Journal of Toxicology and Environmental Health, Part B Critical Reviews

ISSN: 1093-7404 (Print) 1521-6950 (Online) Journal homepage: http://www.tandfonline.com/loi/uteb20

Indoor Air Quality and Sources in Schools and Related Health Effects Isabella Annesi-Maesano , Nour Baiz , Soutrik Banerjee , Peter Rudnai , Solenne Rive & on behalf of the SINPHONIE Group To cite this article: Isabella Annesi-Maesano , Nour Baiz , Soutrik Banerjee , Peter Rudnai , Solenne Rive & on behalf of the SINPHONIE Group (2013) Indoor Air Quality and Sources in Schools and Related Health Effects, Journal of Toxicology and Environmental Health, Part B, 16:8, 491-550, DOI: 10.1080/10937404.2013.853609 To link to this article: https://doi.org/10.1080/10937404.2013.853609

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Journal of Toxicology and Environmental Health, Part B, 16:491–550, 2013 Copyright © Taylor & Francis Group, LLC ISSN: 1093-7404 print / 1521-6950 online DOI: 10.1080/10937404.2013.853609

INDOOR AIR QUALITY AND SOURCES IN SCHOOLS AND RELATED HEALTH EFFECTS Isabella Annesi-Maesano1,2, Nour Baiz1,2, Soutrik Banerjee1,2, Peter Rudnai3, Solenne Rive1,2, on behalf of the SINPHONIE Group 1

Université Pierre et Marie Curie, Paris 6, UMR S 707: EPAR (Epidémiologie des maladies allergiques et respiratoires), Medical School Saint-Antoine Paris, France 2 INSERM U 707: EPAR, Paris, France 3 NIEH, Budapest, Hungary Good indoor air quality in schools is important to provide a safe, healthy, productive, and comfortable environment for students, teachers, and other school staff. However, existing studies demonstrated that various air pollutants are found in classrooms, sometimes at elevated concentrations. Data also indicated that poor air quality may impact children’s health, in particular respiratory health, attendance, and academic performance. Nevertheless, it should be noted that there are other adverse health effects that are less documented. Few data exist for teachers and other adults that work in schools. Allergic individuals seem to be at a higher risk for adverse respiratory health consequences. Air quality improvement represents an important measure for prevention of adverse health consequences in children and adults in schools.

Children constitute a sensitive population to environmental contaminants exposure, including air pollution (Bennett et al., 2008; Firestone et al., 2008; Foos et al., 2008). The respiratory, immune, reproductive, central nervous, and digestive systems in children are not fully developed (Makri et al., 2004). The different anatomic barriers are not yet well established and allow easier entry of toxic substances that affect their organs and development (Firestone et al., 2008; Makri et al., 2004). Children breathe a larger volume of air than adults (Bennett et al., 2008; Foos et al., 2008). Both the route of breathing, nasal versus oral, and the effectiveness of the nose with aerosols may differ between children and adults such that the lungs of children are exposed to higher concentrations of air pollutants (Bennett et al., 2008). Children may be also more exposed to

air pollution because of their behavior, as they are more physically active with an exploratory nature, including exposure by crawling in contact with the floor. Children spend approximately 65 to 90% of their time in indoor environments, with a large portion at school (65% of the indoor time is spent at home). Thus, the indoor school environment requires particular attention. Asthma prevalence has increased in most countries in the past decades (Burney, 1990; Eder, 2006) and asthma has become the predominant chronic disease in childhood. In addition, the frequency of other allergies has also risen in the past decades. Risk factors for asthma and allergy may be categorized as (1) host or (2) environmental. Host factors include heredity, gender, race, and age, with heredity being by far the most significant. However, the recent

The authors thank the SINPHONIE partners and in particular the SINPHONIE coordinators: Dr. Éva Csobod, REC (Hungary), Prof. Eduardo de Oliveira Fernandes, IDMEC-FEUP (Portugal), Dr. Stylianos Kephalopoulos, JRC (European Commission), and Dr. Péter Rudnai, NIEH (Hungary). The SINPHONIE project was funded by the European Parliament and run by European Commission Health and Consumer Protection DG. Address correspondence to Dr. Isabella Annesi-Maesano EPAR Department, UMR-S 707 INSERM and UPMC Paris 6, Medical School Saint-Antoine, 27 rue Chaligny, 75571 Paris CEDEX 12, France. E-mail: [email protected] 491

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increases in the incidence of allergic disorders cannot be explained by genetic factors that are postulated to require longer periods to act than the decades that have seen the asthma and allergies epidemics. Four major environmental candidates are alterations in exposure to infectious diseases during early childhood, environmental pollution, allergen levels, and dietary changes. Among various environmental factors that have changed significantly over time and that may play an important role in the development of asthma and allergies is indoor air pollution, which constitutes a prominent factor due to exposure duration, new efficient buildings insulation techniques, and emergence of new air pollutants such as the volatile organic compounds (VOC). Samet and Krewski reported on the most common indoor air pollutants, with their typical sources and concentrations measured in the home, office, and transportation microenvironments, and addressed the impacts of air pollutants on human health (Samet and Krewski, 2007). Subsequently, an increasing number of studies confirmed that indoor air pollutants were responsible for asthma, allergies, and chronic obstructive pulmonary disease (COPD) (Mendell, 2007; Viegi et al., 2004). Air pollutants were categorized into three major source groups: (1) combustion sources (tobacco smoke, nitrogen dioxide [NO2 ], carbon monoxide [CO], and wood smoke), (2) biologic sources (infectious agents, molds, and allergens), and (3) other sources (radon, VOC, and formaldehyde [HCHO]). All three families of air pollutants were found to produce airways injury, damage, and adverse effects if inhaled in sufficient quantities and concentrations. Viegi et al. (2004) noted that indoor air pollution may increase the risk of allergic sensitization, irritation phenomena, acute and chronic respiratory disorders, and lung function impairment. Indoor air pollutants considered were environmental tobacco smoke, particulate matter (PM), nitrogen dioxide, carbon monoxide, volatile organic compounds, cleaning products, and biological allergens. Mendell (2007) summarized 21 studies on the associations between indoor residential chemical emissions,

