Self-reported rhinitis of students from different universities in the Netherlands and its association with their home environment

Background: While the indoor environmental quality of student homes is a potential issue since it may affect the wellbeing of the students, the relations are still poorly studied. This study aimed to investigate the relations between home building characteristics and rhinitis in students. Material and methods: A questionnaire was distributed among four groups of students from three different universities in The Netherlands. Self-reported characteristics of 396 students and their homes were linked to self-reported rhinitis. Logistic regression modelling was applied to explore relations between building characteristics and rhinitis. Results: Among the students studied, 33% declared to suffer from rhinitis in the last 12 months. After full adjustment, the regression model revealed that having relatives with rhinitis was positively associated with rhinitis (OR:5.27, CI: 3.02 e 9.21) as well as the presence of less than one-year old furniture made of MDF in the bedroom (OR:2.26, CI: 1.17 e 4.37). Both working out and having no pets was negatively linked to rhinitis (respectively OR:0.50, CI: 0.25 e 0.99 and OR: 0.37, CI: 0.18 e 0.74). Opening the window in the bedroom more than once a week also reduced the risk for rhinitis (OR: 0.55, CI: 0.31 e 0.98). Conclusions: The study shows that biological pollutants (caused by pets), chemical pollutants (caused by MDF in bedroom), ventilation (opening window in bedroom) and workout, were associated with rhinitis in students. Further studies are needed to investigate the underlying causes to prevent rhinitis in young adults. © 2016 The Authors.


Introduction
There is an increasing concern about the quality of the indoor environment in homes and the rising prevalence of allergic and respiratory diseases. The indoor residential risk factors of primary interest for asthma, allergies and respiratory health, include allergens (e.g. dust-mites, cockroaches and pet dander), moisture, mould and endotoxin, combustion products from appliances, tobacco or other combustion sources (e.g. traffic), and indoor chemical emissions or emission-related materials or activities (e.g. formaldehyde or particleboard, phthalates or plastic materials, and volatile organic compounds or recent painting), renovation and cleaning activities, new furniture, carpets or textile wallpaper (e.g. reviews in Refs. [1e3]), and several building factors (building location, type of construction and design of the heating, cooling and ventilation systems applied, furnishings and furniture) (e.g. Refs. [4,5]). Besides the environmental risk factors, potential risk factors for asthma, allergies and respiratory health are personal factors (e.g. sex, age, genetics, educational level), lifestyle-related behaviours (e.g. smoking, alcohol use, physical activity, sedentary behaviour) and psychosocial factors (e.g. mood).
Up to now, very few studies have investigated simultaneously the impact of environmental and individual factors on health, while it is important to consider physical, physiological, psychological and social factors to explain the responses of people [6]. Moreover, indoor environmental studies in homes mainly involve children (e.g. Refs. [7e11]). However, indoor environmental quality may also affect the well-being of students [12,13]. Studies involving this population have focussed mainly on their school environment, but not their home environment. Therefore, a survey was performed among students from different universities in the Netherlands [14]. In this survey, rhinitis was reported to be the most prevalent health condition. Rhinitis is a worldwide health problem with negative impacts on quality of life [15]. There exist several forms of rhinitis: allergic rhinitis, caused by an immune response against allergens (e.g. indoor allergens such as dust mites, moulds, insects -cockroaches-and animal dander) and non-allergic rhinitis, caused by non-allergic conditions resulting in similar symptoms (e.g. infections, emotional, physical and chemical factors, and use of certain drugs) [4]. The relations between environmental factors, individual factors and rhinitis are not clearly understood.
In this context, using the large database from the survey conducted in Dutch universities, this study aimed to explore the associations between the indoor environment of the students' homes and rhinitis, taking into account all potential confounders, as a first important step towards unravelling the indoor environmental causes of rhinitis in students.

Study design
In the spring of 2015, four groups of students from three different universities in the Netherlands were recruited for a survey on their health and comfort in relation to their homes: the universities were the Delft University of Technology (TUD) (including two groups: bachelor and master students), Wageningen University (WUR) (bachelor students), and the Technical University of Technology (TU/e) (master students), located in the West, East and South of the Netherlands, respectively.
In all cases, the procedure was similar. At least three weeks before the lecture, the students of the specific courses received an invitation by e-mail with a link to the digital on-line questionnaire.
In the e-mail the purpose and the procedure of the survey were explained and the deadline for completing the questionnaire was given (in general one week before the lecture). All students who were registered to the course received an invitation. It was estimated that the questionnaire would take about 30 min to complete and respondents could save the survey at any time and resume it later.

