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Original Research: COPD |

Chinese Water-Pipe Smoking and the Risk of COPDNew Risk of COPD FREE TO VIEW

Jun She, MD, PhD; Ping Yang, MD, PhD; Yuqi Wang, MD, PhD; Xinyu Qin, MD, PhD; Jia Fan, MD, PhD; Yi Wang, PhD; Guangsuo Gao, MD; Guangxiong Luo, MD; Kaixiang Ma, MD; Baoyan Li, MD; Caihua Li, MD; Xiangdong Wang, MD, PhD; Yuanlin Song, MD; Chunxue Bai, MD, PhD, FCCP
Author and Funding Information

From the Department of Pulmonary Medicine (Drs She, Yuqi Wang, Qin, Fan, X. Wang, Song, and Bai), Zhongshan Hospital, Fudan University, Shanghai, China; the Department of Health Sciences Research (Drs Yang and Yi Wang), Mayo Clinic, Rochester, MN; Fuyuan County Hospital (Drs Gao, Luo, Ma, B. Li, and C. Li), Yunnan, China; And the Division of Preventive Medicine (Dr Yi Wang), Wenzhou Medical University, Zhejiang, China.

CORRESPONDENCE TO: Chunxue Bai, MD, PhD, FCCP, Department of Pulmonary Medicine, Zhongshan Hospital, Fudan University, 180 Fenglin Rd, Shanghai, China, 200032; e-mail: bai.chunxue@zs-hospital.sh.cn


FOR EDITORIAL COMMENT SEE PAGE 875

This study was presented as an oral presentation at CHEST 2012, October 20-25, 2012, Atlanta, GA.

FUNDING/SUPPORT: This work was supported primarily by the National Key Scientific and Technology Support Program: Collaborative Innovation of Clinical Research for Chronic Obstructive Pulmonary Disease and Lung Cancer [2013BAI09B09]. Dr She was supported by the National Natural Science Foundation for Young Scholars of China [ 81200051]; the Research Fund for the Doctoral Program of Higher Education of China [20110071120060]; the Science Foundation for Young Scholars in Zhongshan Hospital [2012ZSQN04]; and the Scientific Project for Fudan University [20520133474].

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2014;146(4):924-931. doi:10.1378/chest.13-1499
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BACKGROUND:  Studies show that the incidence of COPD has remained high in southwest China despite the 1976 National Stove Improvement Program for indoor air quality. Chinese water-pipe tobacco smoking (commonly referred to as water-pipe smoking), which is thought to be less harmful under the assumption that no charcoal is used and water filters tobacco smoke, is popular in China. We investigated whether Chinese water-pipe use and exposure are associated with the risk of COPD.

METHODS:  This multicenter, cross-sectional study enrolled 1,238 individuals from 10 towns in the Fuyuan area, Yunnan Province, China. A matched design was used to estimate the impact of active and passive exposure to Chinese water-pipe smoking on COPD risk; multivariate analyses adjusted for other risk factors. We also collected the water from Chinese water pipes to assess the mutagenicity of its major components and simulated Chinese water-pipe smoke exposure fine particulate 2.5 (PM2.5) by using the High Volume Air Sampler and individuals’ sera to search for the potential protein biomarkers of COPD.

RESULTS:  The increased risk of COPD was profound for Chinese water-pipe smokers (adjusted OR, 10.61; 95% CI, 6.89-16.34), Chinese water-pipe passive smokers (adjusted OR, 5.50; 95% CI, 3.61-8.38), cigarette smokers (adjusted OR, 3.18; 95% CI, 2.06-4.91), and cigarette passive smokers (adjusted OR, 2.52; 95% CI, 1.62-3.91) compared with never-smoking control subjects. Chinese water-pipe use aggravates lungs with more PM2.5 compared with cigarettes. ChemR23 and tissue inhibitor of metalloproteinase-1 may be potential protein biomarkers of COPD.

CONCLUSIONS:  Chinese water-pipe smoking significantly increases the risk of COPD, including the risk to women who are exposed to the water-pipe smoke.

