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The effect of habitual waterpipe tobacco smoking on pulmonary function and exercise capacity in young healthy males: A pilot study
Respiratory Medicine 122 (2017) 71e75
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The effect of habitual waterpipe tobacco smoking on pulmonary function and exercise capacity in young healthy males: A pilot study F.I. Hawari a, b, *, N.A. Obeidat b, I.M. Ghonimat c, H.S. Ayub d, S.S. Dawahreh c a
Section of Pulmonary and Critical Care, Department of Medicine, King Hussein Cancer Center, Amman, Jordan Cancer Control Office, King Hussein Cancer Center, Amman, Jordan c Respiratory Therapy Services, King Hussein Cancer Center, Amman, Jordan d Independent Tobacco Control & Tobacco Dependence Treatment Consultant, Private Practice, Jordan b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 February 2016 Received in revised form 21 November 2016 Accepted 30 November 2016 Available online 30 November 2016
Background: Evidence regarding the health effects of habitual waterpipe smoking is limited, particularly in young smokers. Respiratory health and cardiopulmonary exercise tests were compared in young male habitual waterpipe smokers (WPS) versus non-smokers. Methods: 69 WPS (3 times/week for three years) and 69 non-smokers were studied. Respiratory health was assessed through the American Thoracic Society and the Division of Lung Diseases (ATS-DLD-78) adult questionnaire. Pulmonary function and cardiopulmonary exercise tests were performed. Selfreported respiratory symptoms, forced expiratory volume in first second (FEV1), forced vital capacity (FVC), FEV1/FVC ratio, forced expiratory flow between 25 and 75% of FVC (FEF25e75%), peak expiratory flow (PEF), exercise time, peak end-tidal CO2 tension (PetCO2), subject-reported leg fatigue and dyspnea; peak O2 uptake (VO2 max), and end-expiratory lung volume (EELV) change from baseline (at peak exercise) were measured. Results: WPS were more likely than non-smokers to report respiratory symptoms. WPS also demonstrated: shorter exercise time; lower peak VO2; higher perceived dyspnea at mid-exercise; lower values of the following: FEV1, FVC, PEF, and EELV change. Conclusion: Habitual waterpipe tobacco smoking in young seemingly healthy individuals is associated with a greater burden of respiratory symptoms and impaired exercise capacity. © 2016 Elsevier Ltd. All rights reserved.
Keywords: Waterpipe Exercise testing Lung function Respiratory symptoms Youth
1. Introduction Various toxic chemicals have been found in waterpipe smoke [1], and waterpipe smoking has been associated with several detrimental health outcomes such as cardiovascular and respiratory diseases, as well as cancer [2e6]. Despite its toxic content [1], waterpipe use has been growing globally, and is particularly popular among youth, the main driving force behind a new worldwide epidemic [7,8]. Waterpipe use also has been shown to predispose its users to cigarette smoking initiation [6,9]. However, knowledge with regards to the health effects of waterpipe on such a young population remains limited [10]. Beyond measuring heart rate and blood pressure, few studies
* Corresponding author. Cancer Control Office, King Hussein Cancer Center, Queen Rania Al Abdullah Street, P.O. Box 1269, Al-Jubeiha, Amman 11941, Jordan. E-mail address: [email protected] (F.I. Hawari). http://dx.doi.org/10.1016/j.rmed.2016.11.024 0954-6111/© 2016 Elsevier Ltd. All rights reserved.
[11e13] have attempted to characterize the cardiopulmonary effects of acute waterpipe smoke exposure in young users, and none have evaluated the early onset effects (if any) of habitual and extended waterpipe smoking. This is an important and timely subject to begin examining. The waterpipe is becoming increasingly popular, even among young groups that were traditionally deemed low-risk for tobacco use (such as athletes) [14]. It is therefore not implausible, as some data are already suggesting [15], that waterpipe use may become more habitual among its users. Providing evidence that can preempt or deter this trend is judicious. In an exploratory pilot study, we sought to assess the range of effects that habitual waterpipe smoking may exert on the cardiopulmonary health of young smokers. Such research is in line with the call for more efforts to elucidate the harmful nature of waterpipe smoking [10]. Specifically, we compared habitual waterpipe smokers (WPS) to non-users of tobacco (non-smokers) in three areas: burden of respiratory symptoms, lung function, and
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cardiopulmonary exercise capacity. We anticipated that WPS would fare worse than non-smokers across all these measures. 2. Methods There is scarce clinical data on waterpipe health effects specifically in habitual young users. Our clinical study was designed as a pilot to prospectively examine the effect of waterpipe on young, habitual users, and generate hypotheses with regards to the potential clinical effect size as a result of habitual waterpipe use (thereby informing future waterpipe clinical research studies with regards to which specific endpoints should be incorporated). The study was conducted in accordance with the amended Declaration of Helsinki. The institutional review board at King Hussein Cancer Center (KHCC) approved the protocol and written informed consent was obtained from all participants. Data collection spanned approximately two years (from August 2013 through to June 2015). 2.1. Participants Participants were recruited through announcements made within several universities in Jordan. Initial contact and screening were conducted via phone. All males who reported being healthy and between the ages of 18 and 26, and who reported either never using tobacco or being WPS who smoked three or more times a week for the past three years atleast (with no other form of tobacco used) were invited to join the study. Those who agreed to participate were invited to a single testing session at KHCC's Cardiopulmonary Exercise Testing (CPET) laboratory. A session lasted approximately two and a half hours. Participants were asked to avoid strenuous exercises or activities, and refrain from smoking for 48 hours prior to their visit. Participants were confirmed healthy by a medical examination. The following exclusion criteria were applied: body-mass index (BMI) of 40.0 kg/m2 or more; active chronic medical conditions; use of chronic prescription medications; illicit drug use; abnormal heart rhythm or abnormal resting heart rate; (>100 or < 50 beats per minute); high blood pressure (>140/90 mmHg); or low oxygen (O2) saturation (<95%). 