I. ANNESI-MAESANO ET AL.

or emission-related materials or activities, and respiratory health or allergy in infants or children. Risk factors identified most frequently included formaldehyde (HCHO) or particle board, phthalates or plastic materials, and recent painting. Findings for other air pollutants, such as aromatic and aliphatic chemical compounds, were limited but suggestive. Elevated risks were also reported for sources of air pollutants such as renovation and cleaning activities, new furniture, and carpets or textile wallpaper. Recently, Hulin et al. (2012) described the main epidemiological studies that evaluated the respiratory effects of indoor air pollutants as assessed through objective quantitative measurements in industrialized countries. The evidence was reliable for indoor NO2 and particulate matter (PM), which are associated with asthma, bronchitis, and COPD. Whereas HCHO and VOC seem to be the main pollutants in indoor settings, relevant studies on their respiratory effects are still scarce, and are limited to asthma and bronchitis. Molds have been associated with an enhanced risk of asthma and COPD. Contradictory results were found between endotoxins and asthma. The roles of phthalates, persistent organic pollutants, and flame retardants in respiratory diseases remain to be established. Indoor environments considered in these studies included dwellings, workplaces, schools and day-care centers, bars, discotheques, and vehicles, and all classes of age were included without stratification. Daisey et al. (2003) focused specifically on school environment, in which children spend the largest part of their time after home, by reviewing the literature published until 1999 on indoor air quality (IAQ), ventilation, and building characteristics in schools and identified commonly reported school buildingrelated health symptoms. Air pollutants for which data were available in schools according to this study encompassed the following: carbon dioxide (CO2 ), VOC, including formaldehyde (HCHO), bacteria, house-dust mites, and animal allergens. Reported associations between the presence of specific air pollutants and health effects included: (1) CO2

INDOOR AIR QUALITY AND HEALTH EFFECTS IN SCHOOLS

and headaches, dizziness, tiredness, and inability to concentrate; (2) mold exposure and throat and nasal complaints; (3) respirable dust and eye problems; and (4) VOC, HCHO, bacteria, viable molds, and cat allergens in settled dust and asthma. It was also noted that schools buildings frequently encountered inadequate ventilation, as the American Society of Heating, Refrigerating and Air-Conditioning Engineers (ASHRAE) standards (1000 ppm CO2 , equivalent to a minimum ventilation rate of 8 L/s-person for classrooms) were exceeded in many situations. One of the main outcomes of this study was to identify the lack of information regarding the school environment, in particular the prevalence of symptoms and diseases in schoolchildren or teachers with exposures to air pollutants quantitatively measured in schools. This argument is still valid today. Since then, data have been published on the impact of air pollutants and building characteristics on health of occupants in schools, but no comprehensive review has apparently been published on these topics with the exception of a study by Cartieaux et al. (2011) that focused on air pollutants and related sources in classrooms. The impact of health effects of school environments is currently an urgent need globally, as the number of students and teachers continues to grow and is increasing. There are more than 64 million students and almost 4.5 million teachers attended preprimary (15 million), primary (28 million), and lower secondary (22 million) schools in 2012 in Europe, where children daily spend up to onethird of their time in school buildings, including kindergartens, making schools a relevant source of exposure. In many of the European Union countries, schoolchildren aged 7–10 years are taught for more than 800 h per year and students aged 10 years or more spend a further 50–100 h in classrooms (EUROSTAT). At school, each pupil is exposed to indoor air pollutants potentially producing adverse health implications for the state of health of a large and sensitive proportion of the population. In 1999, the European Federation of Asthma and Allergy Association (EFA) launched

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a European-funded project called Indoor Air Pollution in Schools, with the primary goal being to collect information on air pollution in European schools and its consequent effects on asthma and allergy. This corresponding report presents the reviewed European air quality data obtained from measurements in school buildings during varies studies, published in various languages by different research groups. The objective was to generate an overview of (1) measured air pollutant concentrations in schools throughout Europe, (2) social and technical building parameters that were found to be related to the presence of specific air pollutants in school buildings, and (3) reported relationships between the presence of certain indoor air pollutants and adverse health effects. In addition, the air pollutant concentrations were compared to the existing guidelines of ASHRAE for CO2 (1000 ppm) and the National Ambient Air Quality Standard (NAAQS) for NO2 (99.7 μg/m3 or 0.053 ppm). Formaldehyde concentrations were compared to levels reported to be associated with adverse health effects. Currently, HCHO guideline values exist in various countries. The SINPHONIE (Schools Indoor Pollution and Health Observatory Network in Europe) project is a complex research project funded by the European Union (EU), intended to improve air quality in schools and kindergartens, to reduce respiratory disease due to outdoor and indoor air pollution in children and teachers, and to define policy recommendations on remedial measures in the school environment. Twenty-three countries from all of Europe are involved in this project. The aim of the present investigation was to provide a state of the art of the literature on adverse health effects, particularly respiratory health, because of the inhalation route of air pollutants that are associated with IAQ and/or building characteristics in schools as a constitutive stage of forthcoming projects focusing on health effects of indoor environmental quality in schools in order to ensure long-term environmental equalities and health at schools for school children and teachers.