TRIAL REGISTRY:  Chinese Clinical Trial Registry; No.: ChiCTR-CCH-12002235; URL: www.chictr.org/cn/

Figures in this Article

COPD is a major global health problem with rising incidence and morbidity, and it is anticipated that it will become the fourth-leading cause of death worldwide before 2030. Its prevalence is 9% to 10% in adults older than 40 years of age.1 Most studies in China have demonstrated that the high incidence of COPD is associated with indoor air pollution in southwest China (ie, burning of biomass fuels at home, such as coal and wood for cooking and heating).25 Since 1976, the National Stove Improvement Program (NSIP) in China has improved indoor air quality by introducing > 180 million stoves with chimneys (Fig 1),4,5 but the Fuyuan area of Yunnan Province in China is an example of an area that still has a high lung disease prevalence.6 Epidemiology studies indicate that the incidence of COPD is double the national mean7,8 and, in reality, the NSIP has not been as effective as expected in preventing lung diseases.9,10

Figure Jump LinkFigure 1 –  A, Chinese water pipe (A-1), inside of Chinese water pipe (A-2), Chinese water-pipe holder (A-3), and Arabic water pipe (A-4). B, The National Stove Improvement Program to improve indoor air quality in China. Improved stove (B-1) with chimney (B-2).Grahic Jump Location

The global increase in tobacco smoking with a water pipe (ie, hookah, narghile, or shisha) has contributed to the health consequences of COPD and its related diseases.11 The Chinese water pipe (Fig 1A) is popular in Asia, including, but not limited to, China, Burma, Laos, and Vietnam.12 However, little information is known by the public about a regional endemic related to the Chinese water pipe, which is different from the Arabic water pipe. Traditionally, the Chinese water pipe has been misconceived as less harmful for three reasons: (1) no charcoal is used, in contrast to the Arabic water pipe; (2) tobacco smoke passes through the water, unlike in cigarette smoking (ie, Chinese water-pipe smoke is filtered by the water); and (3) smoking through a large-volume water pipe may “improve lung function” (assuming breath strength and vital capacity increase after long-term smoking of the water pipe; this is disproven in our current study).6,13

We postulated that active and passive Chinese water-pipe exposure may be a culprit that could impair pulmonary function via large volumes of smoke containing toxic constituents. Additionally, we simulated Chinese water-pipe smoke exposure fine particulate 2.5 (PM2.5) by using the High Volume Air Sampler (G701, Thermo Andersen), and collected subjects’ sera to search for potential protein biomarkers for the high rates of COPD.

Individuals and Study Design

This multicenter, population-based, cross-sectional study (October 15, 2011 to January 12, 2013) enrolled 1,238 individuals from 10 towns (Dahe, Dongshan, Housuo, Fuchun, Zhongan, Yingshang, Zhuyuan, Laochang, Shibalianshan, and Huangnihe) covering a wide geographic area in Fuyuan County, Yunnan Province, China, and representing a total population of > 780,000.

We targeted all residents ≥ 40 years of age14 and used a random-digit phone sampling at 12 local hospitals and clinics (see e-Appendix 1). In these areas, nearly all people who smoke Chinese water pipes are men; female water-pipe smokers are extremely rare. Therefore, a Chinese water pipe is commonly smoked in the household by the man and the wife would be exposed to passive smoking.

Passive smoke refers to the smoke that nonsmokers breathe in from active smokers. People who spend time around smokers are breathing in either the smoke from the end of burning cigarette or the smoke expelled by the active smoker. Consequently, study individuals were assigned to six groups (cases 1-4 and control subjects 5-6): (1) Chinese water-pipe smokers (CWSs) (all men), (2) Chinese water-pipe passive smokers (CWPSs) (all women), (3) cigarette smokers (CSs) (all men), (4) cigarette passive smokers (CPSs) (all women), (5) healthy control subjects never smokers (NSs) (all men), and (6) never passive smokers (NPSs) (all women).

Cases and control groups were frequency matched (Table 1). Individuals were excluded if they were hospitalized or had an unknown tobacco smoke history.15 People with a history of severe heart, liver, kidney, nervous and muscle diseases or smoking cessation due to these diseases, and those who had a current infectious disease, were also excluded from the study.

Table Graphic Jump Location
TABLE 1 ]  Characteristics of the Study Individuals

Data are shown as mean (SD) or No. (%) unless otherwise indicated. In the Fuyuan area, most of the people who smoke the Chinese water pipe are men; female water-pipe smokers are rare. Alcohol consumption was defined as drinking alcohol on at least 12 occasions during the past 12 mo. Hypertension was defined as a mean systolic BP of 140 mm Hg or higher, a diastolic BP of 90 mm Hg or higher, or the use of an antihypertensive medication. COPD was diagnosed by lung function; chronic bronchitis and emphysema were diagnosed by chest radiograph. CS = cigarette smoker; CPS = cigarette passive smoker; CWPS = Chinese water-pipe passive smoker; CWS = Chinese water-pipe smoker; NPS = never passive smoker; NS = never smoker.

a 

P < .01 CWS vs CS.

b 

P < .01 CWS vs NS.

c 

P < .01 CWPS vs NPS.

d 

P < .01 CWPS vs CPS.

e 

P < .05 CWPS vs CPS.

f 

P < .05 CWS vs CS.

g 

P < .05 CWS vs NS.

