Housing Characteristics in Relation to Exhaled Nitric Oxide in China Fan Hou, MPH; Xiji Huang, MD; Chuanyao Liu, MPH; Huizhen Sun, MD; Ting Zhou, MD; Yuanchao Song, MD; Yi Rong, MD; Beibei Zhu, MD; Wei Chen, MD; Jing Wang, MD; Jianshu Wang, MPH; Meian He, MD; Xiaopin Miao, MD, PhD; Barbara Hoffmann, PhD; Tangchun Wu, MD, PhD; Weihong Chen, MD; Jing Yuan, MD
Objective: To investigate indoor factors affecting fractional exhaled nitric oxide (FeNO) in community residents. Methods: A total of 2404 adults (865 men, 1539 women, mean age 51.7 ± 13.3 years) were recruited to the study. Factors affecting FeNO were analyzed by multiple linear regression analysis. Results: Participants without a kitchen exhaust fan/hood had higher FeNO (GM: 10.21%, 95% CI: 4.18%-16.59%). Participants engaged in home cooking who used only liquefied petroleum gas had
G
ood indoor air quality is associated with positive health.1 Poor indoor air quality increases risk of cardiovascular and respiratory diseases, asthma, and decline in lung function.2,3 People in many developing countries are commonly exposed to multiple indoor pollutants (such as particulates, carbon monoxide, and sulfur oxides) from the combustion of solid fuels in open fires or traditional stoves.4 Fan Hou, Xiji Huang, Chuanyao Liu, Huizhen Sun, Ting Zhou, Yuanchao Song, Yi Rong, Jing Wang, Jianshu Wang, Meian He, Associate Professor, Weihong Chen, Tangchun Wu, and Jing Yuan, Professors, Department of Occupational and Environmental Health, Key Laboratory of Environment and Health, Ministry of Education & Ministry of Environmental Protection, and State Key Laboratory of Environment Health (Incubation), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology. Beibei Zhu, Wei Chen and Xiaopin Miao, Professor, Department of Epidemiology and Biostatistics; Key Laboratory of Environment and Health, Ministry of Education & Ministry of Environmental Protection, and State Key Laboratory of Environment Health (Incubation), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology. Barbara Hoffmann, Professor, IUF Leibniz-Institut für umweltmedizinische Forschung Heinrich Heine Universität Düsseldorf, Dusseldorf, Germany. Fan Hou, Xiji Huang and Chuanyao Liu contributed equally to this work. Correspondence: Dr Jing Yuan; [email protected] and Dr Weihong Chen; [email protected]
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higher FeNO (GM: 5.75%, 95% CI: 0.10%11.73%) compared to those using natural gas for residential (home) cooking. Conclusion: Nonuse of a kitchen exhaust fan/hood and use of liquefied petroleum gas among persons engaged in home cooking were associated with higher FeNO levels. Key words: exhaled nitric oxide; housing characteristics; cooking fuel type; kitchen ventilation Am J Health Behav. 2015;39(1)88-98 DOI: http://dx.doi.org/10.5993/AJHB.39.1.10
Next to the contribution of outdoor particles, human activities, including smoking and cooking, often lead to indoor hazardous concentrations of carbon monoxide and airborne particulate matters smaller than 2.5 µm in diameter (PM2.5).5 For instance, cooking episodes produce a large amount of ultrafine particles (UFP) after just 15 minutes.6 It is noted that PM2.5, and specifically, UFP with multiple toxic components, can escape pulmonary filtering mechanisms and then enter the circulatory system of the body. They can cause potential toxic effects by binding directly to intracellular proteins and DNA within the cells because of their high surface-to-volume ratios per unit of mass.7 A previous study showed that the major contributing source of indoor PM was cooking oil fumes, which were responsible for about 52.5% of the personal exposure samples and 43.2% of the residential indoor concentrations.8 Cooking emissions including PM2.5, UFP, carbon dioxide, and black carbon are dependent largely on the type of kitchen stove and cooking style.9,10 Chronic exposure to cooking fuels shows a positive association with the prevalence of respiratory symptoms, including reduced lung function.11 In addition, gas stoves are the most important source of UFP in nonsmoking homes.12 Potentially toxic concentrations of particulate matter and high concentrations of nitrogen oxides were found while cooking meals using gas in poorly ventilated kitchens.13 Emission concentration of in-
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Table 1 Socio-demographic Characteristics of Study Population Variable
Men: N = 865
Women: N = 1539
Total: N = 2404
p
52.5±13.4
51.3±13.3
51.7±13.3
.024a
18-44
237(27.4)
472(30.7)
709(29.5)
45-59
368(42.5)
678(44.1)
1046(43.5)
≥60
260(30.1)
389(25.3)
649(27.0)
Age (year, N, %)
Education (years, N, %)
< .001b
0-6
101(11.7)
389(25.3)
490(20.4)
7-12
620(71.7)
996(64.7)
1616(67.2)
>12
144(16.6)
154(10.0)
298(12.4)
Marital status (N, %)
< .001b
Never married
48(5.5)
46(3.0)
94(3.9)
Married
787(91)
1307(84.9)
2094(87.1)
Widowed
18(2.1)
153(9.9)
171(7.1)
Divorced
9(1.0)
23(1.5)
32(1.3)
Remarried
3(0.3)
10(0.6)
13(0.5)
Current occupational status (N, %)
< .001b
Students
12(1.4)
6(0.4)
18(0.7)
Workers
489(56.5)
568(36.9)
1057(44.0)
Unemployed
96(11.1)
291(18.9)
387(16.1)
Retired
196(22.7)
463(30.1)
659(27.4)
Others
72(8.3)
211(13.7)
283(11.8) (continued on next page)
door particles from cooking with a gas stove was markedly higher (60-118 mg/m3) than that from frying with an electric stove (12-27 mg/m3).14 However, effective exhaust hoods can mitigate the impact of pollutants emitted from home cooking processes on indoor air quality15 Higher lung function growth was associated with the use of household ventilation devices during the cooking process.16 Various factors can cause airway inflammation. For instance, PM exposure is associated with systemic inflammation in the body.17 Nitric oxide (NO) is a mediator and regulator of inflammatory responses.18 It plays an important role in various physiological and pathological events.19,20 Change in the production of nitric oxide relates to multiple organ dysfunction and associated syndromes. Nitric oxide synthases (NOS, including inducible iNOS; endothelial eNOS; and neuronal nNOS) participate in the processes of NO production.18 The production of iNOS-derived NO is associated with eosinophils, endothelial cells, and cardiac myo-
cytes.21 Measurement of fractional exhaled nitric oxide (FeNO) often is used as a marker of airway inflammation or as a marker for adverse respiratory health effects caused by indoor air pollution.22 Moreover, ambient particle matter and nitrogen dioxide (NO2) also show positive associations with FeNO level.23 FeNO level is associated with asthma symptoms; its level is influenced by sex, age, ethnicity height, weight, neutrophil counts, and environmental pollutants.24 In this study, we investigated the association between cooking fuel type and use of a kitchen exhaust fan/hood with FeNO levels using baseline data from a Chinese community cohort study, after controlling potential confounders.
