencies in 13- to 14-year-old children were 33.3, 34.1, 18.4, and 3.8%. In both 6- to 7-year-old and 13- to14-year-old children, all rhinitis items were associated with asthma symptoms, dermatitis symptoms, paracetamolconsumption, and maternal smoking (odds ratio, �1; p � 0.05). The main risk factors associated with allergic rhinitissymptoms in children and adolescents from cities in northern Mexico were other allergic conditions, paracetamolconsumption, and passive smoking.
(Allergy Asthma Proc 31:e53–e62, 2010; doi: 10.2500/aap.2010.31.3346)
Key words: Allergy, International Study of Asthma and Allergies in Childhood, ISAAC, Mexico, prevalence,paracetamol, passive smoking, rhinitis, risk factors
The prevalence of atopy continues to rise in someparts of the world.1 The demand for resources to
deal with these illnesses has also increased.2 For thisreason, the International Study of Asthma and Aller-gies in Childhood (ISAAC) was formed in the 1990s tostudy and compare the prevalence of asthma, allergicrhinitis, and eczema in populations in different coun-tries using standardized methodology that allows in-ternational cooperation and data comparison.3
In the ISAAC Phase I, children 13–14 years of age at155 centers in 56 countries (n � 463,801) and children6–7 years (n � 257,601) at 91 centers in 38 countrieswere studied using a questionnaire that asked aboutasthma, rhinoconjunctivitis, and eczema symptoms.The questions were answered by the adolescents or, inthe case of children, by the parents. During Phase I,questions about genetic, lifestyle, and environmentalfactors were included to establish a framework forfurther etiologic research.4 During Phase II, possibleetiologic factors in children 9–11 years of age from 30centers in 22 countries were studied by including skin-prick tests for atopy, total and specific serum IgE leveldetermination, a hypertonic saline aerosol challenge,house-dust mite antigen measurement (for aeroaller-gen and endotoxin analysis), and DNA analysis forgenetic polymorphisms associated with asthma andallergies. Phase II studied 9- to 11-year-old childrenbecause at this age the children could participate in theblood extraction and pulmonary function tests thatwere required in this phase.5 Phase III was performed
From the 1Hospital Universitario “Dr. Jose E. Gonzalez,” Monterrey, Nuevo Leon,Mexico, 2Hospital Infantil de Mexico “Federico Gomez,” Ciudad de Mexico,Mexico, 3Hospital General Tijuana, Baja California, Mexico, 4Hospital Infantil deTamaulipas, Ciudad Victoria, Tamaulipas, Mexico, 5Hospital General de Mexicali,Baja California, Mexico, and 6Foundation for the Advancement of Science, MexicoCity, DF, MexicoThe authors have nothing to disclose pertaining to this articleAddress correspondence and reprint requests to Blanca Estela Del Río-Navarro, M.D.,Departamento de Alergia e Inmunología Clínica, Dr. Marquez No. 162 Col. Doctores,C.P. 06720 D.F., MexicoE-mail address: [email protected] © 2010, OceanSide Publications, Inc., U.S.A.
Allergy and Asthma Proceedings e53
DO NOT C
OPY
Delivered by Publishing Technology to: Hinari - Cameroon IP: 190.221.48.174 On: Sat, 04 Sep 2010 16:19:41Copyright (c) Oceanside Publications, Inc. All rights reserved.
For permission to copy go to www.copyright.com
with an instrument similar to Phase I and aimed toexamine trends over time in the prevalence of asthma,rhinoconjuctivitis, and eczema symptoms in the cen-ters that had participated in Phase I (Phase IIIA) andthose that had not (Phase IIIB).6
The development of allergic rhinitis depends oncomplex interactions between genetic and environ-mental factors that still are not fully understood.7 Inaddition, recent studies have shown that environmen-tal conditions in utero also influence the developmentof allergies.8,9 It is therefore very useful to study theepidemiology and prevalence of allergies in differentregions not only to track the frequency of these dis-eases in particular areas, but also to identify risk factorsthat are specific to each region.
The epidemiology of allergic diseases has not beenstudied extensively in Mexico. The ISAAC study meth-odology, both Phase I and Phase III, was performed, inpart, in the cities of Cuernavaca10,11 and Ciudad Juarez(Chihuahua).12 Results from ISAAC Phase IIIB in chil-dren from the northern area of Mexico City have beenreported previously.13 We still have very little infor-mation about the dimension and evolution of allergicdiseases, as well as their variations, in different areas ofMexico. The present study was performed to deter-mine the prevalence and risk factors associated withallergic rhinitis and rhinoconjunctivitis symptoms inthe pediatric population in several cities in northernMexico using data from ISAAC Phase IIIB.
METHODS
Study DesignThis report is based on an observational, cross-sec-
tional, descriptive study performed in children 6–7years of age and adolescents 13–14 years of age inelementary and secondary schools in 2002 and 2003.
QuestionnaireThe Spanish version of the ISAAC Phase IIIB ques-
tionnaire was used as the collection instrument (aspart of ISAAC Latin America) in all elementary andsecondary schools (public and private) in three citiesin northern Mexico: Victoria, Mexicali, and Tijuana.In a fourth city, Monterrey, the researchers includedonly public schools in the city and nearby counties.Therefore, we did not use any method of random-ization to obtain the sample size required for ISAACPhase III design. Data collection was performed inparticipating cities by the following researchers: Al-berto Jose Escalante-Domínguez, M.D. (HospitalGeneral Tijuana, Baja California); Roberto GerardoGarcía-Almaraz, M.D. (Hospital Infantil de Tama-ulipas, Ciudad Victoria, Tamaulipas); Sandra NoraGonzalez-Díaz, M.D. (Hospital Universitario “Dr.Jose E. Gonzalez”, Monterrey, Nuevo Leon); and
Valente Merida-Palacio, M.D. (Hospital General deMexicali, Baja California).
