Objective Although accumulating evidence suggests harmful effects of waterpipe smoking, there is limited information about its direct association with chronic diseases, notably cancer. We provide an up-to-date systematic review and meta-analysis of the association between waterpipe smoking and cancer.
Data sources Systematic search of articles indexed in main biomedical databases: Pubmed, EmBase, Google Scholar and Web of Science, published between 1962 and September 2014. Search keywords included a combination of waterpipe or hookah, sheesha, nargile, hubble-bubble, goza or gaylan, and cancer.
Study selection Focus on observational studies (cohort, case–control, cross-sectional) that evaluated the association between waterpipe smoking and cancer. Studies with mixed exposures excluded.
Data extraction Two investigators independently extracted data and reached consensus on all items.
Data synthesis 13 case–control studies met the inclusion criteria and were considered for meta-analysis. The methodological quality of included studies was assessed using the Newcastle-Ottawa Scale (NOS). Meta-analysis revealed a positive association between waterpipe smoking and lung cancer (OR=4.58 (2.61 to 8.03); I2=44.67%), and oesophageal cancer (OR=3.63 (1.39 to 9.44); I2 =94.49%). The majority of studies had a NOS score of 5–6 or 7, indicating ‘fair’ or ‘good’ quality, respectively.
Conclusions Our findings support a positive association between waterpipe smoking and cancer risk. However, high-quality studies with standardised exposure measurements are needed to clarify the contribution of waterpipe smoking to chronic diseases. More investments in initiatives for surveillance, intervention and regulatory policy for waterpipe smoking are urgently warranted.
- Smoking Caused Disease
- Non-cigarette tobacco products
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Waterpipe smoking is a method of tobacco use which is known by different names around the world such as shisha, hookah, hubble-bubble, narghile and qalyan. Waterpipe smoking originated in Iran (ancient Persia) and India about 500 years ago, then it spread through Middle Eastern and Asian countries. In the Eastern Mediterranean, parts of Asia including the Indian subcontinent, and North Africa, waterpipes are typically smoked in social gatherings and this custom is embedded in their cultures.1 There are different types of waterpipes, but all of them consist of a smoking apparatus which includes a head, body, bowl and hose. Traditional waterpipes come from the Middle East and Mediterranean countries and are generally larger and constructed with heavier material compared to modern waterpipes which are lighter and typically made in China and marketed by companies mostly based in the USA, but also in other countries. Waterpipe products differ widely from region to region, but the most common practice involves burning embers or charcoal to heat a heavily sweetened and flavoured tobacco mixture to produce the preferred sweeter and flavoured smoke. In particular, Maassel, a moisturised mixture of tobacco, sweetener and different aromas including fruit, honey, candy, chocolate, or mint, is the most popular flavoured tobacco used by the majority of smokers mainly youth.2 While this custom was previously common in Eastern Mediterranean and Southeast Asia, it is now expanding outside of these regions and is becoming a global trend. In 2003, it was estimated that over 100 million people smoked tobacco from waterpipes on a daily basis in Africa, Asia and several Mediterranean countries,3 and the prevalence of use has been steadily increasing to the extent that waterpipe smoking has been described as a global epidemic.4 Historically, in these countries, waterpipe smokers were predominantly older men. Recently, there have been reports of substantial prevalence of waterpipe smoking in young people in the Eastern Mediterranean region and in Western countries.5–12 According to the Surgeon General's Report in USA, 2014, waterpipe smoking among high school students increased from 4.15% to 5.4% during 2011–2012, and increased from 1% to 1.3% among middle school students.13
Compelling evidence points for potentially hazardous substances in waterpipe tobacco smoke, suggesting that waterpipe smoking would be expected to have long-term effects on health.14–18 However, although waterpipe smoking has a long history in developing countries, currently, little is known about its potential health effects. Indeed, WHO stated in 200519 that ‘there is surprisingly little research addressing tobacco smoking using a waterpipe’. As the social nature of waterpipe smoking may include sharing the hose used to inhale the smoke, there is some evidence suggesting that waterpipe smoking increases the potential risk of spreading infectious diseases, such as tuberculosis, hepatitis and herpes.20 ,21 A meta-analysis of studies published up to 2008 indicated positive associations between waterpipe smoking and chronic diseases such as lung and bladder cancer, respiratory illness, low birth weight and periodontal diseases, but the quality of evidence was appraised as low.22 This systematic review did not distinguish the effects of waterpipe smoking as the sole form of exposure to tobacco from waterpipe smoking in combination with other forms of tobacco smoking. In addition, the possible carcinogenicity of waterpipe smoking was not specifically appraised in the 2012 International Agency for Research on Cancer Monograph on Tobacco Smoking,23 or the 2014 Report of the US Surgeon General on the Health Consequences of Smoking.13 Therefore, here, we carried out a systematic literature review and meta-analysis of currently available studies reporting on the effect of waterpipe on cancer, and we focused on the association between waterpipe smoking as the sole form of exposure to tobacco and cancer risk.