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METHODS Study Population and Physical Examination The baseline survey of the cohort study was carried out during April and May 2011 in the Hankou and Hanyang districts in Wuhan metropolitan
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Housing Characteristics in Relation to Exhaled Nitric Oxide in China
Table 1 (continued) Socio-demographic Characteristics of Study Population Variable
Men: N = 865
Women: N = 1539
Total: N = 2404
Smoking status (N, %) Never smoker
p < .001b
294(34.0)
1491(96.9)
1785(74.3)
Former smoker
114(13.2)
6(0.4)
120(5.0)
Current smoker
457(52.8)
42(2.7)
499(20.8)
Passive smoke exposure (N, %)
.002b
Yes
398(46.0)
803(52.2)
1201(50.0)
No
467(54.0)
736(47.8)
1203(50.0)
Drinking status (N, %)
< .001b
Never drinker
402(46.5)
1457(94.7)
1859(77.3)
Former drinker
71(8.2)
15(1.0)
86(3.6)
Current drinker
392(45.3)
67(4.4)
459(19.1)
Physical activity (N, %)
.060b
Yes
370(42.8)
651(42.3)
1021(42.5)
No
495(57.2)
888(57.7)
1383(57.5)
Kitchen exhaust fan/hood (N, %)
.973b
Yes
765(88.4)
1361(88.5)
2126(88.4)
No
100(11.6)
178(11.6)
278(11.6)
Self-catering
< .001b
Yes
443(51.2)
1257(81.7)
1700(70.7)
No
422(48.8)
282(18.3)
704(29.3) (continued on next page)
area, China. The local temperatures were between 20° C (68.0° F) and 32°C (89.6° F) during the investigation. A total of 3698 community residents who had lived in the city for at least 5 years were invited to participate in the study. Of these, only persons aged 18 and over were included as participants for analysis purposes. Participants who did not agree to provide blood samples or answer questionnaire information (N = 577) and participants under the age of 18 years (N = 29) were excluded. Participants with missing data on FeNO measurement (N = 126), on lung function measurement (N = 67), or on neutrophil count (N = 149) were excluded from our analysis. We also excluded participants with self-reported asthma (N = 33), chronic bronchitis (N = 160), or diabetes (N = 153). Thus, 2404 adults (865 men, 1539 women) aged ≥ 18 years (mean age 51.7 ± 13.3 years) were included. Data were collected by questionnaire and included social-demographic characteristics, lifestyle habits, cooking fuel type (natural gas, liquefied petroleum gas, coal, and electricity), type of kitchen ventilation (venting through opening the windows, use of kitchen exhaust fan/hood), housing conditions (such as home ventilation, way of heating
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the home, per capita living space and floor), pet ownership (including cat, dog, avian pets, tortoise, and aquatic pets) as well as personal and family medical history. Physicians conducted physical examinations on all participants according to standard methods, including measurements of height, weight, waist circumference, hip circumference, heart rate, and blood pressure. Body mass index was calculated by body weight in kilograms divided by height in meters squared. Complete Blood Count Test We collected 2ml of venous peripheral blood in a vacutainer tube containing an anticoagulant (ethylenediaminetetra-acetate and sodium citrate) from each participant. A complete blood count test was performed immediately using a Hematology Analyzer (pocH-100i, Sysmex Corporation, Kobe, Japan). Exhaled Nitric Oxide Measurement FeNO measurement was performed using a Nano Coulomb Nitric Oxide Analyzer (SV-02E, Sunvou Medical Electronics Co., Ltd. Wuxi, Jiangsu, China). This device for measurement of FeNO is based
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Table 1 (continued) Socio-demographic Characteristics of Study Population Variable
Men: N = 865
Women: N = 1539
Total: N = 2404
House condition (N, %)
.669b
Tiled one-story brick house
15(1.7)
20(1.3)
35(1.5)
Hovels
4(0.5)
6(0.4)
10(0.4)
846(97.8)
1513(98.3)
2359(98.1)
≤2
399(47.2)
676(44.7)
1075(45.6)
3
176(20.8)
313(20.7)
489(20.7)
Apartment (floors, N, %)
>3 Housing area (m2, mean±SD)
271(32.0)
524(34.6)
795(24.3)
111.9±91.1
102.3±79.8
105.8±84.1
Heating appliances in winter (N, %) Never used Natural gas heating system Radiator
d
Coal stove and heater brick bed
517(59.8)
860(55.9)
1377(57.3)
6(0.7)
14(0.9)
20(0.8)
336(38.8)
656(42.6)
992(41.3)
6(0.7)
9(0.6)
15(0.6)
.029c
.762b 32(3.7)
53(3.4)
85(3.5)
Natural gas only
208(24.0)
343(22.3)
551(70.8)
Liquefied petroleum gas
601(69.5)
1100(71.5)
1701 (22.9)
24(2.8)
43(2.8)
67(2.8)
Firewood plus coal
.401b
.284b
Cooing fuel type (N, %) Electromagnetic oven only
p
Note. a Student’s t test was used to compare the mean values of the continuous variables. b Chi-square test was used to observe the association between 2 categorical variables. c Mann-Whitney test was used to compare 2 groups of abnormal distribution data. d Radiator: including oil-filled radiator, electric blanket, quartz heater and air conditioning.
on the potentiostatic coulometry approach through electrolysis of exhaled nitric oxide following Faraday’s laws. The device was validated through correlation and agreement comparisons for both standard bottled gas and exhaled air with an electrochemical analyzer (NIOX MINO, Aerocrrine AB, Solina, Sweden) with a correlation coefficient of 0.984, by SFDA (the State Food and Drug Administration of China). To ensure comparability with other standard approaches for FeNO measurement during this study, the device also was validated and calibrated by standard bottled gas (15, 75 and 150 ppb) and NIOX MINO on a weekly basis. The measurement procedure was performed according to the 2005 ATS/ERS guidelines before conducting spirometry. The participant was asked to fast (eating and drinking) and refrain from smoking for at least one hour and strenuous exercise at least onehalf hour before measurement. Under the instruction of the technician, the participant was seated comfortably and asked to inhale deeply. A NO-free air filter was placed in his/her mouth before exhaling smoothly at a speed of 50 ± 5 milliliters per
second for 4 to 10 seconds. The initial 3 seconds were used to exclude “dead space” volume as well as possible effects of inhaled ambient gas. The exhaled gas was analyzed online and the stable mean FeNO value was recorded. The lowest detection limit is 5 part per billion (ppb) and the analytical accuracy is ± 3 ppb when the measured value is < 50 ppb, or ± 10% when measured value ≥ 50 ppb. FeNO values were expressed as ppb.
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Pulmonary Function Tests Pulmonary function tests were performed on all eligible participants, using the portable battery-operated spirometers (CHESTGRAPH HI-101, Chest MI, Inc, Tokyo, Japan). The parameters including vital capacity (VC), forced vital capacity (FVC) and forced expiratory volume produced in the first second (FEV1) were measured. Participants were asked to perform several forced expiratory maneuvers to obtain 3 repeatable maneuvers according to the recommendations of the American Thoracic Society (ATS) 2005 guidelines on the interpretation of lung function tests.
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Housing Characteristics in Relation to Exhaled Nitric Oxide in China
Table 2 Clinical Characteristics of Study Population Men: N = 865
Women: N = 1539
Total: N = 2404
p
Height (cm, mean±SD)
166.7±6.4
155.7±5.7
159.6±7.9
< .001a
Weight (kg, mean±SD)
67.6±10.8
57.8±8.8
61.3±10.6
< .001b
Body mass index (BMI, kg/m2, mean±SD)
24.3±3.4
23.8±3.5
24.0±3.4
< .001b
Waist circumference (mm, mean±SD)
851.8±93.6
795.8±93.2
816.1±97.2
< .001a
Hip circumference (mm, mean±SD)
953.3±61.4
938.2±63.9
943.7±63.4
< .001b
Heart rate (beats/min, mean±SD)
73.8±11.4
75.6±10.4
74.9±10.8
< .001b
Systolic blood pressure (mmHg, mean±SD)
134.2±20.2
127.8±20.4
130.1±20.5
< .001b
Diastolic blood pressure (mmHg, mean±SD)
79.3±11.6
74.9±10.9
76.5±11.4
< .001b
Mean corpuscular hemoglobin (pg, mean±SD)
34.6±3.2
32.7±3.2
33.4±3.3
< .001b
Hemoglobin (g/L, mean±SD)
151.9±23.1
132.8±23.5
139.7±25.1
< .001b
Mean corpuscular volume (femtolitre, mean±SD)
96.5±15.6
95.7±17.1
96.0±16.6
< .001b
0.448±0.102
0.411±0.107
0.424±0.107
< .001b
Count of total white blood cells (109/L, mean±SD)
6.1±2.9
5.6±1.8
5.8±2.3
< .001b
Neutrophil count (109/L, mean±SD)
3.6±1.2
3.2±1.1
3.3±1.1
< .001a
Vital capacity (L, mean±SD)
3.6±0.7
2.7±0.5
3.0±0.7
< .001a
Forced vital capacity (L, mean±SD)
3.10±0.71
2.34±0.52
2.61±0.70
< .001a
FEV 1 (L, mean±SD)
2.65±0.61
2.02±0.44
2.25±0.59
< .001a
FEV1/FVC (%, mean±SD)
85.83±9.33
86.77±8.72
86.43±8.96
< .001b
Variable
Hematocrit (L/L, mean±SD)
FeNO level (ppb, geometric mean(95% CI) )
26.34(25.56-27.16)
21.88(21.34-22.42) 23.39(22.94-23.85) < .001b
Self-reported response to allergen (N, %)
< .001c
Yes
109(12.6)
309(20.1)
418(17.4)
No
756(87.4)
1230(79.9)
1986(82.6)
Self-reported frequent cough (N, %)
< .001c
Yes
151(17.5)
145(9.4)
296(12.3)
No
714(82.5)
1394(90.6)
2108(87.7)
Note. a Student’s t test was used to compare the mean values of the continuous variables. b Mann-Whitney test was used to compare 2 groups of independent data. c Chi-square test was used to observe the association between 2 categorical variables Pg, pico gram; FEV 1, forced expiratory volume in one second; FeNO, fractional exhaled nitric oxide; ppb, part per billion; 95% CI, 95% confidence interval.