2.2. Procedures and data collection Body plethysmograph spirometry (using the Vmax series 777360B © 2005 VIASYS Healthcare Inc.) and cardiopulmonary testing using a bicycle ergometer (Ergoselect 100/200, Cardiosoft v6.2) were conducted. Reference spirometric and cardiopulmonary exercise values were based on widely used sources [16e18]. All procedures were conducted according to the American Thoracic Society/European Respiratory Society guidelines for spirometry and cardiopulmonary measures [19,20]. The following variables were measured: 1. General health information (including weight, height, medical history and exercise habits) and socio-demographic factors were recorded. 2. To evaluate general respiratory health, the American Thoracic Society and the Division of Lung Diseases (ATS-DLD-78) adult questionnaire was administered by staff [21]. The following measured variables were specifically of relevance: bringing up phlegm; shortness of breath upon exertion; suffering from cough; having a chest illness in the past three years that kept a participant off work; coughing and phlegm lasting three or more weeks; colds that usually went to the chest; having a wheezy chest whilst having a cold; having a wheezy chest most
of the time; having a wheezy chest without a cold; and having a wheezing attack that left a participant breathless. 3. To evaluate lung function, spirometry was used to measure: forced expiratory volume at the end of first second (FEV1); forced vital capacity (FVC); forced expiratory flow during mid (25e75%) portion of FVC (FEF25e75%); FEV1/FVC; peak expiratory flow (PEF); and total lung capacity (TLC). 4. Cardiopulmonary exercise testing was conducted using a standardized symptom-limited CPET protocol (two-minute baseline with no resistance, two-minute warm-up at a 20-Watt resistance, and a 30-Watt increase every two-minutes thereafter until exhaustion). Variables measured included: peak systolic blood pressure (SBP); peak diastolic blood pressure (DBP); peak heart rate (HR); peak heart rate reserve (HRR); peak breathing reserve (BR); exercise time in minutes; oxygen consumption adjusted for body weight (VO2); linear relation of heart rate to oxygen consumption (HR/VO2); end-tidal oxygen and carbon dioxide tension (peak PetO2 and peak PetCO2, respectively); ventilatory equivalent ratio for oxygen and carbon dioxide (VE/ VO2 and VE/VCO2, respectively); oxygen pulse (O2 pulse); shortness of breath (dyspnea) at mid (taken at a fixed time point for all subjects, at six minutes) and peak exercise (using 0e10 Borg scale), and leg fatigue at mid (at six minutes) and peak exercise (using 6e20 Borg scale) [22,23]; change from baseline at peak exercise in the end-expiratory lung volume (EELV, using the inspiratory capacity maneuver as described by Yan et al.) [24]; O2 saturation; minute ventilation (VE); and anaerobic threshold as percentage of peak VO2. Investigators and technicians within the study were not blinded to group assignment. 2.3. Analysis Basic univariate statistics were used to describe respiratory health and cardiopulmonary measures at peak exercise. T-tests were used to compare non-smokers and WPS across all measures, and p-values were generated (a cut-off of 0.05 was used). Exercise duration (as a proxy for exercise performance) was a main outcome of interest. Multivariable regression analysis was performed to evaluate the effect of being in the WPS group on exercise duration, while adjusting for baseline differences between subjects that may have influenced exercise duration (e.g. age, general respiratory healthy, being physically active, and BMI). With regards to general respiratory health, reporting of dyspnea upon exertion was specifically used as a proxy measure. 3. Results In total, 138 subjects (69 WPS and 69 non-smokers) were recruited for the study. Table 1 presents the baseline characteristics of the sample of male participants. WPS had been smoking the waterpipe habitually for 4.9 years. Notably, WPS (mean age 22.1) had a higher BMI than non-smokers (mean age 21.4). With regards to respiratory symptoms (Fig. 1), a significantly greater proportion of WPS (72.5%) than non-smokers (21.7%) reported any respiratory symptoms (e.g. bringing up phlegm, having shortness of breath upon exertion, cough, chest illness in the past three years that kept a participant off work, and coughing with phlegm that lasted at least three weeks). CPET and PFT results also revealed differences between nonsmokers and WPS (Table 2). WPS had significantly lower FEV1, FVC, PEF and TLC. At peak exercise, WPS had lower VO2 ml/kg and HR; lower degree of change in EELV; and higher HRR, Pet CO2, and VE/VCO2. WPS also reported higher shortness of breath and leg
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Table 1 Baseline characteristics of sample of young male waterpipe smokers and non-smokers.
Mean age (range) Height in cm Weight in Kg BMI (kg/m2) Waterpipe heads per week Years smoking waterpipe (range) CO (ppm)
Waterpipe smokers (n ¼ 69)
Non-smokers (n ¼ 69)
p-value
22.1 (19.0e26.1) 176.6 (164e192) 79.8 (59e122) 25.6 (17.8e34.2) 8.9 4.9 (3e8) 4.2 (1e13)
21.4 (18.2e26.4) 176.1 (164e189) 73.5 (47e104) 23.7 (16.5e32.2) e e 2.2 (0e9)
0.0016 NS 0.0015 0.0012 e e 0.000
100.0% 90.0% 80.0%
72.5%
70.0% 60.0% 50.0%
36.8%
40.0%
33.8% 27.9%
30.0% 21.7%
25.0%
20.0% 10.1% 11.6% 10.0% 1.5%
1.5%
2.9%
Bring up phlegm*
Shortness of breath upon exertion*
Cough*
8.8% 4.4%
7.4% 4.5%
5.8%
0.0%
0.0% Any of symptoms*
10.3% 5.8%
2.9%
1.5% 2.9%
Wheezing Wheezy Wheezy Chest illness Coughing + Cold usually Wheezy attack in past 3 phlegm go to chest chest with chest most of chest without leaving a cold time years kept off lasting 3 having a cold breathless work* weeks* Smokers
Nonsmokers
* Significant Chi-square test for difference in proportions between waterpipe smokers and non-smokers (p<0.05) Fig. 1. Reported respiratory symptoms in the past year in young male waterpipe smokers and non-smokers.