Literature search: A comprehensive search was performed based on Pubmed, Medline, Embase, Scopus and Google Scholar from 1962 to 30 September 2014 using the Medical Subject Heading (MeSH) terms and keywords listed in box 1. In addition, the references of selected studies were searched to check for additional potentially relevant articles. Observational studies including cohort, case–control, and cross-sectional were considered. All studies that compared waterpipe smokers with non-smokers (never smoke waterpipe) were included. We excluded studies in which waterpipe use could not be distinguished from other types of smoking. We also excluded studies of subgroups that had specific exposures associated with increased risk of cancer, notably miners (which led to the exclusion of studies of Chinese bamboo-waterpipe and long-stem pipe exposure) and people infected with Heliobacter pylori. No exclusion was made on the basis of language. A list of excluded studies including reasons for exclusion is provided as online supplementary web appendix A. The search process was conducted by two authors. Following preliminary review of titles and abstracts, articles were selected for further screening, according to inclusion/exclusion criteria. In the case of disagreement between reviewers, the article was reviewed by a third investigator and a final decision made after a careful discussion. Data were extracted on definition of waterpipe smoking; study design and setting; sample size, description and base population; prevalence of waterpipe smoking; reported ORs and CI without frequencies were also considered. Data were extracted, using a data extraction form (see web figure), independently by two authors. Any disagreement was resolved by discussion with a third author. The quality of included articles was assessed independently by two of the authors using the Newcastle-Ottawa Scale (NOS).24 The scale measures three items; selection of cases and controls including their definition and representativeness; comparability of cases and controls in design and analysis; and exposure ascertainment. The scale has a minimum score of 0 and a maximum score of 9. Studies scoring 7 or more (correspond to 78% of the maximum score) were regarded as having a low risk of bias (‘good’ quality)25; 4–6 a modest risk of bias (‘fair’ quality); and studies <3 were considered to be at substantial risk of bias (‘poor’ quality). Spearman’s rank correlation coefficient was used to measure the degree of agreement between the authors’ judgments. Disagreements were resolved through discussion. No exclusion based on risk of bias was performed. Studies were further classified in two groups, either those with substantial or modest risk of bias versus those with a low risk of bias, for sensitivity analysis. Details of study quality are presented in online supplementary appendix.
Medical Subject Heading (MeSH) terms and keywords used in the literature search
MeSH: waterpipe smoking/OR Hookah smoking
Keywords: waterpipe OR water pipe OR Hookah OR sheesha OR shisha OR
nargile OR hubble bubble OR goza OR gaylan OR
(water pipe, cancer) OR (shisha, cancer) OR (sheesha, cancer) OR
(hookah, cancer) OR (nargile, cancer) OR (gaylan, cancer)
Statistical analysis: We carried out a systematic review and meta-analysis to derive summary effect of the association between waterpipe smoking and human cancers. The risk of cancer and waterpipe smoking was estimated for each study by OR and 95% CI. Meta-analysis was applied for each cancer type separately with at least three studies. Basing on the χ2 test, an inconsistency coefficient was computed (I2 statistic) where a value >50% indicated moderate, and >75% indicated high heterogeneity.26 ORs were pooled with a random effects model.27 For each specific type of cancer, ORs with their 95% confidence limits for the individual studies and summary estimates of effect were graphically displayed in forest plots. We calculated a summary OR for the two types of cancers for which there were more than two studies. Sensitivity analyses were performed to evaluate the stability of the results by removing one study from each meta-analysis at a time to examine the influence of each study on the pooled ORs. Potential small-study effects were investigated based on Begg's funnel plot and Egger's regression test.28 ,29 All analyses were performed using open-source R (http://www.R-project.org), and metafor package30 based on 2×2 table for each study included frequencies of waterpipe smokers/non-smokers in case and control.
