Research ArticleldquoEffects of Tobacco Smoke on Aeroallergen Sensitization andClinical Severity among University Students and Staff withAllergic Rhinitisrdquo

Theerapan Songnuy 1 Stephen J Scholand2 and Sarawut Panprayoon3

1Department of Clinical Medical Science Walailak University School of Medicine Nakhon Si ammarat 80160 ailand2Department of Medicine University of Arizona Tucson AZ 85724 USA3Department of Social Medicine Walailak University Hospital Nakhon Si ammarat 80160 ailand

Correspondence should be addressed to eerapan Songnuy theerapansowuacth

Received 12 June 2020 Revised 17 September 2020 Accepted 24 September 2020 Published 8 October 2020

Academic Editor Felix Broecker

Copyright copy 2020 eerapan Songnuy et al is 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 isproperly cited

Allergic diseases affecting a variety of organs have continuously increased both in developed and developing countries Tobaccosmoke exposure increases prevalence of allergic rhinitis (AR) and may affect allergic sensitization is study was designed tocompare indoor-aeroallergen sensitization between those not exposed and exposed to tobacco smoke in university students andstaff with allergic rhinitis A cross-sectional descriptive study among university students and staff with allergic rhinitis wasperformed from February 1 2018 to March 31 2019 Questionnaires regarding demography clinical symptoms and tobaccosmoke exposure were implemented A current smoker was defined as using at least 1 cigarette per day for at least 1 month Asecondhand smoker was defined as the one who never smoked but lived with a current smoker at least for 1 month A skin pricktest for eight common indoor aeroallergens Dermatophagoides pteronyssinus Dermatophagoides farinae Periplaneta americanacat dander dog dander para grass careless weed and Cladosporium spp was performed Sensitization was defined as positivityto at least 1 aeroallergen One hundred and twenty-eight adult patients were eligible participants for the study and 68 cases(5310) were classified as having tobacco smoke exposure Among these most of them were secondhand smokers (50 cases7350) ere was no statistically significant difference between exposure and nonexposure to tobacco smoke and indooraeroallergen sensitization except for the Periplaneta americana antigen (p 0013) Most of those in the nonexposure group (34cases 5670) were classified as having intermittent allergic rhinitis whereas the tobacco exposure group had significantly moreprevalence of severe clinical symptoms In conclusion tobacco smoke exposure did not appear to have much influence onaeroallergen sensitization for 7 of the 8 antigens examined However for the Periplaneta americana antigen there was a highlysignificant correlation with patients experiencing worsened allergic rhinitis symptoms Overall it was observed that allergicrhinitis patients exposed to tobacco smoke had more severe clinical symptoms Future studies should look for other potentialantigens of interest such as mould Implementation of public health practices reducing exposure to tobacco smoke could havebenefits in allergic rhinitis patients

1 Introduction

Stimulation of allergic diseases affects a variety of organsystems including respiratory gastrointestinal and der-matological as a result of the pathophysiology Symptomscan affect patients in many ways including the nasal mucosa(rhinorrhea and sneezing) conjunctiva (itching and wateryeyes) respiratory mucosa (cough bronchospasm and

asthma) gastrointestinal tract (nausea abdominal pain anddiarrhea) and skin (rashes hives and urticaria) Epidemi-ologic data show that allergic diseases have continuouslyincreased both in developed and developing countries [1]e prevalence of asthma and allergic rhinitis (AR)according to the recent WHO statistics comprises 334 and400 million patients respectively [1 2] e prevalence ofatopic dermatitis (AD) has increased in Europe Mideast

HindawiJournal of Environmental and Public HealthVolume 2020 Article ID 1692930 7 pageshttpsdoiorg10115520201692930

Asia and Africa [3] In the US food allergy prevalenceappears to increase as well with 1ndash10 of adults and 8 ofchildren being affected [4 5] Different definitions of foodallergy categories of food and inclusion and diagnosticcriteria all affect different estimates of disease prevalence [6]

Direct and indirect negative impacts of AR include acuteand chronic sinusitis otitis media sleep disruption con-centration difficulties and behavioural disturbances [7]ere is overlap in the allergic disease spectrum with manyasthmatic patients suffering from coincident AR [8] Af-fected patients experience a decreased quality of life [9 10]Some examples include increased school or work absenceand increased health-care expenditures In 2003 the esti-mated total cost related to AR in the US ranged from 2 to 5billion US dollars [11] Data in 2011 in the UK showed thatthe total cost of asthma was 11 billion pounds [12]Moreover indirect costs including loss of work day anddecreased productivity are problematic for national eco-nomic and social development [13ndash16]

Clinical evaluation of patients through history andthorough physical examination are themain components formaking the diagnosis in allergic diseases Specific investi-gations are needed in confirmative diagnoses (ie a skinprick test or blood tests for specific IgE response to aero-allergens) [17ndash19] Normally in primary care settings thephysician does not rely on specific investigations but usuallydepends on the clinical information especially for children[20] If affected patients do undergo testing for specificaeroallergens avoidance measures are advised us thelevels of disease control could be improved with morewidespread testing and as a result the utilization of med-ications for symptom control would be optimized [21] Inthe general population the skin prick testing is a benefit fordefining sensitization If a sensitized individual adapts to hisher indoor environment the chance of clinical allergysymptoms in the future would be decreased [22ndash24] Apopulation-based case control study in Finland [25] revealedthat indoor-aeroallergen sensitization in allergic asthma was5500 whereas it was 3900 in the control group In 2009indoor-aeroallergen sensitization among ai asthmaticchildren showed that 4850 were positive to Dermato-phagoids pteronyssinus and Dermatophagoids farinae while2630 were positive to Periplaneta americana and 710were positive to cat dander [26] In asymptomatic indi-viduals 4200 were positive to at least one aeroallergen[27] Most of them were sensitized to two indoor aero-allergens house dust mite and cockroach antigen

As shown from many previous studies tobacco smokeexposure increases the prevalence of allergic rhinitis [28 29]In addition it also influences sensitization of both food andaeroallergens [30] Some studies showed that tobacco smokeexposure increased sensitization [31ndash33] On the other handa lot of researchers found an inverse impact [28 29 34 35]

In daily practice if physicians can investigate for specificinformation on the state of sensitization among their allergicrhinitis patients it may help optimize their managementFor example patients may adopt avoidance measures orundergo allergen immunotherapy Exposure to tobaccosmoke may further harm these patients through

sensitization to various aeroallergens Hence this study aimsto compare indoor-aeroallergen sensitization in adults withAR between those not exposed and exposed to tobaccosmoke

2 Materials and Methods

21 Study Design and Sample Size We performed a cross-sectional descriptive analytic study of indoor aeroallergensensitization among university students and staff with AR inthose exposed and not exposed to tobacco smoke Werecruited eligible participants from February 1 2018 toMarch 31 2019 at an out-patient department at WalailakUniversity Hospital Nakhon Si ammarat ailand Bycalculation we used the formula for study the differencebetween 2 independent variables for numerical data asfollows [36]

n Zα2

2P(1 minus P)