fatigue at mid exercise. Exercise time was significantly shorter for WPS than nonsmokers in both bivariate and multivariate analyses (Table 3). 4. Discussion Waterpipe smoking has increased worldwide particularly among youth, and there have been calls to study its potential to cause lung disease in order to provide the necessary evidence to curb its spread [10,25]. Our pilot study is unique in that it evaluated in young men the effect of habitual long-term waterpipe use on pulmonary symptoms, pulmonary function, and cardiopulmonary exercise capacity. To our knowledge, this is the first study that explores the adverse effects of waterpipe smoking in this collective manner, and within a sample of young habitual waterpipe users. Our data suggest that, in young males, habitual waterpipe use for an average of almost five years, a time relatively short for a history of smoking, can already be associated with various symptoms such as greater burden of respiratory symptoms, PFT abnormalities, and reduced exercise capacity. In general, the occurrence of pulmonary symptoms is a sign of respiratory system distress. In our findings, substantially more WPS reported pulmonary symptoms over the past year (especially shortness of breath upon exertion, sputum production, and
frequent coughing) than non-smokers. In addition, several spirometry parameters (FEV1, FVC, FEF25e75%, and PEF) were trending lower among WPS. These parameters did fall within normal ranges, but the lower trend is nevertheless consistent with other findings in our study, and may indicate early smoking-related pulmonary impairment. For example, although the significance of low PEF in the young has not been studied, PEF has been used in the evaluation of the effect of air pollution in normal and asthmatics [26]. Furthermore, low PEF has been shown to be significantly related to smoking [27], and has been associated with chronic respiratory symptoms including cough and dyspnea on exertion [28], both shown to be more common among WPS in our study. Our data also show that waterpipe smoking was associated with reduced exercise capacity. WPS exercised for a significantly shorter time and generated lower VO2 max values than non-smokers. WPS also reported higher perception of dyspnea and leg fatigue at midexercise. Furthermore, WPS produced significantly higher VE/VCO2 readings, indicating lower breathing efficiency. Many factors are known to affect VE/VCO2 during exercise, such as airway obstruction, hyperinflation, increased dead space ventilation, abnormal resting hemodynamics, and muscle endurance [29e31]. Although our study was not designed to characterize the exact reasons why WPS had a higher VE/VCO2 than non-smokers, it is plausible that waterpipe smoking may have influenced breathing efficiency
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Table 2 Cardiopulmonary results comparing young male waterpipe smokers and non-smokers.
Pulmonary parameters (standard deviation) FEV1, L - % predicted value FVC, L - % predicted value FEV1/FVC - % predicted value FEF25-75%, L - % predicted value PEF, L - % predicted value TLC, L - % predicted value CPET parameters (standard deviation) VO2, ml/min/kg - % predicted value HR/VO2, beats/ml/Kg VO2/Work (ml/min/watt) Work (watt), % predicted Anaerobic threshold as percentage of peak VO2max Exercise time, minutes O2 pulse, ml/beat, % predicted value Systolic blood pressure, mmHg Diastolic blood pressure, mmHg Heart rate, beats/min - % predicted value Heart rate reserve, beats/min Breathing reserve Borg scale e mid Borg scale e peak Leg fatigue e mid Leg fatigue e peak EELV at peak, change from baseline Pet CO2, mmHg Pet O2, mmHg VE - % predicted value VE/VO2 VE/VCO2
Waterpipe smokers (n ¼ 69)
Non-smokers (n ¼ 69)
p-value
98.9 (11.8) 94.1 (11.4) 106.3 (7.8) 101.9 (21.3) 86.9 (16.0) 99.6 (14.8)
102.4 (13.3) 98.0 (14.9) 107.1 (6.4) 105.7 (23.9) 92.2 (18.0) 109.1 (21.9)
0.05 0.04 ns ns 0.03 0.002
57.5 (11.2) 2.8 (0.73) 12.9 (3.2) 60% (8.7) 33.6 (10.4) 8.5 (1.0) 81.3 (16.0) 144.1 (17.1) 79.4 (14.82) 87.0 (9.0) 25.3 (15.8) 51.7 (9.7) 2.9 (1.4) 5.4 (1.6) 11.7 (2.2) 15.3 (2.6) 0.25 (0.47) 38.0 (4.8) 94.2 (4.5) 53.7 (10.6) 22.3 (4.8) 25.1 (2.6)
61.2 (10.11) 3.0 (0.99) 12.3 (3.2) 63.6% (12.0) 32.8 (8.6) 8.9 (1.2) 77.7 (18.3) 142.3 (20.3) 79.3 (12.7) 93.1 (6.4) 14.6 (10.6) 49.4 (12.5) 1.8 (0.98) 3.9 (1.4) 10.75 (1.9) 15.0 (1.8) 0.41 (0.32) 36.4 (15.4) 95.3 (5.3) 56.1 (13.2) 21.6 (3.6) 23.8 (2.7)
0.02 ns ns 0.024 ns 0.03 ns ns ns 0.000 0.000 ns 0.000 0.000 0.003 ns 0.01 0.04 ns ns ns 0.0018
Table 3 Multivariate linear regression of factors influencing duration of exercise in sample of young males (waterpipe smokers and non-smokers).