Statistical Methods The logarithm-transformed FeNO values (Kolmogorov-Smirnov p < .001) were expressed as the geometric means (GM) and 95% CIs. In subgroup analyses, we stratified the analysis by possible effect modifiers including sex, age, smoking status, passive smoking exposure, and current occupational status. Multiple linear regression was used to analyze the association of cooking fuel type and use/nonuse of a kitchen exhaust fan/hood with FeNO levels. We began with an unadjusted anal-
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ysis (model 1), only including domestic cooking fuel exposure and use of a kitchen exhaust fan/ hood, as well as possible confounders and predictors each in separate analyses. We then performed model 2, including sex, age, annual family income, education level, cooking style at home, including fuel type and use/nonuse of a kitchen exhaust fan/hood. Model 3 represents the analysis adjusted for covariates in model 2 plus smoking, passive smoking exposure, height, weight, complete blood count, and heart rate. Model 4 adjusts for covari-
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Table 3 Multiple Regression Analysis Association between FeNO Levels (Log10) and the Selected Parameters Model 1a Variable
Partial Power regression of coefficient parameter
Model 2b Δ% of FeNO (95% CI)
Partial Power regression of coefficient parameter
Δ% of FeNO (95% CI)
Sex
0.081**
1.204
20.43(15.69-25.36)
0.078**
1.198
19.76(15.09-24.63)
Age (10 years)
0.020**
1.047
4.74(3.23-6.28)
0.019**
1.044
4.35(2.87-5.86)
Education
-
-
-
-
-
-
Marital status
-
-
-
-
-
-
-
-
-
Annual family income Height
-
-
-
0.043**
1.104
10.42(7.76-13.14)
Weight
0.001**
1.003
0.31(0.17-0.45)
Systolic blood pressure
0.001**
1.001
0.14(0.05-0.23)
Diastolic blood pressure
-
-
-
Heart rate
-
-
-
Hemoglobin
-
-
-
Mean corpuscular volume Hematocrit
-
-
-
0.203**
1.596
59.68(33.03-91.66)
Count of total white blood cells
-
-
-
Neutrophil count
-
-
-
Vital capacity
0.028**
1.067
6.75(3.92-9.65)
Forced vital capacity
0.026**
1.062
6.20(3.28-9.21)
FEV1
0.030**
1.071
7.09(3.61-10.69)
0.000
1.000
-
Former smoker
0.087**
1.221
22.10(11.56-33.62)
Current smoker
-0.005
0.989
-1.10(-5.78-3.81) -
-
-
0.044**
1.107
10.72(4.43-17.40)
0.042**
1.101
10.09(3.96-16.57)
0.000
1.000
-
0.000
1.000
-
Liquefied petroleum gas
-
-
-
-
-
-
Firewood plus coal
-
-
-
-
-
-
Electromagnetic oven only
-
-
-
-
-
-
Smoking status Never smoker
Self-catering Kitchen exhaust fan/hood Cooking fuel type Natural gas only (reference)
(continued on next page)
ates in model 3 plus current occupational status, physical exercise, pet ownership, FVC, VC, and FEV1. All statistical tests were performed using SPSS 12.0 software (SPSS, Chicago, IL, USA). RESULTS Characteristics of the Participants As Table 1 shows, the average age of participants was 51.7 ± 13.3 years. There were differences between the 2 sexes in educational attainment, mari-
tal status, current occupational status, active and passive smoking, alcohol consumption, housing area, and self-catering (p < .01 for all). As Table 2 shows, there were differences in the medical parameters between men and women. Prevalence of most medical conditions were higher in men than in women (p < .01), with the exception of the indicators including heart rate, FEV 1/ FVC ratio, and self-reported allergic disease. The FeNO level of participants was 23.39 ppb (95%
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Housing Characteristics in Relation to Exhaled Nitric Oxide in China
Table 3 (continued) Multiple Regression Analysis Association between FeNO Levels (Log10) and the Selected Parameters Model 3c Variable
Partial Power regression of coefficient parameter
Model 4d Δ% of FeNO (95% CI)
Partial Power regression of coefficient parameter
Δ% of FeNO (95% CI)
Sex
0.100**
1.258
25.83(18.10-34.07)
0.091**
1.234
23.37(15.50-31.78)
Age (10 years)
0.024**
1.056
5.60(4.04-7.18)
0.028**
1.066
6.63(4.79-8.50)
Education
-
-
-
-
-
-
Marital status
-
-
-
-
-
-
Annual family income
-
-
-
-
-
-
0.039**
1.095
9.49(5.93-13.18)
0.033**
1.080
7.96(4.18-11.86)
Weight
-
-
-
-
-
-
Systolic blood pressure
-
-
-
-
-
-
Height (10 cm)
Diastolic blood pressure
-
-
-
-
-
-
Heart rate (10 beats/min)
0.010**
1.024
2.36(0.59-4.17)
0.010**
1.024
2.36(0.59-4.16)
Hemoglobin
-
-
-
-
-
-
Mean corpuscular volume
-
-
-
-
-
-
Hematocrit
-
-
-
-
-
-
Count of total white blood cells
-
-
-
-
-
-
Neutrophil count
-
-
-
-
-
-
Vital capacity
-
-
-
Forced vital capacity
-
-
-
0.023*
1.054
5.39(0.38-10.65)
FEV1(L) Smoking status Never smoker
0.000
1.000
-
0.000
1.000
-
Former smoker
-0.040
0.911
-8.87(-17.30-0.41)
-0.038
0.917
-8.34(-16.82-1.00)
Current smoker
-0.116**
0.765
-23.51(-28.10-18.62)
-0.116**
0.766
-23.44(-28.03-18.55)
-
-
-
-
1.099
9.93(3.92-16.29)
1.102
10.21(4.18-16.59)
Self-catering Kitchen exhaust fan/hood Cooking fuel type
0.041**
0.042**
-
-
-
-
-
-
0.000
1.000
-
0.000
1.000
-
Liquefied petroleum gas
-
-
-
-
-
-
Firewood plus coal
-
-
-
-
-
-
Electromagnetic oven only
-
-
-
-
-
-
Natural gas only (reference )
*p < .05 **p < .01 Note. a Model 1: Unadjusted model. b Model 2: Adjusted for sex, age, annual family income, education level, self-catering, cooking fuel type and nonuse of a kitchen exhaust fan/hood. c Model 3: Model 2 plus smoking status, passive smoking exposure, height, weight, complete blood count and heart rate. d Model 4: Model 3 plus current occupational status, physical exercise, pet, VC, FVC and FEV1. FeNO, fractional exhaled nitric oxide; 95% CI, 95% confidence interval; FEV1, forced expiratory volume in one second.
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Table 4 Multiple Regression Analysis Associations between FeNO Levels (Log10) and the Selected Parameters by Cooking Participants without self-cateringa (N = 704)
Participants with self-catering a (N = 1700)
Partial regression coefficient
Power of parameter
△% of FeNO (95% CI)
Partial Power regression of paracoefficient meter
Sex
0.106**
1.276
27.61(14.56-42.15)
0.098**
1.255
25.46(15.59-36.17)
Age (10 years)
0.017**
1.040
4.04(1.60-6.54)
0.025**
1.060
5.98(3.92-8.09)
Education level
-
-
-
-
-
-
Annual family income
-
-
-
-
-
-
0.050**
1.122
12.22(5.60-19.25)
0.034**
1.082
8.19(3.98-12.57)
Heart rate (10 beats/min)
-
-
-
-
-
-
FEV1
-
-
-
-
-
-
Never smoker (reference)
0.000
1.000
-
0.000
1.000
-
Former smoker
-0.039
0.914
-8.56(-21.18-6.09)
-0.038
0.917
-8.32(-19.41-4.29)
Current smoker
-0.115**
0.767
-23.26(-30.02--15.84)
-0.118**
0.762
-23.75(-29.88--17.09)
0.052**
1.128
12.81(2.13-24.61)
0.034*
1.081
8.12(0.74-16.03)
0.000
1.000
-
0.000
1.000
-
Liquefied petroleum gas
-
-
-
0.024*
1.058
5.75(0.10-11.73)
Firewood plus coal
-
-
-
0.012
1.028
2.79(-11.04-18.77)
Electromagnetic oven only
-
-
-
0.019
1.045
4.54(-8.93-20)
Variable
Height (10 cm)
△% of FeNO (95% CI)
Smoking status
Exhaust fan/range hood Cooking fuel type Natural gas only (reference)
*p < .05 **p < .01 Note. a Adjusted for sex, age, annual family income, education level, smoking status, height, heart rate, FEV1, nonuse of a kitchen exhaust fan/hood and cooking fuel type. FeNO, fractional exhaled nitric oxide; 95% CI, 95% confidence interval; FEV 1, forced expiratory volume in one second.