1113968+ Zβ

p1 1 minus p1( 1113857

1113969

+ p2 1 minus p2( 111385711138751113876 11138772

p1 minus p2( 11138572

(1)

where n sample size for each group p1 proportion part 1(prevalence of aeroallergen sensitization in the tobaccoexposure group with allergic rhinitis 067 (house dustmite) [37] and p2 proportion part 2 (prevalence of aer-oallergen sensitization in nontobacco exposure group withallergic rhinitis 037 (house dust mite) [37] P (p1 + p2) 2 (067 + 037) 2 052 Zα2 α 005 (two-tailed) 196and Zβ β 01 (one-tailed) 128

e calculated sample size was 5575 (56) per groupOverall we included 128 participants eligible for

enrolment is study was approved by the committee of theInstitutional Review Board (IRB) of Walailak University(Approval Number WUEC-18-016-01)

22 Eligibility Criteria One hundred and twenty-eightparticipants met the inclusion criteria of adults with AR atWalailak University (staff or current students) during thestudy period All of these were previously diagnosed as AR orhad developed a clinical history of AR at least 12 monthsprior based on the ARIA guidelines [38] and accepted theperformance of skin prick testing e exclusion criteriaincluded individuals who currently used antihistamines orrelated medications within 7 days prior to enrolment hadactive skin lesions such as urticaria eczema and impetigodermatographism uncontrolled asthma HIVAIDs hepa-titis B and hepatitis C or were unwilling to be a participantWritten informed consent was obtained from all partici-pants before enrolment in the study

Demographic and clinical data were collected using aquestionnaire AR severity was classified as follows Inter-mittent was defined as symptoms are present for lt4 days aweek or for lt4 consecutive weeks Persistent was defined assymptoms are present more than 4 days a week and for morethan 4 consecutive weeks Moderatesevere persistent wasdefined as one or more of the following items are presentwith troublesome symptoms such as sleep disturbance

2 Journal of Environmental and Public Health

impairment of daily activities leisure andor sport andimpairment of school or work In mild persistent the patienthad only a small amount of symptoms without troubles [39]e status of tobacco smoke exposure was defined as acurrent smoker secondhand smoker current smoker livingwith an active smoker and nonexposure A current smokerwas defined as an individual who smoked at least 1 ciga-retteday for at least 1 month in the previous year beforeenrolment A secondhand smoker was defined as a nonactivesmoker who reported living with ge1 smokers in the past 1month or longer Nonexposure was defined as neversmoking in their lifetime and not living with a currentsmoker [35]

23 SkinPrickTest e skin prick testing with eight commonindoor aeroallergens was performed including Dermato-phagoides pteronyssinus Dermatophagoides farinae Peri-planeta americana cat dander dog dander para grasscareless weed and Cladosporium spp All standard allergenextract panels were used (Greater Pharma Nakhon Phathomailand) Positive and negative controls including histamineand glycerinated phenol-saline respectively were used eskin prick testing was performed on the volar surface of theforearm and skin reactions were evaluated 15 minutes afterthe application of the skin test Positive test results weredefined as a reaction of redness and wheal as per the worksDogru et al andHosseini et al [40 41] Individuals who had apositive test for at least one aeroallergen were defined asallergen sensitization and further processed for data analysis

24 Statistical Analyses Categorical and numerical data forthe demography of all participants were described usingfrequency () mean (plusmnSD) and range Tobacco exposureand clinical data used frequency () and mean (plusmnSD)Statistical association between the tobacco smoke exposurestatus and allergen sensitization and clinical severity of ARutilized the Chi-square test All statistical analyses of thedemographic and clinical characteristics data were per-formed using PSPP version 120 (2016 Free SoftwareFoundation Inc) e p value of lt005 was considered to bestatistically significant

3 Results

31 Demographic Characteristics of Participants is studywas performed from February 1 2018 to March 31 2019 atWalailak University Hospital out-patient department Onehundred and twenty-eight AR patients were eligible par-ticipants for the study e mean age was 2222plusmn 722 yearsand 7110wasmaleemean BMI was 2246plusmn 425 kgm2One hundred and sixteen (9060) participants werebachelorrsquos degreediploma and most of all participants wereuniversity students (8980) (Table1)

32 Tobacco Smoke Exposure and Clinical Data Sixty par-ticipants (4690) were tobacco nonexposure e sec-ondhand smoker current smoker and current smoker living

with active smoker were 3910 850 and 550 re-spectively Only 48 participants (3750) were previouslydiagnosed as AR by physician e most common comor-bidity was atopic dermatitis (1800) Oral antihistaminewas the most common medication used by participants(Table 2)

33 Sensitization to Aeroallergens in Tobacco Smoke Exposureand Nonexposure Sensitization to eight aeroallergens inallergic rhinitis patients are shown in Table 3 Tobaccosmoke exposure affected more sensitization only in cock-roach (Periplaneta americana) aeroallergen compared tononexposure with statistical significance (p 0013) Forsubgroup analysis a current smoker had more prevalence ofsensitization to cat dander and Cladosporium spp than asecondhand smoker with p 0012 and 0002 respectively(data not shown)

34 Prevalence of the Tobacco Smoke Status and Severity ofAllergic Rhinitis From 60 nonexposure individuals most ofthem (5670) were classified as intermittent allergic rhi-nitis On the other hand tobacco smoke exposure patientswere distributed mostly in mild persistent allergic rhinitiswith 41cases (60 30) e tobacco exposure group wasshown to have more severe prevalence of clinical allergicrhinitis as compared to nonexposure with statistical sig-nificance (plt 0001) as shown in Figure 1

4 Discussion

Changes in the respiratory tract caused by exposure to to-bacco smoke have been well described [42] Tobacco smokecan directly affect the respiratory tract leading to thickeningof the lower airway walls impaired mucociliary clearanceand altered airway immune function is study aimed toexamine further the interface of allergic symptoms in AR

Table 1 Demographic characteristics of participants (n 128)

Characteristic Meanplusmn SD or n ()Age (year) 2222plusmn 722 (1600ndash5900)Weight (kg) 6428plusmn 1425 (4340ndash11500)Height (cm) 16887plusmn 770 (14800ndash18700)BMI (kgm2) 2246plusmn 425 (1653ndash3526)Male 91 (7110)Educational level

Junior high school 1 (080)High school 3 (230)Bachelorrsquos degreediploma 116 (9060)Masterrsquos degree and above 8 (630)

OccupationUniversity student 115 (8980)University staff 13 (1020)

Income of family (US$month)le600 31 (2420)601ndash1667 54 (4220)1668ndash3333 38 (2970)ge3334 5 (390)

lowastExchange rate Dec 15 2019

Journal of Environmental and Public Health 3

and tobacco smoke us we evaluated the associationbetween tobacco smoke exposure and allergic sensitizationand severity of allergic rhinitis adult patients