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I. ANNESI-MAESANO ET AL.

APPROACH The scientific literature on school environment, indoor air quality particularly, and associated adverse health effects was reviewed from 1992 to 2012. Studies examined in PubMed included the two following topics: (1) air quality at school and health effects in school children or teachers, including air quality in classrooms and in school yards; and (2) school building characteristics and health effects in schoolchildren. The following keywords were used in our search: all principals indoor air pollutants (nitrogen dioxide or NO2 , ozone or O3 , formaldehyde, molds, bacteria, allergens, sulfur dioxide or SO2 , carbon dioxide or CO2 , carbon monoxide or CO, volatile organic compounds [VOC], and particulate matter such as PM10 , PM2.5 ), indoor air quality, school, children, ventilation, heating, building characteristics, temperature, humidity, health, respiratory health, and asthma. Articles had to be written in English and available on the PubMed website. Overall, 67 papers written in English existed on air quality or air pollution in schools, 56 on ventilation in schools, 6 on comfort parameters in schools, and 12 on school building characteristics. Air Pollutants Measured in Schools and Related Adverse Health Effects Air Pollutants and Sources Found in the School Environment Thus far, the following air pollutants and related sources have been objectively assessed in schools: NO2 , O3 , HCHO, SO2 , CO2 , CO, VOC, PM10 , PM2.5 , mold, bacteria, and allergens (Table 1). In classrooms, CO, CO2 , and NO2 are known mainly to derive from combustion sources such as heaters, gas-and woodstoves, fireplaces and smoking when allowed. The children’s metabolism is also a source of CO and CO2 . Main outdoor sources of CO, CO2 , NO2 , and O3 in urban settings are vehicle traffic emissions. Street-level intake vents and attached garages also produce an elevation of their indoor concentrations (Batterman et al., 2007). In schools, highest NO2 concentrations were measured by proximity to vehicular traffic roads (Norback

et al., 2000). Besides inorganic gaseous pollutants, combustion sources release HCHO, suspended particulates that are inhaled, and other toxic chemicals. Formaldehyde is emitted also via urea formaldehyde foam insulation, glues, fibreboard, pressed board, plywood, particle board, carpet backing, and fabrics (http://www.hc-sc.gc.ca/ewh-semt/air/in/poll/ construction/formaldehyde-eng.php). More than 1000 VOC have been identified thus far (U.S. Environmental Protection Agency [EPA], 1989). VOC are emitted from (upholstered) furnishings such as desks, shelves, and chairs and tend to increase under high temperatures (Norbäck, 1995; Smedje et al., 1997). Other known emission sources of VOC in schools are resins of wood products, adhesives, glues, paints, polyurethane, coatings, sealants, polishes, cleaning products, carpets, tiles, outdoor air (traffic emissions), and personal care products. In addition, VOC were found to be related to building dampness (Norbäck, 1995). Finally, in the countries where smoking at school is not forbidden, tobacco products also release a mixture of more than 4000 compounds, including VOC. Various factors may affect IAQ. Outdoor pollutants including pollen and traffic and factory emissions enter buildings through open windows, ventilation system air intakes, and building leaks and cracks. These contaminants, along with those that arise inside the building, such as mold spores and chemical emissions from carpeting, wallpaper, furnishings, and cleaning products, concentrate in tightly sealed buildings with inadequate ventilation. Ventilation systems meant to bring in clean or filtered outdoor air to flush out “used” indoor air do not always function properly, because of either poor design or poor maintenance. Many of these described factors were found to be related to concentrations of air pollutants measured inside school buildings. Health Outcomes Assessment Most studies reporting on health effects of school environment were conducted in Europe, the United States, and China using different assessments of health outcomes (Table 2).

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Produced by incomplete combustion of carbon material.

Naturally produced by biological process: metabolic activity of many microorganisms, human being breath. Produced by carbon material combustion of products used by human’s activity.

Carbon dioxide (CO2 )

Monoxide nitrogen (NO) is produced from high-temperature combustion phenomena by air nitrogen oxidation. Dioxide nitrogen (NO2 ) is a secondary pollutant produced by NO oxidation in air.

Characteristics

Carbon monoxide (CO)

Gaseous pollutants Nitrogen oxide (NOx)

Pollutants

TABLE 1. Characteristics and Sources of Air Pollutants in Schools

• Industry • Traffic, combustion activities

• Exhaust gas

• Traffic • Industry

Outdoors (to which schoolchildren and teachers are exposed in the courtyards or indoors by transfer)

Main sources

• Combustion activities • Human being breath In schools: • Same as in the other indoor environments

In general:

• Gas appliances or heater • Outdoor air (transfer) • Cigarette smokers (when allowed)

In schools:

• Combustion appliance not or badly connects with an exhaust duct, using in badly ventilation condition, badly maintained or badly used. • Gas exhaust duck leak • Cigarette smoke

In general:

• Gas appliances or heater • Transfer from outdoors • Cigarette smokers (when allowed)

In schools:

• Gas appliances (gas stove, gas heater, gas boiler, water-heater, and oil heater), • Wood heater • Cigarette smoke

In general:

Indoors (to which schoolchildren and teachers are exposed in classrooms or other school premises)

Indoors

(Continued)

Both outdoors and indoors

Both outdoors and indoors

Assessment in schools

496

Semivolatile organic compounds (SVOC)

Volatile organic compounds (VOC)

Sulfur dioxide (SO2 )

Pollutants

TABLE 1. (Continued)

SVOC are nonvolatile compounds at ambient temperature but volatile with a hot source contact (such as a heater). Their ebullition point is > 250◦ C. These compounds can be phthalates, PAH, and PCB and most of the pesticides.