The study was approved by the ethics committees of Zhongshan Hospital, Fudan University, in accordance with the Declaration of Helsinki.16 All literate participants gave written informed consent. For illiterate participants, the study goals and procedures were explained verbally; then each illiterate participant voluntarily put his or her fingerprint on the informed consent document.3

Data Collection

Data on demographic characteristics, medical history, and lifestyle risk factors were obtained using a standard questionnaire administered by trained personnel.16 Chinese water-pipe and cigarette smoking were defined as having smoked at least 400 cigarettes per year ≥ 1 years, and one cigarette was considered to be equivalent to 1 g of tobacco. Lung function (ie, FEV1, FVC, and FEV1/FVC) was examined by spirometry (CHEST HI-801; CHEST M.I., Inc).17 Subjects with airflow limitations underwent postbronchodilator testing at 15 to 20 min after inhaling a dose of 200 μg of salbutamol (Ventolin; GlaxoSmithKline). According to the diagnostic criteria of the GOLD (Global Initiative for Chronic Obstructive Lung Disease),14 we defined subjects with a postbronchodilator FEV1/FVC < 70% as having COPD. Restrictive disorder was defined as FEV1/FVC ≥ 70% and FVC < 80% of predicted values.

Chest radiographs were performed in local hospitals. In cases of emphysema, chest radiographs showed an increased lung size, as measured from front to back; focal bullae; flattening of the diaphragm; and a long narrow heart. In cases of chronic bronchitis, chest radiographs revealed1 thickening of bronchial walls and crowding of the bronchi,2 occasional hyperinflation, and3 collapse and consolidation of the lung areas. We also provided radiologists with individuals’ symptoms (ie, no cough, expectoration, bloody sputum, shortness of breath, difficulty breathing, and how long the symptoms last) to obtain accurate diagnoses. The data were blinded to avoid potential bias (ie, no patient names, lifestyles, smoking status, and so forth, were provided to the radiologists). The aforementioned criteria for the entire study group were first examined by trained individual radiologists at local hospitals. All of the imaging films were then reviewed by a senior radiologist at Zhongshan Hospital.

Carbon monoxide (CO) concentration was measured18 by Micro CO (Micro CO MC02; Micro Medical Ltd) and blood samples were collected by vacuum tubes. The sera samples from six subjects were then pooled into one sample representing the group and molecular analysis was carried out. Samples were analyzed using a 507 human protein array (RayBio Label Based Human Antibody Array 507 [L-507]; RayBiotech, Inc) designed to simultaneously analyze 507 specific proteins. For the label-based array experiment, each sample (20 μL serum) was dialyzed, followed by a biotin-labeling step in which the primary amine was biotinylated.

The muddy water used in Chinese water pipes, taken from 10 town hospitals in the study areas, was tested by inductively coupled plasma atomic emission spectrometry to assess the mutagenicity of the major components. The water samples were also assayed for PM2.5, to which the smoke exposure was mimicked by the High Volume Air Sampler (G701; Thermo Andersen).2 The parameter setting based on the length of cigarette combustion (see e-Appendix 1). Zhongshan Hospital at Fudan University (Shanghai, China) was exclusively responsible for the data management and analysis and quality control of the study.

Statistical Analysis

All statistical analyses for baseline characteristics and outcomes were reported as means (SD) or as percentages within groups. Age, height, weight, mean smoking duration, number of cigarettes smoked per day, and postbronchodilator lung function including FEV1 % predicted, FVC % predicted, and FEV1/FVC were analyzed by a one-way analysis of variance test.16 Some nonparameters, including lung symptoms, hypertension, abnormal lung function, and COPD were diagnosed by spirometry; chronic bronchitis and emphysema were shown by chest radiograph and were analyzed by the Kruskal-Wallis test.16

The CWS, CWPS, CS, and CPS groups were treated as cases, and the NS and NPS groups were healthy control subjects.3 Calculations of ORs and 95% CI values for COPD in relation to potential risk factors were performed with binary logistic regression models14; these covariates included age, BMI, comorbidities (ie, hypertension), and unimproved stoves with chimneys in the house.