After performing skin prick testing in tobacco smokeexposure and nonexposure allergic rhinitis patients we foundthat only cockroach (Periplaneta americana) antigen from apanel of eight aeroallergens yielded higher rates of positivitywhereas the other seven aeroallergens showed no statisticallysignificant differences Many reports have shown that tobaccosmoke increased allergen sensitization among allergic rhinitispatients [31ndash33] However some reports have shown aninverse effect of tobacco smoke on sensitization [29 34 35]For example in a US adult population cross-sectional study areverse relationship between tobacco smoke and inhaledallergen sensitization was found [28] Without doubt theissue is complex and may relate to a number of factors Onefactor could be the timing of exposure to tobacco smoke as a

recent systematic and meta-analysis study showed that earlylife exposure to environmental tobacco smoke increased therisk of sensitization [43] e present study did not definetobacco exposure duration long enough hence the effect oftobacco smoke on allergens sensitization yielded mostlyinsignificant

As consistent with many previous reports [29 34] thepresent study demonstrated that tobacco smoke exposureled to worsened clinical severity in allergic symptomscompared to the nonexposure group Rhinomanometry inone study examining the effect of tobacco smoke on severityof symptoms in perennial allergic rhinitis patients showedincreased nasal resistance a correlate of worsened inflam-mation [44] Another study found that exposure to tobaccosmoke among allergic rhinitis patients did not change se-verity of disease [45]

It remains to be seen whether the pathophysiologicmechanisms between smoking and IgE-mediated allergicsensitization may be distinct from those between smokingand severity of allergic rhinitis e skin prick testing mightnot be affected by exposure to tobacco smoke

e present study has some limitations including a lackof quantitative measurement for the level of tobacco ex-posure both in current smokers and secondhand smokers Inaddition the severity of allergic rhinitis was classified mainlyby history and clinical manifestations without objectivemeasurement Future research should include history ofcigarette use per day length of time that a secondhandsmoker is exposed to smoking as well as cotinine analyses inblood urine or even hair as a marker of exposure [46] Inaddition rhinomanometry may be useful for assessing real-time nasal conditions in the participants Finally testing ofother aeroallergens particularly moulds would be worth aninvestigation

Table 2 Tobacco smoke exposure and clinical data (n 128)

Parameters Meanplusmn SD or n ()Tobacco exposureNonexposure 60 (4690)Secondhand smoker 50 (3910)Current smoker 11 (860)Current smoker living with active smoker 7 (550)

AR diagnosisPrevious diagnosis by physician 48 (3750)First AR diagnosis 80 (6250)

ComorbidityAD 23 (1800)Asthma 17 (1330)Food allergy 14 (1090)Allergic conjunctivitis (AC) 13 (1020)Anaphylaxis 4 (310)Otherslowast 14 (1090)

Current medicationOral antihistamine 36 (2810)Normal saline irrigation 20 (1560)Intranasal corticosteroid 10 (780)Leukotriene receptor antagonist 5 (390)Intranasal decongestant 4 (310)

Other lowastInsect stings and drugs allergy

Table 3 Sensitization to aeroallergens in tobacco smoke exposureand nonexposure (n 128)

AeroallergensTobacco smoke exposure status

p valueNonexposure(n 60)

Exposure(n 68)

Dp 41 (683) 51 (75) 0403Df 38 (633) 52 (765) 0105CR 11 (183) 26 (382) 0013lowastCAT 9 (15) 11 (162) 0855DOG 3 (5) 6 (88) 0398Para grass 3 (5) 7 (103) 0265Careless weed 1 (17) 2 (29) 0634Clado 1 (17) 2 (29) 0634Dp Dermatophagoides pteronyssinus Df Dermatophagoides farinae CRcockroach (Periplaneta americana) CAT cat dander DOG dog danderClado Cladosporium spp

4 Journal of Environmental and Public Health

5 Conclusions

is study demonstrated that tobacco smoke exposureworsened allergic rhinitis in patients exposed to tobaccosmoke e other aeroallergens studied appeared to havenegligible impact Complicated mechanisms of tobaccosmoke exposure may affect the allergic response differentlyfor different disorders along the allergy spectrum We be-lieve public health efforts concerning smoking cessationneed to continue in the earnest as this study has helpeddemonstrate that the detrimental health effects of tobaccosmoke are far reaching

Data Availability

e data used to support the findings of this study are in-cluded within the article

Conflicts of Interest

e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

e authors thank the study participants Director ofWalailak University Hospital and Dean of Walailak Uni-versity School of Medicine

References

[1] R Pawankar GW Canonica S T Holgate R F Lockey andM S Blaiss e World Allergy Organization (WAO) WhiteBook on Allergy Update World Allergy Organization Mil-waukee Wisconsin 2013 httpswwwworldallergyorgUserFilesfileWhiteBook2-2013-v8pdf

[2] Global Asthma Network ldquoe global asthma report 2014rdquo2014 httpwwwglobalasthmareportorg

[3] I A G Deckers S McLean S Linssen M MommersC P van Schayck and A Sheikh ldquoInvestigating internationaltime trends in the incidence and prevalence of atopic eczema1990-2010 A systematic review of epidemiological studiesrdquoPLoS One vol 7 no 7 Article ID e39803 2012

[4] J J S Chafen S J Newberry M A Riedl et al ldquoDiagnosingand managing common food allergiesrdquo JAMA vol 303no 18 pp 1848ndash1856 2010

[5] R S Gupta E E Springston M R Warrier et al ldquoeprevalence severity and distribution of childhood food al-lergy in the United Statesrdquo Pediatrics vol 128 no 1pp e9ndashe17 2011

[6] R J Rona T Keil C Summers et al ldquoe prevalence of foodallergy a meta-analysisrdquo Journal of Allergy and ClinicalImmunology vol 120 no 3 pp 638ndash646 2005

[7] G Lack ldquoPediatric allergic rhinitis and comorbid disordersrdquoJournal of Allergy and Clinical Immunology vol 108 no 1pp S9ndashS15 2001

[8] M J Brydon ldquoSkin prick testing in general practicerdquo Journalof Advanced Nursing vol 27 no 2 pp 442ndash444 1998

[9] V Jaruvongvanich P Mongkolpathumrat H Chantaphakuland J Klaewsongkram ldquoExtranasal symptoms of allergicrhinitis are difficult to treat and affect quality of liferdquo Aller-gology International vol 65 no 2 pp 199ndash203 2016

[10] E O Meltzer ldquoQuality of life in adults and children withallergic rhinitisrdquo Journal of Allergy and Clinical Immunologyvol 108 no 1 pp S45ndashS53 2001

[11] S D Reed T A Lee and D C McCrory ldquoe economicburden of allergic rhinitisrdquo Pharmacoeconomics vol 22 no 6pp 345ndash361 2004

[12] M Mukherjee A Stoddart R P Gupta et al ldquoe epide-miology healthcare and societal burden and costs of asthmain the UK and its member nations analyses of standalone andlinked national databasesrdquo BMC Medicine vol 14 no 1p 113 2016