The ethics committee of each participating hospitalpreviously approved the study design and method-ology. Each participating school was in the metro-politan areas of the cities; however, in Monterrey,schools from seven other counties in the state ofNuevo Leon were also included. The objectives, aswell as the procedure for collecting data, were ex-plained to the participants and their parents, andinformed consent was obtained for each includedsubject. For children 6 –7 years of age, the question-naires were completed by parents or tutors at thechildren’s homes. If there was no response after 1week, another questionnaire was sent home, andthen a third. If there was still no response, the stu-dent was included in the nonresponding group.Children 13 and 14 years of age answered the ques-tions by themselves at school according to the sug-gestions in the Researcher’s Manual for ISAACPhase IIIB3 after seeing a video about the question-naire. The students that did not attend school theday the questionnaire was completed were includedin the nonresponding group. The collection periodswere between June 2001 and January 2003 in theparticipating cities. Each center was responsible forstudy-related expenses.
Primary VariablesThe main variables in the study were the presence of
rhinitis symptoms without a cold at least once in thelast 12 months (current prevalence) or in the child’slifetime (accumulated prevalence), a previous diagno-sis of allergic rhinitis (by any physician, regardless ofspecialty), and symptoms of rhinoconjunctivitis (itchyand watery eyes plus nasal symptoms). In ISAACPhase III, specific questions address each of these vari-ables. Associated environmental factors (foods, passivesmoking, use of acetaminophen paracetamol duringthe 1st year of life and in the last 12 months, number ofsiblings at home, exercise habits, etc.) were obtainedusing the environmental questions from the ISAACPhase IIIB questionnaire.
Processing and Statistical AnalysisThe data from the questionnaires were entered twice
into the digital database at each center, and the datawere sent later to the ISAAC International Data Center.Inconsistencies (e.g., differences in the stated age) wereidentified and corrected by reviewing the originalquestionnaires. The databases were approved for in-clusion in the global analysis of ISAAC Phase III,except for the center in Tijuana, because of a delay insending final corrections. To detect variables thatwere likely to be related to an increased or decreased
e54 July–August 2010, Vol. 31, No. 4
DO NOT C
OPY
Delivered by Publishing Technology to: Hinari - Cameroon IP: 190.221.48.174 On: Sat, 04 Sep 2010 16:19:41Copyright (c) Oceanside Publications, Inc. All rights reserved.
For permission to copy go to www.copyright.com
risk (p � 0.10) of symptoms of accumulated or cur-rent rhinitis, we performed a chi-squared test forcategorical variables. The impact of possible associ-ated factors and their relationships with environ-mental variables were analyzed by logistic regres-sion using a conditional method to obtain modelsthat explained each manifestation of rhinitis. Analy-sis was performed using SPSS 8.0 (SPSS, Inc., Chi-cago, IL).
RESULTSA total of 25,162 students were eligible to complete
the questionnaire; of these, 1971 (8%) did not partic-ipate. The final sample consisted of 23,191 question-naires that were completed: 10,892 (47%) from chil-dren 6 –7 years of age and 12,299 (53%) fromadolescents 13–14 years of age. Tables 1 and 2 showthe prevalence for both sexes by age group. Forchildren 6 –7 years of age, the global frequency forrhinitis symptoms (ever) was 27.9% (range, 24.5–30.9%) and the global frequency for current rhinitissymptoms was 24.2% (range, 21.3–28.2%). With re-
gard to rhinoconjunctivitis symptoms, the global fre-quency was 9.2% (range, 7.3–12.7%), but the globalfrequency for allergic rhinitis diagnosis was 5.5%(range, 3.6 –7.0%). Compared with the children, theadolescent group had a higher prevalence for eachcategory except for the diagnosis of allergic rhinitis(3.8%). These figures are in line with data reportedby others for allergic rhinitis in this region of LatinAmerica, which has the highest prevalence of aller-gic diseases in pediatric patients in the world.14
Table 3 shows the risk factors that were identified bylogistic regression analysis to be associated with allergicrhinitis symptoms. The main factors for increased risk(odds ratio [OR] � 1; p � 0.05) of symptoms of bothrhinitis or rhinoconjunctivitis (either current or previous)in 6- to 7-year-old children were asthma symptoms (cur-rent wheezing or wheezing in the last 12 months), symp-toms suggestive of eczema or diagnosed eczema, use ofacetaminophen in the 1st year of life or in the last 12months, and current maternal tobacco smoking. Simi-larly, the main factors for increased risk of symptoms ofrhinitis or rhinoconjunctivitis (either current or previous)
Table 1 Prevalence of rhinitis (accumulated, current) and rhinoconjunctivitis (current) symptoms andrhinoconjunctivitis diagnosis (ever) in children 6–7 years old and adolescents 13–14 years old from fournorthern Mexican centers, according to the International Study of Asthma and Allergies in Childhood, PhaseIIIB, 2001–2003
Rhinitis Symptoms byCategory, Center, and Age
Children 6–7 yr Old Adolescents 13–14 yr Old
n n Prevalence(%)
LowerLimitsCI (%)
UpperLimitsCI (%)
n n Prevalence(%)
LowerLimitsCI (%)
UpperLimitsCI (%)
Rhinitis symptoms everMonterrey 799 2.973 26.9 25.3 28.5 1271 2.966 42.9 41.1 44.6Ciudad Victoria 638 2.602 24.5 22.9 26.2 1417 3.121 45.4 43.7 47.1Mexicali 762 2.468 30.9 29.1 32.7 1334 2.967 45.0 43.2 46.8Tijuana 839 2.849 29.4 27.8 31.1 1283 3.245 39.5 37.9 41.2
Current rhinitis symptomsMonterrey 679 2.973 22.8 21.3 24.3 955 2.966 32.2 30.5 33.9Ciudad Victoria 553 2.602 21.3 19.7 22.8 1093 3.121 35.0 33.3 36.7Mexicali 695 2.468 28.2 26.4 29.9 1233 2.967 41.6 39.8 43.3Tijuana 697 2.849 24.5 22.9 26.0 902 3.245 27.8 26.3 29.3
Current rhinoconjunctivitissymptoms
Monterrey 252 2.973 8.5 7.5 9.5 402 2.966 13.6 12.3 14.8Ciudad Victoria 190 2.602 7.3 6.3 8.3 616 3.121 19.7 18.3 21.1Mexicali 313 2.468 12.7 11.4 14.0 862 2.967 29.1 27.4 30.7Tijuana 233 2.849 8.2 7.2 9.2 359 3.245 11.1 10.0 12.1
Rhinoconjunctivitisdiagnosis
Monterrey 201 2.973 6.8 5.9 7.7 138 2.966 4.7 3.9 5.4Ciudad Victoria 93 2.602 3.6 2.9 4.3 91 3.121 3.0 2.4 3.6Mexicali 172 2.468 7.0 6.0 8.0 41 2.967 1.4 1.0 1.8Tijuana 131 2.849 4.6 3.8 5.4 197 3.245 6.1 5.2 6.9
Allergy and Asthma Proceedings e55
DO NOT C
OPY
Delivered by Publishing Technology to: Hinari - Cameroon IP: 190.221.48.174 On: Sat, 04 Sep 2010 16:19:41Copyright (c) Oceanside Publications, Inc. All rights reserved.
