|Year : 2022 | Volume
| Issue : 1 | Page : 79
The effect of water-pipe and cigarette smoking on exhaled nitric oxide
Amir Houshang Mehrparvar1, Laleh Ghanbari2, Seyyed Jalil Mirmohammadi1, Mohammad Javad Zare Sakhvidi2, Mahmood Vakili3, Mohammad Hossein Davari2, Masoud Mirzaei4
1 Industrial Diseases Research Center, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
2 Department of Occupational Medicine, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
3 Department of Community Medicine, Monitoring of Health Research Center, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
4 Yazd Cardiovascular Research Center, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
|Date of Submission||02-Feb-2021|
|Date of Acceptance||17-Mar-2021|
|Date of Web Publication||27-Apr-2022|
Mohammad Hossein Davari
Industrial Diseases Research Center, Shahid Rahnemoun hospital, Farrokhi Ave., Yazd
Source of Support: None, Conflict of Interest: None
Context: Fractional exhaled nitric oxide can be used as a biomarker of some respiratory diseases. Aims: This study was conducted to compare exhaled nitric oxide in cigarette and water-pipe smokers with nonsmokers. Methods: This cross-sectional study was conducted on 549 adult subjects as a sub-study of Shahedieh cohort in Yazd. Participants were divided into 5 groups according to their smoking habits: non-smokers (n = 202), cigarette smokers (n = 121), water-pipe smokers (n = 129), cigarette ex-smokers (n = 58), water-pipe and cigarette smokers (n = 39). The smokers were also categorized into heavy and light smokers. Fractional exhaled nitric oxide was compared between the groups. Statistical Analysis Used: The data were analyzed by SPSS (ver. 20) using Kolmogorov-Smirnov, Kruskal-Wallis, and Mann-Whitney U tests. Results: Fractional exhaled NO was lower in all smokers than nonsmokers, but cigarette smokers showed the least level of NO than other groups. Fractional exhaled NO was not significantly lower in water-pipe smokers than nonsmokers. Conclusions: Cigarette smoking significantly affect fractional exhaled NO, but water-pipe smoking did not significantly affect exhaled NO level.
Keywords: Cigarette smoking, nitric oxide, water pipe smoking
|How to cite this article:|
Mehrparvar AH, Ghanbari L, Mirmohammadi SJ, Zare Sakhvidi MJ, Vakili M, Davari MH, Mirzaei M. The effect of water-pipe and cigarette smoking on exhaled nitric oxide. Int J Prev Med 2022;13:79
|How to cite this URL:|
Mehrparvar AH, Ghanbari L, Mirmohammadi SJ, Zare Sakhvidi MJ, Vakili M, Davari MH, Mirzaei M. The effect of water-pipe and cigarette smoking on exhaled nitric oxide. Int J Prev Med [serial online] 2022 [cited 2023 Mar 27];13:79. Available from: https://www.ijpvmjournal.net/text.asp?2022/13/1/79/344224
| Introduction|| |
Nitric oxide (NO), an endogenous gas, is a component of human's breath. It plays an important role in some respiratory processes such as vascular regulation, host defense, and it may have cytoprotective effects. The fractional concentration of NO in exhaled breath (FeNO) is now used as a biomarker which may help diagnose some respiratory diseases.,,
Cigarette smoking can reduce FeNO. FeNO increase shortly after smoking but long-term exposure to cigarette smoke reduced it. It has been shown as well that this effect was influenced by smoking history, and it may be reversed after smoking cessation. In cigarette smokers, NO metabolism is changed due to the oxidation of NO. So, results of FeNO in different disease states should be interpreted cautiously in smokers. Some other factors such as BMI or some other occupational or environmental exposures may affect FeNO as well.,
Water-pipe (other names: hubble-bubble, hookah, narghile, arghile, qalyan, and sheesha) is a traditional device to smoke tobacco in the Middle East and its use was common in Iran, in the past. Recently, its use is increased again especially among females and the young with a probable belief that it is harmless. The prevalence of water-pipe smoking in the adolescents in the Middle East countries is about 6-34%.