[13] C E Lamb P H Ratner C E Johnson et al ldquoEconomicimpact of workplace productivity losses due to allergic rhinitiscompared with select medical conditions in the United Statesfrom an employer perspectiverdquo Current Medical Research andOpinion vol 22 no 6 pp 1203ndash1210 2006

0

10

20

30

40

50

60

70

Intermittent AR Mild persistent AR Moderate persistent AR Severe persistent ARSeverity of allergic rhinitis

567

30

133162 162

74

0

603

Secondhand smokerCurrent smoker living with active smokerCurrent smoker

Nonexposure

Perc

enta

ge o

f sub

grou

p re

lated

to to

bacc

o sm

oke

expo

sure

lowast

lowast

lowast

lowast

Figure 1 Prevalence of the tobacco smoke status and severity of allergic rhinitis lowastplt 0001

Journal of Environmental and Public Health 5

impairment of daily activities leisure andor sport andimpairment of school or work In mild persistent the patienthad only a small amount of symptoms without troubles [39]e status of tobacco smoke exposure was defined as acurrent smoker secondhand smoker current smoker livingwith an active smoker and nonexposure A current smokerwas defined as an individual who smoked at least 1 ciga-retteday for at least 1 month in the previous year beforeenrolment A secondhand smoker was defined as a nonactivesmoker who reported living with ge1 smokers in the past 1month or longer Nonexposure was defined as neversmoking in their lifetime and not living with a currentsmoker [35]

23 SkinPrickTest e skin prick testing with eight commonindoor aeroallergens was performed including Dermato-phagoides pteronyssinus Dermatophagoides farinae Peri-planeta americana cat dander dog dander para grasscareless weed and Cladosporium spp All standard allergenextract panels were used (Greater Pharma Nakhon Phathomailand) Positive and negative controls including histamineand glycerinated phenol-saline respectively were used eskin prick testing was performed on the volar surface of theforearm and skin reactions were evaluated 15 minutes afterthe application of the skin test Positive test results weredefined as a reaction of redness and wheal as per the worksDogru et al andHosseini et al [40 41] Individuals who had apositive test for at least one aeroallergen were defined asallergen sensitization and further processed for data analysis

24 Statistical Analyses Categorical and numerical data forthe demography of all participants were described usingfrequency () mean (plusmnSD) and range Tobacco exposureand clinical data used frequency () and mean (plusmnSD)Statistical association between the tobacco smoke exposurestatus and allergen sensitization and clinical severity of ARutilized the Chi-square test All statistical analyses of thedemographic and clinical characteristics data were per-formed using PSPP version 120 (2016 Free SoftwareFoundation Inc) e p value of lt005 was considered to bestatistically significant

3 Results

31 Demographic Characteristics of Participants is studywas performed from February 1 2018 to March 31 2019 atWalailak University Hospital out-patient department Onehundred and twenty-eight AR patients were eligible par-ticipants for the study e mean age was 2222plusmn 722 yearsand 7110wasmaleemean BMI was 2246plusmn 425 kgm2One hundred and sixteen (9060) participants werebachelorrsquos degreediploma and most of all participants wereuniversity students (8980) (Table1)

32 Tobacco Smoke Exposure and Clinical Data Sixty par-ticipants (4690) were tobacco nonexposure e sec-ondhand smoker current smoker and current smoker living

with active smoker were 3910 850 and 550 re-spectively Only 48 participants (3750) were previouslydiagnosed as AR by physician e most common comor-bidity was atopic dermatitis (1800) Oral antihistaminewas the most common medication used by participants(Table 2)

33 Sensitization to Aeroallergens in Tobacco Smoke Exposureand Nonexposure Sensitization to eight aeroallergens inallergic rhinitis patients are shown in Table 3 Tobaccosmoke exposure affected more sensitization only in cock-roach (Periplaneta americana) aeroallergen compared tononexposure with statistical significance (p 0013) Forsubgroup analysis a current smoker had more prevalence ofsensitization to cat dander and Cladosporium spp than asecondhand smoker with p 0012 and 0002 respectively(data not shown)

34 Prevalence of the Tobacco Smoke Status and Severity ofAllergic Rhinitis From 60 nonexposure individuals most ofthem (5670) were classified as intermittent allergic rhi-nitis On the other hand tobacco smoke exposure patientswere distributed mostly in mild persistent allergic rhinitiswith 41cases (60 30) e tobacco exposure group wasshown to have more severe prevalence of clinical allergicrhinitis as compared to nonexposure with statistical sig-nificance (plt 0001) as shown in Figure 1

4 Discussion

Changes in the respiratory tract caused by exposure to to-bacco smoke have been well described [42] Tobacco smokecan directly affect the respiratory tract leading to thickeningof the lower airway walls impaired mucociliary clearanceand altered airway immune function is study aimed toexamine further the interface of allergic symptoms in AR

Table 1 Demographic characteristics of participants (n 128)

Characteristic Meanplusmn SD or n ()Age (year) 2222plusmn 722 (1600ndash5900)Weight (kg) 6428plusmn 1425 (4340ndash11500)Height (cm) 16887plusmn 770 (14800ndash18700)BMI (kgm2) 2246plusmn 425 (1653ndash3526)Male 91 (7110)Educational level

Junior high school 1 (080)High school 3 (230)Bachelorrsquos degreediploma 116 (9060)Masterrsquos degree and above 8 (630)

OccupationUniversity student 115 (8980)University staff 13 (1020)

Income of family (US$month)le600 31 (2420)601ndash1667 54 (4220)1668ndash3333 38 (2970)ge3334 5 (390)

lowastExchange rate Dec 15 2019

Journal of Environmental and Public Health 3

and tobacco smoke us we evaluated the associationbetween tobacco smoke exposure and allergic sensitizationand severity of allergic rhinitis adult patients

After performing skin prick testing in tobacco smokeexposure and nonexposure allergic rhinitis patients we foundthat only cockroach (Periplaneta americana) antigen from apanel of eight aeroallergens yielded higher rates of positivitywhereas the other seven aeroallergens showed no statisticallysignificant differences Many reports have shown that tobaccosmoke increased allergen sensitization among allergic rhinitispatients [31ndash33] However some reports have shown aninverse effect of tobacco smoke on sensitization [29 34 35]For example in a US adult population cross-sectional study areverse relationship between tobacco smoke and inhaledallergen sensitization was found [28] Without doubt theissue is complex and may relate to a number of factors Onefactor could be the timing of exposure to tobacco smoke as a

recent systematic and meta-analysis study showed that earlylife exposure to environmental tobacco smoke increased therisk of sensitization [43] e present study did not definetobacco exposure duration long enough hence the effect oftobacco smoke on allergens sensitization yielded mostlyinsignificant

As consistent with many previous reports [29 34] thepresent study demonstrated that tobacco smoke exposureled to worsened clinical severity in allergic symptomscompared to the nonexposure group Rhinomanometry inone study examining the effect of tobacco smoke on severityof symptoms in perennial allergic rhinitis patients showedincreased nasal resistance a correlate of worsened inflam-mation [44] Another study found that exposure to tobaccosmoke among allergic rhinitis patients did not change se-verity of disease [45]

