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    Association of air-conditioning with respiratory symptoms in office

    workers in tropical climate

    Introduction

    The life-style of the urban population has been rapidlychanging along the last decades. The increasedamount of time spent indoors, even in tropicalcountries, makes the indoor air quality (IAQ) a veryimportant topic worldwide. Problems associated toindoor environment are one of the most commonenvironmental health issues faced by clinicians (Led-ford, 1994), but the factors associated with theperceived IAQ are not fully understood. They includetemperature, humidity, air exchange rates, odors, airmovement, ventilation, biological contaminants, vola-tile organic compounds, bacterial toxins, labor andpsychosocial factors (Apter et al., 1994). One of the

    most important factors affecting IAQ is the presenceand the characteristics of the heating, ventilation and

    air-conditioning systems (HVAC) in the places studied(Mendell and Smith, 1990). In a recent reanalysis ofprevalence studies, there was an increase in prevalenceof indoor air-related symptoms between 30 and 200%in buildings with air-conditioning, with or withouthumidification, when compared with natural ventila-tion systems (Seppanen and Fisk, 2002). The authorsstressed the need of data in tropical cities with hotand humid air most of the year. The geographicvariations can lead to different IAQ perception(Spaul, 1994). The existing evidence of the associationof HVAC systems and IAQ complains is to bedetermined in hot and humid air conditions.

    Abstract To evaluate the association of heating, ventilation and air-conditioningsystems (HVAC) and respiratory symptoms in a tropical city, self-administeredquestionnaires were given to 2000 individuals working in air-conditioned officebuildings and to 500 control workers in naturally ventilated buildings. Reportedsymptoms from the two populations were analyzed using chi-square tests, uni-variate and multiple logistic regressions models. Symptoms were the outcomevariable and the odds ratios were adjusted by gender, age, accumulated worktime, smoking habits and atopic background. There was a 79.8% response rateand there was a positive association of nasal symptoms (odds ratio, OR 1.59,

    95% confidence interval, CI

    1.112.28), naso-ocular symptoms (OR

    1.58,95% CI 1.052.38), persistent cough (OR 3.04, 95% CI 2.004.63)sinusitis symptoms (OR 1.85, 95% CI 1.272.71) and building-relatedworsening of the symptoms (OR 4.92, 95% CI 2.938.27) with working inair-conditioned buildings. In conclusion, our study suggests that artificial air-conditioning is a matter of concern for respiratory symptoms in cities with hotand humid climate.

    G. S. Graudenz1, C. H. Oliveira2,A. Tribess3, C. Mendes, Jr3,M. R. D. O. Latorre4, J. Kalil11Division of Allergy and Clinical Immunology, Internal

    Medicine Department, School of Medicine, Millennium

    Institute, University of So Paulo, So Paulo,2Pediatric

    Department, School of Medicine, University of

    Campinas, Campinas,3Department of Mechanical

    Engineering, Polytechnic School and 4Department of

    Epidemiology, School of Public Health, University of

    So Paulo, So Paulo, Brazil

    Key words: Air-conditioning; Air pollution; Indoor;

    Environmental exposure; Occupational health; Allergy.

    Gustavo Silveira Graudenz

    Rua Girassol 1317/21, So Paulo, SP 05433-002, Brazil

    Tel.: 55 11 30316642

    Fax: 55 11 30321019

    e-mail: [email protected]

    Received for review 23 March 2004. Accepted for

    publication 6 October 2004.

    Practical ImplicationsThis study suggests that indoor air-related respiratory symptoms are a matter of concern in places with hot and humidclimate. The regression models were adjusted by confounders that could be used in further reanalysis of indoor airquality related symptoms and ventilation systems with expanded variety of climatic conditions.

    Indoor Air 2005; 15: 6266www.blackwellpublishing.com/inaPrinted in Denmark. All rights reserved

    Copyright Blackwell Munksgaard 2004

    INDOOR AIRdoi:10.1111/j.1600-0668.2004.00324.x

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    The use of air-conditioning systems is widespread inBrazil and the standard equipments lack heating orhumidification systems even in inland dryer regions.Sao Paulo is the largest city in South America witharound 10 million inhabitants. High temperatures (1535C) and high relative humidity (6094%) occurthroughout the year. A typical day has a temperature

    of 32C and relative air humidity of 70%, whichcorresponds to an absolute air humidity of 23 g ofwater per kg of dry air.