CI: 22.94-23.85 ppb). The FeNO levels of men and women were 26.34 ppb (95% CI: 25.56-27.16 ppb) and 21.88 ppb (95% CI: 21.34-22.42 ppb, p < .01), respectively. Multiple Factors Analysis for FeNO Levels As shown in Table 3, in crude models, sex, age, height, weight, systolic blood pressure, hematocrit, vital capacity, forced vital capacity, FEV1, former smoking, and nonuse of a kitchen exhaust fan/hood all showed a positive association with FeNO (p < .01). In model 2, after adjusting for the confounding variables including sex, age, annual family income, education level, residential cook-
ing, cooking fuel type, and use/nonuse of a kitchen exhaust fan/hood, we found that age, sex and nonuse of a kitchen exhaust fan/hood showed a positive association with FeNO (p < .01). In model 3, after adjusting for the covariates in model 2 plus smoking status, passive smoking exposure, height, weight, complete blood count, and heart rate, we found that sex, age, height, heart rate and nonuse of a kitchen exhaust fan/hood were positively associated with FeNO (p < .01), but current smoking was negatively associated with FeNO (p < .01). In model 4, after adjusting for the covariates in model 3 plus current occupational status, physical exercise, pet ownership, FVC, VC and
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Housing Characteristics in Relation to Exhaled Nitric Oxide in China FEV1, we obtained similar results to those in model 3. We found that the relative increase of FeNO in men was 23.37% (95% CI: 15.50-31.78%) compared to women; current smoking reduced FeNO by 23.44%; moreover, nonuse of a kitchen exhaust fan/hood was associated with 10.21% (95% CI: 4.18-16.59%) increase in FeNO. Increases in age by 10 years, in height by 10 centimeters, in heart rate by 10-beats/min and in FEV1 by one liter were associated with increases of FeNO by 6.63, 7.96, 2.36 and 5.39%, respectively. We did not find associations between FeNO and education, marital status, annual family income, weight, blood pressure, complete blood count, FVC, VC physical exercise, and being a pet owner (p > .05). As Table 4 shows, the relative increase of FeNO through residential cooking and use of liquefied petroleum gas among participants was 5.75% (95% CI: 0.10-11.73%), compared with persons who cooked at home using natural gas only, in addition to increases associated with the risk factors included in model 4. DISCUSSION In addition to pollution created by active smoking, the incomplete combustion of cooking fuels is a source of indoor particulate matter, thereby contributing further to poor air quality.25 The complex composition of UFP including carbon (soot), aerosols, fungal spores, and bacterial endotoxins can penetrate the lung epithelium and be transferred to the liver, brain, and heart, potentially leading to a systemic inflammatory response. Our results showed that use of liquefied petroleum gas as a cooking fuel had a positive association with the FeNO levels among participants cooking at home; but, it was negatively associated with the FeNO levels in those using a kitchen exhaust fan/hood. Use of a kitchen exhaust fan/hood improved indoor air quality via reducing indoor air pollutants (such as PM, nitrogen oxides, and carbon monoxide) emitted from household activities like indoor smoking and cooking on stoves. Gas cooking in homes with poor ventilation or a kitchen without an exhaust fan/hood often leads to hazardous concentrations of multiple indoor pollutants including particulate matters and nitrogen oxides, even causing adverse health effects, particularly, an increased risk of respiratory diseases.13,26 In addition, an elevated FeNO level among participants was related to exposure to ambient particulate matters and nitrogen dioxide.23 Some Chinese still use traditional energy sources such as coal and liquefied petroleum gas to meet their cooking and heating demands; thus, people are exposed to a broad range of pollutants from indoor sources.26,27 Several studies in China show that indoor air quality is commonly affected by cooking fumes emitted from Chinese-style cooking processes.5,28 Domestic cooking appliances and Chinese cooking processes lead to the generation and emission of substantial amounts of air pol-
96
lutants;10,29 however, cooking accompanied by a kitchen exhaust hood reduces exposure to UFP.26 Exposure to cooking fumes may be responsible for elevated FeNO.10 Our findings indicated that using liquefied petroleum gas as cooking fuel was associated with elevated FeNO levels in participants who cooked at home; however, participants who used a kitchen exhaust fan/hood had reduced FeNO levels, indicating that indoor air quality was improved and potentially adverse health effects were successfully mitigated. This hypothesis is supported by the finding that wearing a face mask as a short-term measure reduced the cardiovascular effects of high ambient particulate air pollution.30 Apart from this, window position and air exchange rate in homes might affect FeNO levels via affecting indoor UFP concentration.23,31 In our study, current smokers had lower FeNO (with a 23.44% reduction) relative to never smokers, which is consistent with previous studies reporting that current smokers had reduced FeNO levels.32,33 For example, one study reported that FeNO levels were lower in current smokers (a 70% reduction) than in nonsmokers.32 Reduced FeNO could be an early indicator of effects of smoking on lungs by downward regulation of eNOS and iNOS.34,35 However, FeNO was not associated with nicotine.36 Elevated FeNO among participants exposed to air pollution may be due to direct modulation of normal physiological function or potentiation of compromised organ responses. Both extrinsic (environmental exposure and asthma treatment) and intrinsic factors (age, race, and NO synthase gene) affect personal FeNO.37 Moreover, elevated FeNO was related to clinic manifestations among patients with atopic diseases.38 We found FeNO differences between and within populations. FeNO in this study was higher (GM: 23.39 ppb, 95% CI: 22.94-23.85 ppb) than among Germans (GM: 13.9 ppb, 95% CI: 10.8-79.4 ppb),24 among healthy Japanese adults (GM: 15.4 ppb, mean ± 2SD: 6.5-36.8 ppb), and among persons in a Sweden-based sample (median: 16.0 ppb, range: 2.4-199 ppb).39 Racial characteristics, higher baseline indoor and outdoor air pollution, as well as study-specific characteristics, such as selection of participants might contribute to observed higher FeNO of Chinese adults in this study. Furthermore, we realized that the implications of the findings regarding indoor air pollutants emitted from cooking with use of liquefied petroleum or nonuse of an exhaust fan were not the only factors affecting elevated FeNO, because elevated FeNO levels were associated with certain diseases such as bronchial asthma.40 In conclusion, participants who engaged in residential cooking without using a kitchen exhaust fan/hood had higher FeNO levels. Participants who cooked with liquefied petroleum gas in their homes had higher FeNO levels. Our findings reveal that housing characteristics may be related to higher FeNO levels in these Chinese adults.
Hou et al The present study has certain limitations: firstly, individual-level exposure to both indoor and outdoor air pollutants and allergens was not monitored, so we had to rely on published observations relating to impacts of China cooking styles on indoor air quality and human health. Secondly, the study was a cross-sectional investigation and causality cannot be inferred. Thirdly, data concerning the variation in human responses to air pollutants and allergens across individuals were not available.
1. Kim KH, Jahan SA, Kabir E. A review of diseases associated with household air pollution due to the use of biomass fuels. J Hazard Mater. 2011;192(2):425-431. 2. Jie Y, Ismail NH, Jie X, et al. Do indoor environments influence asthma and asthma-related symptoms among adults in homes? A review of the literature. J Formos Med Assoc. 2011;110(9):555-563. 3. Fullerton DG, Suseno A, Semple S, et al. Wood smoke exposure, poverty and impaired lung function in Malawian adults. Int J Tuberc Lung Dis. 2011;15(3):391-398. 4. Galeone C, Pelucchi C, La Vecchia C, et al. Indoor air pollution from solid fuel use, chronic lung diseases and lung cancer in Harbin, Northeast China. Eur J Cancer Prev. 2008;17(5):473-478. 5. Wallace L, Ott W. Personal exposure to ultrafine particles. J Expo Sci Environ Epidemiol. 2011;21(1):20-30. 6. Wallace LA, Emmerich SJ, Howard-Reed C. Source strengths of ultrafine and fine particles due to cooking with a gas stove. Environ Sci Technol. 2004;38(8):23042311. 7. Moller W, Felten K, Sommerer K, et al. Deposition, retention, and translocation of ultrafine particles from the central airways and lung periphery. Am J Respir Crit Care Med. 2008;177(4):426-432. 8. Zhao W, Hopke PK, Norris G, et al. Source apportionment and analysis on ambient and personal exposure samples with a combined receptor model and an adaptive blank estimation strategy. Atmos Environ. 2006;40(20):37883801. 9. Bordado JC, Gomes JF, Albuquerque PC. Exposure to airborne ultrafine particles from cooking in Portuguese homes. J Air Waste Manag Assoc. 2012;62(10):11161126. 10. Zhang Q, Gangupomu RH, Ramirez D, et al. Measurement of ultrafine particles and other air pollutants emitted by cooking activities. Int J Environ Res Public Health. 2010;7(4):1744-1759.