All hypothesis tests were two sided, and a P value of .05 was deemed significant. Statistical analyses were conducted with validated software packages (SAS 9.13 and SPSS16; SAS Institute Inc and IBM, respectively).

Individual Characteristics

A total of 1,238 individuals were included in the analysis (Fig 2); baseline characteristics are presented in Table 1. Smokers and passive smokers were similar in individual demographics including age, height, weight, and hypertension, whereas the NS group tended to consume less alcohol compared with the CWS and CS groups.

Figure Jump LinkFigure 2 –  Study profile: number of people who were enrolled and analyzed in the study.Grahic Jump Location
Pulmonary Impairment

The mean smoking duration (years) was similar in the CWS and CS groups (28 ± 11.2 vs 28.5 ± 13.5) (Table 1). The CWS group subconsciously increased the daily frequency of Chinese water-pipe smoking compared with the CS group (17.9 ± 8.9 vs 15.6 ± 8.5, P < .01). Pulmonary symptoms (ie, cough and sputum) were higher in the CWS and CS groups than in the NS group (P < .01), whereas coughing and wheezing were more common in the CWPS group than in the CPS and NPS groups.

With regard to lung function, the CWS group had the highest mean FVC % predicted (93.1%) but the lowest FEV1/FVC among all groups, indicating that the CWS group had impaired, instead of improved, lung function. At the same time, lung function in the CWPS group was significantly worse than in the CPS and NPS groups. The most compelling evidence was increased emphysema prevalence in the CWS and CWPS groups compared with the CS and CPS groups and the healthy control groups (NS and NPS) by chest radiograph (P < .01) (Table 1).

CO produced by smoking has been linked to COPD.18 The CO levels of the CWS group (28.4 ± 10.72 parts per million [ppm]; range, 6-71 ppm) were significantly higher than those of the CS (16.0 ± 7.44 ppm) and NS (3.8 ± 2.77 ppm) groups. Similar results were also seen in the CWPS group (15.4 ± 6.41 ppm vs 8.5 ± 4.91 ppm and 3.3 ± 2.78 ppm). Although Chinese water pipes do not use charcoal, in contrast to the Arabic water pipe, high CO levels have been attributed to the incomplete combustion of tobacco produced by the large volumes of smoke produced by the Chinese water pipe (Fig 3D).

Figure Jump LinkFigure 3 –  Prevalence of COPD. A, Prevalence of COPD and abnormal lung function. Abnormal lung function included airflow obstruction and restriction. According to the diagnostic criteria of GOLD (the Global Initiative for Chronic Obstructive Lung Disease), subjects with a postbronchodilator FEV1/FVC < 70% have COPD. Restrictive disorder was defined as FEV1/FVC ≥ 70% and FVC < 80% predicted values.14 B, Mean water change time in days of the Chinese water pipe. Dirty water levels increase as the water change time in days increases. C, Exposure to fine particulate matter (PM2.5) of smoke. The particulate matter < 2.5 μm in diameter, which is measured at the Department of Environmental Science and Engineering, Fudan University, by using a High Volume Air Sampler (G701; Thermo Andersen). D, Exhaled carbon monoxide (CO) levels. E, Trend of ChemR23 (E-1 in men; E-2 in women) and TIMP1 (E-3 in men; E-4 in women). The blood and exhaled CO measurements for smokers were not immediate, because many of the subjects were measured 12 h after smoking. Data are presented as mean ± SD. **P < .01, CWS vs NS; ##P < .01, CWS vs CS; ††P < .01, CWPS vs NPS; ‡‡P < .01, CWPS vs CPS. TIMP1 = tissue inhibitor of metalloproteinase-1. See Figure 2 legend for expansion of other abbreviations.Grahic Jump Location