    The role of respiratory allergy such as asthma andallergic rhinitis, is still a matter of debate because itis consistently involved as a risk factor to developIAQ-related symptoms in epidemiological studies(Bjornsson et al., 1998; Brooks, 1994; Ooi and Goh,1996). However, no significant exposure of aeroaller-gens to explain IAQ-related symptoms is usuallyfound (Graudenz et al., 2002a; Menzies et al., 1998).Most previous epidemiological studies have not used

    standardized questionnaires for the diagnosis ofallergic symptoms. Therefore, the use of specificmethods for addressing the host susceptibility couldadd more information for this group of atopicindividuals, specially in Brazil with high prevalenceof allergic diseases (Sole et al., 2001; Vanna et al.,2001).

    The aim of this study was to evaluate the associationof respiratory symptoms of full-time workers frombuildings with air-conditioning without humidificationsystems in comparison with naturally ventilated build-ings in a city with hot and humid climate.

    Material and methods

    Office buildings

    A total of 2000 full-time office workers from eightdifferent office buildings, located in the downtown areaof Sao Paulo were studied. All offices were sealed, withHVAC systems without humidification devices oropening windows, fully carpeted, and with artificialfluorescent illumination. None of the selected placeswere at the ground level, varying from the 3rd to the35th floor and with 1535 years of commercial use. All

    HVAC systems had periodical maintenance, opera-tional and organizational standard procedures toassure filtering, exchange air rates, total particulatematter, dioxide carbon levels, temperature and humid-ity under national safety limits (Sanitaria, AgenciaNacional de Vigilancia Sanitaria, 2003). Previousevaluation of indoor biological and allergenic contentsfrom these air-conditioned buildings showed no con-taminations (Graudenz et al., 2002b). The workers didnot know the characteristics of their air-conditioningsystem, or the specific objective of the study that wasconducted during an evaluation of the non-smokingpolicy in commercial offices of Sao Paulo. Individuals

    not working full-time (8 h a day or more) under theHVAC systems were excluded.

    The control group was composed of 500 workersmostly clerical workers and trainees, staying full-timein three public buildings with natural ventilation vialeakage paths and intentional openings, with nothermal control or presence of sealed windows. They

    were located in the same city of the air-conditionedbuildings and evaluated at the same season of the yearStaffs allocated in sections equipped with any kind ofair-conditioning or mechanical air exhaust system wereexcluded. Control buildings ranged from 30 to 45 yearsold, had partial carpeted coverings and were alsodependent of artificial illumination. Control individu-als who were exposed to any kind of HVAC or air-conditioning systems, for more than 36 h a week werearbitrarily excluded.

    In all buildings, offices were equipped with laserprinters, fax machines and video terminal displays. No

    print shops, internal loading docks, stored chemicals orgas-fired heating systems were present in any buildingThere were no reports of major building renovation orwater incursion in the locations studied. None of thebuildings studied were previously known as sickbuildings. After the authorization of the managersand workers of the companies settled in the buildings,and the approval of the Ethics Committee of the SaoPaulo University, a self-administered questionnaireregarding allergy background, smoking status, respir-atory symptoms, previous medical diagnosis of asthmaand rhinitis and work relation with respiratory symp-toms was given by a medical doctor and explained to

    the managers of each studied section of the buildingsThe questionnaire was a combination of two previously standardized and validated for Portuguese lan-guage questionnaires; the ATS-DLD-78,(Esteves et al.1999a,b; Ferris, 1978) and the ISAAC (Asher et al.1995; Esteves et al., 1999a,b). The main questions onasthma symptoms were: Did you have wheezing orwhistling in your chest in the last 12 months when youdid not have flu? Have you ever had attacks obreathlessness with wheezing? The core questions onnasal symptoms were: In the past 6 months have youhad a problem with sneezing, a runny or a blocked

    nose when you did not have flu? In the past 6 monthshas this nose problem been accompanied by itchywatery eyes? The question about sinusitis was: In thepast 12 months did you have purulent nasal dischargeaccompanied by frontal or maxillary headache? Andwhere do the above symptoms more frequently occur?

    Statistical analysis

    The population characteristics according to exposureto air-conditioning systems were analyzed using chisquare tests. Univariate and multiple logistic modelwere estimated in order to analyze the variables

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    associated with nasal and eye symptoms, recurrentwheezing and building-related worsening of the symp-toms. The comparison of the crude symptoms preval-ence and the symptoms-adjusted odds ratios in naturalventilation and HVAC groups assessed the role of air-conditioning as determinant of the symptoms. Thesymptoms were the dependent variables and the

    independent variables were gender, age, accumulatedworking time in the building, smoking habits, passivesmoking, history of familiar allergy, previous medicaldiagnosis of asthma and rhinitis and the air-condition-ing system groups. The variables that remained at thefinal model were either significant (P < 0.05) or wereconfounding.

    Results

    The response rate was 79.8%, totalizing 1994 respond-ers of 2500. Among the responders, 1885 subjects

    identified themselves and 139 decided to be anony-mous. The characteristics of the population studied arepresented in Table 1.