For permission to copy go to www.copyright.com
for 13- to 14-year-old children were current or previoussymptoms of asthma, symptoms suggestive of eczema ordiagnosed eczema (current or previous), use of acetamin-ophen in the last 12 months, and the presence of at leastone tobacco smoker at home.
We found no relationship between rhinitis and theuse of antibiotics in the 1st year of life. Interaction witholder siblings resulted in a decreased risk of diagnosisof allergic rhinitis in children but not in adolescents. Inadolescents, no protective factors were associated witha lower risk of rhinitis symptoms.
DISCUSSIONEnvironmental factors and lifestyle appear to be
important in the expression of allergic diseases.7 Thisstudy is the first to explore risk factors for allergicrhinitis in a pediatric population in northern Mexicousing standardized methodology (the ISAAC study).Others have reported that the gross national productper capita (GNPpc) can be a confounding factor thatshould be considered when analyzing epidemiolog-ical studies of allergic diseases,15 especially in stud-ies that analyze populations from countries with
Table 2 Prevalence of rhinitis symptoms (accumulated, current), rhinoconjunctivitis symptoms (current), andallergic rhinitis diagnosis (ever) in children 6–7 yr old and adolescents 13–14 yr old, by gender, from fournorthern Mexican centers according to International Study of Asthma and Allergies in Childhood, PhaseIIIB, 2001–2003
Symptoms Prevalence by Category n n Prevalence (%) Lower LimitCI 95%
Upper LimitCI 95%
Children 6–7 yr oldRhinitis symptoms ever
Male 1569 5470 28.7 27.5 29.9Female 1469 5422 27.1 25.9 28.3Global 3038 10,892 27.9 26.2 29.6
Rhinitis symptoms in last 12 moMale 1372 5470 25.1 23.9 26.2Female 1252 5422 23.1 22.0 24.2Global 2624 10,892 24.2 22.6 25.8
Rhinoconjunctivitis symptoms in last 12 moMale 511 5470 9.34 8.57 10.11Female 477 5422 8.80 8.04 9.55Global 988 10,892 9.2 8.1 10.2
Allergic rhinitis diagnosisMale 340 5470 6.2 5.6 6.9Female 257 5422 4.7 4.2 5.3Global 597 10,892 5.5 4.6 6.3
Adolescents 13–14 yr oldRhinitis symptoms ever
Male 2513 6017 41.8 40.5 43.0Female 2792 6282 44.4 43.2 45.7Global 5305 12,299 33.3 32.0 34.6
Rhinitis symptoms in last 12 moMale 1980 6017 32.9 31.7 34.1Female 2203 6282 35.1 33.9 36.2Global 4183 12,299 34.1 32.5 35.8
Rhinoconjunctivitis symptoms in last 12 moMale 1976 21,784 16.9 15.9 17.8Female 3441 38,098 19.5 18.5 20.4Global 6405 70,774 18.2 17.5 18.9
Allergic rhinitis diagnosisMale 228 6017 3.8 3.3 4.3Female 239 6282 3.8 3.3 4.3Global 467 12,299 3.8 3.1 4.4
e56 July–August 2010, Vol. 31, No. 4
DO NOT C
OPY
Delivered by Publishing Technology to: Hinari - Cameroon IP: 190.221.48.174 On: Sat, 04 Sep 2010 16:19:41Copyright (c) Oceanside Publications, Inc. All rights reserved.
For permission to copy go to www.copyright.com
different GNPpc’s. In 2003, the GNPpc of Mexicowas US$6230.00, which places it in the group ofcountries with an upper-middle income.16 Althoughthe GNPpc varies greatly from state to state in Mex-ico, the individuals included in this study were fromstates in which the GNPpc’s are similar and higherthan the national average,17 ruling out this potentialbias. In our study population, a greater percentage ofadolescents had current or previous symptoms of rhinitisand diagnoses of allergic rhinitis compared with theyounger age group. The tendency for the prevalence ofallergic rhinitis to increase with age has been shown inother longitudinal studies of the natural history of thedisease.18 Although, the underlying cause is unknown,this could be caused by increased exposure to allergensover the years19 with the subsequent development ofallergic rhinitis.