In total, over 630 titles were reviewed, of which 52 publications reporting on association between waterpipe smoking and human cancer were identified, see online supplementary appendix, and 13 studies, all of which were of the case–control design, met the inclusion criteria (table 1). These studies were published between 1997 and 2013, all in English. In aggregate, the studies included a total of 2717 cases (range: 26–702) and 5027 controls (range: 73–1648); there were 1867 waterpipe smokers and 5877 non-smokers (no smokers of waterpipe). Of the 13 eligible studies, 3 studies related to lung cancer, 5 to oesophageal cancer, 2 to cancers of the head and neck (one of which was restricted to nasopharyngeal cancer), and the remaining 3 studies examined a single type of cancer (bladder, gastric and prostate). Table 2 presents raw data, OR along with 95% CI for each study and results of meta-analyses. We found a significant positive association between waterpipe smoking and the risk of developing lung cancer, the pooled OR is 4.58 with 95% CI (2.61 to 8.03), with low heterogeneity, I2=44.67%. A significant positive association was also observed between waterpipe smoking and oesophageal cancer based on pooled data from 5 case–control studies, and the pooled OR is 3.63 (95% CI 1.39 to 9.44), table 2, with high heterogeneity, I2=94.5% (see figures 1 and 2).
On the basis of the funnel plots and Egger's regression tests, there was no statistically significant evidence of small-study effects for lung cancer (p=0.880) or oesophageal cancer (p=0.885). Funnel plots are presented in figures 3 and 4.
Each study was evaluated according to the scoring system NOS based on three categories: selection, comparability and exposure. There are four criteria for selection, and a study receives a maximum of one star for each criterion, one criterion for comparability with a maximum of two stars, and three criteria for exposure with up to one star for each. Assessments of included case–control studies are shown in online supplementary appendix. Briefly, the total score for 3 studies is 7 (high quality); for 1 study is 5, and for 7 studies is 6 (fair quality), and there is 1 study for which the score is 2 (poor quality). One study was not evaluated since we did not have access to the full paper.
In this systematic review and meta-analysis, we summarise the evidence of association between waterpipe smoking and cancer risk.
Overall, 13 relevant case–control studies reporting on different cancer types matched our selection criteria. In aggregate, these 13 studies included data on 2717 cases and 5027 controls. Cancer-site-specific meta-analysis revealed a significant positive association between waterpipe smoking and lung cancer, and a similar association was also observed for oesophageal cancer. Regarding the lung cancer outcome, our meta-analysis results align with the findings from Akl et al22 which also showed a positive association between waterpipe smoking and lung cancer risk, though the quality of evidence was judged to be low. However, Akl et al22 did not detect any association between waterpipe smoking and bladder, nasopharyngeal and oesophageal cancers. The slight discrepancy between our findings and the results from this previous meta-analysis could be explained by several reasons, including mainly the difference in selection criteria and the method used to limit the confounding factors as well as the difference in publication and searching time between both studies. In particular, our selection criteria were more stringent compared to those of Akl et al.22 While Akl et al considered the effects of waterpipe smoking in combination with other forms of tobacco smoking, in this study, potential confounding was limited by restriction. Thus, studies in which waterpipe smoking was mixed with other types of active smoking exposure were excluded, as were studies in miners related to Chinese bamboo-waterpipe and long-stem pipes use because of potential for confounding by factors such as underground radon exposure. In addition, the present study includes a larger sample size than that of Akl et al,22 since it includes articles published after Akl et al conducted their search in 2008.
Although limited research has been conducted on the health effects of waterpipe use, available evidence strongly indicates that waterpipe contains many of the same harmful toxins as cigarette smoke.44–46 The wood cinders or charcoal used to heat the tobacco may cause negative health effects by producing high levels of carbon monoxide (CO), metals and carcinogenic chemicals. Even after it has passed through water, waterpipe smoke contains high levels of these toxicant agents. The herbal product used in most cafés, particularly in Canada, for which there is no regulation, is supposed to be nicotine-free, but recent investigations showed that it may contain toxic traces of metals and polycyclic aromatic hydrocarbons (PAHs) in concentrations equivalent to, or even more than that detected in cigarettes.47 The main and side stream of the herbal product compared with tobacco also showed that it contains equal or more carcinogens of tobacco, and the air quality of a waterpipe café (using the herbal product) demonstrates the level of CO content as significantly higher compared to a casino, where cigarette smoking is permitted.47 Waterpipe smoking may increase exposure to toxicants, since relative to smoking a single cigarette which takes 5–10 min to complete, a waterpipe smoking session lasts much longer, typically 45–60 min.48 Thus, due to the longer and more sustained period of inhalation and exposure, it was suggested that a single session of waterpipe smoking may correspond to consuming 100 or more cigarettes.