    The group of individuals working under HVACsystems had a higher prevalence of nasal, naso-ocular,sinusitis symptoms, persistent cough and buildingrelation of the symptoms, when compared with indi-viduals under natural ventilation (P < 0.05) (Table 2).

    Upper airways symptoms such as nasal, naso-ocularand sinusitis had a significant association with workingunder the HVAC system in the univariate logisticregression. Breathlessness episodes, persistent coughand building relation of the symptoms also hadsignificant association with air-conditioning (Table 3).

    Upper airways symptoms such as nasal, naso-ocular

    and sinusitis maintained positive significant associa-tions with working under the HVAC systems, whereaslower airways as chest wheezing or breathlessnessepisodes showed no significant association with air-conditioning in the multivariate model. Persistentcough and building relation of the symptoms hadsignificant association with the HVAC system after theadjustment (Table 4).

    Discussion

    This work suggests that sealed buildings with air-

    conditioning are associated with a higher prevalence ofwork-related upper respiratory symptoms than build-ings with natural ventilation, in spite of being a tropicalcountry with high relative and absolute humidity ratesall around the year.

    All self-administered questionnaires can lead to bias.Workers experiencing more symptoms and perceptionof disease are more likely to complete the question-naire. Differences in response rates were attributed todifferent work organizations and collaborative profile,however a selection bias cannot be ruled out, in spite ofgood percentage of overall responders (79.8%). Thereare some potential information biases such as different

    job organizations factors (public to private practices),job satisfaction, quantity of work and job-related stressand other unknown job-related factors that couldinfluence the outcomes (Crawford and Bolas, 1996), inspite of the evidence that these factors could notaccount for the differences between the buildings (Skovet al., 1989). The participants were informed about thegeneral objective of studying the environmental health,launched together with the non-smoking policy in largepublic and office buildings. The blinding of the studyobjective and the blinding of the division of the groupsprobably minimized the information bias and other

    selection biases seems unlikely as the survey was notbased on previous sick-buildings symptoms reports.The adequacy of the control population is alwaysquestionable, because there are virtually no officebuildings without any kind of air-conditioning ormechanical ventilation. Differences between bothgroups such as age, gender, accumulated work time,smoking habits and atopic background were adjustedin the multivariate regression. The reported previousdiagnosis of asthma of 10.912.8% and allergic rhinitisfrom 31.8 to 32.1%, are in accordance with previousprevalence studies of allergic diseases in Brazil (Soleet al., 2001; Vanna et al., 2001). The overall respiratory

    Table 1 Population characteristics according to their ventilation system

    Variable HVAC group Control group

    Response rate 77.1 90.6Gender (male) 45.8 85.9

    Age (years; s.e.m.) 29; 0.29 20; 0.09

    Accumulated work ti me (years; s.e. m. ) 3. 00; 0.18 3. 00; 0.11

    Smoking (active) 15.4 4.8

    Passive smoking

    At home 16.2 14.1

    At work 7.4 10.4

    Allergy

    Familial allergy 14.1 16.2

    Previous diagnosis of asthma 10.9 12.8

    Previous diagnosis of allergic rhinitis 32.1 31.8

    Values are presented as percentage unless indicated.

    HVAC, heating, ventilation and air-conditioning, control group, natural ventilation;

    s.e.m., standard error of mean.

    Table 2 Symptoms distribution according to ventilation system

    Symptom

    Natural ventilation

    (n 453) n (%)

    HVAC (n 1541)

    n (%) P-value (v2)

    Nasal symptoms 271 (60) 1023 (66.4) 0.011

    Naso-ocular symptoms 120 (38.3) 563 (46.9) 0.007

    Sinusitis symptoms 114 (25.2) 538 (35.0)

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    symptoms prevalence in air-conditioned buildings issimilar to other studies in Brazil (Costa and Brickus,2000; Graudenz et al., 2002a; Santos et al., 1992),

    confirming indoor air related problems as an importantissue in Brazil.

    Atopic related (allergic) conditions such as previousdiagnosis of asthma or allergic rhinitis, were consis-tently associated with IAQ complains as demonstratedin other studies (Bjornsson et al., 1998; Brooks, 1994;Ooi and Goh, 1996), possibly because of a lowerthreshold of the respiratory mucosal immune system todifferent stimuli, as most studies on allergen exposureassessment and symptoms in office buildings show lowallergen levels and no correlation of symptoms withmeasured allergens (Graudenz et al., 2002b; Menzies