11. Casas L, Tischer C, Tiesler C, et al. Association of gas cooking with children’s respiratory health: results from GINIplus and LISAplus birth cohort studies. Indoor Air. 2012;22(6):476-482. 12. See SW, Balasubramanian R. Risk assessment of exposure to indoor aerosols associated with Chinese cooking. Environ Res. 2006;102(2):197-204. 13. Dennekamp M, Howarth S, Dick C, et al. Ultrafine particles and nitrogen oxides generated by gas and electric cooking. Occup Environ Med. 2001;58(8):511-516. 14. Buonanno G, Morawska L, Stabile L. Particle emission factors during cooking activities. Atmos Environ. 2009;43(20):3235-3242. 15. Lunden MM, Delp WW, Singer BC. Capture efficiency of cooking‐related fine and ultrafine particles by residential exhaust hoods. Indoor Air. 2014. doi: 10.1111/ ina.12118. 16. Turner WJ, Logue JM, Wray CP. A combined energy and IAQ assessment of the potential value of commissioning residential mechanical ventilation systems. Building and Environment. 2013;60:194-201. 17. Anderson JO, Thundiyil JG, Stolbach A. Clearing the air: a review of the effects of particulate matter air pollution on human health. J Med Toxicol. 2012;8(2):166-175. 18. Korhonen R, Lahti A, Kankaanranta H, et al. Nitric oxide production and signaling in inflammation. Curr Drug Targets Inflamm Allergy. 2005;4(4):471-479. 19. Rosselli M, Keller PJ, Dubey RK. Role of nitric oxide in the biology, physiology and pathophysiology of reproduction. Hum Reprod Update. 1998;4(1):3-24. 20. Ricciardolo FL. Multiple roles of nitric oxide in the airways. Thorax. 2003;58(2):175-182. 21. Silva JS, Machado FS, Martins GA. The role of nitric oxide in the pathogenesis of Chagas disease. Front Biosci. 2003;8:s314-325. 22. Flamant-Hulin M, Caillaud D, Sacco P, et al. Air pollution and increased levels of fractional exhaled nitric oxide in children with no history of airway damage. J Toxicol Environ Health A. 2010;73(4):272-283. 23. La Grutta S, Ferrante G, Malizia V, et al. Environmental effects on fractional exhaled nitric oxide in allergic children. J Allergy (Cairo). 2012;2012:916-926. 24. Karrasch S, Ernst K, Behr J, et al. Exhaled nitric oxide and influencing factors in a random population sample. Respir Med. 2011;105(5):713-718. 25. Murray EL, Klein M, Brondi L, et al. Rainfall, household crowding, and acute respiratory infections in the tropics. Epidemiol Infect. 2012;140(1):78-86. 26. Rim D, Wallace L, Nabinger S, et al. Reduction of exposure to ultrafine particles by kitchen exhaust hoods: the effects of exhaust flow rates, particle size, and burner position. Sci Total Environ. 2012;432:350-356. 27. Perez P, Schilmann A, Riojas R. Respiratory health effects of indoor air pollution. Int J Tuberc Lung Dis. 2010;14(9):1079-1086. 28. Barone-Adesi F, Chapman RS, Silverman DT, et al. Risk of lung cancer associated with domestic use of coal in Xuanwei, China: retrospective cohort study. BMJ. 2012;345:e5414. 29. Liao CM, Chen SC, Chen JW, et al. Contributions of Chinese-style cooking and incense burning to personal exposure and residential PM concentrations in Taiwan region. Sci Total Environ. 2006;358(1-3):72-84. 30. Langrish JP, Li X, Wang S, et al. Reducing personal exposure to particulate air pollution improves cardiovascular health in patients with coronary heart disease. Environ Health Perspect. 2012;120(3):367-372. 31. Rim D, Wallace LA, Persily AK. Indoor ultrafine particles of outdoor origin: importance of window opening area and fan operation condition. Environ Sci Technol. 2013;47(4):1922-1929. 32. Olin A-C, Rosengren A, Thelle DS, et al. Height, age, and
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Human Subjects Statement The study was approved by the Medical Research Ethics Committee of Tongji Medical College. Written informed consent was obtained from all participants. Conflict of Interest Statement The authors declare no potential conflicts of interests with respect to the authorship and/or publication of this article. Acknowledgment This work was supported by research funds from the National Basic Research Program of China (2011CB512102) and National Key Basic Research and Development Program (2011CB503804). References
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Housing Characteristics in Relation to Exhaled Nitric Oxide in China atopy are associated with fraction of exhaled nitric oxide in a large adult general population sample. Chest. 2006;130(5):1319-1325. 33. Zhang X, Gray DJ, Huot Y, et al. Comparison of optically derived particle size distributions: scattering over the full angular range versus diffraction at near forward angles. Appl Opt. 2012;51(21):5085-5099. 34. Habib SS, Ahmed SM, Al Drees AM, et al. Effect of cigarette smoking on fractional exhaled nitric oxide in Saudi medical college students. J Pak Med Assoc. 2011;61(2):120-123. 35. Beg MF, Alzoghaibi MA, Abba AA, et al. Exhaled nitric oxide in stable chronic obstructive pulmonary disease. Ann Thorac Med. 2009;4(2):65-70. 36. Spanier AJ, Hornung R, Lierl M, et al. Environmental exposures and exhaled nitric oxide in children with asth-
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ma. J Pediatr. 2006;149(2):220-226. 37. Cornell AG, Chillrud SN, Mellins RB, et al. Domestic airborne black carbon and exhaled nitric oxide in children in NYC. J Expo Sci Environ Epidemiol. 2012;22(3):258266. 38. Franklin PJ, Stick SM, Le Souef PN, et al. Measuring exhaled nitric oxide levels in adults: the importance of atopy and airway responsiveness. Chest. 2004;126(5):15401545. 39. Olin AC, Rosengren A, Thelle DS, et al. Height, age, and atopy are associated with fraction of exhaled nitric oxide in a large adult general population sample. Chest. 2006;130(5):1319-1325. 40. Munakata M. Exhaled nitric oxide (FeNO) as a non-invasive marker of airway inflammation. Allergology International. 2012;61(3):365.
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Objective: To investigate indoor factors affecting fractional exhaled nitric oxide (FeNO) in community residents. Methods: A total of 2404 adults (865 men, 1539 women, mean age 51.7 ± 13.3 years) were recruited to the study. Factors affecting FeNO were analyzed by multiple linear regression analysis. Results: Participants without a kitchen exhaust fan/hood had higher FeNO (GM: 10.21%, 95% CI: 4.18%-16.59%). Participants engaged in home cooking who used only liquefied petroleum gas had
G
ood indoor air quality is associated with positive health.1 Poor indoor air quality increases risk of cardiovascular and respiratory diseases, asthma, and decline in lung function.2,3 People in many developing countries are commonly exposed to multiple indoor pollutants (such as particulates, carbon monoxide, and sulfur oxides) from the combustion of solid fuels in open fires or traditional stoves.4 Fan Hou, Xiji Huang, Chuanyao Liu, Huizhen Sun, Ting Zhou, Yuanchao Song, Yi Rong, Jing Wang, Jianshu Wang, Meian He, Associate Professor, Weihong Chen, Tangchun Wu, and Jing Yuan, Professors, Department of Occupational and Environmental Health, Key Laboratory of Environment and Health, Ministry of Education & Ministry of Environmental Protection, and State Key Laboratory of Environment Health (Incubation), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology. Beibei Zhu, Wei Chen and Xiaopin Miao, Professor, Department of Epidemiology and Biostatistics; Key Laboratory of Environment and Health, Ministry of Education & Ministry of Environmental Protection, and State Key Laboratory of Environment Health (Incubation), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology. Barbara Hoffmann, Professor, IUF Leibniz-Institut für umweltmedizinische Forschung Heinrich Heine Universität Düsseldorf, Dusseldorf, Germany. Fan Hou, Xiji Huang and Chuanyao Liu contributed equally to this work. Correspondence: Dr Jing Yuan; [email protected] and Dr Weihong Chen; [email protected]
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higher FeNO (GM: 5.75%, 95% CI: 0.10%11.73%) compared to those using natural gas for residential (home) cooking. Conclusion: Nonuse of a kitchen exhaust fan/hood and use of liquefied petroleum gas among persons engaged in home cooking were associated with higher FeNO levels. Key words: exhaled nitric oxide; housing characteristics; cooking fuel type; kitchen ventilation Am J Health Behav. 2015;39(1)88-98 DOI: http://dx.doi.org/10.5993/AJHB.39.1.10
Next to the contribution of outdoor particles, human activities, including smoking and cooking, often lead to indoor hazardous concentrations of carbon monoxide and airborne particulate matters smaller than 2.5 µm in diameter (PM2.5).5 For instance, cooking episodes produce a large amount of ultrafine particles (UFP) after just 15 minutes.6 It is noted that PM2.5, and specifically, UFP with multiple toxic components, can escape pulmonary filtering mechanisms and then enter the circulatory system of the body. They can cause potential toxic effects by binding directly to intracellular proteins and DNA within the cells because of their high surface-to-volume ratios per unit of mass.7 A previous study showed that the major contributing source of indoor PM was cooking oil fumes, which were responsible for about 52.5% of the personal exposure samples and 43.2% of the residential indoor concentrations.8 Cooking emissions including PM2.5, UFP, carbon dioxide, and black carbon are dependent largely on the type of kitchen stove and cooking style.9,10 Chronic exposure to cooking fuels shows a positive association with the prevalence of respiratory symptoms, including reduced lung function.11 In addition, gas stoves are the most important source of UFP in nonsmoking homes.12 Potentially toxic concentrations of particulate matter and high concentrations of nitrogen oxides were found while cooking meals using gas in poorly ventilated kitchens.13 Emission concentration of in-
Hou et al
Table 1 Socio-demographic Characteristics of Study Population Variable
Men: N = 865
Women: N = 1539
Total: N = 2404
p
52.5±13.4
51.3±13.3
51.7±13.3
.024a
18-44
237(27.4)
472(30.7)
709(29.5)
45-59
368(42.5)
678(44.1)
1046(43.5)
≥60
260(30.1)
389(25.3)
649(27.0)
Age (year, N, %)
Education (years, N, %)
< .001b
0-6
101(11.7)
389(25.3)
490(20.4)
7-12
620(71.7)
996(64.7)
1616(67.2)
>12
144(16.6)
154(10.0)
298(12.4)
Marital status (N, %)
< .001b
Never married
48(5.5)
46(3.0)
94(3.9)
Married
787(91)
1307(84.9)
2094(87.1)
Widowed
18(2.1)
153(9.9)
171(7.1)
Divorced
9(1.0)
23(1.5)
32(1.3)
Remarried
3(0.3)
10(0.6)
13(0.5)
Current occupational status (N, %)
< .001b
Students
12(1.4)
6(0.4)
18(0.7)
Workers
489(56.5)
568(36.9)
1057(44.0)
Unemployed
96(11.1)
291(18.9)
387(16.1)
Retired
196(22.7)
463(30.1)
659(27.4)
Others
72(8.3)
211(13.7)
283(11.8) (continued on next page)
door particles from cooking with a gas stove was markedly higher (60-118 mg/m3) than that from frying with an electric stove (12-27 mg/m3).14 However, effective exhaust hoods can mitigate the impact of pollutants emitted from home cooking processes on indoor air quality15 Higher lung function growth was associated with the use of household ventilation devices during the cooking process.16 Various factors can cause airway inflammation. For instance, PM exposure is associated with systemic inflammation in the body.17 Nitric oxide (NO) is a mediator and regulator of inflammatory responses.18 It plays an important role in various physiological and pathological events.19,20 Change in the production of nitric oxide relates to multiple organ dysfunction and associated syndromes. Nitric oxide synthases (NOS, including inducible iNOS; endothelial eNOS; and neuronal nNOS) participate in the processes of NO production.18 The production of iNOS-derived NO is associated with eosinophils, endothelial cells, and cardiac myo-
cytes.21 Measurement of fractional exhaled nitric oxide (FeNO) often is used as a marker of airway inflammation or as a marker for adverse respiratory health effects caused by indoor air pollution.22 Moreover, ambient particle matter and nitrogen dioxide (NO2) also show positive associations with FeNO level.23 FeNO level is associated with asthma symptoms; its level is influenced by sex, age, ethnicity height, weight, neutrophil counts, and environmental pollutants.24 In this study, we investigated the association between cooking fuel type and use of a kitchen exhaust fan/hood with FeNO levels using baseline data from a Chinese community cohort study, after controlling potential confounders.