Age BMI Regular exercise Waterpipe use Report shortness of breath upon exertion
through effecting one of these factors. However, WPS had comparable breathing reserve, ETO2, VE/VO2, and oxygen saturation to non-smokers. Thus, abnormal ventilatory and gas exchange responses were less likely a cause for their reduced exercise capacity. The effect of waterpipe smoking on muscle endurance (and therefore breathing efficiency) may be a particular factor of interest to focus on in future research. Smoking is known to cause fatigue of the skeletal muscles, and other studies have concluded that abnormalities in skeletal muscles endurance can result in abnormalities in breathing efficiency [29,32,33]. Furthermore, reduced exercise capacity due to muscle fatigue has been associated with hyperinflation at peak exercise [34]. In our study, signs of hyperinflation were observed in WPS, who demonstrated significantly lower values of EELV change when compared to non-smokers. Although other causes such as airflow limitation and airway obstruction have been associated with dynamic hyperinflation [35,36], this is unlikely, given that our subjects' spirometry values were well within normal limits. Rather, reduced exercise time, lower EELV change, higher reported leg fatigue, and higher VE/ VCO2, collectively point to muscle fatigue as a plausible reason for exercise limitation among WPS. While deconditioning may also be at play [37], both smokers and non-smokers reported similar exercise patterns. It was notable that WPS in our pilot were on average 6 Kg
Coefficient (standard error)
p-value
0.06 (0.06) 0.11 (0.02) 0.28 (0.19) 0.46 (0.21) 0.19 (0.27)
0.35 0.000 0.15 0.027 0.48
heavier, although we did not find a significant difference in the history of daily exercise pattern between WPS and non-smokers. While obesity may impact lung function, our subjects did not meet the definition of obesity (their average BMI was at the lower range of being overweight rather than obese). Nevertheless, considering the way in which the waterpipe is smoked (sitting down for extended amounts of times, often with easy access to food and beverages), the difference in BMI is conceivable and consistent with other findings [38]. We also controlled for BMI in our multivariable analysis, which found that waterpipe smoking was significantly and independently associated with a shorter duration of exercise. Waterpipe smoking in young healthy adults appeared to have similar effects on heart rate (during exercise) as those of cigarette smoking [39]. Our smokers failed to reach their maximum predicted heart rate and had at least 40% more heart reserve than nonsmokers. Whether this was due to reduced exercise capacity and/or down-regulation of beta-adrenergic receptors, as has been suggested in studies examining the effect of cigarette smoking [40,41], is worth further studying, particularly given that our subjects were young, had a relatively short history of tobacco exposure, and comparable [to non-smokers] O2 pulse, blood pressure, and electrocardiogram (at rest and at peak exercise). To our knowledge, this pilot study is the first to evaluate the
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cardiopulmonary effects of waterpipe use among a young group of habitual WPS. However, some limitations exist. Given the difficulty of accessing subjects fitting our inclusion criteria (habitual, longterm waterpipe use), participants were purposively sampled. Furthermore, due to its pilot nature and small size, our study findings are preliminary, but nevertheless suggestive of significant impact. They should thus be useful in directing researchers seeking to elucidate the pathophysiology of waterpipe damage with regards to which specific elements of cardiopulmonary function to focus on. 5. Conclusion Habitual waterpipe smoking in young seemingly healthy individuals is associated with a higher burden of clinical respiratory symptoms and impaired cardiopulmonary exercise capacity. Conflict of interest The authors have no conflict of interest. References [1] A. Shihadeh, J. Schubert, J. Klaiany, M. El Sabban, A. Luch, N.A. Saliba, Toxicant content, physical properties and biological activity of waterpipe tobacco smoke and its tobacco-free alternatives, Tob. Control 24 (Suppl 1) (2015) i22ei30. [2] E.A. Akl, S. Gaddam, S.K. Gunukula, R. Honeine, P.A. Jaoude, J. Irani, The effects of waterpipe tobacco smoking on health outcomes: a systematic review, Int. J. Epidemiol. 39 (3) (2010) 834e857. [3] D. Raad, S. Gaddam, H.J. Schunemann, J. Irani, P. Abou Jaoude, R. Honeine, E.A. Akl, Effects of water-pipe smoking on lung function: a systematic review and meta-analysis, Chest 139 (4) (2011) 764e774. [4] S.A. Meo, K.A. AlShehri, B.B. AlHarbi, O.R. Barayyan, A.S. Bawazir, O.A. Alanazi, A.R. Al-Zuhair, Effect of shisha (waterpipe) smoking on lung functions and fractional exhaled nitric oxide (FeNO) among Saudi young adult shisha smokers, Int. J. Environ. Res. Public Health 11 (9) (2014) 9638e9648. [5] Z.M. El-Zaatari, H.A. Chami, G.S. Zaatari, Health effects associated with waterpipe smoking, Tob. Control 24 (Suppl 1) (2015) i31ei43. [6] R. Jaber, P. Madhivanan, E. Veledar, Y. Khader, F. Mzayek, W. Maziak, Waterpipe a gateway to cigarette smoking initiation among adolescents in Irbid, Jordan: a longitudinal study, Int. J. Tuberc. Lung Dis. 19 (4) (2015) 481e487. [7] E.A. Akl, K.D. Ward, D. Bteddini, R. Khaliel, A.C. Alexander, T. Lotfi, H. Alaouie, R.A. Afifi, The