It remains to be seen whether the pathophysiologicmechanisms between smoking and IgE-mediated allergicsensitization may be distinct from those between smokingand severity of allergic rhinitis e skin prick testing mightnot be affected by exposure to tobacco smoke

e present study has some limitations including a lackof quantitative measurement for the level of tobacco ex-posure both in current smokers and secondhand smokers Inaddition the severity of allergic rhinitis was classified mainlyby history and clinical manifestations without objectivemeasurement Future research should include history ofcigarette use per day length of time that a secondhandsmoker is exposed to smoking as well as cotinine analyses inblood urine or even hair as a marker of exposure [46] Inaddition rhinomanometry may be useful for assessing real-time nasal conditions in the participants Finally testing ofother aeroallergens particularly moulds would be worth aninvestigation

Table 2 Tobacco smoke exposure and clinical data (n 128)

Parameters Meanplusmn SD or n ()Tobacco exposureNonexposure 60 (4690)Secondhand smoker 50 (3910)Current smoker 11 (860)Current smoker living with active smoker 7 (550)

AR diagnosisPrevious diagnosis by physician 48 (3750)First AR diagnosis 80 (6250)

ComorbidityAD 23 (1800)Asthma 17 (1330)Food allergy 14 (1090)Allergic conjunctivitis (AC) 13 (1020)Anaphylaxis 4 (310)Otherslowast 14 (1090)

Current medicationOral antihistamine 36 (2810)Normal saline irrigation 20 (1560)Intranasal corticosteroid 10 (780)Leukotriene receptor antagonist 5 (390)Intranasal decongestant 4 (310)

Other lowastInsect stings and drugs allergy

Table 3 Sensitization to aeroallergens in tobacco smoke exposureand nonexposure (n 128)

AeroallergensTobacco smoke exposure status

p valueNonexposure(n 60)

Exposure(n 68)

Dp 41 (683) 51 (75) 0403Df 38 (633) 52 (765) 0105CR 11 (183) 26 (382) 0013lowastCAT 9 (15) 11 (162) 0855DOG 3 (5) 6 (88) 0398Para grass 3 (5) 7 (103) 0265Careless weed 1 (17) 2 (29) 0634Clado 1 (17) 2 (29) 0634Dp Dermatophagoides pteronyssinus Df Dermatophagoides farinae CRcockroach (Periplaneta americana) CAT cat dander DOG dog danderClado Cladosporium spp

4 Journal of Environmental and Public Health

5 Conclusions

is study demonstrated that tobacco smoke exposureworsened allergic rhinitis in patients exposed to tobaccosmoke e other aeroallergens studied appeared to havenegligible impact Complicated mechanisms of tobaccosmoke exposure may affect the allergic response differentlyfor different disorders along the allergy spectrum We be-lieve public health efforts concerning smoking cessationneed to continue in the earnest as this study has helpeddemonstrate that the detrimental health effects of tobaccosmoke are far reaching

Data Availability

e data used to support the findings of this study are in-cluded within the article

Conflicts of Interest

e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

e authors thank the study participants Director ofWalailak University Hospital and Dean of Walailak Uni-versity School of Medicine

References

[1] R Pawankar GW Canonica S T Holgate R F Lockey andM S Blaiss e World Allergy Organization (WAO) WhiteBook on Allergy Update World Allergy Organization Mil-waukee Wisconsin 2013 httpswwwworldallergyorgUserFilesfileWhiteBook2-2013-v8pdf

[2] Global Asthma Network ldquoe global asthma report 2014rdquo2014 httpwwwglobalasthmareportorg

[3] I A G Deckers S McLean S Linssen M MommersC P van Schayck and A Sheikh ldquoInvestigating internationaltime trends in the incidence and prevalence of atopic eczema1990-2010 A systematic review of epidemiological studiesrdquoPLoS One vol 7 no 7 Article ID e39803 2012

[4] J J S Chafen S J Newberry M A Riedl et al ldquoDiagnosingand managing common food allergiesrdquo JAMA vol 303no 18 pp 1848ndash1856 2010

[5] R S Gupta E E Springston M R Warrier et al ldquoeprevalence severity and distribution of childhood food al-lergy in the United Statesrdquo Pediatrics vol 128 no 1pp e9ndashe17 2011

[6] R J Rona T Keil C Summers et al ldquoe prevalence of foodallergy a meta-analysisrdquo Journal of Allergy and ClinicalImmunology vol 120 no 3 pp 638ndash646 2005

[7] G Lack ldquoPediatric allergic rhinitis and comorbid disordersrdquoJournal of Allergy and Clinical Immunology vol 108 no 1pp S9ndashS15 2001

[8] M J Brydon ldquoSkin prick testing in general practicerdquo Journalof Advanced Nursing vol 27 no 2 pp 442ndash444 1998

[9] V Jaruvongvanich P Mongkolpathumrat H Chantaphakuland J Klaewsongkram ldquoExtranasal symptoms of allergicrhinitis are difficult to treat and affect quality of liferdquo Aller-gology International vol 65 no 2 pp 199ndash203 2016

[10] E O Meltzer ldquoQuality of life in adults and children withallergic rhinitisrdquo Journal of Allergy and Clinical Immunologyvol 108 no 1 pp S45ndashS53 2001

[11] S D Reed T A Lee and D C McCrory ldquoe economicburden of allergic rhinitisrdquo Pharmacoeconomics vol 22 no 6pp 345ndash361 2004

[12] M Mukherjee A Stoddart R P Gupta et al ldquoe epide-miology healthcare and societal burden and costs of asthmain the UK and its member nations analyses of standalone andlinked national databasesrdquo BMC Medicine vol 14 no 1p 113 2016

[13] C E Lamb P H Ratner C E Johnson et al ldquoEconomicimpact of workplace productivity losses due to allergic rhinitiscompared with select medical conditions in the United Statesfrom an employer perspectiverdquo Current Medical Research andOpinion vol 22 no 6 pp 1203ndash1210 2006

0

10

20

30

40

50

60

70

Intermittent AR Mild persistent AR Moderate persistent AR Severe persistent ARSeverity of allergic rhinitis

567

30

133162 162

74

0

603

Secondhand smokerCurrent smoker living with active smokerCurrent smoker

Nonexposure

Perc

enta

ge o

f sub

grou

p re

lated

to to

bacc

o sm

oke

expo

sure

lowast

lowast

lowast

lowast

Figure 1 Prevalence of the tobacco smoke status and severity of allergic rhinitis lowastplt 0001

Journal of Environmental and Public Health 5

and tobacco smoke us we evaluated the associationbetween tobacco smoke exposure and allergic sensitizationand severity of allergic rhinitis adult patients