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METHODS Study Population and Physical Examination The baseline survey of the cohort study was carried out during April and May 2011 in the Hankou and Hanyang districts in Wuhan metropolitan
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Housing Characteristics in Relation to Exhaled Nitric Oxide in China
Table 1 (continued) Socio-demographic Characteristics of Study Population Variable
Men: N = 865
Women: N = 1539
Total: N = 2404
Smoking status (N, %) Never smoker
p < .001b
294(34.0)
1491(96.9)
1785(74.3)
Former smoker
114(13.2)
6(0.4)
120(5.0)
Current smoker
457(52.8)
42(2.7)
499(20.8)
Passive smoke exposure (N, %)
.002b
Yes
398(46.0)
803(52.2)
1201(50.0)
No
467(54.0)
736(47.8)
1203(50.0)
Drinking status (N, %)
< .001b
Never drinker
402(46.5)
1457(94.7)
1859(77.3)
Former drinker
71(8.2)
15(1.0)
86(3.6)
Current drinker
392(45.3)
67(4.4)
459(19.1)
Physical activity (N, %)
.060b
Yes
370(42.8)
651(42.3)
1021(42.5)
No
495(57.2)
888(57.7)
1383(57.5)
Kitchen exhaust fan/hood (N, %)
.973b
Yes
765(88.4)
1361(88.5)
2126(88.4)
No
100(11.6)
178(11.6)
278(11.6)
Self-catering
< .001b
Yes
443(51.2)
1257(81.7)
1700(70.7)
No
422(48.8)
282(18.3)
704(29.3) (continued on next page)
area, China. The local temperatures were between 20° C (68.0° F) and 32°C (89.6° F) during the investigation. A total of 3698 community residents who had lived in the city for at least 5 years were invited to participate in the study. Of these, only persons aged 18 and over were included as participants for analysis purposes. Participants who did not agree to provide blood samples or answer questionnaire information (N = 577) and participants under the age of 18 years (N = 29) were excluded. Participants with missing data on FeNO measurement (N = 126), on lung function measurement (N = 67), or on neutrophil count (N = 149) were excluded from our analysis. We also excluded participants with self-reported asthma (N = 33), chronic bronchitis (N = 160), or diabetes (N = 153). Thus, 2404 adults (865 men, 1539 women) aged ≥ 18 years (mean age 51.7 ± 13.3 years) were included. Data were collected by questionnaire and included social-demographic characteristics, lifestyle habits, cooking fuel type (natural gas, liquefied petroleum gas, coal, and electricity), type of kitchen ventilation (venting through opening the windows, use of kitchen exhaust fan/hood), housing conditions (such as home ventilation, way of heating
90
the home, per capita living space and floor), pet ownership (including cat, dog, avian pets, tortoise, and aquatic pets) as well as personal and family medical history. Physicians conducted physical examinations on all participants according to standard methods, including measurements of height, weight, waist circumference, hip circumference, heart rate, and blood pressure. Body mass index was calculated by body weight in kilograms divided by height in meters squared. Complete Blood Count Test We collected 2ml of venous peripheral blood in a vacutainer tube containing an anticoagulant (ethylenediaminetetra-acetate and sodium citrate) from each participant. A complete blood count test was performed immediately using a Hematology Analyzer (pocH-100i, Sysmex Corporation, Kobe, Japan). Exhaled Nitric Oxide Measurement FeNO measurement was performed using a Nano Coulomb Nitric Oxide Analyzer (SV-02E, Sunvou Medical Electronics Co., Ltd. Wuxi, Jiangsu, China). This device for measurement of FeNO is based
Hou et al
Table 1 (continued) Socio-demographic Characteristics of Study Population Variable
Men: N = 865
Women: N = 1539
Total: N = 2404
House condition (N, %)
.669b
Tiled one-story brick house
15(1.7)
20(1.3)
35(1.5)
Hovels
4(0.5)
6(0.4)
10(0.4)
846(97.8)
1513(98.3)
2359(98.1)
≤2
399(47.2)
676(44.7)
1075(45.6)
3
176(20.8)
313(20.7)
489(20.7)
Apartment (floors, N, %)
>3 Housing area (m2, mean±SD)
271(32.0)
524(34.6)
795(24.3)
111.9±91.1
102.3±79.8
105.8±84.1
Heating appliances in winter (N, %) Never used Natural gas heating system Radiator
d
Coal stove and heater brick bed
517(59.8)
860(55.9)
1377(57.3)
6(0.7)
14(0.9)
20(0.8)
336(38.8)
656(42.6)
992(41.3)
6(0.7)
9(0.6)
15(0.6)
.029c
.762b 32(3.7)
53(3.4)
85(3.5)
Natural gas only
208(24.0)
343(22.3)
551(70.8)
Liquefied petroleum gas
601(69.5)
1100(71.5)
1701 (22.9)
24(2.8)
43(2.8)
67(2.8)
Firewood plus coal
.401b
.284b
Cooing fuel type (N, %) Electromagnetic oven only
p
Note. a Student’s t test was used to compare the mean values of the continuous variables. b Chi-square test was used to observe the association between 2 categorical variables. c Mann-Whitney test was used to compare 2 groups of abnormal distribution data. d Radiator: including oil-filled radiator, electric blanket, quartz heater and air conditioning.
on the potentiostatic coulometry approach through electrolysis of exhaled nitric oxide following Faraday’s laws. The device was validated through correlation and agreement comparisons for both standard bottled gas and exhaled air with an electrochemical analyzer (NIOX MINO, Aerocrrine AB, Solina, Sweden) with a correlation coefficient of 0.984, by SFDA (the State Food and Drug Administration of China). To ensure comparability with other standard approaches for FeNO measurement during this study, the device also was validated and calibrated by standard bottled gas (15, 75 and 150 ppb) and NIOX MINO on a weekly basis. The measurement procedure was performed according to the 2005 ATS/ERS guidelines before conducting spirometry. The participant was asked to fast (eating and drinking) and refrain from smoking for at least one hour and strenuous exercise at least onehalf hour before measurement. Under the instruction of the technician, the participant was seated comfortably and asked to inhale deeply. A NO-free air filter was placed in his/her mouth before exhaling smoothly at a speed of 50 ± 5 milliliters per
second for 4 to 10 seconds. The initial 3 seconds were used to exclude “dead space” volume as well as possible effects of inhaled ambient gas. The exhaled gas was analyzed online and the stable mean FeNO value was recorded. The lowest detection limit is 5 part per billion (ppb) and the analytical accuracy is ± 3 ppb when the measured value is < 50 ppb, or ± 10% when measured value ≥ 50 ppb. FeNO values were expressed as ppb.
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Pulmonary Function Tests Pulmonary function tests were performed on all eligible participants, using the portable battery-operated spirometers (CHESTGRAPH HI-101, Chest MI, Inc, Tokyo, Japan). The parameters including vital capacity (VC), forced vital capacity (FVC) and forced expiratory volume produced in the first second (FEV1) were measured. Participants were asked to perform several forced expiratory maneuvers to obtain 3 repeatable maneuvers according to the recommendations of the American Thoracic Society (ATS) 2005 guidelines on the interpretation of lung function tests.