allure of the waterpipe: a narrative review of factors affecting the epidemic rise in waterpipe smoking among young persons globally, Tob. Control 24 (Suppl 1) (2015) i13ei21. [8] W. Maziak, Z.B. Taleb, R. Bahelah, F. Islam, R. Jaber, R. Auf, R.G. Salloum, The global epidemiology of waterpipe smoking, Tob. Control 24 (Suppl 1) (2015) i3ei12. [9] P.D. Jensen, R. Cortes, G. Engholm, S. Kremers, M. Gislum, Waterpipe use predicts progression to regular cigarette smoking among Danish youth, Subst. Use Misuse 45 (7e8) (2010) 1245e1261. [10] World Health Organization Study Group on Tobacco Product Regulation (TobReg), Advisory Note: Waterpipe Tobacco Smoking: Health Effects, Research Needs and Recommended Actions for Regulators, second ed., 2015. Retrieved from http://apps.who.int/iris/bitstream/10665/161991/1/ 9789241508469_eng.pdf?ua¼1,%202015. [11] M.A. Alomari, O.F. Khabour, K.H. Alzoubi, D.M. Shqair, T. Eissenberg, Central and peripheral cardiovascular changes immediately after waterpipe smoking, Inhal. Toxicol. 26 (10) (2014) 579e587. [12] L. Bentur, E. Hellou, A. Goldbart, G. Pillar, E. Monovich, M. Salameh, I. Scherb, Y. Bentur, Laboratory and clinical acute effects of active and passive indoor group water-pipe (narghile) smoking, Chest 145 (4) (2014) 803e809. [13] F.I. Hawari, N.A. Obeidat, H. Ayub, I. Ghonimat, T. Eissenberg, S. Dawahrah, H. Beano, The acute effects of waterpipe smoking on lung function and exercise capacity in a pilot study of healthy participants, Inhal. Toxicol. 25 (9) (2013) 492e497. [14] B.A. Primack, C.I. Fertman, K.R. Rice, A.M. Adachi-Mejia, M.J. Fine, Waterpipe and cigarette smoking among college athletes in the United States, J. Adolesc. Health 46 (1) (2010) 45e51. [15] B.A. Primack, P. Freedman-Doan, J.E. Sidani, D. Rosen, A. Shensa, A.E. James, J. Wallace, Sustained waterpipe tobacco smoking and trends over time, Am. J. Prev. Med. 49 (6) (2015) 859e867. [16] J.F. Morris, A. Koski, L.C. Johnson, Spirometric standards for healthy nonsmoking adults, Am. Rev. Respir. Dis. 103 (1) (1971) 57e67. [17] G. Polgar, V. Promadhat, Pulmonary Function Testing in Children: Techniques
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Respiratory Medicine journal homepage: www.elsevier.com/locate/rmed
The effect of habitual waterpipe tobacco smoking on pulmonary function and exercise capacity in young healthy males: A pilot study F.I. Hawari a, b, *, N.A. Obeidat b, I.M. Ghonimat c, H.S. Ayub d, S.S. Dawahreh c a
Section of Pulmonary and Critical Care, Department of Medicine, King Hussein Cancer Center, Amman, Jordan Cancer Control Office, King Hussein Cancer Center, Amman, Jordan c Respiratory Therapy Services, King Hussein Cancer Center, Amman, Jordan d Independent Tobacco Control & Tobacco Dependence Treatment Consultant, Private Practice, Jordan b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 February 2016 Received in revised form 21 November 2016 Accepted 30 November 2016 Available online 30 November 2016
Background: Evidence regarding the health effects of habitual waterpipe smoking is limited, particularly in young smokers. Respiratory health and cardiopulmonary exercise tests were compared in young male habitual waterpipe smokers (WPS) versus non-smokers. Methods: 69 WPS (3 times/week for three years) and 69 non-smokers were studied. Respiratory health was assessed through the American Thoracic Society and the Division of Lung Diseases (ATS-DLD-78) adult questionnaire. Pulmonary function and cardiopulmonary exercise tests were performed. Selfreported respiratory symptoms, forced expiratory volume in first second (FEV1), forced vital capacity (FVC), FEV1/FVC ratio, forced expiratory flow between 25 and 75% of FVC (FEF25e75%), peak expiratory flow (PEF), exercise time, peak end-tidal CO2 tension (PetCO2), subject-reported leg fatigue and dyspnea; peak O2 uptake (VO2 max), and end-expiratory lung volume (EELV) change from baseline (at peak exercise) were measured. Results: WPS were more likely than non-smokers to report respiratory symptoms. WPS also demonstrated: shorter exercise time; lower peak VO2; higher perceived dyspnea at mid-exercise; lower values of the following: FEV1, FVC, PEF, and EELV change. Conclusion: Habitual waterpipe tobacco smoking in young seemingly healthy individuals is associated with a greater burden of respiratory symptoms and impaired exercise capacity. © 2016 Elsevier Ltd. All rights reserved.
Keywords: Waterpipe Exercise testing Lung function Respiratory symptoms Youth
1. Introduction Various toxic chemicals have been found in waterpipe smoke [1], and waterpipe smoking has been associated with several detrimental health outcomes such as cardiovascular and respiratory diseases, as well as cancer [2e6]. Despite its toxic content [1], waterpipe use has been growing globally, and is particularly popular among youth, the main driving force behind a new worldwide epidemic [7,8]. Waterpipe use also has been shown to predispose its users to cigarette smoking initiation [6,9]. However, knowledge with regards to the health effects of waterpipe on such a young population remains limited [10]. Beyond measuring heart rate and blood pressure, few studies
* Corresponding author. Cancer Control Office, King Hussein Cancer Center, Queen Rania Al Abdullah Street, P.O. Box 1269, Al-Jubeiha, Amman 11941, Jordan. E-mail address: [email protected] (F.I. Hawari). http://dx.doi.org/10.1016/j.rmed.2016.11.024 0954-6111/© 2016 Elsevier Ltd. All rights reserved.