When we performed a comparative analysis of thefour centers, Ciudad Victoria had the lowest percent-age of children 6 –7 years of age with symptoms ofrhinoconjunctivitis (7.3%), and Tijuana had the low-est percentage of adolescents with symptoms of rhi-noconjunctivitis (11.1%). The highest rates were re-ported in Mexicali for both age groups (12.7% forchildren and 29.1% for adolescents). These datashowed considerable variation, particularly for ado-lescents. In a previous study, the relationship ofsome climatic factors and the prevalence of allergicdiseases around the world were analyzed using dataobtained from ISAAC Phase I. A positive relation-ship was found between asthma and the estimatedaverage annual relative humidity, and a negativerelationship was found between asthma and altitudeand annual variation of outdoors temperature andhumidity. A positive correlation with latitude and anegative correlation with annual outside averagetemperature were found for the prevalence of ec-zema. However, there was no significant associationwith any climatic factor for rhinitis symptoms.20
Some of the climatic characteristics of the study cen-ters and the corresponding rhinoconjunctivitis symp-tom frequencies are shown in Table 4.21,22 Mexicali isnotable in that it reported higher rates of rhinoconjunc-tivitis in both groups of subjects and has the lowestaltitude of the included centers. In children, the nexthighest rate was in Monterrey, and the third highestwas in Tijuana. Because Monterrey and Ciudad Victo-ria are at very different altitudes than Mexicali, therewas no relationship between altitude and the preva-lence of rhinoconjunctivitis in this study. However,other climatic factors, such as average annual insidetemperature, outside temperature, inside relative hu-midity, etc., were not studied, and their impact onallergic rhinitis should not be ruled out. The results ofthe ISAAC Phase III in 21 Brazilian centers showed asignificant negative association between latitude and
physician-diagnosed asthma and atopic eczema, par-ticularly among adolescents. However, that study didnot find any relationship between climatic factors andallergic rhinitis symptoms,23 which is in agreementwith the international analysis report of ISAAC PhaseIII. The close relationship of allergic diseases appearsto be related to common genetic and environmentalfactors; however, current evidence shows that climaticfactors affect allergic symptoms in different ways. Fur-ther research is needed, especially for allergic rhinitis.
A study of children in the northern area of MexicoCity by Del Rio Navarro et al. reported a twofoldgreater prevalence of rhinoconjunctivitis symptoms inchildren 6–7 years of age than what we found (20.3%versus 9.2%).13 In addition, the report of the globalprevalence of rhinoconjunctivitis symptoms in infancy,based on data from ISAAC Phase III,14 showed sub-stantial differences in frequencies at centers within thesame country, just as we observed in Mexico. In termsof global variation in the prevalence and severity ofasthma symptoms, the ISAAC Phase III report alsonoted some differences at centers in the countries,24
although these differences were not so marked. Thereason for this variability is currently unknown. Be-cause the findings are similar in different parts of theworld, there does not seem to be methodological bias;however, a different investigator collected the data atevery center, which is a potential source of bias. It ispossible that interactions between genetic and environ-mental factors result in a wide range of clinical symp-toms, even in a population with the same ethnic back-ground. Additional studies are needed to determinethe underlying causes of prevalence variation found incenters within a country, especially in studies withmethodology similar to that used in ISAAC Phase II.
The prevalence of nasal and ocular symptoms meritsspecial attention, because this is the best predictor ofallergic rhinitis.18 In our series, the prevalence of rhi-noconjunctivitis symptoms was in line with results ofprevious studies10,11 in children, but the prevalencewas twofold greater for adolescents. This discrepancymay be caused by differences in study design becausethe ISAAC methodology was followed incompletely inthe previous studies (the age of the included popula-tion was different). For comparison and to clarify thesedifferences, future studies must have the same design.The diagnosis of allergic rhinitis was low (4.6% in ourseries) considering the data for rhinoconjunctivitissymptoms, suggesting a high level of underdiagnosis.The original question in the ISAAC Phase IIIB surveythat related to this topic did not discriminate betweenprimary care doctors and specialists. The low numberof allergic rhinitis diagnoses agrees with the observa-tion that according to a global map from ISAAC PhaseIII, Latin America has one of the highest incidences ofsevere rhinoconjunctivitis. This may be related to poor
Allergy and Asthma Proceedings e57
DO NOT C
OPY
Delivered by Publishing Technology to: Hinari - Cameroon IP: 190.221.48.174 On: Sat, 04 Sep 2010 16:19:41Copyright (c) Oceanside Publications, Inc. All rights reserved.
For permission to copy go to www.copyright.com
Tab
le3
Rh
init
issy
mp
tom
s,rh
inoc
onju
nct
ivit
issy
mp
tom
s,an
dd
iagn
osis
ofal
lerg
icrh
init
isri
skfa
ctor
sb
yca
tego
ries
and
gen
der
,ob
tain
edw
ith
logi
stic
regr
essi
onm
odel
inch
ild
ren
6–7
yrol
dan
dad
oles
cen
ts13
–14
yrol
dfr
omfo
ur
nor
ther
nM
exic
ance
nte
rsac
cord
ing
toIn
tern
atio
nal
Stu
dy
ofA
sth
ma
and
All
ergi
esin
Ch
ild
hoo
d,P
has
eII
IB,2
001–
2003
pO
RC
I95
%�
CI
95%
�p
OR
CI
95%
�C
I95
%�
Rhi
niti
sev
erin
boys
6–7
yrol
dR
hini
tis
ever
inbo
ys13
–14
yrol
dW
heez
ing
ever
0.00
02.
52.
92.
1W
heez
ing
ever
0.00
03.
34.
22.
6C
urre
ntw
heez
ing
0.00
02.
63.
42.
0R
ash
ever
0.00
02.
22.
81.
7R
ash
ever
0.00
01.
92.
31.
5Po
tato
0.00
10.
80.
90.
7E
czem
ad
iagn
osis
ever
0.00
03.
04.
32.
0Fr
uit
0.00
31.
21.
41.
1C
urre
ntpa
race
tam
ol0.
000
1.4
1.6
1.2
Past
a0.