After performing skin prick testing in tobacco smokeexposure and nonexposure allergic rhinitis patients we foundthat only cockroach (Periplaneta americana) antigen from apanel of eight aeroallergens yielded higher rates of positivitywhereas the other seven aeroallergens showed no statisticallysignificant differences Many reports have shown that tobaccosmoke increased allergen sensitization among allergic rhinitispatients [31ndash33] However some reports have shown aninverse effect of tobacco smoke on sensitization [29 34 35]For example in a US adult population cross-sectional study areverse relationship between tobacco smoke and inhaledallergen sensitization was found [28] Without doubt theissue is complex and may relate to a number of factors Onefactor could be the timing of exposure to tobacco smoke as a

recent systematic and meta-analysis study showed that earlylife exposure to environmental tobacco smoke increased therisk of sensitization [43] e present study did not definetobacco exposure duration long enough hence the effect oftobacco smoke on allergens sensitization yielded mostlyinsignificant

As consistent with many previous reports [29 34] thepresent study demonstrated that tobacco smoke exposureled to worsened clinical severity in allergic symptomscompared to the nonexposure group Rhinomanometry inone study examining the effect of tobacco smoke on severityof symptoms in perennial allergic rhinitis patients showedincreased nasal resistance a correlate of worsened inflam-mation [44] Another study found that exposure to tobaccosmoke among allergic rhinitis patients did not change se-verity of disease [45]

It remains to be seen whether the pathophysiologicmechanisms between smoking and IgE-mediated allergicsensitization may be distinct from those between smokingand severity of allergic rhinitis e skin prick testing mightnot be affected by exposure to tobacco smoke

e present study has some limitations including a lackof quantitative measurement for the level of tobacco ex-posure both in current smokers and secondhand smokers Inaddition the severity of allergic rhinitis was classified mainlyby history and clinical manifestations without objectivemeasurement Future research should include history ofcigarette use per day length of time that a secondhandsmoker is exposed to smoking as well as cotinine analyses inblood urine or even hair as a marker of exposure [46] Inaddition rhinomanometry may be useful for assessing real-time nasal conditions in the participants Finally testing ofother aeroallergens particularly moulds would be worth aninvestigation

Table 2 Tobacco smoke exposure and clinical data (n 128)

Parameters Meanplusmn SD or n ()Tobacco exposureNonexposure 60 (4690)Secondhand smoker 50 (3910)Current smoker 11 (860)Current smoker living with active smoker 7 (550)

AR diagnosisPrevious diagnosis by physician 48 (3750)First AR diagnosis 80 (6250)

ComorbidityAD 23 (1800)Asthma 17 (1330)Food allergy 14 (1090)Allergic conjunctivitis (AC) 13 (1020)Anaphylaxis 4 (310)Otherslowast 14 (1090)

Current medicationOral antihistamine 36 (2810)Normal saline irrigation 20 (1560)Intranasal corticosteroid 10 (780)Leukotriene receptor antagonist 5 (390)Intranasal decongestant 4 (310)

Other lowastInsect stings and drugs allergy

Table 3 Sensitization to aeroallergens in tobacco smoke exposureand nonexposure (n 128)

AeroallergensTobacco smoke exposure status

p valueNonexposure(n 60)

Exposure(n 68)

Dp 41 (683) 51 (75) 0403Df 38 (633) 52 (765) 0105CR 11 (183) 26 (382) 0013lowastCAT 9 (15) 11 (162) 0855DOG 3 (5) 6 (88) 0398Para grass 3 (5) 7 (103) 0265Careless weed 1 (17) 2 (29) 0634Clado 1 (17) 2 (29) 0634Dp Dermatophagoides pteronyssinus Df Dermatophagoides farinae CRcockroach (Periplaneta americana) CAT cat dander DOG dog danderClado Cladosporium spp

4 Journal of Environmental and Public Health

5 Conclusions

is study demonstrated that tobacco smoke exposureworsened allergic rhinitis in patients exposed to tobaccosmoke e other aeroallergens studied appeared to havenegligible impact Complicated mechanisms of tobaccosmoke exposure may affect the allergic response differentlyfor different disorders along the allergy spectrum We be-lieve public health efforts concerning smoking cessationneed to continue in the earnest as this study has helpeddemonstrate that the detrimental health effects of tobaccosmoke are far reaching

Data Availability

e data used to support the findings of this study are in-cluded within the article

Conflicts of Interest

e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

e authors thank the study participants Director ofWalailak University Hospital and Dean of Walailak Uni-versity School of Medicine

References

[1] R Pawankar GW Canonica S T Holgate R F Lockey andM S Blaiss e World Allergy Organization (WAO) WhiteBook on Allergy Update World Allergy Organization Mil-waukee Wisconsin 2013 httpswwwworldallergyorgUserFilesfileWhiteBook2-2013-v8pdf

[2] Global Asthma Network ldquoe global asthma report 2014rdquo2014 httpwwwglobalasthmareportorg

[3] I A G Deckers S McLean S Linssen M MommersC P van Schayck and A Sheikh ldquoInvestigating internationaltime trends in the incidence and prevalence of atopic eczema1990-2010 A systematic review of epidemiological studiesrdquoPLoS One vol 7 no 7 Article ID e39803 2012

[4] J J S Chafen S J Newberry M A Riedl et al ldquoDiagnosingand managing common food allergiesrdquo JAMA vol 303no 18 pp 1848ndash1856 2010

[5] R S Gupta E E Springston M R Warrier et al ldquoeprevalence severity and distribution of childhood food al-lergy in the United Statesrdquo Pediatrics vol 128 no 1pp e9ndashe17 2011

[6] R J Rona T Keil C Summers et al ldquoe prevalence of foodallergy a meta-analysisrdquo Journal of Allergy and ClinicalImmunology vol 120 no 3 pp 638ndash646 2005

[7] G Lack ldquoPediatric allergic rhinitis and comorbid disordersrdquoJournal of Allergy and Clinical Immunology vol 108 no 1pp S9ndashS15 2001

[8] M J Brydon ldquoSkin prick testing in general practicerdquo Journalof Advanced Nursing vol 27 no 2 pp 442ndash444 1998

[9] V Jaruvongvanich P Mongkolpathumrat H Chantaphakuland J Klaewsongkram ldquoExtranasal symptoms of allergicrhinitis are difficult to treat and affect quality of liferdquo Aller-gology International vol 65 no 2 pp 199ndash203 2016

[10] E O Meltzer ldquoQuality of life in adults and children withallergic rhinitisrdquo Journal of Allergy and Clinical Immunologyvol 108 no 1 pp S45ndashS53 2001

[11] S D Reed T A Lee and D C McCrory ldquoe economicburden of allergic rhinitisrdquo Pharmacoeconomics vol 22 no 6pp 345ndash361 2004

[12] M Mukherjee A Stoddart R P Gupta et al ldquoe epide-miology healthcare and societal burden and costs of asthmain the UK and its member nations analyses of standalone andlinked national databasesrdquo BMC Medicine vol 14 no 1p 113 2016