[11e13] have attempted to characterize the cardiopulmonary effects of acute waterpipe smoke exposure in young users, and none have evaluated the early onset effects (if any) of habitual and extended waterpipe smoking. This is an important and timely subject to begin examining. The waterpipe is becoming increasingly popular, even among young groups that were traditionally deemed low-risk for tobacco use (such as athletes) [14]. It is therefore not implausible, as some data are already suggesting [15], that waterpipe use may become more habitual among its users. Providing evidence that can preempt or deter this trend is judicious. In an exploratory pilot study, we sought to assess the range of effects that habitual waterpipe smoking may exert on the cardiopulmonary health of young smokers. Such research is in line with the call for more efforts to elucidate the harmful nature of waterpipe smoking [10]. Specifically, we compared habitual waterpipe smokers (WPS) to non-users of tobacco (non-smokers) in three areas: burden of respiratory symptoms, lung function, and
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cardiopulmonary exercise capacity. We anticipated that WPS would fare worse than non-smokers across all these measures. 2. Methods There is scarce clinical data on waterpipe health effects specifically in habitual young users. Our clinical study was designed as a pilot to prospectively examine the effect of waterpipe on young, habitual users, and generate hypotheses with regards to the potential clinical effect size as a result of habitual waterpipe use (thereby informing future waterpipe clinical research studies with regards to which specific endpoints should be incorporated). The study was conducted in accordance with the amended Declaration of Helsinki. The institutional review board at King Hussein Cancer Center (KHCC) approved the protocol and written informed consent was obtained from all participants. Data collection spanned approximately two years (from August 2013 through to June 2015). 2.1. Participants Participants were recruited through announcements made within several universities in Jordan. Initial contact and screening were conducted via phone. All males who reported being healthy and between the ages of 18 and 26, and who reported either never using tobacco or being WPS who smoked three or more times a week for the past three years atleast (with no other form of tobacco used) were invited to join the study. Those who agreed to participate were invited to a single testing session at KHCC's Cardiopulmonary Exercise Testing (CPET) laboratory. A session lasted approximately two and a half hours. Participants were asked to avoid strenuous exercises or activities, and refrain from smoking for 48 hours prior to their visit. Participants were confirmed healthy by a medical examination. The following exclusion criteria were applied: body-mass index (BMI) of 40.0 kg/m2 or more; active chronic medical conditions; use of chronic prescription medications; illicit drug use; abnormal heart rhythm or abnormal resting heart rate; (>100 or < 50 beats per minute); high blood pressure (>140/90 mmHg); or low oxygen (O2) saturation (<95%). 2.2. Procedures and data collection Body plethysmograph spirometry (using the Vmax series 777360B © 2005 VIASYS Healthcare Inc.) and cardiopulmonary testing using a bicycle ergometer (Ergoselect 100/200, Cardiosoft v6.2) were conducted. Reference spirometric and cardiopulmonary exercise values were based on widely used sources [16e18]. All procedures were conducted according to the American Thoracic Society/European Respiratory Society guidelines for spirometry and cardiopulmonary measures [19,20]. The following variables were measured: 1. General health information (including weight, height, medical history and exercise habits) and socio-demographic factors were recorded. 2. To evaluate general respiratory health, the American Thoracic Society and the Division of Lung Diseases (ATS-DLD-78) adult questionnaire was administered by staff [21]. The following measured variables were specifically of relevance: bringing up phlegm; shortness of breath upon exertion; suffering from cough; having a chest illness in the past three years that kept a participant off work; coughing and phlegm lasting three or more weeks; colds that usually went to the chest; having a wheezy chest whilst having a cold; having a wheezy chest most
of the time; having a wheezy chest without a cold; and having a wheezing attack that left a participant breathless. 3. To evaluate lung function, spirometry was used to measure: forced expiratory volume at the end of first second (FEV1); forced vital capacity (FVC); forced expiratory flow during mid (25e75%) portion of FVC (FEF25e75%); FEV1/FVC; peak expiratory flow (PEF); and total lung capacity (TLC). 4. Cardiopulmonary exercise testing was conducted using a standardized symptom-limited CPET protocol (two-minute baseline with no resistance, two-minute warm-up at a 20-Watt resistance, and a 30-Watt increase every two-minutes thereafter until exhaustion). Variables measured included: peak systolic blood pressure (SBP); peak diastolic blood pressure (DBP); peak heart rate (HR); peak heart rate reserve (HRR); peak breathing reserve (BR); exercise time in minutes; oxygen consumption adjusted for body weight (VO2); linear relation of heart rate to oxygen consumption (HR/VO2); end-tidal oxygen and carbon dioxide tension (peak PetO2 and peak PetCO2, respectively); ventilatory equivalent ratio for oxygen and carbon dioxide (VE/ VO2 and VE/VCO2, respectively); oxygen pulse (O2 pulse); shortness of breath (dyspnea) at mid (taken at a fixed time point for all subjects, at six minutes) and peak exercise (using 0e10 Borg scale), and leg fatigue at mid (at six minutes) and peak exercise (using 6e20 Borg scale) [22,23]; change from baseline at peak exercise in the end-expiratory lung volume (EELV, using the inspiratory capacity maneuver as described by Yan et al.) [24]; O2 saturation; minute ventilation (VE); and anaerobic threshold as percentage of peak VO2. Investigators and technicians within the study were not blinded to group assignment. 