Each session of hookah smoking includes about 50-200 puffs which contains about 10 g tobacco and produces about 25 mg of nicotine,, which is equivalent to smoking about 100 cigarettes. Nowadays, besides pure tobacco, some fruit extracts have been added to tobacco leaves which are smoked by this device.
The studies on the effect of water-pipe on different organs and especially respiratory system mostly have shown a negative effect, though with controversial results., Most studies on the effect of water-pipe smoking on respiratory function have shown a negative effect in comparison to non-smokers,, and a systematic review found that water-pipe smoking is probably as harmful as cigarette smoking. Raad et al. in a systematic review concluded that water-pipe negatively affects respiratory system and is probably one of the causes of COPD, although some studies did not find a significant difference in lung function between water-pipe smokers and non-smokers., The effect of water-pipe smoking on pulmonary function tests in comparison to cigarette smoking is controversial.
We could find few studies on the effects of water-pipe on FeNO. Some studies showed a lower FeNO among water-pipe smokers than non-smokers and an immediate effect of water-pipe on FENO.,
Due to the not conclusive results about the effect of water-pipe smoking on FeNO (in comparison to cigarette smoking and not smoking) and the large differences in various populations in the devices and methods of smoking water-pipe, this study was performed to assess the effect of water-pipe smoking on FeNO in comparison to non-smokers, cigarette smokers, and ex-smokers in an Iranian suburban adult population.
| Subjects and Methods|| |
This was a cross-sectional study on 549 adult subjects as a sub-study of Shahedieh cohort (n = 10194) in Yazd. Shahedieh cohort is a branch of a national cohort study (PERSIAN cohort) on adult population (age range: 35–70 years) which has begun in Yazd from 2015. The subjects were randomly selected from Shahedieh cohort participants who did not suffer from a diagnosed respiratory disorder in Yazd and were divided into 5 groups according to their smoking habits: non-smokers (n = 202), cigarette smokers (n = 121), water-pipe smokers (n = 129), cigarette ex-smokers (n = 58), water-pipe, and cigarette smokers (n = 39). Demographic data were extracted from the cohort database. Smoking history and its related information have been collected by standard questionnaires during the enrollment phase of the cohort study. All cigarette smokers and almost all water-pipe smokers were males, so females in the non-smoker group were also excluded from the study, so all participants were males.
The subjects with at least 1 pack year cigarette smoking and 2 water-pipe sessions (heads) per week were considered as cigarette and water-pipe smokers, and those who had quitted cigarette smoking for at least 1 year were considered as ex-smokers. The cigarette smokers were also categorized into heavy (smoked more than 10 pack-years, n = 48) and light smokers (n = 73) according to their pack-years of smoking; and water-pipe smokers were also categorized to heavy (smoked more than 395 water-pipes lifelong, n = 34) and light (n = 95) smokers. This categorization was done according to the median of pack/years of cigarette smoking and number of lifelong water-pipe smoking sessions.
FeNO was measured by a portable electrochemistry-based device (NObreath, Bedfont Scientific Ltd., UK). American Thoracic Society/European Respiratory Society (ATS/ERS) guidelines were used to perform tests. NO concentration was measured in part per billion (ppb). The test was performed in sitting position and the participant was asked to perform expiration for 10 s with a constant flow (50 ml/s) and pressure (10 CmH2O). After performing at least two acceptable maneuvers, the test was terminated and the mean of two measurements with less than 4 ppb difference was reported as the final result. Heavy exercise, having large meals, and smoking 1 h before test were considered as the intervening factors and the test was postponed to 1 h later.
The data were analyzed by SPSS (ver. 20) using Kolmogorov-Smirnov, Kruskal-Wallis, and Mann-Whitney U tests. This study was a residency thesis in occupational medicine in Shahid Sadoughi University of Medical Sciences. The protocol of the study was approved by the ethics committee of the university.
| Results|| |
Totally 549 participants were assessed regarding their exhaled breath NO concentration. Mean age of the participants was 48.4 ± 8.0 years (range, 38-70). The highest mean age was observed in ex-smokers (52.2 ± 6.8 years) which was significantly higher than other groups, but the difference in age was not significant between other study groups. Body mass index was not significantly different between groups. [Table 1] shows descriptive statistics of the study participants.
|Table 1: Descriptive statistics of the study participants in different groups according to smoking status|
Click here to view
There was a significant difference between groups regarding FeNO (P < 0.001). The lowest FENO was observed in cigarette smokers. [Table 2] shows pairwise comparisons between groups regarding FeNO.