COPD prevalence in our study, defined in accordance with the GOLD (Global Initiative for Chronic Obstructive Lung Disease) standard for spirometry,14,19,20 is shown in Fig 3A: 56.1% in the CWS group (OR, 10.61; 95% CI, 6.89-16.34) and 39.3% in the CWPS group (OR, 5.50; 95% Cl, 3.61-8.38), which were both significantly higher than in the CS (33.7%; OR, 3.18; 95% CI, 2.06-4.91) and CPS (27.5%; OR, 2.52; 95% CI, 1.63-3.91) groups (Table 2). Other COPD potential risk factors in the study included age (OR,1.08; 95% CI, 1.06-1.09) and unimproved stoves with chimneys in the house (OR,1.47; 95% CI, 1.05-2.06). However, hypertension and BMI were not related to COPD according to our logistic model. Interestingly, the prevalence of COPD in our study was 31.18% (35.37% in men and 27.17% in women), which is notably higher than the mean national COPD prevalence in China (8.2%; 12.4% in men and 5.1% in women).14

Table Graphic Jump Location
TABLE 2 ]  Risk Factors for COPD

The logistic equation is LogitP = −12.371 + 2.362CWS + 1.705CWPS + 1.157CS + 0.924CPS + 0.073age + 0.386 (unimproved stove with chimney). See Table 1 legend for expansion of abbreviations.

For the human protein array, after visualization by a laser scanner, expressions of ChemR23 in the CWS and CWPS groups were higher than in the two reference groups, whereas the tissue inhibitor of metalloproteinase-1 (TIMP-1) expression was the lowest (Fig 3E). Five individuals were tested for and confirmed as having lung cancer by CT scan and pathology evaluations: three in the CWS group (lung adenocarcinoma), one in the CWPS group (lung adenocarcinoma), and one in the CS group (lung squamous cell carcinoma).

Chinese Water Pipe and Fine Particulates

The Chinese water pipe (Fig 1A) is composed of a cigarette holder and a long stem (about 60-90 cm) with a large diameter (about 8-14 cm). The average capacity of the Chinese water pipe is > 4,000 mL, with 400 to 500 mL of water. Thus, to use the Chinese water pipe, smokers must have a large lung volume.

In evaluating the potential difference between Chinese water-pipe use and exposure from cigarettes, we found that the water from the Chinese water pipe was dirty; the mean time for changing the water was 3.2 days by self-report (Fig 3B). The total organic carbon content of the water was 47 to 100 times greater than that found in standard drinking water. The polycyclic aromatic hydrocarbon (PAH) indicator, Benzo[α]pyrene, was 58 times higher than that found in drinking water and heavy metals (Al, Cd, Cr, Fe, Mn, Pb, and Sb), which were generally increased, especially Cd, Cr, and Pb (see e-Appendix 1), whereas exposure to the accumulation of PAHs and heavy metals have been identified as animal carcinogens.2 Mean PM2.5 from the Chinese water-pipe smoke was twice as high as from cigarette smoke (232.2 mg vs 112.3 mg) per 10 cigarettes (Fig 3C), indicating that more PM2.5 of the smoke, along with the muddy vapor (ie, toxic constituents), were inhaled from the Chinese water pipe compared with the cigarette.

We provide robust results that large-volume Chinese water-pipe use and exposure are associated with the elevated prevalence of COPD, which has been identified by epidemiologic, physiologic, radiologic, and toxicologic findings for the first time. One thousand two hundred and thirty-eight individuals, 40 years of age or older, were enrolled from 10 towns. In our study, potential risk factors for COPD included the following: CWS (OR, 10.61; 95% Cl, 6.89-16.34), CWPS (OR, 5.50; 95% Cl, 3.61-8.38), CS (OR, 3.18; 95% Cl, 2.06-4.91), CPS (OR, 2.52; 95% Cl, 1.63-3.91), unimproved stoves with chimneys in the house (OR,1.47; 95% Cl, 1.05-2.06), and age (OR,1.08; 95% Cl, 1.06-1.09), whereas hypertension and BMI were not related to COPD according to our logistic model. Chinese water-pipe use and exposure were the most related to COPD in our study.

Previous studies showed that although the high incidence of COPD was associated with indoor coal smoke exposure in southwest China,2,3 the effect of smoking on COPD risk became considerably stronger after the NSIP.4 However, the time interval between the study and the NSIP (10 years’ follow-up from 1976) was too short for an objective observation of a changing COPD prevalence. Moreover, most studies’ outcomes were from the complaints of patients without COPD diagnosed by spirometry. Similarly, in a Japanese study, only 9.4% of cases with airflow limitation reported a previous diagnosis of COPD.21 This suggests that a diagnosis of COPD based on symptoms may not be adequate. The prevalence of COPD in our study was 31.18% (35.37% in men and 27.17% in women), which is notably higher than the mean national COPD prevalence of 8.2% in China,14 let alone 6.3% in the United States.22 Our study, like other studies,69 also demonstrates that the rate of COPD is still rising, even though over the past 2 decades efforts have been made to improve living standards and to provide better ventilation in dwellings in southwest China.