Data collection
The electronic-based questionnaire was voluntary, anonymous and in English. It was based on the OFFICAIR questionnaire [16], while also including the International Positive and Negative Affect Schedule Short Form, I-PANAS-SF [17], the Emocards tool to assess the self-reported emotional status at the moment of filling in the questionnaire [18], the dwelling questionnaire [19], and the HOPE checklist for homes [20]. In total, the questionnaire included 125 questions at the most (without skip-logic questions) and one optional question about the respondents' interest in the questionnaire and ease of filling it in. It included questions to collect sociodemographic data about the respondent (e.g. gender, age, marital status, educational level), life-style information (e.g. time spent inside the home, workout, smoking status, and alcohol habits), psycho-social aspects (e.g. mood via Emocards, recent positive and negative events -such as birth, wedding, death, accident, severe illness -, and general positive and negative affects via I-PANAS-SF), health and medical history (e.g. personal medical history, family medical history, health at home), and comfort data (e.g. overall comfort, indoor comfort perception). Additionally, the questionnaire included a checklist to collect information about different types of occupants of the home environment (e.g. people, pets and pests), the systems and activities (e.g. heating, cooling and cooking, do-it-yourself activities, cleaning activities, consumer products), the presence of materials, coverings and furniture (e.g. asbestos, lead, floor and wall coverings, ceiling surface, painting, new carpeting, particle board, open shelves), the ventilation type and window characteristics (e.g. natural ventilation, mechanical ventilation, maintenance, window frame, window opening), and humidity problems (e.g. humidity signs, condensation, washer and/ or drying).
The I-PANAS-SF is composed of 5-item positive affect subscales (alert, inspired, determined, attentive and active) and 5-item negative affect subscales (upset, hostile, ashamed, nervous, and afraid). Each item is rated from 1 'never' to 5 'always'. The Emocards tool includes eight cards with facial expressions for distinct emotional expressions varying on the basis of the dimensions 'pleasantness' and 'arousal' (physical state of activation). The cards are presented with a female or a male cartoon character, appropriately for both female and male participants [18].
Concerning health data, the following question was asked for a number of diseases, including allergic rhinitis: 'Have you suffered from disease/disorder?' The following options were the possible answers: 'Never', 'Yes, in the last 12 months', 'Yes, but not in the last 12 months'. To identify health symptoms that the students suffered from, the following was asked: 'In the past 3 months, how often have you suffered from Health symptom while you have been in your home (on average)?' The possible answers were: 'every day', '3e4 days a week', '1e2 days a week', 'once every 2e3 weeks', 'less often or never'. If the answer was 'once every 2e3 weeks' or more often, the following additional question was asked: 'Do you think that this is because of your indoor environment?' with possible answers: 'yes', 'no', 'partly'.

Ethical aspects
The students were asked to give an informed consent to start the survey. Participants were able to skip any question that they were not comfortable answering. To decrease involuntary missing answers, an automatic check of completeness was performed, and missing answers were pointed out to the participant at the end of each page of the questionnaire.

Data management
All data were digitally completed and stored in Collector © (an online questionnaire tool).
Data were prepared by removing incomplete questionnaires (e.g. 7 from TUE who answered only the first ten questions), a questionnaire of a non-student (teacher from TUD BSc) and one respondent from TUD MSc, who answered the questions in a nonserious way.

Descriptive analysis
Descriptive statistics such as percentages, range (minimumemaximum), or arithmetic mean with standard deviation (SD) were used to summarize the characteristics of the students and their homes. Since there was no overall difference between the different student groups, data were pooled for further analyses.