FeNO was much lower in heavy cigarette smokers, but the difference was not statistically significant. [Table 3] compares FeNO between heavy and light cigarette and water-pipe smokers.
|Table 3: Comparison of FeNO between heavy and light cigarette and water-pipe smokers|
Click here to view
| Discussion|| |
Water-pipe smoking is increasing recently in our country with a premise that water-pipe smoking does not harm their health. In this cross-sectional study as a sub-study of Shaedieh cohort, we compared the long-term effect of cigarette and water-pipe smoking on FeNO.
In accordance with many previous studies, this study showed that smoking reduced FeNO, but this decrease in comparison to non-smokers was statistically significant only in the cigarette smokers, but not in water-pipe smokers.
Water-pipe is a device for tobacco smoking, especially in the Middle East. Water-pipe smoking may induce diseases which are attributed to cigarette smoking, such as lung cancer, esophageal cancer, and periodontal diseases. Some studies have shown a negative effect on pulmonary function tests for water-pipe smoking, although with different effect sizes comparing cigarette smoking. Most previous studies have assessed the effect of water-pipe on spirometric parameters. In Kiter et al. study, the effect of water-pipe on spirometric parameters was not as great as cigarette, although Boskabadi et al. and Baiee et al. found that the negative effect of water-pipe smoking on spirometric parameters is almost similar to cigarette smoking., Few studies have assessed the effect of water-pipe smoking on FeNO.,
NO is a free radical which can react with other molecules and is useful in the diagnosis of some respiratory diseases such as asthma and atopy. Cigarette smoke contains NO and can increase FeNO immediately after smoking, but may reduce its production in the body as a negative feedback mechanism, by inhibition of NO synthase (NOS) or by presenting such molecules as superoxide which may react with NO.
In the current study, cigarette smokers had the lowest FeNO which was significantly lower than non-smokers and water-pipe smokers. Most previous studies have shown a lower FeNO in cigarette smokers than non-smokers.,
Quitting cigarette smoking may reverse its effects on FeNO. In this study, ex-smokers had also a lower FeNO than non-smokers, but this difference was not statistically significant, and their FeNO was higher than current smokers, which shows a trend toward non-smokers.
About the effect of age on FeNO, there are controversial results; in this study, all groups were similar regarding age except for ex-smokers who were significantly older than other groups, so our main results were not influenced by age.
Mean FeNO in smokers and non-smokers of our population was much lower than Meo et al. study in Saudi Arabia, which is probably due to genetic factors, anthropometric dimensions and different devices used to assess FeNO or even different kinds of water-pipe devices or tobaccos. In the present study, FeNO in water-pipe smokers was significantly higher than cigarette smokers, but non-significantly lower than non-smokers, which was in contrast to the results of Meo et al. study who found a significantly lower FeNO in water-pipe smokers than non-smokers. This difference is probably due to different methods of water-pipe smoking, different devices or different tobaccos used in two countries or even different genetic factors.
Hakim et al. assessed the effects of water-pipe on FeNO and showed that water-pipe can reduce FeNO immediately after smoking. We measured FeNO after at least 1 hour of smoking, so acute effect was not possible to assess in this study.
Considering the amount of smoking (pack-years of cigarettes and numbers of water-pipe sessions), this study failed to show a statistically significant difference between heavy and light smokers, although FeNO was much lower in heavy cigarette smokers than light smokers, but this difference was not statistically significant. Probably a larger sample size may show this effect. Similarly, in the water-pipe smokers, the number of smoked water-pipes was not associated with decreased FeNO.