2.3. Analysis Basic univariate statistics were used to describe respiratory health and cardiopulmonary measures at peak exercise. T-tests were used to compare non-smokers and WPS across all measures, and p-values were generated (a cut-off of 0.05 was used). Exercise duration (as a proxy for exercise performance) was a main outcome of interest. Multivariable regression analysis was performed to evaluate the effect of being in the WPS group on exercise duration, while adjusting for baseline differences between subjects that may have influenced exercise duration (e.g. age, general respiratory healthy, being physically active, and BMI). With regards to general respiratory health, reporting of dyspnea upon exertion was specifically used as a proxy measure. 3. Results In total, 138 subjects (69 WPS and 69 non-smokers) were recruited for the study. Table 1 presents the baseline characteristics of the sample of male participants. WPS had been smoking the waterpipe habitually for 4.9 years. Notably, WPS (mean age 22.1) had a higher BMI than non-smokers (mean age 21.4). With regards to respiratory symptoms (Fig. 1), a significantly greater proportion of WPS (72.5%) than non-smokers (21.7%) reported any respiratory symptoms (e.g. bringing up phlegm, having shortness of breath upon exertion, cough, chest illness in the past three years that kept a participant off work, and coughing with phlegm that lasted at least three weeks). CPET and PFT results also revealed differences between nonsmokers and WPS (Table 2). WPS had significantly lower FEV1, FVC, PEF and TLC. At peak exercise, WPS had lower VO2 ml/kg and HR; lower degree of change in EELV; and higher HRR, Pet CO2, and VE/VCO2. WPS also reported higher shortness of breath and leg
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Table 1 Baseline characteristics of sample of young male waterpipe smokers and non-smokers.
Mean age (range) Height in cm Weight in Kg BMI (kg/m2) Waterpipe heads per week Years smoking waterpipe (range) CO (ppm)
Waterpipe smokers (n ¼ 69)
Non-smokers (n ¼ 69)
p-value
22.1 (19.0e26.1) 176.6 (164e192) 79.8 (59e122) 25.6 (17.8e34.2) 8.9 4.9 (3e8) 4.2 (1e13)
21.4 (18.2e26.4) 176.1 (164e189) 73.5 (47e104) 23.7 (16.5e32.2) e e 2.2 (0e9)
0.0016 NS 0.0015 0.0012 e e 0.000
100.0% 90.0% 80.0%
72.5%
70.0% 60.0% 50.0%
36.8%
40.0%
33.8% 27.9%
30.0% 21.7%
25.0%
20.0% 10.1% 11.6% 10.0% 1.5%
1.5%
2.9%
Bring up phlegm*
Shortness of breath upon exertion*
Cough*
8.8% 4.4%
7.4% 4.5%
5.8%
0.0%
0.0% Any of symptoms*
10.3% 5.8%
2.9%
1.5% 2.9%
Wheezing Wheezy Wheezy Chest illness Coughing + Cold usually Wheezy attack in past 3 phlegm go to chest chest with chest most of chest without leaving a cold time years kept off lasting 3 having a cold breathless work* weeks* Smokers
Nonsmokers
* Significant Chi-square test for difference in proportions between waterpipe smokers and non-smokers (p<0.05) Fig. 1. Reported respiratory symptoms in the past year in young male waterpipe smokers and non-smokers.
fatigue at mid exercise. Exercise time was significantly shorter for WPS than nonsmokers in both bivariate and multivariate analyses (Table 3). 4. Discussion Waterpipe smoking has increased worldwide particularly among youth, and there have been calls to study its potential to cause lung disease in order to provide the necessary evidence to curb its spread [10,25]. Our pilot study is unique in that it evaluated in young men the effect of habitual long-term waterpipe use on pulmonary symptoms, pulmonary function, and cardiopulmonary exercise capacity. To our knowledge, this is the first study that explores the adverse effects of waterpipe smoking in this collective manner, and within a sample of young habitual waterpipe users. Our data suggest that, in young males, habitual waterpipe use for an average of almost five years, a time relatively short for a history of smoking, can already be associated with various symptoms such as greater burden of respiratory symptoms, PFT abnormalities, and reduced exercise capacity. In general, the occurrence of pulmonary symptoms is a sign of respiratory system distress. In our findings, substantially more WPS reported pulmonary symptoms over the past year (especially shortness of breath upon exertion, sputum production, and
frequent coughing) than non-smokers. In addition, several spirometry parameters (FEV1, FVC, FEF25e75%, and PEF) were trending lower among WPS. These parameters did fall within normal ranges, but the lower trend is nevertheless consistent with other findings in our study, and may indicate early smoking-related pulmonary impairment. For example, although the significance of low PEF in the young has not been studied, PEF has been used in the evaluation of the effect of air pollution in normal and asthmatics [26]. Furthermore, low PEF has been shown to be significantly related to smoking [27], and has been associated with chronic respiratory symptoms including cough and dyspnea on exertion [28], both shown to be more common among WPS in our study. Our data also show that waterpipe smoking was associated with reduced exercise capacity. WPS exercised for a significantly shorter time and generated lower VO2 max values than non-smokers. WPS also reported higher perception of dyspnea and leg fatigue at midexercise. Furthermore, WPS produced significantly higher VE/VCO2 readings, indicating lower breathing efficiency. Many factors are known to affect VE/VCO2 during exercise, such as airway obstruction, hyperinflation, increased dead space ventilation, abnormal resting hemodynamics, and muscle endurance [29e31]. Although our study was not designed to characterize the exact reasons why WPS had a higher VE/VCO2 than non-smokers, it is plausible that waterpipe smoking may have influenced breathing efficiency
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Table 2 Cardiopulmonary results comparing young male waterpipe smokers and non-smokers.