008
1.2
1.3
1.0
Rhi
niti
sev
erin
girl
s6–
7yr
old
Rhi
niti
sev
erin
girl
s13
–14
yrol
dC
urre
ntw
heez
ing
0.00
03.
94.
93.
1W
heez
ing
ever
0.00
03.
13.
92.
5E
czem
aev
er0.
000
2.5
3.6
1.8
Ras
hev
er0.
000
3.3
4.2
2.6
Past
ain
die
tla
stye
ar0.
022
0.9
1.0
0.8
Seaf
ood
0.00
01.
31.
51.
2Pa
race
tam
olfi
rst
year
0.00
01.
61.
81.
4B
utte
r0.
000
1.3
1.5
1.1
Para
ceta
mol
last
year
0.00
01.
31.
41.
1Fa
st-f
ood
0.00
00.
80.
90.
7A
ntib
ioti
csfi
rst
year
0.03
01.
21.
31.
0Sm
oker
s0.
001
1.1
1.2
1.0
Cur
rent
mat
erna
lsm
oke
0.00
41.
41.
71.
1M
arga
rine
0.00
30.
80.
90.
7C
urre
ntrh
init
isin
boys
6–7
yrol
dC
urre
ntrh
init
isin
boys
13–1
4yr
old
Whe
ezin
gev
er0.
000
1.9
2.3
1.6
Whe
ezin
gev
er0.
000
3.3
4.1
2.6
Cur
rent
whe
ezin
g0.
000
2.6
3.4
2.0
Ras
hev
er0.
000
2.3
2.9
1.8
Ast
hma
dia
gnos
isev
er0.
000
1.7
2.2
1.3
Seaf
ood
0.00
01.
21.
41.
1R
ash
ever
0.00
02.
12.
61.
7Po
tato
0.00
00.
80.
90.
7Pa
race
tam
olfi
rst
year
0.00
01.
41.
61.
2Sm
oker
s0.
000
1.2
1.2
1.1
Cur
rent
mat
erna
lsm
oke
0.03
61.
31.
61.
0Pa
race
tam
olla
stye
ar0.
001
1.2
1.4
1.1
Cur
rent
rhin
itis
ingi
rls
6–7
yrol
dC
urre
ntrh
init
isin
girl
s13
–14
yrol
dC
urre
ntw
heez
ing
0.00
04.
86.
13.
9W
heez
ing
ever
0.00
02.
53.
12.
0R
ash
ever
0.00
02.
32.
91.
9C
urre
ntw
heez
ing
0.00
11.
62.
11.
2Pa
race
tam
ofi
rst
year
0.00
01.
82.
11.
5R
ash
ever
0.00
02.
53.
12.
1A
ntib
ioti
csfi
rst
year
0.01
21.
21.
41.
0Se
afoo
d0.
000
1.4
1.5
1.3
Cur
rent
mat
erna
lsm
oke
0.02
11.
31.
61.
0B
utte
r0.
000
1.4
1.5
1.3
Cur
rent
rhin
ocon
junc
tivi
tis
inbo
ys6–
7yr
old
Cur
rent
rhin
ocon
junc
tivi
tis
inbo
ys13
–14
yrol
dW
heez
ing
ever
0.00
02.
02.
71.
5W
heez
ing
ever
0.00
03.
44.
12.
8C
urre
ntw
heez
ing
0.00
03.
44.
62.
4M
eat
0.00
00.
80.
90.
7R
ash
ever
0.00
03.
14.
02.
4Se
afoo
d0.
000
1.7
1.9
1.5
Para
ceta
mol
last
year
0.00
01.
41.
71.
2R
ice
0.00
01.
51.
71.
3C
urre
ntm
ater
nal
smok
e0.
010
1.5
2.0
1.1
Nut
s0.
000
1.4
1.6
1.2
e58 July–August 2010, Vol. 31, No. 4
DO NOT C
OPY
Delivered by Publishing Technology to: Hinari - Cameroon IP: 190.221.48.174 On: Sat, 04 Sep 2010 16:19:41Copyright (c) Oceanside Publications, Inc. All rights reserved.
For permission to copy go to www.copyright.com
Tab
le3
Con
tin
ued
pO
RC
I95%
�C
I95
%�
pO
RC
I95
%�
CI
95%
�
Cur
rent
rhin
ocon
junc
tivi
tis
ingi
rls
6–7
yrol
dC
urre
ntrh
inoc
onju
ncti
viti
sin
girl
s13
–14
yrol
dW
heez
ing
ever
0.00
02.
63.
71.
9W
heez
ing
ever
0.00
02.
43.
31.
7C
urre
ntw
heez
ing
0.00
02.
43.
61.
6R
ash
ever
0.00
03.
44.
42.
6C
urre
ntra
sh0.
000
3.0
4.5
2.0
Seaf
ood
0.00
01.
61.
91.
4Pu
lses
(bea
ns,p
eas)
0.00
20.
80.
90.
6B
utte
r0.
000
1.4
1.6
1.2
Para
ceta
mol
firs
tye
ar0.
001
1.7
2.3
1.2
Nut
s0.
000
1.4
1.7
1.2
Para
ceta
mol
last
year
0.00
02.
02.
51.
5Po
tato
0.00
00.
70.
80.
6O
lder
sibl
ings
0.00
61.
21.
31.
0Fa
st-f
ood
0.00
00.
70.
80.
6R
hino
conj
unct
ivit
isev
erin
boys
6–7
yrol
dR
hino
conj
unct
ivit
isev
erin
boys
13–1
4yr
old
Whe
ezin
gev
er0.
000
2.7
4.0
1.8
Cur
rent
whe
ezin
g0.
000
2.9
4.1
2.0
Cur
rent
whe
ezin
g0.
001
2.2
3.5
1.4
Ast
hma
ever
0.00
03.
04.
52.
0E
czem
ad
iagn
osis
ever
0.00
04.