This study had some limitations: Our population was older than 35 years and all participants were males, so we could not assess the young population and females. We did not have data about the type of tobacco, cigarettes and water-pipe device which may affect the results.
| Conclusion|| |
The results of this study showed that cigarette and water-pipe smoking decreased FeNO in middle-aged male population in comparison to non-smokers, but this decrease was statistically significant only in cigarette smokers. Quitting cigarette smoking may reverse the effects of smoking on FeNO.
The authors would like to express their appreciation to Shahedieh Cohort participants and principal investigators of PERSIAN cohort.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Barnes PJ, Belsivi MG. Nitric oxide and lung disease. Thorax 1993;48:1034-43.
Van der Vliet A, Eiserich JP, Shigenaga MK, Cross CE. Reactive nitrogen species and tyrosine nitration in the respiratory tract: Epiphenomena or a pathobiologic mechanism of disease? Am J Respir Crit Care Med 1999;160:1-9.
Saito J, Inoue K, Sugawara A, Yoshikawa M, Watanabe K, Ishida T, et al
. Exhaled nitric oxide as a marker of airway inflammation for an epidemiologic study in schoolchildren. J Allergy Clin Immunol 2004;114:512-6.
Ansarin K, Chatkin JM, Ferreira IM, Gutierrez CA, Zamel N, Chapman KR. Exhaled nitric oxide in chronic obstructive pulmonary disease: Relationship to pulmonary function. Eur Respir J 2001;17:934-8.
Olin AC, Alving K, Toren K. Exhaled nitric oxide: Relation to sensitization and respiratory symptoms. Clin Exp Allergy 2004;34:221-6.
Kharitonov SA, Robbins RA, Yates D, Keatings V, Barnes PJ. Acute and chronic effects of cigarette smoking on exhaled nitric oxide. Am J Respir Crit Care Med 1995;152:609-12.
McSharry CP, McKay IC, Chaudhuri R, Livingston E, Fraser I, Thomson NC. Short and long-term effects of cigarette smoking independently influence exhaled nitric oxide concentration in asthma. J Allergy Clin Immunol 2005;116:88-93.
Robbins RA, Millatmal T, Lassi K, Rennard S, Daughton D. Smoking cessation is associated with an increase in exhaled nitric oxide. Chest 1971;12:313-8.
Balint B, Donnelly LE, Hanazawa T, Kharitonov SA, Barnes PJ. Increased nitric oxide metabolites in exhaled breath condensate after exposure to tobacco smoke. Thorax 2001;56:456-61.
Dressel H, de la Mottea D, Reicherta J, Ochmanna U, Petrua R, Angerera P, et al
. Exhaled nitric oxide: Independent effects of atopy, smoking, respiratory tract infection. gender and height. Respir Med 2008;102:962-9.
Mirmohammadi SJ, Mehrparvar AH, Safaei S, Samimi E, Torab Jahromi M. The association between exhaled nitric oxide and sleep apnea: The role of BMI. Respir Med 2014;108:1229-33.
Mirmohammadi SJ, Mehrparvar AH, Safaei S, Salmani Nodoushan M, Torab Jahromi M. Across-shift changes of exhaled nitric oxide and spirometric indices among cotton textile workers. Int J Occup Med Environ Health 2014;27:707-15.
Aslam HM, Saleem S, German S, Qureshi WA. Harmful effects of shisha: Literature review. Int Arch Med 2014;7:16.
Maziak W. The global epidemic of waterpipe smoking. Addict Behav 2011;36:1-5.
Boskabady MH, Farhang L, Mahmodinia M, Boskabady M, Heydari GR. Comparison of pulmonary function and respiratory symptoms in water pipe and cigarette smokers. Respirology 2012;17:950-6.
Al Mutairi SS, Shihab-Eldeen AA, Mojiminiyi OA, Anwar AA. Comparative analysis of the effects of hubble-bubble (Sheesha) and cigarette smoking on respiratory and metabolic parameters in hubble-bubble and cigarette smokers. Respirology 2006;11:449-55.
Knishkowy B, Amitai Y. Water-pipe (narghile) smoking: An emerging health risk behavior. Pediatrics 2005;116:e113-9.