Associations between building characteristics and rhinitis
The relations between building characteristics and rhinitis ('yes in the last 12 months' equalled yes; while 'yes, but not in the last 12 months' and 'never' equalled 'no') were examined using unconditional logistic regression modelling.
Potential personal factors were: gender, parental history of rhinitis, smoking status (yes versus no), alcohol consumption (yes versus no), and psychological aspects (PANAS negative and positive). Age was not considered because the standard deviation was small.
Concerning the building characteristics: building type 'detached' versus 'not detached' (as a measure for density of buildings), construction date (before 1945 versus after 1945), building location (urban ecombining mixed area, city centre, town, versus rural area ecombining suburban, village or rural area), and outdoor pollution sources were analysed.
Heating and cooking amenities ('gas' versus 'no gas'), type of wall/floor coverings, furniture and presence of plants, cleaning activities ('at least once a week' versus 'less than once a week'), use of consumer products ('at least once a week' versus 'less than once a week'), ventilation systems, humidity signs and opening of windows ('more than once a week' versus 'once per week or less'), were also taken into account.
Variables associated with a P-value of less than 0.20 and with well-known risk factors were included in the multivariate analysis. The final model was obtained by eliminating variables associated with a P-value greater than 0.20. Collinearity among variables in the model was measured by the variance inflation factor (VIF). No multicollinearity was detected (VIF<4). No potential modification effect of parental history of rhinitis or negative events was identified. Results are expressed as adjusted odds ratios (OR) with their confidence intervals at 95% (95% CIs).

Participation rate and characteristics of the study respondents
Overall, the response rate was 78% (ranging from 26 to 98.5%) ( Table 1). Table 2 shows the characteristics of the respondents. While about half of the respondents from both technical universities were female, at the WUR only one male student participated. The mean (SD) age of the respondents for all groups was 22 (3) years, with a range of 18e45 years. Concerning their lifestyle, 76% and 5% were never, and were former smokers, respectively. Current smokers consumed on average 8.6 (5.1) cigarettes per day, with a range of 2e22 cigarettes per day. A total of 16% of the students were exposed to second-hand smoke (SHS) at home. Daily or occasional alcohol consumption was declared by 84% of the respondents, while 16% drank no alcohol at all. On average students reported to drink 10 beers per week, with a maximum of 100 beers per week. On average, 84% reported to do some form of exercise for 4 days a week.
About 35% and 34% of the respondents experienced a recent positive and a negative event, respectively. On average 23% of the respondents were tense, irritated, sad, or bored at the time they filled in the questionnaire.
On average students scored 17 for the positive affect with a range from 6 to 24; and 11 for the negative affect with a range from 5 to 22.
Concerning their health, about 33% of the respondents suffered from rhinitis in the last 12 months. While 36% declared that their relatives suffered from rhinitis. The most prevalent symptoms experienced in the last 3 months (at least once every 2e3 weeks), related to the indoor environment, were sneezing (30%) and blocked or stuffy nose (27%).

Characteristics of the student homes
Self-reported characteristics of the homes of the respondents, which might be related to rhinitis, is presented in Table 3.
The buildings were located in different areas: 29% in town with no or small gardens, 22% in city centre with densely packed housing, 21% in suburbs with large gardens, 20% in mixed areas (industrial, commercial, residential) and 8% in village or rural areas. For nearby sources of pollution, 58% of the respondents declared busy road, 43% cars parked close to the building, 20% a railway station, 13% an attached garage, 8% industrial and agricultural sources and 5% a direct access from a basement or a roof car park.
The main floor covering in the students' homes was wood (41%), followed by synthetic smooth floor covering (27%) and carpet (15%). Exposed concrete/plaster was the main wall covering for 34%, wall paper for 26%, and dispersion/emulsion paint for 20% of the homes. The main ceiling surface was exposed/concrete plaster (45%), followed by paint (31%). Less than one-year furniture made of MDF was declared by 23% in the bedroom, 22% in the living room and 16% in the kitchen. Natural decorative plants were reported by 55% of the students.
With respect to (un)wanted occupants in their homes, 76% of the students reported to have no pets, 45% declared to have no problems with pests, while 20% did have problems with mice. Doit-yourself activities performed most involved the use of paint (14%) and model glues (12%). 51% declared to have performed recent painting/remodelling of their home. At least once per week, floors/carpets were swept/vacuumed by 72%, while 64% dusted the surfaces and 46% washed the floors. Mattresses were turned at least once per month by 25% of respondents. Consumer products most used (at least once per week) were air fresheners (32%), hair sprays (18%) and window cleaners (16%). 70% of the students used a gas cooker (cooks on gas), 13% used an unvented gas water heating system, and 23% a dryer vented outdoors.
93% of the students reported to have operable windows, while opening of bedroom windows (more than once per week) was declared by 67%, by 60% in kitchen and by 58% in the living room. 35% reported to have a ventilation grille as ventilation type, and 23% had mechanical ventilation, while air conditioning was present in 12% of the homes.
Finally, 58% reported no humidity signs. Among potential humidity signs, water leakage or water damage indoors was reported the most (25%), followed by visible mould growth (24%). 33% declared condensation on the inside of the windows, while 47% had no condensation on either inside, between or outside the glazing. Table 4 presents the results from the univariate analyses and the results with adjustment for gender, smoking, family rhinitis and negative events. Rhinitis was negatively associated with workout, absence of pets, opening of windows in bedroom more than once a week, natural plants and agricultural sources of pollution. A tendency was observed with presence of rodents (mice and rats), with mattresses turned at least once a month, with opening of windows in living room more than once a week, with air conditioning and with SHS exposure. Rhinitis was positively associated with the home location in an urban area. less than one-year old furniture made of MDF in the bedroom and the direct access to the basement/roof car park, tended to be positively associated with rhinitis. Table 5 shows the results from the multivariate logistic regression model. Having relatives with rhinitis was positively associated with rhinitis (adjusted OR: 5.27, CI: 3.02e9.21). Working out (OR: 0.50, CI: 0.25e0.99), having no pets (OR: 0.37, CI: 0.18e0.74), and opening windows in the bedroom at least once a week or more (OR: 0.55, CI: 0.31e0.98), were negatively linked to rhinitis. Presence of less than one-year old furniture made of MDF in the bedroom was positively linked to rhinitis (OR: 2.26, CI: 1.17e4.37).