57.
72.
6R
ash
ever
0.00
02.
12.
91.
5A
ntib
ioti
csfi
rst
year
0.00
21.
72.
41.
2E
czem
aev
er0.
000
4.0
7.0
2.3
Ter
tiar
ym
othe
red
ucat
ion
0.00
10.
50.
70.
3R
hino
conj
unct
ivit
isev
erin
girl
s6–
7yr
old
Rhi
noco
njun
ctiv
itis
ever
ingi
rls
13-
yrol
dW
heez
ing
ever
0.00
03.
34.
92.
3W
heez
ing
last
year
0.00
02.
13.
11.
5E
czem
aev
er0.
000
3.6
6.7
1.9
Ast
hma
ever
0.00
03.
55.
22.
4M
othe
rsm
okin
gla
stye
ar0.
032
1.9
3.5
1.1
Ras
hev
er0.
000
2.2
3.1
1.6
Ter
tiar
ym
othe
red
ucat
ion
0.04
40.
61.
00.
4E
czem
aev
er0.
000
6.6
10.8
4.0
Puls
es(b
eans
,pea
s)0.
051
0.8
1.0
0.6
Dog
inho
me
last
year
0.04
80.
71.
00.
6
Allergy and Asthma Proceedings e59
DO NOT C
OPY
Delivered by Publishing Technology to: Hinari - Cameroon IP: 190.221.48.174 On: Sat, 04 Sep 2010 16:19:41Copyright (c) Oceanside Publications, Inc. All rights reserved.
For permission to copy go to www.copyright.com
medical diagnosis and treatment. To improve our ap-proach to allergic diseases in childhood, we need toimprove medical knowledge at the primary care level.However, it is possible that the prevalence was over-estimated,25 because the ISAAC data were derivedfrom a questionnaire.
International variation in the prevalence of rhinitisand other allergic diseases and the relationship ofthis variation with seasonal and perennial allergens(using the ISAAC Phase II methodology),26 –28 wasanalyzed recently. Atopy could not explain all of thesymptoms, particularly in centers in countries withlower GNPpc’s. This emphasizes the need to increaseour knowledge of nonatopic factors in the expressionof allergic diseases, especially in subjects with symp-toms that are not usually related to atopy (e.g., rhi-nitis without ocular symptoms).
The phenotypes of allergic diseases such as asthmaand allergic rhinitis are closely related in terms oftheir epidemiology and are usually present in familygroups, suggesting shared etiology. This relation-ship is termed “chronic allergic respiratory syn-drome”29 and was evident in the pediatric popula-tion in this study: we found that the main risk factorfor the development of rhinitis was asthma symp-toms (current or past wheezing or an asthma diag-nosis). Conversely, the main risk factor for the de-velopment of asthma is allergic rhinitis.13,30,31 Thus,primary care physicians must be aware of the closerelationship of these diseases to ensure timely diag-nosis and treatment. Eczema (both symptoms and amedical diagnosis) was also identified as a risk factorfor the development of allergic rhinitis in both agegroups studied, supporting the concept of “atopicmarch.” Thus, eczema is related to a greater risk ofdeveloping allergic rhinitis and asthma in Mexican
children, as has been shown in other populations.32
Diverse environmental and lifestyle factors can con-tribute to the expression of allergic diseases, espe-cially during the 1st years of life; these factors in-clude diet, maternal smoking, obesity, exposure tomicrobes, allergens, pets in the home, and use ofantibiotics and acetaminophen.33–38
In our study population, the use of acetaminophen(during the first 12 months of life and within the last 12months) for treatment of infection-related fever wasassociated with a greater risk of rhinitis in both agegroups. Because of the cross-sectional nature of theISAAC Phase III design, we can not know if this drughas a causal effect or whether patients were treatedwith acetaminophen for their allergy symptoms, whichmay resemble symptoms of infection. A proposed eti-ologic mechanism for asthma is a depletion of gluta-thione in the lungs. At least in toxic doses, acetamino-phen metabolites bind irreversibly to glutathione,decreasing the ability to mitigate oxidative stress pro-duced by reactive oxygen species. This triggers a cas-cade of epithelial desquamation, edema, release of leu-kotrienes, bronchoconstriction, and inflammatory cellstimulation.36 Although it has not been shown whethera similar phenomenon occurs with rhinitis, the epide-miological evidence in this study supports a similarmechanism. This is in accordance with data from aprevious study in Mexico37 and with the global reportof ISAAC Phase III in children 6–7 years of age regard-ing the association of acetaminophen with the risk ofasthma, rhinoconjunctivitis, and eczema.38 Prospectivestudies are needed to evaluate the causal relationshipbetween acetaminophen and allergic diseases.
It is noteworthy that current maternal smoking or thepresence of at least one smoker in the home was pos-itively associated with symptoms of rhinitis and aller-
Table 4 Climatic conditions of four cities from northern Mexico and current rhinoconjunctivitis symptomsprevalence rates in children 6–7 yr old and adolescents 13–14 yr old, according to International Study ofAsthma and Allergies in Childhood, Phase IIIB: 2001–2003
City Location (latitudeand longitude)
Altitude(MASL)
OutdoorTemperature
OutdoorRelative
Humidity
CurrentRhinoconjunctivitis
Prevalence
6–7 yr 13–14 yr
Mexicali LN 30°53� 3 Maximum, 50°C 56% 12.7% 29.1%LO 115°66� Minimum, �5°C
Tijuana LN 32°31� 20 Maximum, 29°C 65% 8.2% 11.1%LO 117° Minimum, 12°C
Ciudad Victoria LN 23°44� 320 Maximum, 47°C 50% 7.3% 19.7%LO 99°07� Minimum, 0–4°C
Monterrey LN 23°11� 537 Maximum, 41°C 56% 8.5% 13.6%LO 101°14� Minimum, 1.1°C
MASL � meters above sea level.
e60 July–August 2010, Vol. 31, No. 4
DO NOT C
OPY
Delivered by Publishing Technology to: Hinari - Cameroon IP: 190.221.48.174 On: Sat, 04 Sep 2010 16:19:41Copyright (c) Oceanside Publications, Inc. All rights reserved.