It comes from fossil fuels combustion where sulfurated impurities are oxidized by air oxygen in sulfur dioxide. Gas very soluble in water. When this pollutant is hydrated it becomes sulfuric acid, a very corrosive acid. VOC is composed by a set of substance (more than 500 identified in indoor environment) belonging to different chemical families. Substances common point is to evaporate at ambient temperature. VOC can be of natural origin (terpenes, aldehydes from wood) or of organic origin (benzene, toluene, xylene). A VOC is defined by its ebullition point, which must be ≤ 250◦ C in normal pressure conditions.

Characteristics

/

• Industries • Traffic

• Diesel motor cars • Industry (sulfuric acid production, oil refining, etc.) • Electric production plants • Urban boiler rooms • Carbon combustion • Volcano

Outdoors (to which schoolchildren and teachers are exposed in the courtyards or indoors by transfer)

Main sources

• PVC floor, plasticizing In schools: • Same

In schools: • Same In general:

Sprays Cleaning product Indoor perfumes Do-it-yourself product Insecticide Gasoline vapor New books and magazines Furniture Wall covering (paints), floor covering (wooden floor, linoleum, PVC floor), ceiling • Implementation and finish products (solvents, glue, varnish)

• • • • • • • • •

In general:

• Outdoor air (industries, factories . . . ) • Domestic heaters In schools: • Appliances or heater • Outdoor air (transfer)

In general:

Indoors (to which schoolchildren and teachers are exposed in classrooms or other school premises)

Both outdoors and indoors

Mainly outdoors

Assessment in schools

497

Radon

Formaldehyde

Microbial volatile organic compounds (MVOC)

Organic compound from aldehydes family. Gas very volatile and soluble in water but instable. Radioactive and natural gas, from uranium and radium disintegration. Found in Earth’s crust, in particular granitic and volcanic stones.

Microbial volatile organic compounds (MVOC) are composed of low molecular weight alcohols, aldehydes, amines, ketones, terpenes, aromatic and chlorinated hydrocarbons, and sulfur-based compounds, all of which are variations of carbon-based molecules. MVOC have a very low odor threshold, thus making them easily detectable by smell.

• Ground, water (contamination by groundwater)

/

Microbes and molds

In schools: • Same

In general: • Some material building (with granite) • Indoor contamination by gas infiltration from the ground by building cracks.

Tobacco Candles, incense stick Gas stove and heater Oil heater, opened chimney • Implementation and finish products • Furnishing products In schools: • Gas stove and heater • Furnishing products • Tobacco smoking (when allowed)

• • • •

In general: Microbes and molds. In schools: Same as in the other indoor environments In general:

Indoors

(Continued)

Both outdoors and indoors

Mostly indoors

498 Gram-negative bacteria membrane contains endotoxins, components that can inflame respiratory mucous membrane by inhalation.

– Viable bacteria: cultivable or revivifiable – Viable bacteria not cultivable or revivifiable (do not develop on a nourishing environment, can be observed in stress conditions) – Dead bacteria: no metabolic activity – Lysed bacteria

Ubiquitous organisms able to develop on a multitude of environments. They can be find in different physiologic states:

Gas very reactive. Secondary pollutant product from transformation, under solar radiation, of pollutants (NO2 , CO, VOCs).

Ozone

Biological pollutants Bacteria

Characteristics

Pollutants

TABLE 1. (Continued)

• Breeding animals • Contagion from human beings

• From pollutant emitted by traffic

Outdoors (to which schoolchildren and teachers are exposed in the courtyards or indoors by transfer)

Main sources

• Domestic animals • Humidity • Miss hygiene • Damp areas In schools: • Pets • Contagion from human beings • Damp areas

At proximity of schools:

Indoors

Both outdoors and indoors

At proximity of schools: • Outdoor air In schools: • Old laser print • Photocopier • Air humidifier • Opening of window

Assessment in schools

Indoors (to which schoolchildren and teachers are exposed in classrooms or other school premises)

499

The most common allergens are:

Allergens

– Dust mite allergens: principally the shells and excrement. Species frequently found are Derp1 and Derf1. – Cockroach allergens: principally their shells and excrements; the most common are Blag1 and Blag2. – Domestic animals allergens: found in saliva, anal glands, and skin. Principal allergens: cat Feld1, dog Canf1, mouse Musm1 – Spore molds: Alt1 for Alternaria alternate – Pollen allergens: birch Betv1, ambrosia Amba1

Many species found in indoor environment, the most common being Aspergillus and Penicillium. Can emit in atmosphere different substances including allergens, mycotoxins, glucans, and special VOCs.