Qasim H, Alarabi AB, Alzoubi KH, Karim ZA, Alshbool FZ, Fadi T, et al
. The effects of hookah/waterpipe smoking on general health and the cardiovascular system. Environ Health Prev Med 2019;24:58.
Alshayban DM, Pottoo FH, Aftab MT. Genotoxic burden of water pipe smoking in Arabian countries: The risk in female population. Imam J Appl Sci 2019;4:31-8. [Full text]
Alwan Baiee H, Ibrahim Mahmoud R. Pulmonary function test for water pipe smokers and cigarette smokers in males in Al-Hilla city during the year 2014. Med J Babylon 2014;11:1029-36.
Haddad L, Kelly DL, Weglicki LS, Barnett TE, Ferrell AV, Ghadban R. A systematic review of effects of waterpipe smoking on cardiovascular and respiratory health outcomes. Tob Use Insights 2016;9:13-28.
Raad D, Gaddam S, Schunemann HJ, Irani J, Abou Jaoude P, Honeine R, et al
. Effects of water-pipe smoking on lung function: A systematic review and meta-analysis. Chest 2011;139:764-74.
Kiter G, Uçan ES, Ceylan E, Kilinç O. Water-pipe smoking and pulmonary functions. Respir Med 2000;94:891-4.
Köseoğlu N, Aydin A, Uçan ES, Ceylan E, Eminoğlu O, Durak H, et al
. The effects of water-pipe, cigarette and passive smoking on mucociliary clearance [in Turkish]. Tuberk Toraks 2006;54:222-8.
Ben Saad H, Khemiss M, Nhari S, Ben Essghaier M, Rouatbi S. Pulmonary functions of narghile smokers compared to cigarette smokers: A case-control study. Libyan J Med 2013;8:22650.
Meo SA, AlShehri KA, AlHarbi BB, Barayyan OR, Bawazir AS, Alanazi OA, et al
. 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 2014;11:9638-48.
Hakim F, Hellou E, Goldbart A, Katz R, Bentur Y, Bentur L. The acute effects of water-pipe smoking on the cardiorespiratory system. Chest 2011;139:775-81.
Lappas A, Behrakis P, Konstantinidi E, Tzortzi A, Stathopoulou C. Immediate effects of water-pipe smoking on respiratory mechanics and FENO among young smokers. Eur Respir J 2014;44(Suppl 58):P1806-9.
Poustchi H, Eghtesad S, Kamangar F, Etemadi A, Keshtkar A-A, Hekmatdoost A, et al
. Prospective Epidemiological Research Studies in Iran (the PERSIAN cohort study): Rationale, objectives, and design. Am J Epidemiol 2018;187:647-55.
American Thoracic Society; European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med 2005;171:912-30.
Akl EA, Gaddam S, Gunukula SK, Honeine R, Jaoude PA, Irani J. The effects of waterpipe tobacco smoking on health outcomes: A systematic review. Int J Epidemiol 2010;39:834-57.
Silkoff PE, McClean P, Spino M, Erlich L, Slutsky AS, Zamel N. Dose-response relationship and reproducibility of the fall in exhaled nitric oxide after inhaled beclomethasone dipropionate therapy in asthma patients. Chest 2001;119:1322-8.
Taylor DR, Pijnenburg MW, Smith AD, De Jongste JC. Exhaled nitric oxide measurements: Clinical application and interpretation. Thorax 2006;61:817-27.
Assreuy J, Cunha FQ, Liew FY, Moncada S. Feedback inhibition of nitric oxide synthase activity by nitric oxide. Br J Pharmacol 1993;108:833-7.
Beckman JS. Oxidative damage and tyrosine nitration from peroxynitrite. Chem Res Toxicol 1996;9:836-44.
Hogman M, Holmkvist T, Walinder R, Meriläinen P, Lúdvíksdóttir D, Håkansson L, et al
. Increased nitric oxide elimination from the airways after smoking cessation. Clin Sci (Lond) 2002;103:15-9.
[Table 1], [Table 2], [Table 3]