For permission to copy go to www.copyright.com
gic rhinitis, especially in children. Other reports haveindicated a causal relationship between exposure totobacco smoke during pregnancy and early infancyand allergic diseases, especially asthma.7 The proposedmechanism is that tobacco smoke reduces �1-antitryp-sin, a lung protease that blocks normal inactivation ofallergenic house-dust mite proteases in the airways.This results in an increased risk of sensitization to theseallergens.7
The ISAAC questionnaire includes data related tofoods in the diet. In our series, margarine intake wasassociated with rhinitis symptoms in children as wellas adolescents (OR � 1.18 in both groups). Potatointake had a negative relationship (OR � 0.88) withrhinitis only in adolescents. These observations con-trast with those of Ellwood et al.,39 who found that theprevalence of asthma, rhinitis, and eczema was in-versely related to starch, cereal, and vegetable intake.However, because the ISAAC Phase I and III studiesare both based on a cross-sectional survey, this obser-vation is subject to several types of bias. Thus, thecurrent information has many limitations and must beverified in studies that use a different methodology.
This study has several limitations. Data were col-lected using a questionnaire, so the responses de-pended in part on the subject’s or parent’s memory.This could introduce bias, and the prevalence must beconsidered an estimate. Longitudinal studies and stud-ies using other diagnostic parameters are needed toconfirm the results of this cross-sectional study. Inaddition, the ISAAC Phase III study can not discrimi-nate between atopic disease and related nonatopic dis-eases, such as rhinitis, especially in countries such asMexico where the income varies widely in the popu-lation and where nonatopic factors may be important.
Despite its limitations, this study helps establishthe prevalence of rhinitis and other childhood aller-gic diseases in children and adolescents in Mexicoand identifies environmental elements that may af-fect the expression of allergic diseases. This informa-tion is valuable in that it encourages timely diagnosisand treatment of allergic diseases by primary carephysicians. It also suggests preventive measures thatcan be taken to protect children from developingallergic rhinitis, such as changes in the child’s envi-ronment.
ACKNOWLEDGMENTSThe authors thank Paul Kretchmer, Managing Director of San
Francisco Edit, for his support in reviewing the English translation ofthis article.
REFERENCES1. Settipane RA. Rhinitis: A dose of epidemiological reality. Al-
lergy Asthma Proc 24:147–154, 2003.
2. Gupta R, Sheik A, Strachan DP, and Anderson HR. Time trendsin allergic disorders in the UK. Thorax 62:91–96, 2007.
3. ISAAC Phase Three Manual. Auckland, New Zealand: ISAACInternational Data Centre, July 2000. Available online at www.isaac.auckland.ac.nz; last accessed May 28, 2010.
4. Innes Asher M, Montefort S, Bjorksten B, et al. Worldwide timetrends in the prevalence of symptoms of asthma, allergic rhi-noconjunctivitis, and eczema in childhood: ISAAC phases oneand three repeat multicountry cross-sectional surveys. Lancet368:733–743, 2006.
5. Weiland SK, Bjorksten Bengt, Brunekreef B, et al. Phase II of theInternational Study of Asthma and Allergies in Childhood(ISAAC II): Rationale and methods. Eur Respir J 24:406–412,2004.
6. Bjorksten B, Clayton T, Ellwood P, et al., and the ISAAC PhaseIII Study Group. Worldwide time trends for symptoms of rhi-nitis and conjunctivitis: Phase III of the international study ofasthma and allergies in childhood. Pediatr Allergy Immunol19:110–124, 2008.
7. Nolte H, Backer V, and Porsbjerg C. Environmental factors as acause for the increase in allergic disease. Ann Allergy AsthmaImmunol 87(suppl):7–11, 2001.
8. Wright AL. The epidemiology of the atopic child: Who is at riskfor what? J Allergy Clin Immunol 113:S2–S7, 2004.
9. Hersoug LG, and Linneberg A. The link between the epidemicsof obesity and allergic diseases: Does obesity induce decreasedimmune tolerance? Allergy 62:1205–1213, 2007.
10. Tatto-Cano MI, Sanín-Aguirre LH, Gonzalez V, et al. Prevalen-cia de asma, rinitis y eczema en escolares de la ciudad deCuernavaca, Mexico. Salud Publica Mex 39:497–506, 1997.
11. Barraza-Villarreal A, Hernandez-Cadena L, Moreno-Macias H,et al. Trends in the prevalence of asthma and other allergicdiseases in schoolchildren from Cuernavaca, Mexico. AllergyAsthma Proc 28:368–374, 2007.
12. Villarreal AB, Sanín-Aguirre LH, Tellez-Rojo MM, et al. Riskfactors for asthma in school children from Ciudad Juarez, Chi-huahua. J Asthma 40:413–423, 2003.
13. Del-Río-Navarro BE, Luna-Pech JA, Berber A, et al. Factorsassociated with allergic rhinitis in children from northern Mex-ico City. J Investig Allergol Clin Immunol 17:77–84, 2007.
14. Aït-Khaled N, Pearce N, Anderson HR, et al. Global map of theprevalence of symptoms of rhinoconjunctivitis in children: TheInternational Study of Asthma and Allergies in Childhood(ISAAC) Phase Three. Allergy 64:123–148, 2009.
15. Stewart AW, Mitchell EA, Pearce N, et al. The relationship ofper capita gross national product to the prevalence of symp-toms of asthma and other atopic diseases in children (ISAAC).Int J Epidemiol 30:173–179, 2001.
16. World Bank, Classification of economies 2002. Available onlineat www.siteresources.worldbank.org/INTRGEP2004/Resources/classification.pdf; last accessed August 13, 2009.