Mold

• Pollens from vegetation • Water damage • Domestic animals

• Water damage

In schools: Same (but in the case of pets)

• Water damage • Humidity • Nourishing element presence (organic matter: building material, etc.) • Domestic animals • Bedding • Soft furnishing • Houseplant • Dust • Outdoor air (pollens and molds)

In general:

In schools: • Same

Infiltration, water damage Humidity Insulation badly controlled Nourishing element presence (organic matter: building material, etc.) • Poor maintenance of the ventilation system

• • • •

In general:

Indoors

Indoors

(Continued)

500

Particle pollutants Fibers and particles (do not include asbestos)

Pollutants

TABLE 1. (Continued)

Fiber are lengthened particles where length is three times superior at least to the diameter: (length/diameter) > 3. Fibers in which diameter is 1 indicate that exposure to the unflued gas heater compared with the flued gas heater is associated with an increase risk of symptoms All Morning wheeze: Atopic subgroupMorning symptoms: Morning cough: Morning wheeze: Stomachache: Use of bronchodilators for relief of symptoms: Prevalence of both upper and lower respiratory symptoms were significantly higher in the school with coal-fired heating than in that with central heating

Statistically significant relationships (odds ratios or relative risk [95% confidence interval])

Aint 60/38∗∗∗ Aref 42/39 Bint 52/54 Bref 54/53 Aint 60/41∗∗∗ Aref 44/36 Bint 59/58 Bref 57/51 Aint 46/22∗∗∗ Aref 26/25 Bint41/41 Bref 38/36 Aint 28/13∗∗∗ Aref16/16 Bint 30/29 Bref22/25 Aint 19/15 Aref 18/15 Bint 12/9 Bref 13/17 Aint 36/18∗∗∗ Aref 24/22 Bint 26/25 Bref 24/22 Aint 23/13∗∗∗ Aref 20/20 Bint 33/26∗ Bref33/27 Aint 34/12∗∗∗ Aref 16/17 Bint 16/16 Bref 18/17 Aint 19/7∗∗∗ Aref 10/7 Bint 10/10 Bref 10/9

1.6∗∗ [1.17–2.2] 0.8∗∗ [0.6–0.99] 0.76∗∗ [0.6–0.97] 1.85∗∗ [1.3–2.7] 1.6∗∗ [1.06–2.5] 1.87∗∗ [1.07–3.24]

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Koskinen et al. 1997

Taskinen et al. 1997

Taskinen et al. 1999

Ahman et al. 2000

RR. 4 schools: 2 mold-exposed (1 and 3), 2 non mold-exposed (2 and 4) (1 vs.2) //3 vs.4). First follow-up period: Sore throat: 2.22 [1.39–3.55]//2.96 [1.59–5.48] Hoarseness: –//2.23 [1.49–3.33] Nasal congestion: 2.24 [1.70–2.95]//– Purulent nasal discharge: 1.77 [1.26–2.49]//1.61 [1.12–2.31] Nonpurulent nasal discharge: 1.94 [1.4-2.7]//– RR. 4 schools: 2 mold-exposed, 2 non mold-exposed (1 vs.2//3 vs.4). Second follow-up period: Hoarseness: –//2.4 [1.02–5.66] Nasal congestion: 2.27 [1.42–3.64]//1.6 [1.04–2.44] Purulent nasal discharge: 4.06 [1.38–11.92]//2.24 [1.24–4.05]

– All but one of the children with asthma came from the moisture problem schools. – Asthma and wheezing symptoms were more common if moisture problems were observed at home and at school. – Significant association between positive reactions to moisture indicative molds and asthma

(Continued)

Fatigue (fall): Aint 46/32∗∗∗ Aref 28/36∗ Bint 67/64 Bref56/64∗ Headache (fall): Aint 53/40∗∗∗ Aref 36/36 Bint 61/61 Bref 49/52 Difficulties in concentration (fall): Aint 19/17 Aref 15/14 Bint 30/27 Bref 20/25 Before the intervention (A = damaged school and B = reference school) Results among personnel: Frequency of dry throat and hoarseness was significantly elevated in school (A) and there was a tendency to more eye irritation, cough, dyspnea. headache and fatigue Results among children: Generally less complaints than the personnel The frequency of eye irritation, stuffy nose and fatigue was significantly elevated at school (A) After the intervention Results among personnel: Most of symptoms had diminished and compared to school (B) were no longer significantly elevated (except for skin irritation in the face) Results among pupils: Slight decrease of symptoms was noted and the occurrence of eye irritation was significantly reduced. In comparison with the school (B) there were still elevated frequencies of several symptoms at school (A) Asthma prevalence was similar in index school (with moisture problems) and in reference school (4.8%). The children of the index school more often had wheezing (16% vs. 6%, p < .001) and cough (21% vs. 9%, p < .001). The difference between the schools was significant in emergency visits, OR = 2, p < .01 and antibiotic courses, OR = 2.1, p < .01 No significant differences in the frequencies of asthma, asthma-like conditions or allergic diseases between the children from the four schools with different grades of moisture problems and mold exposure. Preliminary evidence for an association between moisture or mold problem in the school building and the presence of manifest and occult asthma in the pupils:

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Carpet on the floor and woken up by wheeze at night, OR =1.64 (1.12–2.41) Poor ventilation and higher prevalence of bronchitic and asthmatic symptoms Protective effect of air conditioning for bronchitic symptoms Wall-to-wall carpet in the workplace was related to chronic symptoms Removal of wall to wall carpet reduced the number of symptoms (p < .05) Current asthma: Size of school+ : 1.6∗∗∗ [1.2–2.1], + OR expressed as change of coefficient per 10 employees Shelf factor: 1.4∗∗∗ [1.2–1.6] OR tertiles: Asthma hospitalization rate > 11.68/10,000 (top tertile) Roofing: 1.76∗∗ [1.13–2.74] Exterior walls: 2.24∗∗ [1.31–3.83] Floor finishes: 1.75∗∗ [1.14–2.69] Boiler/furnace: 1.71∗∗ [0.99–2.94] Among children, no correlation was demonstrated between symptoms/diseases and the results of technical measurements of manmade mineral fiber (MMMF) in the ceiling. Among adults, the concentration of airborne respirable/nonrespirable MMMFs was positively correlated to eye irritation (p = .03/p = .004). The presence of settled nonrespirable MMMFs on surfaces occasionally cleaned was positively correlated to skin irritation among adults (p = .005). For higher frequency of both floor mopping and desk cleaning there is beneficial effect on clinical signs of the nasal mucosa. The use of wet mopping seemed disadvantageous in comparison with dry mopping.

Plastic floor covering and doctor-diagnosed allergies, OR = 1.33 (1.12–1.58)

The traditional classroom type; relative to a portable classroom was associated with approximately 2% increase in attendance and with a 2.5% decrease in absence OR 95% CI for moisture damaged schools vs. reference schools stratified on building type All schools Nocturnal cough: 1.5∗∗ [1.19–1.9] Cough without phlegm (spring): 1.55∗∗ [1.24–1.92] Cough with phlegm (spring): 1.36∗∗ [1.11–1.68] Concrete/brick schools Nocturnal cough: 1.45∗∗ [1.12–1.87] Cough without phlegm: 1.58∗∗ [1.24–2.03] Wooden schools Cough with phlegm (spring): 2.25∗∗ [1.26–4.02]

Adjusted risk of work-related eye and respiratory symptoms was in general higher among day-care workers exposed to both water damage and mold odor than among the unexposed.

Statistically significant relationships (odds ratios or relative risk [95% confidence interval])

Note. Significant differences indicated by: ∗ p < .05; ∗∗ p < .01; ∗∗∗ p < .001.

Walinder et al. 1999

Rindel et al. 1987

Belanger et al. 2006

Smedje et al. 1997

Norbäck et al. 1990

Other characteristics Csobod et al. 2010 (SEARCH Study)

Meklin et al. 2002

Building type Shendell et al. 2004

Ruotsalainen et al. 1995

Building characteristics

TABLE 19. (Continued)

INDOOR AIR QUALITY AND HEALTH EFFECTS IN SCHOOLS

Respiratory symptoms were also higher in the first case. Marks et al. (2010) compared pollution levels and health effects of flued and unflued gas heaters. It appeared that pollutant concentrations were higher in the case of unflued gas heaters (Marks et al., 2010). In addition, this heating type was associated with morning wheeze and with morning cough, wheeze, and use of a bronchodilator in the atopic group. Finally, building age is suspected to have an impact on occupant health. Kim et al. (2007) showed a tendency for more symptoms in newer schools compared with older ones. Other Building Characteristics Other building characteristics that have been studied are renovation in health and moisture damage effects. Renovation appears to be beneficial in most cases for children’s health, with a positive effect on stuffy nose, rhinitis, sore throat, hoarseness, cough, eye symptoms, and fatigue (Meklin et al., 2005; Lignell et al., 2005). Building moisture damage exerts a negative impact on health, with symptoms more frequently occurring in damaged schools (Taskinen et al., 1997, 1999; Koskinen et al., 1997). In addition, more mold proliferation was observed in damaged schools than in reference schools (Lignell et al., 2005). Koskinen et al. (1997) noted thay a mold problem in day-care centers was associated with overall morbidity increase in comparison with reference day-care centers. Children suffered from upper-respiratory-tract symptoms at least once during the study period (sore throat and nasal congestion). A significantly elevated risk for sore throat, hoarseness, nasal congestion, purulent and nonpurulent nasal discharge, cough, and common cold was found when total numbers of symptoms days were compared. The mold-exposed children displayed such symptoms repeatedly or symptoms were prolonged. Finally, in schools made with bricks a higher risk of nocturnal cough and cough without phlegm due to moisture damage than in schools made with wood was found (Meklin et al., 2002). Materials used inside for floors or walls also impact on health. Csobod et al. (2010)

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(http://search.rec.org) reported that plastic floor were linked with doctor-diagnosed allergies in children (OR = 1.33). Norbäck et al. (1990) found that wall-to-wall carpets in the workplace were related to chronic symptoms in teachers. Smedje et al. (1997) also showed that the presence of shelves in classroom increased the risk of current asthma (OR 1.4, 95% CI 1.2–1.6). Human activities inside school buildings have also been associated with occupants’ health. Cleaning frequency and material used may exert an effect on schoolchildren’s and teachers’ health (Walinder et al., 1999). However, these have rarely been investigated. Other Health Effects of School Environments In addition to respiratory diseases, indoor air pollutants are at the origin of other adverse effects (Table 3). Formaldehyde has been related to headache (Wantke et al., 1996), and CO to eye problems (Carrer et al., 1994). VOC are associated with adverse health effects like irritation of the eyes and skin, and at higher concentrations many of the VOC produce liver and kidney damage (Wieslander and Norback, 2010). In general, IAQ was correlated with sick building syndrome (SBS) (Norback et al., 1990). There is persuasive evidence linking higher indoor concentrations of NO2 to reduced school attendance, and suggestive evidence correlating low ventilation rates to reduced performance. Regarding indirect associations, many studies linked indoor dampness and microbiologic pollutants (primarily in homes) to asthma exacerbations and respiratory infections, which subsequently were associated with reduced performance and attendance. Overall, evidence suggests that poor indoor environmental quality (IEQ) in schools is common and adversely influences the performance and attendance of students, primarily through adverse health effects attributed to indoor pollutants (Mendell, 2005). In addition, HCHO and benzene, which were detected in schools, are well known for their carcinogenic effects, which also applies to radon. Formaldehyde, benzene,