[13] C E Lamb P H Ratner C E Johnson et al ldquoEconomicimpact of workplace productivity losses due to allergic rhinitiscompared with select medical conditions in the United Statesfrom an employer perspectiverdquo Current Medical Research andOpinion vol 22 no 6 pp 1203ndash1210 2006

0

10

20

30

40

50

60

70

Intermittent AR Mild persistent AR Moderate persistent AR Severe persistent ARSeverity of allergic rhinitis

567

30

133162 162

74

0

603

Secondhand smokerCurrent smoker living with active smokerCurrent smoker

Nonexposure

Perc

enta

ge o

f sub

grou

p re

lated

to to

bacc

o sm

oke

expo

sure

lowast

lowast

lowast

lowast

Figure 1 Prevalence of the tobacco smoke status and severity of allergic rhinitis lowastplt 0001

Journal of Environmental and Public Health 5

5 Conclusions

is study demonstrated that tobacco smoke exposureworsened allergic rhinitis in patients exposed to tobaccosmoke e other aeroallergens studied appeared to havenegligible impact Complicated mechanisms of tobaccosmoke exposure may affect the allergic response differentlyfor different disorders along the allergy spectrum We be-lieve public health efforts concerning smoking cessationneed to continue in the earnest as this study has helpeddemonstrate that the detrimental health effects of tobaccosmoke are far reaching

Data Availability

e data used to support the findings of this study are in-cluded within the article

Conflicts of Interest

e authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

e authors thank the study participants Director ofWalailak University Hospital and Dean of Walailak Uni-versity School of Medicine

References

[1] R Pawankar GW Canonica S T Holgate R F Lockey andM S Blaiss e World Allergy Organization (WAO) WhiteBook on Allergy Update World Allergy Organization Mil-waukee Wisconsin 2013 httpswwwworldallergyorgUserFilesfileWhiteBook2-2013-v8pdf

[2] Global Asthma Network ldquoe global asthma report 2014rdquo2014 httpwwwglobalasthmareportorg

[3] I A G Deckers S McLean S Linssen M MommersC P van Schayck and A Sheikh ldquoInvestigating internationaltime trends in the incidence and prevalence of atopic eczema1990-2010 A systematic review of epidemiological studiesrdquoPLoS One vol 7 no 7 Article ID e39803 2012

[4] J J S Chafen S J Newberry M A Riedl et al ldquoDiagnosingand managing common food allergiesrdquo JAMA vol 303no 18 pp 1848ndash1856 2010

[5] R S Gupta E E Springston M R Warrier et al ldquoeprevalence severity and distribution of childhood food al-lergy in the United Statesrdquo Pediatrics vol 128 no 1pp e9ndashe17 2011

[6] R J Rona T Keil C Summers et al ldquoe prevalence of foodallergy a meta-analysisrdquo Journal of Allergy and ClinicalImmunology vol 120 no 3 pp 638ndash646 2005

[7] G Lack ldquoPediatric allergic rhinitis and comorbid disordersrdquoJournal of Allergy and Clinical Immunology vol 108 no 1pp S9ndashS15 2001

[8] M J Brydon ldquoSkin prick testing in general practicerdquo Journalof Advanced Nursing vol 27 no 2 pp 442ndash444 1998

[9] V Jaruvongvanich P Mongkolpathumrat H Chantaphakuland J Klaewsongkram ldquoExtranasal symptoms of allergicrhinitis are difficult to treat and affect quality of liferdquo Aller-gology International vol 65 no 2 pp 199ndash203 2016

[10] E O Meltzer ldquoQuality of life in adults and children withallergic rhinitisrdquo Journal of Allergy and Clinical Immunologyvol 108 no 1 pp S45ndashS53 2001

[11] S D Reed T A Lee and D C McCrory ldquoe economicburden of allergic rhinitisrdquo Pharmacoeconomics vol 22 no 6pp 345ndash361 2004

[12] M Mukherjee A Stoddart R P Gupta et al ldquoe epide-miology healthcare and societal burden and costs of asthmain the UK and its member nations analyses of standalone andlinked national databasesrdquo BMC Medicine vol 14 no 1p 113 2016

[13] C E Lamb P H Ratner C E Johnson et al ldquoEconomicimpact of workplace productivity losses due to allergic rhinitiscompared with select medical conditions in the United Statesfrom an employer perspectiverdquo Current Medical Research andOpinion vol 22 no 6 pp 1203ndash1210 2006

0

10

20

30

40

50

60

70

Intermittent AR Mild persistent AR Moderate persistent AR Severe persistent ARSeverity of allergic rhinitis

567

30

133162 162

74

0

603

Secondhand smokerCurrent smoker living with active smokerCurrent smoker

Nonexposure

Perc

enta

ge o

f sub

grou

p re

lated

to to

bacc

o sm

oke

expo

sure

lowast

lowast

lowast

lowast

Figure 1 Prevalence of the tobacco smoke status and severity of allergic rhinitis lowastplt 0001

Journal of Environmental and Public Health 5

[14] J Crystal-Peters W H Crown R Z Goetzel andD C Schutt ldquoe cost of productivity losses associated withallergic rhinitisrdquo e American Journal of Managed Carevol 6 pp 373ndash378 2000

[15] S Walker S Khan-Wasti M Fletcher P Cullinan J Harrisand A Sheikh ldquoSeasonal allergic rhinitis is associated with adetrimental effect on examination performance in UnitedKingdom teenagers case-control studyrdquo Journal of Allergyand Clinical Immunology vol 120 no 2 pp 381ndash387 2007

[16] L-O Cardell P Olsson M Andersson et al ldquoTOTALL highcost of allergic rhinitis-a national Swedish population-basedquestionnaire studyrdquoNPJ Primary Care Respiratory Medicinevol 26 no 1 p 15082 2016

[17] D R Rao J M Gaffin S N Baxi W J SheehanE B Hoffman and W Phipatanakul ldquoe utility of forcedexpiratory flow between 25 and 75 of vital capacity inpredicting childhood asthma morbidity and severityrdquo eJournal of Asthma Official Journal of the Association for theCare of Asthma vol 49 no 6 pp 586ndash592 2012

[18] L B Bacharier R C Strunk D Mauger D WhiteR F Lemanske and C A Sorkness ldquoClassifying asthmaseverity in childrenrdquo American Journal of Respiratory andCritical Care Medicine vol 170 no 4 pp 426ndash432 2004

[19] A L Fuhlbrigge B T Kitch A D Paltiel et al ldquoFEV1 isassociated with risk of asthma attacks in a pediatric pop-ulationrdquo Journal of Allergy and Clinical Immunology vol 107no 1 pp 61ndash67 2001

[20] H Kamalaporn A Chawalitdamrong and A Preutthipanldquoai pediatriciansrsquo current practice toward childhoodasthmardquo Journal of Asthma vol 55 no 4 pp 402ndash415 2018