Strength and limitations
The study is based on the survey among students from different universities collecting data on a broad range of relevant stressors for this population group (students with a mean age of 22 years   old), including personal factors, other factors of influence, and events. The response rate of 78% was high, even though the data were collected via an on-line questionnaire. This could be related to the fact that the survey was connected to a university course and to a small guide explaining the requested information [21]. The study sample was not representative of students attending Dutch universities in general (approximately 250,000). All students attended the course of Prof. Bluyssen and all students were enrolled at a Technical university (total number of students: cc. 25,000 at TU Delft, 8000 at TU/e and 10,000 at WUR), which can introduce a potential bias in the results, and the results cannot be generalized to the entire student population.
Because of the cross-sectional nature of the study, no causal pathway could be established. Additionally, the study comprised of self-reported data only. Notwithstanding, self-administered questionnaires have shown a good agreement between self-reported Sick Building Syndrome symptoms and a medical interview [22], however, for a correct diagnosis of rhinitis, clinical diagnoses are more reliable [4].

(Allergic) rhinitis
In the Netherlands, Droste et al. [23] investigated nasal symptoms in 2167 subjects with an age between 20 and 70 years old. 29.5% suffered from nasal symptoms, which is comparable to the self-reported symptoms such as sneezing (30%) and blocked or stuffy nose (27%), reported by the students. In our study, 78% of the students who declared to suffer from rhinitis also reported blocked/ study nose (P < 0.001) and 72% reported also sneezing (P ¼ 0.005), which confirms previous studies [6].
Dykewicz and Hamilos [24] estimated that 10e25% of the population in Western societies have rhinitis. Bousquet et al. [4] indicated a range of 17e28.5% in Europe, while Wheatley and Togias [25] presented a range of 15e30% for the population of the USA. The self-reported 'allergic' rhinitis of the students, 33% with a range of 26%e35% was even higher than that. It should be noted that the prevalence of rhinitis differs in the literature due to health outcome definition.
Multivariate analysis in the underlying study confirmed an association of rhinitis with both allergic and non-allergic conditions: biological allergens from the presence of pets and chemical pollutants (e.g. formaldehyde) emitted by less than one-year old furniture made of MDF in the bedroom, ventilation by opening window in bedroom more than once per week, and physical conditions by working out (exercise). The strongest association was found for students that have relatives who suffer from rhinitis (P < 0.001), with an adjusted OR of 5.27 (CI ¼ 3.02e9.21). This is consistent with the statement that 'Rhinitis is a multifactorial disease induced by gene-environment interactions' [4].