Interestingly, the toxicants exposure from waterpipe smoking have been recently compared with exposure from cigarette smoking using biomarker measurements, and waterpipe use was shown to be associated with substantial amounts of nicotine, greater exposure to CO and tar (nicotine-free dry particles), and an abundance of several toxicant chemicals.46 ,49 ,50 In particular, carcinogenic agents, notably benzene and high molecular weight PAHs, that are thought to be causal factors in the elevated incidence of cancer, cardiovascular disease and addiction in cigarette smokers, have been detected in biological fluids from waterpipe tobacco smokers.46 ,49 ,50 The positive association between waterpipe smoking and the high ORs for lung and oesophageal cancers observed in this study corroborate these emerging findings suggesting a possible causal effect of waterpipe smoking in human cancer.46 ,49 ,50 However, the health effects of waterpipe smoking remain largely under-studied, and available studies have limitations and reflect mixed exposure from many different types of waterpipe products.
Therefore, the first limitation of this study was the lack of a large number of relevant studies assessing the association between waterpipe smoking and cancer. Indeed, the geographical area of our meta-analyses was limited mainly to India, Middle East and African countries. Particularly, there is a significant lack of research studies of waterpipe smoking health effects in Western populations, even though current evidence indicates that Middle Eastern waterpipe smoking is on the rise in this part of the world, and is becoming second to cigarette smoking, and gaining popularity among the youth.2 ,51 Our analysis also showed a considerable heterogeneity between studies (ie, I2=94.5% for oesophageal cancer) suggesting that available studies might have major methodological limitations. The heterogeneity among studies could be due to inappropriate handling of confounding factors among studies. The methodological quality of studies included in our meta-analyses was assessed using the NOS, and each study is judged based on three perspectives: selection, comparability and exposure.24 According to NOS score, the majority of selected studies showed a low risk of bias (score ≥7, classified as good and moderate or intermediate quality). The low risk of bias was mainly related to the lack of reporting complete information about cases and controls, or waterpipe smoking was not the main issue of the study since the low score was mainly related to the exposure part. In addition, since the practice of waterpipe smoking could vary widely and no standardised measurement method has been used in different studies, there is a possibility of measurement bias, a potential methodological limitation which could have affected the results from our meta-analyses. However, although waterpipe products may differ widely from region to region, the available international data indicate that Maassel is the most popular flavoured tobacco used in waterpipes for the majority of smokers, particularly youth.2 Thus, although caution must be taken given the geographical representation of the studies presented in our meta-analyses, the observed outcome is also likely relevant for the Western waterpipe users.
In conclusion, the findings from this study indicate an association between waterpipe smoking and increased cancer risk, specifically lung and oesophageal cancer. However, high-quality research studies using standardised exposure measurements tools are needed to ascertain the health effects of waterpipe smoking as the sole form of exposure to tobacco, and evaluate its possible relationship with other types of tobacco smoking. Since waterpipe smoking is currently showing all the signs of a global epidemic, with serious implications for public health and tobacco control worldwide, awareness about the potential harmful health effects of waterpipe smoking among the public, particularly youth smokers, and policymakers is urgently required. Therefore, more investments in research initiatives aimed to develop surveillance, public health intervention and regulatory policy specific to waterpipe smoking need to become one of the public health priorities.
What this paper adds
There is a positive association between waterpipe smoking and human cancer, for which the greatest volume of evidence is for lung and oesophageal cancers.
Although knowledge is accumulating about the negative health and addictive effects of waterpipe smoking, there is a lack of well-designed epidemiological studies clarifying the health effects of waterpipe smoking and its association with chronic diseases, including cancer.
Contributors ZM and HE-K conducted systematic review and extracting data. Statistical analysis was done by ZM. ZM, CN and JL contributed in writing and revising manuscript.
Funding This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.
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