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and radon are classified by the International Agency for Research on Cancer (IARC) as certain carcinogens (group 1) for humans. The European Community recommends action on indoor radon pollution when this pollutant exceeds 400 Bq/m3 for old buildings and 200 Bq/m3 for new buildings. A study conduct in 20 Slovenian schools showed that radon measurements in schools were over these values in most cases (Vaupotic, 2002). Another European study (Darby et al., 2005) found that radon accumulated in dwellings is responsible in Europe for 9% of death by lung cancer. Overall, such potential dangers present in schools need to be considered. DISCUSSION Indoor air quality in schools may be poor and thus responsible for acute and chronic health effects. In terms of short-term events, both chemical and biological air pollutants have been related to various acute symptoms. Zhao et al. (2008) found that when HCHO exposure increased by 1 μg/m3 this was associated with a higher risk of nocturnal attacks of breathlessness in children. Norbäck et al. (2000) showed that higher concentrations of this pollutant and NO2 were correlated with decreased nasal patency and an increase of ECP and lysosyme in NAL in teachers. Simoni et al. (2010) and Fraga et al. (2009) noted that high exposure to CO2 was associated with cough at night. Kim et al. (2005) demonstrated that dog and horse allergens were correlated with higher wheeze risk. PM10 was linked with airway inflammation (Graveland et al., 2011) and a decrease in baseline lung function (Castro et al., 2009; Scarlett et al., 1996). High concentrations of this pollutant were also associated with cough (Simoni et al., 2010; http://search. rec.org). A significant positive correlation was found between exercise induced-asthma (EIA) and the levels of PM2.5 and acrolein (AnnesiMaesano et al., 2012). SO2 and microbial VOC were associated with nocturnal breathlessness (Kim et al., 2007; Zhao et al., 2008). Finally, higher prevalences of headache, dizziness, concentration problems, itching facial skin, nasal

congestion, and throat irritation were observed in presence of high mold concentration (Meyer et al., 2004, 2011). In terms of chronic events, schoolchildren’s asthma was associated with all air pollutants studied in this review, except SO2 and CO. Risks of asthma attacks, asthma medication, and current asthma were increased in Mi et al. (2006) by 1.18, 1.15, and 1.18 for a rise of 100 ppm in CO2 concentration. In this same study, higher NO2 concentrations were related to current asthma and asthma medication (Mi et al., 2006). An elevated prevalence of past year asthma was found in the classrooms with high levels of NO2 compared with others in the Six Cities Study (Annesi-Maesano et al., 2012). This relationship was observed predominantly for allergic asthma as evidenced by skinprick test (SPT). Annesi-Maesano et al. (2012) correlated asthma in the past year to overall allergic school children to PM2.5 and acrolein. Risks were 1.21-fold higher for children highly exposed in classrooms versus the others. Total VOC concentration was related to chronic airway, chronic general, and chronic eye symptoms by Norbäck et al. (1990). Allergy risks were reported by Annesi-Maesano et al. (2007) with a higher risk of allergic rhinitis in the presence of HCHO concentrations in classrooms and of atopic dermatitis in the presence of high PM2.5 and NO2 concentrations in the school yards. Smedje et al. (1997) first noted an OR of 1.8 between asthma and cat allergens and then a risk of 1.4 with MVOC. Doctor-diagnosed asthma was linked with an OR of 2.07 by Kim et al. (2007). Current asthma risk was increased by 1.4, 1.3, and 1.32 for high bacteria concentrations, VOC levels, and RH (Smedje et al., 1997). Mi et al. (2006) also found for a 10% RH increment a higher current asthma risk (OR 1.8). In one study conducted in teachers, Ebbehoj et al. (2005) noted that women’s reported symptoms from mucous membranes and skin and general symptoms were positively associated with mold exposure. Air pollution in schools was associated with lack of attention and greater absenteeism rate. CO2 and O3 concentration and high temperature increased absenteeism rate in