17. Instituto Nacional para la Evaluacion de la Educacion, Pan-orama educativo de Mexico 2003. Available online at www.inee.edu.mx/tei/file/%5Cusr/local/tei2/repositorio/contenido/2005/PanoramaEducativoDeMexico/CS/CS08/2005_CS08_.pdf?index�main; last accessed September 20, 2009.
18. Greisner WA, Settipane RJ, and Settipane GA. Natural historyof hay fever: A 23-year follow-up of college students. AllergyAsthma Proc 19:271–275, 1998.
19. Peroni DG, Piacentini GL, Alfonsi L, et al. Rhinitis in pre-schoolchildren: Prevalence, association with allergic diseases and riskfactors. Clin Exp Allergy 33:1349–1354, 2003.
20. Weiland SK, Husing A, Strachan DP, et al., and The ISAACPhase I Study Group. Climate and the prevalence of symptomsof asthma, allergic rhinitis and atopic eczema in children. OccupEnviron Med 61:609–616, 2004.
Allergy and Asthma Proceedings e61
DO NOT C
OPY
Delivered by Publishing Technology to: Hinari - Cameroon IP: 190.221.48.174 On: Sat, 04 Sep 2010 16:19:41Copyright (c) Oceanside Publications, Inc. All rights reserved.
For permission to copy go to www.copyright.com
21. Tu tiempo Network, S.L. El Tiempo en Mexico. Available onlineat www.tutiempo.net/tiempo/Mexico/MX.html; last accessedSeptember 20, 2009.
22. Molina Jose JC. La humedad relativa en los Estados UnidosMexicanos. Universidad de Granada. Available online at www.dialnet.unirioja.es; last accessed January 10, 2009.
23. Sole D, Wandalsen GF, Camelo-Nunes IC, Naspitz CK, andISAAC grupo Brasileiro. Prevalence of Symptoms of asthma,rhinitis and atopic eczema among Brazilian children and ado-lescents identified by International Study of Asthma and Aller-gies in Childhood (ISAAC)-Phase III. J Pediatr (Rio J) 82:341–346, 2006.
24. Lai CKW, Beasley R, Crane J, et al. Global variation in theirprevalence and severity of asthma symptoms: Phase Three ofthe International Study of Asthma and Allergies in Childhood(ISAAC). Thorax 64:476–483, 2009.
25. Bousquet J, Khaltaev N, Cruz AA, et al. Allergic Rhinitis and itsImpact on Asthma (ARIA) 2008 update. Allergy 63(suppl 86):8–160, 2008.
26. Weinmayr G, Forastiere F, Weiland SK, et al. Internationalvariation in prevalence of rhinitis and its relationship withsensitisation to perennial and seasonal allergens. Eur Respir J32:1250–1261, 2008.
27. Weinmayr G, Weiland SK, Bjorksten B, et al. Atopic sensitiza-tion and the international variation of asthma symptom preva-lence in children. Am J Respir Crit Care Med 176:565–574, 2007.
28. Flohr C, Weiland SK, Weinmayr G, et al. The role of atopicsensitization in flexular eczema: Findings from the internationalstudy of asthma and allergies in childhood phase two. J AllergyClin Immunol 121:141–147, 2008.
29. Togras A. Rhinitis and asthma: Evidence for respiratory systemintegration. J Allergy Clin Immunol 111:1171–1183, 2003.
30. Del-Rio-Navarro B, Berber A, Blandon-Vijil V, et al. Identifica-tion of asthma risk factors in Mexico City in an InternationalStudy of Asthma and Allergy in Childhood survey. AllergyAsthma Proc 27:325–333, 2006.
31. Riedinger F, Kuehr J, Strauch E, et al., and the Ozone WorkingGroup. Natural history of hay fever and pollen sensitization,and doctor’s diagnosis of hay fever and pollen asthma in Ger-man schoolchildren. Allergy 57:488–492, 2002.
32. Gustafsson D, Sjoberg O, and Foucard T. Development of aller-gies and asthma in infants and young children with atopicdermatitis—A prospective follow up to 7 years. Allergy 55:240–245, 2000.
33. Asher MI, Montefort S, Bjorksten B, et al. Worldwide timetrends in the prevalence of symptoms of asthma, allergic rhi-noconjuntivitis, and eczema in childhood: ISAAC Phases Oneand Three repeat multicountry cross-sectional surveys. Lancet368:733–743, 2006.
34. Hijazi N, Abalkhail B, and Seaton A. Diet and childhood asthmain a society in transition: A study in urban and rural SaudiArabia. Thorax 55:775–779, 2000.
35. Marra F, Lynd L, Coombes M, et al. Does antibiotic exposureduring infancy lead to development of asthma? Chest 129:610–618, 2006.
36. Eneli I, Sadri K, Camargo C, and Barr G. Acetaminophen andthe risk of asthma. Chest 127:604–612, 2005.
37. Barragan-Meijueiro MM, Morfín-Maciel B, and Nava-OcampoAA. A Mexican population-based study on exposure to parac-etamol and the risk of wheezing, rhinitis and eczema in child-hood. J Investig Allergol Clin Immunol 16:247–252, 2006.
38. Beasley R, Clayton T, Crane J, et al. Association betweenparacetamol use in infancy and childhood, and risk ofasthma, rhinoconjunctivitis, and eczema in children aged 6 –7years: Analysis from phase three of the ISAAC programe.Lancet 372:1039 –1048, 2008.
39. Ellwood P, Asher MI, Bjorksten B, et al. Diet and asthma,allergic rhinoconjunctivitis and atopic eczema symptom prev-alence: An ecological analysis of the international study ofasthma and allergies in childhood (ISAAC) data. Eur Respir J17:436–443, 2001. e
e62 July–August 2010, Vol. 31, No. 4
DO NOT C
OPY