Passive smoking is a risk factor for many of the health problems associated with direct smoking.2325 However, little information is known about the water-pipe passive smoker. In our study, we found female passive smokers were more sensitive to the smoke produced by the smokers. The higher number of cigarettes per day the CWS group smoked (1 g of tobacco equals one cigarette) compared with the CS group, the more fine particulate smoke resulting from incomplete combustion of tobacco they would produce. Subsequently, the CWPS group would develop more clinical symptoms and pulmonary damage after exposure to a high concentration of fine particulates in the smoke compared with the CPS group (Table 2). These results are consistent with those of previous reports26 and have important public health implications.

The limitations of the water’s filtering capacity in the water pipe have been illustrated27; active and passive Chinese water-pipe smoking may cause exposure to smoke gases and nicotine in combination with the toxic vapor. Matter from the Chinese water pipe contained high levels of carcinogenic compounds, including high levels of CO,18 PM2.5, PAHs, and heavy metals, which may be deposited effectively in the lungs rather than staying in the airways after inhalation of large-lung-volume smoking. Indeed, these fine particulates are often enriched with toxic heavy metals compared with particulate matter (PM10), which is of particular concern for human health.28 Long-term exposure would inevitably cause damage in the alveolar epithelial cells27 and loss of more “reserved” lung to compensate, and would contribute to mutagenicity. In our study, three in the CWS group and one in the CWPS group were confirmed to have lung cancer by CT scan and pathology. We must pay greater attention to and must strengthen the monitoring of lung cancer.

It is well known that chronic inflammation caused by smoking can induce COPD and lung cancer.15 In the current study, we detected protein microarray by sera and found that the tendency of ChemR23 in the CWS and CWPS groups was higher than in the two reference groups, whereas TIMP-1 expression was the lowest (Fig 3E). ChemR23 signaling was identified in macrophages and plasmacytoid dendritic cells and could induce cell migration, which directs innate and adaptive immune cells to smoking-exposed lung inflammation; the decreased expression of TIMP-1 could lead to lung epithelial and extracellular matrix microenvironment destruction.29

Our study was limited by the lack of availability of medical facilities because of the poverty and backwardness of rural communities in the study areas. Low-dose CT scans have high detection rates of lung cancer compared with chest radiographs.30 Our original plan was to screen for lung cancer by low-dose CT scans. However, there was only one CT scanner available in the Fuyuan area and the inconvenience of local traffic made it difficult to use. Furthermore, although we measured BP and heart rate, there were not enough data to diagnose ischemic heart disease.31 Finally, study enrollment was small, so we reported only five individuals with lung cancer. Future research needs to focus on recruiting more individuals to screen for biomarkers to confirm the results.

In conclusion, the Chinese water pipe has mistakenly been deemed as less harmful. Our study has provided evidence confirming this misconception. Exposure to active and passive Chinese water-pipe smoke may be a significant risk factor for developing COPD. The damage from Chinese water-pipe use and exposure is worse than that from cigarettes. Our results highlight that smoking cessation in Chinese water-pipe users is as important as the smoking cessation of other tobacco products in the preventive intervention of COPD. In addition, Chinese water-pipe use and exposure are associated with COPD; the PM2.5 from the Chinese water-pipe smoke was twice as high as that from cigarette smoke. Our results also predict that the prevalence of COPD will be increased by long-term exposure to high concentrations of PM2.5, which will bring a huge economic and social burden to the globe and calls for more research to be directed toward preventive measures and efforts.

Author contributions: C. B. takes responsibility for the content of the manuscript, including data and analysis. J. S. contributed to the conduct of the study; J. S., P. Y., Yuqi Wang, X. Q., J. F., Yi Wang, G. G., G. L., K. M., B. L., C. L., X. Wang, Y. S., and C. B. contributed to the completion of the work and development of the manuscript; J. S. contributed to the drafting of the manuscript; P. Y. contributed to the design of the work and revision of the manuscript; Yuqi Wang, X. Q., J. F., X. Wang, and Y. S. contributed to data collection; Yi Wang contributed to statistical analysis; G. G., G. L., K. M., B. L. and C. L. contributed to the epidemiologic work; and C. B. contributed to the design and supervision of the whole study.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Role of sponsors: The sponsors contributed to the study design, data analysis, and preparation of the manuscript.