Pulmonary parameters (standard deviation) FEV1, L - % predicted value FVC, L - % predicted value FEV1/FVC - % predicted value FEF25-75%, L - % predicted value PEF, L - % predicted value TLC, L - % predicted value CPET parameters (standard deviation) VO2, ml/min/kg - % predicted value HR/VO2, beats/ml/Kg VO2/Work (ml/min/watt) Work (watt), % predicted Anaerobic threshold as percentage of peak VO2max Exercise time, minutes O2 pulse, ml/beat, % predicted value Systolic blood pressure, mmHg Diastolic blood pressure, mmHg Heart rate, beats/min - % predicted value Heart rate reserve, beats/min Breathing reserve Borg scale e mid Borg scale e peak Leg fatigue e mid Leg fatigue e peak EELV at peak, change from baseline Pet CO2, mmHg Pet O2, mmHg VE - % predicted value VE/VO2 VE/VCO2
Waterpipe smokers (n ¼ 69)
Non-smokers (n ¼ 69)
p-value
98.9 (11.8) 94.1 (11.4) 106.3 (7.8) 101.9 (21.3) 86.9 (16.0) 99.6 (14.8)
102.4 (13.3) 98.0 (14.9) 107.1 (6.4) 105.7 (23.9) 92.2 (18.0) 109.1 (21.9)
0.05 0.04 ns ns 0.03 0.002
57.5 (11.2) 2.8 (0.73) 12.9 (3.2) 60% (8.7) 33.6 (10.4) 8.5 (1.0) 81.3 (16.0) 144.1 (17.1) 79.4 (14.82) 87.0 (9.0) 25.3 (15.8) 51.7 (9.7) 2.9 (1.4) 5.4 (1.6) 11.7 (2.2) 15.3 (2.6) 0.25 (0.47) 38.0 (4.8) 94.2 (4.5) 53.7 (10.6) 22.3 (4.8) 25.1 (2.6)
61.2 (10.11) 3.0 (0.99) 12.3 (3.2) 63.6% (12.0) 32.8 (8.6) 8.9 (1.2) 77.7 (18.3) 142.3 (20.3) 79.3 (12.7) 93.1 (6.4) 14.6 (10.6) 49.4 (12.5) 1.8 (0.98) 3.9 (1.4) 10.75 (1.9) 15.0 (1.8) 0.41 (0.32) 36.4 (15.4) 95.3 (5.3) 56.1 (13.2) 21.6 (3.6) 23.8 (2.7)
0.02 ns ns 0.024 ns 0.03 ns ns ns 0.000 0.000 ns 0.000 0.000 0.003 ns 0.01 0.04 ns ns ns 0.0018
Table 3 Multivariate linear regression of factors influencing duration of exercise in sample of young males (waterpipe smokers and non-smokers).
Age BMI Regular exercise Waterpipe use Report shortness of breath upon exertion
through effecting one of these factors. However, WPS had comparable breathing reserve, ETO2, VE/VO2, and oxygen saturation to non-smokers. Thus, abnormal ventilatory and gas exchange responses were less likely a cause for their reduced exercise capacity. The effect of waterpipe smoking on muscle endurance (and therefore breathing efficiency) may be a particular factor of interest to focus on in future research. Smoking is known to cause fatigue of the skeletal muscles, and other studies have concluded that abnormalities in skeletal muscles endurance can result in abnormalities in breathing efficiency [29,32,33]. Furthermore, reduced exercise capacity due to muscle fatigue has been associated with hyperinflation at peak exercise [34]. In our study, signs of hyperinflation were observed in WPS, who demonstrated significantly lower values of EELV change when compared to non-smokers. Although other causes such as airflow limitation and airway obstruction have been associated with dynamic hyperinflation [35,36], this is unlikely, given that our subjects' spirometry values were well within normal limits. Rather, reduced exercise time, lower EELV change, higher reported leg fatigue, and higher VE/ VCO2, collectively point to muscle fatigue as a plausible reason for exercise limitation among WPS. While deconditioning may also be at play [37], both smokers and non-smokers reported similar exercise patterns. It was notable that WPS in our pilot were on average 6 Kg
Coefficient (standard error)
p-value
0.06 (0.06) 0.11 (0.02) 0.28 (0.19) 0.46 (0.21) 0.19 (0.27)
0.35 0.000 0.15 0.027 0.48
heavier, although we did not find a significant difference in the history of daily exercise pattern between WPS and non-smokers. While obesity may impact lung function, our subjects did not meet the definition of obesity (their average BMI was at the lower range of being overweight rather than obese). Nevertheless, considering the way in which the waterpipe is smoked (sitting down for extended amounts of times, often with easy access to food and beverages), the difference in BMI is conceivable and consistent with other findings [38]. We also controlled for BMI in our multivariable analysis, which found that waterpipe smoking was significantly and independently associated with a shorter duration of exercise. Waterpipe smoking in young healthy adults appeared to have similar effects on heart rate (during exercise) as those of cigarette smoking [39]. Our smokers failed to reach their maximum predicted heart rate and had at least 40% more heart reserve than nonsmokers. Whether this was due to reduced exercise capacity and/or down-regulation of beta-adrenergic receptors, as has been suggested in studies examining the effect of cigarette smoking [40,41], is worth further studying, particularly given that our subjects were young, had a relatively short history of tobacco exposure, and comparable [to non-smokers] O2 pulse, blood pressure, and electrocardiogram (at rest and at peak exercise). To our knowledge, this pilot study is the first to evaluate the
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