[21] U Schauer K-C Bergmann M Gerstlauer et al ldquoImprovedasthma control in patients with severe persistent allergicasthma after 12 months of nightly temperature-controlledlaminar airflow an observational study with retrospectivecomparisonsrdquo European Clinical Respiratory Journal vol 2no 1 Article ID 28531 2015

[22] U Wahn S Lau R Bergmann et al ldquoIndoor allergen ex-posure is a risk factor for sensitization during the first threeyears of liferdquo Journal of Allergy and Clinical Immunologyvol 99 no 6 pp 763ndash769 1997

[23] J Li HWang Y Chen J Zheng GWWong and N ZhongldquoHouse dust mite sensitization is the main risk factor for theincrease in prevalence of wheeze in 13- to 14-year-oldschoolchildren in Guangzhou city Chinardquo Clinical and Ex-perimental Allergy Journal of the British Society for Allergyand Clinical Immunology vol 131 no 2 p AB52 2013

[24] S H Arshad J Bojarskas S Tsitoura et al ldquoPrevention ofsensitization to house dust mite by allergen avoidance inschool age children a randomized controlled studyrdquo ClinicalExperimental Allergy vol 32 no 6 pp 843ndash849 2002

[25] S Toppila-Salmi H Huhtala J Karjalainen et al ldquoSensiti-zation pattern affects the asthma risk in Finnish adult pop-ulationrdquo Allergy vol 70 no 9 pp 1112ndash1120 2015

[26] A Yuenyongviwat D Koonrangsesomboon andP Sangsupawanich ldquoRecent 5-year trends of asthmaseverity and allergen sensitization among children insouthern ailandrdquo Asian Pacific Journal of Allergy andImmunology vol 31 pp 242ndash246 2013

[27] P Supakthanasiri J Klaewsongkram and H ChantaphakulldquoReactivity of allergy skin test in healthy volunteersrdquo Sin-gapore Med Journal vol 55 no 1 pp 34ndash36 2014

[28] J Shargorodsky E Garcia-Esquinas GalanI A Navas-Acienand S Y Lin ldquoAllergic sensitization rhinitis and tobacco

smoke exposure in US adultsrdquo PLoS ONE vol 10 no 7Article ID e0131957 2015

[29] T-C Yao S-W Chang W-C Chang et al ldquoExposure totobacco smoke and childhood rhinitis a population-basedstudyrdquo Scientific Reports vol 7 Article ID 42836 2017

[30] J D acher O Gruziere G Perchagen et al ldquoParentalsmoking and development of allergic sensitization from birthto adolescencerdquo Allergy vol 71 no 2 pp 239ndash248 2016

[31] T Keil S Lau S Roll et al ldquoMaternal smoking increases riskof allergic sensitization and wheezing only in children withallergic predisposition longitudinal analysis from birth to 10yearsrdquo Allergy vol 64 pp 445ndash451 2008

[32] W Feleszko M Ruszczynski J Jaworska et al ldquoEnviron-mental tobacco smoke exposure and risk of allergic sensiti-zation in children a systematic review and meta-analysisrdquoArchives of Disease in Childhood vol 99 pp 985ndash992 2014

[33] H A Khazaei B Khazaei G A Dashtizadeh andM Mohammadi ldquoCigarette smoking and skin prick test inpatients with allergic rhinitisrdquo International Journal of HighRisk Behaviors and Addiction vol 4 no 3 Article ID e234832015

[34] J Shargorodsky E Garcia-Esquinas A Navas-Acien andS Y Lin ldquoAllergic sensitization rhinitis and tobacco smokeexposure in US children and adolescentsrdquo InternationalForum of Allergy amp Rhinology vol 5 no 6 pp 471ndash476 2015

[35] R J Hancox D Welch R Poulton et al ldquoCigarette smokingand allergic sensitization a 32-year population- based cohortstudyrdquo Journal of Allergy and Clinical Immunology vol 121pp 38ndash42 2008

[36] P Hawanondha and V Panyasaeng ldquoSample size calcula-tionrdquo in Research Principle to Success in Practice P Sum-patanukul Ed pp 255ndash271 e Focal Image Printing GroupLimited Bangkok ailand 2011

[37] H A Khazaei B Khazaei G A Dashtizadeh andM Mohammadi ldquoCigarette smoking and skin prick test inpatients with allergic rhinitisrdquo International Journal of HighRisk Behaviors and Addiction vol 4 no 3 2015

[38] J Bousquet N Khaltaev A A Cruz et al ldquoAllergic rhinitisand its impact on asthma (ARIA) 2008 update (in collabo-ration with the world health organization GA(2)len andAllerGen)rdquo Allergy vol 63 no 86 pp S8ndashS160 2008

[39] J Bousquet P Van Cauwenberge and N Khaltaev ldquoAllergicrhinitis and its impact on asthmardquo Journal of Allergy ClinicalImmunology vol 108 no 5 pp S147ndashS334 2001

[40] M Dogru I Bostanci S Ozmen T Ginis and H Duman ldquoIsthere a need for repetition of skin test in childhood allergicdiseases Repetition of skin testand allergic diseasesrdquo Aller-gology International vol 63 no 2 pp 227ndash233 2014

[41] S Hosseini R S Shoormasti R Akramian et al ldquoSkin pricktest reactivity to common aero and food allergens amongchildren with allergyrdquo Iran Journal of Medical Science vol 39no 1 pp 29ndash35 2014

[42] J C Hogg ldquoPathophysiology of airflow limitation in chronicobstructive pulmonary diseaserdquo e Lancet vol 364pp 709ndash721 2004

[43] J Gaffin ldquoPostnatal environmental tobacco smoke exposure isassociated with objective markers atopy in preschool agedchildrenrdquo Evidence BasedMedicine vol 20 no 6 p 219 2015

[44] B B Montano-Velazquez R C Navarreta M D MogicaMartinez M Becerril Angeles and K Jauregui-RenaudldquoRhinomanometry in young patients with perennial allergicrhinitis withwithout recent exposure to tobacco smokerdquoClinical Otolaryngology vol 36 no 4 pp 320ndash324 2011

6 Journal of Environmental and Public Health

[45] P J Bousquet C Cropet J Klossek B Allaf F Neukirch andJ Bousquet ldquoEffect of smoking on symptoms of allergicrhinitisrdquo Annals of Allergy Asthma amp Immunology vol 103pp 195ndash200 2009

[46] H J Yang ldquoImpact of perinatal environmental tobacco smokeon the development of childhood allergic diseasesrdquo KoreanJournal of Pediatrics vol 59 no 8 pp 319ndash327 2016

Journal of Environmental and Public Health 7

[45] P J Bousquet C Cropet J Klossek B Allaf F Neukirch andJ Bousquet ldquoEffect of smoking on symptoms of allergicrhinitisrdquo Annals of Allergy Asthma amp Immunology vol 103pp 195ndash200 2009

[46] H J Yang ldquoImpact of perinatal environmental tobacco smokeon the development of childhood allergic diseasesrdquo KoreanJournal of Pediatrics vol 59 no 8 pp 319ndash327 2016

Journal of Environmental and Public Health 7