Other contributions: The authors thank Susan Ernst, MA, Mayo Clinic, for her technical support in the English editing of this manuscript.

Additional information: The e-Appendix can be found in the Supplemental Materials section of the online article.

CO

carbon monoxide

CPS

cigarette passive smoker

CS

cigarette smoker

CWPS

Chinese water-pipe passive smoker

CWS

Chinese water-pipe smoker

NPS

never passive smoker

NS

healthy control subjects never smoker

NSIP

National Stove Improvement Program

PAH

polycyclic aromatic hydrocarbon

PM2.5

fine particulate 2.5

ppm

parts per million

TIMP-1

tissue inhibitor of metalloproteinase-1

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Fukuchi Y, Nishimura M, Ichinose M, et al. COPD in Japan: the Nippon COPD epidemiology study. Respirology. 2004;9(4):458-465. [CrossRef] [PubMed]
 
COPD prevalence rates reported by all 50 states. Medscape website. http://www.medscape.com/viewarticle/775098. Accessed January 3, 2013.
 
Yin P, Jiang CQ, Cheng KK, et al. Passive smoking exposure and risk of COPD among adults in China: the Guangzhou Biobank Cohort Study. Lancet. 2007;370(9589):751-757. [CrossRef] [PubMed]
 
She J, Yang P, Hong QY, Bai CX. Lung cancer in China: challenges and interventions. Chest. 2013;143(4):1117-1126. [CrossRef] [PubMed]
 
Novak K. Passive smoking: out from the haze. Nature. 2007;447(7148):1049-1051. [CrossRef] [PubMed]
 
Pope CA III, Burnett RT, Thun MJ, et al. Lung cancer, cardiopulmonary mortality, and long-term exposure to fine particulate air pollution. JAMA. 2002;287(9):1132-1141. [CrossRef] [PubMed]
 
World Health Organization (WHO) Regional Office for the Eastern Mediterranean. Tobacco use in Shisha: studies on waterpipe smoking in Egypt. EMRO nonserial publication. WHO website. http://apps.who.int/bookorders/anglais/detart1.jsp?codlan=1&codcol=46&codcch=40. Accessed January 3, 2013.
 
Li X, Zhang Y, Tan M, et al. Atmospheric lead pollution in fine particulate matter in Shanghai, China. J Environ Sci (China). 2009;21(8):1118-1124. [CrossRef] [PubMed]
 
Demoor T, Bracke KR, Dupont LL, et al. The role of ChemR23 in the induction and resolution of cigarette smoke-induced inflammation. J Immunol. 2011;186(9):5457-5467. [CrossRef] [PubMed]
 
National Lung Screening Trial Research Team;Aberle DR, Adams AM, Berg CD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):395-409. [CrossRef] [PubMed]
 
He Y, Lam TH, Jiang B, et al. Passive smoking and risk of peripheral arterial disease and ischemic stroke in Chinese women who never smoked. Circulation. 2008;118(15):1535-1540. [CrossRef] [PubMed]
 

Figures

Figure Jump LinkFigure 1 –  A, Chinese water pipe (A-1), inside of Chinese water pipe (A-2), Chinese water-pipe holder (A-3), and Arabic water pipe (A-4). B, The National Stove Improvement Program to improve indoor air quality in China. Improved stove (B-1) with chimney (B-2).Grahic Jump Location
Figure Jump LinkFigure 2 –  Study profile: number of people who were enrolled and analyzed in the study.Grahic Jump Location
Figure Jump LinkFigure 3 –  Prevalence of COPD. A, Prevalence of COPD and abnormal lung function. Abnormal lung function included airflow obstruction and restriction. According to the diagnostic criteria of GOLD (the Global Initiative for Chronic Obstructive Lung Disease), subjects with a postbronchodilator FEV1/FVC < 70% have COPD. Restrictive disorder was defined as FEV1/FVC ≥ 70% and FVC < 80% predicted values.14 B, Mean water change time in days of the Chinese water pipe. Dirty water levels increase as the water change time in days increases. C, Exposure to fine particulate matter (PM2.5) of smoke. The particulate matter < 2.5 μm in diameter, which is measured at the Department of Environmental Science and Engineering, Fudan University, by using a High Volume Air Sampler (G701; Thermo Andersen). D, Exhaled carbon monoxide (CO) levels. E, Trend of ChemR23 (E-1 in men; E-2 in women) and TIMP1 (E-3 in men; E-4 in women). The blood and exhaled CO measurements for smokers were not immediate, because many of the subjects were measured 12 h after smoking. Data are presented as mean ± SD. **P < .01, CWS vs NS; ##P < .01, CWS vs CS; ††P < .01, CWPS vs NPS; ‡‡P < .01, CWPS vs CPS. TIMP1 = tissue inhibitor of metalloproteinase-1. See Figure 2 legend for expansion of other abbreviations.Grahic Jump Location