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Shendell et al. (2004) and Romieu et al. (1992). Mendell (2005) reported influence of school pollutants on school performance and absenteeism: High NO2 concentrations reduced school attendance and low ventilation rate reduced school performance. As a whole, the impact of IAQ was determined in urban schools. Hulin et al. (2011) showed that IAQ was better in rural classrooms than in urban ones, with concentrations up to sixfold lower in the case of NO2 , PM2.5 , HCO, and acetaldehyde. A higher prevalence of asthma and allergies was observed among urban children who attended school with high concentrations of indoor pollutants. From the methodological point of view, comparison between studies is difficult. Materials and methods are different between investigations. The same pollutant may not have been measured with the same material or during the same time period. In dealing with the impact of school environment on the health of students and teachers, it is important to keep in mind the fact that individuals are also exposed to air pollution elsewhere, so that it is not possible to establish a controlled, regulated role of exposure to air pollution in classrooms in the development and/or the aggravation of symptoms and diseases. Thus far, only one study (Martins et al., 2011) considered this feature by introducing the notion of total exposure to air pollution as the sum of the exposures in different microenvironments including the school after having taken into account the daily activity pattern. Still regarding the exposure, the representativeness of the measured concentrations has not been tested through reliability studies. Selection bias constitutes another pitfall of existing surveys because it challenges the representativeness of the studied populations. Misclassification of exposure or health outcomes might also occur. Taking into account potential confounders, there has been scanty information on the impact of IAQ on schoolchildren and teachers. However, recent studies have adjusted for parental smoking, indoor air pollution at home, and frequency of asthma. Finally, the multipollutant mixture issue has not been considered in these school studies

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despite the fact that indoor air pollutants are highly intercorrelated and that appropriate statistical methods have been implemented (Billionnet et al., 2012). In order to improve IAQ at school, indoor sources of air pollution need to be identified. As expected, ventilation plays an important role in pollutants extraction and thus on frequency and severity of symptoms and disease prevalence. Shaughnessy et al. (2013) found that a better ventilation rate improved student performance. Marks et al. (2010) showed that heating strategy is an important choice, as unflued gas heaters were responsible for higher emissions of air pollutants at school and a consequent higher prevalence of symptoms. A recent study focused on examination of ventilation rates in classrooms in Finland and Portugal with two different types of ventilation systems: natural and mechanical, respectively (Canha et al., 2013). The use of ventilation in many buildings indicated a potentially serious IAQ problem and strengthened the need for intervention to improve ventilation rates in naturally ventilated classrooms. It was shown that ventilation affects air pollution differently (Canha et al., 2013). In Portugal in naturally ventilated schools a significant contribution from the activities of occupants inside classrooms yielded higher indoor levels of PM10 levels, whereas the fine fraction of PM2.5 and PM1 was primarily influenced by outdoor concentrations (Madureira et al., 2012). In German schools, indoor PM10 concentrations were approximately sixfold higher than outdoor air (Oeder et al., 2012). In addition, recent data demonstrated that indoor air PM10 on an equal weight base was toxicologically more active than outdoor PM10 (Oeder et al., 2012). All these results indicated that exposure to PM was high among schoolchildren and teachers and highlighted the need for strategies that provide healthier school environments. In particular, ventilation of classrooms with outdoor air will improve IAQ and is likely to provide a health benefit. It is also easier than cleaning PM10 from indoor air, which has proven to be tedious. Interventions are needed also for mold and dampness problems that are frequent in schools and related

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to development of asthma and other general symptoms. Cleaning activities can also be monitored and performed in the absence of the public. Intervention studies to evaluate the effectiveness of preventive measures need to be implemented. Research Needs More research needs to be performed to examine the IAQ in schools in relation to the development of health problems. This requires: 1. Representative IAQ audits in schools using the principal measurements of IAQ (CO2 , VOC, ventilation, biocontaminants, and allergens) in combination with an evaluation of building characteristics and building use. 2. Implementation of epidemiological methodology. Standard questionnaires, medical visits, and some objective tests need be used to establish a system of medical surveillance and screening of schoolchildren. This system should provide prevalence, incidence, and remission rates of symptoms/disease, which might be an important complement to the environmental measurements taken to ensure a good air quality in schools. An appropriate sample survey needs to map different situations in various European countries, identify the main specific IAQ problems and gaps, and evaluate the impact of poor air quality on the health of the overall population. 3. Studies of the impact of the IAQ in schools on health and its effects on learning and life style of children. These studies have to consider both urban and rural settings in order to be representative. 4. Studies to develop specific IAQ standards and guidelines for schools, including the optimal cost-effective ventilation level with respect to health, productivity, learning, and use of energy. 5. Studies to develop building operation, maintenance, and IAQ monitoring programs for schools.

Conclusions This review on indoor air pollution at school has led to the following conclusions: 1. Indoor air quality (IAQ) in schools has been much less studied than IAQ in other buildings (e.g., offices and other working places). Consequently, scarce attention has been given to IAQ in schools, consequent related adverse health effects, and the effectiveness of remedial measures. 2. Available data show that schools frequently have severe indoor air problems because of poor building construction and maintenance, poor cleaning, and poor ventilation (CO2 > 1000 ppm). In addition, high levels of VOC, allergens, and molds (RH) are frequently found. 3. Various building characteristics were found to be related to the levels of different air pollutants. However, these have not been investigated sufficiently or with a standardized procedure. 4. Poor air quality in schools has been associated significantly with a large spectrum of diseases. Respiratory health is particularly challenged by air pollutants found in schools. Allergic individuals are at a higher risk. 5. Few studies examined the impact of exposure and health measures that need to be taken to improve air quality. More investigations need to be conducted on air pollution at school and related adverse health effects. These studies need to use standardized protocols and methodology in order to provide comparable data. However, further investigations need to better consider the school IEQ as a whole (Figure 1) by including simultaneously IAQ and thermal comfort, as well as other physical and psychological aspects of life indoors including lighting, visual quality, and acoustics. The SINPHONIE project (http:/ /www.sinphonie.eu) is one of the responses to such a need.

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FIGURE 1. Indoor environmental quality in schools (color figure available online).

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