Personal factors
Besides a family connection (genes from parents), several other personal factors have been shown to be associated with rhinitis. Age, gender, and smoking and/or being exposed to second-handsmokie (SHS) are well-known personal factors [26]. In this study no gender difference was statistically identified, and age was not considered because it was rather narrow (SD ¼ 3; mean ¼ 22).
The counter-intuitive tendency of association between SHS exposure and rhinitis (OR: 0.46, CI: 0.21e1.02) may be explained by the fact that when people smoke indoors, windows are opened. Indeed, among 61 students who reported SHS exposure, 77% declared opening windows in the living room, and from those who did not report SHS exposure (322 students), 56% declared opening windows in the living room (p ¼ 0.003).
It is known that negative events influence one's general feeling of wellbeing. In a postal survey on risk factors for asthma and atopic diseases among 10,667 Finnish first-year university students aged 18e25 years, it was found that stressful life events increased the risk of manifestation of allergic rhinoconjunctivitis (or rhinitis) when adjusted for parental atopic disease, education, and passive smoking [27]. In the underlying study, a tendency of an increase was observed for negative events (P ¼ 0.054) by a student population with a mean age of 22 years of age.
Working out was negatively associated with rhinitis (OR: 0.50, CI: 0.25e0.99), indicating that the more one works out, the smaller the risk of acquiring rhinitis. Recent studies show that physical activity could reduce respiratory health diseases or conditions. Swimming pool attendance was documented as a protective factor for rhinitis in children [28]. However, we cannot exclude the fact that students who suffered from rhinitis are potentially less engaged in physical activity.

Biological pollutants
Allergic pollutants that have been associated with rhinitis are: animal dander and secretions (e.g. cats, dogs, rodents and others), waste from insects (e.g. cockroaches, house dust mites), and fungal allergens from moulds [26].
It has been well-established that the presence of pets can cause allergic responses in both children and adults [26]. In this study 'not having pets' resulted in a decreased risk for rhinitis (OR: 0.37, CI: 0.18e0.74), confirming earlier findings.
The counter-intuitive tendency of association between the  presence of rodents (mice and/or rats) and rhinitis (OR: 0.58, CI: 0.31e1.11), may be explained by the fact that when students know they have rodents pests, they clean more (60% of the students having rodents washed their floor more than once a week versus 45% of the students who did not declare to have rodents pests, P ¼ 0.014). Another explanation is the floor level on which they live. A higher percentage of students living on the groundfloor or first floor, declared to have rodents (53%) than students not having declared to have rodents (38%) (P ¼ 0.014). Also, the age of the building can have an influence. From the students who declared to have rodents, 40% live in a building constructed before 1945, versus 18% who declared not to have rodents (P ¼ 0.001).
Although indoor mould and dampness in buildings have been associated with multiple allergic and respiratory effects, it has been difficult to explain this association with specific chemical or microbial factors [29]. Visible mould growth is used as an indicator for dampness in buildings [30]. Moulds can produce spores, MVOCs (Microbial volatile organic compounds), mycotoxins, and other toxic compounds [31]. In this study, no statistical association was found between visible mould growth and rhinitis. Lorentzen et al. [32] suggested that annoying odour (from mould) may also contribute to adverse health effects. However, the smell of mould was not found to be related to rhinitis.
Although the normal amount of plants present in a space has not shown to contribute to less indoor air pollutants, positive effects of plants on people's perception of an indoor environment such as how stressful the space is perceived, have been found in several studies [33]. In this study, a tendency of a decrease in rhinitis (OR: 0.61, CI: 0.36e1.05, P ¼ 0.075) was observed.

Chemical pollutants
An increased risk of rhinitis was found with the presence of less than one-year old furniture made of MDF in the bedroom (OR: 2.26, CI: 1.17e4.37), while a reduced risk was found for opening windows (more than once per week) in the bedroom (OR: 0.55, CI: 0.31e0.98). Additionally, a tendency of a reduced risk of rhinitis was observed for having air conditioning (OR: 0.48, CI: 0.19e1.21, P ¼ 0.121), indicating that with more ventilation in the bedroom, the risk decreases. Less than one-year old furniture made of MDF, has the potential of specifically emitting aldehydes (e.g. formaldehyde) [34]. This emission increases as humidity increases, another indicator for a damp building.
In order to study the effect of outdoor pollutants on rhinitis, such as exhaust fumes from traffic, the risk of living in an urban vs. rural area (assuming less outdoor pollutants) was tested. No significant association was found. However, a tendency was observed with the presence of agricultural sources (OR: 0.46, CI: 0.16e1.33, P ¼ 0.152), which could be a surrogate for living in a rural area.

Conclusions
The findings of this study show that rhinitis was associated with biological pollutants (presence of pets) and chemical pollutants (presence of MDF from less than one-year old furniture), ventilation (opening windows in bedroom more than once a week), and with personal factors, working out (physical activity).
Besides genetics, this study confirms that rhinitis is a multifactorial disease; as both personal and environmental factors are linked to this disease in young adults.