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Housing Characteristics in Relation to Exhaled Nitric Oxide in China
Table 2 Clinical Characteristics of Study Population Men: N = 865
Women: N = 1539
Total: N = 2404
p
Height (cm, mean±SD)
166.7±6.4
155.7±5.7
159.6±7.9
< .001a
Weight (kg, mean±SD)
67.6±10.8
57.8±8.8
61.3±10.6
< .001b
Body mass index (BMI, kg/m2, mean±SD)
24.3±3.4
23.8±3.5
24.0±3.4
< .001b
Waist circumference (mm, mean±SD)
851.8±93.6
795.8±93.2
816.1±97.2
< .001a
Hip circumference (mm, mean±SD)
953.3±61.4
938.2±63.9
943.7±63.4
< .001b
Heart rate (beats/min, mean±SD)
73.8±11.4
75.6±10.4
74.9±10.8
< .001b
Systolic blood pressure (mmHg, mean±SD)
134.2±20.2
127.8±20.4
130.1±20.5
< .001b
Diastolic blood pressure (mmHg, mean±SD)
79.3±11.6
74.9±10.9
76.5±11.4
< .001b
Mean corpuscular hemoglobin (pg, mean±SD)
34.6±3.2
32.7±3.2
33.4±3.3
< .001b
Hemoglobin (g/L, mean±SD)
151.9±23.1
132.8±23.5
139.7±25.1
< .001b
Mean corpuscular volume (femtolitre, mean±SD)
96.5±15.6
95.7±17.1
96.0±16.6
< .001b
0.448±0.102
0.411±0.107
0.424±0.107
< .001b
Count of total white blood cells (109/L, mean±SD)
6.1±2.9
5.6±1.8
5.8±2.3
< .001b
Neutrophil count (109/L, mean±SD)
3.6±1.2
3.2±1.1
3.3±1.1
< .001a
Vital capacity (L, mean±SD)
3.6±0.7
2.7±0.5
3.0±0.7
< .001a
Forced vital capacity (L, mean±SD)
3.10±0.71
2.34±0.52
2.61±0.70
< .001a
FEV 1 (L, mean±SD)
2.65±0.61
2.02±0.44
2.25±0.59
< .001a
FEV1/FVC (%, mean±SD)
85.83±9.33
86.77±8.72
86.43±8.96
< .001b
Variable
Hematocrit (L/L, mean±SD)
FeNO level (ppb, geometric mean(95% CI) )
26.34(25.56-27.16)
21.88(21.34-22.42) 23.39(22.94-23.85) < .001b
Self-reported response to allergen (N, %)
< .001c
Yes
109(12.6)
309(20.1)
418(17.4)
No
756(87.4)
1230(79.9)
1986(82.6)
Self-reported frequent cough (N, %)
< .001c
Yes
151(17.5)
145(9.4)
296(12.3)
No
714(82.5)
1394(90.6)
2108(87.7)
Note. a Student’s t test was used to compare the mean values of the continuous variables. b Mann-Whitney test was used to compare 2 groups of independent data. c Chi-square test was used to observe the association between 2 categorical variables Pg, pico gram; FEV 1, forced expiratory volume in one second; FeNO, fractional exhaled nitric oxide; ppb, part per billion; 95% CI, 95% confidence interval.
Statistical Methods The logarithm-transformed FeNO values (Kolmogorov-Smirnov p < .001) were expressed as the geometric means (GM) and 95% CIs. In subgroup analyses, we stratified the analysis by possible effect modifiers including sex, age, smoking status, passive smoking exposure, and current occupational status. Multiple linear regression was used to analyze the association of cooking fuel type and use/nonuse of a kitchen exhaust fan/hood with FeNO levels. We began with an unadjusted anal-
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ysis (model 1), only including domestic cooking fuel exposure and use of a kitchen exhaust fan/ hood, as well as possible confounders and predictors each in separate analyses. We then performed model 2, including sex, age, annual family income, education level, cooking style at home, including fuel type and use/nonuse of a kitchen exhaust fan/hood. Model 3 represents the analysis adjusted for covariates in model 2 plus smoking, passive smoking exposure, height, weight, complete blood count, and heart rate. Model 4 adjusts for covari-
Hou et al
Table 3 Multiple Regression Analysis Association between FeNO Levels (Log10) and the Selected Parameters Model 1a Variable
Partial Power regression of coefficient parameter
Model 2b Δ% of FeNO (95% CI)
Partial Power regression of coefficient parameter
Δ% of FeNO (95% CI)
Sex
0.081**
1.204
20.43(15.69-25.36)
0.078**
1.198
19.76(15.09-24.63)
Age (10 years)
0.020**
1.047
4.74(3.23-6.28)
0.019**
1.044
4.35(2.87-5.86)
Education
-
-
-
-
-
-
Marital status
-
-
-
-
-
-
-
-
-
Annual family income Height
-
-
-
0.043**
1.104
10.42(7.76-13.14)
Weight
0.001**
1.003
0.31(0.17-0.45)
Systolic blood pressure
0.001**
1.001
0.14(0.05-0.23)
Diastolic blood pressure
-
-
-
Heart rate
-
-
-
Hemoglobin
-
-
-
Mean corpuscular volume Hematocrit
-
-
-
0.203**
1.596
59.68(33.03-91.66)
Count of total white blood cells
-
-
-
Neutrophil count
-
-
-
Vital capacity
0.028**
1.067
6.75(3.92-9.65)
Forced vital capacity
0.026**
1.062
6.20(3.28-9.21)
FEV1
0.030**
1.071
7.09(3.61-10.69)
0.000
1.000
-
Former smoker
0.087**
1.221
22.10(11.56-33.62)
Current smoker
-0.005
0.989
-1.10(-5.78-3.81) -
-
-
0.044**
1.107
10.72(4.43-17.40)
0.042**
1.101
10.09(3.96-16.57)
0.000
1.000
-
0.000
1.000
-
Liquefied petroleum gas
-
-
-
-
-
-
Firewood plus coal
-
-
-
-
-
-
Electromagnetic oven only
-
-
-
-
-
-
Smoking status Never smoker
Self-catering Kitchen exhaust fan/hood Cooking fuel type Natural gas only (reference)
(continued on next page)
ates in model 3 plus current occupational status, physical exercise, pet ownership, FVC, VC, and FEV1. All statistical tests were performed using SPSS 12.0 software (SPSS, Chicago, IL, USA). RESULTS Characteristics of the Participants As Table 1 shows, the average age of participants was 51.7 ± 13.3 years. There were differences between the 2 sexes in educational attainment, mari-
tal status, current occupational status, active and passive smoking, alcohol consumption, housing area, and self-catering (p < .01 for all). As Table 2 shows, there were differences in the medical parameters between men and women. Prevalence of most medical conditions were higher in men than in women (p < .01), with the exception of the indicators including heart rate, FEV 1/ FVC ratio, and self-reported allergic disease. The FeNO level of participants was 23.39 ppb (95%
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Housing Characteristics in Relation to Exhaled Nitric Oxide in China
Table 3 (continued) Multiple Regression Analysis Association between FeNO Levels (Log10) and the Selected Parameters Model 3c Variable
Partial Power regression of coefficient parameter
Model 4d Δ% of FeNO (95% CI)
Partial Power regression of coefficient parameter
Δ% of FeNO (95% CI)
Sex
0.100**
1.258
25.83(18.10-34.07)
0.091**
1.234
23.37(15.50-31.78)
Age (10 years)
0.024**
1.056
5.60(4.04-7.18)
0.028**
1.066
6.63(4.79-8.50)
Education
-
-
-
-
-
-
Marital status
-
-
-
-
-
-
Annual family income
-
-
-
-
-
-
0.039**
1.095
9.49(5.93-13.18)
0.033**
1.080
7.96(4.18-11.86)
Weight
-
-
-
-
-
-
Systolic blood pressure
-
-
-
-
-
-
Height (10 cm)
Diastolic blood pressure
-
-
-
-
-
-
Heart rate (10 beats/min)
0.010**
1.024
2.36(0.59-4.17)
0.010**
1.024
2.36(0.59-4.16)
Hemoglobin
-
-
-
-
-
-
Mean corpuscular volume
-
-
-
-
-
-
Hematocrit
-
-
-
-
-
-
Count of total white blood cells
-
-
-
-
-
-
Neutrophil count
-
-
-
-
-
-
Vital capacity
-
-
-
Forced vital capacity
-
-
-
0.023*
1.054
5.39(0.38-10.65)
FEV1(L) Smoking status Never smoker
0.000
1.000
-
0.000
1.000
-
Former smoker
-0.040
0.911
-8.87(-17.30-0.41)
-0.038
0.917
-8.34(-16.82-1.00)
Current smoker
-0.116**
0.765
-23.51(-28.10-18.62)
-0.116**
0.766
-23.44(-28.03-18.55)
-
-
-
-
1.099
9.93(3.92-16.29)
1.102
10.21(4.18-16.59)
Self-catering Kitchen exhaust fan/hood Cooking fuel type
0.041**
0.042**
-
-
-
-
-
-
0.000
1.000
-
0.000
1.000
-
Liquefied petroleum gas
-
-
-
-
-
-
Firewood plus coal
-
-
-
-
-
-
Electromagnetic oven only
-
-
-
-
-
-
Natural gas only (reference )
*p < .05 **p < .01 Note. a Model 1: Unadjusted model. b Model 2: Adjusted for sex, age, annual family income, education level, self-catering, cooking fuel type and nonuse of a kitchen exhaust fan/hood. c Model 3: Model 2 plus smoking status, passive smoking exposure, height, weight, complete blood count and heart rate. d Model 4: Model 3 plus current occupational status, physical exercise, pet, VC, FVC and FEV1. FeNO, fractional exhaled nitric oxide; 95% CI, 95% confidence interval; FEV1, forced expiratory volume in one second.