    and Bourbeau, 1997).The association of nasal symptoms of itching,pruritus and nasal discharge with HVAC systems,when compared with natural ventilation (OR 1.59,95% CI 1.112.28) are similar to those reported byJaakkola and Miettinen, 1995, and to the study ofreanalysis of epidemiologic studies by Mendell andSmith (1990). The ocular involvement found in ourstudy have also similar OR to these two previousstudies. The positive association of persistent cough toHVAC without humidification systems was significant(OR 3.04, 95% CI 2.004.63). Coughing is a non-specific symptom, which could reflect irritation or

    inflammation either from upper or lower airways, butits association to building occupancy is an importantmarker of poor IAQ (Allermann et al., 2003; Wan andLi, 1999; WHO, 1983). Of great interest is theassociation of sinusitis symptoms and this type of air-

    conditioning system. Sinusitis can be a result odifferent conditions including viral, bacterial, fungaltoxic and allergic conditions that affect the sinussystem. Sinusitis can be aggravated by concomitanrhinitis commonly reported in indoor air surveys, butits diagnosis frequently needs an imaging complement-ary exam.

    Lower respiratory symptoms such as wheezingshortness of breath and tight chest symptoms can berelated to IAQ problems (Burge et al., 1985; Jaakkolaand Jaakkola, 1999; Mendell et al., 1996). Symptomsof wheezing and shortness of breath were not associated with air-conditioning in our population sample

    This is in accordance with another study with similardesign (Robertson et al., 1985), suggesting that inabsence of conditions such as hypersensivity pneumo-nitis, or humidifier fever, upper airways could bemore sensitive to air-conditioning-related conditionsthan lower airways in this context (Graudenz et al.2002b). These results should be carefully interpretedas lower respiratory symptoms are rare symptoms andthe non-statistically significance may be misguidingbecause of large CIs. Prospective studies and detailedinvestigation on cases may add additional informationon this specific subject. More research in differen

    climatic and geographic conditions are needed toconfirm IAQ issues as a global matter of publichealth.

    Acknowledgements

    This work was partially supported by grants obtainedfrom the following Brazilian institutions: FAPESP(Sao Paulo State Foundation for Research Supportand CNPq (National Research Council). We thankDr Paulo Hilario Saldiva for insightful discussionsDr Latorre thanks the CNPq for the researchfellowship.

    Table 3 Univariate analysis of risk factors associated with respiratory symptoms

    Outcome Working under HVAC Atopic background Female gender Active smoking habits Second-hand smoke

    Nasal symptoms 1.33 (1.071.65) 9.63 (7.1512.98)a 1.57 (1.291.91) 0.61 (0.470.79) 1.86 (1.312.64)

    Naso-ocular symptoms 1.42 (1.101.83) 2.80 (2.343.59)a 1.42 (1.101.83) 1.22 (0.891.69) 1.29 (0.941.79)

    Sinusitis 1.56 (1.241.97) 2.83 (2.323.45)a 1.47 (1.211.79) 1.99 (1.452.73) 1.15 (0.891.49)

    Persistent cough 1.90 (1.482.44) 2.93 (2.233.85)b 1.43 (1.171.75) 0.89 (0.661.19) 1.03 (0.791.34)

    Chest wheezing 1.00 (0.751.33) 8.24 (6.1511.05)b

    0.99 (0.771.29) 1.60 (1.152.22) 1.28 (0.861.91)

    Breathlessness 1.42 (1.091.85) 17.26 (12.5523.74)b

    1.72 (1.382.14) 0.86 (0.621.19) 1.43 (1.021.99)Buil ding related worseni ng 5. 38 ( 3.807.63) 0. 82 ( 0. 661.02)a 1.59 (1.271.99) 0.80 (0.571.13) 2.03 (1.432.89)

    Values are presented as OR (95% CI).

    Analysis of odds ratio for univariate logistic regression.

    Atopic background: aprevious diagnosis of allergic rhinitis, bprevious diagnosis of asthma.

    Table 4 Working with HVAC systems as a risk factor for respiratory symptoms as

    compared with natural ventilation

    Outcome

    OR

    crude

    95% CI

    crude OR

    OR

    adjustedb

    95% CI

    adjusted ORb

    H & La

    Nasal symptoms 1.32 1.071.64 1.59 1.112.28 0.57

    Naso-ocular symptoms 1. 42 1.101.83 1 .58 1.052.38 0. 55Sinusitis 1.60 1.262.03 1.85 1.272.71 0.94

    Persistent cough 1.90 1.482.43 3.04 2.004.63 0.41

    Chest wheezing 1.01 0.751.35 1.33 0.842.11 0.59

    Breathlessness 1.43 1.101.87 1.36 0.852.17 0.00

    Building-related worsening 5.33 3.807.47 4.92 2.938.27 0.20

    aHosmer and Lemeshow goodness of fit.bAdjusted by age, gender, atopic background, smoking habits and accumulated work time.

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