Tables

Table Graphic Jump Location
TABLE 1 ]  Characteristics of the Study Individuals

Data are shown as mean (SD) or No. (%) unless otherwise indicated. In the Fuyuan area, most of the people who smoke the Chinese water pipe are men; female water-pipe smokers are rare. Alcohol consumption was defined as drinking alcohol on at least 12 occasions during the past 12 mo. Hypertension was defined as a mean systolic BP of 140 mm Hg or higher, a diastolic BP of 90 mm Hg or higher, or the use of an antihypertensive medication. COPD was diagnosed by lung function; chronic bronchitis and emphysema were diagnosed by chest radiograph. CS = cigarette smoker; CPS = cigarette passive smoker; CWPS = Chinese water-pipe passive smoker; CWS = Chinese water-pipe smoker; NPS = never passive smoker; NS = never smoker.

a 

P < .01 CWS vs CS.

b 

P < .01 CWS vs NS.

c 

P < .01 CWPS vs NPS.

d 

P < .01 CWPS vs CPS.

e 

P < .05 CWPS vs CPS.

f 

P < .05 CWS vs CS.

g 

P < .05 CWS vs NS.

Table Graphic Jump Location
TABLE 2 ]  Risk Factors for COPD

The logistic equation is LogitP = −12.371 + 2.362CWS + 1.705CWPS + 1.157CS + 0.924CPS + 0.073age + 0.386 (unimproved stove with chimney). See Table 1 legend for expansion of abbreviations.

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Global initiative for chronic obstructive lung disease. GOLD website. http://www.goldcopd.org/. Accessed January 3, 2013.
 
Fukuchi Y, Nishimura M, Ichinose M, et al. COPD in Japan: the Nippon COPD epidemiology study. Respirology. 2004;9(4):458-465. [CrossRef] [PubMed]
 
COPD prevalence rates reported by all 50 states. Medscape website. http://www.medscape.com/viewarticle/775098. Accessed January 3, 2013.
 
Yin P, Jiang CQ, Cheng KK, et al. Passive smoking exposure and risk of COPD among adults in China: the Guangzhou Biobank Cohort Study. Lancet. 2007;370(9589):751-757. [CrossRef] [PubMed]
 
She J, Yang P, Hong QY, Bai CX. Lung cancer in China: challenges and interventions. Chest. 2013;143(4):1117-1126. [CrossRef] [PubMed]
 
Novak K. Passive smoking: out from the haze. Nature. 2007;447(7148):1049-1051. [CrossRef] [PubMed]
 
Pope CA III, Burnett RT, Thun MJ, et al. Lung cancer, cardiopulmonary mortality, and long-term exposure to fine particulate air pollution. JAMA. 2002;287(9):1132-1141. [CrossRef] [PubMed]
 
World Health Organization (WHO) Regional Office for the Eastern Mediterranean. Tobacco use in Shisha: studies on waterpipe smoking in Egypt. EMRO nonserial publication. WHO website. http://apps.who.int/bookorders/anglais/detart1.jsp?codlan=1&codcol=46&codcch=40. Accessed January 3, 2013.
 
Li X, Zhang Y, Tan M, et al. Atmospheric lead pollution in fine particulate matter in Shanghai, China. J Environ Sci (China). 2009;21(8):1118-1124. [CrossRef] [PubMed]
 
Demoor T, Bracke KR, Dupont LL, et al. The role of ChemR23 in the induction and resolution of cigarette smoke-induced inflammation. J Immunol. 2011;186(9):5457-5467. [CrossRef] [PubMed]
 
National Lung Screening Trial Research Team;Aberle DR, Adams AM, Berg CD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):395-409. [CrossRef] [PubMed]
 
He Y, Lam TH, Jiang B, et al. Passive smoking and risk of peripheral arterial disease and ischemic stroke in Chinese women who never smoked. Circulation. 2008;118(15):1535-1540. [CrossRef] [PubMed]
 
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