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Table 4 Multiple Regression Analysis Associations between FeNO Levels (Log10) and the Selected Parameters by Cooking Participants without self-cateringa (N = 704)
Participants with self-catering a (N = 1700)
Partial regression coefficient
Power of parameter
△% of FeNO (95% CI)
Partial Power regression of paracoefficient meter
Sex
0.106**
1.276
27.61(14.56-42.15)
0.098**
1.255
25.46(15.59-36.17)
Age (10 years)
0.017**
1.040
4.04(1.60-6.54)
0.025**
1.060
5.98(3.92-8.09)
Education level
-
-
-
-
-
-
Annual family income
-
-
-
-
-
-
0.050**
1.122
12.22(5.60-19.25)
0.034**
1.082
8.19(3.98-12.57)
Heart rate (10 beats/min)
-
-
-
-
-
-
FEV1
-
-
-
-
-
-
Never smoker (reference)
0.000
1.000
-
0.000
1.000
-
Former smoker
-0.039
0.914
-8.56(-21.18-6.09)
-0.038
0.917
-8.32(-19.41-4.29)
Current smoker
-0.115**
0.767
-23.26(-30.02--15.84)
-0.118**
0.762
-23.75(-29.88--17.09)
0.052**
1.128
12.81(2.13-24.61)
0.034*
1.081
8.12(0.74-16.03)
0.000
1.000
-
0.000
1.000
-
Liquefied petroleum gas
-
-
-
0.024*
1.058
5.75(0.10-11.73)
Firewood plus coal
-
-
-
0.012
1.028
2.79(-11.04-18.77)
Electromagnetic oven only
-
-
-
0.019
1.045
4.54(-8.93-20)
Variable
Height (10 cm)
△% of FeNO (95% CI)
Smoking status
Exhaust fan/range hood Cooking fuel type Natural gas only (reference)
*p < .05 **p < .01 Note. a Adjusted for sex, age, annual family income, education level, smoking status, height, heart rate, FEV1, nonuse of a kitchen exhaust fan/hood and cooking fuel type. FeNO, fractional exhaled nitric oxide; 95% CI, 95% confidence interval; FEV 1, forced expiratory volume in one second.
CI: 22.94-23.85 ppb). The FeNO levels of men and women were 26.34 ppb (95% CI: 25.56-27.16 ppb) and 21.88 ppb (95% CI: 21.34-22.42 ppb, p < .01), respectively. Multiple Factors Analysis for FeNO Levels As shown in Table 3, in crude models, sex, age, height, weight, systolic blood pressure, hematocrit, vital capacity, forced vital capacity, FEV1, former smoking, and nonuse of a kitchen exhaust fan/hood all showed a positive association with FeNO (p < .01). In model 2, after adjusting for the confounding variables including sex, age, annual family income, education level, residential cook-
ing, cooking fuel type, and use/nonuse of a kitchen exhaust fan/hood, we found that age, sex and nonuse of a kitchen exhaust fan/hood showed a positive association with FeNO (p < .01). In model 3, after adjusting for the covariates in model 2 plus smoking status, passive smoking exposure, height, weight, complete blood count, and heart rate, we found that sex, age, height, heart rate and nonuse of a kitchen exhaust fan/hood were positively associated with FeNO (p < .01), but current smoking was negatively associated with FeNO (p < .01). In model 4, after adjusting for the covariates in model 3 plus current occupational status, physical exercise, pet ownership, FVC, VC and
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Housing Characteristics in Relation to Exhaled Nitric Oxide in China FEV1, we obtained similar results to those in model 3. We found that the relative increase of FeNO in men was 23.37% (95% CI: 15.50-31.78%) compared to women; current smoking reduced FeNO by 23.44%; moreover, nonuse of a kitchen exhaust fan/hood was associated with 10.21% (95% CI: 4.18-16.59%) increase in FeNO. Increases in age by 10 years, in height by 10 centimeters, in heart rate by 10-beats/min and in FEV1 by one liter were associated with increases of FeNO by 6.63, 7.96, 2.36 and 5.39%, respectively. We did not find associations between FeNO and education, marital status, annual family income, weight, blood pressure, complete blood count, FVC, VC physical exercise, and being a pet owner (p > .05). As Table 4 shows, the relative increase of FeNO through residential cooking and use of liquefied petroleum gas among participants was 5.75% (95% CI: 0.10-11.73%), compared with persons who cooked at home using natural gas only, in addition to increases associated with the risk factors included in model 4. DISCUSSION In addition to pollution created by active smoking, the incomplete combustion of cooking fuels is a source of indoor particulate matter, thereby contributing further to poor air quality.25 The complex composition of UFP including carbon (soot), aerosols, fungal spores, and bacterial endotoxins can penetrate the lung epithelium and be transferred to the liver, brain, and heart, potentially leading to a systemic inflammatory response. Our results showed that use of liquefied petroleum gas as a cooking fuel had a positive association with the FeNO levels among participants cooking at home; but, it was negatively associated with the FeNO levels in those using a kitchen exhaust fan/hood. Use of a kitchen exhaust fan/hood improved indoor air quality via reducing indoor air pollutants (such as PM, nitrogen oxides, and carbon monoxide) emitted from household activities like indoor smoking and cooking on stoves. Gas cooking in homes with poor ventilation or a kitchen without an exhaust fan/hood often leads to hazardous concentrations of multiple indoor pollutants including particulate matters and nitrogen oxides, even causing adverse health effects, particularly, an increased risk of respiratory diseases.13,26 In addition, an elevated FeNO level among participants was related to exposure to ambient particulate matters and nitrogen dioxide.23 Some Chinese still use traditional energy sources such as coal and liquefied petroleum gas to meet their cooking and heating demands; thus, people are exposed to a broad range of pollutants from indoor sources.26,27 Several studies in China show that indoor air quality is commonly affected by cooking fumes emitted from Chinese-style cooking processes.5,28 Domestic cooking appliances and Chinese cooking processes lead to the generation and emission of substantial amounts of air pol-
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lutants;10,29 however, cooking accompanied by a kitchen exhaust hood reduces exposure to UFP.26 Exposure to cooking fumes may be responsible for elevated FeNO.10 Our findings indicated that using liquefied petroleum gas as cooking fuel was associated with elevated FeNO levels in participants who cooked at home; however, participants who used a kitchen exhaust fan/hood had reduced FeNO levels, indicating that indoor air quality was improved and potentially adverse health effects were successfully mitigated. This hypothesis is supported by the finding that wearing a face mask as a short-term measure reduced the cardiovascular effects of high ambient particulate air pollution.30 Apart from this, window position and air exchange rate in homes might affect FeNO levels via affecting indoor UFP concentration.23,31 In our study, current smokers had lower FeNO (with a 23.44% reduction) relative to never smokers, which is consistent with previous studies reporting that current smokers had reduced FeNO levels.32,33 For example, one study reported that FeNO levels were lower in current smokers (a 70% reduction) than in nonsmokers.32 Reduced FeNO could be an early indicator of effects of smoking on lungs by downward regulation of eNOS and iNOS.34,35 However, FeNO was not associated with nicotine.36 Elevated FeNO among participants exposed to air pollution may be due to direct modulation of normal physiological function or potentiation of compromised organ responses. Both extrinsic (environmental exposure and asthma treatment) and intrinsic factors (age, race, and NO synthase gene) affect personal FeNO.37 Moreover, elevated FeNO was related to clinic manifestations among patients with atopic diseases.38 We found FeNO differences between and within populations. FeNO in this study was higher (GM: 23.39 ppb, 95% CI: 22.94-23.85 ppb) than among Germans (GM: 13.9 ppb, 95% CI: 10.8-79.4 ppb),24 among healthy Japanese adults (GM: 15.4 ppb, mean ± 2SD: 6.5-36.8 ppb), and among persons in a Sweden-based sample (median: 16.0 ppb, range: 2.4-199 ppb).39 Racial characteristics, higher baseline indoor and outdoor air pollution, as well as study-specific characteristics, such as selection of participants might contribute to observed higher FeNO of Chinese adults in this study. Furthermore, we realized that the implications of the findings regarding indoor air pollutants emitted from cooking with use of liquefied petroleum or nonuse of an exhaust fan were not the only factors affecting elevated FeNO, because elevated FeNO levels were associated with certain diseases such as bronchial asthma.40 In conclusion, participants who engaged in residential cooking without using a kitchen exhaust fan/hood had higher FeNO levels. Participants who cooked with liquefied petroleum gas in their homes had higher FeNO levels. Our findings reveal that housing characteristics may be related to higher FeNO levels in these Chinese adults.
Hou et al The present study has certain limitations: firstly, individual-level exposure to both indoor and outdoor air pollutants and allergens was not monitored, so we had to rely on published observations relating to impacts of China cooking styles on indoor air quality and human health. Secondly, the study was a cross-sectional investigation and causality cannot be inferred. Thirdly, data concerning the variation in human responses to air pollutants and allergens across individuals were not available.
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Human Subjects Statement The study was approved by the Medical Research Ethics Committee of Tongji Medical College. Written informed consent was obtained from all participants. Conflict of Interest Statement The authors declare no potential conflicts of interests with respect to the authorship and/or publication of this article. Acknowledgment This work was supported by research funds from the National Basic Research Program of China (2011CB512102) and National Key Basic Research and Development Program (2011CB503804). References
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